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INHIBITION
in Cognition
Edited by
David S. Gorfein and
Colin MLMacLeod
DECADE
<>/BEHAVIOR/0
Published by
American Psychological Association
750 First Street, NE
Washington, DC 20002
www.apa.org
The opinions and statements published are the responsibility of the authors, and such opinions
and statements do not necessarily represent the policies of the American Psychological
Association.
BF323.148154 2007
153—dc22 2007002957
Contributors xi
Preface xv
Acknowledgments xvii
Part I. Introduction 1
Introduction
The Concept of Inhibition
in Cognition
Colin M. MacLeod
Everyone knows what inhibition is—and that creates a very real problem. The
idea is so ingrained that it is difficult to discuss it as a scientific concept without
contamination from existing world knowledge. Yet discussing it is exactly what
cognitive scientists have been attempting to do with renewed vigor in the recent
past, owing to at least three factors: the growth of cognitive neuroscience,
developments in cognitive modeling, and newly described cognitive phenomena.
Beginning with the phenomenon of negative priming (for reviews, see Fox,
1995; May, Kane, & Hasher, 1995; Tipper, 2001) and spurred by two influential
books that appeared in quick succession just over a decade ago (Dagenbach &
Carr, 1994; Dempster & Brainerd, 1995), interest in cognitive inhibition grew.
Of course, the desire to mesh cognition with neuroscience also has provided a
powerful impetus for understanding the place of inhibition in the current
conceptualization of mind and brain. This interest is well illustrated by the
inclusion of inhibition as one of only 16 core concepts in a recent effort to grapple
with concepts—free of empirical research findings—that are fundamental to
memory (Roediger, Dudai, & Fitzpatrick, in press).
This chapter is intended as a broad introduction to the concept of inhibition
in cognition and consequently to this book as a whole. For this reason, I take
no strong stand on the value of the concept (although I have expressed a
skeptical point of view elsewhere; see MacLeod, in press; MacLeod, Dodd,
Sheard, Wilson, & Bibi, 2003). In this chapter, the goal is to set out the issues
involved in the empirical study and theoretical understanding of the concept
of inhibition as it applies to the operation of cognition. So I begin with what
this chapter is and is not about. This chapter is not about the neural concept
of inhibition: It is accepted that neurons certainly can inhibit each other. This
chapter also is not about the physical-response concept of inhibition: It is
Preparation of this chapter was supported by Discovery Grant A7459 from the Natural Sciences
and Engineering Research Council of Canada. I greatly appreciate discussions with my colleagues
Ori Friedman and Steve Spencer and with my friend Kevin Dunbar about the research described
in the first part of the chapter. I also thank Nigel Gopie and Kathleen Hourihan for their careful,
helpful comments.
COLIN M. MACLEOD
accepted that actions can be initiated and then cancelled (Logan & Cowan,
1984), although the extent to which these two domains of inhibition relate to
each other remains to be established. This chapter is about the concept of
cognitive inhibition—the idea that mental processes or representations can
be inhibited.
Trying to force these two levels of analysis to fit together so that they can
share a common term is unlikely to help advance understanding of either, a
point that was made a long time ago (Breese, 1899). Indeed, it is noteworthy
that even Anderson and Spellman (1995) chose to set aside one of the hallmark
features of neural inhibition—its brief duration—in their argument for a much
longer lasting cognitive inhibition, saying, "The strong assumption that cogni-
tive inhibition should follow the characteristics of individual neurons receiving
a single inhibitory input ... is likely to be far too simple" (p. 95).
To reiterate, then, this chapter is about the cognitive or mental concept
of inhibition, also variously called repression, suppression, or restraining (and
sometimes even blocking, although blocking appears to have a different mean-
ing for most investigators). For excellent histories of ideas concerning inhibi-
THE CONCEPT OF INHIBITION IN COGNITION 5
tion, the reader should consult S. Diamond, Balvin, and Diamond (1963) and
particularly the more recent treatment by Smith (1992). As a point of departure,
The Oxford English Dictionary (1989) lists four meanings for inhibition. The
first two relate to the societal or legal prohibition senses and so are not relevant
here. The remaining two relate to the physiological and psychological senses,
consistent with the admonishment (MacLeod, in press; MacLeod et al., 2003)
to keep these two senses distinct.
