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 Enhancing
Cognitive
Functioning and
Brain Plasticity

Wojtek Chodzko-Zajko, PhD

University of Illinois at Urbana-Champaign

Arthur F. Kramer, PhD

University of Illinois at Urbana-Champaign

Leonard W. Poon, PhD

University of Georgia

Editors

Human Kinetics
 Library of Congress Cataloging-in-Publication Data
Enhancing cognitive functioning and brain plasticity / Wojtek Chodzko-Zajko,
Arthur F. Kramer, Leonard W. Poon, editors.
p. ; cm. -- (Aging, exercise, and cognition series ; v. 3)
Includes bibliographical references and index.
ISBN-13: 978-0-7360-5791-2 (hard cover)
ISBN-10: 0-7360-5791-9 (hard cover)
1. Cognition--Effect of exercise on. 2. Exercise--Psychological aspects. 3.
Neuroplasticity. 4. Cognition in old age. I. Chodzko-Zajko, Wojtek J. II.
Kramer, Arthur F. III. Poon, Leonard W., 1942- IV. Series: Aging, exercise,
and cognition series ; v. 3.
[DNLM: 1. Aging--physiology. 2. Cognition--physiology. 3. Aged. 4.
Brain--physiology. 5. Exercise. 6. Neuronal Plasticity--physiology. WT 145
E58 2009]
BF311.E54 2009
155.67'13--dc22
2009013298
ISBN-10: 0-7360-5791-9 (print) ISBN-10: 0-7360-8542-4 (Adobe PDF)
ISBN-13: 978-0-7360-5791-2 (print) ISBN-13: 978-0-7360-8542-7 (Adobe PDF)
Copyright © 2009 by Wojtek Chodzko-Zajko, Arthur Kramer, and Leonard W. Poon
All rights reserved. Except for use in a review, the reproduction or utilization of this work in
any form or by any electronic, mechanical, or other means, now known or hereafter invented,
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retrieval system, is forbidden without the written permission of the publisher.
Chapter 2: The Effects of the Cognitive Complexity of Occupational Conditions and Leisure-
Time Activities on the Intellectual Functioning of Older Adults by Carmi Schooler was
written as part of Ms. Schooler’s work with the National Institutes of Health and as such is
considered public domain and not subject to copyright.
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 Contents

Contributors vii
Preface ix

Chapter 1 Brain Imaging Probes Into the Cognitive

and Physiological Effects of Aging 1
Monica Fabiani and Gabriele Gratton

Chapter 2 The Effects of the Cognitive Complexity

of Occupational Conditions and Leisure-Time Activities
on the Intellectual Functioning of Older Adults 15
Carmi Schooler, PhD

Chapter 3 Enhancing Cognitive Function in Older Adults 35

Michelle L. Meade and Denise C. Park, PhD

Chapter 4 A Contextual Approach to Aging and Expertise 49

Daniel G. Morrow

Chapter 5 Exercise Effects on Learning

and Neural Systems 61
Brenda J. Anderson, PhD; Daniel P. McCloskey; Nefta A. Mitchell;
and Despina A. Tata

Chapter 6 Physical Activity and Neurocognitive Function

Across the Life Span 85
Charles H. Hillman, PhD; Sarah M. Buck; and Jason R. Themanson

v
 Contents

Chapter 7 Effects of Acute Exercise on Event-Related

Brain Potentials 111
Keita Kamijo, PhD

Chapter 8 Effects of Hormone Replacement Therapy

on the Brains of Postmenopausal Women: A Review
of Human Neuroimaging Studies 133
Kirk I. Erickson, PhD; and Donna L. Korol

