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THE DEVELOPMENT OF IMPLICIT

AND EXPLICIT MEMORY

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ADVANCES IN CONSCIOUSNESS RESEARCH

ADVANCES IN CONSCIOUSNESS RESEARCH provides a forum for scholars
from different scientific disciplines and fields of knowledge who study conscious-
ness in its multifaceted aspects. Thus the Series will include (but not be limited to)
the various areas of cognitive science, including cognitive psychology, linguistics,
brain science and philosophy. The orientation of the Series is toward developing
new interdisciplinary and integrative approaches for the investigation, description
and theory of consciousness, as well as the practical consequences of this research
for the individual and society.
Series B: Research in Progress. Experimental, descriptive and clinical research in
consciousness.

EDITOR
Maxim I. Stamenov
(Bulgarian Academy of Sciences)

EDITORIAL BOARD
David Chalmers (University of Arizona)
Gordon G. Globus (University of California at Irvine)
Ray Jackendoff (Brandeis University)
Christof Koch (California Institute of Technology)
Stephen Kosslyn (Harvard University)
Earl Mac Cormac (Duke University)
George Mandler (University of California at San Diego)
John R. Searle (University of California at Berkeley)
Petra Stoerig (Universität Düsseldorf)
Francisco Varela (C.R.E.A., Ecole Polytechnique, Paris)

Volume 24

Carolyn Rovee-Collier, Harlene Hayne and Michael Colombo

The Development of Implicit and Explicit Memory

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THE DEVELOPMENT
OF IMPLICIT AND
EXPLICIT MEMORY

CAROLYN ROVEE-COLLIER
Rutgers University
HARLENE HAYNE
University of Otago
MICHAEL COLOMBO
University of Otago

JOHN BENJAMINS PUBLISHING COMPANY

AMSTERDAM/PHILADELPHIA

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TM The paper used in this publication meets the minimum requirements of

8

American National Standard for Information Sciences — Permanence of

Paper for Printed Library Materials, ansi z39.48–1984.

Library of Congress Cataloging-in-Publication Data

Rovee-Collier, Carolyn K.
The development of implicit and explicit memory / Carolyn Rovee-Collier, Harlene Hayne,
Michael Colombo.
p. cm. -- (Advances in consciousness research, ISSN 1381-589X ; v. 24)
Includes bibliographical references and index.
1. Memory in children. 2. Implicit memory. 3. Explicit memory. I. Hayne, Harlene. II.
Colombo, Michael. III. Title. IV. Series.
BF723.M4.R68 2000
153.1’3--dc21 00-034218
ISBN 90 272 5144 4 (Eur.) / 1 55619 724 1 (US) (Pb)
© 2001 - John Benjamins B.V.
No part of this book may be reproduced in any form, by print, photoprint, microfilm, or any other
means, without written permission from the publisher.
John Benjamins Publishing Co. • P.O.Box 75577 • 1070 AN Amsterdam • The Netherlands
John Benjamins North America • P.O.Box 27519 • Philadelphia PA 19118-0519 • USA

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To our collective children, and to George

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Table of Contents

Preface ix
CHAPTER 1
Background of the Problem 1
CHAPTER 2
Distinctions between Implicit and Explicit Memory 7
CHAPTER 3
Neuroanatomical Basis of Implicit and Explicit Memory 29
CHAPTER 4
The Jacksonian Principle and Memory Development 65
CHAPTER 5
Development of Implicit and Explicit Memory in Nonhuman Primates 83
CHAPTER 6
Development of Implicit and Explicit Memory in Human Infants 97
CHAPTER 7
Memory Dissociations in Human Infants 127
CHAPTER 8
Structural and Processing Accounts of Memory Dissociations 189
CHAPTER 9
Interactions between Implicit and Explicit Memories in Infants 231
CHAPTER 10
Epilogue 247
References 253
Author Index 291
Subject Index 303

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Preface

This book evolved out of our concern that researchers who study memory in
human adults have constructed a scenario of the ontogeny of memory in
human infants without reference to empirical studies of infants themselves.
This scenario is largely based on studies of brain-damaged adults and brain-
lesioned animals and, because it fits neatly into a simple theoretical frame-
work, is intuitively appealing — but it is wrong.
At the core of this scenario are two assumptions — the assumption that
ontogeny recapitulates phylogeny and the assumption that the Jacksonian
first-in, last-out principle applies to the development and dissolution of
memory systems. In the first instance, evolutionary biologists have long
recognized the error of designating species as “higher” or “lower” when the
phylogenetic scale is tree-like and branching rather than linear. In the present
context, this error has translated into the flawed conclusion that human
newborns mirror lower animals and, over the course of development, come
increasingly to resemble higher animals, namely, adult (or verbal) humans. In
the second instance, studies with animals and human infants have failed to
find support for the Jacksonian principle. Moreover, predicting the sequence
of the normal dissolution of neural function from the sequence of its normal
development is different from predicting the sequence of the normal develop-
ment of neural function from the sequence of its normal dissolution. Taking
this one step further, predicting the sequence of the normal development of
neural function from the sequence of its abnormal dissolution due to localized
brain damage is radically — and conceptually — different. In fact, some have
even questioned whether the abnormal aging brain is an adequate model of the
abnormal developing brain.
Finally, those of us who study infants for a living have come to realize the
risk inherent in proclaiming that infants cannot do this or that. The study of
human infants is itself in its infancy. It has become increasingly apparent that
infants may do tomorrow what they seemed unable to do yesterday. Our new
insights have resulted from the time-honored principle of “building a better

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x THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

mousetrap.” As researchers discover new and better techniques for asking

infants what they can and cannot do, we acquire new and ever-changing views
of their capacities. That, in a nutshell, is what this book is all about.
For the title of this book, we selected the descriptive terms implicit and
explicit memory because they refer to forms of memory and do not commit us
to a particular memory-systems or processing approach. Our first aim in
preparing this book is to provide a state-of-the-art exposition of the issues and
facts surrounding the early development of implicit and explicit memory. Our
second aim is to encourage young researchers to ask Big Questions — and to
not be dissuaded by the current Zeitgeist from doing so.
The research reported in this book was supported by grant nos. R37-
MH32307 and K05-MH00902 from the National Institute of Mental Health
(CRC) and by Marsden grant nos. U00609 and U00703 from the Royal
Society of New Zealand (HH, MC).

Carolyn Rovee-Collier, Piscataway, New Jersey, USA

Harlene Hayne, Dunedin, New Zealand
Michael Colombo, Dunedin, New Zealand

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CHAPTER 1

Background of the Problem

This chapter reviews the origins of the popular notion that two, functionally distinct
memory systems mature at different rates during the infancy period. Young infants are
thought to share with amnesics an early memory system which supports implicit memory;
the late memory system, which is damaged in amnesia and supports explicit memory, is
thought to mature late in the first year. Recent evidence from preverbal infants, however, is
inconsistent with this view.

How memory develops has been a topic of long-standing debate. Early

theorists argued that the behavior of older infants and children is shaped by
their earlier experiences (Watson 1930) and that adult personality is shaped by
memories of events that occurred in infancy (Freud 1935). Their underlying
assumption was that infants are endowed with a capacity for long-term
memory — a means of preserving a relatively enduring record of their early
experiences. Later theorists argued that infants younger than 18 months of age
are incapable of representation (Piaget 1952), are not capable of forming
enduring memories early in development (Kagan 1984), and cannot remember
events over long periods before they are able to talk about them (Nelson
1990). These views are consistent with the assumption that young infants
possess only a primitive memory system that mediates memories of proce-
dures and simple learning (i.e., implicit memories) and lack the more ad-
vanced memory system that mediates memories of specific experiences (i.e.,
explicit memories) until relatively late in their first year (Nelson 1995;
Schacter & Moscovitch 1984; Squire 1992a). The assumption that infants
cannot retain information about their past experiences leads to fundamentally
different conclusions about the importance of early experience.
Over the years, the debate over the development of implicit and explicit
memory has been waged in the absence of data from infants themselves,
largely because of the difficult problem of finding a task that could be used to

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2 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

study immature infants over an extended period of development. Now, this

problem has been solved, enabling scientists to take a fresh look at the
development of infant memory.

History of the problem

The notion that adults possess multiple memory systems is not new. As long ago
as the late 1800s, philosophers, psychologists, psychiatrists, and neurologists
proposed different typologies of long-term memory (for a listing, see Hermann
1982). What is new, however, is the notion that these memory systems develop
hierarchically during the infancy period (Naito 1990; Schacter & Moscovitch
1984; Tulving 1983). How did this notion come about?
The origins of this belief are two-fold. For one thing, it seemed intuitively
unlikely that organisms as immature and helpless as infants could have
memories that in any way resemble our own. Over the years, this intuitive
belief has been reiterated in countless general psychology and child develop-
ment texts (e.g., Bjorklund, 2000). Secondly, the initial studies of infant
memory suggested that young infants were incapable of retention longer than
only a few seconds or minutes at most (e.g., Kagan & Hamburg 1981; Werner
& Perlmutter 1979). These findings, however, were derived from measures of
young infants’ looking behavior in a task that is an analog of the delayed-
matching-to-sample paradigm — the paradigm that researchers traditionally
used to study short-term memory in rats (Roberts 1972a, 1974), pigeons
(Grant & Roberts 1973; Roberts & Grant 1976; Shimp & Moffitt 1974;
Zentall 1973), and monkeys (D’Amato 1973; Jarrard & Moise 1971; Jarvik,
Goldfarb & Carley 1969). Findings that older infants can remember for longer
periods of time came from motorically more demanding tasks, such as object
search tasks, that very young infants are physically incapable of performing.
In the mid-1980s, the disparity between the memory performance of
younger and older infants was attributed to two different and functionally
distinct memory systems — the early memory system and the late memory
system — that were hypothesized to mature at different rates during the
infancy period (Schacter & Moscovitch 1984). The early memory system was
thought to mediate implicit memory — a primitive form of memory for
procedures or skills that is long-lasting and does not require conscious recol-
lection or intentional retrieval, whereas the late memory system was thought

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BACKGROUND OF THE PROBLEM 3

to mediate explicit memory — the more advanced, adult-like form of memory

for events that requires intentional retrieval and is accompanied by the con-
scious awareness of having experienced the event before.
The hypothesis that two distinct memory systems mature at different rates
and mediate different forms of memory has been repeated so often that it is
now generally regarded as a statement of fact. Most scientists, for example,
believe that empirical evidence actually supports the widespread claim that
very young infants are capable only of implicit memory and that the capacity
for a qualitatively different form of memory does not appear until infants are
much older — but no such evidence exists. In fact, until recently, the develop-
ment of memory had not even been systematically studied with infants.

Origins of the developmental hypothesis

The notion that two, functionally distinct memory systems underlie memory
performance initially arose when researchers found that amnesic and Korsakoff
patients exhibited excellent performance on some memory tests but were
severely impaired on others (Milner, Corkin & Teuber 1968; Scoville & Milner
1957; Warrington & Weiskrantz 1968, 1970). Subsequently, Tulving (1972,
1983) proposed that there were two types of memory systems — the semantic
memory system and the episodic memory system, citing data from amnesics in
support of this dichotomy. He characterized the semantic memory system as
appearing early in development and the episodic memory system as appearing
late in development. Schacter and Moscovitch (1984), however, were the first
to draw a direct parallel between the memory abilities of infants and amnesics,
suggesting that both possess only an early memory system. They assumed that
the memory system that was lost in amnesia matured late in the first year of life.
One year later, Graf and Schacter (1985) introduced the terms implicit and
explicit memory, which were then applied to the forms of memory supported by
the early and late memory systems, respectively. Since that time, the poor
memory performance of brain-damaged amnesics has generally been accepted
as the evidence that implicit and explicit memory emerge sequentially in infancy
during the course of normal development.
Ironically, researchers have only recently begun to study memory devel-
opment directly in infants. Two approaches are commonly taken to study the
development of implicit and explicit memory during the infancy period. The

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4 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

first approach emphasizes conscious recollection as the defining characteristic

of explicit memory. Researchers who follow this approach seek tasks that
amnesics fail but that normal adults solve using conscious recollection. If
preverbal infants can also solve them, then they are assumed to have solved
them by using conscious recollection.
The second approach is strictly empirical and does not invoke the concept
of conscious awareness one way or another. Researchers who follow this
approach assess the functional relationships between various independent
variables that affect adults’ implicit and explicit memory performance differ-
ently on implicit and explicit tasks. If the variables that have a profound effect
on explicit memory performance but have little or no effect on implicit
memory performance in normal adults produce the same functional memory
dissociations in preverbal infants, then infants’ memory performance is as-
sumed to reflect the operation of the same underlying memory systems.

The present exposition

In the following chapters, we review what is known about the development of

implicit and explicit memory. In Chapter 2, we describe the general character-
istics of implicit and explicit memory and the tasks that have been used with
adults to measure them. In Chapter 3, we review what is known about the
neural mechanisms that underlie implicit and explicit memory and discuss the
classic studies of human amnesics that prompted researchers to search for
different neuroanatomically-based memory systems in the first place. In
Chapter 4, we describe the Jacksonian principle and the evidence for the
development and dissolution of memory from studies with rats. We also
consider the generality of the Jacksonian principle for the development of
implicit and explicit memory in verbally competent children and its dissolu-
tion in human adults. In Chapter 5, we review the developmental evidence
from nonhuman primates that is typically cited as support for the proposition
that two different memory systems mature at different rates. In Chapter 6, we
introduce the various memory tasks that have been used with human infants
and evaluate what these tasks have revealed about the development of implicit
and explicit memory. In Chapter 7, we consider the large number of experi-
mental dissociations that are taken as evidence for implicit and explicit
memory in adults and review evidence that corresponding functional dissocia-

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BACKGROUND OF THE PROBLEM 5

tions also characterize the memory performance of preverbal infants. In

Chapter 8, we review the major structural and processing accounts of memory
dissociations in adults and consider their adequacy for describing infant
memory performance. In Chapter 9, we consider the implications of data from
infants for current concepts of implicit and explicit memory. Finally, in the
Epilogue (Chapter 10), we summarize what recent studies with young,
preverbal infants have revealed about the development of implicit and explicit
memory and reflect on the lingering resistance in some quarters to the over-
whelming amount of experimental evidence that implicit and explicit memory
do not develop hierarchically.

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CHAPTER 2

Distinctions between
Implicit and Explicit Memory

In this chapter, we review the characteristics that distinguish implicit from explicit memory
and describe the various tasks that have been used to measure them. Memory retrieval that
is accompanied by conscious awareness of having previously experienced an event is
widely regarded as the defining characteristic of explicit memory. Because animals and
very young children are thought to lack the capacity for conscious recollection, they are also
thought to be incapable of explicit memory. Therefore, we have focused particularly on the
potential contributions of conscious and unconscious processes to memory performance,
the means by which their contributions might be differentiated, and the significance of
consciousness for memory research with infants. Finally, we consider whether implicit
memory is a meaningful construct.

Popular support for two, functionally distinct memory systems initially arose
from empirical dissociations in the memory performance of amnesic adults
(Warrington & Weiskrantz 1968, 1970). Subsequently, similar dissociations
were observed in the memory performance of normal adults who were admin-
istered different instructional sets (Graf, Mandler & Haden 1982; Graf &
Schacter 1985). These memory dissociations have led to a number of impor-
tant inferences about functional dissociations in the cognitive processes and
neural mechanisms that might underlie them (see Chapter 3).

Experimental dissociations in adult memory performance

Tulving (1983) described the rule of experimental dissociation as follows:

“Dissociation is said to have occurred if it is found that the manipulated
variable affects subjects’ performance in one of two tasks, but not in the other,
or affects the performance in different directions in the two tasks. Thus,

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8 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

dissociation refers to the absence of a positive association between dependent

variables of two different tasks” (p. 73).

He suggested that an analogous logic could be applied to studies of develop-

mental or pathological dissociations by comparing the performance of groups
differing in age or pathology on two tasks.
In fact, one of the earliest reported dissociations was of the latter type.
Warrington and Weiskrantz (1970) administered free recall and recognition
tests as well as two priming tests (word-fragment completion involving de-
graded letters and stem-completion tests) to a group of brain-damaged amnesics
and a control group composed of patients without brain damage. They found
that amnesics’ retention on the first two tests was impaired, but their perfor-
mance on the priming tests was not. Since then, other researchers using a variety
of tasks have obtained similar results, namely, preserved learning on one
general type of task but not on another (Jacoby & Witherspoon 1982;
Moscovitch 1982; Shimamura & Squire 1984; for review, see Shimamura
1986).
Analogous dissociations were subsequently documented in normal adults,
who performed differently on recall/recognition tasks than on various priming
tasks as a function of a variety of independent variables after being instructed
to base their test response on a prior specific episode (e.g., the study episode)
or to respond with the first answer that comes to mind, making no reference to
a prior episode, respectively (Graf et al. 1982; Graf & Schacter 1985; Hintzman
1990; Schacter 1987; for review, see Richardson-Klavehn & Bjork 1988).
These findings suggested that amnesics were capable of initially encoding
information about a specific event but subsequently had difficulty in gaining
awareness of it (Crowder 1988).

Characteristics of implicit and explicit memory

Implicit and explicit memory are descriptive concepts that originally referred
to different forms of memory as well as to the memory tests that were used to
measure them (Graf & Schacter 1985). The type of memory tapped by priming
tests was referred to as implicit memory, whereas the type of memory tapped
by recall and recognition tests was referred to as explicit memory. Graf and
Schacter cited three lines of evidence supporting a distinction between im-
plicit and explicit memory. First, healthy adults performed differently on

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DISTINCTIONS BETWEEN IMPLICIT AND EXPLICIT MEMORY 9

priming and recall/recognition tests in response to a variety of different

experimental manipulations: Manipulations that affected their performance on
recall/recognition tasks typically did not affect their performance on priming
tasks. These performance differences are characterized as functional dissocia-
tions. Second, performance on recall/recognition tasks was stochastically
independent of performance on priming tasks. Third, the memory perfor-
mance of densely amnesic patients was impaired on recall/recognition tasks
but not on priming tasks.
Although the terms implicit and explicit were not originally intended to
refer to hypothetical memory systems, such as procedural and declarative
memory (Squire 1987) or semantic and episodic memory (Tulving 1983),
many researchers currently use these terms to refer to different underlying
memory systems (e.g., Nelson 1998; see also Willingham & Preuss 1995) — a
practice that has engendered increasing concern (e.g., Schacter & Tulving
1994). Moreover, the same evidence that Graf and Schacter (1985) originally
cited as support for distinguishing between implicit and explicit forms of
memory and the tests that measure them has also been cited as support for
distinguishing between different memory systems. As forms of memory,
however, implicit and explicit memory are equally amenable to explanation
by various processing accounts that are based on a single memory system (see
Chapter 8).
Generally speaking, what most laymen think of as everyday memory is
what theorists have described as explicit memory. In contrast, the category of
implicit memory is relatively new. It is commonly assumed that explicit
memories are dated by the time and place that an event occurred; implicit
memories are not. Thus, a woman may look familiar to an individual, but he
may be unable to specify when or where he previously encountered her, which
is the hallmark of explicit memory. Theorists frequently associate the term
remember with explicit memories and the term know with implicit memories
(Gardiner & Java 1993). The difference pertains to the rememberer’s self-
awareness of the time and/or place of a particular past happening versus the
individual’s general world knowledge.
The features that have been used to distinguish implicit memory from
explicit memory are summarized in Table 2.1. These features include many of
those that were originally proposed by Mandler (1985, p. 93) to distinguish
between automatic and nonautomatic memories and by Tulving (1983, p. 35)
to distinguish between semantic and episodic memory. Implicit memory is seen

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10 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

as a phylogenetically primitive form of memory, whereas explicit memory is

thought to have appeared relatively late in phylogeny (Sherry & Schacter 1987).
Also, whereas implicit memory is widely thought to become functional early in
ontogeny, explicit memory is thought to become functionally mature much later
in the infancy period (Schacter & Moscovitch 1984). Implicit memory is
preserved after explicit memory has been impaired by the brain damage that is
associated with various forms of organic amnesia.
Additionally, access to explicit memories tends to be effortful, deliberate
(intentional or voluntary), and slow. A college student who tries to remember
the name of his former biology teacher, for example, may end up recollecting
a number of things about the teacher or the biology class before eventually
remembering the sought-for name — if he ever does. Being able to retrieve
some but not all aspects of an explicit memory for which one is searching is
known as the tip-of-the-tongue phenomenon. Moreover, while trying to re-
member the name, the student cannot readily engage in other mental activities.

Table 2.1. Frequently Cited Distinctions Between Implicit and Explicit Memory
Implicit Memory Explicit Memory
phylogenetically primitive phylogenetically more advanced
early maturing late maturing
spared in amnesia impaired in amnesia
unconscious conscious
nonepisodic episodic
general highly specific
abstract concrete
automatic controlled
involuntary voluntary
direct access indirect access
fast access slow access
all-or-none retrieval partial retrieval
no capacity demand limited capacity
weighted for object form weighted for object function
perceptually-based conceptually-based
context-free context-dependent
incidental intentional
nonassociative associative
temporally persistent time-limited
inflexible flexible
know remember

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DISTINCTIONS BETWEEN IMPLICIT AND EXPLICIT MEMORY 11

Thus, the capacity of explicit memory is limited. In contrast, access to implicit

memories is noneffortful, incidental, and fast. An implicit memory simply
pops into mind, uncontrollably and involuntarily. In fact, it may intrude into
the individual’s consciousness while he or she is doing something else. Its
retrieval does not result from a time-consuming search process and requires no
conscious capacity.
In fact, of the many characteristics in Table 2.1 that distinguish implicit
from explicit memory, the distinction that is most often invoked is the role of
conscious awareness in memory retrieval. Explicit memory requires that an
individual be consciously aware of having previously had a specific experi-
ence (i.e., a sense of pastness), whereas implicit memory does not. Schacter
(1989) enunciated this distinction clearly:
“Explicit memory is roughly equivalent to ‘memory with consciousness’ or
‘memory with awareness.’ Implicit memory, on the other hand, refers to
situations in which previous experiences facilitate performance on tests that
do not require intentional or deliberate remembering” (p. 356).

Implicit and explicit memory tasks

The terms direct and indirect were introduced by Johnson and Hasher (1987)
to refer to different types of memory tasks and are often used interchangeably
with the terms explicit and implicit. Both explicit and direct tasks are generally
thought to require conscious recollection of a prior experience, whereas both
implicit and indirect tasks do not. Whereas memory performance on both
explicit and direct tasks is impaired in amnesia, memory performance on both
implicit and indirect tasks is not. The terms explicit and implicit, however, also
refer to different forms of memory, whereas the terms direct and indirect do not.
The tasks that are used in studies of explicit memory are familiar to
students of memory — recall, cued-recall, and recognition — and presumably
require the explicit remembering of a specific, prior study episode. According
to Mandler (1990), for example:
“Recall is defined as accessing (bringing to awareness) information about
something that is not perceptually present. By definition, recall is a conscious
product” (p. 486).

The various tasks that are used in studies of implicit memory are less familiar
(see Table 2.2). The implicit tasks that have figured prominently in studies of

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12 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

memory development are considered in more detail below. In these tasks,

participants are shown an initial study list and are asked to report the first word
that comes to mind during the ensuing memory test. Implicit tasks are de-
scribed as repetition priming tasks (or, simply, as priming tasks) because the
initial presentation of an item presumably primes or increases its accessibility,
thereby facilitating the accuracy and rapidity of responding when the item is
presented again during the test. (In all instances, an explicit version of these
tasks can be constructed by showing participants the same study list but asking
them to recognize or recall a specific item that had appeared on the original
list.) Although verbal materials were originally used in explicit and implicit
tasks, pictorial materials have been used more recently in some studies (e.g.,
Musen & Treisman 1990; Schacter & Cooper 1993; Schacter, Cooper &
Delaney 1990; Schacter, Cooper, Delaney, Peterson & Tharan 1991a), par-
ticularly in memory studies with young children.

Table 2.2. Implicit Memory Tasks Used with Amnesics and Normal (Instructed) Adults
Task Study
fragmented picture identification Warrington & Weiskrantz 1968
word completion Warrington & Weiskrantz 1970
short-term memory Baddeley & Warrington 1970
free association of related information Schacter 1986; Shimamura & Squire 1984
preference judgments Kunst-Wilson & Zajonc 1980
perceptual identification (words) Jacoby & Dallas 1981
word-stem completion Graf, Mandler & Haden 1982
lexical decision Moscovitch 1982
homophone spelling Jacoby & Witherspoon 1982
shadow-face identification Tulving 1984
anagram solution Dominowski & Ekstrand 1967
word completion with new associates Graf & Schacter 1985
serial reaction time Nissen & Bullemer 1987
classical conditioning Woodruff-Pak 1993
skill learning Schwartz & Hashtroudi 1991
perceptual identification (objects) Biederman & Cooper 1991, 1992
object decision Cooper, Schacter, Ballesteros & Moore 1992
precuing serial order Clayton, Habibi & Bendele 1995

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DISTINCTIONS BETWEEN IMPLICIT AND EXPLICIT MEMORY 13

Word-stem or word-fragment completion

In these tasks, adults are asked to study a list of words and are then presented
with either word stems composed of the first three letters at the beginning of
the words (ass-) or word fragments with several letters missing (a - - a - - - -).
Their task is to complete the word stem or word fragment with the first word
that comes to mind. Some or all of the word stems can be completed with
words that previously appeared on the study list (assassin) or with a number of
other words (assiduous, assail, asset), but each word fragment has a unique
solution and can be completed only with a word from the prior study list.
Subjects tend to use words from the previously studied list to complete both
the stems or fragments.

Picture or picture-fragment completion

These tasks are like the word-stem or word-fragment completion tasks except
that participants are tested with nonverbal materials. In these tasks, subjects
study a set of pictures and then are asked to perceptually identify them from
either fragmented or otherwise degraded versions of the same picture. In some
studies, researchers present picture fragments at a number of different levels
of perceptual completion, from most fragmented to most complete, via an
ascending method of limits until the fragment is correctly identified (e.g.,
Mitchell 1993; Snodgrass & Feenan 1990). The priming effect is measured as
the difference in accuracy of identifying old and new pictures.

Object and lexical decision tasks

In the object decision task, adults are shown line drawings of unfamiliar
objects, some that can actually exist in three-dimensional space (possible
objects), and some that cannot (impossible objects). During the initial expo-
sure phase, subjects are asked to judge the direction that each object faces.
During testing with some old and some new objects, they must decide as
rapidly as possible whether the test objects are possible or impossible. Pos-
sible objects that have been seen before show priming effects, but impossible
objects do not (Cooper, Schacter, Ballesteros & Moore 1992). The lexical
decision task, an older verbal version of this task, is the same except that the
study list contains either words or nonwords, and subjects must decide during

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14 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

testing whether a letter string represents a real word or a nonword (e.g.,

Moscovitch 1982).

Serial reaction time (SRT) task

This task was introduced by Nissen and Bullemer (1987) and has since been
used with both normal and amnesic adults (for review, see Curran 1998) and
children (Meulemans, Van der Linden & Perruchet 1998). In this task, a cue
light is illumined on each trial under one of four keys that are arranged
horizontally. The subject’s task is to press the key above the light as rapidly as
possible. When the response key is pressed, the cue light goes off and, after a
brief delay, another cue light is illumined under a different key. The cue lights
are illumined in either a repeating or a random sequence, but subjects are not
informed when the sequence of lights is repeating. The RTs of subjects tested
on a repeating sequence decrease over successive trials, suggesting that sub-
jects are learning the sequence and anticipating which key will be signaled
next. However, a decrease in RT per se is not sufficient for inferring sequence
learning because subjects become practiced with nonsequential aspects of the
task as well (e.g., mapping the response key to the corresponding stimulus).
Therefore, the difference in RT on adjacent trial blocks on which the sequence
is repeating (S) and random (R) is usually taken as the primary measure of
sequence learning (R-S).
The clearest evidence that the SRT task measures implicit memory comes
from a within-subjects study in which students were given scopolamine, a
drug that induces temporary amnesia. Although the drug did not impair their
retention of the repeating-sequence SRT task, they were unable to press the
correct key when asked where the next light would appear — an explicit
memory task (Nissen, Knopman & Schacter 1987).

Simple classical conditioning

In classical conditioning, an association is learned between two stimuli — an

unconditional stimulus (UCS) that initially elicits an unlearned or involuntary
reflex (the unconditional response, or UCR) and a conditional stimulus (CS)
that does not initially elicit that reflex. In the classical conditioning paradigm,
the CS is repeatedly paired with the UCS in close temporal contiguity until it
elicits a reflex (the conditional response or CR) that is fundamentally the same

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DISTINCTIONS BETWEEN IMPLICIT AND EXPLICIT MEMORY 15

as the unlearned reflex that the UCS had originally elicited. The percent of
trials on which a CR occurred indexes how well the subject learned that the CS
predicts the UCS. The development of the CR during acquisition can be
measured by either its occurrence on successive UCS-omission trials (e.g., on
every fifth trial, the CS is presented without the UCS) or its anticipatory
production in the interval between the CS and the UCS over successive trials.
In the latter case, the CR initially occurs immediately after the CS and then its
latency becomes progressively longer until it immediately precedes and par-
tially overlaps with the UCS. The gradual increase in the occurrence of the
anticipatory CR over trials is usually classified as an instance of procedural
memory or implicit memory. Retention is usually expressed in terms of
savings during reacquisition. Because the two events that become associated
need not be verbal, and verbal instructions are unnecessary for performing the
task, classical conditioning can be used with nonverbal subjects.
Woodruff-Pak (1993) found that the amnesic H.M. exhibited savings in
classical eyeblink conditioning to a tone 2 years after his original condition-
ing, reaching criterion in one-tenth the number of original acquisition trials,
even though he could not remember them.

Problems with the implicit/explicit distinction: Consciousness and

independence

Consciousness

Tulving (1985) distinguished three kinds of consciousness, each of which was

associated with a different memory system. At one end of the continuum was
anoetic consciousness or nonknowing consciousness, which characterized
procedural memory — the most primitive memory system. Tulving associated
this type of consciousness (or lack of consciousness) with the prewired or
preprogrammed reactions of simple animals, plants, computers, and learning
machines to external or internal stimuli (e.g., the expression of fixed action
patterns, instinctive behavior, skill learning, classical and operant condition-
ing, and any gradually incrementing behavior that accrued with what came
before). The intermediate level of consciousness, noetic consciousness or
knowing consciousness, characterized semantic memory — a specialized
subsystem that evolved out of procedural memory. Tulving described this type

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16 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

of consciousness as making possible the introspective behavior and factual

world knowledge of lower animals, human infants, and brain-damaged indi-
viduals. Because they operate without conscious awareness, Tulving likened
procedural and semantic memory to implicit memory.
At the other end of the continuum was autonoetic consciousness or self-
knowing consciousness. Autonoetic consciousness characterized episodic
memory — a specialized subsystem of semantic memory — and allowed
individuals the subjective sense of self awareness that accompanies the autobio-
graphical recollection of the past and the realization of future existence. By this
account, consciousness at a particular level on the continuum could be impaired
without affecting consciousness at a lower level. Amnesics and infants, for
example, lack episodic memory and autonoetic consciousness but have proce-
dural memory and noetic consciousness. Because it requires conscious recollec-
tion, Tulving likened episodic memory to explicit memory.
Obviously, Tulving’s (1985) distinctions are untenable from both devel-
opmental and comparative perspectives. Whether an infant or an animal is
consciously aware of having previously experienced an event or has a sense of
pastness cannot be directly tested and will always remain in the sole domain of
philosophical speculation (see also Shapiro & Olton 1994). Yet, this distinc-
tion has become the primary basis for assuming that memory in preverbal
infants and animals is implicit only — an assumption that is shared by most
memory researchers whether they posit multiple memory systems or only a
single memory system with multiple processes (e.g., Bauer 1996; Mandler
1984, 1990; McDonough, Mandler, McKee & Squire 1995; McKee & Squire
1993; Naito & Komatsu 1990; Schacter & Moscovitch 1984; Tulving &
Schacter 1990). Apparently, because it is impossible to demonstrate directly
that preverbal infants and animals are capable of explicit memory, and perhaps
because researchers also have little or no recollection of their own infantile or
early childhood experiences, they have simply assumed that infants lack the
capacity for explicit memory. To quote Olton (1989), however, “the absence
of proof … is not proof of absence” (p. 167).
Ironically, data from hippocampal lesion studies with rats and nonhuman
primates, in whom conscious awareness also cannot be measured, are fre-
quently cited as evidence for the distinction between implicit and explicit
memory (e.g., Zola-Morgan & Squire 1984; for reviews, see Bachevalier
1990; Nadel 1994; Squire 1987, 1992b; Zola-Morgan & Squire 1985b). In
addition, some investigators have developed animal models of human amne-

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DISTINCTIONS BETWEEN IMPLICIT AND EXPLICIT MEMORY 17

sia that use a delayed-nonmatching-to-sample task as a recognition test (e.g.,

Clower, Alvarez-Royo, Zola-Morgan & Squire 1991; Zola-Morgan & Squire
1985b, 1990b). Both of these practices were challenged by Olton (1989).
Willingham and Preuss (1995) concluded that because people cannot
agree about what consciousness is, its role in memory cannot be defined and,
as a result, the construct does not add to our understanding of memory. They
argued that classifying memory into two fundamentally different types re-
quires that they have two fundamentally different explanations, but question
whether consciousness can be the critical attribute that distinguishes them.
Because the role of consciousness is unknown, hence too are the ways in
which conscious and unconscious memory systems would need to be differ-
ent: “Consciousness, because we know nothing about it, implies nothing about
why memories that have or do not have it might be different” (Willingham &
Preuss 1995 [4.8]).
Dissociating Conscious and Unconscious Contributions to Memory Per-
formance. A number of researchers have warned that performance on tests of
implicit and explicit memory is rarely process-pure; that is, performance on
implicit tests often reflects the contribution of an explicit component, and vice
versa (e.g., Jacoby, Toth & Yonelinas 1993; Rajaram 1993; Snodgrass 1989).
Jacoby (1991) wrote:
“most past investigations of automatic (unconscious) influences of memory
or perception assumed a one-to-one mapping between processes and tests.
The drawing of conclusions, then, requires that tests be factor- or process-
pure with regard to the type of processing they measure. A difficulty for
identifying processes with tasks is that tasks are probably never process-
pure….That problem is not fully solved by finding task dissociations between
manipulations or between subject populations and type of test” (p. 531).

The problem of cross-contamination in interpreting data from implicit tests is

compounded by the possibility that, after a few trials, some subjects may catch
on to the fact that some of the items on the implicit test had been on the study
list and intentionally recall information from the study session to perform the
task. In this case, the implicit test would, practically speaking, be an explicit
test (see also Richardson-Klavehn & Bjork 1988). The magnitude of this
problem is illustrated in a study on implicit memory development by Russo,
Nichelli, Gibertoni and Cornia (1995; see Chapter 4). Using the picture-
fragment completion task, previous researchers had found that implicit
memory performance improved with age (Parkin 1993; Parkin & Streete

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18 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

1988). Because explicit memory performance typically improves with age,

but implicit memory performance does not, these results raised the possibility
that conscious recollection may have contributed to subjects’ implicit test
performance. When Russo et al. partialed out the influence of explicit recol-
lection, however, they found that implicit memory performance was age-
invariant.
As it became increasingly apparent that memory performance on implicit
and explicit tasks was unlikely to reflect the exclusive operation of either an
explicit or an implicit memory process, researchers struggled to find a way of
splitting the relative contributions of conscious from unconscious processes to
memory performance. The retrieval intentionality criterion solution was intro-
duced to control for the effects of unconscious influences on explicit memory
performance (Schacter, Bowers & Booker 1989). Schacter et al. (1989) pro-
posed that before data are accepted as measures of explicit and implicit memory,
they should meet a retrieval intentionality criterion. The criterion was necessi-
tated by the fact that normal adults occasionally exhibited parallel effects on
explicit and implicit tests when the manipulated variables produced memory
dissociations on the same tests in amnesics. Based on the assumption that a
memory dissociation on explicit and implicit tests cannot result if retrieval in
both cases is intentional, the criterion provides an empirical means of ruling out
the contribution of intentional retrieval on implicit tasks.
The retrieval intentionality criterion has two basic parts. Its first part
requires that the study episode be the same for both types of test and that all of
the nominal retrieval cues provided at the time of testing also be identical
except the instructions given to the subject prior to each test. Instructions for
implicit tests do not require subjects to think back to the study episode in order
to respond, whereas instructions for explicit tests do. The latter stipulation was
based on the original observation by Graf et al. (1982) that changing the
instructions for normal adults altered the nature of their memory test from a
priming to a cued-recall test. As a result, normal adults and amnesics exhibited
the same memory dissociations on implicit and explicit memory tests. Its
second part requires that the independent (manipulated) variable have a differ-
ent effect on memory performance in implicit and explicit tests. In this way,
differential performance on the test would presumably be attributable only to
the retrieval processes associated with the instructions; that is, retrieval would
be either intentional (explicit memory) or unintentional (implicit memory).
Graf and Schacter (1985) confirmed that the instructions that were used

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DISTINCTIONS BETWEEN IMPLICIT AND EXPLICIT MEMORY 19

to induce memory performance affected the sensitivity of a test as a measure

of implicit or explicit memory. In Experiment 1 of their study, they varied the
instructions that were given to college students prior to performing implicit
and explicit tests of memory for related word pairs. For the priming (implicit
memory) test, they instructed students to complete word-fragments as quickly
as possible with “the first word that [came] to mind.” For the cued-recall
(explicit memory) test, they reminded students of the word pairs they had
previously studied, told them that the test words were the stimulus words from
those pairs, and instructed them to recall the response word that had been
paired with each stimulus word. As before, normal, healthy adults exhibited
the same dissociation on explicit and implicit tests as amnesics if explicitly
instructed to respond on the basis of the original study episode or not,
respectively.
In a follow-up experiment, they gave a new group of students a list of
unrelated word pairs and instructed them before both tests (word completion
and cued-recall) that the cues were related to the word pairs they had studied
and that they should use the cues to aid recall of the words from the study list.
Their basic assumption was that if the instructions defined the form of
memory that the test measured, then identical instructions would transform
both tests into tests of explicit memory. In fact, this was their finding, confirm-
ing that the test instructions determine whether a particular test that is used
with normal adults measures implicit or explicit memory.
The process-dissociation procedure was also introduced to disentangle the
conscious and unconscious contributions to adults’ memory performance but
was in reaction to the concerns that had motivated the retrieval intentionality
criterion, namely, that memory performance on indirect or implicit tasks might
be contaminated by intentional or conscious influences. Jacoby et al. (1993)
were concerned that memory performance on direct or explicit tests might be
contaminated by unintentional or unconscious influences. The probability of
recollection would be overestimated, for example, if automatic influences were
to increase the probability of correct guessing on cued-recall tests.
To correct for such influences, Jacoby et al. pitted the probability of
informed guessing or familiarity-based responding against the probability of
genuine recollection-based responding. Thus, for example, on a word-stem
completion test, unconscious influences would make subjects more likely to
complete the word stems with previously studied words (i.e., words that
automatically come to mind) than with new ones. Instructing subjects to

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20 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

complete the stems with words that were not presented earlier, however,
would produce the opposite result. To the extent that responding was under
their conscious control, Jacoby et al. assumed that subjects would select
against old words that they could actually recollect. Should they respond with
an old word, then their response would be attributed to unconscious influ-
ences, and the difference between responding with old and new words would
be taken as the measure of conscious recollection. The probability of using a
particular word as a completion for a stem when that word was not presented
during study serves as a baseline against which the effects of prior study can
be assessed. This baseline was subtracted from the calculated probability that
a word would automatically come to mind.
Although this procedure has revealed that recollection and familiarity
make statistically independent contributions to memory performance, there
are at least two problems with using the process-dissociation procedure to
assess the role of consciousness in memory processing. First, as Ratcliff and
colleagues pointed out:
“Process dissociation equations have two parameters (the probability of
recollection and the probability of familiarity being above a threshold), and
the equations are applied to only two data points in each experimental
condition. This means that the method will always produce estimates of two
components, even if the data were actually generated from a single process …
Furthermore, the interpretations of the components are valid only under the
process dissociation assumptions….Therefore, what is learned about con-
scious versus unconscious processes [in recognition] is theory dependent, and
process dissociation does not provide a theory-independent means of examin-
ing memory processes” (Ratcliff, Van Zandt & McKoon 1995, p. 359).

Second, the process-dissociation procedure cannot be used with nonverbal

subjects, and it is probably also unsuitable for younger children, who would be
likely to find the instructions about what to exclude from their responding
confusing.
Are Infants and Other Nonverbal Organisms Consciously Aware? The
question of whether organisms other than verbally competent humans possess
conscious awareness has vexed philosophers since the time of the ancient
Greeks. The issue was temporarily resolved in the 17th century by the Carte-
sian distinction between mind versus matter, or dualism. The recent introduc-
tion of the explicit versus implicit memory dichotomy with emphasis on
conscious awareness, however, has reinvigorated advocates of dualism as
well as its critics. In considering how conscious experience might be defined,

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DISTINCTIONS BETWEEN IMPLICIT AND EXPLICIT MEMORY 21

the philosopher John Searle suggested adopting a common-sense rather than

an analytic definition:
“‘Consciousness’ refers to those states of sentience and awareness that typi-
cally begin when we awake from a dreamless sleep and continue until we go
to sleep again, or fall into a coma or die or otherwise become ‘unconscious’”
(Searle 1995, p. 60).

Searle (1998) rejected dualism as obsolete. His conceptualization of con-

sciousness is grounded in three basic principles: (1) Consciousness consists of
inner, qualitative, subjective states and processes. (2) Consciousness cannot
be reduced to third-person phenomena investigated in the neurosciences. (3)
Consciousness is a biological process — a higher-order, natural feature of the
organic brain. In concluding that brain processes cause consciousness, he
echoed Hubbard’s (1975) earlier conclusion that mental phenomena are direct
consequences of neural activity. In arguing that conscious experience is an
emergent property of neurobiological processes in the brain, Searle likened it
to the solidity of a table, which is an emergent feature of the table’s molecular
structure: “mental states are both caused by the operations of the brain and
realized in the structure of the brain” (Searle 1983, p. 265). In other words, he
placed consciousness squarely in the realm of other, ordinary biological
phenomena, such as physiological thermoregulation, mitosis, and digestive
processes (Searle 1984, 1995).
In response to such arguments, however, Tulving (1987) argued that
“the problem of consciousness and memory is different from problems of
consciousness with which many generations of thinkers have wrestled …
problems such as what consciousness is, and how it emerges from the
physical-chemical brain activity… . [Instead it is] the selective but systematic
occurrence of conscious awareness in remembering, as well as in other mental
activities: Why are we — why must we be — consciously aware when we
remember a recent event that we have witnessed, and why is the same kind of
awareness missing when we use our stored knowledge, say, in solving a new
complicated problem?” (p. 75)

Pointing to the literature on memory dissociations in amnesics, Tulving drew a

sharp distinction between the form of memory in which amnesics express
knowledge in behavior without any accompanying awareness that they pos-
sessed that knowledge (i.e., implicit memory) and the form of memory of
which amnesics are incapable — the expression of knowledge which includes
their introspective awareness of it (i.e., explicit memory). Although the dis-

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22 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

tinction between consciousness and conscious awareness is intuitively appeal-

ing, Tulving did not offer an operational definition of conscious awareness
(see also Shapiro & Olton 1994, p. 108), nor did he suggest a way of
distinguishing it from consciousness or conscious experience.
Several decades ago, a similar issue arose in the field of animal communi-
cation. At that time, the common assumption underlying distinctions between
animal language and human language was that animals lack both conscious
awareness of their own mental experiences (if they had any) and a conscious
intent to communicate (e.g., Terwilliger 1968). Griffin (1976), however,
characterized this assumption as antagonistic to the “general principle of
evolutionary kinship and continuity” between animals and men and argued:
“the hypothesis that some animals are indeed aware of what they do, and of
internal images that affect their behavior, simplifies our view of the universe
by removing the need to maintain an unparsimonious assumption that our
species is qualitatively unique in this important attribute” (p. 101).

Like Searle, Griffin proposed that mental experiences are directly linked to
neurophysiological processes which, he noted, are highly similar in all multi-
cellular animals.

Independence

A major source of evidence supporting a distinction between two memory

systems is that memory performance on an implicit test is independent of
memory performance on an explicit test. Independence can take two forms —
stochastic independence (Graf & Schacter 1985; Tulving, Schacter & Stark
1982) and functional independence (Tulving 1985; Tulving et al. 1982).
Stochastic independence is demonstrated when the joint probability of memory
performance on implicit and explicit tasks is equal to the product of their simple
probabilities. Functional independence is demonstrated when an independent
variable affects memory performance on implicit and explicit tasks differently.
These two kinds of independence, however, need not coexist in the same data
set. Greene (1986), for example, failed to find stochastic independence between
memory performance on a word-stem completion task and on a recall task in
which word stems were used as explicit retrieval cues, but he did find functional
independence between memory performance on the two tests. A similar result
turned up in data obtained by Graf and Mandler (1984, Experiment 3), who had

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DISTINCTIONS BETWEEN IMPLICIT AND EXPLICIT MEMORY 23

compared memory performance on a word-stem completion test with memory

performance on a cued-recall test in which word stems were the retrieval cues.
Although Graf and Mandler reported evidence of functional independence
between the tests, a reanalysis of their data found no evidence of stochastic
independence between them (Greene 1986).
Stochastic Independence. One criterion for distinguishing two forms of
memory is that memory performance on two different tests of the same items
that presumably reflect the operation of different memory systems should be
stochastically independent. This requirement means that subjects should be as
likely to complete word-stems with old words or words they recognized as
with new words or words they did not recognize. On the other hand, memory
performance on two different tests that reflect the operation of the same
memory system should be correlated, meaning that they measure the same
thing — whatever it is. Tulving et al. (1982), for example, argued that if
memory performance on the two tests were mediated by the same memory
system, then subjects’ memory for individual items on the two tests should
have been correlated — but that also was not the case. He found that the joint
probability of recognition and word-fragment completion was indistinguish-
able from the product of the simple probabilities of recognition and fragment
completion, indicating that performance on one test was independent of
performance on the other. Moreover, this effect was found four times — for
both kinds of items (old, new) after two test delays (1 hour, 7 days).
In contrast, adults’ memory for individual items on recognition tests is
strongly correlated with their memory for individual items on recall tests (both
tests of explicit memory). Ogilvie, Tulving, Paskowitcz and Jones (1980), for
example, showed college students a list of familiar words and then gave them
both a yes/no recognition test and a cued-recall test in which associatively
related or rhyming words were the retrieval cues for words on the study list.
Four outcomes were possible — list words could be recognized and recalled,
recognized but not recalled, not recognized but recalled, and neither recog-
nized nor recalled. They found that the conditional probability of recognition
given recall was .90 for associative cues and .91 for rhyming cues. The fact
that the proportion of recalled words that subjects also recognized was greater
than the proportion of all words that they recognized indicated that the
measures of recall and recognition were positively correlated.
Interpretations of stochastic independence between implicit and explicit
tasks have been criticized because they are necessarily based on multiple

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24 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

measures of the same items. Thus, recognition is biased in the direction of

independence by the fact that subjects previously saw the same items on a
priming test hence experienced an additional “study” trial or exposure
(Greene 1986; Shimamura 1985; Tulving et al. 1982). More recent advances
in quantitative techniques hold promise for overcoming this problem. Using a
linear structural modeling approach, for example, Nyberg (1994) tested the fit
of a one-factor (i.e., one system) versus a two-factor model to students’
memory dissociations on two types of memory tests (semantic and episodic)
and rejected the one-factor but not the two-factor model. Nyberg noted that the
notion of a unitary memory system was not rejected, however, if semantic and
episodic memory were viewed as separate factors within the same memory
system, for example, in the declarative memory system.
Functional Independence. Functional independence refers to the relation
between two dependent variables that is found when a particular independent
variable (e.g., the retention interval) or subject variable (age, amnesia) affects
performance on one test but not the other (see Table 7.2). Functional indepen-
dence is manifested as a dissociation in memory performance on an implicit
and explicit test following the manipulation of a particular independent or
subject variable. Tulving et al. (1982), for example, argued that if a single
memory system had mediated adults’ performance on a word-fragment
completion (implicit memory) task and on a recognition (explicit memory)
task, then either they should have exhibited forgetting of previously studied
information over a 7-day retention interval on both implicit and explicit
memory tasks or they should have exhibited no forgetting on both tasks over
the same delay — but they did not. Instead, adults exhibited forgetting on the
explicit memory task but no forgetting on the implicit memory task.

What is implicit memory? A second look

Although explicit (declarative) memory appears to be a fairly coherent form of

memory that is associated with a fairly well-defined set of neuroanatomical
structures (Shimamura 1990; Squire, Knowlton & Musen 1993; Squire &
Zola-Morgan 1991), implicit (procedural) memory is not (Shimamura 1990;
Willingham & Preuss 1995). One characteristic that supposedly sets implicit
memories apart from explicit ones is their specificity or sensitivity to the
physical conditions of encoding and retrieval: Implicit (nondeclarative)
memories have been described as highly specific, whereas explicit (declara-

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DISTINCTIONS BETWEEN IMPLICIT AND EXPLICIT MEMORY 25

tive) memories have been described as relatively flexible (Cohen &

Eichenbaum 1993). Although evidence for specificity in rats and monkeys is
compelling, evidence for specificity in humans on priming, motor skill, and
other implicit memory tasks depends strongly on the conditions of testing (for
review, see Willingham 1998a).
The absence of conscious awareness is also thought to distinguish perfor-
mance on implicit memory tasks from performance on explicit ones, but
researchers cannot agree on how to define conscious awareness. Neuropsy-
chological data provide some basis for arguing that memories for which
subjects evidence conscious recollection require the integrity of the medial
temporal lobe and diencephalon, whereas memories that may not be associ-
ated with conscious recollection do not require these structures (Willingham
1994). As Willingham and Preuss (1995) pointed out, however:
“The role of consciousness in memory parallels the neuroscientific data in
another way. Lack of awareness as a characteristic does not really unify
implicit memory; rather, awareness sets explicit memory apart from the
others. Similarly, not relying on the hippocampus does not unify implicit
memories; rather, relying on the hippocampus sets explicit memory apart [our
italics]” (4.9).

Other researchers have expressed concern about the grab-bag nature of implicit
memory (Johnson & Hirst 1993; Roediger 1990a; Roediger, Srinivas & Weldon
1989a; Schwartz & Hashtroudi 1991; Willingham & Preuss 1995). A major
source of concern, for example, is the repeated finding of parallels in memory
performance on tests of implicit memory and explicit memory and functional
dissociations in memory performance on different tests of implicit memory. As
reviewed earlier, theorists have attributed the parallels to the contribution of
conscious recollection on implicit memory tests and to the contribution of
unconscious influences on explicit memory tests. The finding of dissociations
between tasks of implicit memory, however, is particularly problematic for the
construct validity of implicit memory. On the surface, for example, word-
fragment completion and perceptual word-identification tasks would seem to be
highly related, but researchers have found that memory performance on these
two tasks is not only uncorrelated (Perruchet & Baveux 1989) but is stochasti-
cally independent (Hayman & Tulving 1989; Witherspoon & Moscovitch
1989).
Some of the clearest evidence that different implicit tasks are functionally
independent has surfaced in studies comparing performance on the serial

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26 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

reaction time (SRT) task with performance on other tasks of implicit memory.
Healthy adults exhibit a decrease in RTs over successive trials when trained
with a repeating sequence (Willingham, Nissen & Bullemer 1989), as do
patients with Alzheimer’s disease (Knopman & Nissen 1987) and Korsakoff
syndrome (Nissen & Bullemer 1987). Like healthy adults, Korsakoff patients
also retain their memory of the repeating sequence for 1 week (Nissen,
Willingham & Hartman 1989). In contrast to their normal learning and
memory on the repeating-sequence SRT task, however, Korsakoff patients’
ability to learn a tactual style maze in which all blind alleys are blocked is
significantly impaired (Nissen et al. 1989). Because both the maze task and
the SRT task require the learning of a spatial sequence and, in normal adults,
performance on these tasks is facilitated by prior training, both are thought to
measure implicit memory. These data, then, reveal a memory dissociation
between two tasks of implicit memory.
Schwartz and Hashtroudi (1991) similarly found a dissociation between
implicit memory tasks. In Experiment 1 of their study, college students
exhibited skill learning in partial-word identification and inverted reading
tasks but not in a word-fragment completion task, but their amount of priming
in all tasks was the same. In Experiment 2, they tested priming and skill
learning with degraded words in the partial-word identification task. The
amount of priming was the same whether students had acquired the skill of
identifying degraded words or not. Importantly, the correlation between skill
improvement over trials and priming performance was negligible whether
subjects were tested immediately (r = .01) or after 1 week (r = .06). In
Experiment 3 of their study, they hypothesized that students might be more
skilled in learning to identify degraded words to which they had been
preexperimentally exposed more often (high-frequency words) than words
that occurred in language less often. If priming were unrelated to skill learn-
ing, however, then the frequency of occurrence of the words should not affect
it. They found that skill learning was significantly affected by word frequency,
but the amount of priming was not.
The large number of implicit memory tests that were functionally inde-
pendent of each other prompted researchers to elaborate different mechanisms
for explaining them. Schacter (1990), for example, proposed that priming
effects in different implicit memory tasks are best understood in terms of a
class of distinct memory modules or subsystems — the visual word form
system, the structural descriptions system — comprising a perceptual repre-

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DISTINCTIONS BETWEEN IMPLICIT AND EXPLICIT MEMORY 27

sentation system (PRS), which itself is a subsystem of semantic memory.

Schacter argued that the effect of word- and object-priming on these tests was
a presemantic phenomenon because performance was affected by perceptual
changes in the surface features of visual stimuli independent of whether the
study task required semantic processing or not. In representing the form and
structure of words (word form system) and objects (structural descriptions
system), these subsystems were thought to be functionally different from the
episodic memory system, which represents information about meaningful
events in space and time, but capable of interacting with it.
As an alternative to explaining memory dissociations in terms of sepa-
rable memory systems or subsystems that represent different kinds of informa-
tion, some researchers adopted a processing approach (e.g., Nelson, LaLomia
& Canas 1991; see Chapter 8) or sought a single theoretical principle (e.g.,
Snodgrass & Feenan 1990) to explain them. In the latter instance, the results of
a series of priming experiments with different levels of picture-fragment
completion led Snodgrass and Feenan (1990) to propose the perceptual clo-
sure hypothesis. By this account, priming effects are explained by a process
that operates at the time of retrieval: The minimal amount of information in the
prime that can support perceptual closure will yield optimal priming. Presum-
ably, the change that is induced in the perceived organization of the prime
allows the prime to be identified and facilitates retrieval. Because the subject’s
attention is focused outward on the physical characteristics of the prime, the
memory representation that is retrieved more or less perceptually matches the
perceived prime and is devoid of self-referent information that would locate
the prime in subjects’ historical past.
On explicit memory tests, however, the perceptual characteristics of the
retrieval cue are either deemphasized (recognition tests) or absent altogether
(recall tests). Rather, explicit tests require subjects to interrogate their memory
as to whether they previously encountered the target stimulus before. This
interrogation focuses subjects’ attention inward and necessitates the retrieval
of autobiographical information pertaining to time or place. According to the
perceptual closure hypothesis, therefore, conscious recollection is not a fun-
damental feature of explicit memory but is simply a by-product of the
attentional demands of explicit tests.

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28 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Conclusions

Despite the large number of recent books devoted to implicit memory, this
form of memory is still poorly understood. Willingham and Preuss (1995)
argued that because implicit memories are not supported by common brain
structures and do not use common processes and representations, implicit
memory is not a coherent system. Moreover, there is no common attribute that
links different implicit memory tasks such as priming, motor skill learning,
classical conditioning, mirror reading, perceptual identification, and so forth.
Johnson and Hirst (1993) made the same observation about procedural
memory tasks, namely, that they share no obvious common characteristics
except that amnesics cannot perform them. Changing the procedural/declara-
tive nomenclature to nondeclarative/declarative (Squire 1992a) did not alter
this basic problem. Nondeclarative memory remains a miscellaneous collec-
tion of tasks that are linked simply by the fact that they can be performed
without the neural structures that are required to perform declarative memory
tasks. In other words, nondeclarative tasks are, simply, not declarative.
Although the absence of conscious awareness is thought to characterize
performance in implicit memory tasks, there is no agreement about how to
define it. Moreover, because the function of conscious awareness is unknown,
it is impossible to specify how a memory system that is based on conscious
awareness differs functionally from one that is not (Willingham & Preuss
1995). As a result, any classification scheme that differentiates memory
systems on the basis of the presence or absence of conscious awareness fails
Sherry and Schacter’s (1987) criterion, the functional incompatibility of op-
erations (see Chapter 8), for establishing a new memory system.

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CHAPTER 3

Neuroanatomical Basis of Explicit and

Implicit Memory

We begin this chapter with an overview of the early studies of human amnesia that gave rise
to the notion of two, dissociable memory systems. We review similar evidence for two
dissociable memory systems in nonhuman animals — primarily, monkeys and rats. We then
discuss evidence for the neural substrates that are believed to underlie implicit and explicit
memory. We note that the concept of multiple memory systems emerged predominantly
from studies in which damage to the medial temporal lobe impaired explicit memory but not
implicit memory. Therefore, we present recent evidence that damage to the striatal system
impairs implicit memory but not explicit memory and consider the implications of this
evidence for multiple memory systems.

Studies of explicit and implicit memory in humans

The effects of MTL lesions

For quite some time, damage to the medial temporal lobes (MTL) in humans
has been known to produce severe memory impairments. The classic and
frequently cited example of the effects of such lesions is the patient H.M., who
underwent bilateral resection of the MTL (hippocampus, amygdala, and sur-
rounding tissue) in an effort to relieve intractable epilepsy that did not respond
to conventional anticonvulsive medication (Scoville & Milner 1957). Al-
though H.M.’s seizures were somewhat alleviated by the operations, he was
left with a profound memory impairment that persists to this date (Corkin
1984; Gabrieli, Cohen & Corkin 1988; Milner 1972; Milner et al. 1968).
In the original 1957 paper, most of H.M.’s memory impairments were
described anecdotally in terms of his postoperative failures to give accurate
dates, his age, or to remember that he had been talking with a particular

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30 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

individual just minutes earlier. For example, H.M. was operated upon in
September, 1953, when he was 27 years old. When asked during a psychologi-
cal examination 19 months later (in April, 1955) for the current date and his
current age, H.M. responded that the current date was March, 1953, and that
he was 27 years old. His response suggested that he had no memory for events
subsequent to his operation. In fact, so serious were his memory impairments
that after the operation,
“this young man could no longer recognize the hospital staff nor find his way
to the bathroom, and he seemed to recall nothing of the day-to-day events of
his hospital life” (Scoville & Milner 1957, p. 14).

According to Scoville and Milner, H.M. and patients with similar extensive
damage to the medial temporal lobe appear to “forget the incidents of their
daily life as fast as they occur” (p. 15).
Despite his profound memory impairment, H.M. performed normally on
tests of intelligence, reasoning, and perceptual abilities (Milner et al. 1968). He
was also able to remember a list of numbers and words if he was not distracted
during the retention interval (Scoville & Milner 1957). Although his memory
for events of his childhood appeared to be quite normal, H.M. did have difficulty
remembering information that occurred within the 3 years prior to his surgery.
In current terminologies, his memory deficits were characterized both by a
severe anterograde amnesia (difficulty in forming new memories) and a limited
retrograde amnesia (memory impairments for events prior to the operation).
The characteristics of H.M.’s memory impairments have since been observed
in many other patients with medial temporal lobe damage (Cummings,
Tomiyasu, Read & Benson 1984; Victor & Agamanolis 1990; Victor,
Angevine, Mancall & Fisher 1961). According to the convention we have
adopted in this book, H.M. is said to suffer from impairments in explicit memory.

Some memories are spared

It soon became apparent that damage to the MTL did not produce a global
amnesia because some memories were affected by the damage, but others
were not. In particular, tasks that required certain motor skills were unaffected
by MTL lesions. Milner (1962) made the first observation of one such spared
memory. She noted that H.M. showed a steady improvement on a mirror-
drawing task which required drawing within the outline of a double star while
looking at a reflection of the star and his hand in a mirror (see Figure 3.1A).

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 31

Not only did H.M. show improvement within a session, but he also showed
retention across sessions, beginning each day’s session at roughly the level he
had finished on the previous day. In spite of near-perfect retention that
spanned 24 hours, he had no recollection of having performed this task on the
preceding day.
The finding of spared memory with respect to the mirror-drawing task
was the first of a series of such descriptions that ultimately formed the
foundation for the idea of dissociable memory systems. Other motor skill tasks
were soon described that also appeared unaffected by MTL lesions. For
example, H.M. showed both improvement within a session and retention
across sessions in the acquisition of a rotary pursuit task (see Figure 3.1B) in
which he had to maintain a metal stylus pen in contact with a rotating metal
disc (Corkin 1968). One advantage of this study over the mirror-drawing
study was that H.M.’s performance was compared to that of a control group of
normal subjects. Although his time-on-target score did improve steadily, his
overall performance was inferior to that of the normal control group. Similar
findings were reported for acquisition and retention of a bimanual tracking
task and a bimanual tapping task, although his performance in the tapping task
more closely approximated that of the normal control group (Corkin 1968).
Based on her early findings, Milner (1965) suggested that the types of
memories spared by MTL damage were those that involved learning a motor
skill. Subsequent studies, however, showed that MTL damage also spared
performance on tasks in which a motor component was not the defining
feature. Warrington and Weiskrantz (1968), for example, showed that patients
with alcoholic Korsakoff’s amnesia, a form of amnesia that produces memory
impairments roughly similar to MTL amnesia, were able to learn the Gollin
incomplete-pictures task. This task consists of a series of five pictures ranging
from very fragmented to complete. Subjects are first shown the most frag-
mented rendition and then progressively less fragmented renditions until they
are able to identify the picture. On the first exposure to the task, correct
identification is likely to occur only when the complete rendition is shown.
With practice, however, the subject is able to identify the picture from increas-
ingly fragmented renditions. In line with the findings from motor skill tasks,
amnesics improved their performance within a session and exhibited near-
perfect retention across sessions (see Figure 3.1C). Also in line with their
performance on other skill-based tasks, their overall error rate was signifi-
cantly higher than that of the control group across the 3 days of testing.

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32 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 3.1. Spared memories in patients with medial temporal lobe damage or alcoholic
Korsakoff’s syndrome. (A) Mirror drawing task. The subject had to draw within the outline
of the figure of a star (redrawn from Milner 1965). (B) Rotary pursuit task. The subject had
to keep a metal pen in contact with a moving metal target (redrawn from Corkin 1968).

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 33

Figure 3.1 (continued) (C) Gollin incomplete-pictures task. The subject saw a series of five
pictures that ranged from degraded to complete. The most degraded picture was presented
first, followed by progressively less degraded pictures, until the subject could identify the
picture (redrawn from Warrington and Weiskrantz 1968). (D) Mirror reading task. The
subject read a list of three mirror-drawn words. Some words appeared more than once
within a session (repeated word triads), whereas others did not (nonrepeated word triads)
(redrawn from Cohen and Squire 1980).

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34 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Another example of a skill that is relatively spared by MTL lesions is

performance on the Tower of Hanoi problem. In this task, the subject must
learn to move a series of disks from a source peg to a goal peg while keeping in
mind that only one peg can be moved at a time and that at no time can a large
peg be placed over a small peg. Again, H.M. improved performance on this
task within a session and exhibited excellent retention from session to session
(Cohen & Corkin 1981). At no time, however, did he ever remember having
performed the task. As described by the authors,
“By the seventh and eighth days of training, despite near-perfect perfor-
mance, his commentary during each trial always sounded as if he were
solving the puzzle for the first time” (Cohen & Corkin 1981, p. 235).

A similar pattern of findings was reported for classical conditioning of an

eyeblink response following MTL lesions (Weiskrantz & Warrington 1979).
Because the number of studies of spared memories following MTL
lesions and the procedures that have been used to reveal them could fill a
chapter by themselves, all will not be reviewed here. Two final studies,
however, deserve special mention. Cohen and Squire (1980) tested amnesic
patients of various etiologies, including alcoholic Korsakoff patients, a patient
(N.A.) who had sustained a stab wound to the diencephalon, and patients
being treated with electroconvulsive therapy, on a mirror reading task. All of
these disorders and injuries produce impairments similar to that seen in MTL
amnesia. Amnesic patients again showed improvement within a session and
retention across sessions (see Figure 3.1D). Most interesting, however, was
the finding that they still showed perfect retention of the task 3 months later.
Despite these results, the amnesic patients performed very poorly on tests of
recognition, had no recollection of having performed the task before, and
could not even remember which words they had just read.
In the second study, Graf et al. (1984) showed that amnesics were
impaired on free-recall and cued-recall tests but performed normally on word-
stem completion tests. The most interesting comparison was between perfor-
mance on the cued-recall test and on the word-stem completion test, which
differed only in the instructions (see Chapter 2). In both cases, subjects were
shown a list of words and then were presented with three letters. Prior to the
cued-recall test, subjects were instructed to complete the three letters with a
word they had seen on the prior study list, whereas prior to the word-stem
completion test, they were simply instructed to complete the three letters with
the first word that came to mind. This subtle difference in the type of instruc-

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 35

tion was critical to the outcome of the experiment. On the word-stem comple-
tion test, amnesics performed like normal controls, whereas on the cued-recall
test, amnesics’ performance was impaired relative to that of normal controls.
In summary, patients with MTL lesions and patients with disorders and
injuries that damage structures related to the MTL suffer from severe memory
impairments. Despite these impairments, they display a variety of forms of
spared memories, ranging from normal motor skills to intact performance on
perceptual and even some cognitive tasks. This simple dissociation led Cohen
and Squire (1980) to distinguish between knowing that, which is impaired
following MTL damage, and knowing how, which is spared following MTL
damage. Over the years, this distinction has taken on many different labels.
These are reviewed in Chapter 8. For our present purposes and for ease of
exposition, we refer to knowing that as explicit memory and knowing how as
implicit memory.

