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Improvement of Processing Speed in Executive Function Immediately following an Increase in Cardiovascular Activity

Improvement of Processing Speed in Executive Function Immediately following an Increase in... Hindawi Publishing Corporation Cardiovascular Psychiatry and Neurology Volume 2013, Article ID 212767, 6 pages http://dx.doi.org/10.1155/2013/212767 Research Article Improvement of Processing Speed in Executive Function Immediately following an Increase in Cardiovascular Activity Nicoladie D. Tam Department of Biological Sciences, University of North Texas, Denton, TX 76023, USA Correspondence should be addressed to Nicoladie D. Tam; nicoladie.tam@unt.edu Received 30 June 2013; Accepted 7 August 2013 Academic Editor: Koichi Hirata Copyright © 2013 Nicoladie D. Tam. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. This study aims to identify the acute eeff cts of physical exercise on specific cognitive functions immediately following an increase in cardiovascular activity. Stair-climbing exercise is used to increase the cardiovascular output of human subjects. The color-naming Stroop Test was used to identify the cognitive improvements in executive function with respect to processing speed and error rate. The study compared the Stroop results before and immediately aer ft exercise and before and aer ft nonexercise, as a control. eTh results show that there is a significant increase in processing speed and a reduction in errors immediately aer ft less than 30 min of aerobic exercise. eTh improvements are greater for the incongruent than for the congruent color tests. This suggests that physical exercise induces a better performance in a task that requires resolving conflict (or interference) than a task that does not. er Th e is no significant improvement for the nonexercise control trials. is Th demonstrates that an increase in cardiovascular activity has significant acute effects on improving the executive function that requires conflict resolution (for the incongruent color tests) immediately following aerobic exercise more than similar executive functions that do not require conflict resolution or involve the attention-inhibition process (for the congruent color tests). 1. Introduction mild cognitive impairment (MCI) [9]. Treadmill exercise has been shown to enhance memory plasticity function in Physical exercise is known to improve brain functions based hippocampus through (brain-derived neurotrophic factors on a large body of evidence, ranging from the improvement BDNF) upregulation (in rats), which is potentiated by antide- in academic performance in children to the improvement in pressant treatment [10]. It reverses stress-induced changes cognitive function in both healthy subjects and patients with by establishing functional reconnection of hippocampal mental disorders. Numerous studies have shown that exercise synapses that is mediated by antidepressant actions [11]. These is linked to an improvement in academic achievement for changes have been shown to be related to gene expression schoolchildren [1–5]. The improvement in academic perfor- in the hippocampus resulted from treadmill exercise [12]. mance is greater for physically tfi children than for obese Exercise can improve motor functions in Parkinson’s patients children [6]. Exercise has shown to improve brain processing by enhancing motor circuitry connectivity based on the func- speed by decreasing the event-related brain potential P300 in tional connectivity MRI (fcMRI) brain imaging studies [13]. healthy subjects with sedentary lifestyles [7]. Brain imaging These long-term eeff cts of exercise on brain functions are well studies also showed that exercise improves cognitive func- establishedinbothchildrenand adults,inphysicallyfitand tions by altering the efficiency of the neural circuitry based overweight individuals, in both healthy subjects and patients, on functional magnetic imaging (fMRI) data, especially for and in individual trials and randomized-control trials [14]. overweight children [8]. In this study, we will focus on immediate eects ff of Physical activities can improve memory and cognitive impairment in Alzheimer’s patients and motor functions in exercise on executive function, instead of long-term effects. Executive control is one of the essential cognitive processes Parkinson’s patients. It improves the logical memory and in higher animals to assess and evaluate information, so they reduces the whole brain cortical atrophy in older adults with 2 Cardiovascular Psychiatry and Neurology can make an appropriate decision in response to the stimuli. Red Yellow Blue Green Black It is the higher-level cognitive function that requires selective Pink Orange Brown Gray Purple attention, judgment, anticipation, planning, and reasoning Green Gray Black Blue