Y. Netz1
R. Tomer2
The Effect of a Single Aerobic Training Session on
Cognitive Flexibility in Late Middle-Aged Adults
Behavioral Sciences
Abstract
Research has shown that aerobic exercise enhances cognitive
function, specifically executive functions. This study examines
the effect of acute aerobic exercise on cognitive flexibility – an
executive function – in late middle-aged individuals. Fourteen
men and 45 women aged 50 – 64, were randomly assigned to
moderate exercise (60 % of heart rate reserve), moderately-intense (70% of heart rate reserve) exercise, and movie-watching
control groups after a maximal exercise test. Prior to and following the exercise or control sessions participants performed two
Introduction
82
It has been proposed [8] that exercise increases the efficiency of
effortful cognitive processes. Consequently, automatic processes,
or processes that are less effortful, are unaffected by exercise,
since there is presumably little need for increased efficiency in
these environments. This logic suggests that tasks requiring conscious control and increased effort, such as executive control
processes, would benefit most from exercise due to the increased
processing efficiency [16].
Studies assessing the effect of a single bout of aerobic exercise on
cognitive function provide support for this proposition. Those
studies show improvements in executive control tasks such as
response inhibition [23], various choice reaction tasks [1, 3],
stimulus detection tasks [12], or allocation of attentional and
S. Axelrad1
E. Argov1
O. Inbar1
cognitive tasks: the Alternate Uses assessing cognitive flexibility
and the Digit Span Forward subtest from the Wechsler Adult Intelligence Scale – Revised assessing attention span. Results indicated significant improvement in Alternate Uses in the exercise
groups but not in the control group. No group differences were
indicated on the Digit Span. These results provide partial support
for the benefit of acute aerobic exercise on cognitive flexibility.
Key words
Alternate uses · single bout · exercise · advanced age
memory resources [14,18]. Two studies also reported improvements in cognitive flexibility [13, 31], although they did not provide any information on exercise intensity during the experiment.
Executive control processes are mediated by the prefrontal regions of the brain [22, p. 89]. Researchers studying the aging
process have reported substantially larger reductions in graymatter volume in the prefrontal and frontal regions, than in sensory cortical regions in old age [27]. Studies of functional brain
activity employing positron emission tomography have reported
similar trends, with prefrontal regions showing substantially
larger decreases in metabolic activity than do sensory areas of
cortex [29]. On the other hand, a recent study [9] also employing
morphometric technique indicated that aerobic fitness reduced
brain tissue loss in aging humans. In agreement with these struc-
Affiliation
1
The Zinman College of Physical Education and Sport Sciences, Wingate Institute, Netania, Israel
2
Department of Psychology, University of Haifa, Haifa, Israel
Correspondence
Yael Netz, Ph.D. Head · School of Exercise and Sport Sciences · The Zinman College of Physical Education and
Sport Sciences · Wingate Institute 42902 · Netania · Israel · Phone: + 972 98 63 93 61 · Fax: + 972 98 65 09 60 ·
E-mail: [email protected]
Accepted after revision: February 6, 2006
Bibliography
Int J Sports Med 2007; 28: 82 – 87 © Georg Thieme Verlag KG · Stuttgart · New York ·
DOI 10.1055/s-2006-924027 · Published online August 17, 2006 ·
ISSN 0172-4622
tural and metabolic changes, large and disproportionate agerelated deficits have been reported in executive control tasks
[35], while these tasks, on the other hand, have been shown to
be disproportionately sensitive to chronic exercise in the aged
[20]. It is therefore surprising that studies assessing the effect of
a single bout of exercise examined predominantly young people.
Table 1 Descriptive information for the randomized study groups
Variable
Women
In the present study, we assessed the effect of a single bout of
aerobic exercise on cognitive flexibility – an executive function
associated with the prefrontal cortex – in late middle-aged
adults. To the best of our knowledge, this particular executive
function has not been studied in advanced age in relation to a
single bout of exercise.
Cognitive flexibility is considered essential for regulating one’s
own behavior [22] and may be manifested in different ways.