Focusing just on cognitive inhibition, the active ingredients appear to be
primarily two: mental withholding and reduced performance. The former is an
inference from the latter, reflecting a confusion that pervades the literature.
In cognition, inhibition is sometimes a measurable phenomenon, sometimes a
theory about the cause of that phenomenon, and often both. As always, it is a
bad idea to name a phenomenon using the label for one of the possible theories
that might explain it. This is not to claim that that theory is wrong, but to
urge avoidance of confusion. Inhibition may—or may not—play a key role in
explaining (aspects of) cognition: That is what this book is about, with the aim
of considering the variety of perspectives.
Developmental Psychology
Social Psychology
A major question in social psychology is what causes a stereotype to come to
mind (activation) and to influence one's impression (application) when one
comes in contact with a member of the stereotype-relevant group. Kunda and
Spencer (2003) proposed that the activation of stereotypes is driven by three
goals. First is the goal of comprehension—simplifying and understanding the
situation. Second is the goal of self-enhancement—the nurturing of self-esteem.
Third is the goal of avoiding prejudice—either to see oneself as egalitarian or
to comply with egalitarian social norms. The comprehension and self-
enhancement goals function similarly: As the strength of the goal increases,
often the likelihood of stereotype activation and application increases as well.
The stereotype simplifies interpretation of the situation and maintains or even
enhances self-esteem.
What makes the Kunda and Spencer (2003) framework unique is the
emphasis on inhibition. They argued that it is also possible that a stronger
goal will lead to inhibiting the stereotype. So for comprehension, when informa-
tion about the specific individual is available, it may be better to inhibit the
stereotype and instead use the individuating information. For self-esteem, if
one is motivated to form a positive impression of an individual, it may be better
to inhibit the (negative) stereotype. In the case of the goal of avoiding prejudice,
the primary process may in fact be inhibitory, acting to suppress the negative
stereotypic information. Kunda and Spencer suggested that the application of
inhibition may be cognitively demanding and may become more likely to fail
as cognitive resource demands increase. Such an emphasis on inhibition in
understanding social processes is not unique to Kunda and Spencer (see, e.g.,
Beer, Heerey, Keltner, Scabini, & Knight, 2003; Forster, Liberman, & Higgins,
2005; Shah, Friedman, & Kruglanski, 2002; von Hippel & Gonsalkorale, 2005;
see also chap. 7, this volume).
Many illustrations are possible in the domain of clinical and personality psy-
chology, but I describe only one. Wood, Mathews, and Dalgleish (2001) asked
subjects who were either high or low in trait anxiety to make decisions on each
trial about whether a single target word was or was not related to the sentence
that preceded it. Sentences were constructed in pairs, differing only in the
final word, an example being "At the party she had some punch/wine," where
the first of the two possible final words was a homograph. The task was to
determine whether the probe word fist was semantically related to the sentence.
The answer should have been no in both cases, but critically, fist is related to
the other sense of the homograph punch. Therefore, failure to suppress that
other sense would slow rejection of fist. The prediction was that such a failure
to inhibit would be more likely in high-anxiety subjects.
In their first experiment, Wood et al. (2001) found that all subjects were
faster to reject the probe fist in response to wine than to punch but that there
was no effect of anxiety level. This finding might seem to conflict with their
8 COLIN M. MACLEOD
prediction, but in their second experiment, when subjects were under higher
cognitive load because they had to rehearse a set of digits during task perfor-
mance, the pattern changed. Anxious subjects showed a pattern suggesting a
general impairment of inhibitory processing. Wood et al. concluded that
"anxiety-prone individuals have a deficit in tasks requiring the inhibition of
currently irrelevant meanings" but that this impairment "may be revealed only
when task-related control strategies are limited by mental load" (p. 176). This
emphasis on inhibition in understanding personality and abnormal behavior
is not unique to Wood et al. (see, e.g., Bohne, Keuthen, Tuschen-Caffier, &
Wilhelm, 2005; Dorahy, Middleton, & Irwin, 2005; Kuhl & Kazen, 1999; see
also chaps. 10, 11, and 13, this volume).