Chapter 9 Physical Activity Programming to Promote

Cognitive Function: Are We Ready for Prescription? 159
Jennifer L. Etnier, PhD

References 177
Index 229
About the Editors 234

vi
 CONTRIBUTORS

Brenda J. Anderson, PhD Donna L. Korol

Department of Psychology and the Department of Psychology, University
Program in Neuroscience, SUNY of Illinois at Urbana-Champaign
Stony Brook Daniel P. McCloskey
Sarah M. Buck Department of Psychology, City Uni-
Department of Health, Physical Edu- versity of New York, Staten Island
cation, and Recreation, Chicago State Michelle L. Meade
University Department of Psychology, Montana
Kirk I. Erickson, PhD State University
Department of Psychology, University Nefta A. Mitchell
of Illinois at Urbana-Champaign Department of Psychology, SUNY
Jennifer L. Etnier, PhD Stony Brook
Department of Exercise and Sport Daniel G. Morrow
Science, University of North Carolina Institute of Aviation, University of
at Greensboro Illinois at Urbana-Champaign
Monica Fabiani Denise C. Park, PhD
Beckman Institute and Psychology School of Behavioral and Brain Sci-
Department, University of Illinois at ences, University of Texas at Dallas
Urbana-Champaign
Carmi Schooler, PhD
Gabriele Gratton National Institutes of Health, Depart-
Beckman Institute and Psychology ment of Health and Human Services
Department, University of Illinois at
Despina A. Tata
Urbana-Champaign
Department of Psychology, Aristotle
Charles H. Hillman, PhD University of Thessaloniki
Department of Kinesiology and Com-
Jason R. Themanson
munity Health, University of Illinois
Department of Psychology, Illinois
at Urbana-Champaign
Wesleyan University
Keita Kamijo, PhD
Institute for Human Science and
Biomedical Engineering, National
Institute of Advanced Industrial Sci-
ence and Technology

vii
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 Preface

T his volume is the third of a series of edited books that examine the
complex role of exercise and physical activity in cognitive functioning
of older adults from a variety of perspectives. The first volume in the series
provided a review of exercise and cognition issues in general and sum-
marized information about the physiological mechanisms relevant to the
understanding of cognitive changes that occur among older adults (Poon,
Chodzko-Zajko, & Tomporowski, 2006). The second volume addressed
mediating and moderating processes that produce individual variations in
the impact of exercise on cognition (Spirduso, Poon, & Chodzko-Zajko,
2007). This third and final volume deals with both exercise and nonexer-
cise interventions that have been shown to influence cognitive and brain
plasticity in older human and nonhuman animals. In all three volumes,
researchers and practitioners who are skilled in exercise, cognition, aging,
neurological or biological mechanisms, or more than one of these areas
came together to discuss these processes and then wrote chapters for the
volumes. It is interesting to note that few authors are experts in all domains,
and the goals of the chapters are to encourage synergy in addressing the
complex issues involved in exercise, physical activities, and cognition in
old age.
In Volume Three, the first chapter by Fabiani and Gratton sets the stage
for later chapters by briefly describing theories of cognitive aging that
have, for the most part, been developed on the basis of behavioral data.
The authors then describe how a variety of complementary neuroimag-
ing measures, including event-related brain potentials, positron emission
tomography, functional magnetic resonance imaging, and event-related
optical imaging, have been used to both test and extend theories of cog-
nitive aging. They also focus on how these neuroimaging measures have
been used to study individual differences in cognition and brain function
particularly with regard to adult aging. They conclude with a prescription
for future research that focuses on the study of adult aging from both
psychological and neuroscience perspectives.
The next three chapters focus on the influence of cognitive training,
intellectual engagement (including cognitively complex work and leisure
activities), and expertise effects on the improvement and maintenance of
selective and general aspects of cognition throughout adulthood. In the