One important aspect of it is the ability to produce a ready flow
of ideas and answers, often in response to a single question. The
flexibility demands in these tasks are found in those processes
which underlie generation of a diversity of responses. This usually requires some form of bypassing automatic and habitual responses and strategies in order to attend to other features and
aspects of knowledge [11]. In the present study, we assessed the
effect of exercise on one task assessing cognitive flexibility,
namely Alternate Uses. In the Alternate Uses test [15], subjects
are required to think beyond common or conventional use of objects to produce instead a variety of alternate uses. This test has
been commonly used for assessing cognitive flexibility [11, 32]. It
was also used by one of the two studies [13] assessing changes in
cognitive flexibility as a result of acute aerobic exercise in young
adults.
Our purpose in the present study was to examine the effect of a
single training session of intensity-controlled aerobic exercise on
cognitive flexibility among late middle-aged individuals. While
cognitive flexibility was expected to benefit from the exercise,
we also measured attention span, which depends less on executive control processes [22, p. 357] so would not be expected to
benefit from the exercise.
Materials and Methods
Participants
Fourteen men and 45 women aged 50 – 64 volunteered to participate in the study. Inclusion criteria, in addition to age, were: no
smoking, no prescribed medication, no neurological or psychiat-
Men
Age (years)
Education (years)
Height (cm)
13
7
70 % HRR*
(n = 20)
14
6
54.99 ± 3.14
56.12 ± 3.4
15.15 ± 1.84
15.15 ± 2.27
168.12 ± 8.4
165.6 ± 7.7
Control
(n = 18)
13
5
54.75 ± 3.01
15.0 ± 1.03
168.46 ± 6.6
Weight (kg)
69.8 ± 13.77
67.4 ± 10.2
64.89 ± 7.31
Habitual physical
activity†
8.25 ± 1.33
8.66 ± 1.41
8.44 ± 1.53
* Heart rate reserve; † An index based on Baecke et al. [4]
ric disease, and no head injury or long-term hospitalization. As
exposure to daily physical activity may stimulate cerebral blood
flow, thus possibly interfering with the effect of a single bout of
exercise on cognitive functioning, participants’ regular physical
activity level was assessed by the Baecke Questionnaire of Habitual Physical Activity [4]. This questionnaire provides three indices of habitual physical activity: occupation activity index, sport
activity index, and leisure activity index. The sport activity index
is composed of multiplication of three scores: level of intensity,
time, and proportion (activity per month). The possible range of
scores on the questionnaire is 3 to 15. The range found in the
present study was 5.13 to 11.42. Therefore, participants reporting
a score of 10.01 or higher were considered highly active, those reporting 8.01 to 10 were considered moderately active, and those
reporting 8 or below were considered sedentary (low activity
level). Participants in each level were then randomly assigned to
one of the following three study groups: moderately-intense
aerobic exercise, moderate aerobic exercise and a control group.
Descriptive information for the three study groups including
gender distribution, age, education, height, weight, and habitual
physical activity is presented in Table 1. One-way analysis of variance (ANOVA) indicated no group differences in any of the descriptive measures.
Physiological measurements
Participants first performed a graded, progressive, maximal exercise test on a motorized treadmill (Woodway, Weil am Rhein,
Germany). During the test heart rate (HR), blood pressure, and
rating of perceived exertion were monitored using a 12-lead
ECG, sphigno-monameter, and Borg scale [5], respectively. The
test served to identify and exclude participants with abnormal
cardiac signs or symptoms, and to verify that participants reach
their respective predicted (+ 5 %) maximal HR (based on the formula: 220-age) and level 17 (or higher) on the Borg scale [5]. The
test, which lasted 9 – 12 minutes [6], commenced with an initial
constant speed of 4.8 km/hr at zero gradient. Thereafter, the
walking speed was increased by 0.3 km/hr every minute until
the fourth minute. From then on, the treadmill speed remained
constant while its gradient was increased by 2 % every minute,
until the participant reached his/her limit of tolerance.
Netz Y et al. Aerobic Session and Cognitive Flexibility… Int J Sports Med 2007; 28: 82 – 87
Behavioral Sciences
Furthermore, the few studies examining the effect of a single
bout of aerobic exercise on advanced-aged adults did not focus
on executive control processes and this is possibly why they
failed to show significant cognitive improvements [10, 25]. The
Emery et al. [10] study did report improvement in verbal fluency
in COPD patients (mean age of 67.8 ± 7.4) but not any improvement in the healthy controls. Another study [21] focused on
executive functions in middle-aged adults (mean age of
42.2 ± 12.2), and did report improvements in response inhibition
tasks. However, participants in that study were medicated depressed patients who may react differently to exercise than
healthy individuals.