Yellow to perform the crucial decision-making functions [15]. But Gray Brown Pink Orange Blue when conflicts arise, an appropriate decision is needed to choose one out of many options in order to resolve such Yellow Red Green Black Gray conflicts. Conflicts arise when there are multiple competing Black Brown Purple Orange Pink options to choose from, but only one of the options can be Purple Black Yellow Red Green selected. aTh t is, a person must choose one but not both at the Orange Pink Brown Gray Purple same time. Choosing one option effectively conflicts with the other options, resulting in nullifying the competing options— Figure 1: An example Stroop Test for congruent colors and words. that is, the dilemma created by “wanting to have the cake, andeat it too.”Ifthe conflictisnot resolved,itwillresult in a deadlock, thus preventing a decision from being made, Red Yellow Blue Green Black when the desire is to want both, but it is impossible to have both. us, Th unresolved conflict interferes with the decision- Pink Orange Brown Gray Purple making process. To resolve a conflict, it requires an attention- Green Gray Black Blue Yellow inhibition process to break the deadlock. It is resolved by Gray Brown Pink Orange Blue suppressing one of the choices, in order to select the alterna- Yellow Red Green Black Gray tive option to make a decision. Insufficient inhibition oen ft Black Brown Purple Orange Pink leads to impulsivity, by choosing the inappropriate action instead of the appropriate one. Impulsivity arises when the Purple Black Yellow Red Green inappropriate action cannot be overridden by the appropriate Orange Pink Brown Gray Purple one, due to a lack of inhibition to the inappropriate choice. Numerous studies have shown that long-term exercise Figure 2: An example Stroop Test for incongruent colors and words. programs can improve the executive function in school-aged children [16]. These improvements are related to an increased bilateral prefrontal cortex activity and a reduced bilateral wrong color. It is one of the many classic cognitive tests posterior parietal cortex activity based on fMRI studies [17]. for identifying the impulsivity of the subjects that requires Exercise can improve reaction time, without compromising executive control by the prefrontal cortex [15]. Using the accuracy [18]. Acuteexerciseimprovesexecutive function example illustrated above in the naming of the color of the in (attention deficit hyperactivity disorder ADHD) children, word “RED,” thesubject hastosuppresswhatthe word says using Wisconsin Card Sorting Test (WCST), regardless of (which says red), in order to identify the color as “blue” not age [19], while the associated increase in the middle cerebral red. eTh tendency is to read the word as “red” impulsively artery blood flow velocity (MCAv) is related to cognition at rather than saying it is “blue.” In order to resolve this color rest (not during exercise). The relationship between different conflict, the task requires the attention-inhibition process hemodynamics measures becomes uncoupled during exer- in the prefrontal cortex to suppress the word-recognition cise in terms of global cerebral blood flow, regional cortical process, so that the color-recognition process can supersede oxygenation, and cortical hemodynamics blood volume [20]. the impulsivity to read the word instead of identifying the Toward the goal to determine the immediate effects of color. exercise on brain function, we will design an experiment to identify the cognitive improvements immediately aeft r physical activities. One of the classic psychophysics tests is 2. Methods the Stroop Test [21–23] that addresses this executive function by invoking an attention-inhibition process to resolve the Healthyhuman subjects (bothmaleand female college conflicting interference. It is a simple name-that-color test students) were recruited in this study to perform the Stroop that requires a human subject to name the color of a word, Test before and aeft r physical exercise. eTh Stroop Test was instead of reading the color name. When the word (color administered on a computer screen using two sets of ran- name) matches the color in which the word is printed on, domized color-recognition tests—one for congruent words such as “RED,” no conflict occurs. But when the word (color and colors (Figure 1) and the other for incongruent words name) does not match the color in which the word is printed and colors (Figure 2). Subjects were asked to perform 20 on,suchas“RED,”aconflictiselicited,becausethesubjecthas randomized Stroop Tests before exercise and 20 randomized to choose whethertonamethe color(blue)orreadthe color Stroop Tests immediately following an aerobic exercise that name (red), but not both. This causes the classic interference increases the cardiovascular activity. eTh timing and the in the