ix
 Preface

second chapter, Carmi Schooler examines the potential reciprocal rela-

tionships between paid employment and leisure-time activities and intel-
lectual functioning among older adults. His chapter provides compelling
evidence that continuing to perform intellectually demanding activities in
mid and later life, during both paid employment and leisure-time activities,
is associated with positive cognitive and psychosocial outcomes. Interest-
ingly, there is also a modest reciprocal relationship such that intellectual
functioning influences the cognitive complexity of work and leisure-time
activities to which individuals are exposed. Schooler argues that examining
the cognitive effects of occupational and nonoccupational activities is of
direct interest to those concerned with understanding how the environ-
ment affects the psychological functioning of older people.
Next, Meade and Park examine the impact of several nonexercise
interventions on human cognitive functioning in older adults. Specifi-
cally, their chapter provides a comparison of the effectiveness of highly
controlled laboratory interventions, in which subjects are trained in an
effort to improve specific cognitive functions, and a variety of more realistic
lifestyle interventions that have been shown to assist in the preservation of
cognitive functioning in older adults. Meade and Park argue that although
most cognitive training studies focus on improving effortful cognitive pro-
cesses, with which older adults have difficulty, a complementary strategy
is to capitalize on cognitive processes that are relatively age invariant (i.e.,
performed relatively automatically) as a means to enhance overall cogni-
tive function. They provide a compelling example of how this might be
achieved from the arena of medical monitoring. Lifestyle factors, including
social interaction, are also discussed in terms of their influence on cogni-
tive function in adulthood.
In chapter 4, the final chapter in this section, Morrow examines the
literature that has addressed the relationship between expertise and aging.
More specifically, his critical review examines how, and to what extent,
expertise in a particular work, sport, or leisure context reduces age-related
declines in both context-specific skills and broader cognitive processes
and abilities. Morrow comes to the conclusion that the maintenance of
high levels of skill requires deliberate and continued practice in a domain
as well as the development of knowledge-based strategies. Furthermore,
maintenance of high levels of skills during aging depends on the charac-
teristics of the person, the task, and the manner in which performance is
assessed. Finally, expertise effects tend to be relatively narrow and pertain
mostly to the domain in which expertise is acquired rather than to general
cognitive abilities.
The next four chapters focus on the influence of specific interventions
on performance, cognition, and brain function of older organisms in both
human and nonhuman models. In chapter 5, Anderson, McCloskey,
Mitchell, and Tata provide a detailed review of what we currently know

x
 Preface

about exercise training effects, with nonhuman animals, on a variety

of brain regions including the hippocampus, cerebellum, motor cortex,
and striatum. The authors examine the extent to which exercise training
effects on performance, learning, and memory are a consequence of the
selective effects of exercise on specific neural systems and mechanisms or
an indirect consequence of general hormonal and vascular responses to
exercise. Their review suggests that exercise has selective effects on brain
areas and that these effects are implicated in the mediation of cognitive
improvements in aging, as reflected in changes in learning and memory.
In chapter 6, Hillman, Buck, and Themanson review the experimental
literature pertaining to the role of exercise and physical activity in aspects
of neurocognitive functioning across the life span. The authors argue that
there is now a wealth of evidence that lifestyle factors protect against cog-
nitive loss during aging. They review the literature suggesting that aging is
associated with disproportionate decrements in executive control processes
relative to other types of cognition and that these declines can be reduced
by exercise interventions. In particular, they summarize evidence for an
association between exercise and physical activity and event-related brain
potential (ERP) activity.
In chapter 7, Keita Kamijo examines issues related to the measure-
ment and assessment of the acute effects of physical activity on several
indices of neuroelectric functioning. Kamijo provides an overview of the
relationship between acute exercise and ERPs. The chapter reviews meth-
odological issues related to the measurement of various components of the
ERP in exercise studies, examining not only the P3 wave but also several
earlier stimulus-locked components (e.g., N1, P2, and N2), as well as the
contingent negative variation (CNV) and error-related negativity (ERN).
The chapter concludes with a discussion of the effects of acute exercise on
ERP indices of cognitive processing in older adults. In the last chapter in
this section, Erickson and Korol examine the impact of a widely employed
nonexercise intervention, hormone replacement therapy (HRT), on cogni-
tive performance in older women. Specifically, they review and synthesize
neuroimaging research, on both brain structure and brain function, that
addresses the effects of HRT in postmenopausal women. On the basis of
findings from preclinical and clinical studies, they argue that HRT affects the
brains of postmenopausal women in a complex and multifactorial fashion,
targeting some brain areas and neural mechanisms but not others. The
authors suggest that future work should utilize neuroimaging techniques
to assess the impact of hormone therapy on cognitive and brain health in
women.
The final chapter considers implications of research on aging, exercise,
and cognition for public health and public policy recommendations. Jen-
nifer Etnier considers whether the strength of the evidence underlying
the relationship between exercise and physical activity interventions

xi
 Preface

and cognitive improvement is sufficient to support specific public health

recommendations. Etnier concludes that based on available evidence,
the prescription of physical activity for the protection or improvement of
cognitive performance is warranted. However, she cautions that specific
details regarding the optimal exercise prescription have yet to be clarified.
Additional research is needed before specific recommendations can be
made regarding the exact type, intensity, and frequency of physical activity
needed to enhance cognitive performance in older adults.
The third Exercise, Cognition, and Aging workshop was sponsored
by the University of Illinois’ Initiative on Aging, the College of Applied
Health Sciences, the NIH Center for Healthy Minds,
the Beckman Institute, and the National Blueprint
Office at the University of Illinois at Urbana-Cham-
paign. The workshop was held at the Levis Faculty
Center, Urbana, Illinois, on October 19-20, 2004.
We acknowledge the valuable assistance and partici-
pation of Lisa Sheppard, Deb Shilts, and Chae-Hee
Park, whose efforts made the conference and this
volume possible.