Studies of explicit and implicit memory in nonhuman animals

Memory tasks used with animals

Shortly after Scoville and Milner (1957) reported severe memory impairments
in humans with MTL damage, attempts were made to develop an animal
model of MTL amnesia. The main problem in this endeavor was expressed
cogently by Orbach, Milner and Rasmussen (1960) when they stated:
“the requirements of the tests applied to man are difficult to adapt to behavior
that is within the repertoire of the monkey” (p. 248).

Nevertheless, over the years, numerous tasks have been used to study the
effects of MTL lesions in nonhuman animals. Because later sections of this
chapter rely heavily on an understanding of these tasks, a brief description of
them is in order. What follows is not an exhaustive list of the tasks that have
been used to assess the effects of brain damage in animals but, rather, descrip-
tions of the tasks used most frequently.
Visual Discrimination. In a visual discrimination task, the animal must
learn which of the two stimuli is associated with reward (see Figure 3.2A). In
a typical session consisting of numerous trials, the same pair of stimuli is
presented on each trial, and the same stimulus always serves as the rewarded

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36 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 3.2. The three primary tasks that have been used with nonhuman animals to study
the effects of damage to the medial temporal lobe on memory performance. (A) Visual
discrimination. The same two stimuli are presented on every trial. The animal must respond
to the same stimulus (A) to obtain a reward (+). Responses to the nonrewarded stimulus (B)
result in punishment (–). (B) Visual delayed nonmatching-to-sample (DNMS). Each trial
consists of two parts. The sample stimulus is presented and then is removed from view for
a delay period. At the end of the delay period, two comparison stimuli are presented. The
animal must respond to the novel stimulus to obtain a reward. Responses to the familiar
stimulus are punished. (C) Visual concurrent discrimination (CD). The animal is trained
with eight pairs of stimuli. Within each pair, the same stimulus is always rewarded, whereas
the other stimulus is not. The animal must learn which stimulus of each pair is the rewarded
stimulus. Each of the eight pairs of stimuli is presented a number of times within each
session.

(positive) stimulus. Of all the tasks used in lesion studies, the discrimination
task is the easiest for animals to learn. Although making the physical identity
of the stimuli more similar increases both the difficulty of the task and the
length of time required to solve it, the acquisition of discrimination tasks is
typically measured in terms of days.
Visual Delayed Nonmatching-to-Sample (DNMS). In a visual DNMS
task, the animal must remember which stimulus it saw most recently. The

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 37

DNMS task has become a standard test of recognition memory in animals and
is perhaps the most frequently used task in studies examining the effects of
brain lesions on memory in monkeys. The procedure is quite simple (see
Figure 3.2B). At the start of a trial, a stimulus is presented to an animal and
then is removed from view for the duration of a delay interval. At the end of
the delay, two stimuli are presented to the animal — one that is the same as the
sample and one that is different. The animal must choose the stimulus that is
different from the sample stimulus, that is, the nonmatching stimulus. Each
session consists of numerous trials in this format. Although the task can also
be structured so that the animal is required to choose the matching stimulus,
the nonmatching task is the preferred version in lesion studies, most likely
because it taps the monkey’s predisposition for novelty (Mishkin & Delacour
1975).
Acquisition of the DNMS task takes considerably longer than acquisition
of a visual discrimination task and is typically measured on a scale of weeks
rather than days. The acquisition of the DNMS task, however, is not of
primary interest in brain lesion experiments. The power of the DNMS proce-
dure is that the delay between the sample and comparison stimuli can be
varied, thereby allowing the experimenter to measure the effects of brain
lesions on short-term retention. This is the context in which the DNMS
procedure is used most often. With training, monkeys can eventually perform
at above-chance levels with delays as long as 40 min between the sample and
the comparison stimuli.
Visual Concurrent Discrimination (CD). The CD task is a complex
version of the visual discrimination task described earlier. Recall that in a
visual discrimination task, the animal obtains a reward by responding to the
positive stimulus of one pair of stimuli that are presented repeatedly within a
session. In the visual CD task, eight pairs of stimuli are presented repeatedly
within a session, and the animal must learn which stimulus in each pair is
associated with reward (see Figure 3.2C). Naturally, given so many pairs of
stimuli, acquisition of a CD task takes longer than acquisition of a visual
discrimination task and also longer than the acquisition of a DNMS task.
Radial Arm Maze. The radial arm maze task is one of the most frequently
used procedures to study the neural basis of learning and memory in rats.
Developed by Olton and Samuelson (1976), the task taps the amazing spatial
abilities of rats. The maze consists of a central arena from which radiate eight
arms (see Figure 3.3A). The rat is placed inside the arena and allowed to

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38 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

collect a piece of food placed at the end of each arm. The optimal strategy is to
enter an arm once and then not revisit that arm. Revisiting an arm that has
already been entered is scored as an error. Each session consists of a single
trial in which the rat attempts to retrieve all eight pieces of food in the maze.
Rats quickly learn to retrieve all the food after entering only eight (no errors)
or nine (1 error) arms. They can achieve such levels of performance within 1
to 2 weeks.
Morris Water Maze. Like the radial arm maze, the Morris water maze
(Morris 1981, 1984) also taps the spatial abilities of rats. Rats are placed in a
circular pool filled with water rendered opaque by the addition of milk (see
Figure 3.3B). Just below the water level in a constant position in the tank is a
hidden platform. The rats are placed in the water in various quadrants of the
tank and, in a short period, learn to locate and escape to the platform. A session
consists of approximately 10 trials. Although rats will reach asymptotic levels
of performance within a few days of testing, considerable learning occurs over
the first 10 trials of the first session.

The effects of MTL lesions

Anterograde Amnesia. One of the earliest attempts to model human MTL

amnesia was reported by Orbach, Milner and Rasmussen (1960), who tested
monkeys with combined amygdala and hippocampal lesions — damage that
was intended to approximate the lesion sustained by H.M. The monkeys were
trained on a battery of visual and somesthetic discrimination problems. In tests
designed to assess the effects of the lesions on postoperative retention, mon-
keys were trained on a task prior to lesioning and were tested for retention
after the operation. In tests designed to assess the effects of the lesions on
initial learning, monkeys were trained on a task after the operation.
Although monkeys with combined damage to the amygdala and hippo-
campus were impaired on both tests of postoperative retention and tests of
initial learning of visual and somesthetic discriminations, three lines of evi-
dence suggest that their impairments were not as profound as those suffered
by humans with MTL lesions. First, all of the lesioned monkeys were eventu-
ally able to learn the visual or somesthetic discriminations. Second, although
the monkeys showed postoperative retention impairments of preoperatively
learned discriminations, they generally showed no postoperative retention
impairment of postoperatively learned discriminations. Finally, in one test of

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 39

Figure 3.3. The two primary tasks that have been used with rats to study the effects of
damage to the hippocampus on memory performance. (A) Radial arm maze. The apparatus
consists of a central arena from which radiate eight arms. The rat is placed within the central
arena and allowed to forage for food that is placed in a recessed well (small circles) at the
end of each arm. The optimal strategy is to enter an arm once and then not return to that arm.
(B) Morris water maze. The apparatus is a tank that contains water that has been rendered
opaque by the addition of milk. Rats are placed in the tank at different positions against the
wall and learn to escape to a hidden platform (small circle) that is submerged just below the
water level.

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40 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

initial postoperative learning with wide spacing between successive discrimi-

nation trials, operated monkeys acquired the task as fast as control animals.
According to Murray (1996),
“in the mid 1960s, replication of the lesions performed in H.M. did not yield
convincing evidence for memory deficits in monkeys, and a role for the
amygdala and hippocampus in stimulus memory looked doubtful” (p. 13).

In contrast to the relatively mild impairments reported by Orbach et al. (1960),

Correll and Scoville (1965) reported that damage to the amygdala and the
hippocampus (and probably to the tissue adjacent to these regions) in monkeys
resulted in a serious postoperative retention impairment on a visual delayed
matching-to-sample (DMS) task (see also Chapter 6). Prior to the operation,
monkeys were initially trained on a simultaneous matching-to-sample task
(i.e., the sample and comparison stimuli were presented concurrently), and
then they were trained on a DMS task with delays as long as 5 s. Following
surgery, all monkeys were impaired in relearning the simultaneous matching-
to-sample task, and only one of four monkeys was able to perform the DMS
task with a 0-s delay.
Despite the serious nature of these impairments, Correll and Scoville
(1965) concluded that the deficits after MTL lesions in monkeys were “related
to structural characteristics of the problem rather than to the rapid decay of a
memory trace” (p. 366). Perhaps for this reason, Correll and Scoville are not
generally credited with developing the first animal model of human MTL
amnesia. This honor belongs to Mishkin (1978), who reported that combined
— but not separate — damage to the amygdala and hippocampus and the
tissue adjacent to these regions in monkeys produced serious impairment on a
DNMS task.
Prior to the operation, the monkeys were trained on the DNMS task with
a 10-s delay. After recovering from the lesion, they were tested for savings.
Monkeys with damage to either the amygdala or the hippocampus were mildly
impaired and required approximately the same number of trials to relearn the
task postoperatively as they had required to learn the task originally. In
contrast, monkeys with combined damage to the amygdala and the hippocam-
pus required, on average, more than seven times as many trials to relearn the
task postoperatively. Nevertheless, two of the three monkeys with combined
lesions were able to relearn the DNMS task to criterion. The initial impairment
and subsequent recovery is generally ignored in favor of the finding that the

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 41

performance of monkeys with combined damage to the amygdala and hippo-

campus was close to chance levels when tested after delays ranging from 30 to
120 s (see Figure 3.4A). In contrast, monkeys with damage to either the
amygdala or hippocampus were only very mildly affected when tested after
these same delays.
In addition to impairments on DNMS tasks, monkeys with damage to the
MTL take much longer to learn an eight-pair CD task than unoperated control
animals (Zola-Morgan & Squire 1985). Although impaired on the task, how-
ever, the lesioned monkeys eventually do learn to solve this task to criterion. In
rats, damage to the hippocampus impairs the learning of both the radial arm
maze (Olton, Becker & Handelmann 1979) and the Morris water maze (Morris,
Garrud, Rawlins & O’Keefe 1982). As is the case with monkeys, rats with
damage to the hippocampus are able to relearn both tasks to criterion. The
DNMS and CD tasks for monkeys and the radial-arm maze and Morris water-
maze tasks for rats are generally regarded as equivalent to explicit memory tasks
in humans.
Retrograde Amnesia. In addition to modeling aspects of anterograde
memory loss, studies with animals have also modeled the retrograde amnesia
that often follows MTL damage in humans. Recall that retrograde amnesia
refers to a loss of memories for events that occurred prior to the damage.
These memory impairments in humans are often temporally graded such that
memory for recent events is usually much worse than memory for more
remote events. Zola-Morgan and Squire (1990a) found that damage to the
hippocampus and amygdala and the adjoining tissue in monkeys also causes
temporally-graded retrograde amnesia. The monkeys were trained 16, 12, 8, 4,
or 2 weeks prior to surgery with five different sets of 20 object discrimina-
tions. An object discrimination task is similar to the visual discrimination task
(see Figure 3.2A) except that the stimuli are objects instead of pictures. Half
of the animals then received damage to the MTL, and half served as unoper-
ated controls. Memory for the 100 discriminations was assessed following
either recovery from surgery (operated animals) or a delay of similar length
(unoperated control animals).
The results are also shown in Figure 3.4B. Control animals produced a
standard forgetting function, remembering discriminations that they learned
more recently (2 weeks prior to the surgery of lesioned animals) better than
discriminations that they learned in the more remote past (16 weeks before-

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42 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 3.4. The effects of damage to components of the medial temporal lobe on antero-
grade and retrograde memory in monkeys. (A) Anterograde memory impairments. The
effects of damage to the amygdala (A), hippocampus (H), or combined amygdala-hippo-
campus (A-H) damage on delayed nonmatching-to-sample performance in monkeys. The
dotted line represents chance levels of performance (redrawn from Mishkin, 1978). (B)
Retrograde memory impairments. The effects of combined amygdala-hippocampus damage
on retention of visual discriminations that were learned prior to surgery (redrawn from
Zola-Morgan and Squire, 1990).

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 43

hand). Like humans, however, monkeys with MTL damage showed the oppo-
site effect, with greater forgetting of discriminations that had been learned in
the recent past. Similar temporally-graded retrograde amnesia curves have
been obtained in studies with rats (Bolhuis, Stewart & Forrest 1994; Cho,
Kesner & Brodale 1995; Kim & Fanselow 1992; Ramos 1998; Winocur
1990). In summary, both anterograde and retrograde memory impairments
that have been noted in humans with MTL damage have been replicated in
monkeys and rats with similar lesions.

Some memories are spared

Recall that humans with MTL damage, although densely amnesic, are never-
theless able to learn certain motor, perceptual, and even problem-solving
tasks. The same appears to be true for monkeys with MTL lesions. Malamut,
Saunders and Mishkin (1984) showed that monkeys with combined damage to
the hippocampus and amygdala were not impaired in the acquisition of a 24-
hour CD task but were impaired on a DNMS task. The claim of spared
performance on the 24-hour CD task was repeated frequently in numerous
books and articles that followed the publication of this paper.
Recall that monkeys with MTL damage are impaired in the acquisition of
an eight-pair CD task. The 24-hour CD task is procedurally almost identical to
the eight-pair CD task with two main exceptions: First, in the 24-hour CD
task, monkeys are trained with 20 pairs of stimuli instead of just eight. Second,
in the 24-hour CD task, each pair of stimuli is presented only once in a session,
whereas in the eight-pair CD task, the pairs of stimuli are presented numerous
times within a session.
In the Malamut et al. (1984) study, seven monkeys with combined
damage to the hippocampus, amygdala, and adjacent tissue and four unoper-
ated controls were trained with 20 pairs of stimuli until they satisfied a
criterion of 90 correct responses in 100 trials in five consecutive sessions.
After they completed training with the first set of 20 pairs of stimuli (set A),
they were trained in a similar fashion with a second set of 20 pairs of stimuli
(set B). The lesioned monkeys were mildly impaired on the acquisition of the
24-hour CD task on set A but not on set B. Moreover, according Malamut et
al., the monkeys who showed an impairment on either set A or set B had
incidental damage to the visual association areas of the brain (area TE), which

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44 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

led the authors to discount damage to the amygdala and hippocampus as the
source of the impairment.
Several aspects of this paper argue against the conclusion that MTL
damage did not affect performance on the 24-hour CD task. Figure 3.5 pre-
sents data for the unoperated control monkeys on the left, for the operated
monkeys that sustained no damage to area TE in the middle, and for the
operated monkeys that sustained additional damage to area TE on the right. In
Figure 3.5, data for monkeys that sustained damage to area TE are arranged
from left to right in order of the increasing amount of damage to this area.
Consider the acquisition of set A (see Figure 3.5A). Although monkey L2–3,
who had the greatest damage to the visual areas, took the longest to learn the
task, a closer inspection of this figure reveals that monkeys L2–2 and L3–2,
who sustained no damage to the visual areas, also performed quite poorly.
Furthermore, monkey L3–1, who learned faster than any other animal (includ-
ing the unoperated animals), had considerable sparing of the amygdala and,
most likely, of the tissue adjacent to the amygdala. In fact, researchers now
recognize that the tissue adjacent to the amygdala — the perirhinal cortex — is
critical for the successful performance of a number of visual memory tasks.
Therefore, monkey L3–1, for whom this critical region was probably spared,
should not be included with the animals that sustained combined damage to
the amygdala and hippocampus.
Despite these problems, it is fair to say that the impairment in animals
with amygdala-hippocampal damage that did not sustain damage to area TE
was relatively mild, and they were eventually able to relearn the task to
criterion. Furthermore, as the data for set B clearly show (see Figure 3.5B),
there was very little difference between operated and control animals in terms
of the number of sessions to learn the task. Therefore, this study has been used
as evidence of spared memory following damage to the MTL in monkeys,
especially because the same operated monkeys were seriously impaired on a
DNMS task.
A second point, however, is also worth noting, namely, that the 24-hour
CD task is easier for monkeys to learn than the eight-pair CD task. On
average, monkeys require almost three times as many trials to learn an eight-
pair CD task (i.e., 550 trials) than to learn a 24-hour CD task (i.e., 195 trials).
The difficulty is even more apparent when one considers how many pairs the
animal is required to learn in each task; monkeys require seven times as many
trials to learn each pair in the eight-pair CD task (i.e., 69 trials) compared to

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 45

Figure 3.5. The effects of combined damage to the amygdala and hippocampus (A-H) on
the 24-hour concurrent discrimination (CD) task. Animals with damage to the visual cortex
are arranged from left to right in terms of increasing damage to the visual cortex (redrawn
from Malamut, Saunders and Mishkin 1984). (A) Set A: Performance with the first set of 20
pairs of stimuli. (B) Set B: Performance with the second set of 20 pairs of stimuli.

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46 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

the 24-hour CD task (i.e., 9.8 trials). For whatever reason, because the eight-
pair CD task is more difficult for monkeys to learn than the 24-hour CD task,
damage to the MTL might reasonably be expected to impair their performance
on the eight-pair CD task before impairing it on the 24-hour CD task.
The effects of MTL lesions on monkeys’ performance on motor tasks are
more similar to the spared performance that has been seen following MTL
lesions in humans, and they are certainly more convincing than the effects of
MTL lesions on monkeys’ acquisition of the 24-hour CD task. Zola-Morgan
and Squire (1984) trained monkeys with medial temporal lobe lesions on both
a Barrier motor-skill task and a Lifesaver task. In the Barrier task, the mon-
keys had to move a breadstick through three rows of a vertically arranged
wooden barrier. In the Lifesaver task, monkeys had to remove a Lifesaver
candy from a horizontal metal rod that contained a 90-deg bend. Monkeys
with MTL lesions showed normal acquisition of both tasks (see Figure 3.6).
Furthermore, in the case of the Lifesaver task, both control and lesioned
animals showed similar levels of retention of the task following a 1-month
pause in testing.
Thus, monkeys, like humans, do show some spared memories following
damage to the MTL.

Parallel findings in humans and nonhumans

Humans have been tested on most of the tasks that are sensitive to MTL
lesions in monkeys, and the results are generally consistent with the monkey
data. Amnesic patients, for example, are impaired in performing the DNMS
task and show the same accelerated delay-dependent decay rates as monkeys
with similar damage (Sidman, Stoddard & Mohr 1968; Squire, Zola-Morgan
& Chen 1988). Human amnesics are also impaired in the acquisition of an
eight-pair CD task (Oscar-Berman & Bonner 1985; Oscar-Berman & Zola-
Morgan 1980; Squire et al. 1988). The only inconsistency between the human
and nonhuman data is in the acquisition of a 24-hour CD task: Monkeys are
generally not impaired on this task, whereas humans are.
Problems with Tasks Used with Nonhumans. The primary problem with
the tasks that are used with animals is that they tend to be defined as either
explicit or implicit according to whether they are impaired by MTL lesions or
not. The DNMS task, for example, is defined as an explicit memory task
because it is sensitive to MTL damage, whereas the 24-hour CD task is defined

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 47

Figure 3.6. The effects of combined damage to the amygdala and hippocampus (A-H) on
two motor skill tasks (redrawn from Zola-Morgan and Squire, 1984). (A) Barrier task. The
monkeys were required to maneuver a breadstick through three rows of vertically arranged
wooden pegs. (B) Lifesaver task. The monkeys were required to maneuver a Lifesaver
candy off a metal rod that contained a 90-deg bend.

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48 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

as an implicit memory task because it is either not impaired by these lesions or

is less impaired by them. Numerous memory theorists have argued that such
circularity does not apply to the tasks used with humans and that the memory
distinctions between performance on different tasks in humans are process-
driven (see Chapter 8). Although the extent to which this argument is true for
tasks used with humans is debatable, it almost certainly is the case that process-
driven accounts do not describe findings from memory research with monkeys.
For example, it is difficult to reconcile the fact that procedurally identical or
nearly identical tasks are often differentially sensitive to MTL lesions.
One example of this problem is animals’ performance on an eight-pair
CD task and their performance on a 24-hour CD task. Procedurally, the tasks
are almost identical, and in both cases, the animal must learn which stimulus
of a pair is consistently associated with reward. Yet, the effects of MTL
lesions are quite different on the two tasks. A second example is animals’
performance on a discrimination task. Zola-Morgan and Squire (1984) found
that monkeys with MTL lesions are only mildly impaired when learning a
difficult discrimination between 2-D stimuli. On the other hand, they found
greater impairments on a procedurally identical discrimination task that used
3-D stimuli. The point here is that the task per se (CD or discrimination)
cannot be classified as an implicit or explicit memory task on the basis of the
procedure because the procedures are virtually identical. Rather, they are
defined as an implicit or explicit memory task on the basis of whether or not
task performance is impaired by MTL lesions, respectively.

Neural substrates of explicit and implicit memory

Neural substrates of explicit memory

Mishkin’s Model. Although the MTL may be critical for normal memory, it is
clear that memories are not stored in this area of the brain. This conclusion
follows from the fact that H.M. and other patients with similar damage to the
MTL, while suffering from severe anterograde amnesia and perhaps some
retrograde amnesia, have some preserved memories for events that occurred
prior to the operation or damage. What exactly, then, does the MTL contribute
to the memory process? And how does it accomplish this feat? Mishkin (1982)
proposed that recognition memory (i.e., explicit memory) is mediated by a

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 49

cortico-limbic-diencephalic-cortico circuit (see Figure 3.7A). According to

this model, memories are stored in higher-order sensory areas of the brain, but
importantly, the storage of that information in cortex requires that the to-be-
stored information course through limbic (hippocampus and amygdala) and
diencephalic structures.
Consider the case of visual memories: Although visual information pro-
cessing is far more parallel than Mishkin’s model depicts, the basic premise of
the model is still correct. Visual information from the eyes is projected to the
primary visual cortex (area OC) in the posterior part of the brain. The
information is then sent through a series of additional visual processing areas

Figure 3.7. Neural substrates of explicit memory. (A) Mishkin (1982) model. In this model,
both the amygdala and the hippocampus contribute equally to visual recognition memory
(redrawn from Mishkin, 1982). (B) Petri and Mishkin (1994) model. In this revised model,
the rhinal cortex is critical for visual recognition memory (redrawn from Petri and Mishkin,
1994).

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50 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

in what today is referred to as the ventral visual stream. Each of these cortical
areas (OB, OA, and TEO) is important for extracting and processing some
aspect of a visual scene, such as color or form. The neurally most veridical
version of visual information is represented and stored in the terminal regions
of the ventral visual stream in the inferior temporal cortex, or area TE. Before
that information can be stored in area TE, however, it must engage the limbic
and diencephalic areas of the brain. By doing so, the information can then be
stamped in to area TE.
According to the model, the memory is initially stored in area TE in a
limbic-dependent fashion, that is, retrieval of the information requires the
participation of the limbic system. Over time, however, the memory in area
TE becomes so well established that it can be retrieved without the assistance
of the limbic regions. At this stage, damage to the limbic system would not
impair information that is already stored in area TE but would impair the
future storage of information in area TE. This is believed to be what occurs in
the case of MTL amnesia: Individuals with MTL damage are no longer able to
form new memories because the limbic regions responsible for stamping in
the memory are damaged. On the other hand, information that has already
been stamped in, and is therefore limbic-independent, is spared following
MTL damage.
Although this model was originally developed for visual memories, one of
its strong features is its applicability to memories in any of the sensory systems
by simply substituting the appropriate higher-order sensory area. For example,
the same model would apply for the auditory system, with the exception that
the auditory cortical areas TC→TB→TA would be substituted for the visual
cortical areas OC→OB→OA→TEO→TE. Such substitution is justified on the
grounds that the visual and auditory systems of the brain are anatomically
similar in both their intrinsic and extrinsic projection patterns (Jones & Powell
1970; Pandya & Kuypers 1969). Furthermore, the behavioral consequences of
damage to the auditory association cortex are virtually identical to the behav-
ioral consequences of damage to the visual association cortex (Colombo,
D’Amato, Rodman & Gross 1990; Colombo, Rodman & Gross 1996).
Modifications of the Model. Mishkin’s basic scheme has remained essen-
tially unchallenged since its inception, but its exact components and their
contributions to memory have changed considerably (see Figure 3.7B). In his
original formulation, both the hippocampus and the amygdala contributed
equally to recognition memory performance, and both had to be damaged to

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 51

cause an impairment in recognition memory. Mishkin (1982) acknowledged

the “unusual practice that has been followed here of treating the amygdala and
the hippocampus as a single functional unit” (p. 94). Nevertheless, this sugges-
tion was reasonable given that damage to the amygdala or the hippocampus
separately produced no appreciable DNMS impairments (see Figure 3.4A).
More than 10 years of research were required to understand why com-
bined lesions of the amygdala and hippocampus are necessary to produce an
impairment in memory. A schematic of the critical limbic structures and how
they are arranged in the medial temporal lobe of the monkey’s brain is shown
in Figure 3.8. The amygdala and the hippocampus lie along the medial aspect
of the temporal lobe, and the amygdala lies anterior to the hippocampus. The
anterior portions of the perirhinal cortex and entorhinal cortex lie adjacent to
the amygdala, and the posterior portions of these areas lie adjacent to the
hippocampus. The parahippocampal gyrus is situated posterior to the perirhi-
nal and entorhinal cortices and adjacent to the hippocampus.
In most lesion studies, damage to the hippocampus and amygdala is
accomplished by subpial aspiration of the tissue. In addition, because the
hippocampus and amygdala are located medially, but the surgical approach is
often from the temporal aspect, damage to these structures invariably results in
damage to the perirhinal cortex, entorhinal cortex, and parahippocampal gyrus.
Therefore, in removing the amygdala and the hippocampus, Mishkin (1978)
also damaged the tissue adjacent to these regions. As a result, it was unclear
whether the DNMS impairments resulted from damage to the amygdala and

Figure 3.8. The spatial arrangement of the critical structures of the limbic system (adapted
from Murray, 1996).

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52 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

hippocampus or from damage to the perirhinal cortex, entorhinal cortex, or

parahippocampal gyrus.
Studies by Larry Squire and Stuart Zola-Morgan throughout the 1980s
and early 1990s helped clarify the contributions to memory made by the
amygdala, hippocampus, perirhinal cortex, entorhinal cortex, and parahippo-
campal gyrus. In one of the earlier studies, Zola-Morgan, Squire and Amaral
(1989a) noted that radiofrequency lesions of the amygdala, which did not
damage the adjacent rhinal tissue, failed to worsen DNMS impairments that
were seen after hippocampal damage. Thus, in contrast to the findings of
Mishkin (1978, 1982), the amygdala appeared to play no role in DNMS
behavior.
A second finding (see Figure 3.9) was that damage restricted to the
perirhinal cortex and the parahippocampal gyrus and sparing the amygdala
and hippocampus (the ++ lesion) produced an impairment in DNMS behavior
that was as severe as the impairment produced by damage that included the
hippocampus (the H++ lesion) (Zola-Morgan, Squire, Amaral & Suzuki
1989b). This result not only served to emphasize that the amygdala was not a
component of the recognition (explicit) memory circuit but also challenged the
role of the hippocampus in this circuit. Nevertheless, these and numerous
other studies that followed indicated that DNMS impairments were largely
attributable to damage of the perirhinal cortex rather than to damage of the
hippocampus.
The Role of the Hippocampus. But does damage to the hippocampus per
se impair recognition memory? This question was difficult to answer because,
unlike the amygdala, which is relatively small, the hippocampus is quite large
and difficult to damage without incurring damage to adjacent tissue. Never-
theless, using a newly developed technique that combines stereotaxic surgery
with magnetic resonance imaging (Alvarez-Royo, Clower, Zola-Morgan &
Squire 1991), Alvarez, Zola-Morgan and Squire (1995) managed to selec-
tively damage the hippocampus using radiofrequency lesions. Their results,
also presented in Figure 3.9, revealed that restricted damage to hippocampus
(the H lesion) produced only minor impairments in DNMS performance after
the longest (10-min) delay (see also Zola-Morgan, Squire, Rempel, Clower &
Amaral 1992).
The finding of an impairment after a long delay in the DNMS task was
not replicated by Murray and Mishkin (1998), who used delays as long as 40
min. Furthermore, the monkeys in the Alvarez et al. (1995) study were not at

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 53

Figure 3.9. The effects of damage to the hippocampus (H), hippocampus plus perirhinal
and parahippocampal cortex (H++), or only the perirhinal cortex and parahippocampal
gyrus (++) on visual memory in monkeys (control animals: redrawn from Zola-Morgan,
Squire, Rempel, Clower and Amaral, 1992; H animals: redrawn from Alvarez, Zola-
Morgan and Squire, 1995; H++ animals: redrawn from Zola-Morgan, Squire, Clower and
Rempel, 1993; ++ animals: redrawn from Suzuki, Zola-Morgan, Squire and Amaral, 1993).

all impaired in learning the eight-pair CD task. Recall that monkeys with
hippocampal lesions that extended to the adjacent tissue were impaired in
learning the eight-pair CD task. These findings suggest, therefore, that the
visual memory deficit that follows damage to the hippocampus is transient at
best. The same appears to be true in the case of rats (Mumby & Pinel 1994;
Mumby, Wood & Pinel 1992).
Although these findings suggest that the hippocampus may not be a
component of the explicit memory circuit, it is important to note that failures

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54 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

to observe memory impairments after hippocampal lesions are generally

restricted to tasks that tap purely visual memory. In contrast, many experi-
ments have shown that damage to the hippocampus in both mammalian and
nonmammalian species reliably impairs performance on a number of tasks
that require spatial memory (Angeli, Murray & Mishkin 1993; Colombo,
Cawley & Broadbent 1997; Feigenbaum, Polkey & Morris 1996; Morris et al.
1982; O’Keefe & Nadel 1978; Olton et al. 1979; Parkinson, Murray &
Mishkin 1988; Smith & Milner 1981). Thus, the hippocampus may indeed
play a role in explicit memory, but one that is limited to the processing and
retention of spatial information.
Other Views of Hippocampal Function. That the hippocampus is impor-
tant for processing spatial information is not the only view of hippocampal
function. A second possibility, related to the view that the hippocampus is
important for processing spatial information, is that the hippocampus is impor-
tant in processing contextual information (Hirsh 1974) or in the formation of
context-dependent memories (Vargha-Khadem, Gadian, Watkins, Connelly,
Paesschen & Mishkin 1997). According to this view, both the hippocampus and
the perirhinal cortex are important for explicit memory, but the hippocampus is
important for context-dependent explicit memory, whereas the perirhinal cor-
tex is important for context-independent explicit memory. A third view is that
the hippocampus is important for the flexible or relational processing of
information across both spatial and nonspatial domains (Eichenbaum, Otto &
Cohen 1994). In short, the exact role of the hippocampus in explicit memory is
still being debated.

Neural substrates of implicit memory

Although the neural substrates of explicit memory are generally well defined,
the neural substrates of implicit memory are not. In much the same way that
the behavioral mechanisms of nondeclarative (implicit) memory are defined
“not by any positive feature so much as by the fact that they are not declarative
[explicit]” (Squire 1994, p. 233), the neural substrates of implicit memory
seem to be defined as those areas of the brain that are not the neural substrates
of explicit memory. According to Squire (1994),
“the memory abilities that are not declarative are not of a single type and are
not subserved by a single brain system [but] embrace several kinds of
memory and depend on multiple brain systems” (p. 233).

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 55

Mishkin and colleagues proposed that a cortico-striatal-cortico circuit medi-

ates habit (implicit) memory (Mishkin & Petri 1984; Mishkin et al. 1984).
These pathways were elaborated by Petri and Mishkin (1994) and are illus-
trated in Figure 3.10. Here, habit memories, like recognition memories, are
stored in the highest-order cortical association areas of the brain. Forming a
permanent trace of the habit memory in the association cortex, however,
requires that to-be-remembered information be processed through the striatal
system.
Why the striatal system was considered to be responsible for habit
memory no doubt relates to the fact that many of the memories that were
spared following MTL damage in humans were based on motor skills. The
striatum consists of the caudate nucleus, which receives widespread connec-
tions from higher-order cortical association areas, and the putamen. The
caudate nucleus and the putamen project to the globus pallidus and, via the
thalamus, to the motor cortex of the brain to effect movement. According to
Mishkin et al. (1984),
“this system of projections therefore provides a mechanism through which
cortically processed sensory input could become associated with motor out-
puts generated in the pallidum [globus pallidus] and so yield the stimulus-
response bonds that constitute habits” (p. 74).

Figure 3.10. Neural substrates of implicit memory (redrawn from Petri and Mishkin 1994).

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56 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

As we have previously noted, in addition to preserved motor skills such as

mirror drawing, rotary pursuit, and bimanual tracking, patients with MTL
amnesia also show preserved perceptual skills such as on the Gollin picture
task (Warrington & Weiskrantz 1968), and preserved cognitive skills such as
on the Tower of Hanoi task (Corkin & Cohen 1981). In addition, amnesics
show normal priming such as on word-stem completion tasks (Graf et al.
1984), normal emotional memory (Bechara, Tranel, Damasio, Adolphs,
Rockland & Damasio 1995), and normal classical conditioning (Weiskrantz &
Warrington 1979).
A different neural system is held responsible for each of these forms of
implicit memory (see Figure 3.11). The neural mechanisms underlying classi-
cal conditioning depend in large part on the cerebellum and its associated
brainstem structures (Thompson 1990b), whereas the neural mechanisms
underlying emotional memory depend on the amygdala (Adolphs, Tranel,
Damasio & Damasio 1994; Scott, Young, Calder, Hellawell, Aggleton &
Johnson 1997). The neural substrates of priming as well as of other perceptual
and cognitive memories that are spared following MTL lesions, however, are
still largely unclear. For the most part, they are said to be dependent on the
neocortex — a term only slightly more informative than saying that they
depend on the brain.
The general vagueness concerning the structures important for implicit
memory performance has left the entire notion of implicit memory open to
criticism. Wise (1996), for example, wrote,
“One might suppose that such enthusiasm [for the habit memory system]
stems from a wealth of empirical data and that the habit hypothesis had, being
well and rigorously tested, withstood an onslaught of skeptical experimenta-
tion and testing. Examination of the published literature, however, reveals a
less convincing body of data” (p. 39).

Most of the evidence implicating the striatal system in implicit memory comes
from patients with Huntington’s disease — a genetically transmitted disorder
that results in atrophy of the striatal system, in particular, of the caudate
nucleus. Patients with Huntington’s disease are impaired on tests of implicit
memory, such as rotary pursuit (Heindel, Butters & Salmon 1988), mirror
reading (Martone, Butters, Payne, Becker & Sax 1984), and the Tower of
Hanoi (Saint-Cyr, Taylor & Lang 1988), but they perform normally on tests of
explicit memory. Evidence of the latter, however, is not at all convincing, and
on some tests, they perform as poorly as patients with MTL-type amnesia

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 57

Figure 3.11. Diagram of the divisions of memory, the behaviors that underlie each division,
and the candidate brain structures that support each behavior (redrawn from Milner, Squire
and Kandel 1998).

(Butters, Wolf, Martone, Granholm & Cermak 1985). Furthermore, they can
perform the implicit memory tasks, but they simply do so at a degraded level
— a point that was also stressed by Wise (1996):
“In the major clinical papers one can find evidence of procedural [implicit]
learning that has often been neglected in favor of emphasizing statistically
significant deficits” (p. 41).

Current issues in explicit and implicit memory research

Functional imaging studies of memory

Most of what we know about the neural basis of memory is based on lesion
studies. The problem, of course, is that lesions rarely abide by functional
boundaries. Even when they do, the consequences of a lesion can extend well

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58 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

beyond the intentionally damaged tissue. The task of ascribing function to a

particular structure, therefore, will always be constrained by some degree of
uncertainty regarding the extent of cortical damage. The solution to this
problem has come in the form of imaging studies, which provide a window
into the neural structures responsible for the processing and retention of
information in the undamaged brain. According to Gabrieli, Brewer and
Poldrack (1998):
“progress in functional neuroimaging has broken the shackles of cognitive
neuroscience memory research with humans” (p. 277).

The two most popular imaging techniques are positron emission tomography
(PET) and functional magnetic resonance imaging (fMRI). Neither technique
directly measures neural activity. Rather, both rely on the fact that those areas
of the brain that are neurally active are also those areas of the brain that are
metabolically active. PET and fMRI are designed to detect changes in brain
metabolism that follow naturally as a function of neural activity. Because the
brain is always active, however, both techniques rely on the method of
subtraction, in which activity during a baseline condition is subtracted from
activity during an experimental condition.
Positron Emission Tomography (PET). PET produces a picture of the
brain by measuring blood flow, oxygen consumption, or glucose metabolism.
In all three cases, the subject is injected with a small amount of a lightly
radioactive substance that decays and emits positively charged particles called
positrons. When these positrons collide with electrons, which are negatively
charged, they annihilate each other and produce energy in the form of two
photons. The PET scanner records the level and origin of the photon activity.
This information is then converted into a color-coded picture with a spatial
resolution of approximately 5 mm and a temporal resolution of 1 min.
Functional Magnetic Resonance Imaging (fMRI). Like PET, fMRI mea-
sures brain metabolism in the form of blood oxygenation. In contrast to PET,
which relies on the decay of an ingested radioactive substance, fMRI mea-
sures the magnetic properties of hemoglobin. Areas of the brain that are
neurally very active are also undergoing greater amounts of blood oxygen-
ation. Because oxygenated blood has more magnetic properties than deoxy-
genated blood, the fMRI scanner can detect this difference and convert this
information into a color-coded picture of neural activity with a spatial resolu-
tion of 1 to 2 mm and a temporal resolution of 2 to 8 s (Ungerleider 1995).

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 59

Imaging Studies of Memory. Studies using PET and fMRI are being used
with increasing frequency to chart the neural structures that are activated during
memory performance (for reviews, see Gabrieli, Brewer & Poldrack 1998;
Schacter 1997; Ungerleider 1995). Although a number of studies have imaged
the brain during memory performance, only recently have studies begun to
address the dissociation between explicit and implicit memory. One of the first
studies of this type was conducted by Squire, Ojeman, Miezin, Petersen, Videen
and Raichle (1992), who asked subjects to study a list of words. To ensure that
they attended to each word, the experimenter asked them to rate how much they
liked each word on a scale of 1 to 5. Their brains were then scanned using PET
while they performed either a word-stem completion (implicit memory) task or
a cued-recall (explicit memory) task. The explicit memory task activated the
hippocampus and parahippocampal gyrus, whereas the implicit memory task
led to a decrease in activity in the right posterior visual cortex. Unfortunately,
the implicit memory task also activated the hippocampus and parahippocampal
gyrus, although to a lesser extent.
The Squire et al. (1992) study fell short of providing the required double
dissociation between memory task (explicit versus implicit) and neural struc-
ture (hippocampus versus posterior visual cortex) that would support the
notion of multiple memory systems. The authors noted, however, that success
on the word-stem completion task was uncharacteristically high (71.5%) and,
more importantly, not that different from success on the cued-recall task
(72.4%). It is possible, they argued, that performance on the word-stem
completion task may have been contaminated by explicit memory influences
(see also Chapter 2), and that the hippocampal activation that was seen during
word-stem completion was a consequence of this contamination.
To address this possibility, Schacter, Alpert, Savage, Rauch and Albert
(1996) repeated the word-stem completion task. Subjects were shown a list of
words, but instead of rating them on a pleasantness scale, they counted the
number of T-junctions in each word. This manipulation deemphasized the
semantic nature of the task and encouraged them to process the words in a
more incidental fashion. The experiment yielded the desired results: Subjects
still showed priming effects, but they completed many fewer word stems than
subjects in the Squire et al. (1992) study. Under these conditions, PET scans
again revealed a decrease in activity in the posterior visual cortex. In contrast
to the findings of Squire et al. (1992), however, no activation was seen in the
hippocampus or parahippocampal gyrus.

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60 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

One memory system or two?

There are a number of possibilities concerning the neural architecture of

memory. The prevailing view is that there are at least two memory systems.
According to this view, damage to one system impairs explicit memory but
not implicit memory, whereas damage to the other system has the opposite
effect. A second possibility is that there is only one memory system and that
damage to this system impairs explicit memory tasks because they are more
resource-demanding than implicit memory tasks.
Although the multiple-memory-systems view is by far the most prevalent
today, in reviewing the literature on the effects of brain damage on memory,
one is almost immediately struck by the fact that the vast majority of studies
report impairments in explicit memory but not in implicit memory. In other
words, the vast majority of evidence is based on a single memory dissociation.
The same is true of evidence from studies with normal human adults who
receive implicit or explicit test instructions (for review, see Chapter 7). The
case for multiple memory systems would be stronger if damage to a second
system could be shown to impair implicit memory while sparing explicit
memory. Is there any evidence for such a double dissociation?
Double Dissociations: Nonhuman Animal Studies. Packard, Hirsh and
White (1989) compared the effects of damage to the caudate nucleus and
fornix (which is roughly equivalent to damage of the hippocampus) on the
acquisition of two versions of the radial arm maze — one designed to measure
implicit memory and the other designed to measure explicit memory. The
explicit version was the standard radial arm maze task in which all eight arms
of the maze were baited, and rats were required to enter an arm to obtain a
reward. Because repeat visits to the same arm were considered an error, rats
were trained to adopt a win-shift strategy. In the implicit version, a light at the
entry to each of four baited arms was lit at the start of a session. The remaining
four arms were neither baited nor lit. If a rat entered a lighted arm, then it was
rewarded, and that arm was rebaited. Following a second entry into the same
arm, the rat received another reward, and then the light was turned off. A third
visit to an arm was considered an error. Thus, rats were trained to visit each of
the four arms twice within a session — a win-stay strategy.
In the explicit version of the task, rats with fornix damage committed
more errors than controls, but rats with damage to the caudate nucleus and
unoperated control animals performed equivalently. In the implicit version of

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 61

the task, rats with damage to the caudate nucleus were impaired relative to
unoperated controls, but rats with damage to the fornix performed better than
controls. (Note, however, that rats with caudate lesions were able to learn the
task to above-chance levels.) In a follow-up study, Packard and White (1991)
found that intracaudate injections of the dopamine (DA) agonist d-amphet-
amine improved performance on the win-stay version of the radial arm maze
task, but intrahippocampal injections had no effect. Conversely, intrahippo-
campal injections improved performance on the win-shift version of the radial
arm maze task, but intracaudal injections had little effect. These studies, then,
revealed a double dissociation of function with respect to both the effects of
lesions and dopaminergic activation.
Packard and McGaugh (1992), who trained rats on two versions of the
two-platform Morris water maze task, provided more evidence of a double
dissociation. In this task, one platform is stable and will support the rat,
whereas the second platform is unstable and sinks when the rat stands on it. In
the spatial (explicit) version of the task, the stable platform always resided in
the same quadrant of the water maze, whereas the unstable platform shifted
between the remaining three quadrants across trials. In the visual (implicit)
version of the task, one visual cue indicated the correct platform, and another
indicated the incorrect platform. Again, rats with fornix lesions were impaired
on the explicit version of the two-platform task, but animals with caudate
lesions performed as well as unoperated controls. Conversely, on the implicit
version of the task, rats with caudate lesions were impaired in learning the
task, but rats with fornix lesions performed no differently from unoperated
controls.
McDonald and White (1993) uncovered evidence of a triple dissociation
of function across the hippocampus, amygdala, and striatum. Unoperated
control animals, as well as animals with damage to the amygdala, were trained
on the win-shift and win-stay versions of the radial arm maze (see above) as
well as on a radial arm maze version of a conditioned cue preference (CCP)
task. In the CCP task, which used only two of the eight arms in the radial arm
maze, one arm was lighted, and the second arm was not. For half of the
animals, the lighted arm signaled reward, and the dark arm signaled no
reward; for the remaining half, the cue-reward associations were reversed.
During testing, rats’ preference for the rewarded arm was measured. The
experiments revealed a triple dissociation: Rats with damage to the fornix
were impaired on the win-shift version but not on the win-stay or CCP

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62 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

versions; rats with dorsal striatum lesions were impaired on the win-stay
version but not on the win-shift or CCP versions; and rats with amygdala
lesions were impaired on the CCP version but not on the win-shift or win-stay
versions.
Double Dissociations: Human Studies. Bechara et al. (1995) reported
data from three patients — one with damage to the amygdala, one with
damage to the hippocampus, and one with damage to both the hippocampus
and amygdala. The patients were trained in a classical conditioning procedure
in which the CS was either pictures or sounds, and the US was a very loud
noise. The dependent measure was the skin conductance response. The patient
with lesions of the amygdala showed no conditioning but could describe facts
about the task, such as the stimuli. The patient with hippocampal damage
exhibited conditioning but was unable to describe facts about the task. The
patient with damage to both the hippocampus and amygdala showed neither
conditioning nor the ability to describe facts about the task. Thus, this study
shows a double dissociation between conditioning (implicit memory) perfor-
mance and declarative (explicit memory) knowledge with respect to the func-
tions of the amygdala and the hippocampus.
A second study demonstrating a double dissociation was conducted by
Gabrieli, Fleischman, Keane, Reminger and Morrell (1995). In this study, a
patient with damage to the right occipital lobe received a perceptual identifica-
tion (implicit memory) test with 24 old and 24 new words. Initially, the stimuli
were presented very briefly, and then the duration of each word presentation
increased until the subject correctly identified the word. In the recognition
test, the patient was presented with 48 words and asked to judge if each word
had been seen before. The patient was no faster at identifying old words than
new words but performed as well as the controls on the test of recognition
memory. According to the authors, this patient, along with amnesics who
showed the opposite pattern of results,
“provides the first neuropsychological evidence for [a double dissociation]
that illuminate[s] the functional neural architecture of human memory: A
memory system mediating visual implicit memory…is separable from the
memory systems mediating explicit memory for words” (p. 81).

In another example of a double-dissociation study in humans, Knowlton,

Mangels and Squire (1996) tested amnesics and patients with Parkinson’s
disease, who have damage to the substantia nigra — a component of the
system thought to support implicit memory. Two tasks were used — a

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NEUROANATOMICAL BASIS OF MEMORY SYSTEMS 63

probabilistic classification learning task (implicit memory) in which subjects

had to learn whether a visual pattern predicted rain or shine, and a multiple-
choice test that assessed their declarative (explicit) memory for the first task.
Both amnesic and control patients learned the probabilistic classification task
at the same rate, but the performance of patients with Parkinson’s disease was
impaired. However, both the Parkinson and control patients did well on the
multiple-choice test, but amnesics performed poorly. The authors concluded
that probabilistic classification learning depends on the integrity of the cau-
date nucleus and the putamen, whereas declarative memory depends on the
integrity of the medial temporal lobe.
Two points are worth mentioning: First, with extended training, the
Parkinson patients were able to perform the implicit task at an above-chance
level, but they simply did not perform it at the same levels in the same number
of trials as amnesic patients. Second, because the Parkinson patients also had
frontal lobe dysfunction, their memory impairment may have resulted from
this damage instead of from damage to the system thought to underlie implicit
memory. The authors addressed this issue by also testing patients with circum-
scribed frontal impairments. They found that these patients’ scores on the
probabilistic classification task were intermediate between the scores of pa-
tients with amnesia and Parkinson’s disease. Therefore, the possibility that
some frontal damage may have contributed to the impairment on the probabi-
listic classification task is difficult to dismiss.

Conclusions

In this chapter, we have reviewed the effects of damage to the medial temporal
lobe on explicit and implicit memory performance in humans and nonhuman
animals. We have also reviewed the neural substrates of explicit and implicit
memory. Finally, we have tackled the question of whether this evidence points
to a single memory system or a multiple memory system.
There is ample evidence to suggest that explicit and implicit memory are
mediated by two distinct neural systems — one that taps structures in the
medial temporal lobe, and the other that taps structures in the striatal system.
This view, however, is not without problems. It is hard to escape the fact, for
example, that the vast majority of studies have reported impairments in
explicit but not implicit memory performance. Furthermore, although a few

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64 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

studies have noted impairments in implicit but not explicit memory perfor-
mance after damage to structures that are believed to support implicit memory,
it is usually the case that some learning on implicit tasks is still possible. For
that matter, some learning on explicit tasks is also possible after damage to
structures that are believed to support explicit memory. With respect to
multiple memory systems, there seems to be ample support for the soft
definition of a double dissociation in memory performance but very little
support for the hard definition of a double dissociation.

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CHAPTER 4

The Jacksonian Principle and Memory

Development

The Jacksonian principle states that the nervous system is organized hierarchically and that
the development and dissolution of function follow a first-in, last-out sequence. The general
finding that implicit memory is spared in brain-damaged human amnesics but explicit
memory is not, encouraged the application of the Jacksonian principle to the development
and dissolution of memory systems. This principle attributes implicit memory to a primitive
memory system that matures quite early in development and explicit memory to a late-
maturing memory system. This chapter reviews the Jacksonian principle and evidence of its
applicability to the hierarchical development and dissolution of memory in animals and
children.

The Jacksonian principle

In 1884, John Hughlings Jackson introduced the concept that the nervous
system — and the behavior that it controlled — was vertically and hierarchi-
cally organized. By this account, the neural functions that appeared first in
evolution are also those that appear first in development and disappear last in
disease. This progression reflects the fact that earlier-appearing neural ele-
ments are overlaid or suppressed by new functions under higher levels of
neural control as the nervous system continues to develop. The later-appearing
neural elements are increasingly more fragile or susceptible to disruption by
disease or other challenges. As a result, adverse conditions can reverse the
stages of evolution and the development of the nervous system such that the
neural control of behavior reverts to that of a more primitive stage. This
account is referred to as the Jacksonian principle of the development and
dissolution of function. In brief, the Jacksonian principle states that the last
functions to develop are the first to disappear after brain damage from injury,

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66 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

disease, or aging, whereas the first functions to develop are the last to be
affected when the organism undergoes demise.
Classic examples of the Jacksonian principle come from studies of reflex-
ive development. The first objective reports of fetal reflexive development
were by Hooker (1952), who filmed exteriorized, prevital foetuses in a tem-
perature-controlled water bath as they underwent anoxia. Hooker reported that
the first foetal response to tactile stimulation at 7½ postmenstrual weeks was a
contralateral reflex in which the head and upper trunk bent away from the site
of stimulation. Contralateral reflexes are referred to as avoiding reactions
because they move the stimulated region away from the stimulating source
(Angulo y Gonzales 1932; Coghill 1916, 1929). Beginning at 11½ post-
menstrual weeks, contralateral reflexes began to be replaced by ipsilateral
reflexes. The earliest appearing reflexes were total-pattern reflexes. Later
appearing reflexes were increasingly specific to the site of stimulation and
progressed cephalocaudally with age: Stimulated head movements preceded
stimulated hand movements, which preceded stimulated plantar movements,
which preceded integrated hand-mouth reflexes (Humphrey 1969). This same
sequence was subsequently observed in spontaneous activity by de Vries,
Visser and Prechtl (1984), who recorded foetal activity longitudinally over the
course of gestation.
Critical support for the Jacksonian principle was Hooker’s finding that as
the foetus progressively underwent anoxia, stimulated reflexes disappeared in
the reverse order of their original appearance, with the most primitive reflexes
being preserved the longest. As one example, ipsilateral reflexes were replaced
by contralateral reflexes. A reversion in the sequence of reflexes accompany-
ing anoxia was also reported by Angulo y Gonzales (1932). Hooker attributed
this reversion to the fact that the reflexes that appeared first in development
required less oxygen to perform:
“The low oxygen capacity of the early embryo is evidently without untoward
effect upon the activity of the primary reflex arcs. They have developed in a
still lower oxygen environment and the greater supply at the time of their
beginning function is entirely adequate. This is not the case, however, with
newer neural mechanisms which become active later. It is particularly not the
case in connection with those centers which have their synapses at higher
levels of the central nervous system…all newer neural components which
develop find a decreasing increment in oxygen supply….As a result, there is a
tendency for newer neural mechanisms at higher levels to succumb relatively
early to the effects of anoxia and asphyxia. This causes a reversion in the

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THE JACKSONIAN PRINCIPLE AND MEMORY DEVELOPMENT 67

behavior pattern to an earlier type of activity in young fetuses” (Hooker 1952,

pp. 104–105).

Humphrey (1969) reported that the developmental sequence of the appearance

of prenatal reflexes was recapitulated postnatally during the transition from
elicited to voluntary activity. She hypothesized that the postnatal repetition of
fetal activity sequences was similarly due to the lower oxygen requirement of
more primitive fetal reflex arcs. That is, those reflexes that were mediated by
reflex arcs that had functioned the longest required less oxygen to be initiated
than reflexes that were mediated by reflex arcs that had matured more re-
cently. However, the sequence in which the postnatal reflexes appeared, like
the sequence of prenatal reflexes previously observed by Hooker, was re-
versed when the organism underwent challenge:
“Thus when the oxygen supply is decreased or conditions are unfavourable for
other reasons, the reflexes that develop earliest are the most readily elicited.
Since recently developed centres require a higher oxygen level, motoneurones
that have been active for a longer time are more easily fired than newly
functioning motor nerve cells, and so become regulated earlier by descending
fibre systems than do those that mature later” (Humphrey 1969, p. 67).

In other words, the developing organism always reverts to earlier maturing

reflexes if the oxygen supply is not good because the reflexes that matured
more recently require more oxygen in order to be elicited. Thus, for example,
if the neonate is stressed, then primitive contralateral reactions reappear
(Humphrey 1969). Likewise, following some kinds of brain injury (Willis &
Grossman 1973), adults exhibit the Babkin reflex — a very rudimentary reflex
that consists of opening the mouth or gaping, returning the head to midline, and
raising or flexion of the head (Babkin 1960). It has been observed in premature
infants as early as 14 weeks of gestational age but is suppressed between the
third and fourth postnatal month (Humphrey 1969). Also, during advanced
stages of senility, adult patients often exhibit primitive foetal and infantile
reflexes (Paulson 1977). For example, infantile sucking and grasping reflexes
reappear in patients with advanced senile dementia (Paulson & Gotlieb 1968).
Support for the Jacksonian principle has also been found in the domain of
sensory function. This was described by Gottlieb (1971), who reviewed the
development of sensory function in a variety of avian and mammalian species,
including man. He found that the sequential onset of function was the same in
all species — tactile, vestibular, auditory, and visual. Alberts (1978) extended

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68 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

this sequence to the developing rat, finding that the thermal and chemical
(olfaction, gustation) senses were the last to develop prenatally — after
vestibular and tactile sensation; audition and vision began functioning postna-
tally. In the course of normal aging in humans, these functions (olfaction,
thermal sensitivity, audition, and vision) decline in the reverse order of their
onset.

The Jacksonian principle and animal memory

The Campbell, Sananes, and Gaddy study

One of the first attempts to apply the Jacksonian principle to the development
and dissolution of memory function in animals was undertaken by Campbell,
Sananes and Gaddy (1984, 1985). Given evidence that developing animals
typically exhibit poorer memory than adults (Campbell & Spear 1972), these
investigators asked if the Jacksonian principle describes the sequential appear-
ance of various memory abilities in infant animals and the sequential decline
of the same memory abilities in aging animals. To answer this question,
Campbell et al. (1984) conducted a major review of the studies of memory
performance on tasks that had been used in common with infant, young adult,
and aged rats. This section reviews their basic assumptions, the relevant
findings, and their final conclusions.
The Basic Assumptions. In order to provide a compelling test of the
Jacksonian principle, Campbell et al.’s analysis was based on four assump-
tions. First, they required that the tasks that were used with normal adult and
aged rats had to be solved sequentially during development by the prewean-
ling rat. Three representative tasks for which infants exhibited sequential
development of long-term memory were conditioned taste aversion, which
infants learn at the youngest age; the auditory conditioned emotional re-
sponse, which infants learn when they are slightly older; and visually-based
passive avoidance, which infants learn when they are older yet. The rate at
which rat pups acquired these three tasks mirrored the sequential development
of the sensory systems on which they depended (Alberts 1984) — gustation,
audition, and vision, respectively. A fourth task, spatial learning, also relies
heavily on visual cues and appears quite late in infancy. Animals’ perfor-
mance on this task will be considered separately below (“Final Conclusions”).

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THE JACKSONIAN PRINCIPLE AND MEMORY DEVELOPMENT 69

Second, Campbell et al. required that a common metric be used to

compare retention of the various tasks across the different ages. For this, they
used percent retention scores, defining 100% retention as the terminal training
score or the preset ceiling level, and 0% retention as either the score on the
first training trial or the test score of an untrained control group. Third, they
required that young adults exhibit a relatively low rate of forgetting in order
that greater forgetting on the part of younger and older subjects could be seen.
And fourth, as evidence for the Jacksonian principle, they required that aged
adults exhibit a sequential loss of memory in the reverse order from that
exhibited by infants.
The Findings. The corresponding percent retention data for preweanlings,
normal adults, and aging adults as a function of the retention interval are
presented in Figure 4.1 for the three tasks. The studies from which these data
were drawn are listed in Table 4.1. The data of infants (in the left panel of each
figure) show that they forgot each of the three tasks rapidly. The data of young

Table 4.1. Studies that Assessed the Memory Performance of Infant, Young Adult, and Aged
Adult Rats on Conditioned Taste Aversion, Auditory Conditioned Emotional Response, and
Passive-Avoidance Tasks (Cited in Campbell, Sananes & Gaddy 1984)
Task x Age Study
Conditioned Taste Aversion
Infants Campbell & Alberts, 1979; Gregg et al., 1978; Schweitzer
& Green, 1982
Young Adults Campbell & Alberts, 1979; Cooper et al., 1980;
Guanowsky & Misanin, 1983; Klein et al., 1977;
Steinert et al., 1980
Aged Adults Cooper et al., 1980; Guanowsky & Misanin, 1983

Auditory Conditioned Emotional Response

Infants Dean et al., 1981
Young Adults Campbell & Campbell, 1962; Campbell et al., 1980
Aged Adults Campbell et al., 1980

Passive Avoidance
Infants Schulenberg et al., 1981; Stehouwer & Campbell, 1980
Young Adults Bartus et al., 1980; Campbell et al., 1980; Dean et al., 1981;
Gold et al., 1981; Jensen et al., 1980; Schulenberg et al.,
1981
Aged Adults Bartus et al., 1980; Campbell et al., 1980; Dean et al., 1981;
Gold et al., 1981; Jensen et al., 1980

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70 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 4.1. Scatterplots of transformed retention data from differently-aged rats in condi-
tioned taste aversion tasks (top panel), auditory conditioned emotional response tasks
(middle panel), and passive-avoidance tasks (bottom panel). From left to right, panels
contain data from infants, young adults, and aged adults, respectively. Each point represents
an independent observation from one of the studies listed in Table 4.1.

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THE JACKSONIAN PRINCIPLE AND MEMORY DEVELOPMENT 71

adults (in the middle panel of each figure) reveal that they exhibited little or no
forgetting of any task after any retention interval, thereby meeting Campbell et
al.’s third requirement. The sole exception occurred in a passive-avoidance
study in which the researchers had used a single training trial, a weak shock,
and a very long retention interval (Gold, McGaugh, Hankins, Rose & Vasquez
1981). The data of old adults are presented in the right panel of each figure.
As shown in Figure 4.1, the pattern of retention across tasks reveals no
consistent relation between forgetting by the aged rats and forgetting by the
infants. Whereas infants exhibited rapid forgetting in the conditioned taste
aversion and auditory conditioned emotional response tasks, for example,
aged rats exhibited almost perfect retention in the same tasks over the same
delays. Recall, however, that the passive-avoidance task is the last task to be
learned during development, and only in some studies using this task did the
aged adults forget as rapidly as infants — in several other studies, they
exhibited near-perfect retention after very long delays.
Only one task provided support for the Jacksonian hypothesis. Prewean-
lings exhibited no spatial learning prior to 20 days of age whether they were
tested in an eight-arm radial maze (Rauch & Raskin 1984) or in a Morris water
maze (Schenk, Inglin & Morris 1983). Likewise, old adults failed to attain the
final level of performance of young adults in the eight-arm radial maze even
after extensive training (Davis, Idowu & Gibson 1983; Wallace, Krauter &
Campbell 1980); similar results were found in the Morris water maze when the
hidden platform was moved (Gage, Dunnett & Bjorklund 1984). These data,
then, yield the inverted U-shaped function of acquisition and retention that is
predicted by the Jacksonian hypothesis. (The extent to which age-related
deficits in perception, motivation, or motoric competence contributed to these
results is not known.)
Final Conclusions. Campbell et al. asked whether the Jacksonian hypoth-
esis predicts the development and dissolution of memory in animals. They
found that rats’ memories for the two tasks that were acquired sequentially
early in ontogeny (conditioned taste aversion, the auditory conditioned emo-
tional response) were completely spared in aged rats. Aged rats exhibited no
evidence of sequential loss. Although memory for the spatial learning task,
which is acquired late in ontogeny, was consistently impaired in aged rats,
their memory for the passive-avoidance task, which also is acquired late in
ontogeny — and after the taste aversion and conditioned emotional response
tasks, was not. In fact, in some passive-avoidance studies, aged rats exhibited

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72 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

near-perfect retention. Again, then, aged rats exhibited no evidence of sequen-

tial loss. Based on these studies, Campbell et al. concluded that there was no
compelling evidence for extending the Jacksonian hypothesis to the develop-
ment and dissolution of memory in animals.

The Jacksonian principle and pathology in human memory

Extending the Jacksonian principle to human memory also requires evidence

that the sequential appearance and disappearance of memory capabilities
follow an inverted U-shaped function. This function has long been docu-
mented in cases of human pathology. Ribot (1882) anticipated the Jacksonian
principle in cognitive functioning and cited extensive anecdotal evidence that
more recent memories are more vulnerable. The temporally organized dissolu-
tion of memory is illustrated in an anecdote that Ribot (1882) obtained from a
physician in Philadelphia:
“Dr. Scandella, an ingenious Italian who visited this country a few years ago,
was a master of the Italian, French, and English languages. In the beginning of
the yellow fever, which terminated his life…he spoke English only; in the
middle of the disease, he spoke French only; but, on the day of his death, he
spoke only in the language of his native country” (Ribot 1882, p. 182).

Modern data on the phenomenon of retrograde amnesia suggest that although

most amnesics forget memories of at least some events that occurred before
the onset of their pathology, they continue to remember events that occurred
earlier in their lives. Using a questionnaire consisting of multiple-choice
questions about television programs that had been broadcast for only 1 year at
different times in the past, for example, Squire and Slater (1975) found that
amnesics’ memory for programs within the 5 to 10 years that preceded testing
was poor relative to their memory for programs from the more distant past.
Another example of the development and dissolution of human cognitive
functioning was reported by Ajuriaguerra, Rey-Bellet-Muller and Tissot
(1964), who observed that the sequence in which Piagetian abilities emerged
in childhood (Piaget 1952) disappeared in the reverse order as the cognitive
abilities of senile adults progressively degenerated. In general, the capacities
that children acquired last over the course of development dropped out first
when adults became senile.
Retrograde amnesia can also accompany more temporary amnesic states.

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THE JACKSONIAN PRINCIPLE AND MEMORY DEVELOPMENT 73

Scoville and Milner (1957), for example, described a middle-aged doctor

(D.G.) who was densely amnesic for events that immediately followed his
temporal-lobe surgery but had clear and detailed memories of his childhood
and medical training. Finally, even benign senescence can be accompanied by
a loss of memories for events from the recent past and the preservation of
memories from childhood. In both of these cases, however, adults’ preserved
memories of childhood events do not include events from the early childhood
period that is typically characterized by infantile amnesia (Rozin 1976).

The Jacksonian principle and multiple memory systems

Memory studies with adults

Many scientists have argued that the order in which memory systems fail in
elderly and amnesic adults predicts the order in which they appear in infancy
(Nadel 1990; Naito & Komatsu 1993; Parkin 1993; Schacter & Moscovitch
1984; Tulving & Schacter 1990). Nadel (1990), for example, proposed that the
hippocampal system is essential for the formation of cognitive maps and that,
during development, an increasingly greater proportion of it becomes func-
tional until a threshold level of connectivity is passed and the structure as a
whole can function. Invoking the Jacksonian principle, he wrote:
“[This view] seems to provide a handle not only on the up-side of life
(development), but also on the down-side (senescence, or brain damage). It is
well known that many brain functions undergo what ‘connectionist’ modelers
have come to call ‘graceful degradation’ with aging/damage. That is, the
progressive removal of functional elements from the system has little impact
until some critical extent is reached, at which point the system rapidly
deteriorates. This phase transition is really the mirror image of what is seen
during early life [italics ours]…” (p. 621).

In fact, that part of the Jacksonian principle that applies to the hierarchical
dissolution of multiple memory systems has met with some success. Most
research on the effects of age on the memory performance of healthy individu-
als has found that elderly adults are inferior to young adults on explicit
memory tasks but perform as well as young adults on implicit memory tasks
(for reviews, see Graf 1990; Light & Lavoie 1993). In particular, age-related
memory deficits have been found on tests of recognition and cued recall, but
age differences on various single-item priming tests have been small or absent

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74 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

altogether (e.g., Isingrini, Vazoiu & Leroy 1995; Java & Gardiner 1991; Light
& Albertson 1989; Light & Singh 1987; Mitchell, Brown & Murphy 1990).
Mitchell and Schmitt (1992, cited in Mitchell 1993), for example, com-
pared the memory performance of young adults, healthy older adults, and older
patients with Alzheimer’s disease on two explicit memory tasks (cued recall
and free recall) and an implicit memory task (priming). They found that
performance on the free-recall task was worse for both groups of older adults
than for the younger adults, performance on the cued-recall task was the same
for the younger and healthy older adults but was impaired for older adults with
Alzheimer’s disease; in contrast, performance on the priming task (picture-
naming latencies) was equally excellent for all groups. They concluded that the
brain damage associated with Alzheimer’s disease hastened the dissolution of
the memory system responsible for performance on the free-recall task but
spared the memory system responsible for performance on the priming task.
Developmental changes in healthy young and older adults’ ability to
recognize specific item, location, and color information in isolation was
examined by Chalfonte and Johnson (1996). Participants studied a particular
feature of a set of line-drawn objects (from Snodgrass & Vanderwart 1980)
that were arranged on a grid and were not in their original color. They then
received a recognition test for one type of feature. For the item recognition
test, they saw old and new black and white objects; for the location recogni-
tion test, they saw black Xs in old and new locations on the grid; and for the
color recognition test, they saw old and new colors on rectangles. Young and
older adults recognized item and color information equivalently, but older
adults’ recognition of location information was impaired.
Although healthy elderly adults perform more poorly than young adults
on tasks that require them to retrieve factual knowledge that was presented
earlier (Radvansky, Zacks & Hasher 1996), they perform as well as or better
than young adults on tasks that require subjects to exhibit more global levels
of understanding, for example, the ability to understand what is being referred
to by the presented information (Radvansky 1999). Thus, although the decline
of memory functioning in elderly adults is consistent with the Jacksonian
principle, their excellent-to-superior performance on some higher-level cogni-
tive tasks is not.