60% HRR*
(n = 20)
83
Behavioral Sciences
84
In a second visit (within 10 days from first visit), participants of
the two exercise groups performed a single typical aerobic training session following 20 minutes of sitting at rest during which
HR was determined. The session started by three minutes of slow
walking on the treadmill at a speed that elicited an HR no higher
than 95 b/min (warm-up period). The treadmill speed was then
increased until the participant’s HR reached either 70% (moderately-intense) or 60 % (moderate) of his/her heart rate reserve
(HRR = HRmax – HRrest). Once the target HR was reached (within
three minutes), 35 minutes of walking at the predetermined target HR was then maintained by adjusting the slope and/or speed
of the treadmill belt, followed by a three minutes cool down
(walking at 4.8 km/hr on a level surface). The duration of the
training session was, therefore, 44 minutes. Participants in the
control group watched a nature movie for approximately the
same duration.
Psychological measurements
Assessments
Baseline cognitive performance was assessed immediately before the aerobic (or control) session. Based on the observation of
Heckler and Croce [17] that participants’ cognitive performance
remained heightened when measured immediately, 5 min, and
15 min following exercise, and on the observation of Hillman et
al. [18] that alterations in executive control functions last at least
until participants return to within 10% of baseline HR level, the
cognitive assessments following the sessions were conducted
five minutes after the session, to allow participants cool-down.
Cognitive assessment was conducted by a research assistant
trained in administering neuropsychological tests.
Cognitive tasks
Participants performed two cognitive tasks which were administered in random order: 1. The Alternate Uses (AU) test [15], in
which they were asked to produce as many uses, other than the
common one, for familiar objects. As an example, newspaper is
used most commonly for reading, but alternatively could be used
to start a fire, to wrap garbage, to swat flies, as stuffing to pack
boxes, to line drawers or shelves, etc. [11]. Acceptable responses
must meet criteria of being conceivable uses that are different
from each other and from the common use. Subjects were asked
to produce as many alterative uses (within 90 seconds) for each
object. In total, six objects were included, divided into two sets of
three objects each. One set consisted of a paper clip, a shoe, and a
soft drink can; the other consisted of a glass, a carton box, and a
tire. T-test to assess differences between the two sets and oneway analysis of variance to assess differences between the six
objects, revealed no differences. One set (chosen at random)
served to determine the baseline, and the other was used following the exercise or control session. Four scores were calculated:
(a) AU unique – correct responses excluding repetitions of the
same use. This score represents uncontaminated “pure” cognitive flexibility; (b) AU perseveration within – repeating the same
use for one object (e.g., using a newspaper to wrap a book and
using a newspaper to wrap a box of chocolates), representing a
failure to monitor responses or inhibit an inappropriate response; (c) AU perseveration between – repeating the same use
for different objects (e.g., throwing a shoe at somebody and
throwing a can at somebody), another measure representing a
failure to monitor responses and/or inhibit inappropriate re-
sponse; and (d) AU rule break – responses that do not comply
with the instructions (e.g., stating the regular use of an object,
such as using a glass for drinking). This score represents a failure
to inhibit prepotent responses. Therefore, an improvement in
performance of the AU task includes primarily a higher score on
AU unique, with no change or reduction in the other three scores.
All responses were recorded by the tester, and a neuropsychologist, blind to the group assignment and test session, scored the
responses according to the criteria described above.
2. The Digit Span Forward, a subtest of the Wechsler Adult Intelligence Scale – Revised (WAIS-R), assessing immediate verbal recall [34], provided a measure of attention span. In this test, the
subject listens to random number sequences (length: 3 – 7, two
trials for each sequence length) and is asked to repeat each sequence immediately after hearing it. The participant’s score was
the number of digits in the longest series of numbers he/she
could correctly repeat. As this task involves maintaining information and simply repeating it without any manipulation, it is
considered an attention span task [22, p. 357].
While differing in the level of cognitive demands, neither cognitive task require motor responses.