xii
 Chapter 1
Brain Imaging Probes Into the
Cognitive and Physiological
Effects of Aging
Monica Fabiani
Beckman Institute and Psychology Department,
University of Illinois at Urbana-Champaign

Gabriele Gratton
Beckman Institute and Psychology Department,
University of Illinois at Urbana-Champaign

C ognitive aging is both a very important practical concern and a health-

related problem because it influences (directly or indirectly) a large
proportion of the U.S. population. Therefore, not surprisingly, it is the
target of a large number of studies in a variety of domains—from basic
science work to applied work in the fields of gerontology and geriatrics.
In this chapter we present a selective review of psychophysiological and
brain imaging data. We highlight possible mechanisms that may underlie
cognitive aging in the context of extant psychological theories of aging
based on behavioral data. We also emphasize the role of individual dif-
ferences in enhancing our understanding of the main factors underlying
age-related changes.

Theories of Cognitive Aging:

Behavioral, Psychophysiological,
and Neuroimaging Evidence
Normal cognitive aging is characterized mainly by problems of memory,
attention, and easy fatigue, whereas language abilities appear relatively
spared (Park et al., 1996). Psychologists have developed three major theo-
ries to account for the effects of cognitive aging. These accounts, which
are not necessarily mutually exclusive, include (a) generalized slowing

This work was supported by ADRD grant #C-6-29710 and NIA grant #AG21887 to Monica
Fabiani.

1
 Fabiani and Gratton

(Salthouse, 1996; for a review see Birren & Fisher, 1995), (b) diminished
inhibitory processes (Hasher & Zacks, 1988), and (c) deficits in working
memory function (Craik & Byrd, 1982). These theories are largely based
on behavioral outcomes obtained from comparison of younger and older
adults’ performance in cognitive tasks, and are briefly reviewed later in
this section. In the last 15 years, the increased availability of noninvasive
imaging tools has made it possible to start investigating the physiologi-
cal and anatomical bases of cognitive aging. This knowledge promises to
be extremely useful in identifying target areas that may be amenable to
intervention—in the form of either preventive action or remediation.

Generalized Slowing of Cognitive Processes

Slowing of cognitive processing is typically observed in normal aging using
reaction time or other speeded tasks (Salthouse, 1996). Birren and Fisher
(1995) review an extensive series of studies and conclude that almost all
tasks in which speed is a factor are impaired in aging. Basic measures of
electroencephalographic rhythms (such as the alpha rhythm) are reported
to be slowed down in aging (for a review see Woodruff-Pak, 1997). Simi-
larly, psychophysiological measures of the latency of brain responses (such
as the latency of the P300 component of the event-related brain potential,
ERP) show clear latency increases with aging (Polich et al., 1985).

Reduced Inhibitory Function

Hasher and Zacks (1988) observed that older adults have more difficulty
than younger adults in inhibiting prepotent responses that are no longer
appropriate. Further they observed that tasks involving response conflict
are disproportionately affected by aging. Finally, evidence indicates that
older adults are more easily distracted by irrelevant stimuli than younger
subjects (Kausler & Hakami, 1982; see also Rabbitt, 1965). Taken together,
these data suggest a reduced ability of older adults to inhibit processes or
responses that are not directly relevant to the task at hand. Psychophysi-
ological and neuroimaging evidence consistent with this view is reviewed
later in this section.

Deficits in Working Memory

Several authors have observed that aging is associated with a decline of
executive and working memory function (West, 1996; Moscovitch & Win-
ocur, 1992). In several cases, the working memory deficits are most evident
when distracters are used during the test. These and other similar data point
to a strong relationship between working memory and attention control
(e.g., Kane & Engle, 2000). In this context, the reduced-inhibition account
just discussed can also explain the working memory deficit often observed in

2
 Brain Imaging In Aging

older adults (as a reflection of interference effects, e.g., Bowles & Salthouse,
2003). It is also possible to use the reduced-inhibition hypothesis to account
for generalized slowing effects, as the latter can be the result of more “noise”
at multiple levels within the information-processing system.