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THE JACKSONIAN PRINCIPLE AND MEMORY DEVELOPMENT 75

Memory studies with children

That part of the Jacksonian principle that applies to the hierarchical develop-
ment of multiple memory systems in childhood has yielded findings that, on
the surface, appear to be consistent with the Jacksonian hypothesis. When
analyzed more carefully, however, the findings appear to be more inconclu-
sive. The issue is whether or not implicit memory performance, as measured in
these studies, remains stable over age. Most research on the effects of age on
the performance of children on explicit and implicit memory tasks has re-
ported that performance on recall and recognition tests improves with age,
while performance on priming tests remains stable (e.g., Carroll, Byrne &
Kirsner 1985; DiGiulio, Seidenberg, O’Leary & Raz 1994; Greenbaum &
Graf 1989; Naito 1990; Parkin 1989; Parkin & Streete 1988). Based on this
pattern, most researchers concluded that implicit memory develops earlier
than explicit memory in childhood. Parkin (1993), for example, attributed the
earlier appearance of implicit memory to phylogenetic influences. In doing so,
he invoked Jackson’s (1880) argument that the neural systems that are evolu-
tionarily more primitive (e.g., those that mediate the organism’s perceptually-
based responding) are more localized than the neural systems that appeared
later in evolution (e.g., those that mediate higher-level neural functions) and
are more widely distributed throughout the brain. Assuming that ontogeny
recapitulates phylogeny — an assumption that the noted evolutionary biolo-
gist Steven Jay Gould has vigorously disputed (Gould 1998), Parkin con-
cluded that the phylogenetic system that is more primitive and mediates
perceptually-based memory performance (i.e., implicit memory) appears ear-
lier in development and is less susceptible to insult in old age than the
phylogenetic system that mediates higher-level memory performance (i.e.,
explicit memory).
Studies of children’s memory performance on implicit and explicit tests
have increased in frequency over the last decade. Their general finding is that
memory performance on implicit tests is invariant over age, whereas memory
performance on explicit tests increases with age. A pervasive interpretative
problem in studies of children’s memory development, however, is the ready
tendency of researchers to attribute age-related changes in memory perfor-
mance to maturational changes in the brain. Although such changes are just as
likely to reflect age-related differences in experience or language develop-
ment, this possibility is rarely considered.

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76 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

In a typical study (Naito 1990), groups of first-, third-, and sixth-grade

children and college students were shown a list of 32 words, one per page, in a
study booklet and were asked whether a word contained a particular letter and
what the word’s category name was. The study list was followed by a 4-min
distractor task. In Experiment 1 of this study, children received a word-
fragment completion test of implicit memory consisting of the original 32
words and 16 new ones. All age groups completed old items more accurately
than new items, and adults completed more items than the other age groups,
who did not differ; there was no interaction. In addition, whether encoding
was orthographic (shallow) or elaborative (deep) did not differentially affect
memory performance at any age, and the magnitude of proportional repetition
priming on the implicit test was approximately the same at all ages.
In Experiment 2 of the same study, Naito repeated the preceding proce-
dure but this time asked children to recall the words that had been on the study
list — an explicit memory test. The number of words correctly recalled
increased with age, and all children except the first graders recalled more
words in the elaborative than in the orthographic encoding condition. Taken
together, these experiments revealed that performance on implicit memory
tests is stable over age and is insensitive to encoding condition, whereas
performance on explicit memory tests increases with age and is affected by the
conditions of encoding.
These studies, however, like most studies of children’s memory develop-
ment, have used verbal materials — the practice commonly followed with
adults. Unfortunately, this practice has introduced a major confound into the
memory data from children in terms of age differences in verbal competence.
Some researchers have sidestepped this problem by testing children with
pictorial stimuli. Not only is children’s memory performance better when they
are tested with pictures than with words (Madigan 1983), but also pictures can
be used in memory tests with all ages and species (e.g., Cornell 1974; Wright,
Santiago, Sands, Kendrick & Cook 1985). Mitchell (1993) performed a meta-
analysis over nine developmental studies that had used pictorial stimuli and
had compared at least two age groups of children or adults on both an explicit
and an implicit memory test. All studies in his analysis met the retrieval
intentionality criterion for distinguishing between intentional and uninten-
tional retrieval on explicit and implicit tests, respectively (Schacter et al. 1989;
see Chapter 2). In addition, all studies used recognition tests of explicit
memory except two, which used cued-recall tests. The implicit memory tests

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THE JACKSONIAN PRINCIPLE AND MEMORY DEVELOPMENT 77

that they used were picture naming, picture-fragment completion, object

decision, and category exemplar generation.
Mitchell found no significant age differences in accuracy or latency on
implicit tests. On the explicit tests, however, he found large age differences in
accuracy that were described by an inverted U-shaped function, with older
children performing significantly better than younger children (age range = 3
to 12 years) and older adults performing significantly worse than younger
adults (age range = 18 to 71 years). Moreover, the memory dissociation on
implicit and explicit tests was just as robust between 3 and 5 years of age as
between 18 and 71 years of age. He concluded that memory performance on
tasks using pictorial materials was similar to memory performance on tasks
using verbal materials: Performance on explicit memory tests changes over
the course of normal aging, whereas performance on implicit memory tests
does not. Characterizing memory development over the life span in traditional
Jacksonian terms, he wrote:
“As the most specialized system, episodic memory is the last to develop fully
in childhood. Its unique specialization, however, may also make it the most
fragile, and therefore it is the first to go in the course of normal aging.
Procedural memory…seem[s] to be hard-wired from the start and…[is] very
hardy in surviving the effects of aging” (Mitchell 1993, p. 173).

Snodgrass (1989), however, was concerned that correct identification on

picture-completion tests could arise from one or more of three sources — pure
guessing, when subjects actually cannot identify a test item; learning a specific
association between an unrecognized fragment and its name during test trials,
so that the fragment itself actually becomes the retrieval cue; or true perceptual
learning at the time of priming, which results from phenomenologically
reexperiencing the previously studied event and retrieving it automatically and
effortlessly from semantic memory. She hypothesized that true perceptual
priming may reflect how correct identification is measured. Typically, research-
ers measure correct identification as the savings in accuracy of identifying old
versus new pictures, but this could be expressed as either the absolute difference
between the number of old and new pictures correctly identified (e.g., Jacoby
& Dallas 1981; Roediger & Weldon 1987) or as the relative difference (the
absolute difference divided by the maximum possible difference). The absolute
measure disregards initial baseline performance, whereas the relative measure
takes into account the total number of pictures that subjects had an opportunity
to learn during testing. Using both measures to analyze a prior data set, she and

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78 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

her colleagues found that the relative measure provided a better fit to the data
(Snodgrass, Smith, Feenan & Corwin 1987).
The particular savings measure that is used has major consequences for
conclusions about whether priming changes with age. Mitchell’s meta-analy-
sis, for example, included a study by Parkin and Streete (1988) with subjects
ranging from 3 years of age to young adults. When they expressed savings as
the absolute difference in correct identifications of old and new items, they
found that priming increased with age, but when they calculated the difference
proportionally to take baseline differences into consideration (i.e., the number
of items correctly identified on trial 2 minus the number of items correctly
identified on trial 1/the number of items correctly identified on trial 2), they
found that priming was age-invariant (see also Graf 1990). When Parkin
(1993) recalculated the amount of priming in the original data set using
Snodgrass’s (1989) measure of relative difference, however, he again found
that priming increased significantly with age.
In a subsequent study using pictorial stimuli, Russo et al. (1995) at-
tempted to exclude potential explicit memory influences from the final esti-
mate of implicit memory (for discussion, see Jacoby et al. 1993; Russo &
Parkin 1993) and to eliminate age differences in baseline responding. In an
initial experiment, preschoolers between 4 and 6 years of age and a group of
young adults participated in two tasks — a picture-completion (implicit
memory) task and a cued-recall (explicit memory) task. Two sets of pictures
were used for the implicit task and a third set was added for the explicit task.
During the study phase of both tasks, children were asked to name the objects
that appeared in 12 pictures.
In the picture-completion test, children were shown up to eight versions
each of the old pictures and 12 new ones and were asked to identify the objects
in the pictures as quickly as possible. The most fragmented version of all
objects was presented first, followed by the next most fragmented version of
all objects, and so forth until the whole object was presented. Once an object
was correctly identified, it was not tested further. Scoring was based on the
level of fragmentation at which an object was correctly identified. For the
cued-recall test, children were shown the fragmented versions of the old
objects and asked to use them as cues to try and remember what they had seen
during the study phase. The two ages did not perform differently on the
priming test, but 6-year-olds were superior on the cued-recall test.

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THE JACKSONIAN PRINCIPLE AND MEMORY DEVELOPMENT 79

In a follow-up experiment, Russo et al. repeated the preceding procedure

but included a group of young adults and asked all subjects to recall the
pictures they had previously named before performing the picture-completion
test. All age groups exhibited equivalent priming, but the number of pictures
recalled increased with age. To determine whether prior recall on the explicit
test had contaminated performance on the ensuing repetition priming test,
separate proportional priming scores were calculated for the objects that had
been recalled and for those that had not. Adults’ priming scores were signifi-
cantly higher for previously recalled objects, but children’s priming scores
were the same regardless of whether they had initially recalled the object.
These data reveal that when researchers are careful to control for the potential
contribution of explicit influences on implicit memory performance, implicit
memory is age-invariant from at least 4 years of age (the age of the youngest
children in the present study), whereas explicit memory improves with age.
More recently, researchers have used the serial reaction time (SRT) task
(see Chapter 2) to study the development of implicit and explicit learning and
memory (Meulemans et al. 1998; Thomas 1997). Using a within-subject
design, for example, Meulemans et al. (1998) trained 6- and 10-year-olds and
adults for either one session or two sessions separated by 1 week and tested
their retention immediately after their last (or only) session. On each trial,
subjects saw four arrows on a computer screen with a star underneath one of
the arrows. They were instructed to press the button on the computer keyboard
(X, C, N, M) that corresponded to the starred arrow as quickly as possible but
to try to make as few mistakes as possible. Alternating blocks of 10 trials were
programmed so that the sequence of starred spatial positions was either
random or repeating. Immediately before the recognition test, subjects were
told that one of their study sequences had been repeating. During the test, they
saw eight sequences of four stimuli from the repeating-sequence condition
(old) and eight sequences that they had never seen (new) and were asked to
rate on a scale from 1 to 5 (“I am sure I never saw it,” “I believe I never saw it,”
“I don’t know,” “I believe I saw it,” “I know I saw it”) whether each four-item
test sequence had been part of the repeating sequence or not. As expected, RTs
decreased over successive trial blocks and were faster for older subjects and
on repeating than on random sequences. The pattern of RTs on the two types
of sequences, however, was the same at all ages. In addition, more errors were
made by children than adults and on random than on repeating sequences; this
effect did not change over blocks.

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80 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

One week later, RTs were significantly faster at the outset of session 2 than
they had been at the end of session 1 for both 6- and 10-year-olds but not for
adults, whose RTs could not decrease further. Although adults responded that
they had seen a test sequence before more often than children whether it was old
or new, the most frequent response was “I don’t know,” and performance on the
recognition test was unrelated to performance during the sequence-learning
task. These data, then, are consistent with prior evidence that performance on
implicit tasks does not change over development and is statistically indepen-
dent of performance on explicit tests of the same information.
Pictures have also been used to assess the basic features of an object that
children of different ages recognize. Using exactly the same line-drawn stimuli
that had been used with healthy adults (Chalfonte & Johnson 1996), Gulya,

Figure 4.2. Mean corrected recognition scores for 5-, 7-, and 10-year-old children on three
nonverbal feature recognition tests.

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THE JACKSONIAN PRINCIPLE AND MEMORY DEVELOPMENT 81

Rossi-George, Hartshorn, Rovee-Collier, Johnson and Chalfonte (submitted)

obtained recognition data for the identity, color, and location of objects from
4-, 5-, 7-, and 10-year-olds and analyzed them with the data previously
obtained from 19- and 70-year-olds on identical feature tests. These analyses
revealed that memories for different types of features develop at different rates
over the childhood period and that their decline in old age approximates the
reverse order of their acquisition. As shown in Figure 4.2, item recognition was
already excellent by 4–5 years of age, whereas color recognition improved
significantly between 5 and 10 years of age and peaked at 10 years of age.
Children’s memory for location was poor at all ages, but location memory
peaked at 19 years of age (see Figure 4.3). Conversely, by 70 years of age,

Figure 4.3. A comparison of the mean corrected recognition scores of 10-year-old children
19-year-old (young) adults, and 70-year-old (elderly) adults. An identical pencil-and-paper
version of the feature recognition task with identical study and test stimuli was used with
children and adults.

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82 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

adults’ memory for location had significantly worsened, and their color recog-
nition had begun to decline as well, predictive of an even greater decline at
older ages. Nonetheless, elderly adults’ item recognition was excellent and at
the same high level as that of the youngest children. This inverted U-shaped
function is consistent with Jackson’s first-in, last-out principle and suggests
that the Jacksonian principle describes the development and dissolution of
memory for individual features.

Conclusions

The Jacksonian principle states that the development and dissolution of func-
tion follow a first-in, last-out sequence. The present chapter reviewed evi-
dence that this principle also describes the development and dissolution of
memory. Studies of memory function with infant, young adult, and aged
animals failed to support the Jacksonian principle. In all but one instance, the
tasks that were acquired earliest in ontogeny were not learned or remembered
better at other ages than the tasks that were acquired later in ontogeny. Studies
with young adults and healthy elderly adults, however, found that normal
memory performance declines late in adulthood on explicit but not implicit
tests, and studies that were free of age confounds in verbal competence or base
rates of responding found that memory performance improves during child-
hood on explicit tests but not implicit tests. The combined results of these
studies portray explicit memory performance as an inverted-U shaped func-
tion of age and implicit memory performance as age-invariant over the major
portion of the life span.
These studies, however, assessed developmental changes in implicit and
explicit memory performance in individuals for whom both types of memory
were already functional. They did not ask whether the onset of implicit and
explicit memory function is hierarchical, which is the first half of the Jackso-
nian principle. To answer this question, we next will consider studies of
implicit and explicit memory in infants (Chapters 5, 6, and 7).

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CHAPTER 5

Development of Implicit and Explicit

Memory in Nonhuman Primates

In this chapter, we review the evidence for a developmental dissociation between implicit
and explicit memory in nonhuman primates. We begin with the classic study conducted by
Bachevalier and Mishkin (1984) in which monkeys were shown to master one memory task
substantially earlier than another during development. We then describe the neural mecha-
nisms that are thought to underpin this age-related change in memory performance. Finally,
we reconsider the notion that there is a developmental dissociation between two memory
systems in nonhuman primates.

As described in Chapter 3, studies with both human and nonhuman adults

have shown that damage to the medial temporal lobe results in a syndrome of
global amnesia. What is particularly intriguing about this phenomenon is that
adults with temporal lobe damage exhibit profound impairment on some
memory tasks but little or no impairment on other memory tasks. This disso-
ciation in memory performance has been the cornerstone for the claim that
memory is not a unitary phenomenon but, rather, is comprised of at least two
functionally distinct systems with different underlying neural pathways.
A second line of evidence often marshaled in support of the multiple-
memory-systems view is that these systems are dissociable during the course
of normal development as well, with one system emerging substantially
earlier than the other (Bachevalier 1990, 1992; Nadel & Zola-Morgan 1984;
Nelson 1995; Rudy 1991; Rudy & Sutherland 1989; Schacter & Moscovitch
1984). The underlying assumption here is that the neural pathways that
support implicit memory mature earlier in ontogeny than the neural pathways
that support explicit memory. In the present chapter, we review the empirical
literature behind the claim that two memory systems emerge independently
during the course of normal development in nonhuman primates. We then

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84 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

discuss the revisions to this claim that are required in light of recent findings.
In Chapters 6 and 7, we address the issue of a developmental dissociation in
the memory performance of human infants.

Historical background

The notion that there is a developmental dissociation in the memory perfor-

mance of nonhuman primates began with a hallmark study by Bachevalier and
Mishkin (1984). In that study, the authors traced the development of monkeys’
performance on two memory tasks over the first 3 years of life. As described
in Chapter 3, prior work with adult monkeys had shown that damage to the
medial temporal lobe impaired performance on the delayed-nonmatching-to-
sample (DNMS) task, but the same damage had no effect on performance on

Figure 5.1. Acquisition of the 24-hour concurrent discrimination (CD) task by 3-month-old
and 3-year-old monkeys. The monkeys were trained first on set A and then on set B. Each
set contained 20 different pairs of stimuli (redrawn from Bachevalier and Mishkin 1984).

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MEMORY DEVELOPMENT IN NONHUMAN PRIMATES 85

the 24-hour concurrent discrimination (CD) task (e.g., Malamut, Saunders &
Mishkin 1984). Based on these findings, Bachevalier and Mishkin (1984)
hypothesized that monkeys’ ability to solve these tasks might emerge inde-
pendently during development if the neural systems that supported perfor-
mance on each task matured at different rates.
To test their hypothesis, Bachevalier and Mishkin (1984) compared the
performance of 3- and 36-month-old monkeys on the 24-hour CD task and the
performance of 3-, 6-, 12-, and 36-month-old monkeys on the DNMS task. In
the CD task, monkeys were trained successively with two sets of 20 pairs of
stimuli (set A, set B). On both sets, one stimulus of each pair was designated as
correct, and choosing that stimulus was rewarded. The other stimulus in the
pair was designated as incorrect; choosing that stimulus was not rewarded.
Within each daily session, a pair of stimuli was presented only once. Acquisi-
tion of the CD task is shown in Figure 5.1. Although 3-month-olds were
slower than 3-year-olds to learn the task when trained with set A (see Fig-

Figure 5.2. Number of days required by 3-, 6-, 12-, and 36-month-old monkeys to learn the
delayed-nonmatching-to-sample (DNMS) task. The dashed line represents criterial levels
of performance (redrawn from Bachevalier and Mishkin 1984).

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86 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

ure 5.1, left panel), there was no age-related difference in the number of
sessions required to learn set B (see Figure 5.1, right panel).
In contrast to performance on the CD task, Bachevalier and Mishkin
(1984) documented a significant age-related difference in the number of days
required for monkeys to learn the DNMS task. Three-year-old monkeys
reached criterion (90% correct) on the DNMS task after only 8 days of
training, whereas 3-month-olds required 36 days of training to achieve the
same level of performance (see Figure 5.2). The performance of 6- and 12-
month-olds was intermediate between these two age extremes. When tested
after a 15-day retention interval, there was an inverse relation between age and
the number of trials required for animals to relearn the task (see Figure 5.3).
Furthermore, younger animals were more impaired than older animals when
the delay between the sample and the test stimuli was increased from 10 to
120 s (see Figure 5.4) and when the list length was increased.

Figure 5.3. Number of trials required by 3-, 6-, 12-, and 36-month-old monkeys to learn
(open columns) the delayed-nonmatching-to-sample (DNMS) task and to relearn (shaded
columns) the same task after a 15-day rest period (redrawn from Bachevalier and Mishkin
1984).

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MEMORY DEVELOPMENT IN NONHUMAN PRIMATES 87

On the basis of these findings, Bachevalier and Mishkin (1984) drew two
conclusions. First, given that the monkeys succeeded on the CD task long
before they succeeded on the DNMS task, Bachevalier and Mishkin con-
cluded that one neural system, which they called the habit system, emerged
earlier in development than the other neural system, which they called the
memory system. Using the terminology adopted in the present book, the habit
system is roughly equivalent to implicit memory, and the memory system is
roughly equivalent to explicit memory. Second, given that adult monkeys with
lesions of the medial temporal lobe (including the hippocampus) are impaired
when tested on the DNMS task but not on the 24-hour CD task, Bachevalier
and Mishkin (1984) attributed the delayed development of DNMS perfor-
mance to the delayed maturation of the hippocampus.

Figure 5.4. Performance of 3-, 6-, 12-, and 36-month-old monkeys on the delayed-non-
matching-to-sample (DNMS) task with delays of 10, 30, 60, and 120 s (redrawn from
Bachevalier and Mishkin 1984).

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88 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

The impact of Bachevalier and Mishkin’s (1984) study cannot be overes-

timated. Since its publication, this paper has been used as prima facia evi-
dence of a developmental dissociation of memory function in nonhuman
primates. Subsequent research by Bachevalier, Mishkin, and others, however,
has challenged the original conclusion that maturation of the hippocampus is
responsible for the emergence of DNMS performance. Research with adult
monkeys, for example, has suggested that the hippocampus plays little or no
role in DNMS performance (see Chapter 3). Furthermore, recent behavioral
research has shown that successful memory performance on a response-to-
novelty task that is procedurally similar to DNMS emerges very early during
development. In fact, a careful review of Bachevalier and Mishkin’s (1984)
original data raises fundamental questions about the issue of a developmental
dissociation between the two putative memory systems of nonhuman primates
per se.

Maturation of the hippocampus and DNMS performance

Bachevalier and Mishkin (1984) originally assumed that the slow emergence
of DNMS performance was due to the late development of the hippocampus.
Subsequent research, however, has shown that the time-table for hippocampal
maturation does not match the time-table for mastery on the DNMS task in
nonhuman primates. Bachevalier and Mishkin’s original assumption that the
hippocampus matured late in ontogeny was based primarily on anatomical
studies that had been conducted with rodents (Nadel & Zola-Morgan 1984).
Similar studies with nonhuman primates, however, have revealed that
the hippocampus matures relatively early in development (Bachevalier,
Ungerleider, O’Neill & Friedman 1986; Diamond 1990a). Although only 15%
of the neurons in the dentate gyrus (a component of the hippocampus) are
present at birth in the rat, 80% of these neurons are present at birth in the
monkey (Rakic & Nowakowski 1981). Furthermore, the opiate and muscar-
inic receptor-binding sites in the hippocampus of the nonhuman primate brain
at birth are virtually identical to those found in the adult brain (Bachevalier et
al. 1986; O’Neill, Friedman, Bachevalier & Ungerleider 1986).
Studies using lesion techniques have also challenged links between the
development of DNMS performance and hippocampal maturation. The ration-
ale behind these studies was that lesions of the hippocampus during infancy

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MEMORY DEVELOPMENT IN NONHUMAN PRIMATES 89

should be less disruptive than the same lesions performed during adulthood if
the hippocampus did not mature until late in ontogeny. Contrary to Bachevalier
and Mishkin’s original hypothesis, however, neonatal lesions of the medial
temporal lobe have been found to severely impair performance on the DNMS
task (Bachevalier & Mishkin 1994; Malkova, Mishkin & Bachevalier 1995).
As shown in Figure 5.5, infants who received bilateral lesions of the medial
temporal lobe during the first month of life were impaired on the DNMS task
when they were tested for the first time at 10 months of age (Bachevalier &
Mishkin 1994), and they continued to be impaired when they were retested at
4 to 5 years of age (Malkova et al. 1995). In fact, the effect of neonatal lesions
on DNMS performance is virtually identical to the effect of adult lesions on
performance in the same task (Mishkin 1978; Mishkin & Philips 1990).

Figure 5.5. The delayed-nonmatching-to-sample (DNMS) performance of rhesus monkeys

following neonatal lesions of the medial temporal lobe and of normal controls (redrawn
from Malkova et al. 1995).

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90 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Finally, the involvement of the hippocampus in DNMS performance per

se has recently been challenged by studies with both nonhuman primate adults
and infants. Although lesions of the entire medial temporal lobe produce
severe impairments in DNMS performance by adult monkeys, lesions re-
stricted to the hippocampus alone produce little (Alvarez et al. 1995) or no
(Murray & Mishkin 1998) effect. Similarly, although neonatal lesions of the
entire medial temporal lobe produce severe impairments in DNMS perfor-
mance by juveniles and young adults (see Figure 5.5), neonatal lesions that are
restricted to the hippocampus do not (Bachevalier, Beauregard & Alvarado, in
press). Taken together, these findings suggest that maturation of the hippo-
campus is not requisite either for DNMS performance by adults or for the
emergence of DNMS performance during development.
In light of these findings, Bachevalier (1992; Bachevalier, Malkova &
Beauregard 1996) has revised her view of the neural basis of the development
of visual recognition memory. She has recently proposed that maturation of
brain area TE, rather than maturation of the hippocampus, may underlie the
development of DNMS performance. In a series of experiments, Bachevalier
and her colleagues have shown that, in contrast to adult lesions of area TE,
neonatal lesions of the same area have only a mild and transitory effect on
DNMS performance (Bachevalier, Brickson, Hagger & Mishkin 1990). These
data suggest that, unlike the medial temporal lobe, area TE exhibits a high level
of plasticity during infancy, indicating that this region of the primate brain is
still functionally immature for some time after birth.
Although Bachevalier’s more recent data suggest that maturation of area
TE, rather than maturation of the medial temporal lobe, may influence age-
related changes in DNMS performance, this finding does not address the issue
of a developmental dissociation between the memory systems of nonhuman
primates per se. Although neonatal lesions of area TE have no effect on DNMS
performance (i.e., the explicit memory task), for example, they also have no
effect on CD performance (i.e., the implicit memory task) (Bachevalier 1992;
Bachevalier & Mishkin 1994; Malkova et al. 1995). Furthermore, adult lesions
of area TE impair performance on both the DNMS and CD tasks (Bachevalier
1992). Given that lesions of area TE do not produce a dissociation in perfor-
mance on the two tasks, the finding that area TE is immature at birth has no
bearing on the issue of a dissociation in the development of the habit and
memory systems.

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MEMORY DEVELOPMENT IN NONHUMAN PRIMATES 91

DNMS performance as a measure of explicit memory

Bachevalier and Mishkin’s (1984) original conclusion regarding the develop-

mental dissociation of two memory systems was based exclusively on mon-
keys’ performance on two tasks — 24-hour CD and DNMS. Subsequent
research that has used another recognition memory procedure has challenged
the view that explicit memory is a late-developing system. The visual paired-
comparison (VPC) task was originally developed for use with human infants
(see Chapter 6). In this task, participants are familiarized with a given stimulus
for a brief period of time. Following a delay, they are simultaneously pre-
sented with two stimuli — the familiar one and a novel one, and their visual
behavior toward both is recorded. If subjects spend proportionally more time
looking at the novel stimulus during the test, then the researcher infers that
they recognized the familiar one (Fagan 1970, 1973).
Gunderson and her colleagues were the first to use the visual paired-
comparison task with nonhuman primates (Gunderson & Sackett 1984;
Gunderson & Swartz 1985, 1986). In the first study of this kind, infant pigtailed
macaques were tested using a VPC procedure similar to that used with human
infants (Gunderson & Sackett 1984). During familiarization, monkeys were
exposed to a black-and-white patterned stimulus for 60 s. Following a 30-s
delay, infants were tested simultaneously with the familiar stimulus and a
novel one. Each infant received five familiarization and test trials. Infants who
were 4 weeks old (middle) or older (old) at the time of testing exhibited a
significant novelty preference, but infants who were younger (young) did not
(see Figure 5.6). Subsequent research has shown that infants as young as 6
weeks of age can exhibit a novelty preference after a 30-s delay after as little as
5 s of familiarization time; infants of the same age can exhibit a novelty
preference after a 24-hour delay after as little as 45 s of familiarization time
(Gunderson & Swartz 1986).
Bachevalier (1990) has also used the VPC task to study the development
of visual recognition memory in infant rhesus monkeys. In her experiment,
infants were familiarized and tested with three-dimensional objects. During
the familiarization phase of each trial, the infant was shown a pair of identical
objects for 30 s. Following a 10-s delay, the familiar object and a novel one
were presented together during a 10-s paired-comparison test. After an inter-
trial interval of 20 s, the infant was familiarized with another object, and so
forth, for a total of 10 trials. The amount of time that infants fixated the

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92 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 5.6. Mean percent fixation time to the novel test stimulus in younger (Young: 1 to 2
weeks old), intermediate-aged (Middle: 4 weeks old), and older (Old: 13 weeks old) infant
pigtailed macaques tested in a visual paired-comparison task (redrawn from Gunderson and
Sackett 1984).

familiar and the novel objects during the test was recorded.
The novelty-preference scores (percent time spent looking at the novel
stimulus) obtained by Bachevalier (1990) are shown in Figure 5.7 as a func-
tion of age and gender. Clearly, novelty preference increased as a function of
age. Although 5-day-old monkeys did not exhibit a reliable preference for the
novel stimulus during the test, 30-day-old monkeys did. Furthermore, 15-day-
old females — but not 15-day-old males — also exhibited a preference for the
novel stimulus during the test.

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% Looking to Novel Stimulus MEMORY DEVELOPMENT IN NONHUMAN PRIMATES 93

Figure 5.7. Mean percent fixation time to the novel test stimulus by rhesus monkeys tested
in a visual paired-comparison (VPC) task as a function of age and gender (redrawn from
Bachevalier 1990).

The developmental time course for visual recognition memory as as-

sessed by the VPC task stands in stark contrast to the developmental time
course for visual recognition memory as assessed by the DNMS task and
originally reported by Bachevalier and Mishkin (1984). It is important to bear
in mind that the VPC task is conceptually identical to the DNMS task. In both
tasks, subjects are initially exposed to a single stimulus and then select the
novel stimulus during the test phase. The two tasks differ only in the test
phase: In the DNMS task, the subject reaches for the novel stimulus, whereas
in the VPC task, the subject looks at the novel stimulus. In addition to their

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94 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

procedural similarity, the underlying neural mechanisms that are required to

solve both tasks are similar. Lesions of the medial temporal lobe, for example,
disrupt memory performance on the VPC task (Bachevalier, Brickson &
Hagger 1993), just as they disrupt memory performance on the DNMS task
(Bachevalier 1992).
Because the VPC and DNMS tasks are so similar, the findings obtained
by Gunderson (Gunderson & Sackett 1984; Gunderson & Swartz 1985, 1986)
and Bachevalier (1990) challenge the proposal that recognition memory (i.e.,
explicit memory) does not emerge in nonhuman primates until 4 months of age
(Bachevalier & Mishkin 1984). Obviously, the ability of nonhuman primates
to remember a stimulus even after a 24-hour delay is present substantially
earlier than is predicted by findings obtained using standard DNMS proce-
dures (see also Bachevalier et al. 1993). Researchers now recognize that some
ability other than the development of explicit memory contributes to the
relatively late emergence of DNMS performance (Diamond 1990a, 1995;
Diamond, Churchland, Cruess & Kirkham 1999).
At least one possible explanation for the discrepancy in performance on
tasks of VPC and DNMS is that an inability to inhibit a previously rewarded
response contributes to young infants’ persistent failure on the task. Recall that
in the DNMS procedure, subjects are reinforced for displacing the sample
stimulus during the first phase of the experiment, but they are reinforced for
displacing the other stimulus during the test. Thus, within the same trial,
responding to the sample stimulus is correct in one phase but is incorrect in the
other. The recent finding that lesions of the frontal lobe impair performance on
the DNMS task in adult monkeys provides some support for the conclusion that
inhibition is required for success on the DNMS task (Malkova, Bachevalier,
Webster & Mishkin, in press). Furthermore, recent studies with human infants
have shown that if infants are not reinforced for displacing the sample stimulus
during the initial phase of the trial, then they can succeed on the DNMS task at
the same early age as they succeed on the VPC task (Diamond 1995; see
Chapter 6).
In conclusion, despite the seductive nature of Bachevalier and Mishkin’s
(1984) original findings, it is now clear that age-related changes in perfor-
mance on the DNMS task are due in large part to processes other than
memory. As such, the emergence of DNMS performance during development
should not be used as a yardstick for the emergence of a fundamentally
different memory system.

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MEMORY DEVELOPMENT IN NONHUMAN PRIMATES 95

The developmental dissociation revisited

Bachevalier and Mishkin’s (1984) seminal paper set the stage for more than a
decade of research on the developmental dissociation of memory systems.
More recent research has challenged both the underlying neural mechanism
thought to be responsible for their findings as well as the notion of the
developmental dissociation per se. In fact, Bachevalier and Mishkin’s original
data foreshadowed questions regarding a developmental dissociation between
memory systems.
Consider first the original Bachevalier and Mishkin (1984) finding that
younger animals were not impaired relative to older animals in the acquisition
of a 24-hour CD task. Recall that the monkeys were actually trained in
succession on two 24-hour CD tasks, each using a different set of stimuli (set
A, set B). Although there was no age-related difference in the speed with
which the monkeys learned set B, younger monkeys learned set A more
slowly. This procedure may have contributed to early success on the CD task.
With this in mind, it is possible that had the younger animals also been given a
second exposure to the DNMS task (with new stimuli), they might have
learned the second task as quickly as adult monkeys.
In addition, although the older monkeys clearly learned the DNMS task
faster than the younger monkeys (see Figure 5.2), it is important to keep in
mind that even the youngest monkeys eventually learned the DNMS task to
the same 90% level of performance. Although the authors argue that the
infants were not able to learn the task until they were at least 4 months old,
even at 3 months of age, infants performed above chance and showed a steady
improvement in performance across their first month of training. Furthermore,
although the younger animals required more trials than older animals to
relearn the DNMS task after a 15-day retention interval (see Figure 5.3), even
the youngest animals exhibited substantial savings. Finally, although perfor-
mance by the infants was inferior to that of the 3-year-olds when the delay
between the sample and the test was increased, even the youngest animals
were approximately 90% correct when tested after a 120-s delay (see Fig-
ure 5.4). Taken together, these findings demonstrate that although infants’
performance on the DNMS task was statistically poorer than that of adults, by
all accounts, they still performed remarkably well.

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96 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Conclusions

The hypothesis that two or more memory systems develop independently and
at different rates in nonhuman primates is no longer tenable. When monkeys
were tested on the VPC task, for example, they exhibited long-term (i.e., 24-
hour) recognition memory as early as 1 month of age — well before they could
even be tested in either the CD task or the DNMS task. Although monkeys
clearly master some tasks earlier in life than others, these differential rates of
mastery do not reflect the emergence of different memory systems, but the
emergence of different processes other than memory that are required to
perform the tasks. Although successful performance on the 24-hour CD and
DNMS tasks requires the same degree of perception, attention, and motivation
as well as the same target response (i.e., reaching), the two tasks differ on a
number of other dimensions that may contribute to infants’ differential rate of
success on them. One process that is likely to contribute to the protracted
development of DNMS performance is inhibition. When infants are not
required to inhibit responding to a previously rewarded object (as, for ex-
ample, in the VPC task), visual recognition (explicit) memory emerges very
early in development.
Perhaps the best test of the hypothesis that age-related changes in inhibi-
tion rather than in memory underlie the late emergence of successful perfor-
mance on the DNMS task would be to compare performance on the DNMS
task with performance on the delayed-matching-to-sample (DMS) task. In the
DMS task, monkeys are rewarded for choosing the test stimulus that is the
same as the sample stimulus. In other respects, however, the DMS task is
identical to the DNMS task with the exception that monkeys are not required
to inhibit responding to a previously rewarded stimulus. If inhibition is the
basis for the late emergence of successful DNMS performance, then monkeys
should succeed on the DMS task considerably earlier than on the DNMS task.
We are currently exploring this possibility.

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CHAPTER 6

Development of Implicit and Explicit

Memory in Human Infants

In this chapter, we review some of the experimental procedures that have been used to study
memory in human infants. We then outline the classic claims that have been made regarding
the similarity of memory in human infants and adult amnesics and consider the challenges
that recent data have presented for these claims. Finally, we evaluate the adequacy of the
analogy between infants and amnesics by discussing the problems associated with inferring
conscious recollection on the part of preverbal infants.

The view that memory is comprised of two independent and functionally

distinct systems has had a profound influence on theories of infant memory
development. Psychologists from a number of different theoretical persua-
sions have postulated that these two memory systems mature at different rates
during the infancy period (Mandler 1990; McKee & Squire 1993; Naito &
Komatsu 1993; Nelson 1995; Parkin 1989, 1993; Schacter & Moscovitch
1984; Tulving 1983; Tulving & Schacter 1990). Specifically, all claim that
young human infants possess only an implicit memory system prior to ap-
proximately 9 months of age, after which time they gain access to the more
advanced explicit memory system. In this chapter, we evaluate the validity of
this claim.
Not surprisingly, the empirical study of memory in preverbal human
infants has been fraught with both procedural and interpretive problems. As in
studies with rats and monkeys, for example, memory must be inferred from
nonverbal behavior alone. Furthermore, although age differences in task
performance are typically attributed to differences in memory, subsequent
investigation has often revealed that these differences actually reflect age
differences in the task demands, the degree of motor coordination that the
particular version of a task requires, or particular task parameters.

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98 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Memory tasks used with preverbal infants

Below we describe some of the tasks that have been used in studies of memory
with preverbal infants. Our review is selective (for a complete review, see
Rovee-Collier & Hayne, 2000) and focuses on tasks with direct implications
for the development of implicit and explicit memory.

Response-to-novelty tasks

The two classic response-to-novelty tasks that have been used to study infant
visual recognition memory are the paired-comparison task and the habitua-
tion task, which exploit the young infant’s propensity to look at novel stimuli.
Conceptually, both tasks are based on Sokolov’s (1963) model of habituation
of the orienting reflex. In this model, each time a stimulus is encountered, an
internal representation or engram of it is established. Over successive encoun-
ters with the same stimulus, the initial representation is gradually fleshed out
by new information that the subject notices about the stimulus. As the repre-
sentation becomes progressively more complete, subjects attend to the exter-
nal stimulus less and less; once the representation is complete (i.e., no new
information remains to be added to it), then subjects no longer orient to it. As
the representation decays over time (i.e., forgetting), subjects renew orienting
to the extent that the internal representation and the external stimulus no
longer match. In most response-to-novelty studies conducted with human
infants, the primary dependent variable is visual attention. The measure of
retention of a previously encountered visual stimulus is inferred from the
extent to which an infant does not look at it but directs attention elsewhere,
exhibiting a novelty preference.
Paired-Comparison Task. Fagan (1970) was the first to study infant
memory using a novelty-preference procedure, which he adapted from Fantz’s
(1956) original pioneering work on infants’ visual preferences. In this proce-
dure, infants are initially exposed to a particular stimulus for a fixed duration
or until they have accumulated a specified amount of time looking at it.
Immediately afterward, infants are tested with two stimuli presented simulta-
neously for two trials (counterbalancing for the side of the novel stimulus) (see
Figure 6.1). One stimulus is the previously exposed one (i.e., familiar), and
one is novel.

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MEMORY DEVELOPMENT IN HUMAN INFANTS 99

Figure 6.1. The paired-comparison response-to-novelty task with a 6-month-old infant. The
infant was previously shown two identical pictures (e.g., of the woman’s face). Immediately
afterward, the infant received a paired-comparison test, shown here, with the previously
exposed picture (the woman’s face) and a novel one (the man’s face). Proportionally longer
looking at the novel picture — a novelty preference — is taken as evidence that the infant
recognized the preexposed one. (Test photographs courtesy of J.F. Fagan, III.)

The proportion of time that infants spend looking at the novel member of the
test pair is statistically compared with chance (50% of total looking time).
Proportionally longer looking at a novel stimulus than at the preexposed one is
taken as evidence that infants recognize the preexposed stimulus. Some
researchers have argued, however, that proportionally longer looking at the
preexposed stimulus also indicates that infants recognize that stimulus because
a familiarity preference represents nonchance attention (Cohen & Gelber
1975; Colombo & Bundy 1983; Hunter & Ames 1988; Weizmann, Cohen &
Pratt 1971). For infants of all ages, proportionally equivalent looking at the
novel and the preexposed stimulus is taken as evidence of forgetting.
Habituation Task. In the habituation task, a stimulus is repeatedly pre-
sented until infants’ attention to it has declined to some absolute (e.g., McCall,

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100 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Kennedy & Dodds 1977) or relative (e.g., Cohen, DeLoache & Pearl 1977)
level. At this point, some infants are presented with a novel stimulus, whereas
others are again presented with the original one. Greater looking at the novel
stimulus is again taken as evidence that infants remember the preexposed
(habituation) stimulus. As the delay increases between the last habituation
trial and the test with the original stimulus, infants increasingly respond to it.
At some point, the infant’s responding returns to the level that was seen at the
outset of the habituation trials. Because the original stimulus is physically
absent when infants are tested with the novel one, the habituation procedure
incurs a greater memory load than the paired-comparison procedure.
Infants’ response to novelty in paired-comparison and habituation tasks is
usually measured within a single brief session, and the novel stimulus is
presented within seconds of infants’ prior exposure to the other stimulus.
Under these conditions, the task provides a measure of short-term memory.
When familiarization with the preexposed stimulus occurs over multiple daily
sessions (Fagan 1970, 1973) or when testing occurs across sessions that are
separated by days or weeks (Bahrick & Pickens 1995; Bahrick, Hernandez-
Reif & Pickens 1997; Pascalis & DeSchonen 1994), then long-term memory is
implicated.
Long-Term Familiarization Task. Long-term familiarization is procedur-
ally similar to habituation except that infants are preexposed to a stimulus over
a period of 1 or more days before the final test. During the initial preexposure
phase, the experimenter does not record responding and often is not even
present. In a sense, the long-term familiarization procedure provides a degree
of ecological validity to formal laboratory studies in which stimulus exposure
is highly controlled and typically very brief.
Hunt and his colleagues (Hunt 1970; Hunt & Uzgiris 1964; Kaplan 1967;
Uzgiris & Hunt 1970), for example, used a long-term familiarization task with
infants in their classic studies of the development of visual attention. Kaplan,
for example, exposed infants twice daily between 8 and 14 weeks of age to a
nonmoving mobile, a continuously moving mobile, or a mobile that moved in
response to their own activity. Every 2 weeks, she gave them a 4-min paired-
comparison test with the familiar and a novel mobile (both nonmoving) 24
hours after their last exposure. Until infants were 12 weeks old, they showed
no differential fixations to novel and familiar mobiles, when they fixated
novel mobiles longer. However, the type of movement infants saw during
familiarization interacted with stimulus novelty: Infants familiarized with

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MEMORY DEVELOPMENT IN HUMAN INFANTS 101

continuously moving mobiles showed no novelty preference, those familiar-

ized with a nonmoving mobile showed a slight novelty preference, and infants
familiarized with the responsive mobile looked twice as long at the novel
mobile. This result revealed that, after long-term familiarization, young in-
fants could exhibit 24-hour retention.
Newborns can also retain information about speech stimuli to which they
were exposed in utero. DeCasper and Fifer (1980), for example, tested new-
borns in an operant procedure in which high-amplitude sucking on a nonnutri-
tive nipple turned on a tape-recording of either their own mother’s voice or the
voice of another mother. During testing 33 hours after birth, newborns dis-
played an operant preference, sucking more to hear the voice that they had
heard in utero. In another study, pregnant women recited aloud a passage from
a Dr. Seuss book twice daily during their last 6 weeks of pregnancy, and their
newborns were tested approximately 56 hours after birth (DeCasper & Spence
1986). During testing, infants could suck to present either the preexposed
passage or a novel Dr. Seuss passage that was read by either their own mother
or another mother. A control group that was not prenatally exposed to the
target passage could also listen to the mother read both passages. Again, both
prenatally-exposed groups sucked more to hear the familiar Dr. Seuss passage
(the one to which they were exposed in utero) than the novel one, irrespective
of who read it, revealing that speaker familiarity did not account for their
operant preference. In contrast, the control group displayed no operant prefer-
ence. These studies clearly reveal that memories for both the speaker and a
complex pattern of speech sounds can be established in utero and can be
retained for at least 2 days after birth.
Using a long-term familiarization procedure, other investigators have
found that infants can recognize their mother’s face and discriminate it from the
face of another woman within 3 to 4 days after birth (Field, Cohen, Garcia &
Greenberg 1984; Pascalis, DeSchonen, Morton, Deruelle & Fabre-Grenet
1995).

Delayed-nonmatching-to-sample (DNMS) task

The standard DNMS task that has been used with human infants is procedur-
ally identical to the standard DNMS procedure that has been used with
nonhuman primates (see Chapter 3 and 5). Briefly, infants participate in two
kinds of trials. On sample trials, the sample object is placed over a well that

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102 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

contains a reward. After the infant removes the sample and finds the reward, a
screen is lowered between the infant and the sample object. After a delay, the
screen is raised revealing the sample and a novel object. On these test trials,
the reward is always hidden under the novel object. If the infant responds
correctly by displacing the novel object, then he or she is allowed to retrieve
the reward. If the infant responds incorrectly, then the experimenter reveals
the reward under the novel object but does not let the infant have it. Typically,
a new pair of objects is used on every trial (i.e., trial-unique stimuli). The
maximum delay after which an infant responds correctly is the measure of
memory.
Human infants do not succeed on the standard version of the DNMS task
until midway through their second year of life. In most studies, they do not
reliably choose the novel stimulus until approximately 15 to 21 months of age,
even when the delay between the sample trial and the test trial is only 5 to 10 s
(Diamond, Towle & Boyer 1994; Overman, Bachevalier, Turner & Peuster
1992). Even after younger infants have mastered the task at these short delays,
their performance is still disrupted by delays of 30 s and longer.
The prolonged time course for the development of DNMS during the
infancy period is surprising in view of the procedural similarity between this
task and the visual paired-comparison task. In both tasks, the infant is required
to respond to the novel stimulus during the test. Subsequent research has
shown that minor changes in the behavioral requirements of the DNMS task
can dramatically alter its developmental time course (Diamond 1995; Dia-
mond et al. 1999). In the traditional version of the DNMS task, for example,
infants are required to displace the novel test stimulus in order to retrieve a
reward that is placed beneath it. Alternatively, when the infant’s reward is
simply the opportunity to play with the novel test stimulus (i.e., stimulus =
reward), infants solve the task at 6 months of age and perform significantly
above chance after delays as long as 10 min (Diamond 1995). Their perfor-
mance on the modified version of the DNMS task is virtually identical to their
performance on the standard response-to-novelty paired-comparison task.
Similarly, infants’ performance on the task is also enhanced when verbal
praise of the correct choice is used as a reward (Diamond et al. 1999). Taken
together, these findings have led Diamond (1990b, 1995; Diamond et al.
1999) to conclude that some ability other than memory contributes to the
developmental lag in DNMS performance on the standard task.

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MEMORY DEVELOPMENT IN HUMAN INFANTS 103

Object search task (A-not-B)

The A-not-B search task was originally introduced by Piaget (1954) and has
resurfaced as another method for studying memory development in infants
and young children (Diamond 1985; Fox, Kagan & Weiskopf 1979; Gratch &
Landers 1971). In the standard version of the task, the infant is seated between
two identical wells (A, B) where an object can be hidden. The experimenter
shows the infant an object, places it in well A as the infant watches, and
simultaneously covers both wells. After a delay, the infant is permitted to
reach. Infants reaching to the empty well are shown the object in the other well
but are not given it. The experimenter continues to hide the object in well A
until criterion is achieved (e.g., a correct response on two consecutive trials),
at which point the procedure is repeated with the object hidden in well B. After
the hiding well is reversed, infants often continue to search in well A, despite
having watched the experimenter place it in well B. This behavior is called the
A-not-B error.
When infants are tested in this version of the object search task, the
frequency of the A-not-B error increases as a function of delay, and older
infants tolerate increasingly longer delays between hiding and reaching. Dia-
mond (1985), for example, found that infants who were tested cross-section-
ally tolerated delays of 1 to 2 s at 7 months, 5 s at 9 months, and 10 s at 12
months, whereas infants tested longitudinally tolerated slightly longer delays.
Irrespective of the experimental design, however, the delay at which the A-
not-B error occurred increased gradually and continuously at the rate of
approximately 2 s per month.
As in DNMS studies, seemingly minor variations in the task parameters
produce dramatically different estimates of retention (for review, see Diamond
1990a). These variations have included the use of multiple wells (Diamond,
Cruttenden & Niederman 1989) and the substitution of a different object for the
object that infants either saw hidden or heard named (Ramsay & Campos 1978).
Considered in the light of similar findings obtained with the DNMS task, these
results suggest that developmental improvement on object search tasks is due
not only to age-related changes in memory ability but to nonmemorial factors
as well.

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104 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Delayed response task

The delayed response task was introduced by Hunter (1913) as a measure of

“sensory thought” in animals and children. In the original study, Hunter hid a
food reward behind one of three doors. A light over the door signaled the
location of the reward. After the light was turned off, a delay was imposed
before subjects were allowed to respond. The maximum delay tolerated was
50 s (after 507 trials) at 30 months of age and 25 min (after 15 to 46 trials) at 6
to 8 years of age; however, all children initially encountered difficulty after
delays of 4 to 6 s. Subsequently, Hunter (1917) used delays ranging from 3 to
35 s with a child between 13 and 16 months of age who lacked vocal language.
Here, the child watched the experimenter hide an object in one of three hinged
boxes. During the delay, which was timed from when the lid was shut, the
child was distracted. Between 13 and 15 months of age, the child tolerated a
12-s delay; at 16 months, she tolerated a 24-s delay.
The procedures used in the delayed response task and the object search
task, described above, are almost identical. They differ in that the hiding
location is randomly determined across trials in the delayed response task,
whereas hiding at B occurs only after infants have learned to search success-
fully at A in the object search task. Not surprisingly, infants’ performance on
these tasks is also almost identical (Diamond 1990b; Diamond & Doar 1989).
Across ages, the length of the delay that was tolerated in both tasks increased
gradually (see Figure 6.2); within a given age, the maximum delay that was
tolerated in both tasks was the same.
In studies using visual behavior instead of reaching as the dependent
measure, infants have exhibited retention at a younger age and after much
longer delays. In a series of experiments conducted by Baillargeon and her
colleagues (Baillargeon & Graber 1988; Baillargeon, DeVos & Graber 1989),
for example, 8-month-olds were presented with an object at one of two
locations on a portable stage. Identical screens were then placed in front of
each location; behind one screen was the object, and behind the other, there
was nothing. After a 15-s delay, infants watched a hand retrieve the object
either from behind the screen where it had originally been hidden (the possible
event) or from behind the other screen (the impossible event). Infants looked
significantly longer at the impossible event, suggesting that they remembered
the location of the original object and were surprised when they saw it
retrieved from the other location.

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MEMORY DEVELOPMENT IN HUMAN INFANTS 105

Figure 6.2. Developmental progression in the delay that human infants can tolerate in the
delayed response and A-not-B tasks (redrawn from Diamond 1990b).

Even younger infants succeed in reaching versions of the delayed re-

sponse task if they are required to reach for the object directly rather than to
remove a cover to retrieve it. In an experiment with 5-month-olds — the
youngest age at which infants reliably engage in visually-guided reaching —
Hood and Willatts (1986) showed infants an object at one of two locations and
then turned off the lights and removed the object. After the lights were turned
back on, infants reached more to the side where the object had been. Goubet
and Clifton (1998), also using a cover of darkness, similarly found that young
infants could remember an object’s prior location. In their study, a noisy ball
rolled down one of two Plexiglas tubes on either the left or right of midline
before landing silently in a tray, where infants could retrieve it. When tested in
the dark, 6½-month-olds who had previously practiced in the light reaching
directionally reached significantly more to the correct side and corrected their

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106 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

search errors significantly more often than controls who had practiced reach-
ing to midline in the light.

Classical conditioning tasks

Most of the early studies of classical conditioning (Pavlov 1927) with infants
were single-subject studies, and those that tracked an individual’s condition-
ing performance over substantial periods of time provided evidence of long-
term memory. In a hallmark study of this kind, Watson and Rayner (1920)
sounded a loud gong (the unconditioned stimulus, or UCS) which produced
crying and withdrawal (the unconditioned response, or UCR) when an 11-
month-old infant named Albert touched a white rat (the conditioned stimulus,
or CS). This procedure occurred twice. One week later, Albert still withdrew
his hand when tested with the rat (the conditioned response, or CR); in this
session, he also received five more CS-UCS pairings. Five days later, Albert
exhibited CRs when tested with the rat as well as with previously neutral
stimuli that resembled it in some way (a rabbit, a dog, a fur coat, a Santa Claus
mask, and cotton wool) but not to perceptually different stimuli (wooden
blocks). Ten days later, his CR to the rat had become so muted that it was
freshened with another CS-UCS pairing. Also at this time, the UCS was
explicitly paired once each with the rabbit and the dog. One month later,
Albert still exhibited strong CRs to the rat, dog, mask, and fur coat.
In another early study of classical conditioning, Jones (1930) exposed a
7-month-old infant to repeated pairings of a tapping sound (the CS) and an
electrotactual stimulus (the UCS) for five sessions over consecutive days. The
CR, an anticipatory galvanic skin reflex, was established midway through
session 1. Jones found that the infant still exhibited the CR 6 weeks later
despite receiving no additional conditioning trials in the interim. Moreover,
the CR had not completely disappeared 7 weeks after training was over. Later,
Kantrow (1937) reported that an infant less than 10 days old still exhibited a
conditioned leg flexion (CR) to a tone (CS) 18 days after the final conditioning
session.
The most widely studied response in the classical conditioning literature,
irrespective of species or age, is the eyeblink response — a protective reflex.
When the UCS is a corneal air puff, the CR that immediately anticipates the
UCS is also a functional avoidance response. Many of the early failures to
establish a conditioned eyelid reflex in infants undoubtedly resulted from use

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MEMORY DEVELOPMENT IN HUMAN INFANTS 107

of a nonoptimal interstimulus interval (ISI). Little (1970) found that the

optimal interval for eyelid conditioning in newborn infants is three to four
times longer than the 500-ms ISI that is optimal for eyelid conditioning in
studies with human and nonhuman adults (Kimble 1961; Solomon, Pomerleau,
Bennett, James & Morse 1989). Similar evidence that younger organisms
require longer ISIs was also found with nonprimate infants (Caldwell &
Werboff 1962).
The finding that more immature organisms actually require longer ISIs in
order to exhibit classical conditioning is at odds with Schacter and Moscovitch’s
(1984) original conclusion that,
“the absence of a functioning late memory system may create difficulty even
in simple conditioning tasks when reinforcement is delayed or the intertrial
interval is lengthened” (p. 196).

Apparently, the longer ISIs required to produce classical conditioning in

immature subjects reflects an age-related change in synaptic efficacy. Kandel
and Hawkins (1992), for example, found that the 500-ms interval that pro-
motes classical conditioning of the gill-withdrawal reflex in Aplysia is related
to:
“the time during which calcium is elevated in the presynaptic terminal and
binds to calmodulin so as to prime the adenylyl cyclase to produce more
cyclic AMP in response to serotonin” (p. 84).

Their conclusion that cyclic AMP is critically implicated in classical condi-

tioning at the molecular level has been supported by genetic evidence from
fruit flies with single-gene mutations. In these mutants, the genetic defect
impairs both the stimulation of adenylyl cyclase (which is otherwise enriched
in the part of the normal fly brain that is implicated in associative learning) and
their classical conditioning (Kandel & Hawkins 1992).
Little, Lipsitt and Rovee-Collier (1984) demonstrated robust acquisition
and retention of the conditioned eyeblink response in very young infants using
the nonoptimal 500-ms ISI as the control condition and the optimal 1500-ms ISI
as the experimental condition. Infants were trained for a single session at either
10, 20, or 30 days of age with a tone (CS) paired with an air puff (UCS) and were
tested in a second session 10 days later. Only infants in the 1500-ms condition
learned the association, doing so at every age, and infants who were first trained
at 20 and 30 days of age exhibited significant savings (see Figure 6.3). The
percentage of CRs increased with age, and the oldest group attained a higher

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108 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 6.3. Percentage of responses on CS-UCS trials by infants who were initially
conditioned at 10, 20, or 30 days of age (left panels) to blink their eyes to a tone (CS) that
was paired with an air puff (UCS) and were retrained in a second session 10 days later (right
panels). The CS and UCS were separated by either a 1500-ms or 500-ms interstimulus
interval (ISI).

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MEMORY DEVELOPMENT IN HUMAN INFANTS 109

level of conditioning than the youngest group. In addition, infants who were
trained at 20 days of age and tested at 30 days of age performed significantly
better than 30-day-olds being trained for the first time. The finding that infants
exhibited significant retention after 10 days is particularly impressive in view
of the small number of reinforced presentations (50), the small percentage of
reinforced trials (71%), the brevity of the training session (20 min), and the age
at which the youngest infants were trained (10 days).
Solomon, Groccia-Ellison, Levine, Blanchard and Pendlebury (1990)
found that the optimal CS-UCS interval increases during early to late adult-
hood. Whereas young adults conditioned more rapidly with an ISI of 400 ms
than with ISIs of 650 and 900 ms, elderly adults conditioned more slowly with
the 400-ms ISI. Their rate of conditioning was equivalent to that of young
adults who were trained with a 900-ms ISI. Solomon et al. concluded that their
facilitated conditioning at the longest ISI was not a result of age differences in
sensory acuity or motor function but probably reflected age differences in
synaptic efficacy. Taken together, the infant and adult data reveal that the
temporal relationships in classical conditioning are an inverted U-shaped
function of age (see also Chapter 4).
The heart-rate response was successfully conditioned in premature
hydraencephalic and decerebrate infants via a UCS-omission procedure
(Berntson, Tuber, Ronca & Bachman 1983; Tuber, Berntson, Bachman & Allen
1980). Omitting the UCS when it was expected to occur elicited a what-is-it
reflex (Pavlov 1927), which was reflected in the heart-rate CR. The preceding
result is consistent with evidence that amnesics (Warrington & Weiskrantz
1979; Woodruff-Pak 1993), hippocampally-damaged adult animals (O’Keefe
& Nadel 1978), and even Aplysia (Kandel & Hawkins 1992) can be classically
conditioned. Because of such data, many scientists have concluded that all
conditioning tasks — both classical and operant — require only a primitive
memory system, regardless of whether they take a multiple-memory-systems
approach (Mandler 1984, 1998; Schacter & Moscovitch 1984) or a processing
approach (Roediger et al. 1990; Roediger & Srinivas 1993).

Operant conditioning tasks

In operant conditioning, an association is learned between a response and the

outcome it produces. This learning is manifested by the voluntary production
of that response and is measured in terms of an increase in either response rate

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110 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

(number of responses per unit of time) in a free-operant procedure or the

number of correct responses in a discrete-trials procedure. The classification
of operantly conditioned responses, however, is ambiguous with respect to the
type of memory it reflects. In humans, for example, spoken language is a
product of operant conditioning (Skinner 1957). In most of the early studies
that used operant conditioning tasks, infants were trained for multiple ses-
sions. Although designed to study learning, these studies also revealed reten-
tion from one session to the next (e.g., Sameroff 1968; Watson 1984). An
early study of conditioned vocalizations with 3-month-olds is typical
(Rheingold, Gewirtz & Ross 1959). In this study, infants’ baseline vocaliza-
tions to the expressionless experimenter were recorded on days 1 and 2, their
vocalizations were socially reinforced by the experimenter on days 3 and 4,
and the original baseline condition was reinstated on days 5 and 6 (i.e.,
extinction). Infants responded appropriately to all changes in the contingency
and vocalized more on day 4 than on day 3, revealing 24-hour savings.
The majority of operant studies of infant long-term memory, however,
have used the mobile conjugate reinforcement procedure (Rovee & Rovee
1969) with infants between 2 and 6 months of age. During the baseline period
and all retention tests, a mobile is merely hung over the infants from one
suspension bar, and an ankle ribbon is connected to another (see Figure 6.4a).
During the acquisition period, which is interpolated between baseline and
retention testing, infants learn to kick to move a particular mobile via a ribbon
that is strung from one ankle to an overhead suspension hook (see
Figure 6.4b). Typically, they have to meet a learning criterion, which is
responding at 1.5 times their baseline rate. During the long-term retention test,
infants are either exposed to the original training mobile or one that differs in
some way. If they recognize the test mobile, they kick above their baseline
rate; otherwise, they do not. Because the ribbon is not connected to the mobile
during the long-term test, infants’ test performance reflects only what they
remember of their prior training experience and not new learning or savings at
the time of testing.
Because the mobile task is inappropriate for use with infants older than 6
months, a second operant task was developed for infants between 6 and 18
months of age. In this task, infants learn to press a lever to move a miniature
train around a circular track (see Figure 6.5). During the long-term retention
test, the lever is deactivated. Otherwise, all aspects of the two tasks are
identical. Because 6-month-olds exhibit identical memory performance in

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MEMORY DEVELOPMENT IN HUMAN INFANTS 111

Figure 6.4. The mobile task. (a) The experimental arrangement during baseline and the
delayed recognition test. Here, the ankle ribbon is attached to an empty stand while the
mobile is suspended from a second stand. In this arrangement, the infant’s kicks cannot
move the mobile. (b) The experimental arrangement during acquisition. Shown here is a 3-
month-old who is moving the mobile via a ribbon that is strung from his ankle to the same
stand as the mobile.

both tasks (Hartshorn & Rovee-Collier 1997; Hildreth & Rovee-Collier

1999), the train task can be viewed as an upward extension of the mobile task.
The first systematic evidence of 24-hour cued-recall in infants was found
using the mobile task (Rovee & Fagen 1976). In this study, groups of 3-
month-olds were trained for 3 consecutive days with the same mobile. On day
4, the experimental group was presented with a different mobile, whereas the
control group continued to receive the original one. During delayed recogni-
tion tests at the outset of sessions 2 and 3, both groups responded at the same
level at which they had ended the previous day’s session, indicating that they
recognized the mobile after a 24-hour delay. At the outset of session 4,
however, the control group again responded to the original mobile at their
terminal rate of the day before, but infants in the experimental group did not

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112 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 6.5. The train task. Shown here is a 6-month-old pressing the lever below the
Plexiglas window to move the train inside the box during an acquisition phase. During the
delayed recognition test, the lever is deactivated so that lever presses do not move the train.

recognize the novel mobile, failing to respond above their baseline level. Their
behavior was taken as evidence that they discriminated the test mobile as
different from the training mobile they had seen 24 hours earlier.
Subsequent studies using the mobile and train tasks have found that
retention increases linearly between 2 and 18 months of age (Hartshorn, Rovee-
Collier, Gerhardstein, Bhatt, Wondoloski et al. 1998b; see Figure 6.6). When
infants are tested in the mobile conjugate reinforcement paradigm, for example,
2-month-olds exhibit retention for 1 or 2 days, 3-month-olds exhibit retention
for 5 or 6 days, and 6-month-olds exhibit retention for 14 or 15 days. When 6-
month-olds are tested in the operant train task, their maximum retention is
identical to their maximum retention in the mobile conjugate reinforcement
task. Furthermore, as in the mobile task, retention in the train task increases with
age: 6-month-olds exhibit retention for 2 weeks, 9-month-olds exhibit retention
for 6 weeks, 12-month-olds exhibit retention for 8 weeks, 15-month-olds
exhibit retention for 10 weeks, and 18-month-olds exhibit retention for 13
weeks.

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MEMORY DEVELOPMENT IN HUMAN INFANTS 113

Figure 6.6. The maximum duration (in weeks) of delayed recognition of independent
groups of infants who were trained and tested in the mobile task (2 to 6 months of age) and
the train task (6 to 18 months of age). At 6 months of age, infants were trained and tested in
both tasks, and their long-term retention in both tasks was the same. Also shown is the
maximum duration (in weeks) of retention of independent groups of infants who were
tested in the puppet task (6 to 18 months of age). Although the absolute duration of retention
in the operant conditioning and deferred imitation paradigms is different, the pattern of
retention in the two paradigms is identical.

Deferred imitation tasks

Deferred imitation is another task that can be used to study memory during
infancy and early childhood. Simply put, this task incorporates a “monkey see,
monkey do” procedure in which an adult models a behavior, and the infant is
then given the opportunity to imitate it after a delay. Deferred imitation played
an important role in Piaget’s (1962) theory of the emergence of mental
representation during infancy. In tasks that are based on Piaget’s original
conception of deferred imitation, infants do not practice the target behavior(s)
prior to the test. In this way, their memory performance is based exclusively
on a representation of the originally modeled event and not on a memory of
their own prior actions.
According to Piaget (1962), deferred imitation does not emerge until
infants are approximately 18 to 24 months of age. Although a number of

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114 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

studies initially supported Piaget’s developmental time-table (e.g., Abravanel,

Levan-Goldschmidt & Stevenson 1976; McCall, Parke & Kavanaugh 1977),
many lacked essential control groups, making conclusions regarding the first
appearance of deferred imitation uncertain. Meltzoff subsequently challenged
Piaget’s fundamental assumptions and examined deferred imitation under
highly controlled experimental conditions (for review, see Meltzoff 1990). He
demonstrated that 9-month-olds can imitate an experimenter’s unique actions
after a 24-hour delay (Meltzoff 1988) and that 14-month-olds can exhibit
deferred imitation after a 4-month delay (Meltzoff 1995).
For more than a decade, 9 months was considered to be the youngest age
at which infants could exhibit deferred imitation. Recently, however, a num-
ber of studies have reported that infants as young as 6 months can exhibit
deferred imitation after delays of 10 min (Heimann & Nilheim 1999), 24 hours
(Barr, Dowden & Hayne 1996; Collie & Hayne 1999; Hayne, Boniface &
Barr 2000a), and even 14 days (Barr & Vieira 1999). In one of the tasks
commonly used with 6-month-olds, infants watch an experimenter remove a
mitten from a hand-puppet, shake it to ring a bell inside, and replace the

Figure 6.7. The experimental arrangement used with 6- to 24-month-old infants in deferred
imitation studies. Shown here is a 6-month-old removing a mitten from the puppet’s hand
— an action the experimenter had modeled 24 hours earlier.