Behavioral Neuroscience
Colvin, Dunbar, and Grafman (2001) contrasted patients with frontal lobe
lesions with normal subjects performing a water jug task (Luchins, 1942). In
the version of the task that they used, subjects had to manipulate three jugs
with known capacities (A = 8 units, B = 5 units, C = 3 units) to reach a specified
goal state (A = 4 units, B = 4 units, C = 0 units). Patients, particularly those
with left dorsolateral prefrontal lesions, performed poorly, especially when
they had to make a counterintuitive move—one that resulted in a step back
from the goal state and therefore was not predicted by a simple means-end
analysis without planning. In particular, patients tended to prefer to go back
to an earlier state rather than to make a counterintuitive move. Colvin et al.
argued that intact functioning of the left dorsolateral prefrontal region is
necessary in part for "the inhibition of a response generated by an adopted
problem-solving strategy" (p. 1138). Of course, this emphasis on inhibition
in understanding behavior from a neuroscientific perspective is certainly not
unique to Colvin et al. (see, e.g., Amos, 2000; Durston et al., 2002; Gazzaley,
Cooney, Rissman, & D'Esposito, 2005) and is in fact very much in the Zeitgeist
in this domain.
Inhibition in Cognition
In the preceding section, the goal was to indicate the breadth and current
impact of the concept of inhibition as an explanatory element in traditionally
recognized subdomains of psychology other than cognition. Much of this impact
can be placed at the doorstep of cognition, in that the tasks and explanations
in these domains have often been modified from cognitive antecedents. Let us
turn now to cognition itself, where the growth of explanations involving inhibi-
tion has been dramatic in the past 25 to 30 years since research on negative
priming began to lead the charge.
All of the illustrations in the preceding section are instances where cogni-
tive inhibition has been proposed as a key mechanism in explaining observed
behavior. It is fair to say that the concept is by now ubiquitous, having been
applied to, among other cognitive activities, action, language, meaning, mem-
THE CONCEPT OF INHIBITION IN COGNITION 9
Attention
In negative priming experiments, each trial typically involves two stimuli, one
to be attended and one to be ignored. If the ignored stimulus on one trial
becomes the target stimulus on the next trial, responding to it is slower than
would have been the case if the previous trial were completely unrelated. The
argument originally put forward by Neill (1977; for an updated view, see
chap. 4, this volume) and championed by Tipper (1985, 2001) was that the
ignored stimulus was inhibited to permit the target stimulus to control respond-
ing. Then, when that ignored stimulus itself became the target, the inhibition
just applied to it had to be overcome for it to control responding, and this
process took additional time.
This apparently simple task, with its intuitively appealing explanation,
was quickly followed in the attention literature by the phenomenon of inhibition
of return (Posner & Cohen, 1984). The prototypical procedure consists of three
outline boxes with subjects instructed to fixate on the center box and to move
only their attention (not their eyes) during the trial. Then one of the two
peripheral boxes brightens, drawing attention to that cued location despite the
cue not being informative. Shortly thereafter, a target appears. When the time
between cue and target is brief, target detection is faster at the cued location—
the intuitive pattern of automatic capturing of attention by the cue. However,
when the cue-target interval is longer than 300 milliseconds, detection is
slower at the cued location. As the term inhibition of return was intended to
suggest, attention may be inhibited from reorienting back to the cued location,
resulting in delayed or slower processing there (e.g., Rafal, Egly, & Rhodes,
1994; Reuter-Lorenz, Jha, & Rosenquist, 1996).
Much research has followed in which inhibition has been proposed to play
a key role in attentional processing (e.g., task switching in Allport, Styles, &
10 COLIN M. MACLEOD
Hsieh, 1994; visual marking in Watson & Humphreys, 1997; see also chaps.
2-4, this volume). The nature of that role, however, appears to be broad,
leading to the question of what these various forms of inhibition have in com-
mon. Are there common processes or at least a small set of crucial processes?
Such a limitation would seem to be important for the concept of attentional
inhibition to be coherent and parsimonious. Efforts have been made to address
this question. Thus, Rafal and Henik (1994) distinguished three inhibitory
processes. The first is inhibition of responding to signals at unattended loca-
tions, the kind of process involved in spatial versions of negative priming. The
second is endogenous inhibition of reflexes, more akin to stopping a prepotent
response. The third is reflexive inhibition of the detection of subsequent signals,
the kind of process involved in inhibition of return. The glue that links these
processes together as inhibition remains elusive, but that certainly does not
mean that such a linkage cannot or will not be accomplished as research
progresses.