executive control, when the color-naming process errors were recorded for each Stroop Test. conflicts with the word-recognition process in the brain. The exercise was stairs climbing for 15–30 min to increase In order to name the color, the word-recognition process the cardiac output to approximately 50–70% of the maximal has to be suppressed; otherwise, the word-recognition will heart rate of the subject. We chose the stair-climbing exercise supersede the color recognition, resulting in naming the to increase cardiovascular output in this study for multiple Cardiovascular Psychiatry and Neurology 3 reasons. It provides an objective measure of the actual total energy expenditure (and power consumption) by computing the potential energy (energy used to lift the body mass against gravity by the height traveled for the exercise duration), without using any estimation or indirect measures of energy and power. It is a purely physical exercise, without any specific mental or cognitive engagement, so that the results would not be confounded by the added cognitive variables in performing the exercise. Heart rate, breathing rate, and partial pressure of oxygen saturation in hemoglobin were recorded before and aeft r the exercise. In order to compare the effects of exercise versus 10 nonexercise on executive function, the subjects were also asked to perform the same 2 sets of randomized Stroop Tests Exercise Nonexercise Exercise Nonexercise before and aeft r nonexercise (i.e., 15–30 min of resting period) Heart rate (%) Breathing rate (%) on a different day. This would eliminate any practice eeff cts (not associated with exercise) due to the extra practices on the Figure 3: Change in heartrateand breathingratebeforeand Stroop Test for posttests compared to the pretests. A typical aer ft exercise (for exercise versus nonexercise trials). eTh error bar experiment lasted for an hour, with 15 min of Stroop Test represents standard error of the mean. (pretest), 30 min of exercise (or nonexercise), and another 15 min of Stroop Test (posttest). The study protocol was approved by the Institutional Review Board. Exercise Nonexercise Congruent Incongruent Congruent Incongruent color test color test color test color test 3. Results −5 A total of sixty-five voluntary subjects were included in this study, with the average age of22.4±3.9 (mean± standard deviation), average weight of166.5±44.7 pounds, average −10 height of58.03 ±3.8 , and average (body mass index BMI) of24.8±5.1. eTh average duration of exercise was 18.8± 6.3min. eTh totalheightofstairsclimbed was 151.4±66.8 −15 vertical meters (i.e.,496±219 ft, or 34±15 floors) in less than 30 min. −20 Note that because of the individual differences in the resting heart rate, the breathing rate, and the time spent to complete the Stroop Test, it is important to use the percentage −25 change as a metric to compare the difference between the Figure 4: Percentage change in the time spent on completing the pre- and posttests for the same subject, so that the results are Stroop Tests for the congruent and incongruent color tests (for not confounded by the individual differences. In other words, exercise versus nonexercise trials). the results are normalized relative to the individual subject, so that the improvements for that subject can be identiefi d independent of the individual differences in the baseline or the resting rate. time spent to complete the Stroop Test decreased by 10.2% for Figure 3 shows the aerobic exercise signicfi antly increased the exercise trials but only by 5.8% for the nonexercise trials. the heart rate by 68% and the breathing rate by 58% imme- It shows that there is a 4.4% improvement in processing speed diately aeft r the exercise, compared to the nonexercise trials. for the simple name-that-color test with congruent colors The hemoglobin partial pressure of oxygen ( 𝑃 )dropped and words (which does not involve the attention-inhibition from the average of a 96.4% saturation to a 94.6% level. This process). indicates that the subjects experienced a high oxygen demand In contrast, for the incongruent color test (which requires during and aeft r exercise, when the 𝑃 level dropped below conflict resolution of color interference), the time spent 96%. Normal nonhypoxic 𝑃 level is 96–99%. Any level to complete the Stroop Test decreased by 20.6% for the below𝑃 indicates a hypoxic condition. This occurs when exercise trials but only by 8.1% for the nonexercise trials. the oxygen extraction exceeds oxygen delivery, resulting in a This illustrates that exercise does produce a significant 12.5% decrease in the hemodynamic𝑃 measurement. (𝑃 < 0.01 ) improvement in processing speed for resolving Figure 4 shows the percentage change in the time spent to color interference conflicts in executive function. complete theStroopTest, before andaeft rexercise(forexer- The