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MEMORY DEVELOPMENT IN HUMAN INFANTS 115

mitten. The infant’s ability to imitate these target actions is then assessed after
a delay (see Figure 6.7). Six-month-olds can imitate these actions 24 hours
later if the demonstration lasts 60 s but not if it lasts only 30 s (Barr et al.
1996). This latter result suggests that failures to document deferred imitation
by young infants are as likely to reflect the choice of an inappropriate task or
task parameters as the infants’ fundamental inability to imitate what they saw
an adult do earlier.
In a modified version of the deferred imitation procedure, infants are
allowed to practice the target behaviors prior to the retention interval (e.g.,
Bauer, Hertsgaard & Dow 1994). Using this procedure, Bauer and Shore
(1987) reported that 1- to 2-year-olds exhibited retention after 6 weeks.
Infants’ imitation is also influenced by the structure of the target event (Bauer
& Mandler 1989; Bauer & Shore 1987). Without exception, infants’ imitation
of actions that can only be performed in a specific temporal order (causal or
enabling events; e.g., making a rattle by placing a ball in a container, putting a
lid on it, and shaking it) is superior to their imitation of actions that can be
performed in any order (arbitrary events; e.g., dressing a teddy bear by putting
a ring on its finger, a scarf around its neck, and a cap on its head). The finding
occurs even when the enabling and arbitrary events have been matched on the
basis of target actions and event goals (Barr & Hayne 1996) and is identical to
findings with older children (Fivush, Kuebli & Clubb 1992) and adults
(Ratner, Smith & Dion 1986).
The range of behaviors that infants can imitate after a delay expands with
age from facial and body movements (Meltzoff & Moore 1994), to specific
actions on a specific object and then on similar objects (Barr et al. 1996;
Hayne, MacDonald & Barr 1997; Hayne et al. 2000a), to intended actions and
social goals (Meltzoff 1995). This developmental progression is thought to
reflect developmental increases in infants’ motor competence and cognitive
abilities as well as age changes in their social niche.

Memory parallels between infants and amnesics?

Schacter and Moscovitch (1984) were the first to suggest a direct analogy
between the memory performance of infants younger than 9 months of age
and the memory performance of amnesic adults. In their view, infants and
amnesics possess only an early memory system that supports unconscious or

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116 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

implicit memory and lacked the late memory system that supports conscious
recollection or explicit memory. These conclusions were based on the extant
literature on infant memory development.
A closer review of Schacter and Moscovitch’s (1984) arguments, how-
ever, indicates that many of their conclusions were not supported either by the
data that they originally reviewed or by data that have been collected since
their seminal chapter was published. Below we outline four of the parallels
that they drew between the memory performance of amnesics and the memory
performance of human infants younger than 9 months of age. In addition, we
review the evidence for and against each claim.

Effects of retention interval

A number of studies have shown that although adults’ memory performance

on explicit memory tasks such as recognition and recall decreases as a func-
tion of the delay between study and test trials, their performance on implicit
memory tasks such as perceptual identification and word-stem completion
does not. After reviewing infants’ response-to-novelty data, Schacter and
Moscovitch concluded that the forgetting function exhibited by infants in this
task is flat and resembles the forgetting function typically obtained on tests of
implicit memory with adults. Their conclusion was based on the finding that
5-month-olds exhibit little or no forgetting after a 24-hour delay in response-
to-novelty tasks (Fagan 1973). This result, however, is not typical of studies
using this experimental procedure. In general, infants exhibit extremely rapid
forgetting in response-to-novelty tasks, and the amount of forgetting increases
as a function of the delay. Stinson (1971, cited in Werner & Perlmutter 1979),
for example, obtained the first systematic forgetting function using this proce-
dure. In a study with 4-month-olds, he introduced delays of 0, 15, 30, or 75 s
between the final habituation trial and a test trial with the original stimulus and
found that forgetting increased linearly over the delays. After delays longer
than 15 s, infants’ response to the original stimulus was the same as on the first
habituation trial, suggesting that they had forgotten within 15 s — a duration
of retention typical of short-term memory. Other single-session studies using
the paired-comparison task have similarly found retention within the span
typical of short-term memory at 4 months of age (Diamond 1990a). Although
the duration of retention in paired-comparison tasks increases slightly with
age, it rarely exceeds more than a minute or two (e.g., Cohen & Gelber 1975;

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MEMORY DEVELOPMENT IN HUMAN INFANTS 117

Rose 1981). Even when infants exhibit retention across sessions, however,
their memory performance is delay-dependent (Bahrick et al. 1997; Bahrick &
Pickens 1995).

Delayed-nonmatching-to-sample

Schacter and Moscovitch also proposed that infants’ performance on the

DNMS task is analogous to that of amnesic adults. As described in Chapters 3
and 5, performance on the delayed-nonmatching-to-sample (DNMS) task has
been taken as a hallmark of explicit memory. When the delay between the
sample and the test stimulus is more than 15 to 60 s, the memory performance
of human adults with temporal lobe amnesia (Squire, Zola-Morgan & Chen
1984) and nonhuman primates with temporal lobe damage (Mishkin 1978;
Zola-Morgan, Squire & Mishkin 1982) is close to chance. Schacter and
Moscovitch (1984) used the late maturation of DNMS performance in human
infants (Brody 1981) to draw parallels between the memory performance of
infants and amnesics. As described earlier in this chapter, however, human
infants as young as 6 months of age can solve this task even when tested after
a 10-min delay if only minor task modifications are made (Diamond 1995).
Given this result, there is no empirical basis for drawing an analogy between
infants’ and amnesics’ performance on the DNMS task.

A-not-B errors

Schacter and Moscovitch (1984) also cited data from object search tasks to
argue that the performance of infants and amnesics is the same. The data they
cited for amnesics originated in a study with six severely amnesic patients and
six control patients who exhibited mild cognitive deficits but no significant
memory loss and who did not differ from the amnesics in age, education, or
IQ. When tested in an object search task analogous to the traditional tasks that
had been used with infants, the amnesic patients — but not the controls —
committed the A-not-B error. Amnesic patients successfully found the object
when it was hidden at location B if they were tested after no delay, but they
unsuccessfully searched at location A — where the object was previously
found — after a delay.
The corresponding data that were cited for infants came from a study
conducted by Fox et al. (1979). In that study, infants were tested in a standard

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118 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

object search task in which they first learned to search at location A, and then
the object was hidden at location B. Although 8- and 9-month-old infants
searched successfully at B when there was no delay between hiding and
searching, they committed the A-not-B error when there was a 7-s delay. In
contrast, 10-month-old infants successfully searched at B irrespective of
whether the delay was 0 or 7 s. On the basis of these data, Schacter and
Moscovitch (1984) concluded that the search performance of 8- and 9-month-
olds and adult amnesics was analogous.
More recent data, however, have refuted this analogy. Subsequent re-
search using the standard task has shown that the search performance of
infants of all ages declines as the delay between hiding and finding increases
and that the maximum delay that infants will tolerate increases as a function of
age (see Figure 6.2). As such, conclusions regarding the stage-like effect of
age on A-not-B errors from the Fox et al. (1979) study cited by Schacter and
Moscovitch (1984) are limited by the fact that the maximum delay after which
infants were tested was only 7 s. Furthermore, age-related gains in the maxi-
mum delay that infants tolerate increases at a relatively constant rate between
7½ and 12 months of age (Diamond 1985). This latter finding does not support
the view that infants suddenly gain access to the late memory system after 9
months of age. Finally, the finding that infants can solve object search tasks
much earlier in development when looking rather than searching manually
also suggests that their failure on the standard task is due to some process other
than memory (Baillargeon & Graber 1988; Baillargeon et al. 1989).

Recall of specific prior episodes

Under some circumstances, amnesics do learn from prior experience; how-

ever, they are generally unable to recall the specific prior episodes that
contributed to their learning. On the basis of these findings, Schacter and
Moscovitch (1984) attributed the ability to recall specific prior episodes to the
late-maturing system. At the time when their chapter was published, virtually
no data were available from infants that addressed their ability to recall
specific prior episodes from their past experience. Over the past 10 years,
however, infants’ ability to exhibit deferred imitation is often used to argue
that they have the ability to recall a specific prior episode (Bauer & Hertsgaard
1993; Mandler 1988, 1990; McDonough, Mandler, McKee & Squire 1995). In
deferred imitation tasks, the experimenter typically demonstrates the target

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MEMORY DEVELOPMENT IN HUMAN INFANTS 119

actions during a single session, and the infant’s ability to reproduce those
actions is then assessed after a delay. In this task, infants can only respond to
the test stimuli on the basis of their memory for the single demonstration
episode. Given that infants as young as 6 months have been shown to exhibit
deferred imitation, we would conclude that, at least by this age, infants can
recall a single prior episode.
Deferred imitation is not the only task in which infants have exhibited
memory for a single prior episode. Research using the mobile conjugate
reinforcement paradigm has shown that at least by 3 months of age, infants
exhibit retention of an event that occurred on a single prior occasion (Greco et
al. 1990; Hayne, Greco-Vigorito & Rovee-Collier 1993; Rovee-Collier et al.
1993b). In a prototypic study, 3-month-old infants learned to kick to activate a
series of different yellow-block mobiles displaying alphanumeric characters
on each block (see Figure 6.8, bottom) and were subsequently provided with
information that a stained-glass and metal windchime (see Figure 6.8, top)
was movable. This information was provided to the infant during a 3-min
passive-exposure procedure during which the experimenter hung the wind-
chime from the mobile suspension hook and jiggled it while the infant merely
watched. This event occurred on only a single occasion 4 days after training.
When infants were shown the stationary windchime during a delayed recogni-
tion test 1 day later (5 days after training), they kicked vigorously, apparently
attempting to move it by using the response that they had previously used to
move the yellow-block mobiles. The infants kicked, however, only if they had
been provided with information that the windchime could move; infants who
had previously viewed the windchime while it was motionless did not attempt
to move it during the test (Greco et al. 1990; Rovee-Collier et al. 1993b). Also,
because infants had not moved the windchime themselves on that occasion,
they obviously had neither practiced kicking to move it nor been reinforced
for kicking to move it.
In another study demonstrating memory for a single prior episode, 3-
month-olds were trained for three sessions with a series of yellow-block
mobiles (Hayne et al. 1993). During session 3 only, a blue- and red-striped
cloth was draped around the sides of the crib. At the end of session 3, the ankle
ribbon was detached from the overhead suspension hook, the mobile was
removed, and the stationary windchime was suspended over the infant for 3
min in the presence of the blue- and red-striped context. The next day, infants
received a delayed recognition test with the stationary windchime. Even

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120 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 6.8. (Top) The stained-glass and metal butterfly windchime to which 3-month-olds
were briefly exposed on a single occasion. (Bottom) One of the three mobiles with which
infants were initially trained; the blocks on all mobiles were yellow and displayed the same
figure (A or 2) in the same color, but the color of the figures differed from one mobile to the
next.

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MEMORY DEVELOPMENT IN HUMAN INFANTS 121

though the blue- and red-striped context was not present during the test,
infants kicked robustly, apparently trying to move the windchime — even
though they had never before seen it move. A control group was treated
exactly like the experimental group except that the distinctive blue- and red-
striped cloth was not present either during their third session or when they saw
the stationary windchime immediately afterward. This group did not kick
during the delayed recognition test. These data indicated that the shared
session-3 context had linked the representation of the windchime with the
representation of the training event. This study offers unambiguous evidence
that the delayed recognition performance of the experimental group during the
24-hour test resulted from the retrieval of their memory for a single prior
episode — session 3. Moreover, although the training event and the stationary
windchime had been integrated by means of the common context, like a
catalyst, that context was unnecessary for infants’ subsequent test perfor-
mance once the integration had occurred.
Unfortunately, many researchers have summarily dismissed infants’
memory performance in the mobile conjugate reinforcement task without
understanding how the task has actually been exploited to study infants’
memory abilities (e.g., Nelson 1995; Mandler 1998; Schacter & Moscovitch
1984). Because the initial response in this procedure is established by condi-
tioning, for example, they think that studies using this procedure tap only
implicit memory that is acquired gradually or incrementally through rein-
forced practice (e.g., Bauer 1995, 1997; Bauer & Hertsgaard 1993; Mandler
1984, 1990, 1998; Schacter & Moscovitch 1984).
On the contrary, the experimental procedures described above are re-
markably similar to the procedures commonly used in deferred imitation tasks
— tasks that these same individuals argue tap explicit memory (Bauer 1995,
1997; Bauer & Hertsgaard 1993; Mandler 1984, 1990; Nelson 1995, see
below). As in deferred imitation, for example, the target action and its conse-
quence were not physically present at the time of the delayed recognition test
with the windchime in the mobile task. Also, in both the deferred imitation and
mobile tasks, the experimenter provides the subject with a prop (e.g., a
mobile) in lieu of instructions, thereby creating an occasion for cued recall, but
the specific action to be performed is not externally cued. Finally, as in studies
of deferred imitation, infants acquired information about the windchime
through observation alone; during the test, infants merely applied an action
that was already in their behavioral repertoire upon the test object in order to

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122 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

make it function as they had learned it could — even though perceptual

information about its function was not available at the time of testing.

The analogy revisited

Although the analogy between infants and amnesics originally put forward by
Schacter and Moscovitch has not withstood empirical scrutiny, their argument
has been reiterated by others who still contend that the memory processing by
infants and amnesics is the same. In fact, the current strategy used by these
investigators resembles that of Schacter and Moscovitch (1984) in fundamen-
tal ways. Consistent with Schacter and Moscovitch, a common approach to
infant memory development has been to find tasks that amnesics fail and
then determine whether or not infants fail the same tasks (Mandler 1990;
McDonough et al. 1995; McKee & Squire 1993). Although the outcome of
this process is often used to support the analogy between infants and amnesics,
recent empirical work in at least two new domains — deferred imitation and
response-to-novelty tasks — indicates that no such analogy exists.

Deferred imitation tasks

Adult amnesics have recently been shown to fail on two other nonverbal tasks
that are typically used with infants — deferred imitation and response-to-
novelty tasks (McDonough et al. 1995; McKee & Squire 1993). McDonough
et al. (1995), for example, found that human adults with amnesia did not
exhibit retention in a deferred imitation task when tested after a 24-hour delay.
In their study, an experimenter demonstrated a series of three-step actions with
objects. Healthy adults, patients with frontal-lobe damage, and patients with
amnesia were then given the opportunity to reproduce those actions 24 hours
later. Although healthy adults and patients with frontal lobe damage repro-
duced more of the actions during the test than they had prior to the demonstra-
tion (i.e., during baseline), patients with amnesia did not.
Although imitation, like DNMS, has traditionally been viewed as a
relatively late developmental milestone (McCall et al. 1977; Piaget 1962;
Uzgiris 1981), more recent research has shown that at some point during the first
year of life, infants are able to exhibit imitation even when tested for the first
time after a delay (i.e., deferred imitation). In the first experiment of this kind,

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MEMORY DEVELOPMENT IN HUMAN INFANTS 123

Meltzoff (1988) demonstrated deferred imitation by 9-month-old infants who

were tested after a 24-hour delay. Consistent with Schacter and Moscovitch’s
(1984) original view, Meltzoff’s (1988) finding is often cited as new evidence
in support of a transition in memory processing at around 9 months (Mandler
1990; Nelson 1995, 1997). The subsequent finding that infants as young as 6
months can imitate a wide range of novel behaviors after a delay (Barr et al.
1996; Barr & Vieira 1999; Collie & Hayne 1999; Hayne et al. 2000a; Heimann
& Nilheim 1999), however, clearly demonstrates that infants less than 9 months
of age can solve a memory task that human adults with amnesia fail.

Response-to-novelty tasks

Although Schacter and Moscovitch (1984) originally argued that response-to-

novelty tasks tap the early (implicit) memory system, some investigators have
argued more recently that this task taps explicit memory. First, given the
procedural similarity between the response-to-novelty tasks and DNMS tasks
described earlier, it has become increasingly difficult to argue that one task taps
explicit memory while the other does not (Bachevalier, Brickson & Hagger
1993; Diamond 1995). McKee and Squire (1993), for example, found that
human adults with amnesia show extremely rapid forgetting when tested on
response-to-novelty tasks. In their study, amnesic patients and healthy controls
were tested using a visual paired-comparison procedure. Although the novelty
preference of the two groups did not differ immediately after familiarization, the
novelty preference of the amnesic group was significantly lower than that of the
control group when subjects were tested after a 2-min delay.
Even during the first few days of life, however, human infants exhibit
robust recognition memory in a response-to-novelty task like that used by
McKee and Squire (1993) to discriminate the memory performance of amne-
sics from that of healthy controls (Field et al. 1984; Pascalis & DeSchonen
1994; Pascalis et al. 1995). In a study that was actually motivated by the
McKee and Squire finding, Pascalis and DeSchonen (1994) familiarized 3- to
4-day-old infants with a picture of a woman’s face using an infant-controlled
habituation procedure. Independent groups of infants were then given a
paired-comparison test with the familiar picture and a picture of a previously
unseen woman either 2 min or 24 hours later. After both delays, infants looked
proportionally longer at the novel picture. Thus, even newborn infants exhibit
retention under conditions that human amnesics do not.

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124 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Do infants have conscious awareness?

Explicit memory is often distinguished from implicit memory in that explicit

memory is thought to require conscious recollection, whereas implicit memory
is not. That the memory performance of amnesics is selectively impaired in
certain memory tasks is indisputable; however, current evidence disputes the
claim that amnesics’ memory performance parallels the memory performance
of developing infants on equivalent tasks. Our review of the empirical literature
on infant memory has shown that very young infants succeed in tasks that
amnesics often fail. Given this, are we willing to conclude that infants, unlike
amnesics, experience conscious recollection of their past? On a more funda-
mental level, are we willing to conclude that the same processes that mediate
adults’ performance also mediate infants’ performance on the same tasks?
Some researchers have argued that inferences can be made regarding the
conscious and unconscious processes that underlie infants’ success or failure
on a particular memory task. Mandler (1990), for example, claimed that
because verbally competent subjects solve deferred imitation by recall —
which she thinks requires conscious recollection, then deferred imitation by
nonverbal infants must require conscious awareness as well. Although Bauer
(1996) recognized the interpretative difficulty that an exclusive reliance on
nonverbal behavior imposed, she also used that behavior as a surrogate
measure of consciousness:
“Recall is, by definition, a conscious product. When an adult provides a
verbal report of a past experience, there is ample evidence that the remem-
bered material has been made accessible to the conscious mind. Because the
participants of research on memory for experiences early in life are preverbal
or barely verbal, we are unable to query them to ensure their awareness that
their behaviors result from some previous experience. There is ambiguity,
then, as to whether the basis on which we infer memory, namely, a change
in nonverbal behavior, results from conscious recollection or unconscious
influence….What is needed…is a nonverbal task analogous to verbal recall:
The mnemonic behavior must be derived from a task that engages the same
cognitive processes as those involved in verbal recall by older children and
adults…an excellent candidate is elicited imitation of specific action se-
quences” (pp. 30–31).

Bauer’s conclusion is shared by others in the field. According to McDonough,

for example:

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MEMORY DEVELOPMENT IN HUMAN INFANTS 125

“successful deferred imitation relies on brain structures essential for declara-

tive memory, the capacity for intentionally calling to mind specific facts and
events” (quoted in Bower 1995, p. 86).

This conclusion, however, has been vigorously challenged. Thompson

(1990a), Fagan (1990), and Werker (1990), to name a few, have pointed out
that nothing in the behavior of preverbal infants performing a deferred imita-
tion task provides direct evidence of conscious awareness — or intentionality,
for that matter, nor can there be. The conclusion that infants use conscious
recollection in tasks of deferred imitation is only inferred from the assumption
that there is a one-to-one mapping of a particular task onto a particular
memory system — an assumption that Jacoby (1991) characterized as “more
than a little shaky.” Tulving (1990) noted that:
“memory should have something to do with remembering and remembering
is a conscious experience. To remember an event means to be consciously
aware now of something that happened on an earlier occasion” (p. 1).

He warned, however, that because conscious experience and performance on

an explicit memory test are not necessarily related, conscious recollection
cannot be inferred from such behavior. Finally, Jacoby and Witherspoon
(1982) demonstrated that remembering without awareness can accompany
adults’ memory for a specific prior episode. As in studies with rats and
monkeys, whether preverbal infants ever experience conscious recollection of
their prior experiences is impossible to determine, regardless of what experi-
mental tasks are used to test their memory.
Although we will never know if and how infants re-experience their own
personal past, we can gain some critical understanding of the principles that
describe their memory processing by comparing the effect of various experi-
mental manipulations on their performance on priming (implicit) and recogni-
tion (explicit) memory tasks. This analysis is the focus of Chapter 7.

Conclusions

The assumption that the Jacksonian principle extends to the normal develop-
ment and dissolution of memory systems is intuitively appealing, but evidence
on the development of memory in human infants and its dissolution in amne-
sics has not supported this assumption. This result is hardly surprising given

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126 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

that the demise of memory function in adults with severe brain damage does
not even parallel the loss of memory function in healthy, aging adults
(Campbell et al. 1984). In fact, brain-damaged adults do not even provide a
suitable model for understanding many developmental disorders (Karmiloff-
Smith 1998).
The empirical evidence reviewed in this chapter provides no basis for the
analogy between the development of memory in infants and the dissolution of
memory in amnesic adults. First, across experimental tasks, even very young
infants exhibit retention in tasks that adult amnesics do not (see Table 6.1).
Second, age-related changes in infants’ performance within a given task give
no hint of the stage-like transition in memory performance that would be
expected if a fundamentally different memory system, such as the one that is
subsequently lost in amnesia, were to emerge de novo at some point during
development (see Figure 6.2 and Figure 6.6). Third, the memory of preverbal
infants differs in a number of other ways from the memory of adult amnesics.
Not only have infants yet to develop language, for example, but also they have
yet to develop the vast networks of associations that adult amnesics acquired
over a lifetime. Finally, the poor memory that is exhibited by developing
organisms is not a pathological condition, whereas the poor memory that is
exhibited by brain-damaged amnesics clearly is (Campbell et al. 1984). Given
the preceding considerations, the fact that some scientists still take the decline
in memory performance during amnesia as evidence of how memory normally
develops is surprising.

Table 6.1 . The Success of Adults and Human Infants < 9 Months of Age on the DNMS,
Deferred Imitation, and Novelty-Preference Tasks
Group Memory Task
DNMS Deferred Imitation Novelty Preference
Adult Amnesics No No No
Infants < 9 months Yes Yes Yes

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CHAPTER 7

Memory Dissociations In Infants

The ontogenetic hierarchy in which implicit memory develops before explicit memory was
originally inferred from the excellent memory performance of amnesic adults on priming
tests and their poor memory performance on recall/recognition tests. Similar functional
memory dissociations have been produced in normal adults by means of different test
instructions. This chapter reviews evidence that very young infants exhibit memory disso-
ciations exactly like those exhibited by normal adults on priming and recognition tests, and
they do so in response to manipulations of all of the same independent variables.

Recall that infants and amnesics were commonly assumed to possess only
implicit memory. To determine when explicit memory develops, therefore,
some researchers attempted to find tasks that amnesics fail, but normal adults
can solve. Once such a task was found, they then asked at what age preverbal
infants could first solve them. Studies in which researchers took this approach
were discussed in Chapter 6. A second approach to the development of
explicit memory, however, is to ask at what age infants exhibit the same
functional memory dissociations as adults. Studies that have addressed this
question are the focus of Chapter 7.

Memory dissociations in adults

Teuber (1955) was the first to propose the idea of a double dissociation in
memory performance. Tulving (1983) described the rule of experimental
dissociation as follows:
“Dissociation is said to have occurred if it is found that the manipulated
variable affects subjects’ performance in one of two tasks, but not in the other,
or affects the performance in different directions in the two tasks. Thus,

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128 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

dissociation refers to the absence of a positive association between dependent

variables of two different tasks” (p. 73).

He suggested applying an analogous logic to studies of developmental or

pathological dissociations by comparing the performance of groups differing
in either age or pathology on two different memory tasks.
Warrington and Weiskrantz (1970), for example, reported a memory
dissociation between two patient groups that differed in pathology. Brain-
damaged amnesics and a control group of patients without brain damage were
administered free-recall and recognition tests and two priming tests — word-
fragment completion involving degraded letters and stem-completion tests.
Amnesics’ retention on the first two tests was impaired, but their performance
on the priming tests was not. Today, these tests are referred to as explicit and
implicit memory tests, respectively. Since then, many researchers using a
variety of explicit and implicit tests (see Chapter 2) have obtained similar
results, namely, impaired memory performance on explicit tests but spared
memory on implicit tests (Jacoby & Witherspoon 1982; Moscovitch 1982;
Shimamura 1986; Shimamura & Squire 1984). Crowder (1988) interpreted
these findings as an indication that amnesics are capable of initially encoding
information but have difficulty in subsequently gaining awareness of it.
Mandler (1989) similarly interpreted them as reflecting the inability of amne-
sic patients “to use access routes to information that is not available automati-
cally” (p. 96). Others, however, interpreted the dissociations as reflecting the
fact that implicit and explicit tests tapped functionally different memory
systems, and memory dissociations on implicit and explicit tests have now
become a common diagnostic for the existence of two memory systems.
Memory dissociations like those found in studies with amnesics were
subsequently documented in studies with normal adults. In these studies,
adults were instructed to respond on an implicit test with the first word that
came to mind, making no reference to a prior episode, or to respond on an
explicit test with an item from a previously studied list or on the basis of a
specific prior episode (Graf et al. 1982; Graf & Schacter 1985; Schacter et al.
1989; see Chapter 2). In addition, researchers have found that adults perform
differently on implicit and explicit tests as a function of a number of different
independent variables (Hintzman 1990; Jacoby & Dallas 1981; for reviews,
see Richardson-Klavehn & Bjork 1988; Schacter 1987). In every instance, the
manipulated variable produces a functional dissociation that mimics the im-
pact of amnesia on implicit and explicit tests, impairing memory performance

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MEMORY DISSOCIATIONS IN INFANTS 129

on explicit tests but having little or no impact on memory performance on

implicit tests.

Memory dissociations in preverbal infants

Tulving’s (1983) original suggestion of applying the logic of experimental

dissociation to groups differing in age on two different memory tasks has been
followed in studies with children on tasks like those used with adults (see
Chapter 4). The tasks that were used with children and adults, however, are
inappropriate for preverbal infants. To apply the logic of experimental disso-
ciation to infants, therefore, it is necessary to incorporate their instructions
directly into the structure of the tasks. In addition, because different indepen-
dent variables affect adults’ memory performance on implicit and explicit
tests differently, we have manipulated these same variables to see if they
produced corresponding dissociations in infants’ memory performance on the
two kinds of tasks.

Tasks that produce infant memory dissociations

Two general types of task produce dissociations in infants’ memory perfor-

mance — delayed recognition tasks and reactivation (priming) tasks. These
tasks are not specific to a particular paradigm; rather, both have been used
with a variety of infant memory procedures, including response-to-novelty
(Cornell 1979), operant conditioning (Hartshorn & Rovee-Collier 1997;
Rovee-Collier, Sullivan, Enright, Lucas & Fagen 1980), deferred imitation
(Barr 1997; Barr & Vieira 1999), auditory localization (Perris, Myers &
Clifton 1990), and reenactment (Sheffield & Hudson 1994). In addition, both
tasks are introduced after the initial study or training period (e.g., familiariza-
tion, conditioning, modeling) is over. Because the original memory is encoded
before the manipulations that differentiate the two tasks are introduced, differ-
ences in infants’ memory performance on them cannot be attributed to how the
response got into their behavioral repertoire in the first place. This condition
satisfies the retrieval intentionality criterion (Schacter et al. 1989).
Delayed Recognition Task. In this task, the infant is exposed to a retrieval
cue during a long-term retention test that is administered after a specified
amount of time has elapsed since training or modeling (see Figure 7.1a). This

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130 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

is a contemporaneous-cuing procedure (Spear 1978). During the test, infants

are simply shown the study or training cue (a particular mobile, train, or other
prop) and indicate if they recognize it by producing the appropriate response
(kicking, lever-pressing, or other target action). If they do not recognize it,
then they respond at chance (i.e., at the baseline level).
By testing with different types of retrieval cues as memory probes after
different delays, it is possible to ascertain what is still accessible in the original
memory representation at different points in time (e.g., the details or general
features of the training mobile, the immediate and remote context) and what is
not. If infants fail to recognize the altered test stimulus, then we conclude that
the details that were altered or absent at the time of testing must have been
represented in the training memory and are critical for its retrieval. If infants
respond to the altered test stimulus, however, then we conclude that the details
that were altered or removed were either not represented in the original
training memory or were forgotten by the time of testing. This strategy was

Figure 7.1. (A) Schematic of the delayed recognition task showing training and the long-
term retention test (i.e., the delayed recognition test). (B) Schematic of the reactivation task,
showing training, the reactivation treatment, and the long-term retention test. The only
difference between these tasks is the brief reactivation (priming) treatment prior to the long-
term retention test. The memory probe in (A) serves as the reactivation stimulus or memory
prime in (B); the long-term retention test is usually with the original training stimulus.

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MEMORY DISSOCIATIONS IN INFANTS 131

previously used by Tulving (1983) in studies of explicit memory with adults

and has revealed that infants forget different kinds of memory attributes at
different rates (Bhatt & Rovee-Collier 1994, 1996; Boller, Rovee-Collier,
Gulya & Prete 1996; Hitchcock & Rovee-Collier 1996; Rovee-Collier &
Sullivan 1980).
Reactivation Task. The reactivation task is based on the observation that
many memories which have been forgotten (i.e., there is no evidence of
retention in performance on a long-term retention test) can subsequently be re-
activated. Apparently, these memories still remain available in long-term
memory even after they are no longer accessible to retrieval cues that are
presented at the time of the long-term retention test — a distinction originally
made by Tulving (Tulving 1972; Tulving & Pearlstone 1966). During a
reactivation treatment, infants are briefly exposed to a memory prime at some
point before the long-term retention test (see Figure 7.1B). This is a prior-
cuing procedure (Spear 1978). The prime presumably reactivates the latent
memory, increasing its accessibility. Whether the prime was effective (i.e.,
whether the memory was actually reactivated) is then assessed later on a
standard delayed recognition test. If the prime was effective, then infants
respond appropriately to the retrieval cue just as they had at the end of
training. The memory prime is a fractional component of the original event —
as are word stems or word fragments in studies with adults — that is likely to
be represented in the training memory. In most studies, the prime is presented
at a time when infants cannot recognize it — a practice that mimics the
amnesic test condition. (The effect on retention of presenting a prime when
infants can still recognize it is discussed in Chapter 9, Priming and the State of
the Memory.)
Although reactivation was originally used with infant animals (Spear &
Parsons 1976), it was subsequently adapted for preverbal infants (Fagen &
Rovee-Collier 1983; Rovee-Collier et al. 1980; Sullivan 1982) and has since
been used with toddlers who possess some facility with language (Barr 1997;
Sheffield & Hudson 1994). Memory primes that have been used with young
infants include stimuli as diverse as a previously familiarized photograph (see
Figure 7.2a) in response-to-novelty studies (Cornell 1979), the mobile (see
Figure 7.2b) or distinctive training context (see Figure 7.2c) in operant condi-
tioning studies (Rovee-Collier & Hayne 1987), and the hand-puppet (see
Figure 7.2d) in deferred imitation studies (Barr 1997). As a memory prime for
14- and 18-month-olds, a demonstration of three of six activities in which

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132 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

(A) (B)

(C)

(D)

Figure 7.2. Stimuli that have served as memory primes for preverbal infants. (A) the
photograph that 5-month-olds had viewed during the familiarization phase of a response-to-
novelty task (photograph courtesy of J.F. Fagan, III.); (B) the mobile that had been used
during operant conditioning with 2-, 3-, and 6-month-olds; (C) the training context that had
been present during mobile conditioning with 3-month-olds; (D) the hand-puppet on which
target actions had been demonstrated to 6-month-olds in the presence of the train (the bell is
pinned on the puppet’s back instead of inside its mitten).

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MEMORY DISSOCIATIONS IN INFANTS 133

toddlers had previously engaged reactivated their memory of remaining three

activities (Sheffield & Hudson 1994). Effective memory primes for 24-month-
olds were a small-scale model of a room in which infants had engaged in the
activities, a photograph of each of the activities, and a video of three of the six
activities (Agayoff, Sheffield & Hudson 1999).
Figure 7.3 presents data illustrating performance in the delayed recogni-
tion and reactivation tasks. Shown at the left is the forgetting function of 3-
month-old infants whose initial training was completed at Time 0. The first
curve depicts the performance of independent groups on delayed recognition
tests that were administered after different posttraining delays. As can be seen,
the original memory was gradually forgotten within 6 to 8 days. Thirteen days
after training, infants were exposed to a memory prime. The curve at the right
is the reforgetting function of the reactivated memory, which was the perfor-
mance of independent groups on standard recognition tests that were adminis-
tered at different points in time after reactivation. The figure shows that the

Figure 7.3. The forgetting and reforgetting functions of the original memory and the
reactivated memory, respectively, as a function of the number of days after training or
priming when retention testing occurred. The memory prime was presented either 13 or 27
days after training was over (priming), when forgetting was complete. Each data point
represents a different group of 3-month-old infants.

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134 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

prime reactivated the memory and restored infants’ retention to the same level
that it was immediately after training. Note also that the reactivated memory
was not transient but was reforgotten at approximately the same rate as the
original memory.
Examples of Delayed Recognition and Reactivation Tasks. The distinc-
tion between the delayed recognition and the reactivation tasks is well-
illustrated in a series of experiments with 3-month-olds in which we asked if
infants are sensitive to the same primitive perceptual units as adults (Rovee-
Collier, Hankins & Bhatt 1992a). These units, called textons (Julesz 1984) or
critical features (Treisman & Gelade 1980), are thought to be the building
blocks of perception. In the delayed recognition task, 3-month-olds failed to
discriminate between a pair of horizontal and vertical bars (two textons) that
were in different spatial relations (L versus T) after 24 hours, but they did
discriminate +s from both Ls and Ts. Presumably, the latter discrimination
occurred because a + contains an additional texton — a line crossing. In the
reactivation task, however, 3-month-olds discriminated between pairs of hori-
zontal and vertical black bars in all combinations. The procedural details of
these two studies are described below.
The delayed recognition task was used in Experiment 1. Here, indepen-
dent groups of infants were trained in their home cribs for 2 days (9 min per
day) with a five-object, pink-block mobile displaying two computer-gener-
ated black bars arranged as an L, T, or + on all sides of each block. The mobile
was suspended from one of two flexible stands that were clamped to opposing
crib rails (in studies with 6-month-olds, infants are situated in a sling seat
inside a playpen, and the mobile is suspended from one of two horizontal bars
on floor microphone stands that are placed on opposite sides of the playpen.)
During training, infants lay supine in their home cribs, and a white satin ribbon
was connected without slack from one ankle to the overhead mobile suspen-
sion bar (see Figure 6.4b). In this arrangement, each footkick moved the
overhead mobile with a rate and intensity proportional to the rate and vigor of
kicking (conjugate reinforcement: Rovee & Rovee 1969).
Each training session began and ended with a 3-min nonreinforcement
period when the ankle ribbon was attached to an empty stand. At the outset of
session 1, this 3-min period was the baseline phase when the infant’s un-
learned kick rate was measured; at the end of session 2, this 3-min period was
an immediate retention test when the infant’s final level of learning and
retention after zero delay were measured. The 3-min long-term retention test

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MEMORY DISSOCIATIONS IN INFANTS 135

was identical to the baseline phase and immediate retention test and occurred
24 hours after training was over. At this time, either the same mobile (i.e., a
mobile displaying Ls for infants who were trained with Ls) or a different one
(i.e., a mobile displaying Ts or +s for infants who were trained with Ls) was
hung over each infant (see Figure 6.4a).
Retention was indexed by two individual measures of relative respond-
ing. The primary measure, the baseline ratio (response rate during the long-
term test divided by the same infant’s baseline rate), indicated the extent to
which test responding exceeded an infant’s pretraining baseline. Thus, if a
group kicked significantly above its pretraining baseline (i.e., M baseline ratio
significantly > 1.00), then this was taken as evidence of retention (if the test
mobile was the same as the training mobile) or generalization (if the test
mobile was different). If a group did not kick significantly above baseline (i.e.,
M baseline ratio not significantly > 1.00), then this was taken as evidence of
no retention or discrimination, respectively. Convergent evidence of no reten-
tion/discrimination was provided by the retention ratio (response rate during
the immediate retention test divided by the same infant’s response rate during
the long-term test). Thus, if a group kicked significantly less during the long-
term test than it had immediately after training (i.e., M retention ratio signifi-
cantly < 1.00), then this was taken as evidence of discrimination (if the test
mobile was different from the training mobile) or forgetting (if, for example,
the training and test mobiles were the same).
In Experiment 1, the no-change control group exhibited excellent reten-
tion on the 24-hour delayed recognition test, as did infants who were trained
with Ls and tested with Ts (or vice versa). Infants who were trained with either
Ls or Ts and were tested with +s (and vice versa), however, failed to respond
above baseline during the 24-hour test, indicating that they discriminated the
test stimulus from the training one.
The reactivation task was used in Experiment 2. Here, independent
groups of infants were tested exactly like the no-change group in Experiment
1 but were allowed 2 weeks to forget the original training memory first.
Twenty-four hours before the long-term test (13 days after training), these
infants were primed for 3 min with either the original training mobile or a
different one (see Figure 7.4). During the reactivation treatment, the end of the
ribbon was not attached to the infant’s ankle but was drawn and released by
the experimenter at the same rate that each infant had kicked during the final 3
min of training. In this way, each infant saw the mobile moving in a way that

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136 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

was phenomenologically equivalent to what that same infant had seen at the
end of acquisition. During a standard delayed recognition test with the original
training mobile 24 hours after the reactivation treatment (14 days after train-
ing), we tested infants’ retention to determine whether or not the prime had
actually reactivated their forgotten memory. We also tested two control
groups that are requisite in studies of reactivation — a reactivation control
group and a forgetting control group. The reactivation control group was not
originally trained but was primed with the training mobile. This group ensured
that the reactivation treatment per se did not induce new learning that might be
misconstrued as retention during the long-term test. The forgetting control
group was originally trained but was not primed. This group ensured that
forgetting was complete by the time of the long-term retention test.

Figure 7.4. The experimental arrangement during the reactivation or priming treatment
with 3-month-olds. The ribbon was not connected to the infant’s ankle but was held by the
experimenter, who pulled it to move the mobile at the same rate that the infant had moved it
by kicking during the last few training minutes. The infant seat minimized spontaneous
kicking during the reactivation treatment.

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MEMORY DISSOCIATIONS IN INFANTS 137

The no-change group, which was primed with the original training mo-
bile, exhibited excellent retention, but the forgetting control group and the
reactivation control group exhibited none. Infants who were trained with Ls
and primed with either Ts or +s also exhibited no retention during the long-
term test. The fact that Ls were not effective primes for infants trained with Ts
and vice versa suggested that infants in Experiment 1 had originally encoded
the difference between Ls and Ts but had forgotten this distinction by the time
of the 24-hour retention test with the other mobile. This suggestion was
subsequently confirmed: Infants who received a delayed recognition test only
1 hour after the end of training discriminated Ls from Ts and vice versa (Adler
& Rovee-Collier 1994).
The preceding experiments illustrate an important distinction between
reactivation and delayed recognition tasks. Recall that in a delayed recogni-
tion task, infants are tested with a stimulus that is either the same as or
different from the training one, whereas in a reactivation task, infants are
reactivated with a stimulus that is either the same as or different from the
training one. In a delayed recognition task, infants may fail to exhibit retention
(i.e., they discriminate) if the test stimulus differs from the training one; in the
reactivation task, however, they fail to exhibit retention because the reactiva-
tion stimulus differs from the training stimulus — not because the reactivation
stimulus differs from the test stimulus. In other words, they exhibit no reten-
tion if their forgotten memory was never reactivated in the first place (Hayne
& Rovee-Collier 1995; for review, see Rovee-Collier & Hayne 1987).

Comparison between infant and adult memory tasks

The delayed recognition and reactivation tasks that have been used with infants
correspond to two of the prototypic tasks that have been used in tests of implicit
and explicit memory with adults. The delayed recognition task is analogous to
the standard yes/no (e.g., Dorfman, Kihlstrom, Cork & Misiaszek 1995) and
old/new recognition tests (e.g., Mitchell & Brown 1988; Musen & Treisman
1990) that have been used in studies of explicit memory with adults. As in the
adult studies, the retrieval cue is presented at the time of the retention test
instead of before it (see Table 7.1). The reactivation task is analogous to
repetition priming tasks that researchers use to study implicit memory with
adults (see Graf & Schacter 1985; Nelson 1995). In studies with infants, the
reactivation stimulus (i.e., the memory prime) is a fractional component of the

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138 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

original event — as is a word stem or word fragment in repetition priming

studies with adults — that is likely to be represented in the infant’s training
memory and is presented immediately before the retention test. Also, the prime
is presented at a time when infants cannot recognize it — a practice that mimics
the amnesic test condition. Despite being unable to recognize the prime, infants
exhibit item-specific priming, as do adults.

Table 7.1. Tasks That Produce Implicit/Explicit Memory Dissociations in Adults and
Corresponding Tasks Used With Infants
Memory System Adult Task Infant Task
Implicit Priming Reactivation
Explicit Recognition Delayed Recognition

In adults, priming is thought to initiate a relatively pure perceptual

identification process that occurs automatically, devoid of an active search
component (Jacoby 1991; Musen & Treisman 1990). According to Vriezen,
Moscovitch and Bellos (1995):
“the mere presentation and processing of an item is sufficient to leave a trace
in the perceptual representation system (Schacter 1990, 1992; Tulving &
Schacter 1990). It is the reactivation [our italics] of this trace on subsequent
presentations that accounts for the repetition priming effect” (p. 944).

These descriptions are equally applicable to infants. The initial perceptual

processing of a stimulus makes the future processing of that stimulus more
rapid (Cave 1997; Mitchell & Brown 1988; Musen & Treisman 1990). Thus,
Reinitz and Alexander (1996) reported that adults’ perceptual identification of
primed (old) and unprimed (new) pictures was perfectly predicted by a multi-
plicative model which assumes that prior exposure to a stimulus increases the
rate at which visual information is subsequently acquired from the primed
stimulus. Cave, Blake and McNamara (1998), however, reported that priming
decreased the naming latencies of old objects on a perceptual identification
task only when the primes were processed during periods of binocular domi-
nance. Primes that were presented during binocular suppression, which pre-
vents their perceptual attributes from reaching the processing stage at which
they are assembled into nameable objects, did not facilitate adults’ subsequent
naming. On the basis of these data, Cave et al. concluded that successful visual
repetition priming requires that the perceptual attributes of the prime be

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MEMORY DISSOCIATIONS IN INFANTS 139

processed at a stage that assembles those attributes into “relatively high-level

representations” but is below the stage of conscious awareness. Recall that
priming effects are manifested without the need for conscious recollection of
specific prior episodes (Graf & Schacter 1985).
The similarity between the reactivation task and the priming tasks used
with adults has been noted elsewhere (Mandler 1984; Naito & Komatsu 1990;
Nelson 1995). Like primes used in studies of implicit memory with adults, a
prime reactivates either a preexisting memory representation (Tulving &
Schacter 1990) or a representation established by a single exposure to a stimulus
(Graf & Schacter 1985; Musen & Treisman 1992; Naito & Komatsu 1990).
Although effects of priming are typically measured in terms of changes in
reaction time for adults and as renewed retention on an ensuing delayed
recognition task for infants, a closer analysis reveals that these are the same.
Amnesics, in fact, exhibit retention by producing the previously studied
response to a memory prime (e.g., the stem of a previously studied word) on the
ensuing test, and infants exhibit retention by producing the previously acquired
response to the memory prime (e.g., a particular mobile or hand-puppet) on the
ensuing test.
This parallel is best illustrated by infants’ performance in reactivation
tasks in which two memories were initially associated, for example, a mobile/
kick response and a music box/arm-pull response (Timmons 1994) or a train/
lever-press response and a puppet/imitation response (Barr & Vieira 1999). In
each case, both associates were reactivated by priming with only one member
of the associated pair. Which response infants subsequently produced during
testing, however, depended on the particular associate (analogous to a word-
stem) that was presented as the test cue — even if it was not the particular
associate that had reactivated the otherwise inaccessible memory in the first
place. Thus, for both adults and infants, retrieval of the inaccessible memory
was initiated implicitly before the test. For adults, this process occurs prior to
the retention test via the initial verbal instructions to respond with whatever
word comes to mind before they are presented with the cue fragment (Schacter
et al. 1989); for infants, this process occurs via the initial visual instructions
produced by exposure to the moving mobile, the moving train, or the moving
and ringing puppet — also before the cued-recall test — to respond with
whatever response comes to mind — and they do, depending on the particular
fragment or associate that is presented immediately before the test. When
infants are very young, the initial retrieval process takes time, but when they

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140 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

get older, it occurs instantaneously (Hildreth & Rovee-Collier 1999a; see

following section). Even 3-month-olds respond instantaneously, however, if
their initial study phase is closer in time to the test, as usually is the case in
studies with amnesics or instructed adults.
Although whether or not their retrieval is actually intentional is open to
speculation, the delayed recognition and reactivation tasks that have been
used with preverbal infants meet the basic assumptions of the retrieval inten-
tionality criterion (Schacter et al. 1989, see Chapter 2). Because initial train-
ing or study is identical for the delayed recognition and reactivation tasks,
differences in infants’ memory performance on these tasks cannot be attrib-
uted to differences in encoding. Also, because retention testing in the delayed
recognition and reactivation tasks is conducted under identical circumstances
with identical cues present, differences in infants’ memory performance on
the two tasks cannot be attributed to differences in the retrieval cues that are
present at the time of testing. Additionally, the reactivation task is typically
administered after delays so long that infants cannot recognize the target
information, just as amnesics cannot recognize the target information at the
time they are presented with a memory prime. Because infants are preverbal,
however, the instructions in the two tasks are contained in the structure of the
environment. These instructions consist of the different experimental manipu-
lations that are introduced between training and testing. In the reactivation
(implicit memory) task, the retention test is preceded by exposure to a memory
prime, whereas in the delayed recognition (explicit memory) task, it is not.
The parallel between the infant and adult tasks is confirmed by the
parallel results that have been obtained with adults and infants; to put it
colloquially, “the proof is in the pudding.” In reaction time studies with adults,
for example, priming decreased correct naming latencies to items of any
previously studied size (Biederman & Cooper 1992), and in mobile studies
with infants, priming with items of any previously studied size was successful
(Gerhardstein, Adler & Rovee-Collier, 2000) — even though on a recognition
test, both adults and infants had discriminated the same items if they differed
in size from the previously studied size. That is, adults had longer reaction
times to items whose size differed from the previously studied size on a cued-
recall (recognition) test, and infants did not respond above baseline to items
whose size differed from the previously studied size on a cued-recall (delayed
recognition) test. Data such as these reveal that the test that reveals the effect
of priming is not what distinguishes priming from recognition — the test is the

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MEMORY DISSOCIATIONS IN INFANTS 141

same; rather, the prior-cuing procedure and the particular instructions that
precede the test are the distinguishing factors. Twelve other independent
variables that also produce parallel memory dissociations for adults and
infants on recognition and priming tests are reviewed below.

Infants’ response latency to a memory prime

Some researchers have objected to the analogy between reactivation tasks that
are used with infants and priming tasks that are used with adults. Their
objection has been based on initial evidence that the latency of response to a
memory prime by 3-month-olds (Fagen & Rovee-Collier 1983) and 6-month-
olds (Boller, Rovee-Collier, Borovsky, O’Connor & Shyi 1990) in a reactiva-
tion task is so slow — from 1 to 24 hours, whereas in adults, the response
latency to a word fragment or word stem is essentially instantaneous. Hildreth
and Rovee-Collier (1999a), however, found that the latency of responding to a
reactivation stimulus (i.e., a memory prime) decreases linearly over the first
year of life. By 9 months of age, infants respond to a prime within 1 min, and
by 12 months of age, they respond instantaneously, like adults.
These data are summarized in Figure 7.5, which also includes the latency
data previously collected from 3- and 6-month-olds. As can be seen, the
latency of response to a memory prime decreases linearly over the entire first
year of life. This result is particularly impressive when one considers that the
time between forgetting and priming in all experiments was held constant over
age; that is, at all ages, the prime was always presented 1 week after infants
had last remembered the task. Because infants take progressively longer to
forget the original training memory over the first year of life, the prime was
necessarily presented after increasingly longer delays with age. Thus, the
prime was presented 13 days after the original event to 3-month-olds, but it
was presented 2½ months after the original event to 12-month-olds. Despite
this, the latency of priming decreased linearly between 3 and 12 months of
age. In contrast, priming has never been studied in normal adults after forget-
ting is complete (i.e., when subjects cannot recognize the stimulus) but only in
amnesics.
The preceding results suggest that a maturation-based factor is respon-
sible for the age-related decrease in priming latency. This suggestion is
consistent with prior evidence that experimental manipulations that accelerate
or retard CNS maturation in mice produce corresponding effects on long-term

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142 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 7.5. The decrease in the latency (log s) of responding to a memory prime over the
first year of life. Three-month-olds were trained, primed, and tested in the mobile task (open
circles), whereas 9- and 12-month-olds were trained, primed, and tested in the train task
(filled circles); 6-month-olds were studied in both tasks.

memory without affecting original learning (Nagy 1979; Nagy, Misanin,

Newman, Olsen & Hinderliter 1972) and that infant guinea pigs, whose
central nervous system is already mature at birth, display adult levels of
retention (Campbell, Misanin, White & Lytle 1974). Although this evidence
reveals that increasing neurological maturity contributes to the age-related
improvement in memory performance, the specific neural mechanisms or
circuits that are implicated in the decreased response latency to priming are
unknown.
Increasing CNS maturation, however, is not the sole means by which
infants’ response latency to a memory prime can decrease. Even at 3 months
of age, infants responded instantaneously to a prime that was presented only 1
day after training but, still, when infants did not recognize the particular test
mobile (Gulya, Rovee-Collier, Galluccio & Wilk 1998). These data reveal that
the age of the memory (i.e., its relative accessibility) can also be a significant
factor in the latency of response to a memory prime. In addition, the response
latency to a prime can decrease if infants are primed a second time (Hayne,
Gross, Hildreth & Rovee-Collier 2000b). When 3-month-olds were exposed

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MEMORY DISSOCIATIONS IN INFANTS 143

Figure 7.6. The decrease in 3-month-olds’ latency of responding after a second memory
prime. Independent groups of infants were given one (striped columns) or two (dark
columns) reactivation treatments and then were tested from 1 to 24 hours later (14 days after
training). The no-reminder control group (open column), which received no reactivation
treatment, exhibited no retention during the 14-day test.

to a single memory prime 13 days after mobile training, they did not exhibit
renewed retention until 24 hours later. When they were exposed to two primes
— the first on day 7 and the second on day 13, they exhibited renewed
retention only 1 hour later (see Figure 7.6). The preceding data reveal that
prior retrieval experience is also a significant factor in the latency of response
to a memory prime. The latter result is reminiscent of Tulving’s (1983)
description of a reduction in access time to information in semantic memory as
a consequence of repeated retrievals in adults. He characterized this reduction
as an improvement in retrieval skill with practice.

Independent variables that produce memory dissociations in adults

Table 7.2 lists 13 independent variables that produce dissociations on two

tasks — priming and recognition — that are commonly used to distinguish
between implicit and explicit memory, respectively, in studies with amnesics

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144 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Table 7.2. Independent Variables and Their Effects on Adult Performance in Implicit and
Explicit Memory Tasks
Independent Variable Effect on Implicit Tasks Effect on Explicit Tasks
age* none large
amnesia* none large
retention interval none large
vulnerability (interference) limited great
number of study trials small large
study (exposure) time none large
number of items studied none large
level of processing none large
spacing effects none large
affect* important less important
affect none large
serial position transient or none persisistent primacy effect
studied size none large
memory load none large
context dependency less pronounced more pronounced
*Subject variable

and normal adults. These same variables produce the same dissociations in the
memory performance of very young infants, who are thought to lack explicit
memory, on reactivation and delayed recognition tasks. In this section, we
present data from adults that illustrate the memory dissociation produced by
each independent variable on implicit and explicit tasks and data from infants
that illustrate the corresponding memory dissociation produced by the same
independent variable on delayed recognition and reactivation tasks. The bulk
of the infant data was compiled from mobile studies with infants, but infant
data that are available from other paradigms are also presented.
1. Age. As Tulving put it, “The neural pathways that subserve episodic
remembering, maturing late in childhood and deteriorating early in old age,
are not necessary for priming” (Tulving 1991, p. 16). In fact, tests of explicit
memory with 3- to 11-year-olds and young adults (Carroll, Byrne & Kirsner
1985; Greenbaum & Graf 1989; Mitchell 1993; Naito 1990) have found that
recall and recognition improve with age, but the amount of priming remains
stable across age. Performance also improves with age on imitation tests of
explicit memory. The number of logically ordered steps that toddlers success-
fully imitated on an immediate cued-recall test increases between 13 and 20
months of age (Bauer 1996), and the level of deferred imitation of a three-step

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MEMORY DISSOCIATIONS IN INFANTS 145

sequence also increases between 6 and 18 months of age (Hayne et al. 2000a;
Hayne 1997).
Memory performance in mobile studies similarly improves with increas-
ing age over the first half year of life in the delayed recognition task (the
explicit memory task) but not in the memory reactivation task (the implicit
memory task). Gekoski, Fagen, and Pearlman (1984) compared the memory
performance of premature infants who were born between 31.1 and 39.7
weeks of gestational age on a delayed recognition test with that of full-term 3-
month-olds. The mean conceptional age of the preterm and full-term infants at
the time of testing did not differ (51.3 and 53.4 weeks, respectively), but their
mean chronological age did (156.4 and 81.7 days, respectively). All infants
were trained in the mobile task and were tested for recognition of the training
mobile 1 week later. During the 1-week test, only full-term infants exhibited
significant retention. This difference in retention resulted despite the fact that
the preterm infants were of equivalent conceptional age and almost 3 months
older in chronological age than the full-term infants. The memory perfor-
mance of the premature group paralleled that of full-term 2-month-olds, who
also fail to exhibit significant recognition after a 1-week delay.
Figure 7.7 shows that the magnitude of infants’ retention in a delayed
recognition test 1 week after training increases as a function of age despite the
fact that the final levels of acquisition were equivalent (Hayne 1990; Hill,
Borovsky & Rovee-Collier 1988; Rovee-Collier 1984; Sullivan, Rovee-
Collier & Tynes 1979). The same figure also shows that the magnitude of
retention following a reactivation treatment that was administered 3 weeks
after training is not affected by age (Davis & Rovee-Collier 1983; Hayne
1990; Hill et al. 1988; Rovee-Collier 1984; Rovee-Collier et al. 1980; Vander
Linde, Morrongiello & Rovee-Collier 1985).
The age-related increase in infants’ memory performance on delayed
recognition tasks is not unique to the mobile procedure. Hartshorn et al.
(1998b) trained infants between 6 and 18 months of age in the train procedure
(Hartshorn & Rovee-Collier 1997; see Chapter 6) and tested their delayed
recognition after delays that incremented in 1-week steps until they failed to
exhibit significant retention for 2 consecutive weeks. These data were then
combined with delayed recognition data previously obtained from infants
between 2 and 6 months of age who were identically trained and tested in the
mobile procedure. Figure 7.8 summarizes the resulting age changes in reten-
tion over the first year-and-a-half of life. This figure presents infants’ mean

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146 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 7.7. Memory performance of 2-, 3-, and 6-month-olds on a delayed recognition test
(striped columns) 1 week after training and on a reactivation test (filled columns) 3 weeks
after training. (A retention ratio = 1.00 indicates no forgetting from the immediate to the
long-term test.) Asterisks mark groups that displayed retention (M baseline ratio signifi-
cantly > 1.00).

retention ratios after a 0-day retention interval, after the longest retention
interval at which infants of a given age performed significantly above base-
line, and after the longest retention interval at which infants of a given age
were tested (i.e., when they no longer performed significantly above baseline).
As can be seen, all infants exhibited equivalent retention after short test
delays, but infants remembered after progressively longer delays with age,
irrespective of task.
These findings are identical to those originally obtained by Campbell and
Campbell (1962) and in subsequent animal studies of memory development
with a variety of different species (for reviews, see Campbell & Coulter 1976;
Coulter 1979; Nagy 1979). In those studies, animals ranging from prewean-
lings to adults were required to learn a simple response-reinforcement contin-

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MEMORY DISSOCIATIONS IN INFANTS 147

Figure 7.8. Mean retention ratios of independent groups of infants between 2 and 18
months of age who were trained for 2 consecutive days in the mobile task (2 to 6 months,
filled symbols) or the train task (6 to 18 months, open symbols) and received an immediate
retention test after the conclusion of acquisition on day 2. Six-month-olds were trained and
tested in both tasks. Infants of each age received a delayed recognition test after different
retention intervals until, as shown in the last point on each curve, they exhibited no retention
(i.e., M baseline ratio not significantly > 1.00).

gency that was well within the sensorimotor capacity of all ages studied. With
the exception of preweanlings, who occasionally responded at slightly lower
rates and reached the learning asymptote more slowly than more mature
subjects, animals showed no age differences in acquisition, reached the learn-
ing asymptote at the same rate, and exhibited similar levels of retention shortly
after learning. Despite this, younger animals consistently forgot more rapidly.
The maximum duration of retention that was exhibited by infants be-
tween 2 and 18 months of age in the mobile task (Hartshorn et al. 1998b) and
between 6 and 18 months of age in the deferred imitation task (Hayne &
Campbell 1997; Herbert & Hayne 2000) was described in Chapter 6 (see
Figure 6.6). These functions reveal that long-term memory improves mono-
tonically as a function of age over the first 2 years of life. There is no
suggestion that long-term memory is suddenly enhanced at 8 months of age, as

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148 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

was postulated by Kagan (1984; Kagan & Hamburg 1981), or that delayed
recognition changes abruptly at 8 or 9 months of age, when the late-maturing
memory system was thought to become functionally mature (Nadel & Zola-
Morgan 1984; Schacter & Moscovitch 1984), or when the transition from
implicit to pre-explicit memory was hypothesized to occur (Nelson 1995,
1997). Nor is there any indication that memory changes qualitatively with the
emergence of language in the second year of life (Best 1995; Herbert & Hayne
2000; Nelson 1990).
These age differences in retention (see Figure 7.8 and Figure 6.6) are not
due to differences in the baseline levels of activity or the original levels of
learning in either the conditioning or imitation tasks — there were no age
differences. Analyses revealed that infants’ operant levels and degree of
original learning did not change with age whether they were studied in the
mobile or train task over the period of 2 to 18 months (Hartshorn et al., 1998b)
or in the imitation task between 6 and 24 months of age (Herbert & Hayne
2000). These results are particularly striking when one considers the major
physical, behavioral, and cognitive changes that occur over the course of the
infancy period (see Figure 7.9), including marked changes in motoric and
linguistic competence.
The preceding findings demonstrate that immature infants are as capable
of encoding memories as more mature infants. We conclude, therefore, that
age differences in explicit memory must arise from maturational differences in
the neural mechanisms that are responsible for either maintaining access to the

Figure 7.9. Left to right: Infants 2, 3, 6, 9, 12, 15, or 18 months of age. Note the dramatic
physical and behavioral differences between younger and older infants over the first year-
and-a-half of life.

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MEMORY DISSOCIATIONS IN INFANTS 149

stored memory over time or retrieving it. We suspect that these neural mecha-
nisms involve the perceptual mechanisms that are associated with selective
attention. Younger infants would have leaner memories, for example, if they
selectively attended to fewer elements in a given situation. As a result, fewer
effective retrieval cues would be available for them to reperceive at the time of
testing (Treisman 1992), and their retention would suffer. We have previously
obtained evidence from 2- and 3-month-olds that supports this possibility
(Rovee-Collier, Earley & Stafford 1989). At 2 months of age, infants do not
appear to process information about the environmental context within which
mobile training occurs, but at 3 months of age, they do. In a related vein,
Gordon (1979) proposed that age differences in retention might reflect differ-
ences in the content of what is encoded at different ages. By this account,
infants of different ages acquire different kinds of information in the same
learning situation — perhaps because they have different learning histories or
find different components of the learning situation salient. Evidence of onto-
genetic differences in stimulus selection in animals has also been reported by
Spear and Kucharski (1984).
Additional support for the proposition that age differences in selective
attention affect age differences in retention comes from the finding that at 3
months of age, the duration for which infants can recognize a particular
stimulus can be increased or decreased relative to control performance simply
by increasing or decreasing their attention to that stimulus during original
training (Adler, Gerhardstein & Rovee-Collier 1998; see Level of Processing,
below).
A dissociation in memory performance on cued-recall and reactivation
tasks was also found for infants of different ages in a study that used a
reenactment procedure (Sheffield & Hudson 1994). In this study, 14- and 18-
month-olds engaged in a different activity at each of six different stations in a
laboratory playroom during a single visit. Each activity consisted of a defined
set of target actions (e.g., get fish food from the cabinet, feed the fish, put the
food back in the cabinet). On the cued-recall test, children returned to the
playroom and produced as many of the target actions at each station as they
could. The 14-month-olds remembered the initial activities for 8 weeks,
whereas the 18-month-olds remembered them for 10 weeks. After forgetting
was complete, new groups at both ages again engaged in the original activi-
ties. After their original memory was presumably forgotten, they received a
reactivation treatment in which they watched an experimenter model half of

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150 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

the original activities. When tested for retention of the remaining half of the
activities 24 hours later, infants of both ages exhibited the same magnitude of
reactivation (i.e., the number of nonmodeled activities performed). The de-
layed recognition/reactivation dissociation found in this study was identical to
the dissociation that was obtained in mobile studies with younger infants,
despite the fact that the experimental paradigms were very different. Whereas
the younger infants had learned to produce the target response (kicking) via a
conditioning procedure, infants in the preceding study were initially shown
how to find and use the materials required for each activity and then reenacted
that target response.
In the response-to-novelty task, infants who were familiarized with the
training stimulus in a single session also remembered progressively longer
with age on a explicit (recognition) test. Rose (1981) found that 6- and 9-
month-olds exhibited an equivalent novelty preference when given a paired-
comparison test with four different stimuli immediately after familiarization.
After delays ranging from 75 to 150 s, however, 6-month-olds exhibited a
novelty preference only for a facial stimulus, but 9-month-olds continued to
show a novelty preference for all of the stimuli that they had preferred on the
immediate response-to-novelty test. Greco and Daehler (1985) familiarized
even older infants — 2-year-olds — with exemplars of basic-level categories
and found that they still exhibited a novelty preference after 1 week. (Data
from a reactivation task were not collected.)
2. Retention Interval. A basic observation of human memory is that
retention on standard recognition, cued-recall, and free-recall tests declines
with the passage of time (Wickelgren 1972; Woodworth 1938). In contrast,
priming effects are long-lasting in both normal adults and children (Cave
1997; Komatsu & Ohta 1984; Mitchell & Brown 1988; Roediger & Blaxton
1987; Tulving et al. 1982) and amnesics (Cave & Squire 1992; Schacter, Chiu
& Ochsner 1993a; Tulving, Hayman & Macdonald 1991). Tulving et al.
(1982), for example, primed subjects with words and found that their memory
performance on a word-fragment completion test was stable over a period of 1
week, but their performance on a yes/no recognition test declined over the
same delay. Similar data were reported by Naito (1990, Experiment 3), who
assessed the proportion of correct word-fragment completion and recognition
scores for old and new items in Japanese first graders, sixth graders, and
college students after delays of 7 min and 6 days. As in Tulving et al.,
recognition memory scores declined over the retention interval for all ages,

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MEMORY DISSOCIATIONS IN INFANTS 151

but word-fragment completion did not change over the same delay.
Musen and Treisman (1990), using visual patterns with adults, also found
a perceptual priming effect that remained stable across delays ranging from a
few hours to 1 week, but pattern recognition declined significantly across the
same period. In the perceptual priming task, subjects were briefly exposed to a
series of visual patterns that they had previously studied or that were novel.
After each exposure, they attempted to draw the pattern just seen, and the
difference in accuracy between subjects’ reproductions of previously studied
and novel patterns was taken as the measure of implicit memory. For the
measure of explicit memory, subjects were asked to select which pattern of
four alternatives they remembered having studied. Using a picture-naming
paradigm, Cave and Squire (1992) found that amnesics demonstrated a repeti-
tion priming effect that was of normal magnitude 1 week after study, yet
amnesics cannot recognize pictures (an explicit task) after even a short delay.
In adults, repetition priming effects can be quite long-lasting. Mitchell
and Brown (1988) obtained a robust priming effect on a picture-naming task
that remained stable across delays ranging from 1 to 6 weeks, and naming
times were not affected by whether or not the picture was recognized. In
contrast, performance on an old/new picture recognition task declined over the
same period. Cave (1997) replicated their results and found in addition that
adults still exhibited significant repetition priming after delays as long as 48
weeks in the same task. Similarly, 9-month-olds still exhibit a significant
priming effect almost 6 weeks after reactivation in the operant train procedure,
and 12-month-olds still exhibit a significant priming effect at least 8 weeks
afterward (Hildreth & Rovee-Collier 1999b).
The same pattern of memory dissociations was obtained in studies of
deferred imitation with infants. Bauer, Hertsgaard and Wewerka (1995) re-
ported that the number of correctly ordered pairs of actions produced by 14-
month-olds immediately following a verbal prime was approximately
equivalent whether children were tested after 1 week or after 1 month, but
children’s imitation performance on a cued-recall test (i.e., an explicit
memory test) decreased as the retention interval increased from 1 week to 1
month. Hayne and her colleagues have likewise reported that retention in a
deferred imitation task varies both as a function of the retention interval and
age. In all studies, older infants remembered longer (Barr & Hayne, 2000;
Herbert & Hayne 2000)

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152 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

A similar memory dissociation was found for 14- and 18-month-olds who
were trained to perform six distinct activities in a single session in a multiple-
activities paradigm. The magnitude of retention in the delayed recognition task
progressively declined as the retention interval between training and testing
increased to 8 and 10 weeks, respectively (Hudson 1994), but the magnitude of
retention following a reactivation treatment was the same whether the delay
between training and priming was 8 weeks or 10 weeks (Sheffield & Hudson
1994).
In mobile studies with infants ranging in age from 2 through 6 months,
performance on delayed recognition tests is also affected by the retention
interval, but performance on priming tests is not. Figure 7.10, for example,
shows that the memory performance of 3-month-olds on a delayed recognition
test declined steadily with increases in the training-test delay (Hayne 1990;
Rovee-Collier 1984; Sullivan et al. 1979), but the magnitude of their retention
24 hours after a reactivation treatment was the same whether the interval

Figure 7.10. Magnitude of delayed recognition or reactivation as a function of the retention

interval for independent groups of 3-month-olds (a retention ratio = 1.00 indicates no
forgetting from the immediate to the long-term test). Asterisks mark groups that displayed
no retention (M baseline ratio not significantly > 1.00).