Results
One-way analysis of variance (ANOVA) that was performed to assess baseline equivalence indicated no group differences in any
of the cognitive measures. We then performed a two-way ANOVA
with repeated measures to assess pre-post differences. Table 2
presents means, SDs and ANOVA scores for the three groups on
all measures. Significant time main effects (pre-post) were indicated on AU unique, and on Digit Span Forward. Marginally significant (p = 0.06) group-by-time interaction was found for the
AU unique measure, indicating a trend of greater improvement
in the two exercise groups than in the control group on those
measures. This trend of interaction was not noticed on Digit Span
Forward. No time or group-by-time differences were found on
AU perseveration or on AU rule break.
As Tukey HSD post-hoc test did not reveal any differences between the two exercise groups, they were combined into one exercise group. A two-way ANOVA with repeated measures was
then performed for two groups only – the combined exercise
group and the control group. Significant group-by-time interactions were found on AU unique (F [1, 56] = 5.87, p = 0.019) indicating a larger improvement for the exercise combined group than
for the control group. Significant time main effects were found
for Digit Span Forward (F [1, 56] = 4.79, p = 0.033) indicating prepost improvement for both the combined exercise and the control groups. Fig. 1 demonstrates the results on AU unique representing executive control processes and on Digit Span Forward
representing attention span, which depends less on executive
control processes. As indicated in Fig. 1, the improvement in AU
unique is selective for the exercise group, while both groups improved on attention span. No main effects or interactions were
found on AU perseveration within, AU perseveration between,
or on AU rule break.
Netz Y et al. Aerobic Session and Cognitive Flexibility… Int J Sports Med 2007; 28: 82 – 87
Table 2 Cognitive tasks performance: means, standard deviations (SDs), and analyses of variance
60 % HRR* (n = 20)
Variables
AU†
Control (n = 18)
Pre
Mean ± SDs
Post
Mean ± SDs
Pre
Mean ± SDs
Post
Mean ± SDs
15.4 ± 5.61
17.9 ± 5.25
16.94 ± 6.25
16.39 ± 5.1
1.8 ± 1.79
1.5 ± 2.2
1.3 ± 1.2
1.33 ± 1.53
1.61 ± 1.38
1.51
1.53
0.6 ± 0.82
0.5 ± 0.95
0.45 ± 0.69
0.35 ± 0.59
0.56 ± 1.29
0.72 ± 1.99
0.00
0.21
1.5 ± 1.79
1.7 ± 2.22
2.5 ± 2.7
3.15 ± 3.72
1.56 ± 1.79
1.11 ± 1.87
7.95 ± 1.96
8.2 ± 1.94
7.9 ± 2.43
8.3 ± 1.98
6.78 ± 1.55
7.44 ± 1.79
Post
Mean ± SDs
13.85 ± 4.11
15.9 ± 4.51
perseveration
within
1 ± 1.38
perseveration
between
unique
rule Break
forward
Time effect
Time X group
F (1, 55)
F (2, 55)
§
#
§
5.96
2.95
0.27
1.48
4.3
0.32
* Heart rate reserve; † alternate uses; ‡ digit span; § p < 0.05; # p = 0.06
Fig. 1 Means, SEs and results of ANOVA
with repeated measures of Alternate Uses
(AU) unique and Digit Span Forward for the
exercise groups (combined) and the control
group.
Behavioral Sciences
DS‡
70% HRR* (n = 20)
Pre
Mean ± SDs
85
Discussion
While there is literature suggesting a positive effect of a single
bout of aerobic exercise on various executive control functions
[14,18, 23], only two studies examined this effect specifically on
cognitive flexibility [13, 31], and these two studies did not provide any information on the exercise intensity during the experiment. Furthermore, although there is evidence showing that executive control functioning is disproportionately sensitive to
aging [35] and to chronic exercise in the aged [20], no studies
have assessed the effect of a single bout of exercise on cognitive
flexibility in advanced age. The purpose of the present study was
therefore to examine the effect of a single bout of intensity controlled aerobic exercise on cognitive flexibility in late middleaged individuals.