Psychophysiological Evidence
Research on cognitive aging based on ERP measures has yielded substantial
evidence in favor of both slowing of processes and reduced inhibition. The
first phenomenon is typically demonstrated by increases in the latency
of various ERP components as a function of age (Polich et al., 1985). For
instance, the latency of P300 increases by about 1 or 2 ms per year (on
average) between the ages of 20 and 80 years (Polich et al., 1985). Age-
related increases in P300 latency, however, are often dissociated from the
corresponding increases in reaction time (Smulders et al., 1999). Because
P300 latency is often considered sensitive to stimulus evaluation time and
relatively less influenced by response processes (see Fabiani et al., 2007),
these data suggest that both stimulus evaluation and response processes
are delayed in aging, consistent with the generalized slowing hypothesis.
However, there are also cases in which effects of age on ERP latency appear
more specific to particular intervals, and thus perhaps attributable to specific
processing delays (see Smulders et al., 1999).
In addition to latency differences, ERP research has shown two other
types of important findings related to cognitive aging: (a) Older adults show
permanence of responses to task-irrelevant stimuli that are typically sup-
pressed in younger adults (e.g., Yamaguchi & Knight, 1991; Fabiani & Fried-
man, 1995; Fabiani et al., 2006); and (b) the scalp distribution of several
ERP components, most notably the P300, appears to change with age (e.g.,
Yamaguchi & Knight, 1991; Fabiani & Friedman, 1995). The first finding
is consistent with the presence of impairments in inhibitory processes and
increased distractibility often reported in aging. The second finding is prob-
ably related to a change in the relative balance of different brain structures
contributing to the scalp ERPs that are observed in aging.

Neuroimaging Evidence
The scalp distribution changes and the reduced suppression of some ERP
responses to repeated or to-be-ignored stimuli resonate with the most
commonly reported findings from the neuroimaging studies of cogni-
tive aging (based on positron emission tomography [PET] and functional
magnetic resonance imaging [fMRI]). This research has pointed out that
aging is associated not only with a decrement of activity in some brain
areas, but also with an increase in others. The earliest results of this type
focused on the presence of bilateral responses in older adults in conditions

3
 Fabiani and Gratton

typically eliciting unilateral responses in younger adults (Cabeza et al.,

1997; Reuter-Lorenz et al., 2000). Subsequent findings have shown that
this phenomenon is more general—and may be caused by a balance shift
between brain structures more directly related to signal processing and
structures more related to elaborative processing (see Cabeza, 2002 for a
review). Some investigators (e.g., Cabeza, 2002) have proposed that these
changes in brain activity are strategic and that they reflect compensatory
efforts employed by older adults to remediate for some deficit in cognitive
abilities.
The interpretation of these effects is still largely debated. In the remainder
of this chapter we focus on some of our own work in the area of functional
brain changes associated with cognitive aging—work that in large part
stresses the mechanisms that may underlie these changes rather than their
hypothesized purposes. As our work has been based on combining several
different measures of brain function, we first briefly review these different
measures and emphasize their advantages and limitations.

Brain Imaging Methods

for the Study of Cognitive Aging
In considering how brain imaging methods can be useful to assess models
of cognitive aging, we base our analysis on a general framework assuming
that stimuli and tasks requirements induce activity in the brain that, in a
general sense, flows from sensory to association to motor areas. This flow
involves the orderly activation of some areas and inhibition of others, and,
especially during familiar or sustained tasks, may be influenced by top-
down control processes emphasizing certain types of cognitive activities
over others. We assume that in aging, for various and to some extent not
completely specified reasons, this normal flow may be sometimes disrupted,
perhaps because of increased delays and variability in the completion of
processes, reduced excitatory and/or inhibitory influences over particular
areas. These changes may in turn induce the recruitment, either automatic
or voluntary (as mediated by strategic choices), of processing routes that
may be different from those used by younger adults. All of the theories
already discussed can be encompassed by this framework. Thus, it would
appear particularly useful that our measurement approach can provide this
type of description at multiple levels within the system.
This description of the information flow would clearly benefit from
brain imaging methods that combine good spatial and temporal resolution.
These methods would allow us to localize functional slowing and detect
changes in the processing flow, thus affording direct visualization of the
phenomena predicted by different theories.