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MEMORY DISSOCIATIONS IN INFANTS 153

between training and priming was 2, 3, or 4 weeks (Hayne 1990; Rovee-

Collier et al. 1980). The memory was either recovered or it was not. Of the
nine infants primed 34 days after training and tested 1 day afterward, for
example, four infants exhibited perfect retention, and five infants exhibited
none. Similarly, the magnitude of reactivation on priming tests is unaffected
by the delay between priming and testing (see Figure 7.6). Three-month-olds
exhibited the same magnitude of reactivation whether they were tested 1 hour,
4 hours, or 24 hours after priming (Hayne et al. 2000b).
3. Vulnerability. There is a rich tradition of research documenting that
adults’ performance on explicit memory tasks is vulnerable to interference
(Barnes & Underwood 1959; Postman & Underwood 1973), but evidence that
adults’ performance on implicit memory tasks is not vulnerable to interference
is more recent (Graf & Schacter 1987; Sloman, Hayman, Ohta, Law &
Tulving 1988; Tulving 1983). Priming in word-fragment (Sloman et al. 1988),
word-completion (Graf & Schacter 1987), and lexical-decision (Bentin &
Moscovitch 1988) tasks, for example, is unaffected by the same interference
manipulations that impair memory on recognition, cued-recall, and modified
free-recall tests.
A similar dissociation has been observed for infants’ memory perfor-
mance on delayed recognition and reactivation tasks as well. When 3-month-
olds were trained with one mobile in session 1 and with a different mobile in
session 2, they failed to recognize the session-1 mobile during a 24-hour
delayed recognition test — a classic example of retroactive interference
(Fagen, Morrongiello, Rovee-Collier & Gekoski 1984). This retroactive inter-
ference effect occurred even when infants were trained with a single mobile
for a total of 30 min in two sessions and then, immediately after the end of
training, they were merely allowed to view — for only 3 min — a different
mobile being moved by the experimenter. As before, infants failed to recog-
nize the training mobile during a delayed recognition test 24 hours later (Bhatt
1997; Rossi-George & Rovee-Collier 1999; Rovee-Collier, Borza, Adler &
Boller 1993a). At 6 months of age, infants shown the novel mobile for only 2
min after delays as long as 13 days after training were unable to recognize the
training mobile on a delayed recognition test 24 hours later. In contrast, infants
with no interpolated exposure exhibited near-perfect retention on the long-
term test (Muzzio & Rovee-Collier 1996).
Retroactive interference in infants’ delayed recognition performance is
not limited to an interpolated exposure to another mobile. A similar result was

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154 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

obtained when infants were trained with the same mobile in different contexts
(distinctively colored-and-patterned crib or playpen liners) in each of two
sessions and were then tested for recognition of the mobile in the session-1
context. At both 3 months (Rovee-Collier & DuFault 1991) and 6 months
(Amabile & Rovee-Collier 1991), training in a different context in session 2
impaired infants’ ability to recognize the mobile in the original context during
the 24-hour delayed recognition test. Retroactive interference also occurred
when both 3-month-olds (Rossi-George & Rovee-Collier 1999) and 6-month-
olds (Boller & Rovee-Collier 1992) were trained in the same context for 2
days and then were simply allowed to view a novel context immediately after
training. Infants could no longer recognize the training mobile in the original
context 24 hours later; instead, they could recognize it only in the new context.

Figure 7.11. Magnitude of delayed recognition (left panel) 1 day after training and magni-
tude of reactivation (right panel) 3 weeks after training at 6 months of age. After reactiva-
tion in the original context, groups of 6-month-olds were exposed to a novel context
between training or priming and testing (Interference) or were not exposed to an interpo-
lated context (None) and were tested in the original training context 1 day later. (A retention
ratio = 1.00 indicates no forgetting from the immediate to the long-term retention test).
Asterisks mark groups that displayed retention (M baseline ratio significantly > 1.00).

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MEMORY DISSOCIATIONS IN INFANTS 155

In contrast to a memory’s vulnerability to interference on a delayed

recognition test, a reactivated memory is relatively impervious to interference
by new information that is interpolated between the reactivation treatment and
testing. Using the same novel-context exposure conditions that had previously
interfered with 6-month-olds’ ability to recognize the mobile in the training
context (see Figure 7.11, left panel), we were unable to modify a reactivated
memory for contextual information at 6 months of age (Boller & Rovee-
Collier 1994). Whether infants were exposed to the novel context immediately
after a successful reactivation treatment or after delays that extended to 24
hours, infants continued to recognize the mobile in the original context and
never recognized it in the exposed one (see Figure 7.11, right panel).
4. Number of Study Trials. In studies with adults, recognition improves as
the number of study trials or stimulus presentations increases, but the number
of study trials has little or no effect on priming. Musen and Treisman (1990),
for example, gave adults visual patterns to study for 3 s each, after which a
pattern was removed, and subjects were allowed to rehearse it for 7 s before
the next pattern appeared. After this initial study period, some subjects were
reexposed to the sequence of patterns four times (each pattern was re-exposed
for only 1 s), while others received only the initial study trial. Explicit memory
was measured in a fixed-choice recognition test in which subjects indicated
which one of the four test stimuli they had previously studied. Implicit
memory was measured in a perception test in which studied patterns and
distractor patterns were presented singly, followed by a mask, and subjects
were instructed to draw what they had just seen. The priming effect was
measured by comparing performance on the old and the new patterns. Sub-
jects in both the repeated- and the single-trial conditions were tested immedi-
ately after the first session and 8 days later. In addition, some subjects in the
repeated-trials condition were tested in a second session 1 to 3 hours after their
first. Musen and Treisman found that the number of study trials had a small-to-
nonexistent effect on priming whether subjects were tested later on the same
day or after an 8-day delay. In contrast, the decline in recognition accuracy
was almost three times greater in the single-trial group than in the repeated-
trials group after the 8-day delay.
Bentin and Moscovitch (1988) exposed adults to a set of unfamiliar faces
for either one trial or five trials during a study session with lags (number of
items interpolated between stimulus repetitions) of 0, 4, or 15 in each learning
condition. After one trial per set, stimulus repetition facilitated recognition at

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156 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

lag 0 and lag 4 but not at lag 15; after five trials, however, repetition facilitated
recognition, as measured in both reaction time and accuracy, after all lags
(Experiment 3). In addition, although the repetition effect in a recognition
(explicit memory) task was bigger in the five- than in the one-trial learning
condition, in a structural (implicit memory) face/nonface discrimination task,
it was independent of the number of study trials (Experiment 4).
In deferred imitation studies with infants, the benefit of additional study
trials has also been demonstrated. Bauer et al. (1995) gave 14-month-olds
either one or three trials and measured their ability to reproduce a series of
ordered events either 1 week or, for the three-trial group only, 1 month later.
Infants who received only a single trial exhibited excellent cued-recall after 1
week but poor cued-recall after 1 month; infants who received three trials,
however, performed as well after 1 month as infants who received only one
trial performed after 1 week. Likewise, Barr et al. (1996) found that 6-month-
olds could imitate target actions on a hand-puppet 24 hours after watching six
but not three demonstrations of the actions.
In mobile studies with 3-month-olds, the number of training trials also
affects memory performance on delayed recognition tests but not on reactiva-
tion tests. Figure 7.12 shows that increasing the number of study trials from
one to three significantly extended the delayed recognition of 3-month-olds
(Ohr, Fagen, Rovee-Collier, Vander Linde & Hayne 1989) but had no effect
on the magnitude of their retention after a reactivation treatment (Greco,
Hayne & Rovee-Collier 1990; Rovee-Collier et al. 1980). Here, each addi-
tional trial prolonged recognition by an additional week, but both two and
three successive training trials produced exactly the same magnitude of reten-
tion 1 day following a reactivation treatment that was administered 3 weeks
after the end of training.
This result was not age-specific: At 2 months of age, infants trained for 18
min exhibited excellent retention 1 week later, but infants trained for 6 or 12
min exhibited none (Rovee-Collier 1984; Vander Linde et al. 1985). Simi-
larly, at 6 months of age, two training trials also produced poorer 24-hour
delayed recognition than three (Merriman & Rovee-Collier 1995), but two
training trials produced the same magnitude of retention 1 day after a reactiva-
tion treatment (Borovsky & Rovee-Collier 1990) as three (Gulya, Sweeney &
Rovee-Collier 1999) or four (Timmons 1994) training trials. In our experi-
ence, however, an operant task that was acquired in only a single training trial
cannot be reactivated between 2 and 6 months of age, although actions that

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MEMORY DISSOCIATIONS IN INFANTS 157

Figure 7.12. The effect of number of training sessions at 3 months on the magnitude of
delayed recognition (left panel) after different delays and the magnitude of reactivation
(right panel) 3 weeks after training. Asterisks mark groups that exhibited retention (M
baseline ratio significantly > 1.00).

were modeled in a single trial can be reactivated at 6 months of age if they

were associated with an operant task that had been acquired in two sessions
(Barr & Vieira 1999) or if infants were older (i.e., 18 months; Barr 1997).
Finally, the retention advantage of a greater number of trials on a delayed
recognition test occurred even when the total amount of training time was held
constant. Vander Linde et al. (1985) trained 2-month-olds in the mobile task
for either a single 18-min trial or three 6-min trials that were spaced by 24
hours. Three weeks later, infants whose training time was distributed into
three trials exhibited near-perfect retention on a delayed recognition test,
whereas infants who were trained for a single session exhibited none.
The magnitude of priming is also unaffected by the number of prior
reactivations (Greco et al. 1990; Hayne 1990; Hayne et al. 2000b; Rovee-
Collier et al. 1980). Hayne (1990), for example, found that the magnitude of
retention 21 days after training (1 day after a reactivation treatment) was
identical whether 3-month-olds received one, two, or three reactivations (see
Figure 7.13), and Hayne et al. (2000b) found the same result 14 days after
training (1 day after a reactivation treatment) whether 3-month-olds had
received one or two reactivations (see Figure 7.6). The same magnitude of
retention was also obtained 21 and 34 days after training (again, 1 day after a
reactivation treatment) whether 3-month-olds received two reactivations or
three (Hitchcock & Rovee-Collier 1996).

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158 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 7.13. The magnitude of reactivation 3 weeks after training for 3-month-old infants
who had received one, two, or three reactivations. In each case, retention was tested 1 day
after the final reactivation treatment.

5. Spacing Effects. In studies with adults, superior performance on tests

of recall and recognition when study trials are distributed instead of massed is
a common result (for reviews, see Cohen 1985; Crowder 1976). In contrast,
spacing effects on implicit memory tests are inconsistent and relatively infre-
quent (e.g., Jacoby & Dallas 1981; Perruchet 1989). Although Greene (1990)
found a spacing effect on a perceptual identification test under intentional-
learning instructions, for example, the effect disappeared when learning was
incidental or when spacing was manipulated between study lists. Jacoby
(1978; Cuddy & Jacoby 1982) attributed the retention advantage of spaced
study to the greater processing that is required for successful retrieval on
successive repetitions. Assuming that each presentation of an item or trial
initiated the retrieval of its prior presentation, he proposed that retrieval was so
trivial when trials were massed that little processing was required; conversely,
when the interval between successive trials was greater, retrieval was more
difficult, and more processing was involved.
Bjork and his colleagues (Anderson, Bjork & Bjork 1994; Bjork 1975;
Schmidt & Bjork 1992) similarly attributed the retention advantage of spaced
study to the greater retrieval difficulty that is associated with a greater amount

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MEMORY DISSOCIATIONS IN INFANTS 159

of time since the last retrieval. In a classic study (Landauer & Bjork 1978),
adults learned a number of names or name-picture associations during a single
study session in which each item was presented once. They then received three
or four cued-recall tests, but the intervals between succeeding tests were filled
with different numbers of names. Retention was poorest when test items were
massed (no intervening names), better when four or five items intervened
between successive tests, and best when the number of items (hence the time)
between successive tests progressively increased. They concluded that reten-
tion was facilitated because the expanding series of intertrial intervals permitted
adults to practice retrieval under increasingly difficult conditions. Subse-
quently, Rea and Modigliani (1985) found that children’s ability to recall
multiplication facts and spelling lists was significantly enhanced when they
used an expanding series of practice tests.
Both 2-month-olds (Vander Linde et al. 1985) and 3-month-olds (Rovee-
Collier, Evancio & Earley 1995) also exhibited significantly better delayed
recognition a week later when the interval between training sessions was
increased from 1 to 2 days. When the intersession interval was increased to 4
days for the 3-month-olds, however, the infants exhibited no retention whatso-
ever. This result was interpreted in terms of the “time window” construct
(Rovee-Collier 1995), which holds that there is a limited period of time
following an initial event (i.e., session 1) within which subsequent information
(i.e., session 2) can be integrated with the memory representation of the initial
event; if the new information is encountered after the time window has shut,
then it is not integrated with the initial event. In the Rovee-Collier et al. (1995)
study, the time window for integrating the effects of successive training
sessions apparently shut after 3 days (see Figure 7.14). When 3-month-olds
were trained and tested in a reactivation paradigm, however, the magnitude of
retention 1 day after priming was the same whether the sessions were spaced by
1 or 2 days; for infants whose second session was 4 days after their first (outside
the time window), however, the reactivation treatment was ineffective (Rovee-
Collier et al. 1995).
In another study (Rovee-Collier, Greco-Vigorito & Hayne 1993b), 3-
month-olds were trained for three sessions and then were shown a novel
moving object either immediately after training was over (when the time
window opened) or 4 days later (at the end of the time window, which closes
after 4 days with three training sessions). Infants who were exposed to the
object at the beginning of the time window recognized it for only 4 days, but

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160 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 7.14. The effect of spacing between successive training sessions (session 1 = day 0;
session 2 = day 1, 2, or 4) on the magnitude of delayed recognition (left panel) 8 days after
session 1 and the magnitude of reactivation (right panel) 15 days after session 1 at 3 months
of age. Asterisks mark groups that displayed retention (M baseline ratio significantly >
1.00). The magnitude of recognition of group 0–2 is significantly greater than that of group
0–1, but the magnitude of reactivation of the two asterisked groups does not differ. The
second training session on day 4 was not integrated with the first training session on day 0;
that is, day 4 fell outside of the time window.

infants who were exposed to the object at the end of the time window
recognized it for 10 additional days. Although the delay between training and
exposure to the novel object affected infants’ magnitude of delayed recogni-
tion after a retention interval of 1 day, it had no effect on their magnitude of
reactivation after a retention interval of 3 weeks (see Figure 7.15; Greco et al.
1990; Rovee-Collier et al. 1993b).
In studies with 3-month-olds (Greco et al. 1990; Hayne, Rovee-Collier &
Perris 1987; Ohr et al. 1989), infants trained for three sessions on successive
days (days 0–1–2) had exhibited significant retention after 2 weeks but not
after 3 weeks. Hartshorn, Wilk, Muller and Rovee-Collier (1998c) replicated
this finding. In addition, they trained other groups for three sessions but

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MEMORY DISSOCIATIONS IN INFANTS 161

Figure 7.15. The effect of the timing of a brief posttraining exposure to a novel object on
the magnitude of delayed recognition of that object (left panel) 1 day after the exposure and
on the magnitude of reactivation (right panel) 3 weeks after training at 3 months of age. (A
retention ratio = 1.00 indicates no forgetting.) Asterisks indicate that all groups displayed
retention (M baseline ratio significantly > 1.00).

programmed their intersession intervals in either an expanding series (days 0–

2–8) or a constant series (Days 0–4–8). As in Landauer and Bjork (1978), the
mean interval between successive retrievals (i.e., sessions) was the same for
both groups (M = 4 days). During a delayed recognition test 3 weeks after the
final session, the expanding-series group exhibited excellent retention, but the
constant-series group exhibited none.
Using the response-to-novelty task, Cornell (1980) familiarized 5-month-
olds with two photographs of the same face, presented side-by-side, for four
trials. Each familiarization trial lasted until infants had looked at the face for a
total of 5 s. In the massed condition, successive trials were separated by 3 s,
and in the distributed condition, they were separated by 60 s. Infants in both
spacing conditions received a paired-comparison recognition test either 5 s, 1
min, 5 min, or 1 hour after the final familiarization trial. Infants who were
tested 5 s after familiarization exhibited a significant novelty preference in
both conditions, but after longer delays, only infants in the distributed condi-
tion exhibited a significant novelty preference.

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162 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

6. Exposure or Study Time. The total time law is a widely-accepted

principle in human memory. This law states that the degree to which an item is
recalled is a direct function of its total study time, irrespective of the manner in
which that time was distributed (Cohen 1985; Cooper & Pantle 1967; for
review, see Crowder 1976). In addition, the amount of perceptual processing
that can be completed at the time of encoding is constrained by the length of
time a stimulus is physically available to the perceiver. As stimulus exposure
time increases, the perceiver should be able to extract more perceptual infor-
mation from the stimulus. In general, studies with adults find that neither study
time nor stimulus exposure time affects measures of implicit memory, but
both affect measures of explicit memory. Greene (1986), for example, found
that the duration of rehearsal had no effect on memory performance in a word-
stem completion task but significantly improved memory performance on a
recall task. Similarly, von Hippel and Hawkins (1994, Experiment 1) mea-
sured retention in three implicit tasks (word-fragment completion, perceptual
identification, and general knowledge) and found that increasing stimulus
exposure time had no effect on implicit conceptual memory performance
when the encoding task focused on perceptual features of the stimulus. Other
researchers have also reported that increasing stimulus exposure time has no
effect on performance in either a perceptual identification task (Jacoby
& Dallas 1981) or a word-fragment completion task (Neill, Beck, Bottalico &
Molloy 1990) but improves performance in explicit memory tasks (Debner
& Jacoby 1994; Jacoby & Dallas 1981; Neill et al. 1990), including the free
recall of word lists (Roberts 1972b).
Using nonverbal stimulus materials, Schacter et al. (1991a) exposed
adults to either single or multiple presentations of visual objects and measured
their memory performance in an object decision task — presumably, a test of
implicit memory. With an exposure duration of 5 s, a single exposure was as
effective as multiple exposures in facilitating priming. With an exposure
duration of 1 s, however, multiple exposures led to significant priming, but a
single exposure did not. When Musen (1991) increased the duration of a single
exposure of a novel visual figure from 1 s to 10 s, however, she found that
performance on a priming task was not affected, but recognition performance
was significantly enhanced.
Using a deferred imitation task and a cued-recall test with 6-month-olds,
Barr et al. (1996) similarly found no evidence of imitation after a 24-hour
delay in a cued-recall test when infants were exposed to the demonstrator for

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MEMORY DISSOCIATIONS IN INFANTS 163

only 30 s. When the exposure period was increased to 60 s, however, infants’

24-hour deferred imitation was excellent.
In mobile studies with 3-month-olds, increasing the study time similarly
enhances performance on a delayed recognition test. Figure 7.16, for example,
shows that infants receiving a single session lasting 6 or 9 min failed to
recognize the original mobile 1 week later; however, infants displayed signifi-
cant recognition for 1 week if given a 12-min session and for 2 weeks if given
an 18-min session (Ohr et al. 1989).
In studies with 3-month-olds, infants were exposed to a novel mobile for
either 180 s or 10 s immediately after training. On a delayed recognition test
24 hours later, the 180-s exposure interfered with recognition of the original
mobile and led infants to treat the exposed mobile as if they had actually been
trained with it; the 10-s exposure, however, produced these effects on a
delayed recognition test after 1 hour but not after 24 hours (Bhatt 1997). No
reactivation (priming) data are available from any of the infant studies of
exposure duration; however, those who claim that very young infants possess
only an implicit memory system would probably concede that exposure

Figure 7.16. The effect of study time (session duration) on the magnitude of delayed
recognition of independent groups of 3-month-olds tested 7, 14, or 21 days later. Asterisks
mark groups that displayed retention (M baseline ratio significantly > 1.00).

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164 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

duration has no effect on a priming (implicit memory) test. It is the strong

effect of exposure duration on infants’ performance on a delayed recognition
(explicit memory) test for which they cannot account.
7. Number of Studied Items. Mandler (1985) characterized non-automatic
memories as capacity demanding and distinguished them from automatic
memories with no capacity demand. Although he eschewed the explicit-
implicit distinction, similar differences in capacity demand have been found to
affect performance in explicit and implicit memory tasks, respectively. Thus,
for example, increasing the number of studied items produces a dissociation in
both adult and infant memory performance on recognition and priming tasks.
In studies with adults, increasing the number of studied items decreases
performance on explicit memory tasks but does not affect performance on
implicit memory tasks.
It is well documented that adding new items to a study list impairs
subsequent retention in free-recall, cued-recall, and recognition tasks (Atkinson
& Joula 1973; Ratcliff & Murdock 1976; see Crowder 1976, for review). Reinitz
and Demb (1994), for example, had college students study a list of compound
words and then tested them with old words, recombined words, compound
words in which either the first or second parts were new, and completely new
words on either an old/new recognition test or on a perceptual identification test
(each word presented for 40 ms, followed by a 300-ms mask). On the recogni-
tion test, the number of false recognitions increased with the number of studied
components. On the perceptual identification task, however, priming occurred
only for old words; identification of the other test items was poor irrespective
of the number of previously studied components. Mitchell and Brown (1988)
similarly found that the magnitude of repetition priming was not affected by the
number of studied items or list size.
In a mobile study with 2- and 3-month-old infants, the number of studied
items was defined in terms of the number of different types of blocks on the
training mobile — all five mobile blocks were identical, or each was different
(Rovee-Collier et al. 1989). At both 2 and 3 months of age, performance on a
24-hour delayed recognition test was better when the list was shorter (i.e.,
when all objects on the mobile were the same), but the magnitude of retention
following a reactivation treatment administered 3 weeks after training was
unaffected by the number of studied items (see Figure 7.17).
A similar effect on delayed recognition was found when infants were
trained with mobiles containing different numbers of feature combinations.

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MEMORY DISSOCIATIONS IN INFANTS 165

Figure 7.17. The effect of the number of different objects (studied items) on the training
mobile on the magnitude of delayed recognition 1 day after training (left panel) and the
magnitude of reactivation (right panel) 3 weeks after training at 2 and 3 months of age. (A
retention ratio = 1.00 indicates no forgetting.) Asterisks mark groups that displayed
retention (M baseline ratio significantly > 1.00).

Three-month-olds were trained with a six-block mobile containing either two

sets of feature combinations (i.e., three blocks per set) or three sets of feature
combinations (i.e., two blocks per set). For infants in the two-set group, three
mobile blocks displayed red As on a black background, and three displayed
green 2s on a yellow background; for infants in the three-set group, two blocks
each displayed the preceding feature combinations, and two displayed brown
Xs on a blue background. During the 24-hour delayed recognition test, one of
the features was switched or recombined between the sets. Infants trained with
two sets of features, for example, were tested with a figure-color recombina-
tion (green As on a black background and red 2s on a yellow background), a
figure recombination (red 2s on a black background and green As on a yellow
background), or a background color recombination (red As on a yellow
background and green 2s on a black background). If infants discriminated that
the features had been recombined, then this was taken as evidence that they
had learned which training features belonged together. Otherwise, this was
taken as evidence that they recognized the features but did not remember
which features went with which others.

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166 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

In fact, infants who were trained with two sets of features discriminated
the recombinations (Bhatt & Rovee-Collier 1994, 1996), but infants who were
trained with three sets of features did not (see Figure 7.18, left panel), al-
though they did discriminate mobiles on which one of the test features was
novel (Bhatt & Rovee-Collier 1997). Even though they had not discriminated
a feature recombination during the delayed recognition test, however, only the
original mobile reactivated the forgotten memory 2 weeks later; a mobile
displaying feature recombinations did not (see Figure 7.18, right panel). This
is yet another instance of an infant memory dissociation on recognition and
reactivation tests.
Finally, Gulya et al. (1998) trained 6-month-olds to kick using a serial list
composed of three different mobiles. Infants successively viewed each mobile
for 2 min per session for three sessions. Infants subsequently recognized the

Figure 7.18. Left panel: The 24-hour delayed recognition performance of 3-month-olds
who were tested with a mobile displaying three sets of features either in their original
combinations (no change) or in new combinations (3-recomb). Right panel: The magnitude
of reactivation following priming with a mobile displaying three sets of features either in
their original combinations (no change) or in new combinations (3-recomb). Asterisks
mark groups that displayed retention (M baseline ratio significantly > 1.00).

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MEMORY DISSOCIATIONS IN INFANTS 167

test mobile from serial position 1 but not the mobiles from serial positions 2
and 3 during a 24-hour delayed recognition test — a classic primacy effect
(see Figure 7.19, left panel). When the number of mobiles on the study list was
increased from three to five, however, the primacy effect disappeared during
the 24-hour test. Instead, infants recognized mobiles from all serial positions
but failed to recognize a mobile that had not been on the study list (see
Figure 7.19, right panel). Here, the impairing effect of increasing the number
of studied items on infants’ memory for serial order was manifested as a
paradoxical increase in test responding. This increase, however, reflected the
fact that infants still recognized all of the items on the study list but, as
evidenced by elimination of the primacy effect, no longer remembered their
original serial order. A similar result was obtained with adults by Murdock
(1962), who found that increasing the number of words on the study list
impaired adults’ memory for order but not item information.

Figure 7.19. The 24-hour delayed recognition performance of independent groups of 6-

month-olds who were tested with mobiles from the first, middle, and last serial positions of
a three-mobile list (left panel) and a five-mobile list (right panel). Infants trained with both
lists failed to recognize (i.e., discriminated) a novel test mobile. Asterisks mark groups that
displayed retention (M baseline ratio significantly > 1.00).

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168 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

8. Level of Processing. Level of processing (LOP) is an encoding variable

that affects performance on implicit and explicit memory tasks differently. In
their original exposition, Craik and Lockhart (1972) suggested that the dura-
tion of a memory was determined by the level or depth at which the perceptual
input for that memory was processed. Thus, the shallower processing of
phonemic and orthographic features (e.g., searching for specific letters in a
word) should lead to a shorter duration of retention, while the deeper process-
ing required by the generation of a verbal associate or a semantic orienting
task (e.g., rating the pleasantness of words on a study list) should lead to a
longer duration of retention. Since that time, a number of other hypotheses and
theories have been advanced. Craik and Tulving (1975), for example, attrib-
uted retention differences to the degree of stimulus elaboration instead of to
differences in processing depth during encoding, retaining the term “depth” to
refer to “degree of semantic involvement.” Others introduced terms such as
meaningfulness, differentiation, integration, distinctiveness, and so forth (for
review, see Tulving 1983) in attempts to explain encoding difficulty in terms
of a single factor.
In memory studies with adults, manipulations of LOP have been found to
produce strong effects on explicit tests but none on implicit tests (Besson,
Fischler, Boaz & Raney 1992; Graf et al. 1982, 1984; Moscovitch 1994;
Roediger, Weldon, Stadler & Riegler 1992). One of the earliest demonstra-
tions of this dissociation was reported by Jacoby and Dallas (1981). They
asked college students to answer three yes/no questions about each word on a
long list and then assessed their retention on either a perceptual identification
task (an implicit memory task) or a recognition task (an explicit memory task).
The questions pertained to the letters in the word, a rhyme question (both,
shallow encoding conditions), or the meaning of the word (a deep encoding
condition). Initially, each question was presented on a screen for 1 s and then
was replaced by the target word, which remained on the screen until the
student answered the question. During the recognition test, words were pre-
sented for 2 s each, and students responded “yes” to those that had been
presented in the first phase and “no” to those that were new. During the
perceptual identification test, words were simply flashed on the screen and
students reported each word immediately. Jacoby and Dallas found that the
semantic question had longer reaction times than the other two questions, and
“no” responses took longer than “yes” responses. On the recognition memory
test, the probability of a hit (a correct word identification) was significantly

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MEMORY DISSOCIATIONS IN INFANTS 169

higher for semantic questions and questions requiring a “yes” response; on the
perceptual identification test, however, neither question type nor whether the
question required a “yes” or “no” answer affected the probability of a hit.
Although there was no effect of LOP, presentation of a word in the first phase
did produce a significant priming effect in the second phase: Perceptual
identification was significantly enhanced when test items were old; moreover,
the amount of priming was the same whether recognition memory was very
poor or near-perfect.
Examples of the dissociation produced by LOP manipulations have also
been reported in the developmental literature. Carroll et al. (1985) presented a
list composed of pictures to 5-, 7-, and 10-year-olds and a group of adults,
instructing participants either to search for pictures marked with a cross (the
shallow encoding condition) or to judge the weight of the objects that were
pictured (the deep encoding condition). At each age, performance was mea-
sured on both a recognition test (explicit memory task) and a naming test
(implicit memory task). As expected, recognition improved with age. In
addition, however, picture recognition was better in the deep than in the
shallow encoding condition, but the priming measure was unaffected by either
age or encoding condition. Lindberg (1980, Experiment 1) found that explicit
memory performance (free recall) significantly increased from kindergarten to
adulthood following elaborative encoding but not after physical encoding.
Naito (1990) replicated this result and extended the analysis to implicit memory
performance. She found no effect of encoding condition (orthographic or
elaborative encoding) on performance in the implicit word-completion test for
6-, 8-, and 11-year-olds and college students. Memory performance on the
explicit free-recall test, however, was significantly better with elaborative
encoding at all but the youngest age (see Chapter 4).
Adler et al. (1998) obtained a robust effect of LOP on 3-month-old
infants’ memory performance in a delayed recognition task. Infants’ attention
during encoding was enhanced by training them with a pop-out display
composed of a single target (L or +) amidst six distractors (+s or Ls, respec-
tively). This display is thought to enhance attention to the target at the expense
of attention to the distractors (see Figure 7.20).
In Experiment 1, infants who were tested with a mobile composed
entirely of targets or distractors recognized both the original target and the
original distractors during a 24-hour delayed recognition test, confirming that
both were encoded during training. In Experiment 2, infants who were trained

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170 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 7.20. One of the pop-out mobiles that was used with 3-month-olds to enhance
attention during training. The single target (+) amidst six distractors (Ls) stood out from the
display and captured infants’ attention. As a result, infants tested with a mobile displaying
seven +s remembered it longer than infants whose training mobile displayed seven +s in the
first place (see Figure 6.4a).

with the single L target amidst six + distractors recognized a test mobile
displaying seven Ls after delays more than twice as long as infants who were
originally trained with a mobile composed of seven Ls; conversely, the delay
after which infants trained with the pop-out mobile recognized a test mobile
displaying seven +s was less than half as long as that of controls who were
originally trained with a mobile composed of seven +s (Adler & Rovee-
Collier 1994). Finally, Experiment 3 demonstrated that the retention advan-
tage gained by enhancing infants’ attention with a pop-out mobile was not
specific to the particular character that had been used as the target during
encoding. Experiment 2 was replicated even when the characters that served
as target and distractors were reversed. These results were consistent with the

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MEMORY DISSOCIATIONS IN INFANTS 171

adult findings that increasing attention to an item during encoding increases its
depth of processing and thereby protracts its retention on an explicit memory
task (see Figure 7.21).
Training and priming 3-month-olds with a pop-out mobile, however, did
not differentially affect the magnitude of their retention following a reactiva-
tion treatment. Rather, the magnitude of reactivation was the same as when
they were trained and primed with a homogeneous mobile--results consistent
with the effect of LOP on implicit memory tasks used with adults.

Figure 7.21. The LOP effect at 3 months of age shown as the protracted recognition over
days of +s (left panel) and Ls (right panel) when they were the target (white columns) on the
pop-out training mobile. Also shown is the maximum duration of retention of control
groups (striped columns) who were trained with a homogeneous + or L mobile, respec-
tively, and the diminished recognition over days of +s and Ls when they were the distractors
(dark columns) on the L or + pop-out training mobile, respectively. The corresponding
control group for the distractors was trained with a homogeneous mobile displaying the
same character as the distractor. (A retention ratio = 1.00 indicates no forgetting). Asterisks
mark groups that displayed retention (M baseline ratio significantly > 1.00).

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172 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

9. Affect. Most of the research on the role of affect in retention has

focused either on the congruence of the mood during encoding and retrieval or
on the congruence between the nature of the mood at the time of retrieval and
the nature of what is retrieved (e.g., Bower 1981; Eich, Macaulay & Ryan
1994; for review, see Blaney 1986). Recently, researchers have begun to
explore the contribution of affect to memory performance on implicit and
explicit tests (Denny & Hunt 1992; Hertel & Hardin 1990; Macaulay, Ryan &
Eich 1993; Watkins, Mathews, Williamson & Fuller 1992). Research with
both normal adults and adult patient populations has demonstrated that perfor-
mance on explicit tests is sensitive to affect, but performance on implicit tests
is not (Tulving 1983).
Using a between-subjects measure, Hertel and Hardin (1990) queried
nondepressed (scores < 6 on the Beck Depression Inventory; Beck, Ward,
Mendelson, Mock & Erbaugh 1961) and naturally depressed (BDI scores > 6
and < 9) college students about the uncommon meanings of homophones,
gave them depressive- or neutral-mood inductions, and then tested both their
spelling (an implicit task) and their recognition of old and new homophones.
Neither induced nor naturally-occurring depression affected spelling, but both
impaired recognition of the old homophones. Watkins et al. (1992) assessed
memory for affectively valenced words with adults who were clinically diag-
nosed with major depression or dysthymia (BDI scores > 19; M BDI score =
27.53) or were normal (BDI scores < 8, M BDI score = 3.71). Relative to
nondepressed adults, depressed adults’ performance on a cued-recall test was
impaired, but the two groups performed equivalently on a word-completion
test. Similarly, Denny and Hunt (1992) found that the free recall of affectively
valenced words was impaired in a clinically depressed patient population
relative to nondepressed adults, but the two groups performed equivalently on
a word-fragment completion test.
In mobile studies with 3-month-olds, Fagen and his colleagues have
repeatedly found that infants’ delayed recognition is highly sensitive to affect,
but their memory performance in a reactivation task is not (for review, see
Fagen & Prigot 1993). In these studies, infants were typically trained for two
sessions with a 10-object mobile and then were shifted to a nonpreferred 2-
object mobile during a final session. In response to the shift, approximately
50% of the infants usually cried. During delayed recognition tests either 1 day
or 1 week later, noncriers exhibited excellent retention irrespective of whether
they were tested with the 10-object or 2-object mobile, while criers recognized

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MEMORY DISSOCIATIONS IN INFANTS 173

the test mobiles after a 1-day retention interval but not after a 1-week delay
(see Figure 7.22, left panel; Fagen, Ohr, Singer & Klein 1989). Despite the
impaired performance of criers on the 1-week delayed recognition test, when a
reactivation treatment was administered 3 weeks after the conclusion of
training, all infants exhibited the same magnitude of reactivation 1 day later
whether they had cried after a mobile shift or not (see Figure 7.22, right panel;
Fagen, Ohr, Fleckenstein & Ribner 1985).
Singer and Fagen (1992) repeated this procedure but used a measure of
infants’ facial expressions of affect (AFFEX; Izard, Dougherty & Hembree
1980) in addition to crying. Following the shift to the 2-object mobile, criers
exhibited decreasing amounts of interest expressions and increasing amounts
of anger and sadness expressions. During the 1-day recognition test, criers
again displayed significantly more anger expressions than noncriers, but
during the 7-day recognition test, they displayed none. In addition to provid-

Figure 7.22. The effect of crying on the magnitude of delayed recognition 1 day or 7 days
after training (left panel) and the magnitude of reactivation (right panel) 3 weeks after
training at 3 months of age. Asterisks mark groups that displayed retention (M baseline ratio
significantly > 1.00).

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174 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

ing a convergent measure of affect, these data confirmed that the poor perfor-
mance of criers during the 1-week test was not simply a result of their refusal
to participate in the task but an instance of true forgetting (Fagen & Prigot
1993).
Finally, the interval between training with the preferred (preshift) mobile
and training with the nonpreferred (postshift) mobile is an important determi-
nant of the degree of impairment in infants’ delayed recognition performance
(Fagen et al. 1989). When a delay of 0, 2, 5, or 15 min was interpolated
between infants’ exposure to the pre- and post-shift mobiles, criers again
failed to recognize the test mobile 1 week later; when the interpolated delay
was increased to 30 min, however, their performance on the delayed recogni-
tion test was excellent. The performance of noncriers on the 1-week test, by
comparison, was excellent after all pre- to post-shift delays.
The preceding studies with infants were based on between-subjects mea-
sures, as in the Hertel and Hardin (1990) study with adults. For both age
groups, affect differentially affected the magnitude of recognition but not the
magnitude of reactivation (priming). Within-subjects measures of preference
yield the same result but in a slightly different form. In studies with adults,
implicit preference is associated with familiarity: Individuals prefer items that
were on the original study list even though they cannot recognize them. Engen
and Ross (1973), for example, asked college students to indicate whether
different odors were familiar or unfamiliar and whether they liked, disliked, or
were indifferent to each odor. On this implicit test, students were more likely
to like the odors that they had said were familiar and to either dislike or be
indifferent to the odors that they had said were unfamiliar. Of the familiar
odors, for example, 46% were rated like, whereas of the unfamiliar odors, only
11% were. After delays of 1, 7, or 30 days, they gave students a forced-choice
(explicit) recognition test in which odors from the original study list were
pitted against new odors. Students’ accuracy of recognition was unrelated to
whether they had initially classified the odors as familiar. Using a slightly
different procedure, Kunst-Wilson and Zajonc (1980) similarly found that
adults preferred visual stimuli that they had previously seen relative to new
ones, even though the stimuli were exposed for durations too brief to be
recognized.
Using a between-subjects design, Wilk, Klein and Rovee-Collier (2000)
obtained a similar result. They trained 3-month-olds with a particular mobile
and gave them a delayed recognition test in which the original mobile and a

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MEMORY DISSOCIATIONS IN INFANTS 175

novel one were simultaneously presented either 1 day or 4 days later. During
testing, they measured both kicking and looking. Typically, 3-month-olds
exhibit no retention if tested exclusively with a novel mobile 1 day after
training, but they exhibit near-perfect retention if tested exclusively with the
training mobile after the same delay (Hayne, Greco, Earley, Griesler &
Rovee-Collier 1986). As the interval between training and testing increases,
however, 3-month-olds increasingly respond to a novel test mobile, and by 4
days after training, they kick as robustly to a novel mobile as to the training
one (Rovee-Collier & Sullivan 1980). The latter data are taken as evidence
that infants gradually forget the specific details of their training mobile until,
after 4 days, they cannot discriminate between them. In the Wilk et al. study,
as expected, infants exhibited significant recognition 4 days after training.
Despite prior evidence that they cannot discriminate between these test mo-
biles after 4 days on the kicking measure, however, infants also looked
proportionally longer at the original mobile than at the new one after both test
delays. Thus, as in the Kunst-Wilson and Zajonc (1980) study with adults,
although infants do not discriminate the new mobile from the old one after 4
days on the kicking measure, they do discriminate them on the looking
measure, implicitly preferring to look at the familiar mobile.
10. Serial Position. The serial position of items on a study list has long
been known to produce strong and persistent primacy and/or recency effects
on immediate tests of free recall, cued recall, and recognition memory (e.g.,
Bousfield, Whitmarsh & Esterson 1958; Gershberg & Shimamura 1994;
Murdock 1962; Wright et al. 1985). A handful of researchers have found
recency effects on implicit tests of both word-stem completion (McKenzie &
Humphries 1991; Rybash & Osborne 1991) and word-fragment completion
(Sloman et al. 1988), but Brooks (1994) observed that the instructions and
procedures in these reports were either suspect or reported in insufficient
detail.
Two laboratories have recently used the same study instructions and test
stimuli but different instructions for the implicit and explicit tests. Gershberg
and Shimamura (1994) obtained inconsistent evidence for primacy and recency
effects across three experiments. Implicit word-stem completion tests, for
example, yielded a primacy effect in two experiments and a recency effect in
one, and these effects were highly transient when they did occur. Different
explicit tests (word-stem cued recall, free recall) also yielded inconsistent
primacy and/or recency effects across experiments. Using word-stem comple-

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176 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

tion and word-stem cued-recall tests with normal adults, Brooks (1994) found
primacy effects on an explicit test in two experiments and, when the last items
studied were the first ones tested, a recency effect in the second of these. In
neither experiment, however, did serial position affect performance on the
implicit test. Taken together, the data indicated that the serial order of the items
on the study list had no effect on performance in implicit tests but produced a
primacy effect in explicit tests. Finally, in two experiments with Korsakoff and
nonKorsakoff amnesic patients, both patient groups performed more poorly
than controls on tests requiring the recall, recognition, and sequencing of words
and facts (Shimamura, Janowsky & Squire 1990).
Delayed recognition tests with both 3- and 6-month-olds also reveal a
strong and persisting primacy effect (Gulya et al. 1998; Merriman, Rovee-
Collier & Wilk 1997). Independent groups of infants were trained with a list
composed of three different mobiles for 2 min each for 3 successive days and
were given a recognition test 24 hours later with either a mobile from one of
the three serial positions or a completely novel mobile. Infants of both ages
responded only to the test mobile in serial position 1–a strong primacy effect
(see Figure 7.23, left panel). In a follow-up study (see Number of Studied
Items), when the number of mobiles on the original list was increased from
three to five, the primacy effect was eliminated, and infants recognized all of
the mobiles on the 24-hour delayed recognition test. Even so, they still
discriminated a novel test mobile that had not been on the study list (Gulya et
al. 1999).
Gulya et al. (1998) conjectured that infants who had been trained with the
three-mobile list in the initial study had failed to recognize the test mobiles
from serial positions 2 and 3 because those mobiles were out of order when
they had been presented singly to independent groups of infants at the time of
testing. (Recall that infants had always seen the mobile from serial position 1
first at the outset of each daily training session.) In addition, they observed that
a single mobile is not a retrieval cue for serial order, which entails relational
information and hence requires two cues (i.e., this-before-that or this-after-
that). Therefore, they primed 3- and 6-month-old infants who had been trained
on a three-mobile list with the mobile from the preceding serial position
immediately before the 24-hour test. This priming task was procedurally
identical to word-stem and word-fragment completion tasks used in priming
studies with adults except that the materials were not verbal. Although they
had failed to recognize the mobile from serial position 2 on the delayed

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MEMORY DISSOCIATIONS IN INFANTS 177

Figure 7.23. The effect of the serial position of mobiles on a three-mobile list on the
magnitude of delayed recognition (left panel) and the magnitude of reactivation (right
panel) 24 hours after training at 3 months of age. The delayed recognition function (left
panel) shows a classic primacy effect which was eliminated when mobiles in serial
positions 2 and 3 were primed with mobiles from the preceding serial position(s) immedi-
ately before the test (right panel). Asterisks mark groups that displayed retention (M
baseline ratio significantly > 1.00).

recognition test, this time infants of both ages responded to the test mobile
from serial position 2 on the 24-hour test when they were initially primed with
the mobile from serial position 1–the familiar explicit-implicit dissociation
(see Figure 7.23, right panel). If infants were primed with the mobile from
serial position 3, however, they still did not recognize it. In addition, even
though infants of both ages had failed to recognize the mobile from serial
position 3 after 24 hours, when they were successively primed immediately
before the test with the mobiles from serial positions 1 and 2 for 1 min each,
they did respond to the mobile from serial position 3–again, the familiar
explicit-implicit dissociation. When primed for 2 min with the mobile from
serial position 1, however, they failed to respond to the test mobile from serial

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178 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

position 3. These data demonstrated that only valid order cues were effective
memory primes at both 3 and 6 months of age, whereas invalid order cues
were not. This result confirmed that even though infants of both ages had
previously failed to recognize the same mobiles, they responded selectively to
a valid order prime on the basis of their prior training experience.
Using a response-to-novelty task, Cornell and Bergstrom (1983) familiar-
ized independent groups of 7-month-olds during multiple study periods with a
serial list composed of three photographs of adult female faces that were
spaced by 1 s. Infants received a paired-comparison test with a preexposed and
a novel face after delays of 5 s, 1 min, or 5 min. As in recognition studies with
adults (Crowder 1976; Wright et al. 1985), Cornell and Bergstrom obtained a
classic U-shaped serial position effect with both primacy and recency effects
after the shortest delay (5 s) and a persisting primacy effect after the longest
delay (5 min). This result resembles that of Merriman et al. (1997) and Gulya
et al. (1998), who also found only a primacy effect after a long delay (24
hours) when 3- and 6-month-olds were trained and tested on a three-item list
in the mobile procedure.
11. Studied Size. Ungerleider and Mishkin (1982) conjectured that the
memory system represents objects in two separable representations — one that
is size-sensitive and one that is size-invariant — which function in different
situations. In studies with normal adults and amnesic patients, changes in the
studied size of an object at the time of testing impair performance on recogni-
tion memory tasks (Biederman & Cooper 1992; Jolicoeur 1987; Milliken &
Jolicoeur 1992; Schacter, Cooper & Treadwell 1993b) and object decision
(Cooper, Schacter, Ballesteros & Moore 1992; Schacter et al. 1991a) tasks, but
these same study-to-test size changes do not affect priming on either object
naming tasks (Biederman & Cooper 1991, 1992) or object decision tasks
(Schacter, Cooper, Tharan & Rubens 1991b; Schacter et al. 1993b), whether
the objects are novel or familiar.
Biederman and Cooper (1992), for example, presented adults with a set of
line drawings of common objects and asked them to identify the objects.
Following their first exposure, adults who performed a recognition task (same/
different judgment) were slower to recognize previously viewed objects at a
new size than previously viewed objects that were the same size as in the first
exposure. When asked simply to name the objects on their second exposure,
however, the amount by which their naming latency was facilitated by the
prior exposure was the same whether the objects’ size was changed between

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MEMORY DISSOCIATIONS IN INFANTS 179

exposures or not. The facilitative effect of the prior presentation of an item on

memory performance is taken as an indication of priming (Tulving & Schacter
1990). Biederman and Cooper interpreted these findings as indicating that
separate memory systems, one sensitive to size (size-sensitive) and the other
not (size-invariant), were accessed by the two different tasks. These systems,
they suggested, corresponded to explicit and implicit memory, respectively
(Musen & Treisman 1990; Schacter 1987; Tulving & Schacter 1990).
Cooper et al. (1992) obtained similar results using an object decision task.
Adults judged the direction each object faced on its first exposure and,
following a delay, received either a recognition task (old/new judgment) or a
possible/impossible object (perceptual) decision task. The size of the objects
was manipulated between the first and second exposures. Like Biederman and
Cooper (1992), Cooper et al. (1992) found that adults’ latency to recognize old
objects at a new size was substantially slower than their latency to recognize
old objects at their original size. Performance on the object decision task,
however, was not sensitive to size. Adults showed equal priming whether the
possible objects were presented at the studied size or at a different one
(impossible objects showed no priming). Also like Biederman and Cooper,
Cooper et al. (1992) attributed this dissociation to two, functionally different
memory systems — an episodic system in the case of the recognition task, and
a semantic system in the case of the object decision task. A similar dichotomy
in memory performance on recognition and priming tasks has been found for
other stimulus dimensions as well, including color, pattern, contrast, illumina-
tion, reflection, and translation (Biederman & Cooper 1991; Cave, Bost &
Cobb 1996; Cooper et al. 1992; Srinivas 1996).
Cave et al. (1998) found that binocular rivalry suppressed repetition
priming in a picture-naming task. This was not due to a general reduction in
attention during suppression — focal attention is not necessary to elicit priming
(Stankiewicz, Cooper & Hummel 1994), and divided attention has little or no
effect on repetition priming (Mulligan 1997; Mulligan & Hartman 1996).
Rather, the binocular suppression disrupted neural events at an early stage of
visual processing, erasing the target (as well as the prime), which is normally
visible, from consciousness for several seconds at a time. This, in turn,
prevented the local features of the object representation from being
(re)assembled into meaningful global figures or objects during a late, high-
level processing stage, although they were registered. In other words, priming
must transpire at a stage of visual processing that is subsequent to the early

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180 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

stage, where binocular suppression occurs, and during which relatively ab-
stract object representations are registered (Cave et al. 1996; Tulving &
Schacter 1990). Because priming occurs for visual stimuli that never enter
conscious awareness (Kihlstrom, Schacter, Cork, Hurt & Behr 1990; Kunst-
Wilson & Zajonc 1980; Mandler, Nakamura & Van Zandt 1987), this stage of
processing must be intermediate between the stage that mediates suppression
and the stage that supports conscious visual awareness.
The same dissociation — impaired recognition but preserved priming —
has been obtained with 3-month-olds in delayed recognition and reactivation
tests, respectively, following transformations in studied size. In an initial
study, infants who were trained with a mobile composed of seven pink blocks
with a computer-generated black L on each side exhibited excellent retention
in a 24-hour delayed recognition test with the same characters (the control
group); when tested with Ls that were either reduced or increased in size by
25%, however, infants’ performance on the delayed recognition test was
significantly impaired (Adler & Rovee-Collier 1994). In a follow-up study,
Gerhardstein et al. (2000) asked whether 3-month-old infants show a memory
dissociation on delayed recognition and reactivation tests analogous to the
dissociation exhibited by adults on size-sensitive (explicit) and size-invariant
(implicit) memory tests. They found that the 24-hour delayed recognition
performance of 3-month-olds who were trained with a mobile displaying +s of
a particular size was significantly impaired when they were tested with +s that
were either reduced or increased in size by 33% (see Figure 7.24, left panel).
In contrast, their magnitude of retention following a reactivation treatment
with mobiles displaying identically size-transformed +s was unaffected by
whether the +s used to prime the memory were larger or smaller than the +s
they saw during training (see Figure 7.24, right panel). In each case, controls
who were trained and either tested 24 hours later or primed 2 weeks later with
a mobile displaying characters of the same size exhibited excellent retention.
The finding that 3-month-olds, like normal adults, show preserved prim-
ing across size transformations and, also like normal adults, are sensitive to
size transformations on same/different recognition tests suggests that the same
memory systems mediate their memory performance.
12. Memory Load. The term memory load has been used with reference to
both the length of the retention interval (i.e., longer test delays creating a
greater memory load; Quinn & Eimas 1996) and the amount of information that
must be retained (Mandler 1985). Both usages were considered earlier (see

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MEMORY DISSOCIATIONS IN INFANTS 181

Figure 7.24. The effect of changing the size of the training character by 33% on the
magnitude of delayed recognition 24 hours after training (left panel) and the magnitude of
reactivation (right panel) 3 weeks after training at 3 months of age. The performance of no-
change control groups who were trained and either tested or primed with the original
character is also shown. Asterisks mark groups that displayed retention (M baseline ratio
significantly > 1.00).

Retention Interval and Number of Studied Items). Recall that in both instances,
increasing the memory load impaired memory performance on recognition
tests but not on priming tests. A third factor that affects the memory load is the
nature of the to-be-remembered information. For infants as for adults, for
example, relational information creates a greater memory load than absolute
information. Adler and Rovee-Collier (1994) reported that 3-month-old infants
could discriminate horizontal and vertical line segments (two textons) in
different spatial relations (L versus T) during a 1-hour delayed recognition test
but not during a 24-hour test. However, they could discriminate +s, which
contain a line crossing (a third texton), from both Ls and Ts during a 7-day test.
In addition, infants recognized Ls and Ts for only 3 days, but they recognized
+s for 7 days. These data illustrate the predicted memory dissociation: Abso-
lute information (texton number) was remembered longer than relational
information (spatial arrangement) on delayed recognition tests. Infants’ mag-

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182 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

nitude of reactivation, however, was equivalent when exactly the same stimuli
were used as memory primes with 3-month-olds (Rovee-Collier et al. 1992a)
and 6-month-olds (Bhatt, Rovee-Collier & Weiner 1994).
In the following studies, increasing the memory load also selectively
impaired infants’ retention of relational information on a delayed recognition
task but not on a reactivation task. In a sequel to the feature combinations
study described earlier (Bhatt & Rovee-Collier 1997; see Number of Studied
Items), 3-month-olds differentially forgot the correlations between different
training features (relational information) as the retention interval increased
from l day to 3 days, but they still recognized the individual features (absolute
information) and discriminated them from novel features on a delayed recog-
nition test after a 4-day retention interval (Bhatt & Rovee-Collier 1996).
When the number of feature sets on the training mobile was increased from
two to three, infants recognized the feature relations on the two-set mobile but
not on the three-set mobile during a 24-hour delayed recognition test. In a
reactivation task, however, the three-set mobile was an effective memory
prime 2 weeks later if it displayed the original feature combinations but not if
it displayed feature recombinations (Bhatt & Rovee-Collier 1997).
Finally, recall that 6-month-olds who were trained with a three-mobile
list had recognized only the mobile from serial position 1 — a classic primacy
effect — during a 24-hour delayed recognition test (see Figure 7.19, left
panel). When the length of the list was increased from three mobiles to five
mobiles, however, the primacy effect on the delayed recognition test disap-
peared (Figure 7.19, right panel; Gulya et al. 1999). In other words, increasing
the memory load impaired infants’ retention of order (relational) information
but not their retention of item-identity (absolute) information. Murdock
(1962) had similarly found that the primacy effect disappeared when the
number of words that were presented to adults on a study list was increased.
13. Context. The role of context in retention has been of interest to
psychologists for more than 2 decades, yet the term has been used in many
different ways (for review, see Clark & Carlson 1981). Broadly speaking, the
context refers to global aspects of the experimental environment, including
both external (the room, the experimenter, and the apparatus) and internal (the
inner state of the subject, including the pharmacological context, the mood or
affective state, or the point in the circadian cycle) conditions. However, the
context can also refer to the visual stimuli that surround or precede a target
object or the items that accompany the target item on each study trial, also

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MEMORY DISSOCIATIONS IN INFANTS 183

called the local context. In the latter situations, the context facilitates the
interpretation of the target stimulus. As a rule, retention is better when the
encoding and retrieval contexts are the same than when they differ (Cohen
1985; Spear 1978).
Tulving (1983) claimed that episodic memories included spatiotemporal
details, whereas semantic memories did not. Mandler (1985) rejected a mul-
tiple-memory-systems approach but similarly considered non-automatic (i.e.,
explicit) memories to be context-dependent and automatic (i.e., implicit)
memories to be context free. Neely (1989; Neely & Durgunoglu 1985),
however, concluded that the evidence for these distinctions was ambiguous.
Although a change in context between study and test has been shown to impair
adults’ memory performance on recognition and recall tests (Thomson &
Tulving 1970; Underwood & Humphreys 1979), the effect of a context change
on memory performance on implicit tests is less clear. Richardson-Klavehn
and Bjork (1988), for example, observed that small but persistent context
effects appeared over a wide range of perceptual identification (implicit
memory or priming) studies, even though the effects within a particular study
were often not significant.
Jacoby (1983) asked college students to read a list of words and then gave
them a perceptual identification test containing different proportions of words
from the previously read list. Their perceptual identification was facilitated by
the proportional overlap between the study and the test list. Likewise, Graf
and Schacter (1985) found a larger priming effect on a word-fragment
completion task when college students and amnesic patients were primed with
a word from a word pair on a prior study list (same context condition) than
with other words (different context condition), but this difference emerged
only when the study task required elaborative processing. More recently,
however, Allen and Jacoby (1990) determined that the priming effect on a
perceptual identification test was equivalent whether test words had been
generated during study (i.e., were easily recognized) or had only been read
(i.e., were poorly recognized). Changes in the modality of presentation
(Roediger & Blaxton 1987), the visual display of the target stimuli (Jacoby &
Dallas 1981), the environmental setting of encoding and retrieval (Graf 1988;
Smith, Heath & Vela 1990), the perceived sense or meaning of a word
(Lewandowsky, Kirsner & Bainbridge 1989), and mood (Macaulay et al.
1993) have also been reported to disrupt memory performance on implicit
tests.

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184 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

For many years, studies of context effects with young infants were
relatively sparse, probably because the brain structures responsible for repre-
senting information about the environmental context in adults were thought to
be functionally immature in infants younger than 8 or 9 months of age.
Research with both infant rats (Richardson, Riccio & McKenney 1988) and
human infants, however, subsequently challenged this belief. For 3-month-old
human infants, changing the context at the time of testing has no impact on
retention after a retention interval of 1 day (Butler & Rovee-Collier 1989;
Hayne, Rovee-Collier & Borza 1991) but impairs retention after longer delays
(Butler & Rovee-Collier 1989; Rovee-Collier, Griesler & Earley 1985a). At 6
months, a context change impairs retention after both 1 day and 3 days but has
no effect on retention after longer delays (Borovsky & Rovee-Collier 1990).
Training in one room and testing in another one has the same impairing effect
as training in the presence of a distinctive cloth panel and testing in the
presence of another one (Hartshorn & Rovee-Collier 1997).
In addition, memory reactivation is impaired by a context change at both
3 months (Butler & Rovee-Collier 1989; Hayne et al. 1991) and 6 months
(Borovsky & Rovee-Collier 1990; Hartshorn & Rovee-Collier 1997; Shields
& Rovee-Collier 1992). Two-month-olds have not been tested in an altered
context, but attempts have been made to enhance their long-term retention by
both training and testing them in a highly distinctive context (Rovee-Collier et
al. 1989). Although this manipulation facilitates retention in Korsakoff pa-
tients (Winocur & Kinsbourne 1978) and 3-month-olds (Butler & Rovee-
Collier 1989; Hayne & Rovee-Collier 1995), it does not facilitate retention in
2-month-olds.
In an initial study, 3-month-olds recognized the original mobile 1 week
after training in the original context but not in a different one, and the training
context alone — without the mobile — could reactivate the memory 2 weeks
after training, but a novel context could not (Rovee-Collier et al. 1985a).
Hayne and Findlay (1995) replicated the context-alone reactivation result after
delays of 3 and 4 weeks. If the original context, by itself, is an effective
retrieval cue, then it must have been represented in infants’ memory. Butler
and Rovee-Collier (1989) subsequently tested 3-month-olds after delays rang-
ing from 1 to 5 days with all combinations of cues and contexts that were the
same or different from training to testing. This study yielded three important
results. First, infants did not treat the cue and context as a stimulus configura-
tion. Had they done so, then changing either the cue or the context would have

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MEMORY DISSOCIATIONS IN INFANTS 185

impaired retention, but a context change did not impair retention during the 1-
day test. Second, the focal cue, an otherwise effective memory prime, was
rendered ineffective in a novel context. This result has been replicated many
times with both 3- and 6-month-olds. And third, a highly distinctive training
and test context facilitated discrimination of a novel test mobile from the
training mobile after delays when generalization to a novel mobile was seen in
its absence. This result reflects the disambiguating function of context when
the memory of the original cue is fuzzy (Bouton & Bolles 1985).
Butler and Rovee-Collier (1989) proposed a hierarchical, attention-gat-
ing model of memory retrieval, adapted from Reeves and Sperling’s (1986)
model of retrieval from visual short-term memory, to account for the role of
context in memory retrieval. According to their model, the memory represen-
tation of an event is organized hierarchically, with contextual information
occupying a relatively high node. Thus, attention to potential retrieval cues is
first filtered or screened at the level of the context, and perceptual identifica-
tion (an automatic or parallel process) of appropriate retrieval cues in the
context permits attention to flow to the next level (the focal cue). A mismatch
between the contextual information present during testing and that represented
in memory (i.e., a failure of perceptual identification), however, prevents the
attention gate from opening and blocks the flow of attention to the cue. As a
result, the retrieval process is terminated, and infants fail to recognize the cue
during the test. Like Reeves and Sperling, Butler and Rovee-Collier also
assumed that the attention gate might be partially opened under some circum-
stances, for example, if a partial match is made or if a sufficient number or
kind of critical retrieval cues are detected. The latter assumption was sup-
ported by findings that infants exhibit recognition if the test context contains
certain critical features that were present during initial encoding (Earley, Bhatt
& Rovee-Collier 1995; Rovee-Collier, Schechter, Shyi & Shields 1992b).
Context effects have now been studied in the mobile and train tasks with
infants over the entire first year of life (Hartshorn, Rovee-Collier, Gerhard-
stein, Bhatt, Klein et al. 1998a). These data revealed that a context change
impairs retention only at the end of the forgetting function at all ages except 6
months (Borovsky & Rovee-Collier 1990), when it impairs recognition for
only a few days after training only. In deferred imitation studies with 12- to
18-month-olds, infants similarly generalize across widely varying training-
test contexts after delays from 3 min to 4 weeks (Hanna & Meltzoff 1993;
Hayne et al. 2000a; Klein & Meltzoff 1999). At 6 months, however, a context

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186 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

change impairs 24-hour deferred imitation (Hayne et al. 2000a), just as it

impairs 24-hour delayed recognition in mobile studies at this age (Borovsky &
Rovee-Collier 1990; Shields & Rovee-Collier 1992).
The deleterious effect of a context change on delayed recognition can be
overridden by explicitly training infants in a different context in each session
(Amabile & Rovee-Collier 1991; Rovee-Collier & DuFault 1991) — a condi-
tion that has long been known to override the debilitating effect of a context
change on recall by adults (Pan 1926). The same effect has been obtained at 6
months of age by merely exposing infants briefly to a different context within
a day of training (Boller & Rovee-Collier 1992; Boller et al. 1996) and, at 3
months of age, by repeatedly reactivating the original memory (Hitchcock &
Rovee-Collier 1996). In the latter study, after forgetting was complete, infants
were initially primed with the original mobile in the original context, but their
last (either their second or third) reactivation treatment occurred in a different
context. During these subsequent reactivation treatments, their training
memory was successfully primed in the different context. Even during a third
reactivation treatment, however, the original memory could not be reactivated
by a different focal cue (the mobile) in the original context unless that
reactivation treatment occurred after a very long delay (i.e., 5 weeks after
training). Apparently, memory attributes become inaccessible over successive
retrievals, and those that represent contextual information are lost before those
that represent the focal cue (see also Riccio, Ackil & Burch-Vernon 1992).

Conclusions

The functional dissociations in infants’ memory performance in delayed

recognition and reactivation tasks exactly mirror the functional dissociations
that commonly distinguish two different memory systems in adults. Although
the infant data might be dismissed as merely reflecting dissociations within a
single (implicit) memory system, it is illogical to use evidence of the same
dissociations to argue for the existence of two different memory systems in
adults and only a single memory system in infancy. McDonough (cited in
Bower 1995, p. 86), for example, described infants’ memory performance in
the delayed recognition task with mobiles as “only procedural” (see also
Bauer 1996; Bauer & Hertsgaard 1993; Mandler 1984, 1990) because the
response that infants use to indicate recognition is initially learned via an

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MEMORY DISSOCIATIONS IN INFANTS 187

operant conditioning procedure. Similarly, Bauer (1996) dismissed evidence

from mobile studies of delayed recognition and memory reactivation as re-
vealing anything about infants’ ability
“…to construct and maintain accessible…memories …because the behaviors
from which they are derived do not meet the criteria for recall….Because the
participants of research on memory for experiences early in life are preverbal
or barely verbal, we are unable to query them to ensure their awareness that
their behaviors result from some previous experience. There is ambiguity,
then, as to whether the basis on which we infer memory, namely a change in
nonverbal behavior, results from conscious recollection or nonconscious
influence” (p. 30).

Both Bauer and McDonough take the position that deferred imitation is an
explicit memory task. Their approach to the study of memory development in
infants is to find a task that amnesics cannot solve, but normal adults can —
and use conscious recollection to do so (see Chapter 1). Because preverbal
infants can also solve a deferred imitation task, these investigators infer that
they must use conscious recollection to solve it as well. Deferred imitation per
se, however, is neither an explicit nor an implicit task; rather, the type of
memory task (either recognition/cued-recall or priming) in which it is used is
what determines the form of memory it yields. To date, however, only two
studies of deferred imitation have used a reactivation or priming (implicit
memory) task (Barr 1997; Barr & Vieira 1999); all others have used only
cued-recall (explicit memory) tasks.
In retrospect, the mobile and deferred imitation procedures are more
similar than they are different, as the form of the retention function obtained
with each procedure shows. Demonstrating target actions on a particular
object(s) is simply a way of introducing infants to the target information and
providing them with a nonverbal means of indicating whether they recognize
the specific test cue. Likewise, putting critical stimulus information on the
sides of the mobile blocks and reinforcing a distinctive response (a footkick)
in their presence is simply a way of introducing infants to the target informa-
tion and providing them with a nonverbal means of indicating whether they
recognize the specific test cue.
Because operant training in mobile studies (or exposure to the demonstra-
tion in deferred imitation studies) occurs prior to the introduction of the
manipulations that differentiate reactivation from delayed recognition tasks,
any subsequent performance differences in these tasks cannot be attributed to
how the response got into the infant’s behavioral repertoire in the first place.