Our results suggest that a single and typical aerobic training session may have some beneficial effect on cognitive flexibility in
late middle-aged individuals. Participants in the exercise groups,
but not in the control group, improved their ability to think beyond the conventional use of objects following a single bout of
aerobic exercise. The fact that the improvement as a result of exercise was observed selectively in the cognitive flexibility task,
supports the hypothesis that exercise benefits may be most evident in executive functions associated with the prefrontal cortex,
as indicated in young students [18], or in middle-aged depressed
patients [21] both following acute exercise, or in older adults following six months of exercise [20].
The differences between the experimental and control groups on
the baseline scores of the AU unique (Fig. 1), even if not significant, deserve some consideration. It indicates at least the possibility that the controls did not improve because they were performing at ceiling level, whereas the exercise group had some
room for improvement. Thus, while our results show that the exercise had a beneficial effect on ideational fluency, we cannot
rule out the possibility that had these subjects performed better
at baseline, their performance following exercise may have
shown less improvement, suggesting that the exercise only helps
those who perform suboptimally. Further studies are needed to
clarify this issue.
As expected, the attention span task was not affected by exercise,
possibly because of the lower level cognitive demands it requires
[8]. On the other hand, the time effect observed in all groups on
this task may be attributed to practice effect.
No differences were observed between the two exercise-intensity groups. While studies assessing the effect of acute exercise
on cognitive functioning in young individuals often propose that
Netz Y et al. Aerobic Session and Cognitive Flexibility… Int J Sports Med 2007; 28: 82 – 87
Behavioral Sciences
86
high intensity is needed [18], the limited literature examining
middle-aged or older adults does not provide clear evidence regarding the intensity needed to alter cognitive functioning. One
study [25] examining the effect of low, moderate and high intensity acute exercise on reaction time in late middle-aged women
was unable to indicate improvement for any of the intensities.
Another study [10], applying peak intensity level, failed to report
differences in various cognitive tasks in healthy older adults. A
third study, on the other hand [21], reported alterations in executive control tasks following two levels of low and very low intensity exercise in middle-aged participants. However, these participants were depressed patients on anti-depressant medication
whose reaction to exercise may be different than that of healthy
participants.
Our aim in the present study was to assess the effect of a single
typical training session of middle-aged adults on cognitive functioning. Both selected intensities are within the range of 60% to
80 % HRR recommended by the ACSM [2], and reflect “real-life”
conditions that occur in most aerobic exercise sessions. Our results suggest that both the moderate (60 % HRR) and the moderately-intense (70% HRR) intensities are beneficial in producing
some changes in cognitive flexibility. We did not test higher intensity as middle-aged or older adults do not normally exercise
at higher intensity. It is also not clear whether higher intensity
(75 % to 80% HRR) would have resulted in greater improvement
on the cognitive flexibility, or decrease in performance due to fatigue.
As for duration of the training session, the previous findings are
inconsistent. Two of the studies, reporting no changes in older
adults, conducted a session of 14 [25] and 20 minutes [10]. The
third, reporting cognitive improvement in middle-aged depressed patients [21] conducted a 30-minute session. Steinberg
et al. [31] and Gondola [13] reported improvement in cognitive
flexibility following 23 and 20 minutes, respectively, in young
adults. However, they did not indicate intensity level of the training session. The reflection of “real life” conditions also guided us
in terms of duration of the training session. Therefore, our session lasted 44 minutes including warm-up and cool-down periods.
Several mechanisms have been proposed as mediating the effect
of aerobic activity on cognitive function: increased cerebral
blood flow [28], increase of plasma levels of noradrenaline [7],
or change in neuroelectric processes [18]. Another explanation
for the specific improvement observed in the current study is
related to the role of the dopaminergic system. Dopamine has
been shown to play an important role in the modulation of
behavioral flexibility in animals [26] as well as humans [33].
While a gradual decline occurs in dopamine with aging [19], this
decline is significantly smaller in exercising animals, even in animals that began exercising in middle age [24]. Smith and Zigmond [30] have recently suggested that forced exercise in animals can reduce the vulnerability of dopamine neurons to 6-hydroxydopamine, again suggesting a relationship between exercise and the dopaminergic system.