Turning to the neural level, there is also evidence consistent with atten-
tional inhibition operating at intermediate levels of cortical processing, in visual
area V4 and in TEO (the posterior portion of the inferior temporal cortex).
Attention may work in a push—pull fashion to promote processing of what is
attended and to inhibit processing of what is unattended (for a review, see
Kastner & Pinsk, 2004). This push-pull idea is also familiar as center-surround
and goes by other names as well. The extent to which this idea relates directly
to cognitive inhibition must be clarified, but the connection is unquestion-
ably appealing.
Memory
The employment of inhibition as an explanatory tool is no less prominent in
memory than it is in attention. This emphasis began with the work of Hasher
and Zacks (1988; see also chap. 8, this volume) focusing on the cognitive costs
associated with aging and bridging the attention-memory gap. Like Rafal and
Henik (1994), Hasher and Zacks described three components of inhibition, all
seen as influencing the optimal operation of working memory (via attention):
(a) control of the specific information that enters working memory, (b) control
of the information that is deleted from working memory, and (c) prevention of
possibly relevant but incorrect responses from being executed. Their argument,
based on an extended series of studies, is that older people do not execute these
functions as well as younger people because older people do not inhibit as well.
Their research program has made a concerted effort to characterize these
proposed processes, and their account has been influential (for review and
commentary, see Burke, 1997; McDowd, 1997; for other views, see chaps. 9
and 10, this volume). The Hasher and Zacks inhibition-based account of aging
has not been without critics, however: As Chariot and Feyereisen (2005) con-
cluded in their review concerning executive control and prefrontal cortex, "The
changes tied to cognitive aging in the domain of episodic memory cannot be
uniquely explained by a deficit in inhibition" (p. 349, my translation).
THE CONCEPT OF INHIBITION IN COGNITION 11
Next to the work of Hasher and Zacks (1988), the most visible work arguing
for inhibitory processes in memory is that of Anderson and colleagues (Ander-
son, 2005; Anderson & Green, 2001; Anderson & Spellman, 1995). Anderson
and Spellman (1995) had subjects learn an initial list of category-instance
word pairs and then practice half of the items in half of the categories. They
found that the unpracticed half of a category was actually more poorly remem-
bered than a corresponding half from a category in which no items were prac-
ticed. Moreover, not only were the unpracticed items less accessible from their
studied cues, they were also less accessible from independent semantically
related probes. It appeared that these unpracticed items had become generally
less accessible, a pattern consistent with their representations having been
inhibited.
Anderson and Green (2001) went on to develop a clever variation on this
paradigm that they referred to as the "think/no think" paradigm. After studying
a list of pairs, participants were asked to try not to think of a previously studied
word when provided with a cue that had been studied with that word. Having
tried not to think of a word resulted in poorer recall than in the control condition,
where studied pairs were neither thought of nor suppressed. Moreover, the
target word was also less likely to be recalled to a semantic cue that had not
been studied: It appeared that the target word itself, not just the studied pair,
was inhibited as a result of not thinking about it. This cue independence has
been seen by Anderson and Green as the strongest evidence of inhibition being
involved in memory.
There are many other illustrations of inhibitory accounts applied to mem-
ory phenomena. Anderson (2005) pointed to the related paradigm of directed
forgetting (for a review, see MacLeod, 1998), in which it has been argued
(Basden, Basden, & Gargano, 1993) that when the first half of a list is followed
by an instruction to forget, it is more poorly remembered than the second, to-
be-remembered half of the list because it has been inhibited. Similarly, when
subjects are provided with a partial set of members of a studied list to aid the
retrieval of the remainder, this typically hurts rather than helps performance—
the part-list cuing effect (Slamecka, 1968). Bauml and Asian (2006) argued
that this effect is, at least under certain conditions, due to inhibition of retrieval.
There are certainly plenty of other illustrations of memory phenomena held
to be at least in part attributable to inhibition (see, e.g., Brown, Zoccoli, &
Leahy, 2005; Racsmany & Conway, 2006; Veling & van Knippenberg, 2004).