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188 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Consider, for example, that even verbally proficient children and adults ini-
tially had to learn the verbal labels for the objects and patterns with which they
are subsequently tested in implicit and explicit memory tasks. Yet, thought is
rarely given to the specific manner in which these verbal labels were actually
acquired in the first place. Why? Because that information is unimportant in
accounting for adults’ functional dissociations in implicit and explicit memory
tasks. As this chapter documents, that same information is equally unimpor-
tant in accounting for infants’ functional dissociations in implicit and explicit
memory tasks.
We conclude that the functional memory dissociations that are exhibited
by preverbal infants, normal children and adults, and amnesics on priming and
recognition tasks are the same whether the target response was initially
acquired by operant conditioning, modeling (deferred imitation), familiariza-
tion (response-to-novelty), or verbal instructions (“study this list of nonsense
syllables”). Without exception, evidence from infant memory dissociations
reveals that the development of explicit and implicit memory is not hierarchi-
cal during the infancy period, hence is not described by the Jacksonian
principle. In terms of multiple memory systems, these data reveal that the
memory systems that support implicit and explicit memory are both present
from early in infancy.

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CHAPTER 8

Structural and Processing Accounts of

Memory Dissociations

In this chapter, we consider some of the major theoretical accounts that have been advanced
to explain the functional memory dissociations that are exhibited by brain-damaged and
normal (instructed) adults. Whereas accounts based on multiple memory systems empha-
size the cognitive architecture and neural structures that underlie different kinds of memory
performance, processing accounts focus on the cognitive operations that are required to
perform different kinds of memory tasks. Our position is that a satisfactory account must
also explain the memory dissociations that are exhibited by very young infants. Therefore,
we briefly review the major theoretical accounts and consider their implications for the
development of implicit and explicit memory.

Throughout the preceding chapters, we have seen that tasks have been desig-
nated as either explicit or implicit on the basis of whether or not amnesics can
succeed on them, and the common usage of those terms was extended to refer
to the underlying brain systems that were presumed to be responsible for that
performance. In response to this situation, Gardiner and Java (1993) com-
plained that the science of memory had become obfuscated by “terminological
confusion and excess.” They were referring to the fact that the same terms —
implicit and explicit — were used to signify different memory tasks, different
memory systems or processes, and different states of awareness. Their concern
was that such labeling presupposed an “identity between the task and the system
or process, between the system or process and the state of awareness, [and]
between the state of awareness and the task” (Gardiner & Java 1993, p. 163).
Making matters worse, a variety of different labels have been given to
similar memory systems, and increasing numbers of new memory systems and
subsystems have begun to flood the taxonomy of memory classification. Many
of these new systems have resulted from the stochastic and functional indepen-
dence that has been found within tasks of implicit memory (see Chapter 2).

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190 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Within just a few years of the introduction of implicit and explicit memory, for
example, Roediger (1990a) had counted as many as 25 memory systems (for a
cursory list, see Table 8.1), and that number has continued to grow. Noting the
proliferating number of memory systems, Roediger, Rajaram and Srinivas
(1990, p. 585) mused, “Although parsimony is not a pristine scientific virtue
and must be abandoned when the data demand it, we wonder if that point has
been reached yet.”
Perhaps the most fundamental question left to answer is whether multiple
memory systems even exist (e.g., Anderson & Ross 1980; Baddeley 1984;
Craik 1983; Hintzman 1984; Jacoby 1984; Johnson 1992; McKoon, Ratcliff &
Dell 1986; Roediger 1990a; Roediger & Blaxton 1987). Because the multiple-
memory-system view has become so widely accepted in the fields of develop-
mental psychology, cognitive psychology, and behavioral neuroscience, we

Table 8.1. Proposed Memory Systems

Memory Systems Associated Theorist(s)
imagery/verbal Paivio 1971
episodic/semantic Tulving 1972, 1983; Kinsbourne &
Wood 1982
memory in the wide sense/memory in the McDougall 1923; Piaget & Inhelder 1973
narrow sense
specific/general memory Nelson & Brown 1979; Nelson 1984
sensorimotor/representational (conceptual) Mandler 1988, 1990
habit/memory Hirsh 1974; Bachvalier & Mishkin 1984
stimulus-response/representational\organized Ruggiero & Flagg 1976
reference/working Honig 1978
horizontal/vertical Wickelgren 1979
associative/abstract/representational Oakley 1981, 1983
knowing how/knowing that Cohen & Squire 1980; Cohen 1984
procedural/declarative Squire 1987
early-developing/late-developing Schacter & Moscovitch 1984
procedural/semantic/episodic Tulving 1987
semantic/cognitive mediational Warrington & Weiskrantz 1982
event memory/knowledge systems/ Weiskrantz 1987
associative memory priming
taxon/locale Jacobs & Nadel 1985; Nadel 1992
declarative/nondeclarative Squire 1992a
procedural/perceptual representation system/ Tulving 1993
semantic/episodic/short-term (working)
implicit/pre-explicit/explicit Nelson 1995, 1997

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STRUCTURAL AND PROCESSING ACCOUNTS 191

sometimes forget that not all memory researchers share this view. An alterna-
tive to the multiple-memory-system view is that memory is the result of a
unitary process and that experimental dissociations between particular tasks
merely reflect the processing operations that are required by different memory
tasks at the time of study and testing (e.g., Jacoby 1983; Johnson 1983; Mandler
1980; Roediger & Blaxton 1987). Some of the major multiple-memory-
systems and processing accounts are briefly reviewed below. Each account is
accompanied by a brief analysis of the role of conscious awareness, its
implications for implicit/explicit memory and memory development, and its
relation to memory data from human infants.

Multiple-memory-systems accounts

Criteria for proposing different memory systems

One of the critical issues associated with the proliferation of memory systems
concerns the rules for inferring them (Johnson & Hasher 1987; Roediger et al.
1990; Sherry & Schacter 1987; Tulving & Bower 1974; Weiskrantz 1990), but
some attempts at establishing these rules have been less successful than others.
In some of the earlier studies of memory, for example, researchers commonly
varied the types of materials that were presented to subjects. Paivio (1971), for
example, reported that college students who saw either a list of pictures or a
list of the names of the same pictures remembered the pictures better. More-
over, they remembered pictures of concrete objects better than pictures of
abstract ones. Data such as these led him to propose that there are two different
representational systems — the imagery system and the verbal system. This
distinction found some support in neuropsychological evidence that verbal
and nonverbal functions are lateralized in the cerebral hemispheres (e.g.,
Gazzaniga 1972).
Tulving and Bower (1974) reacted to Pavio’s proposition by questioning
if every dissociation that resulted from using a different set of experimental
materials would justify the creation of another memory system:
“It is not clear how one gets from this evidence to two memory systems or two
memory stores. It seems to us that the evidence for a ‘visual imagery’ store is
no better than that for a ‘tactual store,’ ‘olfactory store,’ ‘proprioceptive
store,’ ‘color store,’ and the like. The question is whether we should postulate

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192 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

a distinct memory system for every discriminable stimulus variable and for
every variation of events along values of that variable that produces differ-
ences in memory for those events. If we did, we would soon have more
memory systems or memory stores than we could name. If we did not, it is
necessary to spell out the rules for such postulation when it is deemed
appropriate or necessary. In this connection, it is also interesting to note that it
has not yet been made clear by anyone how the task of explaining memory
phenomena is materially aided by the hypothesized existence of different
memory stores and systems…” (Tulving & Bower 1974, p. 273).

In fact, the same question could be raised today (e.g., Roediger et al. 1990).
A number of different criteria for inferring new memory systems from
performance on explicit and implicit tests have been proposed by different
researchers (for review, see Roediger et al. 1990). These criteria include
stochastic independence (Tulving et al. 1982), functional independence
(Tulving 1985), different underlying neural structures (Squire 1986; Zola-
Morgan & Squire 1990b), functional incompatibility of operations (Sherry &
Schacter 1987), and multiple tests (Tulving 1987). The criteria of stochastic
and functional independence were previously considered in Chapter 2; the
remaining criteria are considered below.
Different Underlying Neural Structures. One of the most successful
arguments for postulating different memory systems rests on the assumption
that different neural processes underlie performance on implicit and explicit
tasks. Most of the data in support of this view have come from studies of brain-
damaged humans and from monkeys with experimentally induced lesions
(see Chapter 3). On the basis of these data, it is currently assumed that the
cerebellum mediates performance on classical conditioning tasks, the medial
temporal-diencephalic and frontal lobe structures mediate event memory, the
temporal and parietal neocortex mediate knowledge systems and representa-
tions, and the cerebellum and/or basal ganglia mediate(s) perceptual-motor
skills (Weiskrantz 1990, p. 106).
Although developmental dissociations in memory performance that are
ascribed to maturation of the brain are also often used to support the multiple-
memory-system view, these developmental dissociations do not actually occur
— as least, not in primates (see Chapters 5 and 6). In one particularly
unsuccessful attempt to draw a one-to-one relation between maturation of the
brain and infants’ memory performance, Nelson (1995, 1997) reviewed neuro-
logical evidence that related different parts of the nervous system to perfor-
mance on different kinds of memory tasks during early development. Using the

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STRUCTURAL AND PROCESSING ACCOUNTS 193

terms implicit and explicit to refer to underlying memory systems, he conjec-

tured that the components of the explicit memory system are not functional
before the end of the first year of life. However, his analysis contained a
number of errors pertaining to the nature of the tasks per se. For example, his
analogy between infants’ footkicking in the mobile task and the spinal reflex of
the decerebrate cat totally disregarded the critical distinction between simple
classical conditioning, which is reflexive, and operant conditioning, which is
not. The spinal reflex of the decerebrate cat is an unconditional reflex that is
elicited by an electrotactile stimulus, and the characteristics of the classically
conditioned response reflect the parameters of the eliciting stimulus (e.g.,
shock intensity or duration).
In contrast, an operant footkick is emitted only when, according to Skinner
(1953), the conditions are ripe. Thus the subject may or may not respond in the
presence of a particular stimulus. Nelson’s analysis also failed to distinguish
between the process of learning and the process of memory for what was
previously learned. This distinction was described by Watson (1984) as
memory in learning and memory of learning, respectively. Indeed, most
cognitive psychologists have failed to recognize that learning and memory
entail different processes. Forming an association between two events during
the course of learning requires only short-term (active) memory, and the
interval between successive events cannot exceed a few milliseconds to
seconds (except in the case of taste aversion learning) or the association will
not be acquired. The process of retrieving what was previously learned from
long-term memory into active memory, however, can occur after retention
intervals ranging from a few minutes to several months or longer. Thompson
(1990a, p. 512) made an identical point many years ago when Mandler (1990)
failed to distinguish between the acquisition process during conditioning and
the memory of what was conditioned.
Shimamura (1990) cautioned that a single memory dissociation on im-
plicit and explicit tasks, as found in amnesics, does not mean that each
measure of memory depends exclusively on a particular underlying neural
process or structure. Rather, it means only that the measure on which memory
performance is not impaired does not depend on the process or structure in
question. As an example, he described a scenario in which many different
neural components or modules interact with each other to produce perfor-
mance on a task presumed to measure one form of memory or another. In this
scenario, some — but not all — of the components that are critical for memory

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194 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

performance on one task (e.g., recall) are also implicated in a second task (e.g.,
recognition), but not in a third one (e.g., word-stem completion). In this
example, disrupting one component by lesioning would impair memory per-
formance on the two tasks for which it was a critical link but would not impair
it on the third task. Importantly, however, this dissociation would reveal
nothing about how many or what other neural components the two affected
tasks might share; rather, it would only reveal that the lesioned component did
not contribute to memory performance on the third task.
Functional Incompatibility of Operations. Another criterion for postulat-
ing more than one memory system grew out of a consideration of the evolution
of multiple memory systems. Sherry and Schacter (1987) argued that unique,
specialized memory systems evolved to handle new environmental demands
that existing memory systems could not. They suggested that different special-
ized memory systems for song, imprinting, and spatial location in birds, for
example, may have evolved to subserve the different functional demands
associated with mating, maternal care, species recognition, food caching, and
navigation. Presumably, each specialized memory system was uniquely con-
strained by temporal factors associated with the encoding (e.g., critical peri-
ods) or retrieval (e.g., seasonal migration) of information admitted into it.
Thus, remembering the prior location of a food cache, a nest, or a predator
would require the storage and retrieval of details of a particular episode. When
and where a given food source is accessible, such as when worms can be
found in the farmer’s field or when a truck arrives at the garbage tip
(McFarland 1977), however, could change weekly, monthly, or seasonally.
Thus, that memory system would have to be sufficiently flexible that details
about time or place could be updated. From an evolutionary perspective, then,
particular memory systems can be found in species whose adaptations reflect
the same functional demands.
Many psychologists, however, have assumed that the appearance of
different memory systems during ontogeny reflects their order of appearance
during phylogeny and have given little or no consideration to the particular
specializations that different species evolved in the course of adapting to
different niches. Analyses of the hierarchical development of multiple
memory systems that are based on the simple notion that ontogeny recapitu-
lates phylogeny make two fundamental errors. First, new memory systems,
such as the system that is implicated in seed-caching by nutcrackers, are
species-specific and reflect an organism’s specialized adaptation to its niche.

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STRUCTURAL AND PROCESSING ACCOUNTS 195

Human infants, who occupy a very different niche (or series of niches), do not
require these same memory systems. Second, ontogeny is linear, but phylog-
eny is not. Evidence gathered over the last half-century now shows that
phylogeny is tree-like and branching rather than ladder-like and linear. In
short, there is no simple relation between the appearance of a capacity in
phylogeny and its appearance in ontogeny.
Multiple Tasks. Tulving (1987) argued that the inference of multiple
memory systems requires that the same dissociation be exhibited on several
tasks, each of which presumably taps the same underlying memory systems.
Thus, if a particular independent variable affects performance on the battery
of tasks thought to tap one memory system differently from the way it affects
performance on the battery of tasks thought to tap a different system, then it is
safe to conclude that the tasks within each battery share something not shared
with the tasks in the other battery. Although some would use such findings to
argue that what is shared by these tasks are common memory systems, it is just
as reasonable to argue that what is shared are common processing operations.
In fact, most studies with adults that have revealed memory dissociations
on one task but not on another have used only two tasks, each presumably
tapping a different underlying memory system. The same criticism — the use
of only two tasks to illustrate an experimental dissociation in memory perfor-
mance — can be levied against most of the infant studies cited in Chapter 7.
Unlike the adult studies in which the materials and temporal parameters of
study and test vary from report to report, however, all of the mobile studies
with infants used exactly the same two tasks, the same task parameters, and
infants from the same population. Thus, instead of manipulating a single
independent variable and producing the same dissociation across multiple
implicit and explicit tasks as in adult studies, the infant studies manipulated
multiple independent variables and produced the same dissociation on a single
implicit and explicit task. In doing so, however, the infant studies have
amassed a large amount of convergent evidence of functional memory disso-
ciations.
Although we have focused on the explicit/implicit distinction in this book,
a number of multiple memory systems have been proposed over the years that
meet one or more of the criteria outlined above. Below, we consider in more
detail the two major classifications of multiple memory systems that have been
proposed, episodic and semantic memory and declarative and procedural
(nondeclarative) memory, and their implications for memory development.

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196 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Episodic and semantic memory

Tulving (1972) was the first to distinguish episodic and semantic memory as
two, functionally distinct memory systems and to differentiate them in terms
of the content of the memories they stored. The episodic system stored
autobiographical information about personally experienced events (episodes)
that were specified by spatiotemporal details. The semantic system, in con-
trast, stored the individual’s general (organized) knowledge. Although re-
trieval from the episodic system altered its content (e.g., by supplementing or
modifying it), retrieval from the semantic system did not. Tulving did not
explicitly specify the relation of episodic and semantic memory to the tradi-
tional distinction between long-term and short-term memory, but by describ-
ing episodic memory as what psychologists studied in laboratory tasks, he
implied that episodic memories were of shorter duration than semantic ones.

Episodic/semantic distinction and development

Tulving proposed that episodic and semantic memory develop sequentially

during ontogeny, with the semantic memory system developing first. The
same developmental sequence is suggested in Schacter and Moscovitch’s
(1984) sequence of early-maturing and late-maturing memory systems, which
correspond closely to the semantic and episodic memory systems, respec-
tively. Other theorists, however, viewed this developmental sequence as
incorrect, arguing that general knowledge (semantic memory) develops out of
an individual’s highly specific experiences or episodic memories (e.g., Anglin
1977; Cermak 1984; Kintsch 1974; Nelson & Brown 1978). The flavor of
their argument is captured in the following quote:
“Are not autobiographic, very long-term memories typical episodic memo-
ries? What happened on your fifth birthday is surely part of your knowledge
of the world, of your long-term memory — but it is not semantic. Rather, it is
episodic; it reflects an event that actually occurred, it is also a part of real
world knowledge, and it may be reconstructed using inferential processes”
(Nelson & Brown 1978, p. 234).

In fact, the question of whether development proceeds from the specific to the
general or from the general to the specific has long occupied developmental
psychologists. Some early researchers viewed development as a process of
increasing generalization. This view is reflected in Watson’s (1930) account

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STRUCTURAL AND PROCESSING ACCOUNTS 197

of the development of fears and conditioned reflexes and in Bridges’ (1932)

account of the development of emotions. Others, however, viewed develop-
ment as a process of increasing differentiation. This view is reflected in
Gibson’s (1969) account of perceptual development and in Olson and Strauss’
(1984) account of the development of infant memory:
“The period from 3–7 months is characterized by elaboration of the infant’s
basic information processing skills….By the end of this period, the infant has
in place the skills for a series of major achievements in cognitive and social
development that will begin in the second half of the first year….Although
the younger infant can only readily show memory for bold patterns and sharp
contrasts between test alternatives, the infant of 6–7 months shows a broad
range of encoding skills that include recognition of details of patterns and
subtle aspects of stimuli” (Olson & Strauss 1984, p. 35).

The latter view, however, does not characterize the development of infant
memory. A large number of studies using different paradigms have now
documented that infants’ early memories are initially highly specific and
become increasingly generalized with age (Hartshorn et al. 1998a; Hayne et
al. 1997), as originally argued by Nelson and Brown (1978). In mobile studies,
for example, even 2-month-olds can detect if their test mobile differs ever so
slightly from the highly detailed, five-object mobile with which they were
trained 24 hours earlier. If more than a single object on the test mobile differs
from what appeared on the training mobile, then they cannot recognize it;
otherwise, their 24-hour recognition is excellent (Hayne et al. 1986). Simi-
larly, if 3-month-olds are trained with a block mobile displaying As on all
sides in a single color (red, green, black, or blue) and are tested 24 hours later
with an identical mobile that displays As (the same form) in a different color,
they cannot recognize it. Nor can they recognize a test mobile that displays 2s
(a different form) in the original training color (Hayne et al. 1987). In other
words, even 3-month-olds can discriminate a difference in just a single at-
tribute after a 24-hour delay.
In other studies, Gerhardstein et al. (2000) found that 3-month-olds could
not recognize a test mobile 24 hours later if the characters it displayed (Ls or
+s) were 33% smaller or larger than the characters on their training mobiles
(see Chapter 7, Studied Size), and Adler and Rovee-Collier (1994) found that
3-month-olds could not recognize a test mobile 24 hours later if it displayed
characters that were 25% smaller. Finally, recall that after 3-month-olds were
trained with a six-block mobile displaying two different sets of feature combi-
nations (red As on black blocks and green 2s on yellow blocks), they discrimi-

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198 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

nated different recombinations of these features (figure color, figure form,

block color) on their test mobiles, even though all of the features that were
present at the time of encoding were still present when they were tested 1 day
later (Bhatt & Rovee-Collier 1994). After a 4-day retention interval, infants
generalized to test recombinations of all attributes; even then, however, they
still discriminated if the test mobile contained a single feature that had not
been on the training mobile (Bhatt & Rovee-Collier 1996). Taken together, the
preceding data provide compelling evidence that infant’s early memories are
highly specific.
By 9 months of age, however, infants generalize to physically different
stimuli, but they do so after short retention intervals only (see Figure 8.1).
After longer retention intervals, older infants — like younger ones — continue
to discriminate a test stimulus that differs from the stimulus that was present
during training (Hartshorn et al. 1998a). Their pattern of generalization/
discrimination as a function of the length of the retention interval indicates
that their generalization after short test delays does not result from perceptual
confusion (i.e., an inability to perceptually distinguish between the training
and the test stimuli). If it did, infants would be unable to discriminate between
the same cues after longer retention intervals. The fact that older infants begin
to generalize to novel stimuli after short delays only suggests that their
generalized responding is strategic — as if they were testing the waters in
order to determine if the discriminably different new objects are functionally
equivalent to the objects that they had previously encountered in the same
context.
This analysis is supported by evidence that the same pattern — increasing
generalization with age — has been observed in studies of deferred imitation
with infants (Barr & Hayne, 2000). Six-month-olds do not imitate previously
modeled actions 24 hours later if the test object is novel (Hayne et al. 1997
2000a). By 12 to 14 months of age, however, infants generalize to a test object
that differs from the object seen during the demonstration in color only. They
do so only after a short delay (i.e., 10 min; Barnat, Klein & Meltzoff 1996;
Hayne et al. 1997), however, and not after a longer one (i.e., 1 day; Hayne &
Campbell 1997; Hayne et al. 1997). By 18 months, they generalize to a cue
that differs in color only after a longer delay (i.e., 1 day), and by 21 months,
they generalize to a cue that differs both in color and form after 1 day (Hayne
et al. 1997). This pattern of development continues throughout the infancy
period (Herbert & Hayne 2000).

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STRUCTURAL AND PROCESSING ACCOUNTS 199

Figure 8.1. Mean baseline ratios of independent groups of infants between 2 and 12 months
of age who were trained for two sessions and tested with a different cue in the original
context after common relative retention intervals that corresponded to the shortest (Early)
or longest (Late) test delays or to the midpoint (Middle) of the forgetting function for each
age group. An asterisk indicates that a group exhibited significant retention (i.e., M baseline
ratio significantly > 1.00). Vertical bars indicate + 1 SE.

Nelson and Brown (1978) complained that Tulving (1972) originally

used the term episodic to refer both to a type of memory and to a class of
laboratory tasks (i.e., tasks in which isolated lists of verbal materials were
deliberately learned). Adults used deliberate mnemonic strategies and were
quite good in solving these tasks, but children — lacking efficient mnemonic
strategies — were not. As a result, theorists generally assumed that children
had poor episodic memories. In the quote at the outset of this section, how-
ever, Nelson and Brown had argued that real world episodic memories (i.e.,
not memories measured in artificial laboratory tasks), being autobiographical,
are the only kind of memories that young children have before the semantic
component has evolved. They concluded that the characterization of young
children’s episodic memory as poor resulted from a failure to distinguish the
underlying type of memory from the particular class of laboratory tasks that
were used to measure it.

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200 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Nelson and Brown (1978) also complained that Tulving’s choice of the
term semantic to refer to words and word meanings reflected the fact that
researchers always used verbal materials in studies with adults — a practice
that was extended to studies with children, although pictures or objects were
substituted for words in studies with very young children. But, they argued,
children’s nonverbal memories for actions, spatial locations, cognitive maps,
scripts, and so forth, were neither clearly semantic nor clearly episodic:
“How such an organized semantic language-based system emerges is at least
one important and central developmental question. But if all real world
knowledge — language based or not, categorically structured or not — is
termed “semantic memory,” the question cannot even be asked using an
episodic-semantic distinction” (p. 240).

Criticisms of the episodic/semantic distinction

In a critical analysis of episodic and semantic memory, McKoon et al. (1986)

concluded that the empirical and neuropsychological evidence supporting the
distinction between them was weak. In response, Tulving (1986) argued that
the distinction was useful for classifying memory phenomena and that future
neurological evidence would justify the distinction. To this, Ratcliff and
McKoon (1986) replied that neurophysiological evidence alone would never
be able to provide an understanding of the mind and that Tulving and Bower’s
(1974, pp. 296–297) original conclusion was still valid:
“It is only in the context of a particular process model that inferences can be
meaningfully drawn from the experimental data. This restriction holds up
regardless of what method is used. When we noted, in discussing various
methods, that the logic was not entirely clear, the difficulty usually lay in the
absence of a set of statements or assumptions about the principles governing
the utilization of the stored information at the time of retrieval. The process
models that would help make sense out of the data on …[memory systems]
need not be complex or highly sophisticated or “correct.” But they must enter
the picture in some form. Even a bad process model is better than none at all.
It would help make clear the logic of the method of specifying…[memory
systems], aid communication, and facilitate cross-comparison of data ob-
tained with different methods. Moreover, it can be improved, revised, or
replaced with a better one. A nonexistent model cannot” (Tulving & Bower
1974, quoted in Ratcliff & McKoon 1986, p. 313).

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STRUCTURAL AND PROCESSING ACCOUNTS 201

Modifications of episodic and semantic memory

The finding that functional dissociations were found within both explicit and
implicit tests revealed that a single memory system could not underlie memory
performance on each type of test. As a result, theorists were motivated to
expand their original dichotomies. Thus, for example, Squire (1987) expanded
the procedural/declarative dichotomy (Squire 1986) to include priming,
simple classical conditioning, and skill learning as subcategories of proce-
dural memory and episodic (working) and semantic (reference) memory as
subcategories of declarative memory. Likewise, Tulving (1985) added proce-
dural memory to the semantic/episodic dichotomy, viewing episodic memory
as roughly corresponding to explicit memory and procedural and semantic
memory as roughly corresponding to implicit memory (Tulving 1987). He
characterized the three-system arrangement as monohierarchical, with epi-
sodic memory being a specialized subsystem that evolved out of semantic
memory, and semantic memory being a specialized subsystem that evolved
out of procedural memory. By this account, the procedural memory system
appeared first in phylogeny and ontogeny, and succeeding memory systems
appeared later:
“Semantic memory develops earlier in childhood than episodic memory:
Children are capable of learning facts of the world before they can remember
their own past experiences” (Tulving 1993, p. 68).

As we saw in preceding chapters, however, this was a statement of faith, not

fact.
Subsequently, Tulving (1993) added working (primary, or short-term)
memory and the perceptual representation system (Tulving & Schacter 1990)
to the preceding three, making a total of five human memory systems. His
major writings, however, have continued to focus on the episodic/semantic
distinction.
The structural descriptions system, a part of the perceptual representation
system (PRS) that has particular relevance for interpretations of infant memory,
was introduced as a subsystem of the perceptual representation system to
account for memory performance that is based solely on perceptual properties
(Schacter 1990). The structural descriptions system is dedicated to the repre-
sentation of information about the form and structure of visual objects, includ-
ing a description of an object’s plane of orientation about a central axis (Cooper,
Schacter & Moore 1991) but not its size (Schacter et al. 1993b). This system

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202 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

also includes no semantic information about objects, for example, information

concerning either the functions that an object can perform or its associative
properties.
The dominant paradigm for evaluating memory performance mediated
by this system in adults is the object decision task, in which subjects make
perceptual decisions about the test stimuli, such as whether or not a particular
drawing could possibly exist as a three-dimensional object or not (Schacter &
Cooper 1993; Schacter et al. 1990, 1991a). The relevant research findings
have demonstrated the familiar memory dissociation: Priming is preserved for
both novel objects (e.g., Schacter et al. 1993b) and familiar ones (Cave &
Squire 1992), but recognition memory is impaired (Biederman & Cooper
1992; Schacter et al. 1993b).
The structural descriptions system has been described as one of the first
memory systems to appear in ontogeny and is thought to mediate memory
processing in early infancy (Schacter 1990) — a view consistent with the
widespread notion that the primary content of infants’ early memories is
strictly perceptual (Olson & Strauss 1984). According to Schacter (1990), the
structural descriptions system does not represent information about object
function, object size, or associative information. Yet, infants as young as 3 to
6 months exhibit memories of this kind of information. The evidence pertain-
ing to the role of object function and associations between memories in very
young infants is described below; evidence pertaining to the effect of object
size (Adler & Rovee-Collier 1994; Gerhardstein et al., 2000) was previously
described in Chapter 7 (see Studied Size).
Evidence for memories of object function in young infants. If infants only
possess the structural descriptions system, then they should not be able to form
memories of object function. However, they can. A mobile that infants had
learned to move by kicking is an effective reminder in a reactivation task if it is
moving but not if it is stationary (Fagen, Yengo, Rovee-Collier & Enright
1981; Greco et al. 1990). In a delayed recognition task, however, the same
mobile readily cues retrieval whether it is moving or not. This difference may
reflect the fact that fewer or different cues are needed to retrieve memories that
are more accessible (Spear 1978). Functional information is not requisite for
reminding, however, if the cue that is used as a reminder was also originally
nonfunctional. The original training context or setting did not move, for
example, yet it is an effective reminder for the training memory when pre-
sented alone, without the original training mobile (Hayne & Findlay 1995;

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STRUCTURAL AND PROCESSING ACCOUNTS 203

Rovee-Collier et al. 1985a).

Additional evidence that object function is represented in infant memory
comes from studies involving a passive-exposure procedure. In this proce-
dure, infants are merely exposed to (i.e., do not interact with) a novel object
functioning in the same way their prior training mobile had functioned. The
exposure is brief — only 3 min for 3-month-olds and only 2 min for 6-month-
olds — and occurs only once, after a posttraining delay that can be as long as
days or weeks. Subsequently, infants receive a delayed recognition test in
which either the original mobile or the exposed one is presented as the
retrieval cue. In a number of studies, we have found that infants’ memories
are readily modified so that they include the exposed object in addition to
(memory expansion) or in place of (memory impairment) the original mobile
(Boller, Grabelle & Rovee-Collier 1995; Boller et al. 1996; Muzzio & Rovee-
Collier 1996; Rossi-George & Rovee-Collier 1999; Rovee-Collier et al. 1994;
Rovee-Collier et al. 1993a; for review, see Rovee-Collier & Boller 1995),
despite the fact that infants otherwise do not generalize to a novel test mobile
after a 24-hour delay. Moreover, this modification occurs even when the novel
exposed object is highly physically dissimilar to the prior training mobile, as
long as it is functionally equivalent to the training mobile (Greco et al. 1990).
If the novel object is exposed in exactly the same manner and after the same
delay but in the absence of equivalent functional information, then infants’
memory of the prior training mobile is not modified, and infants continue to
recognize it instead of responding to the novel mobile 24 hours later (Boller et
al. 1995; Greco et al. 1990).
Evidence for memories of associations in young infants. If infants only
possess the structural descriptions system, then they should not be able to form
memories of associations between objects, but they can. In the traditional
learning literature, this phenomenon is called sensory preconditioning, refer-
ring to the fact that an association is established by the mere simultaneous
occurrence of two sensory events, without the necessity of a distinctive
response (Brogden 1939). When 6-month-olds merely saw the two puppets
side-by-side for an hour per day for 1 week, for example, then they associated
them. This association was not revealed, however, until they subsequently
saw the target actions modeled on one puppet. When tested 1 day later, they
imitated the target actions on the other puppet (Marrott, Barr & Rovee-Collier,
2000). In contrast, infants who were exposed to the two puppets for the same
average amount of time but at different times of day (i.e., unpaired) did not

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204 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

imitate what they had seen modeled on one puppet when they were tested with
the other, even though both puppets were equally familiar. These data reveal
that infants subsequently transferred the memory of the modeled actions to the
second puppet only if they had previously formed an association between it
and the puppet on which the actions were modeled and remembered it.
Boller (1997) obtained a similar result when she repeatedly exposed 6-
month-olds to two distinctively colored and patterned cloth panels side-by-
side for 1 hour per day for 1 week and then subsequently trained them to kick
to move a mobile in the presence of one of the panels. When she tested them
with the mobile in the presence of the other context 1 day after training, they
recognized it. When she preexposed infants to the two panels for an equal
amount of time prior to training but at different times of day, however, they
subsequently did not recognize the mobile when tested with it in the presence
of the other panel, again revealing that infants transferred the training memory
they had acquired in the presence of one panel to the other panel by virtue of
the memory of the association between the two panels that they had previously
formed. If infants were equally familiar with the two panels but had no
opportunity to form an association between them, then the memory that
infants had subsequently acquired in the presence of one panel did not transfer
to the other.
In both of the preceding studies, infants learned that two discriminably
different objects were associated in the course of repeatedly seeing those
objects appear together, irrespective of the experimental paradigm within
which their memory of that association was tested. In both studies, the
memory of the association that infants had picked up by merely looking was
revealed only when they were subsequently given an opportunity to demon-
strate that knowledge through their direct actions.
Evidence for associations between memories in young infants. Finally, if
infants only possess the structural descriptions system, then they should not be
able to form associations between independent memories. However, they can
do this as well. Timmons (1994) obtained evidence that infants form associa-
tions between independent memories by 6 months of age. In an initial study,
she trained 6-month-olds either to move a mobile suspended over the playpen
or to turn on a music box affixed to the front of the playpen by either arm-
pulling or footkicking — an analog of the traditional paired-associate task
used in studies of verbal learning and memory. Infants were trained in a
distinctive context for 2 days on one cue-response pair and, 3 days later,

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STRUCTURAL AND PROCESSING ACCOUNTS 205

learned the other cue-response pair in the same context. Three days after
learning the second pair, infants were tested with each of the cues in a delayed
recognition paradigm. During testing, infants produced only the particular
response (kicking or arm-pulling) that had originally been associated with a
given test cue (mobile or music box), regardless of which response they had
learned last. This result confirmed that infants’ memory of each cue-response
pair had been stored independently and that test responding was highly
specific to the retrieval cue that was presented.
In a second experiment, Timmons trained infants as before, but this time
she waited until both of the training memories had been forgotten (i.e., 3
weeks) and then exposed infants to either the mobile or to the music box as a
memory prime in a reactivation paradigm. On the following day, she adminis-
tered a long-term retention test to all infants using only the mobile as the
retrieval cue. As expected, infants who were both primed and tested with the
mobile exhibited the mobile-appropriate response to the mobile retrieval cue
— the typical finding in memory reactivation studies. Surprisingly, however,
infants who were primed with the music box also exhibited the mobile-
appropriate response (and no other) to the mobile test cue (see Figure 8.2).
Recall that the mobile memory was not directly primed with the mobile
and that it was forgotten at the time the music-box memory was primed.
Timmons assumed, therefore, that the music-box prime had activated the
memory node representing the music box paired-associate and that this activa-
tion had spread to the memory node representing the mobile paired-associate,
thereby enabling infants to perform the mobile-appropriate response to the
mobile cue during the subsequent test. Thus, even though the memory of each
task was independent and highly specific, the two memories were associa-
tively linked — possibly via the common context in which both tasks had
originally been acquired — in a common mnemonic network. As a result,
priming one memory brought to mind the memory of the other.
A similar phenomenon was reported by Barr and Vieira (1999), who
taught 6-month-old infants to associate the operant train procedure with an
imitation procedure. Drawing from Timmons’ (1994) finding that one
memory can be associated with another if the two memories were acquired in
a common context, they asked if 6-month-olds’ memory of the puppet task
would be associated with a memory of the train task if they acquired the two
memories in the same context. Because 6-month-olds remember the puppet
task for only 1 day but remember the train task for 2 weeks (see Figure 8.3),

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206 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 8.2. Associative priming exhibited by 6-month-olds who originally learned to

perform different responses to a mobile and to a music box. Left panel: On a delayed
recognition test 3 days after training was over, infants who were tested with the mobile
produced the mobile response, but infants who were tested with the music box did not.
Right panel: Priming with either the mobile or the music box 3 weeks after training
reactivated the mobile response and facilitated responding to the mobile 24 hours later. The
magnitude of reactivation was the same whether reactivation was direct (Mob) or indirect
(Mus). Asterisks indicate significant retention (M baseline proportion significantly > .50).
Vertical bars indicate + 1 SE.

they hypothesized that the longer-lived train memory might “carry” the asso-
ciated memory of the short-lived puppet task along with it and protract it
longer than otherwise possible. If so, then retrieving the train memory 1 or 2
weeks later might also retrieve infants’ memory of the puppet task, with the
result that infants would imitate the adult’s actions on the puppet after the
longer delay.
To test this, Barr and Vieira trained 6-month-olds in the train task.
Immediately after training was over, the mother — her infant on her lap —
turned her chair sideways so that the train was still in view to the infant’s side.
The experimenter then knelt in front of the infant and demonstrated a series of
three actions on a hand puppet (removing a mitten from the puppet’s hand,
shaking it to ring a bell hidden inside, and replacing the mitten). During the

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STRUCTURAL AND PROCESSING ACCOUNTS 207

Figure 8.3. The duration of retention of 6-month-olds’ independent memories of the

operant train task (open squares, right axis) and the puppet imitation task (black circles, left
axis). Asterisks indicate significant retention; vertical bars indicate ±1 SE.

initial imitation test that followed immediately after the demonstration and
either 1 or 2 weeks later, infants were allowed 120 s from when they first
touched the puppet to imitate the experimenter’s actions. The hypothesis was
confirmed: Infants imitated the target actions after both delays — but only if
they were tested first with the train, not if they were tested first with the puppet
(see Figure 8.4). In other words, retrieving the train memory was necessary in
order to activate infants’ memory of the puppet task as well. Infants in a
baseline control group did not see the actions modeled originally, and they did
not spontaneously produce them during the test. We have recently found that
the puppet task can be associated with the memory of the train task even when
2 weeks have elapsed between learning the train task and initially viewing the
puppet task. The association is formed if the target actions on the puppet task
are modeled in the presence of the nonmoving train. These data clearly
demonstrate that a short-lived memory (the puppet demonstration) that is
associated with a longer-lived memory (the train task) can become longer-
lasting as well.

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208 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 8.4. The duration of retention of 6-month-olds’ independent memory of the puppet
task (left panel, Exp. 1) and their memory of the puppet task after it had been associated with
the train task (right panel, Exp. 2). Asterisks indicate significant retention; vertical bars
indicate ±1 SE.

The first deferred imitation study to use a reactivation procedure was

conducted with 18-month-olds, who typically can imitate modeled actions
that were previously demonstrated on the puppet after a retention interval of 4
weeks but not longer (Barr 1997). Two weeks after they had forgotten the task
(6 weeks after the demonstration), infants who saw the puppet moving and
ringing for 30 s (the memory prime) once again imitated the target actions 1
day later. Subsequently, Barr and Vieira (1999) used the reactivation proce-
dure with 6-month-olds to recover their forgotten associated memories of the
train and puppet tasks. As in Timmons (1994), they found that reactivating
one memory indirectly reactivated the memory that was associated with it.
After establishing the train task-puppet task association (see above), they
allowed 6-month-olds to forget both tasks. After a retention interval of 20
days, they modeled the target actions on the puppet for 30 s as a reactivation
treatment, and immediately before the train test 1 day later, infants were
primed with the moving and ringing puppet (see Figure 7.2c). When tested
with the train, which they had not seen for 3 weeks, infants again recognized it
(see Figure 8.5, right panel). Conversely, a 2-min exposure to the moving

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STRUCTURAL AND PROCESSING ACCOUNTS 209

train reactivated infants’ forgotten memory of the puppet task. One day later,
infants exhibited significant imitation if they were first primed for 2 min with
the train, either moving or nonmoving (see Figure 8.5, left panel). These
infants had seen the puppet demonstration only once and only briefly 3 weeks
earlier. The reactivation control group was not originally exposed to either
task but received the train reactivation treatment on day 20 and was primed
with the moving train immediately before the puppet test on day 21. This
group exhibited no retention when tested with the puppet.
A number of theorists have proposed that memories are represented in a
network and are connected to each other by links (e.g., Nelson & Kosslyn
1975). According to spreading-activation models (Collins & Loftus 1975;
Collins & Quillian 1969), the presentation of a retrieval cue activates a memory

Figure 8.5. Memory performance of 6-month-olds 3 weeks after training/modeling. One

day before the test, infants were exposed for 2 min to the train (left panel) or for 30 s to the
puppet (right panel) and were tested with the other stimulus. Immediately before the puppet
test, groups were primed for 2 min with either the moving train (puppet, middle striped
column) or nonmoving train (right striped column) to retrieve the puppet memory. The
reactivation control group was reactivated, primed, and tested like the puppet group but was
not originally trained on either task. Immediately before the train test, infants were again
primed for 2 min with the moving and ringing puppet (see Figure 7.2c). Asterisks indicate
that the memory was reactivated (i.e., significant retention). Vertical bars indicate ±1 SE.

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210 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

at a particular node in the network; as this excitation subsequently spreads to

other nodes that are linked to the original one, they are activated as well. As a
result, memories associated with the nodes that have been indirectly activated
in this fashion also become more accessible. Although some of the original
network models have fallen from favor, others continue to provide useful
accounts for the facilitative effect of one retrieval on another. We have found
it useful to attribute the priming phenomenon that was observed by Timmons
and by Barr and Vieira to spreading activation. By this account, when the node
corresponding to either the music box (Timmons 1994) or the train (Barr &
Vieira 1999) was activated, the activation spread to the node that corresponds
to the mobile or puppet demonstration, respectively, via the association that was
formed between the memories of the two tasks in each study and linked them
in a common mnemonic network. As a result, priming one memory activated
the other as well.
Sheffield and Hudson (1994) observed a similar associative phenomenon
in a memory study with 14- to 18-month-old toddlers. Using a reenactment
paradigm, they allowed toddlers to actively engage in six different structured
activities at different stations in the laboratory. After toddlers’ memory of
their visit had been forgotten, they were returned to the laboratory, and three
of the activities were modeled by the experimenter while the children merely
watched. Twenty-four hours later, the children were asked to produce the
three activities that they had not seen modeled and the three that they had.
As expected, children of the same age who had not been originally trained
but who had viewed the modeling exhibited deferred imitation of the three
actions they had seen modeled the day before, and children who were not
exposed to the reactivation treatment (the partial modeling) remembered none.
However, children who had been originally trained and had also seen three
activities modeled were not only able to produce the three modeled activities
but also were able to enact the three activities that had not been modeled
during the reactivation treatment, despite the fact that they had not engaged in
them for 10 weeks. Again, as in Timmons (1994), directly reactivating some
activities led to the indirect reactivation of others in the memory network —
again, probably mediated by the common context in which the activities had
initially been performed. Clearly, associative memory is not unique to the
mobile task; it can also be demonstrated in very different memory tasks that
involve no prior conditioning of the target response.
These results have major implications for everyday memory processing

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STRUCTURAL AND PROCESSING ACCOUNTS 211

by persons of all ages. If memories in an associative network need not be

directly accessed in order to be retrieved, then in the normal course of
interacting with their environment, infants and older individuals are likely to
encounter cues that not only directly retrieve the memories in which they are
represented but that also mediate the retrieval of other memories that are
represented in the same mnemonic network. In our personal experience, this is
exactly what happens — remembering one event reminds us of another.
In summary, the preceding evidence demonstrates that information about
an object’s meaning or function is incorporated into infants’ memories by 3
months of age and that memories of associations as well as associations
between independent memories are formed by at least 6 months of age. None
of these memory phenomena can be accounted for by the structural descrip-
tions system.

Declarative and procedural (nondeclarative) memory

These memory systems were proposed by Squire (1986, 1987) and, like
Tulving’s (1972, 1983) memory systems, are distinguished by their content
and its accessibility to conscious recollection. The declarative memory system
stores information about facts and personally experienced events that can be
consciously recollected as a proposition or image, whereas the procedural
memory system (subsequently called the nondeclarative memory system;
Squire 1992a) stores acquired information that is embedded in procedures or
skills and cannot be consciously recollected (i.e., implicit memory). The
different types of information in the two systems have been distinguished as
knowing that and knowing how, respectively (Cohen & Squire 1980). In
Squire’s formulation, however, episodic memory and semantic memory are
subdivisions of the declarative system, and both are accessible to conscious-
ness. Episodic memory represents autobiographical information, whereas se-
mantic memory represents world knowledge. Likewise, episodic memory
represents information that is temporally dated, whereas semantic memory
represents information that is not.
Whereas Tulving’s systems were distinguished in an attempt to create a
taxonomy of memory, that is, for purposes of classification, Squire’s systems
were created for the purpose of developing a “biologically useful” level of
analysis of brain function, that is, an account of “how the brain itself actually

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212 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

stores information” (Squire 1987, p. 160). The declarative/procedural formu-

lation grew out of research with amnesic patients and was necessitated by
evidence that the original episodic/semantic dichotomy did not distinguish the
different neurological organization of episodic and semantic memories. A
case in point is the phenomenon of source amnesia:
“…some amnesic patients…can remember recently acquired items of infor-
mation, without remembering when or where they acquired the information.
Importantly, source amnesia is a separate deficit, unrelated to memory impair-
ment itself. It does not appear in all amnesic patients, but the ones who show
it do so consistently. Moreover, the patients without source amnesia can have
just as severe a memory impairment as patients with source amnesia. If the
term episodic memory is reserved for acts of remembering that are specifi-
cally autobiographical, then episodic memory might refer usefully to that
aspect of memory function that is lost in source amnesia and that ordinarily
permits a sense of personal connection to one’s past. In normal subjects, recall
and recognition are ordinarily accompanied by recollection of the learning
episode. However, in some amnesic patients the quality of personal familiar-
ity and connectedness to a recent episode can be lost despite successful recall
and recognition of material learned in the episode. Preliminary evidence
suggests that frontal lobe pathology may contribute to this phenomenon”
(Squire 1987, p. 173).

Declarative/procedural memory and the explicit/implicit distinction

Explicit memories contain information that is consciously accessible, whereas

implicit memories contain information that is not. Thus, the declarative system
stores explicit memories, whereas the procedural memory system stores im-
plicit memories. Although functional dissociations in memory performance on
explicit and implicit tasks are predicted by the declarative/procedural formula-
tion, the tasks defined as explicit and implicit are different from the tasks defined
as explicit and implicit in Tulving’s (1983) dichotomy because the declarative
system encompasses both episodic and semantic memories, whereas Tulving
distinguished these as separate memory systems. Thus, Tulving predicted
memory dissociations between episodic and semantic memories based on the
absence of conscious awareness of information retrieved from semantic
memory; Squire (1987) did not. However, both predicted a functional dissocia-
tion in memory performance between tasks requiring procedural information
and those that did not. Although Tulving (1987) introduced a procedural
memory system (memory for procedures) that was distinguished from the

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STRUCTURAL AND PROCESSING ACCOUNTS 213

semantic memory system (generic or factual knowledge), only information in

the episodic memory system was accessible to conscious recollection.
Because Squire’s formulation assumes that different brain mechanisms
subserve the declarative and procedural (or nondeclarative) memory systems,
damage to the brain mechanisms associated with one system or subsystem
affects its content but does not affect the content of another system. Moreover,
because the memories stored in each system and subsystem are different
representations, brain damage completely obliterates access to a particular
representation. A different kind of memory test does not simply access the
same representation via a different route; rather, it accesses an entirely differ-
ent representation.

Declarative/procedural memory and development

Squire (1987) suggested that declarative memory may have evolved relatively
late in phylogeny and attained its maximum level of development in mam-
mals. Similarly, he suggested that declarative memory develops later than
procedural memory. This suggestion was based on Bachevalier and Mishkin’s
(1984) evidence from infant monkeys that the memory system develops later
than the habit system (see Chapter 5) and is consistent with other suggestions
that two memory systems that support comparable functions develop sequen-
tially (Schacter & Moscovitch 1984; Tulving 1983). As we have argued in
previous chapteres, a developmental dissociation between these two memory
systems is an article of faith rather than an empirical fact. For this reason, the
questions raised earlier about the developmental relationship between seman-
tic memory to episodic memory are also pertinent here.

Processing accounts

Although functional dissociations have been taken as evidence for multiple

memory systems (Squire 1987; Tulving 1985), they have also been interpreted
as reflecting different information-processing demands of implicit and explicit
tests within a single memory system (Dritschel, Williams, Baddeley & Nimmo-
Smith 1992; McKoon, Ratcliff & Dell 1986; Roediger 1984; Shallice 1988).
Just as the number of proposed memory systems has swelled to accommodate
the variety of diverse memory dissociations, so have the number of processing

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214 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Table 8.2. Examples of Different Processing Accounts of Experimental Dissociations on

Implicit and Explicit Memory Tests with Normal and Amnesic Populations
Processing Account Associated Theorist(s)
data-driven and conceptually-driven processing Jacoby 1983; Roediger & Blaxton 1987
activation and elaboration Mandler 1980
incidental and intentional processing Jacoby 1984, 1991
automatic and controlled processing Mandler 1980, 1985
conscious and non-conscious processing Mandler 1989
processing dimensions Olton 1989
multiple-entry modular model (MEM) Johnson 1983
coherence model Hirst 1989

accounts (see Table 8.2). These accounts emphasize different cognitive opera-
tions within a unitary memory system instead of the different memory content
of different memory systems. The two major processing accounts that have
been proposed, transfer-appropriate processing and the multiple-entry modu-
lar model, are considered below.

Transfer-appropriate processing

A widely known processing account, transfer-appropriate processing, was

advanced by Roediger and his colleagues (e.g., Roediger 1984; Roediger &
Blaxton 1987; Roediger, Weldon & Challis 1989b; Srinivas & Roediger
1990), who argued that in many studies that documented a memory dissocia-
tion on implicit and explicit tasks, the type of memory task was confounded
with the type of processing it required. According to the transfer-appropriate
processing account, evidence of memory would be found only when the
mental operations required at the time of testing matched those required at the
time of encoding; any discrepancy would result in a retrieval failure. The
possible processing operations were described as data-driven (i.e., driven by
the perceptual or surface features of the stimulus) and conceptually-driven
(i.e., driven by the deeper meaning of the stimulus). Because most perceptual
priming tests involve data-driven processing, for example, memory would be
demonstrated on priming tests only to the extent that the study task required
data-driven processing; conversely, because most recall and recognition tests
involve conceptually-driven processing, memory would be demonstrated on
those tests to the extent that the study task required conceptually-driven

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STRUCTURAL AND PROCESSING ACCOUNTS 215

processing. In general, however, manipulations that require conceptually-

driven processing have little or no effect on implicit tests, and manipulations
that require data-driven processing have little or no effect on explicit tests.
Although data-driven and conceptually-driven are usually assumed to
correspond to bottom-up and top-down, respectively, Roediger conceded that
the term data-driven is a misnomer:
“…higher level (top-down) processes must be used in recognizing such
displays [a black-and-white fragmented picture of a Dalmatian]. In all likeli-
hood, repetition of these procedures produces the long-term perceptual prim-
ing effect, not lower-level (data-driven) processes. In verbal tests, the
processes are likely lexical or involve the visual word system (Nelson,
Keelean & Negrao 1989; Tulving & Schacter 1990; Weldon 1991); in non-
verbal tests, priming may result from processes in a ‘geon assembly layer’
(Biederman & Cooper 1991) or a structural descriptions system (Schacter
1990). The point is that the processes that are primed are not as low level as is
implied by the term data-driven” (Roediger & Srinivas 1993, p. 25).

Transfer-appropriate processing and conscious awareness

Conscious recollection is not implicated in the performance of sensorimotor

skills, which are carried out automatically. In fact, pausing to reflect on how to
carry out a skilled act may even impair its performance. Although he differs
from memory-systems advocates in terms of what makes a given task implicit
or explicit, Roediger (1990b) has adopted the view that conscious awareness
is associated with memory performance on explicit tests and that implicit tests
tap an unaware form of retention.

Transfer-appropriate processing and implicit/explicit memory

The transfer-appropriate processing account of functional dissociations on

explicit and implicit tests rests on four basic assumptions: (1) Memory perfor-
mance will benefit to the extent that the operations required at encoding and
retrieval match. (2) Explicit and implicit tests typically require different
operations at encoding and retrieval. (3) Explicit tests typically require con-
ceptually-driven processes that require accessing the encoded meaning of
concepts or items that were processed by semantic or elaborative manipula-
tions, and so forth. (4) Implicit tests typically require data-driven processes
that require accessing the perceptual record of past experiences.

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216 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

By this account, tasks that tap the same memory system would not be
expected to yield the same dissociations in response to every independent
variable; rather, the prediction of a dissociation would depend on the process-
ing requirements during encoding and testing in each instance. Although
transfer-appropriate processing can account for functional dissociations on
implicit and explicit tests by normal adults, it fares less well in accounting for
the memory dissociations of clinical populations who have experienced neural
insult, such as amnesics and Korsakoff patients (Roediger et al. 1989a).
A number of researchers have argued that implicit memories are less
flexible than explicit memories in transferring or generalizing to similar tasks
(Cohen & Eichenbaum 1993; Dienes & Berry 1997; Squire 1992b, 1994).
Willingham (1997, 1998b), however, argued that this distinction was based on
studies in which the structural features of the stimuli were changed at the time
of testing. He presented evidence from other studies that implicit and explicit
memories transfer equally well if the processes engaged in during encoding
and retrieval match and that both forms of memory transfer equally poorly if
the processes during encoding and retrieval differ. By this argument, process-
ing differences in flexibility can be understood in terms of the transfer-
appropriate processing account (Roediger & Blaxton 1987).

Transfer-appropriate processing and infant memory

Evidence of functional dissociations on implicit and explicit tasks with infants

is difficult to explain within a transfer-appropriate processing approach. In the
evidence reviewed in Chapter 7, infants studied the material in exactly the
same way and were tested on it in exactly the same way in both the delayed
recognition and reactivation procedures. This commonality resembles the
requirements of a transfer-appropriate processing account. In the reactivation
task, however, infants were also exposed to a retrieval cue, or prime, in
advance of the test (a prior-cuing procedure; Spear 1978). Because the
memory was forgotten at the time the prime was presented and remained so
for periods ranging from minutes to hours after priming, depending on the
infant’s age or number of prior reactivations, the reactivation process per se
was not directly measured; that is, it was nonapparent. Presumably, the
processing that was initiated by the prime, which reactivated the previously
inactive memory, was strictly perceptual. If that processing differed from the
processing during study, then the transfer-appropriate processing account

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STRUCTURAL AND PROCESSING ACCOUNTS 217

might be applicable; however, given that the effect of priming was measured
during a recognition test and we cannot stipulate the kind of processing in
which infants initially engaged, this aspect of the processing analysis is
strained.
Although nothing in the infant’s behavior allows us to say whether
memory retrieval on a delayed recognition test is conscious or intentional, the
fact that infants do not recognize the reactivation stimulus at the time it is
presented as a memory prime allows us to conclude with confidence that
memory retrieval during reactivation does not result from a deliberate or
intentional search process and thus cannot be accompanied by conscious
awareness. For this reason, we attribute the retrieval that results from reactiva-
tion or priming to an all-or-none automatic, perceptual-identification process.
If the prime is able to reactivate the memory, then we can assume that its
structural or perceptual characteristics were represented in the infant’s
memory at the time of encoding — an assumption consistent with the transfer-
appropriate processing account.
The fact that manipulations such as interference or no interference,
shallow or deep level of processing, longer or shorter study time, and so forth
affect the magnitude of delayed recognition differently than they affect the
magnitude of reactivation, however, acceptance of the transfer-appropriate
processing account would force us to conclude that the operations required to
process these variables at the time of encoding and testing also differ. Yet,
processing differences between the delayed recognition and reactivation tasks
occur only at the time of retrieval. Thus, the onus for matching the input is
placed squarely on the conditions that prevail at the time of retrieval. In studies
with adults, differentiating the operations at the time of encoding is easier
because they can be instructed to attend to different aspects of the study
materials (i.e., engage in different types of processing), and at the time of
testing, the experimenter can provide material that either matched or not what
subjects were instructed to study.
Treisman (1992) referred to encoding and retrieval as perceiving and re-
perceiving, respectively. If an object had not originally been perceived, of
course, it could not be re-perceived. We have found it particularly useful to
focus on the type of processing in which infants and adults engage at the time
of retrieval. There are two fundamental kinds of visual processing — serial
and parallel processing (Treisman & Gelade 1980). Parallel processing is
automatic, preattentive, and rapid and occurs early in the visual system,

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218 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

whereas serial processing is deliberate, requires focused attention in an ele-

ment-by-element search, and occurs late in the visual system. In adults, visual
pop-out results from parallel processing: A single target that is embedded
amidst an array of homogeneous distractors is detected effortlessly and rap-
idly. The diagnostic for parallel processing is subjects’ insensitivity to the
number of distractors in which the target is embedded. In serial searches, the
amount of time required to detect a target (i.e., the RT slope) increases linearly
with the number of stimuli in the array that must be inspected, whereas in
parallel searches, the amount of time required to detect a target remains
constant (i.e., the RT slope is flat) over increasing numbers of stimuli in the
array.
In infants, visual pop-out has been reported in 3-month-olds (Rovee-
Collier et al. 1992a) and 6-month-olds (Bhatt et al. 1994) in both delayed
recognition and reactivation tasks and is similarly insensitive to the number of
distractors. Rovee-Collier, Bhatt and Chazin (1996) trained 6-month-olds to
kick to produce movement in a block mobile that displayed +s on all sides.
Twenty days later, after they had forgotten the task, infants were exposed to a
mobile that contained a single + block amidst a number of blocks that
displayed Ls or a single L block amidst +s during a reactivation treatment (see
Figure 8.6). The number of distractors ranged from 4 to 12. Twenty-four
hours later, all infants were tested with the training mobile (i.e., a mobile
displaying all +s).
Typically, reactivation fails if the prime contains more than a single novel
object (Rovee-Collier et al. 1985b). If the pop-out display captured infants’
attention via a parallel process, however, then only the familiarity or novelty
of the single, attended target should affect reactivation. Therefore, we pre-
dicted that if the unique novel target popped out and captured attention, the
reactivation treatment would be unsuccessful, despite the overwhelming num-
ber of training objects in which it was embedded; if the unique training object
popped out and captured attention, however, then the forgotten memory
would be reactivated despite the overwhelming number of novel objects in
which it was embedded.
In fact, during the 24-hour test, these predictions were borne out. Infants
whose reactivation mobile displayed a single novel target exhibited no reten-
tion, behaving as if they had received no reactivation treatment at all. In
contrast, infants whose reactivation mobile displayed a single training target
exhibited excellent retention. More importantly for the parallel-processing

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STRUCTURAL AND PROCESSING ACCOUNTS 219

Figure 8.6. A pop-out mobile that was used during reactivation with 6-month-olds. This
pop-out mobile contained a single target (L) amidst eight distractors (+s). All infants were
trained and tested with a mobile containing nine blocks. For infants in the novel pop-out
reactivation condition, all blocks on the training and test mobile displayed +s; for infants in
the familiar pop-out reactivation condition, all blocks on the training and test mobile
displayed Ls.

argument, the magnitude of pop-out was the same irrespective of the number
of distractors on the reactivation mobile (see Figure 8.7). Only when the
reactivation mobile contained 13 objects were the predictions reversed — and
for an uninteresting reason: Because the single object was centered in the
display, the largest number of objects on the reactivation mobile obscured it.
In the delayed recognition task at 6 months of age, Bhatt et al. (1994)
found evidence that a top-down serial process can override the automatic
parallel process. Whereas 3-month-olds exhibited significant 24-hour reten-
tion on a delayed recognition test if the test mobile displayed the training
character as the target (pop-out) stimulus but not if it displayed a novel one, 6-
month-olds exhibited significant 24-hour retention whether the single target
was the training character or it was novel and the six distractors were training

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220 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 8.7. Mean baseline ratios as a function of the number of blocks on the reactivation
mobile (set size). A unique novel (open square) or familiar (filled square) block was
embedded amidst either familiar or novel distractor blocks, respectively, on the reactivation
mobile. Whether the reactivation mobile was an effective memory prime was assessed 24
hours later. An asterisk indicates that the memory was reactivated (M baseline ratio
significantly > 1.00). In both the novel and familiar reactivation conditions, test perfor-
mance over set sizes from 5 to 11 blocks did not differ.

characters. Because the single familiar target popped out, the single novel one
must have popped out as well. In the latter instance, however, infants must
have engaged in an attention-demanding serial (element-by-element) search
or they would not have located the predictive cue(s) that enabled them to
exhibit retention. Thus, although there are age-related changes in perceptual
processing, we argue that these are changes in processing speed — not in the
fundamental processes (or systems) that underlie memory performance. Here,
between 3 and 6 months, infants processed the test stimulus more rapidly, just
as they process the prime more rapidly at 6 than at 3 months of age (Hildreth &
Rovee-Collier 1999a).
Musen and Treisman (1990) related parallel and serial processing to

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STRUCTURAL AND PROCESSING ACCOUNTS 221

implicit and explicit memory, respectively. Whereas Tulving and Schacter

(1990) viewed parallel processing as an operation of the perceptual represen-
tation system, Roediger and Blaxton (1987) interpreted it in terms of transfer-
appropriate processing.

Multiple-entry modular memory system (MEM)

The multiple-entry modular model (MEM) describes a unitary memory frame-

work within which different cognitive processes are associated with indepen-
dent processing subsystems that interact with each other to a greater or lesser
degree to give rise to a memory (Johnson 1983). The term multiple-entry
refers to the fact that any given event can create multiple entries (or traces) in
all subsystems. Originally, Johnson envisioned three subsystems — the sen-
sory system, the perceptual system, and the reflection system. The sensory and
perceptual subsystems were specialized to detect and preserve information
about stimuli and relationships among them, whereas the reflection system
was specialized for preserving self-generated thought processes. Subse-
quently, Johnson (1991b) combined the sensory and perceptual subsystems
into a single perceptual system with two subsystems (P-1, P-2) and expanded
the reflection system to include two subsystems (R-1, R-2). The P-1 sub-
system corresponded to the original sensory system and recorded information
pertaining both to modality-specific (e.g., vision, smell, touch) and amodal
(e.g., intensity, frequency, solidity, rate of change) properties of stimuli,
whereas the P-2 subsystem recorded information about the phenomenal prod-
ucts of perception, such as the identity of objects and events. The components
of the reflective subsystem could also function alone or interact. These sub-
systems and the supervisory and control processes are illustrated in Figure 8.8
(top panel).
In addition, each of the four memory subsystems (P-1, P-2, R-1, R-2) was
endowed with a unique set of component processes that allow people to sustain,
organize, and revive information. As defined by Johnson and Chalfonte (1994,
pp. 315–316), the P-1 processes are extracting (invariants from perceptual
arrays), tracking (moving stimuli), locating (stimuli), and resolving (a percep-
tual array into primitive perceptual units). These processes are involved in the
acquisition of various perceptual-motor skills. The P-2 processes are structur-
ing (or abstracting a pattern of organization across a temporally or spatially
extended stimulus), placing (objects or events in spatial relation to one an-

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222 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 8.8. A multiple-entry modular memory system (MEM). Top panel: Two reflective
subsystems (R-1, R-2) and two perceptual subsystems (P-1, P-2). Reflective and perceptual
subsystems can interact through a control (the supervisor) and monitoring (the executive)

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STRUCTURAL AND PROCESSING ACCOUNTS 223

process of R-1 and R-2, respectively. These processes are the means by which the percep-
tion and reflection subsystems interact. They are depicted as cones passing through the
planes that represent the different subsystems. The size of the ellipses at the intersections of
the cones and planes indicates the extent to which each of these processes is involved in the
activities of each subsystem. Thus, the executive process has greater access to the reflection
system than to the perception system and greater access to P-2 than to P-1. Middle panel:
The component processes of R-1 and R-2. Bottom panel: The component processes of P-1
and P-2. ©1991, Plenum Publishing Corporation; adopted with permission. From M.K.
Johnson, Reflection, reality monitoring, and the self. In R. Kunzendorf (Ed.), Mental
imagery: Proceedings of the Eleventh Annual Conference of the American Association for
the Study of Mental Imagery (pp. 3–16). New York: Plenum.

other), examining (or perceptually investigating one or many aspects of a

stimulus array), and identifying (objects and events by combining perceptual
primitives to yield a sense of what something may be or is). P-2 processes
interact to give rise to the phenomenal world of objects and events that make up
a meaningful environment (see Figure 8.8, bottom panel).
In general, R-1 processes are nonstrategic; they include noting (identify-
ing relations among activated information), shifting (changing activation from
one aspect of a stimulus to another), refreshing (prolonging or extending the
persistence of ongoing activation), and reactivating (activating currently inac-
tive information). In contrast, R-2 processes are strategic; they include discov-
ering, initiating (changing one’s perspective by strategically seeking ways to
activate inactivated aspects of information), rehearsing (producing and recy-
cling self-generated codes for activated information, usually with the intent to
keep information accessible in a reportable format), and retrieving (searching
for and self-presenting cues that are not currently active). Whereas refreshing
and rehearsing are processes that operate on active information, reactivating
and retrieving are processes that operate on inactive information (see Fig-
ure 8.8, middle panel). Although they share common agendas, the source of
information used for refreshing and reactivating (R-1 processes) has been
characterized by Johnson and Chalfonte (1994, p. 318) as often being “a
fortuitous combination of agendas and cues” such as noting “agendas and cues
that were previously active together;” in contrast, the information used for
rehearsing and retrieving (R-2 processes) is intentionally self-generated.
Finally, R-1 and R-2 processes have different agendas (i.e., goals, inten-
tions, purposes), collectively called supervisor and executive processes, re-
spectively. These agendas are the means by which reflective and perceptual

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224 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

processes interact (see Figure 8.8, top panel) and can be as simple as a task
demand (“identify the pronouns”) or as complex as a script that specifies the
combination of component processes and the order in which they must be
engaged. Whereas supervisor processes (R-1) are more holistic and global,
executive processes (R-2) are more deliberate and analytic (Johnson & Hirst
1993).

MEM and conscious awareness

In MEM, conscious awareness is neither a defining characteristic of a particu-

lar memory subsystem or process nor a causal agent for different types of
memory (Tulving 1985). Rather, it is an emergent process:
“In MEM, the phenomenal experience of consciousness emerges from [vari-
ous combinations of] component cognitive activities — that is, cognitive
activities involved in perceiving and reflecting confer consciousness rather
than the other way around. If you disrupt some of these activities, you disrupt
consciousness, but it is not possible to disrupt consciousness without inhibit-
ing or disrupting at least some aspects of these activities” (Johnson & Hirst
1993, p. 258).