color-recognition processing speed is doubled for ciseversusnonexercisetrials).Itshowsthat,forthecongruent the executive process that resolves color conflicts (20.6%) color test (that does not elicit conflict or interference), the compared to theexecutive processthatdoesnot require Change in time (%) Change (%) 󸀠󸀠 󸀠󸀠 4 Cardiovascular Psychiatry and Neurology As an informal observation, the subjects oeft n reported it took a lot of mental eo ff rts to complete the incongruent color test compared to the congruent color test. They also reported (aeft r the exercise experiment) that they could complete the Stroop Test so much faster, as if time flied without knowing it. Most interestingly, they were surprised that the incongruent color test became so much easier without any extra mental −5 efforts aer ft the exercise. Thissuggeststhatcardiovascularexercisehas an immedi- −10 ate eeff ct on improving the executive function for both con- gruent and incongruent color Stroop Tests. eTh improvement −15 in processing speed is doubled for the highly demanding task that requires resolving color conflict or interference −20 (incongruent color test) compared to the less demanding Exercise Nonexercise task that does not require resolution of color conflict (the Congruent Incongruent Congruent Incongruent congruent color test). That is, aerobic exercise can improve color test color test color test color test performance by suppressing the impulsivity that interferes with conflict resolution, immediately following an increase Figure 5: Percentage change in errors made during the Stroop Test in cardiovascular activity. It improves the performance by for the congruent and incongruent color tests (for exercise versus increasing the processing speed and by reducing the errors nonexercise trials). made in resolving the color conflict in the Stroop Test. eTh se n fi dings are consistent with those of other studies that reported aerobic exercise accelerated reaction time com- resolve any color conflicts (10.2%). eTh difference in process- pared with the rest condition. The improvement is specific ing speed improvement between incongruent color (8.1%) to Stroop Test that requires conflict resolution in both acute and congruent color tests (5.8%) is not statistically sig- aerobic and strength exercises but not in the Trail Making Test nificant for the nonexercise trials. This differentiates the (for testing visual attention and task switching, which does specific improvements in cognitive functions induced by not require conflict resolution skills) [ 24]. Our results are also the increased cardiovascular activity. eTh processing speed consistent with the n fi dings that the improvement is related to improvement is doubled for a task that requires the attention- cardiovascular activities but not cognitive engagement. Using inhibition process to suppress impulsivity (incongruent color exergaming as the physical activity, other studies have shown test) compared to the speed improvement for a task that does that exercise enhanced children’s speed to resolve interference not require the attention-inhibition process (congruent color from conflicting visuospatial stimuli, but cognitive engage- test). ment (of the exercise game) had no effect on any aspect of Figure 5 shows the percentage change in the errors made task performance [25]. In order to further identify the neural in the Stroop Tests before and aeft r exercise (for exercise circuitryinvolvedinthe executivefunction, Ruedaetal. [26] versus nonexercise trials). It shows a 15% reduction (𝑃< had developed an integrated Attention Network Test (ANT) 0.01) in the errors made for the incongruent color tests aeft r using flanker task [ 27]tomeasure theecffi iencyofthree the exercise trials, whereas there is no statistical significant networks in adults. It showed that moderate aerobic exercise change in errors made aer ft the nonexercise trials. Note modulated the functioning of phasic alertness by increasing that there is little or no change in the congruent color tests the general state of tonic vigilance [28], but aerobic exercise because most subjects did not make any errors when the did not modulate the functioning of either the orienting or color matched the word. It is only when the color did not the executive control attentional networks. This may account match the word that subjects made errors if they did not for the dissimilar results based on other executive function pay attention. This shows that an increase in cardiovascular tests, because these tests tap into the selective attention and activity reduced the error rate following exercise but not aer ft orientation responses rather than into the conflict resolution sedentary resting. process for interference. Taken together, these results show that aerobic exercise can increase the processing speed in