In the memory literature, another way of examining inhibition has been
prominent—that of individual differences. Two different approaches have been
taken—that of Engle and his colleagues and that of N. P. Friedman, Miyake,
and their colleagues. Engle and his colleagues (Conway & Engle, 1994; Engle,
Conway, Tuholski, & Shisler, 1995; Kane & Engle, 2000) put forth a perspective
related to that of Hasher and Zacks (1988) in that it also emphasizes attentional
resources and working memory, although Engle's emphasis on general capacity
distinguishes his view from theirs. Conway and Engle (1994) argued that a
major source of individual differences in cognitive ability is the capacity of
working memory and that these individual differences result from variation
in attentional resources that in turn produce "differences in the ability to
12 COLIN M. MACLEOD
inhibit or suppress irrelevant information" (p. 354). The impact of these differ-
ences should be evident in controlled tasks requiring attention but not in more
automatic tasks. Redick, Heitz, and Engle (chap. 7, this volume) have carried
forward this work.
N. P. Friedman, Miyake, and their colleagues (N. P. Friedman & Miyake,
2004; Miyake, Friedman, Emerson, Witzki, & Howerter, 2000) have taken
the more psychometric approach of seeking patterns of correlations between
cognitive measures. Thus, when N. P. Friedman and Miyake (2004) directed
this approach to examining inhibition, they administered an extensive battery
of tasks, several of which were seen as markers for each of three key inhibitory
abilities: prepotent response inhibition (e.g., Stroop task, stop signal task),
resistance to distractor interference (e.g., Eriksen flanker task, word naming
with distraction), and resistance to proactive interference (e.g., Brown-
Peterson task, cued recall task). Via structural equation modeling, they found
the first two inhibitory abilities to be closely related but the third to be clearly
separate, suggesting to them that the overall "trait" of inhibition was not
unified. More recent work (N. P. Friedman et al., 2006) has suggested that,
unlike updating working memory, which is related to intelligence, inhibiting
prepotent responses (and shifting mental sets) is not.
Turning to the neural level, again multiple approaches have been taken.
Hamilton and Martin (2005; see also chap. 12, this volume) presented a case
study of a participant with left inferior frontal damage in which the pattern
of task dissociation across a series of inhibition tasks seemed incompatible
with a single shared neural substrate. Their work simultaneously supports
that of Miyake et al. (2000) and N. P. Friedman and Miyake (2004)—in showing
dissociations across proposed inhibitory abilities—and conflicts with it—in
showing dissociations within abilities that the Miyake group held to be single
abilities. Hamilton and Martin suggested that one fruitful direction to pursue
would be to consider that variations might hinge not on common brain areas
but rather on common patterns of neurotransmitters, such as dopamine and
norepinephrine, which may influence how different brain areas operate. The
puzzle of the diversity of brain areas involved in some ability might then be
resolved by the commonality in the neurotransmitters affecting these areas.
This is an intriguing idea, although it also highlights the fact that cognitive
neurotopology may be even more complicated than currently viewed.
Gazzaley et al. (2005) used functional magnetic resonance imaging (fMRI)
to examine how aging affects what they saw as a goal-driven mechanism in
support of attention and memory that enhances and suppresses the processing
of sensory information. On each trial, participants watched two faces and two
scenes in random order and tried to remember one type of stimulus or the
other for a subsequent recognition test; the control was passive viewing without
the memory instruction. Like younger adults, older adults showed enhanced
cortical activity for task-relevant representations; unlike younger adults, older
adults were deficient in suppression of cortical activity for task-irrelevant repre-
sentations. Gazzaley et al. saw their results as indicating that the inhibitory
function was deficient in the older subjects but that the enhancement function
was unaffected by aging, which fits nicely with the Hasher and Zacks (1988)
theory (although Gazzaley et al. did note that their results could reflect excita-
THE CONCEPT OF INHIBITION IN COGNITION 13
The following section outlines in brief form four of the key issues related to
understanding cognitive inhibition as a theoretical construct: definition, rela-
tion to neural inhibition, relation to interference, and measurement and the
baseline problem.
Definition
When applied to cognition, the term inhibition definitely does not have a consis-
tent meaning. Many scholars have recognized this, as two recent quotes and
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