In the current study, we assessed immediate cognitive changes
only. Little is known of the time course of the impact of exercise
on cognitive functioning. For example, while the increased plasma levels of such neurohormonal substances as epinephrine and
norepinephrine have been linked to cognitive function [7], the
rate of production of these substances and the length of time
they circulate in the blood stream differs depending on the exercise intensity and duration. Further studies are needed to determine how long cognitive performance remains heightened following exercise. Moreover, the magnitude of the acute effects of
exercise on cognitive function is expected to interact with a variety of individual difference variables. For example, the impact of
exercise on cognitive performance may depend on participants’
level of physical fitness or on their level of experience in exercise.
In the present study, exercise experience was controlled by randomly assigning participants from each level of exercise to each
one of the study groups so all the three study groups included all
levels of exercise. Further studies are needed to determine the
relationship between exercise experience and fitness or other
potential moderating factors, and the impact of acute exercise
on cognitive functioning.
Lastly, although equally distributed among the groups, there
were fewer men than women in this study. Although there are
no data in the neuropsychological literature suggesting differences in performance of these tasks between men and women,
hormones may be involved in the physiological mechanisms mediating the effect of physical activity on cognitive performance.
Further studies should examine this point.
Acknowledgement
The study was undertaken at Zinman College of Physical Education and Sport Sciences at the Wingate Institute, Israel.
References
1
2
3
4
5
6
7
8
9
Adam JJ, Teeken JC, Ypelaar PJC, Verstappen FTJ, Paas FGW. Exercisedinduced arousal and information processing. Int J Sport Psychol 1997;
28: 217 – 226
American College of Sports Medicine. American College of Sports
Medicine’s (ACSM’s) Guidelines for Exercise Testing and Prescription.
Baltimore, Maryland: Lippincott Williams and Wilkins, 2005
Arcelin R, Delignierres D, Brisswalter J. Selective effects of physical exercise on choice reaction processes. Percept Mot Skills 1998; 87: 175 –
185
Baecke JAH, Burema J, Frijters, JER. A short questionnaire for the
measurement of a habitual physical activity in epidemiological studies. Am J Clin Nutr 1982; 36: 936 – 942
Borg G. Psychophysical studies of effort and exertion: some historical
theoretical and empirical aspects. In: Borg G, Ottoson D (eds). The
Perception of Exertion in Physical Work. London: Macmillan, 1986:
3 – 12
Buchfuhrer MJ, Hansen JE, Robinson TE, Sue DY, Wasserman K, Whipp
BJ. Optimizing the exercise protocol for cardiopulmonary assessment.
J Appl Physiol 1983; 55: 1558 – 1564
Chmura J, Nazar K, Kaciuba-Ulscilko H. Choice reaction time during
exercise in relation to blood lactate and plasma catecholamine
threshold. Int J Sports Med 1994; 15: 172 – 176
Chodzko-Zajko WJ. Physical fitness, cognitive performance and aging.
Med Sci Sports Exerc 1991; 23: 868 – 872
Colcombe SJ, Erickson KI, Raz N, Webb AG, Cohen NJ, McAuley E,
Kramer A. Aerobic fitness reduces brain tissue loss in aging humans.
J Gerontol A Biol Sci Med Sci 2003; 58: M176 – M180
Netz Y et al. Aerobic Session and Cognitive Flexibility… Int J Sports Med 2007; 28: 82 – 87
10
11
12
13
14
15
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
MacRae PG, Spirduso WW, Walters TJ, Farrar RP, Wilcox RE. Endurance training effects on striated D2 dopamine receptor binding and
striatal dopamine metabolites in presenescent older rats. Psychopharmacology 1987; 92: 236 – 240
Oweis P, Spinks W. Biopsychological, affective and cognitive response
to acute physical activity. J Sports Med Phys Fitness 2001; 41: 528 –
538
Ragozzino ME. The effects of dopamine D(1) receptor blockade in the
prelimbic-infralimbic areas on behavioral flexibility. Learn Mem
2002; 9: 18 – 28
Raz N. Aging of the brain and its impact on cognitive performance: Integration of structural and functional findings. In: Craik F, Salthouse T
(eds). Handbook of Aging and Cognition. Mahwah, NJ: Erlbaum, 2000:
1 – 90
Rogers RL, Meyer JS, Mortel KF. After reaching retirement age physical
activity sustains cerebral perfusion and cognition. J Am Geriatr Soc
1990; 38: 123 – 128
Salmon E, Marquet P, Sandzot B, Degueldre C, Lemaire C, Franck G. Decrease of frontal metabolism demonstrated by positron emission tomography in a population of healthy elderly volunteers. Acta Neurol
Belg 1992; 91: 288 – 295
Smith AD, Zigmond MJ. Can the brain be protected through exercise?