Earlier, Johnson and Raye (1981) argued that conscious recollection (i.e.,
experiencing a sense of pastness in remembering) is the consequence of a
reality-monitoring process in which a person decides whether a memory
originated in an actual experience (the perception system) or in imagination
(the reflection system) on the basis of its attributes. Presumably, the memory
of an actually experienced event is more vivid, highly detailed, contains
spatiotemporal details, and generally consists of more sensory or perceptual
attributes than a memory of an imagined event, which arises in the reflection
system. In addition, it is consistent with related memories. On the other hand,
an inability to discriminate between the attributes of actually perceived and
self-generated events (i.e., a break-down of reality-monitoring) can lead to
confabulation, when the individual treats an entry in the reflection system as if
it originated in the perception system (Johnson 1991a).

MEM and multiple memory systems

Whereas multiple memory systems are characterized by the common content of

the information about an event that each system encodes and stores (e.g.,

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STRUCTURAL AND PROCESSING ACCOUNTS 225

episodic information, semantic information, procedural information, percep-

tual representations, declarative information, nondeclarative information, etc.),
MEM cuts across memory content and instead distinguishes the common
processes that are required to perform various cognitive activities. Thus,
episodic and semantic memories are the products of interactions of the same (or
some of the same) component processes distributed across different sub-
systems. Likewise, whereas multiple memory systems, in some views, do not
interact (Schacter & Sherry 1987; Squire 1986, 1987), the component processes
of MEM interact within and between its subsystems, depending on the require-
ments of the task at hand. For this reason, these component processes are
viewed as part of a single memory system.
Recall that in Tulving’s (1972, 1983) scheme, episodic memories are
distinguished from semantic memories by two critical features — they are
accompanied by a conscious awareness of having previously experienced an
event and their time and/or place of occurrence can be specified. In MEM,
however, there are not separate stores for autobiographical and generic memo-
ries. Rather, a memory is judged by the rememberer to be autobiographical or
not. This is accomplished by a reality-monitoring process (see preceding
section) in which its attributes are evaluated for the degree of perceptual and
emotional detail. In MEM, spatiotemporal attributes do not have a privileged
status but are simply among the memory attributes that are evaluated. Like-
wise, in MEM, conscious awareness is not a defining characteristic of episodic
memory but is conferred on the memory only if it is judged to be autobio-
graphical (see preceding section).
Finally, MEM side-steps the proliferation problem that results from the
creation of a new memory system to account for each new functional dissocia-
tion that is found within tasks previously thought to tap an existing system
(e.g., Tulving 1993; Tulving & Schacter 1990). The different combinations of
existing subprocesses, programmed in different functional orders, can accom-
modate the processing of content as diverse as riding a bicycle, solving a
crossword puzzle, recognizing a face, or remembering directions to a party.
Likewise, disruptions in specific subprocesses can account for specific pat-
terns of deficit, whereas disruption of an entire memory system would pre-
sumably result in a deficit for all of the memories stored in that
system-episodic, procedural, or whatever.

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226 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

MEM and transfer-appropriate processing

MEM is consistent with the predictions of transfer-appropriate processing in

that both assume that the processes that are active at the time of testing match
those that were active at the time of encoding. Although at first blush, the
processes associated with perception and reflection seem similar to data-
driven and conceptually-driven processing, respectively, they are quite differ-
ent. For one thing, MEM subsystems and processes interact, so that memory
performance rarely reflects only perception or reflection, but memory perfor-
mance by the transfer-appropriate processing account is attributed to one type
of processing or the other. In addition, reflection and perception both contrib-
ute to processing that is considered to be conceptually-driven (for discussion,
see Johnson & Hirst 1993).
In addition, MEM is more complex than the transfer-appropriate process-
ing framework; as a result, it can account for more complex cognitive perfor-
mance. For the same reason, it is better equipped to account for deficits in
cognition. Because combinations of component processes comprise functional
subsystems, a breakdown in any process could disrupt any of the subsystems to
which that component contributed and, as a result, could produce a variety of
patterns of functional deficit. Neuroanatomical data that localize the brain
regions or pathways that may be implicated in the different component pro-
cesses further increase MEM’s potential explanatory value. Evidence of an
impaired ability to bind item and location information in amnesia (Chalfonte,
Verfaellie, Johnson & Reiss 1996), for example, suggests that damage to the
hippocampal structure disrupts reactivating (Johnson & Chalfonte 1994).
Likewise, frontal-lobe damage, which often results in confabulation (profound
source confusion), led to ERP (event-related potential) studies that implicated
the right prefrontal cortex in the evaluation of automatically activated informa-
tion (familiarity, perceptual detail), which is necessary for both recognition and
source identification (Johnson, Kounios & Nolde 1996; Johnson & Raye
1998). Neuroimaging studies, in turn, have implicated the left prefrontal cortex
in both the reflectively guided retrieval of specific details and the more
difficult, systematic evaluation of confirming and disconfirming information,
which are necessary for source attributions (Nolde, Johnson & D’Esposito
1998). Being so general, the transfer-appropriate processing framework cannot
provide as satisfactory an account for the data of amnesics as either MEM or
structural accounts (Roediger et al. 1989a, 1990).

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STRUCTURAL AND PROCESSING ACCOUNTS 227

MEM and implicit/explicit memory

According to MEM, dissociations on implicit and explicit memory tasks

simply reflect the fact that the tasks tap entries in different processing sub-
systems. Because many tasks involve processes from most or all of the
subsystems, the extent to which a task relies more heavily on processes from
one system or another usually determines whether it is described as implicit or
explicit. As we have seen, few if any implicit and explicit tasks are process-
pure (Jacoby 1991). Thus, an implicit memory test such as perceptual identifi-
cation of a degraded picture would rely heavily on component processes from
the perception system (P-1, P-2) to process the physical features or structure of
the stimulus but would also be likely to engage component processes from the
reflective system (e.g., noting relationships between parts, shifting attention
from one aspect of the figure to another). Conversely, an explicit version of
the test would rely more heavily on component processes from the reflection
system, but the component processes from the perception system would still
be recruited to process the physical features of the stimulus.
Accordingly, a memory dissociation on implicit and explicit tasks does not
mean that the two tasks depend on different underlying processes. Rather, it
means that implicit and explicit tasks reflect the relative reliance of different
tasks on different perceptual or reflective subprocesses. As Shimamura (1990)
argued, if memory performance on a particular implicit task is not impaired by
a given experimental manipulation or subject variable (age, amnesia), but
memory performance on a particular explicit task is, then this dissociation can
be taken as evidence that the implicit task recruited a particular process that the
explicit task did not. Because many of the other processes recruited in both tasks
are the same, however, the products they generate may not be accurately
characterized as different or independent forms of memory.

Developmental sequence of MEM subsystems

Johnson and colleagues described the developmental sequence of the four

subsystems from infancy to adulthood as P-1, P-2, R-1, and R-2 and specu-
lated that the four subsystems may have evolved in the same sequence
(Johnson 1991a; Johnson & Chalfonte 1994; Johnson & Hirst 1993). As we
observed earlier, however, evolution is not linear (see Functional Incompat-
ibility of Operations, this chapter).

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228 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

As an example that P-1 develops before P-2, Johnson and Hirst (1993)
noted that infants engage in visual tracking before they can recognize some-
thing as familiar. Evidence for this example and others that one might think of,
however, is either absent or contradictory. Although newborn infants can
track a visual stimulus, they can also distinguish their mother’s voice from that
of a stranger — and prefer it (DeCasper & Fifer 1980). Moreover, newborns
tested 33 hours after birth can distinguish a tape-recording of their mother
reading a familiar Dr. Seuss passage (i.e., one that she had read aloud for 20
min a day during the last 6 weeks of gestation) from a tape-recording of their
mother reading a novel Dr. Seuss passage (DeCasper & Spence 1986). Fur-
ther, newborns prefer the familiar passage.
In the same chapter, however, Johnson and Hirst acknowledged that a
particular memory subsystem or process should not be associated with a
particular age:
“it would be a mistake simply to characterize a human infant as ‘having’ only
P-1 and P-2 subsystems, or to characterize a young child as ‘getting’ R-2
processes at some particular age. For example, some aspects of reflective
processes (e.g., reactivation) may operate from quite early on (Rovee-Collier
1990). Furthermore, specific learning occurs in all subsystems throughout the
lifespan. Acquisition of new information in any particular subsystem depends
on acquisition of prior information. Consequently, differences in ‘sophistica-
tion’ of the subsystems at a given age are partly the consequence of what has
already been learned by the different subsystems. One might have a know-
ledgeable P-1 system and a less educated R-2 system or vice versa” (Johnson
& Hirst 1993, pp. 252-253).

MEM and infant memory

MEM offers a number of distinct advantages for analyses of infant memory.

First, it captures the complexity of memory without requiring that particular
neural mechanisms be functionally mature. Because the developmental time-
table by which different brain mechanisms become functionally mature in
humans is behaviorally based and largely unknown, MEM’s reliance on
cognitive processes rather than neural systems eliminates this problem. Second,
by emphasizing the interaction between different subsystems and processes in
most tasks, MEM does not associate a particular type of task with an underlying
process (i.e., does not make the flawed assumption that a task is process-pure).
Third, MEM eliminates conscious awareness as a defining (or ill-defined)
characteristic of explicit memory. Fourth, it allows the different subsystems to

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STRUCTURAL AND PROCESSING ACCOUNTS 229

develop at different rates depending on an individual’s prior experiences. Fifth,

MEM does not grant special status to autobiographical memory. Of course,
whether the R-2 component processes are within the capability of preverbal
infants will remain in the realm of speculation until someone figures out how
to measure introspective processes in nonverbal organisms, which seems
unlikely. Nonetheless, the bulk of measurable memory phenomena in preverbal
infants is readily accommodated by the P-1, P-2, and R-1 subsystems and their
component processes.
MEM is generally consistent with research findings from infants. Johnson
and Hirst (1993) observed, for example, that reactivating in MEM (an R-1
process) may be analogous to reactivation in infant memory studies. In fact, for
subjects of all ages, reactivating an inactive memory makes it available for
integration with other memories, distortion, and so forth. There are, however,
some problems with this analogy. In the infant literature, reactivation is
considered to be an implicit, automatic priming process that is either directly or
indirectly (as in mediated priming) cued by an external stimulus (for review, see
Chapter 7). Johnson and Chalfonte (1994), however, defined reactivation as an
internally generated repetition of a memory. Even if the R-1 subsystem were to
develop relatively early in infancy, however, this would not challenge Johnson
and Hirst’s (1993) proposal that the sequence of development of the subsystems
is P-1, P-2, R-1, and R-2.
Three lines of evidence from reactivation studies with infants lead us to
conclude that the R-1 subsystem does develop early in the first year of life.
First, memories can be reactivated in infants as young as 2 months of age
(Davis & Rovee-Collier 1983; Rovee-Collier, Hartshorn & DiRubbo 1999).
Second, Barr and Vieira (1999) found that previously associated information
that had become inactive (the memory of the train) could be reactivated by
exposing infants to either member in the association — either the puppet or the
train. Exposing infants to a partial puppet demonstration, for example, reacti-
vated the forgotten memory of the train that was associated with it; as a result,
infants again responded to the train during the ensuing long-term memory test.
This example exactly parallels one of the examples of R-1 reactivating that
was cited in Johnson and Chalfonte (1994) and confirms that the R-1 sub-
system is active by at least 6 months of age. And third, the memory of kicking
to move a mobile in a distinctive context was reactivated 2, 3, and 4 weeks
after it was forgotten by exposing infants to only the distinctive context — the
mobile was not present at the time of the exposure (Hayne & Findlay 1995;

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230 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Rovee-Collier et al. 1985a). This example also exactly parallels one of the
examples of R-1 reactivating that was cited in Johnson and Chalfonte (1994)
and confirms that the R-1 subsystem is active by at least 3 months of age. In
the preceding examples, we cannot say whether infants’ memories were
indirectly reactivated in response to internally-generated cues, as is required
of reactivating in MEM. However, we can say that reactivation in examples 2
and 3 was indirect and mediated by a prior association.
If reactivating in MEM and reactivation in infants and animals are the
same, then the proposed appearance of the four memory subsystems in phy-
logeny must be rethought. Johnson and Chalfonte (1994) cited evidence of
reactivating (MEM) in rats, but reactivation effects have been documented in
organisms at all phyletic levels — from the sea snail Hermissenda (Matzel,
Collin & Alkon 1992) to humans (see Chapter 7).

Conclusions

Both of the two major multiple-memory-systems accounts that have been

advanced to explain the functional memory dissociations that are exhibited by
brain-damaged and normal (instructed) adults hold that the memory system
that mediates explicit memory (i.e., episodic or declarative memory) develops
quite late in the infancy period relative to the memory system that mediates
implicit memory (i.e., semantic or procedural memory), but data obtained
directly from infants indicate otherwise (see Chapter 7). In contrast, the trans-
fer-appropriate processing account does not presume a particular develop-
mental sequence. Because infants’ study and test materials are identical, it
adequately explains infants’ memory performance in delayed recognition
tasks; however, its account of their memory performance in reactivation tasks
is less clear-cut. The MEM model postulates that the processing components
develop sequentially, with the perceptual processes (P1, P2) developing ear-
lier than reflective processes (R1, R2). Recently, the authors of this model
acknowledged that some processing subcomponents of the reflective system
(reactivation) might appear relatively early in the infancy period. They use the
term reactivation differently than it is used in the infant literature, however,
where it refers exclusively to automatic (nonreflective) perceptual processing.
In short, no theoretical models — either multiple-memory-systems models or
processing models — have yet provided a fully satisfactory account of the
functional dissociations in infant memory.

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CHAPTER 9

Interactions between Implicit

and Explicit Memories in Infants

This chapter considers the fate of implicit memories after they have been primed, the effect
of priming when a memory is active versus when it is not, and the effect of priming with a
novel stimulus after delays when a memory can still be explicitly retrieved. The data in this
chapter were obtained exclusively from infants, but they have major implications for
everyday memory in individuals of all ages.

In laboratory experiments on implicit and explicit memory, individuals study

a list of words or pictures and then are asked a simple question to which they
typically respond with an item from the study list whether instructed to do so
(the explicit memory task) or not (the implicit memory task). Even though the
same response may be expressed on both types of test, different theoretical
models propose that the memory which is retrieved is different. Squire
(1992a), for example, proposed that the declarative and nondeclarative sys-
tems encode different memories, and so the memories that are expressed on
the explicit and implicit tests that tap those systems would be different.
Mandler (1980), however, argued for a single memory system in which a
memory is either automatically activated without contextual information or
intentionally retrieved with contextual information. By this account, the im-
plicit memory would presumably be a leaner version of the explicit memory.
Johnson (1983; Johnson & Hirst 1993), who also proposed a theoretical
account based on a unitary memory system, differentiated the memories that
are expressed on implicit and explicit tests in terms of the combinations of
subprocesses that create them. Strategic R-2 processes are more likely to be
engaged on an explicit memory test, whereas nonstrategic R-1 processes are
more likely to be engaged on an implicit memory test (see Chapter 8). Because
interactions involving R-2 processes endow a memory with different qualities

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232 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

than R-1 processes alone, the product of these subprocesses should also differ.
In some ways, however, the distinction between explicit and implicit
memories is not so clear-cut. Adults’ memories that were originally explicit,
for example, can eventually become automatic — a defining characteristic of
implicit memories (Mandler 1985) — if they are repeatedly practiced or
retrieved (Logan 1988, 1990, 1992; Logan & Klapp 1991; Willingham &
Goedert-Eschmann 1999). Logan (1988), for example, proposed that specific
instances of past encounters with a given stimulus and the response that was
made to it are stored as episodic memories that are retrieved when the stimulus
is presented on a future occasion. Over repeated retrievals of prior processing
episodes involving the same stimulus and response (i.e., practice), memory
performance becomes faster and more automatized. Thus, learning to drive a
car with a standard transmission initially requires a great deal of focused
attention, and the dos-and-don’ts from specific prior training episodes are
recalled and rehearsed during later practice sessions. Eventually, however,
clutching, shifting, accelerating, braking, turning on the turn signals or wind-
shield wipers, and steering are performed automatically and effortlessly in a
coordinated manner.
Although some researchers might classify learning to drive as a skill or
procedural memory (Squire 1992a), more complex behavioral acts that defy
simple classification as procedural memories also can become automatic. A
common experience such as driving the car to work — which may require
more than an hour, traverse many miles, and require negotiating all manner of
traffic and hazards, can become frighteningly automatized. Although we
arrive safely at the office, we have no recollection of getting there or what we
saw or did en route.
In everyday life, implicit and explicit memories presumably guide our
normal commerce with the environment and influence our understanding.
Although the long-term effects of retrieving implicit and explicit memories
are clearly important for our future behavior, memory studies with adults have
given little consideration to whether these effects are the same or different.
Whereas instructing normal adults to respond with the first word that comes to
mind (an implicit memory task) yields immediate memory performance that is
similar to that of amnesics, the long-term effect of priming on the subsequent
memory performance of normal and abnormal populations surely differs.
When this question has been asked of normal adults, it has been framed only in
terms of the effect of retrieving explicit memories on future retrieval. In

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EXPLICIT-IMPLICIT INTERACTIONS 233

addition to becoming automatized (Logan 1988), this effect is to facilitate

present understanding (Ross & Bradshaw 1994), produce forgetting of the
memory content that was not previously retrieved (Anderson, Bjork & Bjork
1994; Loftus & Loftus 1974), and protract retention within a limited period of
time (Bjork 1975; Schmidt & Bjork 1992; Roediger & Payne 1982). In
contrast, the long-term effect of priming has gone largely unstudied.
One potentially important factor that distinguishes priming in amnesics
from priming in normal adults is that amnesics are incapable of recognizing
the target item at the time of priming, but normal (instructed) adults are.
Although amnesics are brain-damaged, whether the memory is recognizable
at the time of priming may also affect how long it is subsequently remembered
by normal adults. The duration for which normal adults remember an explicit
memory, for example, increases with the effortfulness or difficulty of its
retrieval, which is operationally defined as the time between original encoding
and subsequent retrieval (Bjork 1975; Schmidt & Bjork 1992). Although the
duration for which an implicit memory is subsequently remembered is un-
known, it might also be affected differently by when the prime was encoun-
tered. On the other hand, because the retrieval of an implicit memory is
effortless and automatic (Besson et al. 1992; Hasher & Zacks 1977; Mandler
1980; Musen & Treisman 1990), its effect on subsequent retention may be
independent of the retention interval.
Conversely, the long-term consequences of priming when the memory is
still recognizable (as it is in priming studies with normal adults) has also not
been explored. Nor have researchers studied the long-term consequences of
priming with a novel stimulus. In the adult literature, priming has been
described as hyperspecific (Tulving & Schacter 1990). Changes in the physi-
cal appearance of a previously studied object usually — but not always —
reduce the amount of priming (see Richardson-Klavehn & Bjork 1988, for
review). The specificity that characterizes effective primes for adults is also
found in reactivation studies with infants whose memories have been forgot-
ten (see Chapter 7). Given that exactly the same stimulus rarely recurs in
nature twice (Wyers, Peeke & Herz 1973), however, we should ask whether
an incidental encounter with a slightly different stimulus might implicitly
prime a memory that can still be retrieved on a recognition test, and, if so, how
that encounter affects future retention.
Given the evidence presented in previous chapters that memory process-
ing by preverbal infants and healthy adults is qualitatively the same, infants

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234 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

may be an ideal population for answering some of the questions that are less
amenable to experimental study with adults. Because 3-month-olds forget
within only 1 week, and 6-month-olds forget within only 3 weeks, their
subsequent retention following administration of a prime after the original
memory was forgotten can be assessed within a reasonable time frame. In
addition, the functional significance of priming when the memory is active
versus when it is not, as well as the effect of priming with a novel stimulus
when the memory is active, can be studied with relative ease. The results of
studies with infants that addressed some of these questions are reviewed
below.

Similarities between infants’ implicit and explicit memories

Despite the numerous functional dissociations that have been found between
implicit and explicit memories in infants (see Chapter 7), other aspects of their
implicit and explicit memories are very similar.

Magnitude of retention

The magnitude of explicit memories declines as the interval between training

and recognition testing increases for both infants (Hartshorn et al. 1998b; Hill
et al. 1988; Sullivan et al. 1979) and adults (Cave 1997; Tulving et al. 1982).
In contrast, the initial magnitude of implicit (reactivated) memories is inde-
pendent of the interval between training and priming for both adults (Tulving
et al. 1982) and infants (Davis & Rovee-Collier 1983; Hayne 1990; Hayne &
Findlay 1995; Hildreth & Rovee-Collier 1999a; Sheffield & Hudson 1994).
These data suggest that explicit and implicit memories are different. Once an
implicit memory has been reactivated, however, its subsequent magnitude
declines with the time since reactivation, just as the magnitude of an explicit
memory declines with the time since training (Hildreth & Rovee-Collier
1999b). In this regard, then, explicit and implicit memories are similar.

Duration of retention

The duration of retention of explicit memories in both delayed recognition and

deferred imitation tests increases linearly with age (Hartshorn et al. 1998b;

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EXPLICIT-IMPLICIT INTERACTIONS 235

Figure 9.1. The duration of retention between 3 and 12 months of age after original training
(dark bars) and after reactivation (striped bars). In both cases, the duration of retention
increases linearly with age.

Hayne et al. 1997; Herbert & Hayne 2000), and the duration of retention of
implicit (reactivated) memories does as well. As can be seen in Figure 9.1, the
duration of a reactivated memory increased linearly between 3 and 12 months
of age in both the mobile and train tasks (Hildreth & Rovee-Collier 1999b).

Rate of forgetting

Since the time of Ebbinghaus (1885), forgetting has been recognized as the
most ubiquitous characteristic of adult memory. This characteristic describes
infant memory as well. Over the first year of life, infants gradually forget
explicit memories over the interval between training and the delayed recogni-
tion test, and they gradually forget implicit (reactivated) memories over the
interval between priming and testing as well. Figure 9.2 shows that the rate of
forgetting explicit and implicit memories was the same over the first year of
life, whether infants were studied with mobiles or trains (Hildreth & Rovee-

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236 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Figure 9.2. The rate at which infants between 3 and 12 months of age forget the original
memory (open squares) and the reactivated memory (filled squares). At each age, the
memory prime was administered 1 week after infants of a given age last remembered the
task. Asterisks indicate no retention (M baseline ratio not significantly > 1.00).

Collier 1999b). This common pattern occurred despite the fact that both
explicit and implicit memories were forgotten over increasingly longer peri-
ods of time with age. A cursory inspection of Figure 9.2 offers no clue as to
which function represents infants’ forgetting of the reactivated memory.
The preceding results are particularly impressive when one considers that
the forgotten memory was always reactivated 1 week after infants of a given
age last remembered the task. When this 1-week delay is taken into account,
we see that exposing infants to a single memory prime at least doubles the
accessibility of the memory over the entire first year of life (see Figure 9.3).
The robustness of this effect encourages us that it probably occurs for older
individuals as well.

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EXPLICIT-IMPLICIT INTERACTIONS 237

Original Memory

Figure 9.3. The retention benefit of a single reactivation over the first year of life. The
maximum duration of retention (weeks) of the training memory is shown before reactiva-
tion (solid line; see Figure 6.6) and after reactivation (dashed line). The single memory
prime was given 1 week after infants of each age last remembered the task.

Although a single memory prime appears to recycle a forgotten memory so

that it is remembered again for as long as it originally was, presenting
additional primes may protract its duration even more. Hayne (1990) gave
one, two, or three reactivation treatments to 3-month-olds. During each reacti-
vation treatment, she merely showed infants the training mobile, in motion, for
3 min. As expected, infants recognized the mobile for as long after a single
reactivation as they had after original training, whether the forgotten memory
was reactivated 2 weeks or 3 weeks after training. After being primed once,
the reactivated memory persisted for 3 days but not for 1 week, but after being
primed twice, the reactivated memory persisted for 2 weeks but not 3 weeks.
Moreover, the retention-enhancing effect of the second prime occurred
whether it was presented 3 weeks or 4 weeks after training. In the latter

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238 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

instance, retention was still seen 6 weeks after infants were initially trained —
a period almost half again their life-time. After being primed three times,
however, infants’ retention was no longer than when they were primed only
once.
Although Hayne found that three reactivations were not as effective as
two, we have found that whether additional reactivations can protract reten-
tion even longer depends on their timing. In a subsequent mobile study with
infants who were only 2 months old when they were trained, we gave infants
the same reactivation treatments as Hayne but spaced them every 3 weeks
through 26 weeks of age (Rovee-Collier et al. 1999). Immediately preceding
each reactivation treatment, we administered a 3-min delayed recognition test
in order to determine whether or not infants exhibited retention. After three to
five reactivations, these younger infants eventually exhibited significant re-
tention 3 weeks after their last reactivation.
Taken together, these data reveal that the durations of explicit and im-
plicit memories differ after a memory has been multiply primed.

Accessibility of different types of memory attributes

Recall that the specific details of both the original mobile and the encoding
context are represented in infants’ training memory. As the interval between
training and testing increases, infants progressively forget the specific details
of the original mobile but continue to remember its general features or gist,
thereby generalizing to novel test mobiles (Rovee-Collier & Sullivan 1980). If
infants are trained and tested in a highly distinctive context, however, the
context primes these forgotten details via a serial attention-gating mechanism.
As a result, infants are able to discriminate the original mobile from a novel
one after longer delays, when they can still recognize the context (Butler &
Rovee-Collier 1989). Likewise, at both 3 and 6 months of age, an implicit
memory is also highly specific to the details of the original cue and context
(Hartshorn & Rovee-Collier 1997; Hayne & Rovee-Collier 1995; Shields &
Rovee-Collier 1992). In this respect, then, explicit and implicit memories are
similar.
After the implicit memory has been forgotten, however, the memory
attributes that represented the details of the encoding context are apparently
lost, because the second time the memory is reactivated, the context can be
different. Moreover, after the twice-reactivated memory has been forgotten,

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EXPLICIT-IMPLICIT INTERACTIONS 239

the memory attributes that represented the details of the original mobile
apparently are lost, because the twice-reactivated and twice-forgotten memory
can be reactivated a third time by a different cue as well as in a different
context (Hitchcock & Rovee-Collier 1996). These data reveal that explicit and
implicit memories differ in the accessibility of their different attributes after
they have been multiply primed, perhaps because multiply primed memories
are older, and older memories are more fragile.
In 1972, Tulving proposed that information is more readily lost from the
episodic than from the semantic memory system. Furlong (1951, cited in
Tulving 1983, p. 17) had similarly hypothesized that retrospective [i.e., epi-
sodic] memory became nonretrospective [i.e., semantic] memory as the con-
text faded. These statements are consistent with the preceding evidence that
contextual information becomes lost from infants’ memories over the course
of repeated reactivations. If an episodic memory eventually becomes context
free because its details pertaining to the time and place of its origin have been
lost, however, then this raises questions about the usefulness of distinguishing
different memory systems in the first place. Does, for example, an episodic
memory become a semantic one, shifting memory systems, after this informa-
tion has been lost? Or does context-specific information become lost because
a memory has been transferred from the episodic to the semantic memory
system? Or does such a transfer even occur? The loss of context specificity
seems to be better accommodated by envisioning memory as a single system
that is characterized by different degrees of specificity, different routes of
access, and so forth (e.g., Mandler 1985).

The effect of priming an active memory on retention

The effect of priming (reactivation) on subsequent retention also depends on

the state of the memory when the prime is administered. Recall that Hayne
(1990) found that two reactivation treatments, each given when the memory
was inactive (13 and 20 days after training), protracted retention for 2 weeks,
whereas a single reactivation treatment given 20 days after training protracted
retention for less than 1 week. She also found that three reactivations given 6,
13, and 20 days after training were no more effective than one (see Fig-
ure 9.4). Hayne speculated that the third reactivation may have lost some of its
effectiveness because it was given only 1 week after the second reactivation

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240 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

treatment — a point when the twice-reactivated memory was still active. But
why would the state of the memory make a difference?
The answer was suggested a number of years ago by a study in which
researchers used memory primes of different durations. Gordon, Smith and
Katz (1979) reported that exposing adult rats to a memory prime for 15 s
reactivated a memory of active avoidance, whereas exposing rats to the prime
for 75 s extinguished it. Subsequently, Arnold and Spear (1993) obtained a
similar result with preweanling rat pups: Exposing pups to a memory prime
for 5 s or 15 s reactivated the forgotten training memory, but exposing them to
the prime for 30 s did not. Given evidence that a memory can be modified only
when it is active (Lewis 1979), Gordon (1981) had hypothesized that reactiva-
tion of a memory begins when a prime is initially exposed and that, after the
memory has been reactivated, the continued presence of the prime can lead to
new learning that can modify it. By this account, then, a lengthy prime
provides an opportunity for the reactivated memory to be modified counter-
acting the original effectiveness of the prime.

Figure 9.4. The duration of retention (days) following one, two, or three reactivation
treatments at 3 months of age. An asterisk indicates significant retention.

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EXPLICIT-IMPLICIT INTERACTIONS 241

In fact, Hayne (1990) observed this result in a control group that was
included to determine whether the retention benefit of two reactivations
resulted because the memory prime was presented twice or because the total
duration of priming was twice as long. When Hayne had exposed infants to
two 3-min primes — each when the memory was inactive, their forgotten
mobile memory had not only been reactivated but had been protracted for 2
weeks. When she exposed infants to one 6-min prime — also when the
memory was inactive, however, infants exhibited no retention at all only 24
hours later. By Gordon’s (1981) account, the 6-min prime initially reactivated
the inactive memory, but its continued exposure enabled new learning that
either competed with or subtracted from what infants had learned before.
If a lengthy exposure to the prime once the memory is inactive can impair
retention, then a shorter exposure to the prime when the memory is already
active should have a similar effect. In fact, when Hayne (1990) gave infants a
third 3-min reactivation treatment only 1 week after the second reactivation
treatment — a time when the twice-reactivated memory was still highly
accessible, infants exhibited excellent retention 1 day later but none 1 week
later — when the benefit of two reactivations had still been seen. Apparently,
presenting the 3-min prime when the memory was still accessible was long
enough to partially counteract the retention benefit produced by the second
reactivation but not so long that it eliminated the effectiveness of the second
reactivation altogether.
As another test of the effect of priming on an accessible memory, Adler et
al. (2000) gave 3-month-olds an initial 3-min reactivation treatment either
immediately (0 days) or 3 days after training — when the original memory
was still relatively accessible — and asked how it affected infants’ subsequent
retention. Although 3-month-olds can remember an explicit memory for 5 but
not 6 days after training is over (Hayne 1990), infants who were primed for 3
min immediately after training exhibited significant retention 6 but not 7 days
later; and infants who were primed 3 days after training exhibited significant
retention 7 but not 9 days after training. Thus, priming an accessible memory
provided a slight memory boost that increased with the delay between training
and priming. Priming when the original memory was active, however, did not
boost retention nearly as long as priming when it was not (e.g., Hayne 1990;
Hildreth & Rovee-Collier 1999b).

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242 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

The effect of a novel prime on retention of an active memory

In the preceding study, Adler et al. (2000) presented the prime 3 days after
training. Because 3-month-old infants have forgotten the specific details of
their original training mobile after this delay, we speculated that the effect of
the prime on the active memory might be different if it were novel. Previously,
we found that priming with a novel mobile for 3 min immediately after
training (day 0), when the memory does not have to be retrieved at all,
retroactively interfered with infants’ recognition of the original mobile the
next day, but this effect was temporary and disappeared within 2 days (Rossi-
George & Rovee-Collier 1999). The same interference phenomenon had
occurred when infants were primed with a novel mobile 3 days after training
and tested with the original mobile the next day (Rovee-Collier et al. 1994).
This phenomenon was also temporary: Although infants who were primed
with a novel mobile 3 days after training had failed to recognize the training
mobile 1 day later, Adler et al. found that they did recognize it 7 days but not
9 days afterward. Thus, as before, a 3-min exposure to a novel prime tempo-
rarily interfered with the original memory. Because priming the active
memory with either a novel mobile or the original mobile 3 days after training
protracted retention for the same duration (i.e., for an additional 2 days), Adler
et al. concluded that the common retention boost was mediated by the general
features that the novel mobile shared with the original one. (Recall that
priming occurred at a time when infants could not behaviorally differentiate a
novel mobile from the training one.) In other words, the prime in Adler et al.
did not protract retention because it was novel but because it was effectively
the same as the training mobile.
Because the original memory becomes progressively less accessible over
time until it finally cannot be retrieved on a delayed recognition test at all, we
thought that what infants actually learned about a novel prime might be
analyzed in more depth if it were exposed at more points along the original
forgetting function. To do this, we had to turn to older infants, who remember
longer. Therefore, we trained 6-month-olds in the mobile task and primed
them with a novel mobile (mobile B) after delays ranging from 1 to 13 days,
testing them with either the training mobile (mobile A) or mobile B 24 hours
later (Muzzio & Rovee-Collier 1996).
Previously, Boller et al. (1995) had primed 6-month-olds with a novel
mobile immediately after training (day 0) and had found that they recognized

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EXPLICIT-IMPLICIT INTERACTIONS 243

both mobile A and mobile B 24 hours later. In the present study, we found that
if 6-month-olds were primed with a novel mobile after delays ranging from 1
to 8 days, then they subsequently recognized only mobile B but not mobile A;
but if they were primed with a novel mobile after delays ranging from 9 to 13
days, then they subsequently recognized neither mobile A nor mobile B (see
Figure 9.5). Because unprimed infants of this age can recognize mobile A for
14 days and can also discriminate it from mobile B after that same delay, we
concluded that priming with the novel mobile after delays longer than 1 day
had interfered with their recognition of mobile A whether they had recognized
mobile B 24 hours later or not.
In addition, both mobile A and mobile B reactivated the training memory
3 weeks later if the novel prime was exposed only 1 day after training, but only
mobile B reactivated the memory if the novel prime was exposed 13 days after

Figure 9.5. The time line for the onset (+) of three qualitatively different consequences of
priming an active memory — memory impairment, source confusion (memory facilitation),
and categorization. After training in the mobile task for 2 days, 6-month-olds were primed
for 2 min with a novel mobile after different delays (exposure delay) between 1 and 14 days
and were tested 1 day later.

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244 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

training. These data are intriguing because infants who were primed with
mobile B after either delay had not recognized mobile A 24 hours later. This
result suggested that mobile A was still represented in the training memory
after the 1-day novel prime but was not after the 13-day novel prime. Because
other attempts to demonstrate that mobile A was still represented in the
training memory after being primed with mobile B after a long delay also
failed, we concluded that its details had probably been replaced in the training
memory by mobile B. These data, like the data of Hitchock and Rovee-Collier
(1996), suggest that older memories are more fragile.
The preceding results reveal that priming with a novel mobile when
infants’ training memory is still relatively accessible can produce either
memory facilitation (i.e., facilitated recognition of the novel prime) or memory
impairment (i.e., impaired recognition of original mobile), depending on the
timing of the prime in relation to the original training event. However, a third
effect of priming a relatively accessible memory with a novel stimulus can
also occur — a categorization effect. Exposing adults to at least two different
exemplars of a category facilitates their subsequent responding to novel
category members (e.g., Flannagan, Fried & Holyoak 1986; Fried & Holyoak
1984), and exposing infants to at least two different exemplars of a category
has the same effect. After being trained with mobile A in one session and
mobile B in another, for example, both 3- and 6-month-olds recognize a novel
category member (mobile C) 1 day later (Hayne et al. 1987; Shields & Rovee-
Collier 1992). The same result occurs when 3-month-olds are primed with a
novel mobile (mobile B) immediately after being trained for 2 days with
mobile A. Apparently, the prior memory of training with mobile A that is
retrieved at the outset of session 2 is recoded to include mobile B. As a result,
infants subsequently behave to mobile C as if they had actually been trained
with two different mobiles in the first place (Rovee-Collier et al. 1993a).
Otherwise, infants trained for 2 days with the same mobile would have
discriminated the novel test mobile (mobile C).
Muzzio and Rovee-Collier (1996) found a similar categorization effect,
but it too depended on when the prime was presented in relation to original
training. When 6-month-olds were primed with mobile B after delays of 1, 3,
6, or 9 days, they responded to mobile C after the two longest priming delays
(6 and 9 days) but not after the two shortest ones (see Figure 9.5). The fact that
infants responded to a completely novel test mobile means that their memory
of mobile A was still intact after 9 days (i.e., the interference by mobile B after

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EXPLICIT-IMPLICIT INTERACTIONS 245

delays up to this point had been temporary) and distinguishes their memory
performance as a genuine categorization effect (recall that categorization
requires exposure to two different category members — A and B).
An important finding of this study is that failing to observe an effect of
recently encountered information or observing one effect (e.g., memory im-
pairment) but not another (e.g., memory facilitation or categorization) cannot
be taken as evidence that priming an accessible memory with a novel stimulus
has no other effects. Here, after priming delays when infants subsequently
recognized neither mobile A nor mobile B (i.e., 9 days), they still recognized
mobile C. Had they not previously been primed with mobiles A and B, then
they would not have responded to mobile C. Likewise, after priming delays
when they recognized neither mobile A nor mobile C, they recognized mobile
B. This study clearly demonstrates that the effect of a prime when the memory
is accessible is strictly determined by the point on the forgetting function at
which it is presented.

Conclusions

Studies with infants have answered several questions about the relation be-
tween implicit and explicit memories that are difficult to address with adults.
They have revealed that implicit memories assume a number of the character-
istics of explicit memories. Over the first year of life, for example, implicit
memories that were forgotten before they were primed are remembered for as
long as explicit memories, and their pattern of forgetting is also the same.
Memories that are still accessible at the time of priming are not remembered as
long as memories that are forgotten. Nonetheless, the extent to which an
already accessible memory is protracted by priming varies with the delay
between training and priming as it does with the delay between training and
recognition testing, even though the duration of retention after priming is not
as great when the memory is accessible. Finally, we previously found that
implicit and explicit memories enter into the same functional relationships
with the context at 3 and 6 months of age (Borovsky & Rovee-Collier 1990;
Butler & Rovee-Collier 1989; Hartshorn & Rovee-Collier 1997; Hayne &
Rovee-Collier 1995; Shields & Rovee-Collier 1992).
Taken together, these findings seem inconsistent with the notion that
explicit and implicit memories are distinctly different memories that are

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246 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

encoded by structurally different memory systems (Squire 1992a). Rather,

because explicit and implicit memories appear to be the same once they have
been retrieved and reactivated, respectively, we propose that they are not
different memories at all but are actually the same memory that has been
retrieved via different routes — either implicitly or explicitly (see also Crowder
1988; Mandler 1985). Speaking colloquially, “If it walks like a duck and
quacks like a duck, then it must be a duck!” Whether these different routes of
access are parts of different memory systems, however, remains unanswered.

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CHAPTER 10

Epilogue

In this chapter, we summarize our basic conclusions and reflect on some of the popular
notions that are based on earlier assumptions about the development of implicit and explicit
memory. Finally, we consider the implications of recent memory research with infants for
theory and research on memory in general.

The practice of attributing cognitive competencies to immature organisms

without actually studying them is not new. In 1885, Wilhelm Preyer, who
pioneered the study of human embryonic development, wrote:
“For thousands of years children have been born and lovingly tended and
watched by their mothers, and for thousands of years learned men have
disputed over the mental growth of the child, without even studying the
children. As a rule, the experimental physiologist seldom visits the nursery,
even when he is a father.”

This practice is nowhere more apparent than in the field of memory develop-
ment, where the central problem is to specify how the superior memory of
adults evolves from the memory abilities of infants. Where do we stand today
in terms of its solution? In one proposed solution, adult memory is cast as the
product of multiple memory systems that develop hierarchically during the
infancy period (Bachevalier & Mishkin 1984; Schacter & Moscovitch 1984;
Squire 1987, 1992a; Tulving 1983, 1993). In the preceding chapters, however,
we reviewed evidence that this solution is not correct for either human or
animal infants, primate or nonprimate. Even if adults possess multiple memory
systems that decline sequentially, those systems most certainly do not develop
hierarchically.
In the face of mounting evidence against it, some scientists have contin-
ued to defend the hierarchical development hypothesis. Why? We can only
speculate that they are either philosophically committed to this solution, have

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248 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

ignored the overwhelming evidence against it, or have not understood it. One
clear source of misunderstanding has centered on the kinds of memory that are
measured in studies of mobile conjugate reinforcement. Nelson (1995), for
example, likened infants’ conditioned footkicks during delayed recognition
tests to the conditioned limb flexion response of the cat. Given that limb
flexion is reflexively elicited by electrical shock, this analogy is obviously
incorrect. Operant kicks are not elicited, and their magnitude obviously cannot
depend on the parameters of the eliciting stimulation. Unlike conditioned limb
reflexes, whether the infant kicks above baseline during a delayed recognition
test depends on the informational content of the test stimulus and the test
context. Moreover, prior to 1 year of age, young infants do not immediately
respond to a priming stimulus, whereas elicited reflexes occur within millisec-
onds. In fact, an infant’s conditioned kicking or lever-pressing is no different
from an adult’s pressing a response key, touching a video screen, circling a
word on a piece of paper, or verbalizing “yes” or “no” as an index of
recognition.
For others, whether infants are capable of explicit memory or behave like
amnesics seems to boil down to the question of whether they can consciously
recollect having seen a stimulus before — a question that cannot be directly
answered. This stance is reflected in the following quote from Eacott (1999, p.
47):
“…a behavioral measure of recall, such as lever pressing, presents a problem,
as all memory abilities may not be alike. An ability to recall facts and events
has been contrasted to the ability to learn and remember how to use skills and
strategies. Memories of facts and events can be brought to mind and be made
consciously available, whereas skills and strategies are often implicit and not
accessible to consciousness. These two aspects of memory are called declara-
tive and nondeclarative (procedural) memory, respectively. The long-term
memory abilities demonstrated in infants may be an example of nondeclara-
tive memory. If so, it may be that they do not have…a late-developing
declarative memory system (Bachevalier & Mishkin 1984).”

In the preceding quote, Eacott classified infants’ kicks and lever presses on
retention tests as skills. Then, asserting that memory for skills does not require
conscious recollection, she concluded that infants’ memory performance —
like that of amnesics — lacks conscious awareness. Bjorklund (2000) ex-
pressed the same view in his text on children’s thinking:
“…conditioning experiments with infants do not seem to require conscious
awareness. That is, unlike most of the memory we will discuss in this chapter,

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EPILOGUE 249

it was not explicit — it did not involve children consciously retrieving

information from their long-term stores” (p. 239).

In the same chapter, he described an increase in the duration of retention with

age as a unique characteristic of explicit memory. Yet, infants between 2 and
18 months of age exhibit delayed recognition for increasingly longer durations
in conditioning studies, as do infants between 6 and 24 months of age in
studies of deferred imitation (see Chapters 6, 7, and 9). We assume, therefore,
that the underlying distinction still boils down to the question of conscious
awareness.
In the same vein, Mandler has complained that mobile studies cannot
possibly reveal anything about human memory (or any other higher-level
cognitive process) because they measure “only conditioning,” and even “cock-
roaches” (1990, p. 515) and “the lowly flatworm” (1998, p. 296) can be
conditioned. This complaint similarly rests on a commitment to conscious
awareness as the sine qua non of explicit memory and the conclusion that
conditioning is devoid of such awareness. In her basic argument, however,
Mandler failed to distinguish between the learning process, which entails
associating the representations of two events in short-term memory and may
well be automatic, and the memory process, which entails retrieving informa-
tion from long-term memory back into short-term memory and may or may not
be automatic. Operant conditioning, however, is not even an underlying
learning process — it is a procedure whose underlying mechanisms are not yet
understood.
As it turns out, a major obstacle to gaining a conceptual handle on the
development of implicit and explicit memory has been the eagerness of
scientists to label the tasks that have been used with infants as either implicit
or implicit. Response-to-novelty tasks, for example, which used to be consid-
ered as implicit tasks (Nelson 1995), are now described as explicit memory
tasks; operant conditioning tasks, as procedural (implicit) memory tasks;
imitation tasks, as declarative (explicit) memory tasks, and so forth. Tasks per
se, however, are neither one nor the other. Just as adults can complete a word
stem or word fragment either implicitly or explicitly, for example, so can
infants perform an imitation, conditioning, or response-to-novelty task either
implicitly or explicitly. As in studies with adults, whether a particular memory
task is implicit or explicit depends on how it is solved. If a memory task is
solved by infants or adults via a prior-cuing procedure, or priming, then it is an
implicit memory task. If a memory task is solved by infants or adults via a

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250 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

contemporaneous-cuing procedure (which, for adults, requires instructions to

respond on the basis of a particular prior experience), then it is an explicit
memory task. Thus, for example, a word stem could be used as either a
memory prime in an implicit task or a retrieval cue in an explicit task,
depending on the instructions. The failure of researchers to recognize this very
fundamental fact has obfuscated the analysis of infant memory.

A look to the future

Studies with infants have yielded novel findings about basic memory phenom-
ena that are difficult to study with older children and impractical to study with
adults. These studies have revealed, for example, that implicit and explicit
memories “behave” identically after they have been retrieved. This finding
suggests that implicit and explicit memories are not different memories from
different systems (Squire 1992a) nor even different forms of memory (Graf &
Schacter 1985) but are the same memory that has simply been retrieved via
different routes — either implicitly or explicitly (Crowder 1988; Mandler
1985). Another finding from studies with infants pertains to the functional
significance of retrieving implicit and explicit memories. Memories that have
been primed remain accessible for as long as they were originally, being
forgotten only gradually and at the same rate. Priming the memory when it is
active, however, has different consequences than priming the memory when it
is not, and refreshing the memory has different consequences yet. All prolong
the life of a memory, but some conditions are more likely to facilitate its
distortion. These findings have major implications for whether and for how
long we can access and use that memory in the future. Finally, if a memory is
repeatedly retrieved either explicitly or implicitly, its contents will change.
New information can be added, and old information can be lost — and some
kinds of information are added and lost more readily. These changes distort
both the specificity and accuracy of the memory that was originally encoded
and thereby will impact what we remember and understand in the future.
These and other findings from studies of infant memory speak directly to
the three major phenomena that, according to Estes (1997), any satisfactory
theory of memory must address — memory retrieval, forgetting, and memory
distortions. Memory theories that have been formulated solely from adult data
and that do not accommodate new findings from infants are incomplete and

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EPILOGUE 251

inadequate. In the past, memory data from infants have been put through a
sieve that lets pass only those fragments that are commensurate with preestab-
lished notions of how memory works at different ages or what different tasks
or procedures can reveal. This is wrong — and it is bad Science. Data from
critically controlled studies with infants must be taken at face value as evi-
dence of what organisms can and cannot do and how their prior experiences
affect their current behavior.
Let us be clear: We do not seek more satisfactory theories of memory
development — such theories inevitably turn out to be theories of language
development. If not, then, what? We seek more satisfactory theories of
memory. Although major aspects of both the brain and behavior change
dramatically over ontogeny, the basic processes of learning and memory and
the general principles that describe them do not. Only by drawing on a
complete data base will memory theorists be able to test the generality and
affirm the validity of their predictions. Only from such a rich data base will
psychologists be able to construct a truly satisfactory theory of memory.

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early phase of infancy. Child Development, 47, 1032–1044.
Adler, S.A., Gerhardstein, P., & Rovee-Collier, C. 1998. Levels-of-processing effects in
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Author Index

Locators annotated with f indicate figures.

Locators annotated with t indicate tables.

A Arnold, H. M., 240, 254

Aaron, F., 185, 197, 198, 265 Atkinson, R. C., 164, 254
Abravanel, E., 114, 253
Ackil, J., 186, 279 B
Adler, S. A., 137, 140, 149, 153, 169, Babkin, P. S., 67, 254
170, 180, 181, 197, 202, 203, 241, 242, Bachevalier, J., 16, 55, 83, 84, 84f, 85,
244, 253, 263, 280, 281 85f, 86, 86f, 87, 87f, 88, 89, 89f, 90, 91,
Adolphs, R., 56, 62, 253, 256 92, 93, 93f, 94, 95, 102, 123, 190t, 213,
Agamanolis, D., 30, 288 247, 248, 254, 271, 273, 276, 277
Agayoff, J. L., 133, 253 Bachman, D. S., 109, 256, 287
Aggleton, J. P., 56, 283 Baddeley, A., 12t, 190, 255
Ajuriaguerra, J. de, 72, 253 Baddeley, A. D., 213, 262
Albert, M. S., 59, 282 Bahrick, L. E., 100, 117, 255
Alberts, J. R., 67, 68, 69t, 253, 257 Baillargeon, R., 104, 118, 255
Albertson, S. A., 74, 270 Bainbridge, V., 183, 270
Alexander, R., 138, 279 Ballesteros, S., 12t, 13, 178, 179, 260
Alkon, D. L., 230, 272 Barnat, S. A., 198, 255
Allen, J. N., 109, 287 Barnes, J. M., 153, 255
Allen, S. W., 183, 253 Barr, R., 114, 115, 123, 129, 131, 139,
Alpert, N. M., 59, 282 145, 151, 156, 157, 162, 185, 186, 187,
Alvarado, M.C., 90 197, 198, 203, 205, 208, 210, 229, 235,
Alvarez, P., 52, 53f, 90, 253 255, 257, 266, 272
Alvarez-Royo, P., 17, 52, 253, 259 Bartus, R. T., 69t, 255, 261
Amabile, T. A., 154, 186, 253 Bauer, P. J., 16, 115, 118, 121, 124, 144,
Amaral, D. G., 52, 53f, 286, 290 151, 156, 186, 187, 256
Ames, E. W., 99, 267 Baveux, P., 25, 278
Amsel, A., 69t, 265 Beauregard, M., 90, 254
Anderson, J. R., 190, 253 Bechara, A., 56, 62, 256
Anderson, M. C., 158, 233, 254 Beck, A. T., 172, 256
Angeli, S. J., 54, 254 Beck, J. L., 162, 275
Angevine, J. B., 30, 288 Becker, J. T., 41, 54, 56, 272, 276
Anglin, J. M., 196, 254 Beer, B., 69t, 261
Angulo Y Gonzales, A. W., 66, 254 Behr, S. E., 180, 269

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292 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Bellos, S. A., 138, 288 Bower, B., 186, 257

Bendele, M. S., 12t, 258 Bower, G. H., 172, 191, 192, 200, 257,
Bennett, L., 107, 285 287
Benson, D. F., 30, 260 Bowers, J., 18, 76, 128, 129, 139, 140,
Bentin, S., 153, 155, 256 283
Bergstrom, L. I., 178, 260 Boyer, K., 102, 262
Berntson, C. G., 109, 256 Bradshaw, G. L., 233, 280
Berntson, G. G., 109, 287 Brewer, J. B., 58, 59, 263
Berry, D., 216, 262 Brickson, M., 90, 94, 123, 254
Besson, M., 168, 233, 256 Bridges, K., 197, 257
Best, C. T., 148, 256 Broadbent, N., 54, 259
Bhatt, R. S., 112, 131, 134, 145, 147, Brodale, S., 43, 258
148, 153, 163, 166, 182, 185, 197, 198, Brody, L. R., 117, 257
218, 219, 234, 256, 262, 265, 281 Brogden, W. J., 203, 257
Biederman, I., 12t, 140, 178, 179, 202, Brooks, B. M., 175, 176, 257
215, 256 Brown, A. L., 190t, 196, 197, 199, 200,
Bjork, E. L., 158, 233, 254 276
Bjork, R. A., 8, 17, 128, 158, 159, 161, Brown, A. S., 74, 137, 138, 150, 151,
183, 233, 254, 256, 270, 279, 283 164, 273
Bjorklund, A., 71, 263 Bullemer, P. T., 12t, 14, 26, 276, 289
Bjorklund, D. F., 2, 248, 256 Bundy, R. S., 99, 259
Blake, R., 138, 179, 258 Burch-Vernon, A., 186, 279
Blanchard, S., 109, 285 Butler, J., 184, 185, 238, 245, 257
Blaney, P. H., 172, 256 Butters, N., 56, 57, 257, 266, 272
Blaxton, T. A., 150, 183, 190, 191, 214, Byrne, B., 75, 144, 169, 258
214t, 216, 221, 256, 279
Boaz, T., 168, 233, 256 C
Bolhuis, J. J., 43, 256 Calder, A. J., 56, 283
Boller, K., 131, 141, 153, 154, 155, 186, Caldwell, D. F., 107, 257
203, 204, 242, 244, 257, 281 Campbell, B. A., 68, 69t, 71, 126, 142,
Bolles, R. C., 185, 257 146, 147, 198, 257, 258, 266, 286, 288
Boniface, J., 114, 115, 123, 145, 185, Campbell, E. H., 69t, 257
186, 257, 266 Campos, J. J., 103, 278
Bonner, R. T., 46, 277 Campos-de-Carvalho, M., 112, 145, 147,
Booker, J., 18, 76, 128, 129, 139, 140, 148, 234, 265
283 Canas, J. J., 27, 275
Borovsky, D., 141, 145, 156, 184, 185, Carley, J. L., 2, 268
186, 234, 245, 257, 267 Carlson, T. B., 182, 258
Borza, M., 184, 266, 281 Carroll, M., 75, 144, 169, 258
Borza, M. A., 153, 203, 242, 244, 280, Cave, C. B., 138, 150, 151, 179, 180,
281 202, 234, 258
Bost, P. R., 179, 180, 258 Cawley, S., 54, 259
Bottalico, K. S., 162, 275 Cermak, L. S., 57, 196, 257, 258
Bousfield, W. A., 175, 257 Chalfonte, B. L., 74, 80, 81, 221, 223,
Bouton, M. E., 185, 257 226, 227, 229, 230, 258, 265, 269

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AUTHOR INDEX 293

Challis, B. H., 214, 280 Cuddy, L. J., 158, 260

Chazin, S., 218, 281 Cummings, J. L., 30, 260
Chen, K. S., 46, 117, 286 Curran, T., 14, 261
Chiu, C. Y. P., 150, 283
Cho, Y. H., 43, 258 D
Churchland, A., 94, 102, 261 Daehler, M. W., 150, 264
Clark, H. H., 182, 258 Dallas, M., 12t, 77, 128, 158, 162, 168,
Clayton, K., 12t, 258 183, 268
Clifton, R. K., 105, 129, 264, 278 Damasio, A. R., 56, 62, 253, 256
Clower, R. P., 17, 52, 53f, 253, 259, 290 Damasio, H., 56, 62, 253, 256
Clubb, P. A., 115, 263 D’Amato, M. R., 2, 50, 259, 261
Cobb, R. I., 179, 180, 258 Davis, H. P., 71, 261
Coghill, G. E., 66, 259 Davis, J., 145, 229, 261
Cohen, D., 101, 123, 263 Dean, R. L., 69t, 255
Cohen, L. B., 99, 100, 116, 259, 289 Dean, R. L., III, 69t, 261
Cohen, N. J., 25, 29, 33f, 34, 35, 54, 56, Debner, J. A., 162, 261
190t, 211, 216, 259, 262, 263 DeCasper, A. J., 101, 228, 261
Cohen, R. L., 158, 162, 183, 259 Delacour, J., 37, 273
Collie, R., 114, 123, 259 Delaney, S. M., 12, 162, 178, 202, 283
Collin, C., 230, 272 Dell, G. S., 190, 200, 213, 272
Collins, A. M., 209, 259 DeLoache, J. S., 100, 259
Colombo, J., 99, 259 Demb, J. B., 164, 279
Colombo, M., 50, 54, 259 Denny, E. B., 172, 261
Connelly, A., 54, 288 Deruelle, C., 101, 123, 277
Cook, R. G., 76, 175, 178, 290 DeSchonen, S., 100, 101, 123, 277
Cooper, E. E., 12t, 140, 178, 179, 202, D’Esposito, M., 226, 276
215, 256, 286 DeVos, J., 104, 118, 255
Cooper, E. H., 162, 259 de Vries, J. I. P., 66, 261
Cooper, L. A., 12, 12t, 13, 162, 178, 179, Diamond, A., 88, 94, 102, 103, 104, 105f,
201, 202, 259, 260, 283 116, 117, 118, 123, 261, 262
Cooper, R. L., 69t, 260 Dienes, Z., 216, 262
Cork, R. C., 137, 180, 262, 269 DiGiulio, D. V., 75, 262
Corkin, S., 3, 29, 30, 31, 31f, 34, 56, 259, Dion, S., 115, 278
260, 263, 273 DiRubbo, M., 229, 281
Cornell, E. H., 76, 129, 131, 161, 178, Doar, B., 104, 262
260 Dodds, C., 100, 122, 272
Cornia, C., 17, 78, 282 Domato, G. C., 69t, 270
Correll, R. E., 40, 260 Dominowski, R. L., 12t, 262
Corwin, J., 78, 285 Domjan, M., 69t, 265
Coulter, X., 146, 258, 260 Dorfman, J., 137, 262
Craik, F. I. M., 168, 190, 260 Dougherty, L. M., 173, 267
Crowder, R. G., 8, 128, 158, 162, 164, Dow, G. A., 115, 255
178, 246, 250, 260 Dowden, A., 114, 115, 123, 156, 162,
Cruess, L., 94, 102, 261 255
Cruttenden, L., 103, 262 Dritschel, B. H., 213, 262

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294 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

DuFault, D., 154, 186, 281 Fried, L. S., 244, 263

Dunnett, S. B., 71, 263 Friedman, D. P., 88, 254
Durgunoglu, A., 183, 275 Friedman, J., 88, 276
Fuller, R. D., 172, 288
E Furlong, 239
Eacott, M. J., 248, 262
Earley, L. A., 149, 159, 164, 175, 184, G
185, 197, 203, 230, 262, 266, 281 Gabrieli, J. D. E., 29, 58, 59, 62, 263
Ebbinghaus, H., 235, 262 Gaddy, J. R., 68, 69t, 126, 258
Eich, E., 172, 183, 262, 271 Gadian, D. G., 54, 288
Eichenbaum, H., 25, 54, 216, 259, 262 Gage, F. J., 71, 263
Eimas, P. D., 180, 278 Galluccio, L., 142, 166, 176, 178, 265
Ekstrand, B. R., 12t, 262 Garcia, R., 101, 123, 263
Engen, T., 174, 262 Gardiner, J. M., 9, 74, 189, 263, 268
Enright, M. K., 129, 131, 145, 153, 156, Garrud, P., 41, 54, 274
157, 202, 263, 281 Gazzaniga, M. S., 191, 263
Erbaugh, J., 172, 256 Gekoski, M. J., 145, 153, 262, 263, 281
Esterson, J., 175, 257 Gelade, G., 134, 217, 287
Estes, W. K., 250, 262 Gelber, E. R., 99, 116, 259
Evancio, S., 159, 281 Gerhardstein, P., 140, 149, 169, 180, 197,
202, 253, 263
F Gerhardstein, P. C., 112, 145, 147, 148,
Fabre-Grenet, M., 101, 123, 277 185, 197, 198, 234, 265
Fagan, J. F., III, 91, 98, 100, 116, 125, Gershberg, F. B., 175, 264
262 Gewirtz, J. L., 110, 279
Fagen, J. W., 111, 129, 131, 141, 145, Gibertoni, M., 17, 78, 282
153, 156, 157, 160, 163, 172, 173, 174, Gibson, E. J., 197, 264
202, 262, 263, 276, 280, 281, 284 Gibson, G. E., 71, 260
Fanselow, M. S., 43, 269 Gilch, J., 112, 147, 148, 234, 265
Fantz, R. L., 98, 263 Goas, J. A., 69t, 255, 261
Feenan, K., 13, 27, 78, 285 Goedert-Eschmann, K., 232, 289
Feigenbaum, J. D., 54, 263 Gold, P. E., 69t, 71, 264
Field, T. M., 101, 123, 263 Goldfarb, T. L., 2, 268
Fifer, W. P., 101, 228, 261 Gordon, W. C., 149, 240, 241, 264
Findlay, N., 184, 202, 229, 234, 266 Gotlieb, G., 67, 278
Fischler, I., 168, 233, 256 Gottlieb, G., 67, 264
Fisher, C. M., 30, 288 Goubet, N., 105, 264
Fivush, R., 115, 263 Gould, S. J., 75, 264
Flagg, S. F., 190t, 282 Grabelle, M., 203, 242, 257
Flannagan, M. J., 244, 263 Graber, M., 104, 118, 255
Fleckenstein, L. K., 173, 262 Graf, P., 3, 7, 8, 9, 12t, 18, 22, 34, 56, 73,
Fleischman, D. A., 62, 263 75, 78, 128, 137, 139, 144, 153, 168,
Forrest, E. M., 43, 256 183, 250, 265
Fox, N. J., 103, 117, 118, 263 Granholm, E., 57, 257
Freud, S., 1, 263 Grant, D. S., 2, 279

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AUTHOR INDEX 295

Gratch, G., 103, 264 137, 142, 145, 147, 148, 151, 152, 153,
Greco, C., 119, 150, 156, 157, 160, 175, 156, 157, 159, 160, 162, 163, 175, 184,
197, 202, 203, 264, 266 185, 186, 197, 198, 202, 203, 218, 229,
Greco-Vigorito, C., 119, 159, 160, 266, 234, 235, 237, 238, 239, 241, 244, 245,
281 255, 257, 259, 264, 266, 276, 281
Green, L., 69t, 283 Heath, F. R., 183, 285
Greenbaum, J. L., 75, 144, 265 Heimann, M., 114, 123, 266
Greenberg, R., 101, 123, 263 Heindel, W. C., 56, 266
Greene, R. L., 22, 23, 24, 158, 162, 265 Hellawell, D. J., 56, 283
Gregg, B. E., 69t, 265 Hembree, E. A., 173, 267
Griesler, P. C., 175, 184, 197, 203, 230, Herbert, J., 147, 148, 151, 198, 235, 266
266, 281 Hermann, D. J., 2, 266
Griffin, D. R., 22, 265 Hernandez-Reif, M., 100, 117, 255
Groccia-Ellison, M., 109, 285 Hertel, P. T., 172, 174, 266
Gross, C. G., 50, 259 Hertsgaard, L. A., 115, 118, 121, 151,
Gross, J., 142, 153, 157, 266 156, 186, 255
Grossman, R. G., 67, 289 Herz, M. J., 233, 290
Guanowsky, V., 69t, 265 Hildreth, K., 111, 140, 141, 142, 151,
Gulya, M., 80, 131, 142, 156, 166, 176, 153, 157, 220, 234, 235, 241, 267
178, 182, 186, 203, 257, 265 Hill, W. H., 145, 234, 267
Gunderson, V. M., 91, 92f, 94, 265 Hinderliter, C. F., 142, 275
Hintzman, D. L., 8, 128, 190, 267
H Hirsh, R., 54, 60, 190t, 267, 277
Habibi, A., 12t, 258 Hirst, W., 25, 28, 214t, 224, 226, 227,
Haden, P., 7, 8, 12t, 18, 128, 168, 264 228, 229, 231, 269
Hagger, C., 90, 94, 123, 254 Hitchcock, D. F.A., 131, 157, 186, 239,
Haklstead, C., 69t, 270 244, 267
Hamburg, M., 2, 148, 269 Holyoak, K. J., 244, 263
Handelmann, G. E., 41, 54, 276 Honig, W. K., 190t, 267
Hankins, E., 134, 182, 218, 281 Hood, B., 105, 267
Hankins, L. L., 69t, 71, 264 Hooker, D., 66, 267
Hanna, E., 185, 265 Hubbard, J. I., 21, 267
Hardin, T. S., 172, 174, 266 Hudson, J., 152, 267
Hartman, M., 26, 179, 274, 276 Hudson, J. A., 129, 131, 133, 149, 210,
Hartshorn, K., 81, 111, 112, 129, 145, 234, 253, 284
147, 148, 160, 184, 185, 197, 198, 229, Hummel, J. E., 179, 286
234, 238, 245, 265, 281 Humphrey, T., 66, 67, 267
Hasher, L., 11, 74, 191, 233, 265, 269, Humphreys, M., 183, 287
278 Humphries, M. S., 175, 272
Hashtroudi, S., 12t, 25, 26, 283 Hunt, J. McV., 100, 267, 288
Hawkins, C., 162, 288 Hunt, R. R., 172, 261
Hawkins, R. D., 107, 109, 269 Hunter, M. A., 99, 267
Hayman, C. A. G., 25, 150, 153, 175, Hunter, W. S., 104, 267
266, 284, 287 Hurt, C. A., 180, 269
Hayne, H., 98, 114, 115, 119, 123, 131,

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296 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

I Kihlstrom, J. F., 137, 180, 262, 269

Idowu, A., 71, 260 Kim, J. J., 43, 269
Infurna, R. N., 69t, 286 Kimble, G., 107, 269
Inglin, F., 71, 283 Kinsbourne, M., 184, 190t, 269, 289
Inhelder, B., 190t, 278 Kintsch, W., 196, 270
Isingrini, M., 74, 267 Kirkham, N. Z., 94, 102, 261
Izard, C. E., 173, 267 Kirsner, K., 75, 144, 169, 183, 258, 270
Kittrell, M. W., 69t, 265
J Klapp, S. T., 232, 271
Jackson, J. H., 65, 75, 268 Klein, L., 174, 289
Jacobs, W. J., 190t, 268 Klein, P., 112, 145, 147, 148, 234, 265
Jacoby, L. L., 8, 12t, 17, 19, 77, 78, 125, Klein, P. J., 185, 197, 198, 255, 265, 270
128, 138, 158, 162, 168, 183, 190, 191, Klein, S. B., 69t, 270
214t, 227, 253, 260, 261, 268 Klein, S. J., 173, 174, 263
James, J., 107, 285 Knopman, D. S., 14, 26, 270, 276
Janowsky, J. S., 176, 284 Knowlton, B., 24, 285
Jarrard, L. E., 2, 268 Knowlton, B. J., 62, 270
Jarvik, M. E., 2, 268 Komatsu, S. I., 16, 73, 97, 139, 150, 270,
Java, R. I., 9, 74, 189, 263, 268 275
Jensen, R. A., 69t, 268 Kosslyn, S., 209, 276
Johnson, M., 56, 283 Kounios, J., 226, 269
Johnson, M. K., 11, 25, 28, 74, 80, 81, Krauter, E. E., 69t, 71, 258, 288
190, 191, 214t, 221, 223, 224, 226, Kucharski, D., 149, 285
227, 228, 229, 230, 231, 258, 265, 268, Kuebli, J., 115, 263
269, 276 Kunst-Wilson, W. R., 12t, 174, 175, 180,
Jolicoeur, P., 178, 269, 273 270
Jones, E. G., 50, 269 Kuypers, H. G. J. M., 50, 277
Jones, G. V., 23, 276
Jones, H. E., 106, 269 L
Joula, J. F., 164, 254 LaLomia, P. D., 27, 275
Landauer, T. K., 159, 161, 270
K Landers, W. F., 103, 264
Kagan, J., 1, 2, 103, 117, 118, 148, 263, Lang, A. E., 56, 282
269 Lavoie, D., 73, 270
Kandel, E. R., 57f, 107, 109, 269, 273 Law, J., 153, 175, 284
Kantrow, R. W., 106, 269 Leroy, P., 74, 267
Kaplan, M. G., 100, 269 Levan-Goldschmidt, E., 114, 253
Karmiloff-Smith, A., 126, 269 Levine, E., 109, 285
Katz, D. S., 240, 264 Lewandowsky, S., 183, 270
Kavanaugh, R. D., 114, 122, 272 Lewis, D. J., 240, 270
Keane, M. M., 62, 263 Light, L. L., 73, 74, 270
Keelean, M. J., 215, 275 Lindberg, M. A., 169, 270
Kendrick, D. F., 76, 175, 178, 290 Lippa, A. S., 69t, 255
Kennedy, C. B., 100, 122, 272 Lipsitt, L. P., 107, 270
Kesner, R. P., 43, 258, 269 Little, A. H., 107, 270

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AUTHOR INDEX 297

Lockhart, R. S., 168, 260 Mendelson, M., 172, 256

Loftus, E. F., 209, 233, 259, 270 Merriman, J., 156, 176, 178, 273
Loftus, G. R., 233, 270 Messing, R. B., 69t, 268
Logan, G. D., 232, 233, 270, 271 Meulemans, T., 14, 79, 273
Lucas, D., 129, 131, 145, 153, 156, 157, Miezin, F. M., 59, 286
281 Mikulka, P. J., 69t, 270
Lytle, L. D., 142, 258 Milliken, B., 178, 273
Milner, B., 3, 29, 30, 31, 32f, 35, 38, 40,
M 54, 57f, 73, 273, 276, 283, 284
Macaulay, D., 172, 183, 262, 271 Misanin, J. R., 69t, 142, 258, 265, 275
Macdonald, C. A., 150, 287 Mishkin, M., 49f, 55, 55f, 278
MacDonald, S., 115, 197, 198, 235, 257, Mishkin, M. M., 37, 40, 42f, 43, 45f, 48,
266 49f, 51, 52, 54, 55, 83, 84, 84f, 85, 85f,
Madigan, S., 76, 271 86, 86f, 87, 87f, 88, 89, 89f, 90, 91, 93,
Malamut, B. L., 43, 45f, 55, 85, 271, 273 94, 95, 117, 178, 190t, 213, 247, 248,
Malkova, L., 89, 89f, 90, 94, 254, 271 254, 271, 273, 274, 277, 288, 290
Mancall, E. L., 30, 288 Misiaszek, J., 137, 262
Mandler, G., 7, 9, 12t, 18, 22, 34, 56, 128, Mitchell, D. B., 13, 74, 76, 77, 137, 138,
164, 168, 180, 183, 191, 193, 214t, 144, 150, 151, 164, 273
231, 232, 233, 239, 246, 250, 264, 271 Mock, J., 172, 256
Mandler, J. M., 11, 16, 97, 109, 115, 118, Modigliani, V., 159, 279
121, 122, 123, 124, 139, 186, 190t, Moffitt, M., 2, 284
255, 271, 272 Mohr, J. P., 46, 284
Mangels, J. A., 62, 270 Moise, S. L., 2, 268
Marrott, H., 203, 272 Molloy, R. D., 162, 275
Marsh, G. R., 69t, 260 Moore, C., 12t, 13, 178, 179, 201, 260
Martinez, J. L., Jr., 69t, 268 Moore, M. K., 115, 272
Martone, M., 56, 57, 257, 272 Morrell, F., 62, 263
Matthews, A., 172, 288 Morris, R. G., 54, 263
Matzel, L. D., 230, 272 Morris, R. G. M., 38, 41, 54, 71, 273,
McCall, R. B., 99, 114, 122, 272 274, 283
McDonald, R. J., 61, 272 Morrongiello, B. A., 145, 153, 156, 157,
McDonough, L., 16, 118, 122, 186, 272 159, 262, 288
McDougall, W., 190t, 272 Morse, D. L., 107, 285
McFarland, D. J., 194, 272 Morton, J., 101, 123, 277
McGaugh, J. L., 61, 69t, 71, 264, 268, Moscovitch, M., 1, 2, 3, 8, 10, 12t, 14, 16,
277 25, 73, 83, 97, 107, 109, 115, 116, 117,
McKee, R. D., 16, 97, 118, 122, 123, 272 118, 121, 122, 123, 128, 138, 148, 153,
McKenney, M., 184, 279 155, 168, 190t, 196, 213, 247, 256,
McKenzie, W. A., 175, 272 274, 283, 288, 290
McKoon, G., 20, 190, 200, 213, 272, 278 Muller, K., 160, 265
McNamara, M. C., 69t, 260 Mulligan, N. W., 179, 274
McNamara, T. P., 138, 179, 258 Mumby, D. G., 53, 274
Meltzoff, A. N., 114, 115, 123, 185, 198, Murdock, B. B., 167, 175, 182, 274
255, 265, 270, 272 Murdock, B. B., Jr., 164, 278

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298 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Murphy, D. R., 74, 273 Olsen, P. L., 142, 275

Murray, E. A., 40, 51f, 52, 54, 90, 254, Olson, G. M., 197, 202, 276
274, 277 Olton, D. S., 16, 17, 22, 37, 41, 54, 214t,
Musen, G., 12, 24, 137, 138, 139, 151, 276, 284
155, 162, 179, 220, 233, 274, 285 O’Neill, J. B., 88, 254, 276
Muzzio, I. A., 153, 203, 242, 244, 274 Orbach, J., 35, 38, 40, 276
Myers, N. A., 129, 278 Osborne, J. L., 175, 282
Oscar-Berman, M., 46, 277
N Otto, T., 54, 262
Nadel, L., 16, 54, 73, 83, 88, 109, 148, Overman, W., 102, 277
190t, 268, 274, 275, 276
Nagy, Z. M., 142, 146, 275 P
Naito, M., 2, 16, 73, 75, 76, 97, 139, 144, Packard, M. G., 60, 61, 277
150, 169, 275 Paivio, A., 190t, 191, 277
Nakamura, Y., 180, 271 Pan, S., 186, 277
Neely, J. H., 183, 275 Pandya, D. N., 50, 277
Negrao, M., 215, 275 Pantle, A. J., 162, 259
Neill, W. T., 162, 275 Parke, R. D., 114, 122, 272
Nelson, C. A., 1, 9, 83, 97, 121, 122, 137, Parkin, A. J., 17, 73, 75, 78, 97, 277, 282
148, 190t, 192, 197, 199, 200, 248, Parkinson, J. K., 54, 277
249, 275 Parsons, P. J., 131, 285
Nelson, D. L., 27, 215, 275 Pascalis, O., 100, 101, 123, 277
Nelson, K., 1, 148, 190t, 196, 209, 275, Paskowitcz, S., 23, 276
276 Patterson, J., 218, 281
Newman, J. A., 142, 275 Paulson, G., 67, 278
Nichelli, P., 17, 78, 282 Paulson, G. W., 67, 277
Niederman, D., 103, 262 Pavlov, I. P., 106, 109, 278
Nilheim, K., 114, 123, 266 Payne, D. G., 233, 279
Nimmo-Smith, I., 213, 262 Payne, M., 56, 272
Nissen, M. J., 12t, 14, 26, 270, 276, 289 Pearl, R. A., 100, 259
Nolde, S. F., 226, 269, 276 Pearlman, M. A., 145, 263
Nowakowski, R. S., 88, 278 Pearlstone, Z., 131, 287
Nyberg, L., 24, 276 Peeke, H. V. S., 233, 290
Pendlebury, W. W., 109, 285
O Perlmutter, M., 2, 116, 289
Oakley, D. A., 190t, 276 Perris, E. E., 129, 160, 197, 244, 266, 278
Ochsner, K. N., 150, 283 Perruchet, P., 14, 25, 79, 158, 273, 278
O’Connor, J., 141, 257 Petersen, S. E., 59, 286
Ogilvie, J. C., 23, 276 Peterson, M. A., 12, 162, 178, 202, 283
Ohr, P., 156, 160, 163, 276 Petri, H. L., 49f, 55, 55f, 273, 278
Ohr, P. S., 173, 174, 263 Peuster, A., 102, 277
Ohta, N., 150, 153, 175, 270, 284 Phillips, R. R., 89, 273
Ojemann, J. G., 59, 286 Piaget, J., 1, 72, 103, 113, 122, 190t, 278
O’Keefe, J., 41, 54, 109, 274, 276 Pickens, J., 100, 117, 255
O’Leary, D. S., 75, 262 Pinel, J .P. J., 53, 274

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AUTHOR INDEX 299

Poldrack, R. A., 58, 59, 263 Ribner, D. R., 173, 262

Polkey, C. E., 54, 263 Ribot, T. A., 72, 279
Pomerleau, D., 107, 285 Riccio, D. C., 184, 186, 283
Postman, L., 153, 278 Richardson, R., 184, 279
Powell, T. P. S., 50, 269 Richardson-Klavehn, A., 8, 17, 128, 183,
Pratt, R. J., 99, 289 233
Prechtl, H. F. R., 66, 261 Riegler, G. L., 168, 280
Prete, K., 131, 186, 203, 257 Roberts, W. A., 2, 162, 279
Preuss, L., 9, 17, 24, 25, 28, 289 Rockland, C., 56, 62, 256
Preyer, W., 247, 278 Rodman, H. R., 50, 259
Prigot, J. A., 172, 174, 263 Roediger, H. L., III, 25, 77, 109, 150,
168, 183, 190, 191, 192, 213, 214,
Q 214t, 215, 216, 221, 226, 233, 279,
Quillian, M. R., 209, 259 280, 286
Quinn, P. C., 180, 278 Ronca, A. E., 109, 256
Rose, R. P., 69t, 71, 264
R Rose, S. A., 117, 150, 280
Radvansky, G. A., 74, 278 Ross, B. H., 190, 233, 253, 280
Raichle, M. E., 59, 286 Ross, B. M., 174, 262
Rajaram, S., 17, 109, 190, 191, 192, 226, Ross, H. W., 110, 279
278, 280 Rossi-George, A., 81, 153, 154, 203, 242,
Rakic, P., 88, 278 265, 280
Ramos, J. M. J., 43, 278 Rovee, C. K., 110, 111, 134, 280
Ramsay, D. S., 103, 278 Rovee, D. T., 110, 134, 280
Raney, G., 168, 233, 256 Rovee-Collier, C., 81, 98, 107, 111, 112,
Raskin, L. A., 71, 279 119, 129, 131, 134, 137, 140, 141, 142,
Rasmussen, T., 35, 38, 40, 276 145, 147, 148, 149, 151, 152, 153, 154,
Ratcliff, R., 20, 164, 190, 200, 213, 272, 155, 156, 157, 159, 160, 163, 164, 166,
278 169, 170, 174, 175, 176, 178, 180, 181,
Ratner, H., 115, 278 182, 184, 185, 186, 197, 198, 202, 203,
Rauch, S. L., 71, 279, 282 218, 219, 220, 228, 229, 230, 234, 235,
Rawlins, J. N. P., 41, 54, 274 236, 238, 239, 241, 242, 244, 245, 253,
Raye, C. L., 224, 226, 269, 276 256, 257, 261, 262, 263, 264, 265, 266,
Rayner, R., 106, 288 267, 270, 272, 273, 274, 276, 280, 281,
Raz, N. , 75, 262 282, 284, 286, 288, 289
Rea, C. P., 159, 279 Rozin, P., 73, 281
Read, S., 30, 260 Rubens, A. B., 178, 283
Reeves, A., 185, 279 Rudy, J. W., 83, 282
Regan, R., 69t, 261 Ruggiero, F. T., 190t, 282
Reinitz, M. T., 138, 164, 279 Russo, R., 17, 78, 282
Reiss, L., 226, 258 Ryan, L., 172, 183, 262, 271
Reminger, S. L., 62, 263 Rybash, J. M., 175, 282
Rempel, N. L., 52, 53f, 290
Rey-Bellet-Muller, M., 72, 253 S
Rheingold, H. L., 110, 279 Sackett, G. P., 91, 92f, 94, 265

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300 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Saint-Cyr, J. A., 56, 282 Sidman, M., 46, 284

Salmon, D. P., 56, 266 Singer, J. M., 173, 174, 263, 284
Sameroff, A. J., 110, 282 Singh, A., 74, 270
Samuelson, R. J., 37, 276 Skinner, B. F., 110, 193, 284
Sananes, C. B., 68, 69t, 126, 258 Slater, P. C., 72, 286
Sands, S. F., 76, 175, 178, 290 Sloman, S. A., 153, 175, 284
Santiago, H. C., 76, 175, 178, 290 Smith, B., 78, 115, 278, 285
Saunders, R. C., 43, 45f, 85, 271 Smith, G. J., 240, 264
Savage, C. R., 59, 282 Smith, M. L., 54, 284
Sax, D. S., 56, 272 Smith, S. M., 183, 285
Schacter, D. L., 1, 2, 3, 7, 8, 9, 10, 11, 12, Snodgrass, J. G., 13, 17, 27, 74, 77, 78,
12t, 13, 14, 16, 18, 22, 23, 24, 26, 28, 285
59, 73, 76, 83, 97, 107, 109, 115, 116, Sokolov, E. N., 98, 285
117, 118, 121, 122, 123, 128, 129, 137, Solomon, P. R., 107, 109, 285
138, 139, 140, 148, 150, 153, 162, 178, Spear, N. E., 68, 130, 131, 149, 183, 202,
179, 180, 183, 190t, 191, 192, 194, 216, 240, 254, 258, 285, 286
196, 201, 202, 213, 215, 221, 225, 233, Spence, M. J., 101, 228, 261
247, 250, 260, 264, 269, 276, 282, 283, Sperling, G., 185, 279
284, 287 Squire, L. R., 1, 8, 9, 12t, 16, 17, 24, 28,
Schechter, A., 185, 281 33f, 34, 35, 41, 42f, 46, 47f, 48, 52, 53f,
Schenk, F., 71, 283 54, 56, 57f, 59, 62, 72, 90, 97, 117,
Schmidt, R. A., 74, 158, 233, 283 118, 122, 123, 128, 150, 151, 168, 176,
Schulenberg, C. J., 69t, 283 190t, 192, 201, 202, 211, 212, 213,
Schwartz, B. L., 12t, 25, 26, 283 216, 225, 231, 232, 246, 247, 250, 253,
Schweitzer, L., 69t, 283 258, 259, 264, 270, 272, 273, 284, 285,
Scott, S. K., 56, 283 286, 290
Scoville, W. B., 3, 29, 30, 35, 40, 73, 260, Srinivas, K., 25, 109, 179, 190, 191, 192,
283 214, 215, 216, 226, 280, 286
Scozzafava, J. A., 69t, 261 Stadler, M. L., 168, 280
Searle, J. R., 21, 284 Stafford, S., 149, 164, 184, 281
Seidenberg, M., 75, 262 Stankiewicz, B. J., 179, 286
Shallice, T., 213, 284 Stark, H. A., 22, 23, 24, 150, 192, 287
Shapiro, M. L., 16, 22, 284 Stehouwer, D. J., 69t, 286
Sheffield, E. G., 129, 131, 133, 149, 152, Steinert, P. A., 69t, 286
210, 234, 253, 284 Stevenson, M. B., 114, 253
Sherry, D. F., 10, 28, 191, 192, 194, 225, Stewart, C. A., 43, 256
284 Stikes, E. S., 69t, 283
Shields, P., 185, 281 Stinson, F. S., 116
Shields, P. J., 184, 186, 238, 244, 245, Stoddard, L. T., 46, 284
284 Strauss, M. S., 197, 202, 276
Shimamura, A. P., 8, 12t, 24, 128, 175, Streete, S., 17, 75, 78, 277
176, 193, 227, 264, 284 Sullivan, M. W., 129, 131, 145, 152, 153,
Shimp, C. P., 2, 284 156, 157, 175, 234, 238, 281, 286
Shore, C. M., 115, 256 Sutherland, R. J., 83, 282
Shyi, G. C.-W., 141, 185, 257, 281 Suzuki, W. A., 52, 53f, 286, 290

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AUTHOR INDEX 301

Swartz, K. B., 91, 94, 265 Van Paesschen, N., 54, 288
Sweeney, B., 156, 176, 182, 265 Van Zandt, B. J. S., 180, 271
Van Zandt, T., 20, 278
T Vargha-Khadem, F., 54, 288
Taylor, A. E., 56, 282 Vasquez, B. J., 69t, 71, 264, 268
Terwilliger, R. F., 22, 286 Vazoiu, F., 74, 267
Teuber, H. L., 3, 29, 30, 127, 273, 286 Vela, E., 183, 285
Tharan, M., 12, 162, 178, 202, 283 Verfaellie, M., 226, 258
Thomas, K. M., 79, 286 Victor, M., 30, 288
Thompson, R. F., 56, 125, 193, 286, 287 Videen, T. O., 59, 286
Thompson, W. C., 69t, 260 Vieira, A., 114, 123, 129, 139, 157, 187,
Thomson, D. M., 183, 286 205, 208, 210, 229, 255
Timmons, C. R., 139, 156, 204, 205, 208, Visser, G. H. A., 66, 261
210, 287 von Hippel, W., 162, 288
Tissot, R., 72, 253 Vriezen, E. R., 138, 288
Tomiyasu, U., 30, 260
Toth, J. P., 17, 19, 78, 268 W
Towle, C., 102, 262 Wallace, J. E., 69t, 71, 258, 288
Tranel, D., 56, 62, 253, 256 Ward, C. H., 172, 256
Treadwell, J., 178, 202, 283 Warrington, E. K., 3, 7, 8, 12t, 33f, 34,
Treisman, A., 12, 134, 137, 138, 139, 56, 109, 128, 190t, 255, 288, 289
149, 151, 155, 179, 217, 220, 233, 274 Watkins, K. E., 54, 288
Tuber, D. S., 109, 256, 287 Watkins, P. C., 172, 288
Tulving, E., 2, 7, 9, 12t, 15, 16, 21, 22, Watson, J. B., 1, 106, 196, 288
23, 24, 25, 73, 97, 125, 127, 129, 131, Watson, J. S., 110, 193, 288
138, 139, 143, 144, 150, 153, 168, 172, Webster, M., 94, 271
175, 179, 180, 183, 190t, 191, 192, Weiner, S., 182, 218, 219, 256
195, 196, 199, 200, 201, 211, 212, 213, Weiskopf, S., 103, 117, 118, 263
215, 221, 224, 225, 233, 239, 247, 260, Weiskrantz, L., 3, 7, 8, 12t, 33f, 34, 56,
266, 276, 283, 284, 286, 287 109, 128, 190t, 191, 192, 288, 289
Turner, M., 102, 277 Weizmann, F., 99, 289
Tynes, D. M., 145, 152, 234, 286 Weldon, M. S., 25, 77, 168, 214, 215,
216, 226, 280
U Werboff, J., 107, 257
Underwood, B., 153, 255, 278 Werker, J., 125, 289
Underwood, B. J., 183, 287 Werner, J. S., 2, 116, 289
Ungerleider, L. G., 58, 59, 88, 178, 254, Wewerka, S. S., 151, 156, 255
276, 288 White, B. C., 142, 258
Uzgiris, I. C., 100, 122, 267, 288 White, N. M., 60, 61, 272, 277
Whitmarsh, G. A., 175, 257
V Wickelgren, W. A., 150, 190t, 289
Vander Linde, E., 145, 156, 157, 159, Wilk, A., 142, 160, 166, 174, 176, 178,
160, 163, 276, 288 241, 242, 253, 265, 273, 289
Van der Linden, M., 14, 79, 273 Willatts, P., 105, 267
Vanderwart, M., 74, 285 Williams, J. M. G., 213, 262

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302 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

Williamson, D. A., 172, 288 Wurtzel, N., 112, 145, 147, 148, 185,
Willingham, D., 26, 276 197, 198, 234, 265
Willingham, D. B., 9, 17, 24, 25, 26, 28, Wyers, E. J., 233, 290
216, 232
Willis, W. D., 67, 289 Y
Winocur, G., 43, 184, 289 Yengo, L. A., 202, 263
Wise, S. P., 56, 57, 289 Yonelinas, A. P., 17, 19, 78, 268
Witherspoon, D., 8, 12t, 25, 125, 128, Young, A. W., 56, 283
268, 290
Wolfe, J., 57, 257 Z
Wondoloski, T. L., 112, 145, 147, 148, Zacks, R. T., 74, 233, 265, 278
185, 197, 198, 234, 265 Zajonc, R. B., 12t, 174, 175, 180, 270
Wood, E. R., 53, 274 Zentall, T. R., 2, 290
Wood, F., 190t, 269 Zola-Morgan, S., 52, 53f, 90, 253
Woodruff-Pak, D. S., 12t, 15, 109, 290 Zola-Morgan, S. M., 16, 17, 24, 41, 42f,
Woodworth, R. S., 150, 290 46, 47f, 48, 52, 53f, 83, 88, 117, 148,
Wright, A. A., 76, 175, 178, 290 192, 253, 259, 275, 277, 286, 290

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Subject Index

Locators annotated with f indicate figures.

Locators annotated with t indicate tables.

A priming in 232-233
absolute information, infant memory and affect, as dissociation variable 172-175,
182 173f
accessibility, of memory age and aging
context impact on 238-239, 245-246 as dissociation variable 144-150,
declarative/procedural 211-213 146f-148f
explicit 10-11, 142-143, 212, 239 in Jacksonian principle 66-68, 71-73
implicit 11, 212, 238 children’s memory and 75-82, 80f-
active memory 81f
mechanisms of 37, 193, 207, 249 multiple memory systems and 73-
priming with 233-234 82, 80f-81f
novel, retention effects of 242-245, memory performance per 17-18, 197,
243f 234-235, 235f
retention effects of 239-241, 240f multiple memory systems and 73-82,
adenosine monophosphate, see cyclic 228
AMP priming latency and 141-143, 142f
adult memory agendas, in MEM memory system 222f,
capacity of 1, 3, 247 223-224
experimental dissociations in 7-8, 127 alcoholic amnesia, see Korsakoff’s
independence in 23-24 syndrome
independent variables in 143-186, Alzheimer’s disease 26, 74
144t amnesia
parallels with amnesics 128 adult memory parallels with 128
parallels with infants 139-141 alcoholic, see Korsakoff’s syndrome
process-dissociation procedure for anterograde 30, 38, 40-41
19-20 conscious awareness with 8, 16, 21
infant memory versus 2-3 drug-induced temporary 14
Jacksonian principle of, multiple infant memory parallels with 115-126,
memory systems and 73-74 120f, 126t, 248
memory dissociations in 186, 188 infantile 73
task comparisons with infants 137- Jacksonian principle and 72-73
141, 138t memory dissociations with 3-4, 7,
tasks for 127-129 128, 193-194

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304 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

brain-damaged versus non-brain- selective 149-150

damaged 3, 8, 10, 16, 128 auditory conditioned emotional re-
independent variables of 143-144, sponse, of nonhumans 68-72, 69t, 70f
144t autobiographical memory, see experi-
parallels with preverbal infants 115- ences
123, 126, 126t automatic memory 9, 232, see also
tasks for 35, 128-129 implicit memory
in memory systems research 3-4, 7, autonoetic consciousness 16
193-194 avoiding reactions, Jacksonian principle
memory tasks for 14-15 and 66-67
explicit versus implicit 35, 128-129
human studies on 29-35, 32f-33f, 56 B
MTL lesions with, memory and 29- Barrier task, with brain damage, spared
35, 32f-33f, 56 memory results of 46, 47f
priming and 232-233 baseline phase, in preverbal infant
retention mechanisms with 139 retention tests 134, see also specific
retrograde 30, 41, 43, 72 study
amygdala baseline ratio, in preverbal infant
lesion studies of 51-52, 53f retention tests 135, see also specific
in humans 29 study
in nonhuman animals 38-46, 45f, Beck Depression Inventory (BDI) 172
47f behavior, per early experiences 1, 115
parallels of 46, 48 bimanual motor tasks, MTL lesions and
memory role of 49-52, 49f, 56, 57f 31, 56
dissociations in 61-63 binocular rivalry, as memory variable
spatial arrangement of 51, 51f 138, 179-180
anger, as memory variable 173 biological process, consciousness as 21-
anoetic consciousness 15 22
anterograde amnesia brain damage, see also specific lesion
in humans 30 classical conditioning and 34, 109
in nonhuman animals 38, 40-41, 42f consciousness with 16, 213
Aplysia, classical conditioning of 107, Jacksonian principle and 65-66
109 memory development studies and,
arbitrary events, in imitation tasks 115 limitations of 125-126
associative memory, infants’ evidence memory dissociations with 3, 8, 10,
for 203-204 16, 128
between independent memories 204- in adults 128-129
211, 206f-209f memory systems and 213
attention reflex reactions and 67, 109, 193
in preverbal infants 98-100, 149, 185, brain metabolism, functional imaging of
238 58-59
mobile studies on 169-171, 170f, brain oxygenation, functional imaging of
220 58-59
transfer-appropriate processing and
218-220

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SUBJECT INDEX 305

C amnesic results of 41, 42f

categorization, with novel priming 244- neural mediation of 53, 62
245 spared memory results of 43
caudate nucleus, memory role of 55-56, eight-pair versus 24-hour 43-44, 46,
55f, 63 48
dissociations in 60-61 nonhuman primates and, memory
causal events, in imitation tasks 115 dissociations with 84f, 85-88
CCP, see conditioned cue preference conditioned cue preference (CCP) 61-62
CD, see concurrent discrimination task conditioned response (CR), in memory
central nervous system (CNS), see tasks 14-15, 193
neuroanatomy, specific component for preverbal infants 106-109, 248
cerebellum, memory role of 56, 57f, 192 conditioned stimulus (CS), in memory
children’s memory tasks 14-15, 193
aging studies on 75-82, 80f-81f for preverbal infants 106-109, 108f,
episodic/semantic studies on 199-200 248
Jacksonian principle of conditioned taste aversion, of nonhuman
multiple memory systems and 75- animals 68-72, 69t, 70f
82 confabulation 224, 226
pathologic 72-73 conscious awareness, see also memory
classical conditioning retrieval
brain damage impact on 34, 109 in amnesics 8, 16
as memory task 14-15 consciousness versus 21-22
for preverbal infants 106-109, 108f as explicit memory component 3-4, 9,
neural mediation of 56, 57f, 62 11, 27
cognitive maps 73 problems with 15-22, 25-27, 249
cognitive processes functional definition of 21-22, 25, 28
amnesia and 35 MEM memory system and 224-225
consciousness and 15-16 memory dissociations and 16-20, 25
general storage of 196, see also in preverbal infants 16, 20-22, 116,
semantic memory system 124-125, 248
Jacksonian dissolution of 72-74 consciousness 21
MEM memory system and 221, 222f, conscious awareness versus 21-22
223-225, 228 memory performance and 17-20
preverbal infants development of 115, memory systems per 15-17, 28
247 contemporaneous-cuing procedure 130,
remembering versus 9-10 250
color recognition context 182
age impact on 81-82 as dissociation variable 183-186
study diversity and 165-167, 165f- cues and 184-186, 248
167f interpolated 153-155, 154f
conceptually-driven processing, in new exposures 164-167, 165f-166f
memory dissociation 214-215 fading of, memory impact of 239
concurrent discrimination task (CD) hippocampal processing of 54
for brain-damaged nonhuman animals contralateral reflexes 66-67
36f, 37

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306 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

cortex independent variables of 144-145,

entorhinal 51-52, 51f, 53f 147, 151, 156, 162, 187
frontal temporal 94, 122, 192, 226 for preverbal infants 113-115, 114f
inferior temporal, see inferior parallels with amnesics 118-122,
temporal cortex 120f, 126t
left prefrontal 226 reactivation procedure with 208-
medial temporal, see medial temporal 210, 209f
lobe delayed-matching-to-sample task
neocortex 56, 57f, 192 (DMS), as memory task 2, 17, 96
perirhinal 44, 49f, 51-52, 51f, 53f delayed-nonmatching-to-sample task
primary visual 49-52, 49f, 51f, 59 (DNMS)
rhinal 44, 49f, 51-52, 51f, 53f for brain-damaged nonhuman animals
cortico-limbic-diencephalic-cortico 36-37, 36f
circuit 49, 49f amnesic results of 40-41, 42f
cortico-striatal-cortico circuit 55, 55f neural mediation of 51-52
CR, see conditioned response nonhuman primates and
crying, as dissociation variable 172-174, developmental memory dissocia-
173f tions in 85-88, 85f-87f
CS, see conditioned stimulus as explicit memory measure 91-95,
cued recall, free recall versus 8-9, 34, 92f-93f
74, 150 hippocampal maturation and 88-91,
cues, in memory tasks 14, 18-19, 27 89f
age and 73-74, 77 inhibition and 96
amnesics and 34-35 for preverbal infants 101-102, 117
context and 184-186, 202 parallels with amnesics 117, 122,
dissociations and 61-62 126t
independence of 22-23 delayed recognition tasks
internally-generated 229-230 independent variables for 143-186,
for preverbal infants 121-122, 129, 144t
202, 204-205 results of 146f-147f, 152f, 154f,
priming variables for 139-141 161f, 163f, 165f, 177f, 181f
spreading-activation model of 209- for preverbal infants 129-130, 130f
210 for adults versus 137-141, 138t
cyclic AMP, in classical conditioning reactivation task versus 137
107 transfer-appropriate processing and
217-220, 219f-220f
D delayed response task, for preverbal
data-driven processing, in memory infants 104-106, 105f
dissociation 214-215 dentate gyrus 88
declarative memory, see also explicit dependence, in experimental dissocia-
memory tions 8-9, 127-128
characteristics of 212-213 depression, as memory variable 172
development of 9, 24, 28, 213 developmental hypothesis, of memory
as system 211-212 systems 3-4
deferred imitation task in nonhuman primates 85-88, 85f-87f

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SUBJECT INDEX 307

specific versus general 196-198, 199f episodic memory system, see also
diencephalon, memory role of 25, 34, explicit memory
49-50, 57f context variable of 183
direct memory tasks 11-12 definition of 3, 9
discovering, in MEM memory system development of 196-200, 199f
222f, 223 infant modifications of
discrete-trials procedure, in operant between associations 204-211,
conditioning 110 206f-209f
discrimination tasks, see concurrent for associations 203-204
discrimination task, somesthetic for object functions 202-203
discrimination task, visual discrimina- structural descriptions system in
tion tasks 201-202
dissociation, see memory dissociations memory subsystems of 201-211
distractors, in transfer-appropriate semantic memory distinction from
processing 218-220, 219f 196-200, 225
DMS, see delayed-matching-to-sample test model for 24, 27
task evolution theory, of multiple memory
DNMS, see delayed-nonmatching-to- systems 194-195, 213
sample task examining, in MEM memory system
dualism 20-21 222f, 223
executive, in MEM memory system 222f
E experiences, previous
elaborative encoding 76, 169 age-related differences in 75, 118
emotional memory 56, 57f, 197 in explicit memory, see conscious
emotional response, auditory condi- awareness
tioned, of nonhumans 68-72, 69t, 70f in implicit memory 9, 232
enabling events, in imitation tasks 115 infants’ ability to recall 118-125, 120f
encoding, initial MEM memory system and 229
amnesics’ capability for 8, 128 response latency and 142-143, 143f
elaborative 76, 169 storage of, see episodic memory
memory development and system
context and 183 transfer-appropriate processing and
implicit component 24-25 215
in infants 76, 129, 148 experimental memory dissociations
level of processing in 168-171, 170f in adults versus infants 127-129, see
orthographic 76, 168-169 also adult memory, infant memory
phonemic 168 processing accounts for 213-214, 214t
transfer-appropriate processing and multiple-entry modular memory
215-217, 226 system 221-230, 222f
engram 98 transfer-appropriate 214-221, 219f-
entorhinal cortex 220f
damage to, memory impact of 52, 53f rule of 7-8, 127-128
spatial arrangement of 51, 51f variables in, see variables
environment, as memory variable 182- explicit memory
184 access to 10-11, 142-143, 212, 239
characteristics of 2-3, 8-11, 54

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308 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

in children, aging impact on 75-82, F

80f-81f feature recognition, age impact on 80-
conscious awareness as component of 81, 81f
3-4, 9, 11, 27 fetal studies, of reflexes 66-67
problems with 15-22, 25-27, 249 first-in, last-out sequence, see Jackso-
dissociation tasks for, in adults versus nian principle
infants 137-141, 138t fMRI, see functional magnetic resonance
as form versus system 9, 11, 54 imaging
hippocampus role in 49-54, 49f, 53f forgetting, see also retention
implicit memory versus 9-11, 10t in adults 235
problems with 15-25, 27 functional independence and 24, 41,
independent variables of 143-186, 42f
144t in preverbal infants 98-99, 116, 174
infants’ capacity for 1, 3, 193 memory dissociations and 130-133,
developmental dissociation of 97- 133f, 136-137
115 rate of 235-238, 236f-237f
experimental tasks for 129-186, fornix, damage to, memory impact of
138t 60-62
implicit memory interactions and free-operant procedure, in operant
231-246 conditioning 110
parallels with adults 139-141 free recall, cued recall versus 8-9, 34,
parallels with amnesics 115-123 74, 150
retention similarities with 234-235, frontal temporal lobe
235f lesions of, memory impact of 94, 122,
transfer-appropriate processing 216- 226
221 memory role of 192
medial temporal lobe role in 25, 35, fruit fly, classical conditioning of 107
48-54 functional imaging studies, of memory
lesions effect on 30-35, 32f-33f 57-59, 226
MEM memory system and 227 functional independence 22, 24
neural substrates of 48-57 memory performance per 22, 24-26,
in nonhuman primates 192
development of 87, 95-96 functional magnetic resonance imaging
DNMS as measure of 91-95, 92f- (fMRI) 58-59
93f
research strategies for 3-4, 249-251 G
tasks for 8, 11-12 generalization, in infant memory 196-
transfer-appropriate processing and 198, 199f
215-216 genetics
in infant memory 216-221 in classical conditioning 107, 149
explicit memory tests 128, 189 in memory pathology 56-57
exposure, see study exposure global amnesia, see amnesia
extracting, in MEM memory system globus pallidus, memory role of 55, 55f
221, 222f Gollin incomplete-pictures task, MTL
eyeblink response, in preverbal infants lesions and 31, 33f, 56
106-107, 108f guessing 19

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SUBJECT INDEX 309

H in adults versus preverbal infants

habit memory, see also implicit memory 137-141, 138t
neural mediation of 55-57, 55t explicit memory versus 9-11, 10t
habit system, in nonhuman primates 87, problems with 15-27
213 as form versus system 9, 11
habituation task, for preverbal infants independent variables of 143-186,
98-100, 116 144t
heart rate response, classical condition- infants’ capacity for 1, 3, 124-125
ing of, in brain-damaged infants 109 developmental dissociation of 97-
hierarchical development hypothesis 2, 115
5, 65, 75, 194, 247 experimental tasks for 129-186,
hierarchical memory dissolution 65, 75 138t
hippocampus explicit memory interactions and
cognition role of 73 231-246
functional imaging of 59 parallels with amnesics 115-123
lesion studies of 16-17, 51-52, 52f retention similarities with 234-235,
in humans 29-35 235f
in nonhuman animals 35, 38-46, transfer-appropriate processing 216-
42f, 45f, 47f, 60-62 221
parallels in 46, 48 medial temporal lobe role in 35, 54-57
memory role of 49-54, 49f, 53f MEM memory system and 227
dissociations in 61-63, 226 neural substrates of 54-57
of nonhuman animals in nonhuman primates, development
lesions, memory impact of 35, 38- of 87, 95-96
46, 42f, 45f, 47f, 60-62 research strategies for 3-4, 249-251
visual recognition memory and 88- tasks for 8, 11-15, 12t
91, 89f transfer-appropriate processing and
spatial arrangement of 51, 51f 215-216
homophones 172 in infant memory 216-221
Huntington’s disease, implicit memory implicit memory tests 128, 189
and 56-57 impossible objects, in memory tasks 13-
14
I in utero stimuli, memory development
identifying, in MEM memory system with 101, 228
221, 222f, 223 independence
imagery system, for research 191-192 in experimental dissociations 7-9, 22,
imaging studies, of brain 57-59, 226 144t
imitation tasks, see deferred imitation study variables of 144t, 150-171,
task 175-186
implicit memory subject variables of 144-150, 144t,
access to 11, 212, 238 172-175
characteristics of 2, 8-11 forms of, memory performance per
in children, aging impact on 75-82, 22-24, 192
80f-81f indirect memory tasks 11-15, 12t
dissociation tasks for 25-26 infant memory

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310 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

adult memory versus 2-3 inferior temporal cortex (TE)

associative 203-211, 206f-209f damage to
capacity of 2, 103-104, 112, 137 in infants versus adults 90
amnesics’ capacity versus 122-123 memory impact of 43-44, 45f
explicit, see explicit memory memory role of 49f, 50, 51f
implicit, see implicit memory in nonhuman primates 90
independent variables of 143-186, visual recognition per maturation of
144t 90
renewed 142-143, 143f, 157, 218- inhibition, visual recognition and 96
219, 219f initiating, in MEM memory system 222f,
similarities in 234-235, 235f 223
developmental types of, see explicit instincts, in memory tasks 15
memory, implicit memory instructions, as memory task variable
experimental dissociation of 18-20, 34, 175, 250
parallels with adults 139-141 for adults versus infants 127, 129, 139
parallels with amnesics 115-126, 120f, for experimental dissociations 127-
126t, 248 129
task interpretations 97-115 interference
forgetting in 98-99, 116, 174 as dissociation variable 153-155, 154f
memory dissociations and 130-133, transfer-appropriate processing and
133f, 136-137 217
rate of 235-238, 236f-237f internally-generated cues, in MEM
implicit/explicit interactions in memory system 229-230
literature review of 231-233 interstimulus interval (ISI), in preverbal
with priming and active memory infant tasks 107, 108f
239-245, 240f, 243f ipsilateral reflex 66
research strategies for 233-234
similarities between 234-239, 235f J
Jacksonian principle of 66-68 Jacksonian principle
in humans 72-73, 75-82 description of 65-66
in nonhuman animals 68-72, 69t, in human memory pathology 72-73
70f multiple memory systems and
MEM memory system and 228-230 in adults 73-74
preverbal, see preverbal infants in children 75-82
primacy effect on 176-178, 177f, 182 in preverbal infants 125-126
reflexive studies on 106-109, 108f in nonhuman animal memory 68-72,
research strategies for 3-4 69t, 70f
transfer-appropriate processing and supportive examples of 66-68
216-221, 219f-220f judging, in MEM memory system 225
younger versus older 2
infants K
encoding capabilities of 76, 129, 148 knowing, remembering versus 9-10
physical and behavioral differences of knowing consciousness 15-16
148, 148f access to 211-213
reflex behaviors of 67, 106-109, 108f knowing how 35, 211

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SUBJECT INDEX 311

knowing that 35, 211 campal damaging 52

knowledge manipulations, experimental, see
MEM memory system processing of variables
221, 222f, 223-225 maturation-based factors
organized storage of 196, see also of neuroanatomy 88-91, 89f, 192
semantic memory system of priming latency 141-143, 142f
Korsakoff’s syndrome maturation rate, of memory systems 3-4,
memory research and 3-4 10
motor skill performance and 31, 32f- medial temporal lobe (MTL)
35f, 34 human lesions of
serial reaction times with 26 memories spared with 30-35, 32f-
33f, 55-56
L memory impairments with 29-30
language development lesion studies of
memory development and 1, 101, 228, human 29-35
251 memory tasks for 30-38, 46, 48
memory dissociation and 188 nonhuman animal 35-48
memory performance and 75-76, 126, parallel findings of 46-48
131 memory role of 57f, 192
latency response, of preverbal infants, in explicit 25, 35, 48-54
reactivation 141-143, 142f-143f implicit 35, 54-57
learning process, memory versus 193, nonhuman animal lesions of
249, 251 memories spared with 43-46, 45f,
level of processing (LOP), as dissocia- 47f
tion variable 168-171, 170f-171f memory dissociation studies with
lexical decision task, as memory task 13- 84-95
14 memory impairments with 35-43,
Lifesaver task, for brain-damaged 36f, 39f, 42f
nonhuman animals 46, 47f MEM memory system, see multiple-
limbic system entry modular memory system
memory role of 49-52, 49f memory, see also specific type
dissociations in 61-63 age of, response latency per 142-143,
spatial arrangement of 51-52, 51f 143f
local context 183 consciousness as construct of 16-17,
locating, in MEM memory system 221, 21-22
222f forms versus systems of 3, 9, 11, 21,
long-term familiarization task, for 189-191
preverbal infants 100-101 as linked network 209-210
long-term memory, infants’ capacity for long-term 193
1 phylogeny of 10, 10t
as process 193, 249, 251
M short-term, see active memory
magnetic resonance imaging (MRI) memory capacity
functional 58-59 of adults 1, 3, 247
with stereotaxic surgery, for hippo- of infants versus 1-2

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312 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

of infants, see infant memory, serial position as 175-178, 177f

preverbal infants spacing effects as 158-161, 160f-
memory development 161f
debate about 1-2 studied size as 178-180
as hierarchical 2, 5, 65, 75, 194, 247 study item quantity as 164-167,
Jacksonian principle of 65-68 165f-167f, 180-181
in humans 72-73 study trial quantity as 155-157, 158f
in nonhuman animals 68-72, 69t, vulnerability as 153-155, 154f
70f in infants
language development and 1, 101, experimental 97-126, 139-141
228, 251 preverbal 129-186
overview of 3-5 interactions between
research on, see also memory research literature review of 231-234
strategies for 3-4, 250-251 with novel priming of active
as sequential 3, 14 memory 242-245, 243f
memory dissociations with priming of active memory 239-
accessibility factors of 10-11, 142- 241, 240f
143, 211-213, 239 similarities between 234-239, 235f-
context impact on 238-239, 245- 237f
246 memory subsystems for 26-27
in adults 127-129 in nonhuman animals 60-62, 83-95,
experimental 7-8, 19-24, 127-128, 85f-87f, 89f
139-141 processing accounts for 213-214, 214t
in amnesic patients 3-4, 7, 128, 193- research shortcomings of 2-3, 16-17,
194 125-126, 249
conscious awareness and 16-20, 25 memory dissolution
definition of 7-8 age impact on 66-68, 71-73
double multiple memory systems and 73-
in humans 62-63, 127-128 82, 80f-81f
in nonhuman animals 60-62, 83 as hierarchical 65, 75
experimental, see experimental Jacksonian principle of 65-68
memory dissociations in humans 72-73
in explicit memory tasks 128 in nonhuman animals 68-72, 69t,
in implicit memory tasks 25-28, 128 70f
independent variables of 143-144, memory facilitation, with novel priming
144t 244-245
affect as 172-175, 173f memory impairment
age as 144-150, 146f-148f with age, see memory dissolution
context as 183-186 with MTL lesions 30, 41, 51-52
exposure time as 162-164, 163f with novel priming 244-245
level of processing as 168-171, memory in learning 193
170f-171f memory load, as dissociation variable
memory load as 180-182, 181f 180-182, 181f
retention interval as 150-153, 152f, memory modules, see memory sub-
180-182 systems

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SUBJECT INDEX 313

memory of learning 193 monohierarchical 201

memory performance memory systems
age impact on 17-18, 141-143, 142f consciousness per 15-17, 28
conscious and unconscious contribu- declarative/procedural 9, 24, 28, 57f,
tions to 17-20, 25 211-213
conscious awareness dissociation and definitional confusion over 3, 9, 11,
16-20, 25 21, 189-191
independence of variables and 22-24 developmental hypothesis of 3-4
language development and 75-76, nonhuman primate studies on 85-
126, 131 88, 85f-87f
with MTL lesions dissociation of, see memory dissocia-
in humans 29-35, 32f-33f tions
in nonhuman animals 35-48, 36f, early, see implicit memory, semantic
39f, 42f, 45f, 47f memory system
memory primes, see priming tasks episodic/semantic
memory process, learning versus 193, development of 3, 9, 183, 196-200
249, 251 distinctions between 24, 27, 168-
memory research 69, 196-201, 225
current issues in 57-59 modifications of 201-211, 206f-
limitations of 2-3, 16-17, 125-126, 207f
248-249 independence in 22-24
representation systems for 191-192, late, see episodic memory system,
213 explicit memory
strategies for 2-4, 7, 17, 233-234, 250- maturation rate of 3-4, 10
251 in nonhuman primates 87, 213
memory retrieval proposed theories of 190-191, 190t
in amnesics 8 single versus multiple 9, 16, 24, 190-
automatized 9, 232-233 191, 231, see also multiple memory
intentional systems
in explicit memory 3-4, 9-11, 18, 27 Jacksonian principle and 73-82,
in preverbal infants 116, 124-125, 80f-81f
140-143 neuroanatomical basis for 59-64,
task criterion for 18-20, 76, 129, 192-194
140 size-sensitive versus size-invariant
tests of, see memory tasks 179-180
transfer-appropriate processing and memory tasks, see also specific task
215-217 direct versus indirect 11-12
memory subsystems implicit versus explicit 128, 189
of episodic/semantic memory 201-211 for implicit versus explicit measure-
of MEM memory system ments, see also memory dissocia-
developmental sequence of 227-229 tions
perceptual 221, 222f, 223-224 in humans 7-9, 11-15, 18
reflective 221, 222f, 223-224 in nonhuman animals 46, 48, 84-95
in memory dissociations 26-27, 189- in preverbal infants 97-115
190 independence in 7-9, 22-27

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314 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

memory systems versus 189-191 Morris water maze, for nonhuman

for MTL lesions animals 41, 71
in animals 35-38, 36f, 46, 48 motor skill tasks
in humans 30-35, 32f-33f basal ganglia mediation of 192
for nonhuman primates 35-38, 46, 48, MTL lesions and
84-95 in humans 30-35, 32f-33f, 43, 55
for preverbal infants in nonhuman animals 46, 47f
for capacity testing 97-115, 99f, preverbal infants development of 115
105f, 108f, 111f-114f MRI, see magnetic resonance imaging
for experimental dissociations 129- MTL, see medial temporal lobe
186 multiple-entry modular memory system
research implications of 3-4, 17 (MEM memory system)
size-dependent 179-180 adult memory and 247-248
mirror-drawing task, MTL lesions and conscious awareness and 224-225
30-31, 32f, 56 description of 221
mirror reading task, MTL lesions and implicit/explicit memory and 227
33f, 34, 56 infant memory and 228-230
Mishkin’s neural model multiple memory systems and 224-
of explicit memory 48-49, 49f 225
modification of 49f, 50-52 processing functions of 221, 222f,
of implicit memory 55-57, 55f 223-224
mobile conjugate reinforcement subprocessing dissociations for 225
procedure 110, 119, 121, 248 subsystems of
mobile tasks, for preverbal infants developmental sequence of 227-229
in active memory priming 241-245, perceptual 221, 222f, 223-224
243f reflective 221, 222f, 223-224
deferred imitation 119-121, 120f transfer-appropriate processing and
for experimental dissociations 226
developmental interpretations of multiple memory systems
197-198 age factor of 73-82, 80f-81f, 228
independent variables of 144-186, dissociation of, see memory dissocia-
147f, 170f-171f, 177f tions
results and discussion of 134-137, Jacksonian principle and
136f, 142f, 143 in adults 73-74
in forgetting studies 235-238, 236f- in children 75-82, 80f-81f
237f MEM memory system and 224-225
limitations of 249 neuroanatomical basis for 59-64
long-term familiarization 100-101 proposed theories of 190-191, 190t
memory systems and 197-198, 202- criteria for 191-196
205, 206f single system versus 9, 16, 24, 231,
operant conditioning 110-112, 111f, 290-191
113f muscarinic receptor-binding sites 88
pop-out 169-171, 170f, 218-219, 219f music boxes, in infant research 139, 205,
mood, see affect 206f, 210
Morris arm maze, for nonhuman animals
38, 39f

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SUBJECT INDEX 315

N anterograde 38, 40-41, 42f

neocortex, memory role of 56, 57f, 192 retrograde 41, 42f, 43
neural substrates conscious awareness in 16, 20-22
of memory explicit memory in, DNMS as
aging impact on 75-82 measure of 91-95, 92f-93f
explicit 48-57 hippocampal maturation in, DNMS
implicit 54-57 performance and 88-90, 89f
of memory systems 59-64, 192-194 implicit memory in, development of
neuroanatomy, of memory 57f 87, 95-96
explicit memory development studies on
human studies on 29-35 Jacksonian principle in 68-72, 69t,
neural substrates in 48-57 70f
nonhuman animal studies on 35-48 limitations of 2, 16-17
functional imaging studies of 57-59, memory dissociations in
226 double 60-62, 83
human studies on 29-35 evidence for 83-84, 88
implicit hippocampal maturation and 88-91,
human studies on 29-35 89f
neural substrates in 48-57 historical background of 84-88, 85f-
nonhuman animal studies on 35-48 87f
maturation factor of 88-91, 89f, 141- measures of 91-96, 92f-93f
143, 142f, 192 MTL lesions of
neural substrates in 48-57, 192 memories spared with 43-46, 45f,
nonhuman animal studies on 35-48 47f
as single versus multiple system 59- memory impairments with 38-43,
64, 192-194 42f
neuroimaging studies, of memory 57-59, memory tasks for 35-38, 36f, 39f
226 parallels to humans 46, 48
neurons 88, 107 nonknowing consciousness 15
neurophysiological process, conscious- nonverbal materials, see also pictorial
ness as 21-22, 25 materials
neuropsychological basis, of explicit in memory tasks 14-15
memory 25 noting, in MEM memory system 222f,
new study items, see novel-context 223
exposure, novel object exposure, novel-context exposure
novel stimulus as dissociation variable 153-155,
noetic consciousness 15-16 154f, 164-165, 165f-166f
nonautomatic memory 9 object function memories and 202-
nondeclarative memory, see also 203
implicit memory novel object exposure
characteristics of 212-213 functional memories of 202-203
development of 24, 28, 57f, 213 memory generalization and 198, 199f
as memory system 211-212 in transfer-appropriate processing
nonhuman animals 218-219, 219f
amnesia in novel priming, active memory retention

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316 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

and 242-245, 243f passive-exposure procedure 203

novel stimulus, priming with 233-234 perceiving, encoding as 217
active memory retention and 242-245, perception subsystem, of MEM memory
243f system 221, 222f, 223-224
novelty preference, in preverbal infants developmental sequence of 227-229
98-101, 99f perceptual closure hypothesis 27
perceptual-identification process,
O automatic 217
object decision task perceptual memory
independent variables of 162, 178-179 basal ganglia mediation of 192
as memory task 13-14, 202 children’s studies on 77
object function, infants’ memories of independent variables of 151, 162,
202-203 168-169, 183-185
object identification, in MEM memory memory dissociation and 62-63
system 221, 222f, 223 MTL lesions and 30-31, 32f-34f, 34,
object search tasks, for preverbal infants 43, 56
2, 103, 117-118 in preverbal infants 120f, 121-122,
OC, see visual cortex 134
odor recognition task 174 in adults versus 138-139
ontogeny, memory development and 10, structural descriptions system for 201-
75, 83 202
hippocampal maturation and 88-89 perceptual representation system (PRS)
systems theory of 194-196, 202 26-27, 201-202
operant conditioning, of preverbal perirhinal cortex
infants 101, 109-113, 111f-113f damage to, memory impact of 52, 53f
research limitations of 248-249 spatial arrangement of 51, 51f
opiate receptor-binding sites 88 visual memory tasks and 44, 49f
orthographic encoding 76, 168-169 personality, per infancy experiences 1
oxygenation Petri’s neural model
of brain, function imaging of 58-59 of explicit memory 49f, 50-52
reflex arc requirements for 66-67 of implicit memory 55-57, 55f
phonemic encoding 168
P phylogeny, of memory 10, 10t, 75, 194-
paired-comparison task, see visual 195
paired-comparison task pictorial materials, in memory tasks 12-
parahippocampal gyrus 13, 191-192
damage to, memory impact of 52, 53f children’s studies on 76-79
functional imaging of 59 independent variables of 151, 169,
spatial arrangement of 51, 51f 179
parallel visual processing, in infant picture-fragment completion, as memory
memory 217-221 task 13, 17, 27
Parkinson’s disease, memory dissocia- children’s studies on 77-79
tion and 62-63 placing, in MEM memory system 221,
passive-avoidance task, for nonhuman 222f
animals 68-72, 69t, 70f pop-out mobile tasks 169-171, 170f,

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SUBJECT INDEX 317

218-219, 219f previous experiences, see experiences

positron emission tomography (PET) 58 primacy effect, in infant memory
possible objects, in memory tasks 13-14 performance 176-178, 177f, 182
prefrontal cortex, left, retrieval role of priming tasks, see also reactivation tasks
226 with active memories 233-234
preverbal infants associative, infants’ memories of 203-
attention in 98-100, 149, 169-171, 211, 206f-209f
170f, 185 in forgetting studies 235-238, 236f-
conscious awareness in 16, 20-22, 237f
116, 124-125, 248 as implicit memory measure 8-9, 26-
episodic/semantic memory system in 27
associations between memories neural mediation of 56, 57f, 59
204-211, 206f-209f in memory dissociation 8, 19
associations memories 203-204 for adults versus preverbal infants
object function memories 202-203 137-141, 138t
structural descriptions system with age and 73-75, 77-78
201-202 independence of 23-24
forgetting in 98-99, 116 independent variables for 143-186,
memory capacity of 1, 4 144t
parallels with amnesics 115-123, infants’ response latency to 141-
120f, 126, 126t 143, 142f-143f
research tasks for 97-115 for preverbal infants, see reactiva-
per retention interval 104-106, 105f, tion tasks
116-117 in normal adults versus amnesics 232-
memory dissociations in 129, 186- 233
188, 248 with novel stimulus 233-234
independent variables that produce prior-cuing procedure 131, 141, 249
143-186, 144t problem-solving skills 4, 43, 187, 249-
parallels with adults 137-141, 138t 250
response latency to memory prime procedural memory
with 141-143, 142f-143f characteristics of 212-213
tasks that produce 129-138, 130f, development of 9, 15-16, 28, 213
132f-133f, 136f as system 211-212
memory tasks for 97-98 process-dissociation procedure, for adult
classical conditioning 106-109, memory 19-20
108f processing accounts
deferred imitation 113-115, 114f, for memory dissociations 213-214,
118-122 214t
delayed response 104-106, 105f multiple-entry modular memory
DNMS 101-102, 117 system 221-230, 222f
object search 103, 117-118 transfer-appropriate 214-221, 219f-
operant conditioning 101, 109-113, 220f
111f-113f processing functions
response-to-novelty 98-101, 99f, automatic 9, 232-233
123, 150, 249 of MEM memory system 221, 222f,
223-224

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318 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

PRS, see perceptual representation amnesics’ performance on 34-35

system as explicit memory measure 8-9, 11-
puppets, in memory systems research 12, 27
203-210, 207f-209f free versus cued 8-9, 34, 74, 150
putamen, memory role of 55, 55f, 63 independence in 22-23
independent variables of 143-186,
R 144t
radial arm maze in memory dissociation 8, 17-19
for brain-damaged nonhuman animals for preverbal infants 111-112, 118-
principles of 37-38, 39f 119, 137
results of 41, 60-62 for adults versus 137-141, 138t
in Jacksonian principle study 71 recognition memory, see visual recogni-
radiofrequency lesions, of limbic system tion memory
52 recognition tests, see recall and recogni-
reaction time (RT), see serial reaction tion tasks
time recollection, see conscious awareness,
reactivating, in MEM memory system memory retrieval
222f, 223, 226, 229-230 recycling, in priming 237
reactivation tasks, see also priming tasks reenactment procedure
independent variables for 143-186, in memory dissociations 149-150
144t in memory systems 210
study results of 160f-161f reflection subsystem, of MEM memory
for preverbal infants system 221, 222f, 223-224
for adults versus 137-141, 138t developmental sequence of 227-229
with deferred imitation task 208- reflex arcs, oxygen requirements of 66-
210, 209f 67
delayed recognition task versus 137 reflexes
examples of 134-137, 136f brain damage impact on 67, 109, 193
principles of 129, 130f, 131-134, in classical conditioning 14-15, 193
132f-133f of preverbal infants 106-109, 108f
response latency to 141-143, 142f- contralateral 66-67
143f fetal studies of, anoxia impact on 66-
transfer-appropriate processing and 67
216-219, 219f-220f ipsilateral 66
retention and Jacksonian principle and 66-67
with active memory 239-245, 240f, memory role of 57f, 197, 248
243f preverbal infant studies of 98-101, 99f
dissociation similarities with 234- refreshing, in MEM memory system
235, 235f 222f, 223
as renewed, in infants 142-143, rehearsing, in MEM memory system
143f, 157, 218-219, 219f 222f, 223
reality-monitoring process 224-225 reinforcement, in memory tasks 146-147
recall 11, see also memory retrieval for preverbal infants 121-122, 134
recall and recognition tasks relational information, infant memory
age impact on 73-74, 78-79 and 182

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SUBJECT INDEX 319

reliance, in MEM memory system 227 term, for preverbal infants 134-135
remembering, knowing versus 9-10 retrieval intentionality criterion 18-19
reperceiving, retrieval as 217 in children’s memory studies 76
repetition priming tasks, see priming in infants’ memory studies 129, 140
tasks retrieving, in MEM memory system
representation, capacity for 1, 213 222f, 223
representation systems retroactive interference 153-154, 154f
for memory research 191-192, 213 retrograde amnesia 41
perceptual 26-27, 201-202 in humans 30, 72
research, see memory research in nonhuman animals 41, 42f, 43
resolving, in MEM memory system 221, rhinal cortex
222f damage to, memory impact of 52, 53f
response-to-novelty task, for preverbal spatial arrangement of 51, 51f
infants 98-101, 99f, 123, 249 visual memory tasks and 44, 49f
independent variables of 150, 161, rotary pursuit task, MTL lesions and 31,
178 32f, 56
parallels with amnesics 123, 126t rule of experimental memory dissocia-
retention, see also forgetting, memory tions 7-8, 127-128
active memory and
novel priming impact on 242-245, S
243f sadness, as memory variable 172-174,
priming effects of 239-241, 240f 173f
in classical conditioning 15 scopolamine, for amnesia 14
infants’ capacity for 2, 103-104, 112, selective attention, age impact on 149-
137 150
amnesics’ capacity versus 122-123 self-knowing consciousness 16
duration of 234-235, 235f, 239-240 semantic memory, memory subsystems
independent variables of 143-186, of 201-211
144t semantic memory system, see also
magnitude of 234 implicit memory
renewed 142-143, 143f, 157, 218- context variable of 183
219, 219f definition of 3, 9
MTL lesions and 31-35, 32f-33f development of 196-200, 199f
postoperative 38, 41, 42f, 43 episodic memory distinction from
retention interval 196-200, 225
as dissociation variable 150-153, 152f, infant modifications of 201
180-182 between associations 204-211,
memory performance per 24, 40, 234 206f-209f
infants’ generalization and 198, for associations 203-204
199f for object functions 202-203
in preverbal infants 104-106, 105f, structural descriptions system in
116-117, 133, 133f 201-202
retention ratio, in preverbal infant tests level of processing and 168-169
135 subsystem of 27
retention tests, immediate versus long- test model for 24, 143

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320 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

senility stereotaxic surgery, for hippocampal

memory dissolution with 72 damaging 52
reflex behaviors with 66-67 stimuli
sensory functions, Jacksonian principle conditional versus unconditional 14-
and 67-68 15, 108f, 109-109, 193, 248
sensory preconditioning 203 in memory tasks
sequence learning, measures of 14 for humans 14-15, 27, 62, 183
sequential memory development 3 for nonhuman animals 35-38, 36f,
serial position, as dissociation variable 93, 95
167, 167f, 175-178, 177f for preverbal infants 98-99, 101-
serial reaction time task (SRT) 102
implicit memory and 25-26 priming variables for 138-141
as memory task 14, 79 in utero 101, 228
serial visual processing, in infant onto-genetic differences in 107, 149
memory 217-221 stochastic independence
shifting, in MEM memory system 222f, definition of 22-23
223 memory performance per 22-25, 192
single memory system, multiple systems striatal system, memory role of 55-57,
versus 9, 16, 24, 190-191, 231 55f, 57f
size-dependent memory tasks 179-180 dissociations in 60-62
size-invariant memory system 179-180 structural descriptions system, implicit
size-sensitive memory system 179-180 memory and 26-27
skill learning 15, 26, 57f, see also structuring, in MEM memory system
specific skill 221, 222f
socialization, memory performance and studied size, as dissociation variable
115, 126 178-180
somesthetic discrimination task, for study, in memory dissociation 144t, 150-
brain-damaged nonhumans 38, 40 171, 175-186
spacing effects, as dissociation variable study exposure, as dissociation variable
158-161, 160f-161f 162-164, 163f
spatial learning interpolated 153-155, 154f
hippocampus role in 49-54, 49f, 51f study item quantity, as dissociation
MEM memory system for 221, 222f, variable 164-167, 165f-167f, 180-181
224-225 study time, as dissociation variable 162-
as memory variable 181-183 164, 163f
of nonhuman animals 68, 71 study trial quantity, as dissociation
speaking, see language development variable 155-157, 158f
specificity study variables, in memory dissociation
in infant memory 118-122, 138, 197 144t, 150-171, 175-186
in priming 233 subject, in memory dissociation 144-
spreading-activation model, of memory 150, 144t, 172-175
209-210 subject variables, in memory dissocia-
SRT, see serial reaction time task tion 144-150, 144t, 172-175
stem-completion tests, see word- substantia nigra, memory role of 62-63
fragment completion supervisor, in MEM memory system
222f

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SUBJECT INDEX 321

T memory tasks 14-15, 193

talking, see language development for preverbal infants 106-109, 108f
tapping tasks, bimanual, MTL lesions unconscious contributions, to memory
and 31 performance 17-20
task training delays, see retention
interval V
tasks, see memory tasks variables, in experimental dissociations
taste aversion, conditioned, of nonhu- 7-9, 17-18, 144t
man animals 68-72, 69t, 70f in adult tasks 127-129, 137-139, 195
TE, see inferior temporal cortex dependence of 127-128
temporal lobe, see frontal temporal lobe, independent 22-24, 143-186, 144t,
inferior temporal cortex, medial 195
temporal lobe in preverbal infants 138-141, 195
textons 134, 181 study-based 144t, 150-171, 175-186
time window construct 159-160, 160f subject-based 144-150, 144t, 172-175
tip-of-the-tongue phenomenon 10 ventral visual stream 50
total time law 162 verbal materials, in memory tasks 8, 12-
Tower of Hanoi task, MTL lesions and 15, 19, 199
33f, 34, 56 representational system for 191-192
tracking, in MEM memory system 221, verbal system, for research 191-192
222f, 228 verbally competent humans, conscious
tracking tasks, bimanual, MTL lesions awareness in 1, 4, 20, 22
and 31, 56 visual association area, see inferior
train tasks, for preverbal infants temporal cortex
in forgetting studies 235-238, 236f- visual attention, see attention
237f visual cortex (OC), primary
independent variables of 147f functional imaging of 59
memory dissociations and 110-112, memory role of 49-52, 49f, 51f
112f-113f, 142f visual discrimination tasks, see also
memory systems and 205-210 specific task
training-test delay, see retention interval for brain-damaged nonhuman animals
transfer-appropriate processing 35-36, 36f
conscious awareness and 215 amnesic results of 38, 40-41, 42f
encoding and 215-217, 226 independent variables of 151
implicit/explicit memory and 215-216 visual paired-comparison task (VPV)
infant memory and 216-221, 219f- for nonhuman primates 91-95, 92f-93f
220f for preverbal infants 98-99, 99f, 123
MEM memory system and 226 independent variables of 150, 161,
for memory dissociation 214-215 178
visual processing
U brain areas for 49-54, 49f, 51f
unconditioned response (UCR), in serial versus parallel 217-221
memory tasks, for preverbal infants visual recognition memory
106, 193 memory tasks for
unconditioned stimulus (UCS), in in nonhuman primates 84-85

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322 THE DEVELOPMENT OF IMPLICIT AND EXPLICIT MEMORY

in preverbal infants 98-99, 123, word form system, implicit memory and
129-130 26-27
neural mediation of 48-51, 49f, 52, 63, word-fragment completion task
90 amnesics’ performance on 34-35
vulnerability, as dissociation variable as memory task 8, 13, 19-20, 250
153-155, 154f children’s studies on 76
functional imaging of 59
W independence in 22-23
what-is-it reflex 109 independent variables of 150-151,
win-shift strategy, for radial arm maze 162, 169, 172, 175-176, 183
60-62 visual stimuli in 26-27
win-stay strategy, for radial arm maze word-identification task, for memory
60-62 performance 25-27
wind chime tasks, for preverbal infants independent variables of 168
120f, 121-122

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In the series ADVANCES IN CONSCIOUSNESS RESEARCH (AiCR) the following titles

have been published thus far or are scheduled for publication:
1. GLOBUS, Gordon G.: The Postmodern Brain. 1995.
2. ELLIS, Ralph D.: Questioning Consciousness. The interplay of imagery, cognition, and
emotion in the human brain. 1995.
3. JIBU, Mari and Kunio YASUE: Quantum Brain Dynamics and Consciousness. An intro-
duction. 1995.
4. HARDCASTLE, Valerie Gray: Locating Consciousness. 1995.
5. STUBENBERG, Leopold: Consciousness and Qualia. 1998.
6. GENNARO, Rocco J.: Consciousness and Self-Consciousness. A defense of the higher-order
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