Lessons from an animal model of parkinsonism. Exp Neurol 2003;
184: 31 – 39
Steinberg H, Sykes EA, Moss T, Lowery S, LeBoutillier N, Dewey A. Exercise enhances creativity independently of mood. Br J Sports Med
1997; 31: 240 – 245
Tomer R, Fisher T, Giladi N, Aharon-Peretz J. Dissociation between
spontaneous and reactive flexibility in early Parkinson’s disease. Neuropsychiat Neuropsychol Behav Neurol 2002; 15: 106 – 112
Volkow ND, Gur RC, Wang GJ, Fowler JS, Moberg PJ, Ding YS, Hitzemann R, Smith G, Logan J. Association between decline in brain dopamine activity with age and cognitive and motor impairment in
healthy individuals. Am J Psychiat 1998; 155: 344 – 349
Wechsler D. WAIS-R Manual. New York: Psychological Corporation,
1981
West R. An application of prefrontal cortex function theory to cognitive aging. Psychol Bull 1996; 120: 272 – 292
Behavioral Sciences
16
Emery CF, Honn VJ, Frid DJ, Lebowitz KR, Diaz PT. Acute effects of exercise on cognition in patients with chronic obstructive pulmonary
disease. Am J Respir Care Med 2001; 164: 1624 – 1627
Eslinger PJ, Grattan LM. Frontal lobe and frontal-striatal substrates for
different forms of human cognitive flexibility. Neuropsychologia
1993; 31: 17 – 28
Fleury M, Bard C. Effects of different types of physical activity on the
performance of perceptual tasks in peripheral and central vision and
coincident timing. Ergonomics 1987; 30: 945 – 958
Gondola JC. The effects of a single bout of aerobic dancing on selected
tests of creativity. J Soc Behav Pers 1987; 2: 275 – 278
Grego F, Vallier JM, Collardeau M, Rousseu C, Cremieux J, Brisswalter J.
Influence of exercise duration and hydration status on cognitive function during prolonged cycling exercise. Int J Sports Med 2005; 26:
27 – 33
Guilford JP, Christensen PR, Merrifield PR, Wilson RC. Alternate Uses:
Manual of Instructions and Interpretations. Orange CA: Sheridan Psychological Services, 1978
Hall CD, Smith AL, Keele SW. The impact of aerobic activity on cognitive function in older adults: a new synthesis based on the concept of
executive control. Eur J Cognitive Psychol 2001; 13: 279 – 300
Heckler B, Croce R. Effects of time of posttest after two durations of
exercise on speed and accuracy of addition and subtraction by fit
and less-fit women. Percept Mot Skills 1992; 75: 1059 – 1065
Hillman CH, Snook EM, Jerome GJ. Acute cardiovascular exercise and
executive control function. Int J Psychophysiol 2003; 48: 307 – 314
Joseph JA, Roth GS. Loss of muscarinic regulation of striatal dopamine
function in senescence. Neurochem Int 1992; 20 (Suppl): 237S – 240S
Kramer AF, Hahn S, Cohen NJ, Banich MT, McAuley E, Harrison CR,
Chason J, Vakil E, Bardell L, Boileau RA, Colcombe A. Ageing, fitness
and neurocognitive function. Nature 1999; 400: 417 – 418
Kubesch S, Bretschneider V, Freudenmann R, Weidenhammer N,
Lechtmann M, Spitzer M, Gron G. Aerobic endurance exercise improves executive functions in depressed patients. J Clin Psychiatry
2003; 64: 1005 – 1012
Lezak MD. Neuropsychological Assessment. 3rd ed. New York: Oxford
University Press, 1995
Lichtman S, Poser EG. The effects of exercise on mood and cognitive
functioning. J Psychosom Res 1983; 27: 43 – 52
87
Netz Y et al. Aerobic Session and Cognitive Flexibility… Int J Sports Med 2007; 28: 82 – 87