resolving conflicting interference and reduce the error rates 4. Discussions that are related to the cardiovascular activity, without neces- eTh results show that there is a signicfi ant improvement in sarily being confounded by any mental cognitive engagement processing executive function aeft r less than 30 min of exer- while doing such exercise. This improvement in executive cise. An increase in cardiovascular activity is demonstrated function may be specific for resolving conflicts of interference to increase the processing speed of executive function and only but not necessary for improving visual attention or task switching processes. to decrease the error rate. eTh improvement in processing speed is doubled for the executive process that requires Note that this is one of the first experiments that identi- the attention-inhibition process to resolve color conflict or fied the specific cognitive improvements attributable to the immediate eeff cts following an increase in cardiovascular interference compared to the executive process that does not require such conflict resolution. activities. As the first phase in the experimental design, Change in errors (%) Cardiovascular Psychiatry and Neurology 5 the present study included a wide range of healthy subjects [3] J. Morales, M. Pellicer-Chenoll, X. Garc´ıa-Masso, ´ M. Gomis, and L.-M. Gonzalez, ´ “Relation between physical activity and (independent of the physical tfi ness level or mental capacity). academic performance in 3rd-year secondary education stu- The present sample in this study included a wide range of dents,” Perceptual and Motor Skills,vol.113,no. 2, pp.539–546, BMI, with an average of24.8±5.1. This suggests that the cognitive improvements were found in both physically tfi and [4] H. J. Syvaoja, M. T. Kantomaa, T. Ahonen, H. Hakonen, A. obese subjects. Given that we have demonstrated the acute Kankaanpaa, and T. H. Tammelin, “Physical activity, sedentary effects of cardiovascular activities on cognitive functions, behavior, and academic performance in Finnish Children,” the next phase in our experimental design will compare the Medicine and Science in Sports and Exercise,2013. specific cognitive improvements between physically active [5] R. A. Wittberg, K. L. Northrup, and L. A. Cottrell, “Children’s and sedentary subjects and between healthy and attention aerobic tfi ness and academic achievement: a longitudinal exam- deficit hyperactivity disorder (ADHD) subjects. Since the ination of students during their h and seventh grade years,” Stroop Test is oen ft used to identify the impulsivity of American Journal of Public Health,vol.102,no. 12,pp. 2303– the subjects, comparing the difference between ADHD and 2307, 2012. healthy subjects will provide specific evidence identifying [6] R. A. London and S. Castrechini, “A longitudinal examination of whetherphysicalexercisewillmakeADHDsubjectsbecome the link between youth physical tfi ness and academic achieve- more impulsive (an increase in both processing speed and ment,” JournalofSchoolHealth,vol.81, no.7,pp. 400–408, 2011. error rate) or pay more concentrated attention (an increase [7] N.Kumar,M.Singh,S.Sood et al., “Eeff ct of acutemoder- in processing speed but a reduction in error rate). Future ate exercise on cognitive P300 in persons having sedentary experiments will identify whether sedentary subjects will lifestyles,” International Journal of Applied and Basic Medical Research,vol.2,no. 1, pp.67–69,2012. benefit more than physically tfi subjects or ADHD subjects [8]C.E.Krafft, N. F. Schwarz, L. Chietal.,“An eightmonth will benefit more than normal subjects. randomized controlled exercise trial alters brain activation during cognitive tasks in overweight children,” Obesity,2013. 5. Summary [9] S.Balsamo,J.M.Willardson,S.Frederico et al., “Eeff ctiveness of exercise on cognitive impairment and Alzheimer’s disease,” This study has demonstrated that an increase in cardiovas- International Journal of General Medicine,vol.6,pp. 387–391, cular activity could have immediate eeff cts on increasing the processing speed and reducing the errors in executive [10] T. Suzuki, H. Shimada, H. Makizako et al., “A randomized control. It doubles the executive function processing speed of controlled trial of multicomponent exercise in older adults with the highly demanding task to resolve conflict or interference mild cognitive impairment,” PLoS One,vol.8,no. 4, ArticleID compared to the less demanding task that does not require e61483, 2013. resolving color conflicts. It suggests that the improvement is [11] Z. H. Fang, C. H. Lee, M. K. Seo et al., “Eeff ct of treadmill more specicfi to enhancing the attention-inhibition process exercise on the BDNF-mediated pathway in the hippocampus than to the executive process that does not require such of stressed rats,” Neuroscience Research,vol.76, no.4,pp. 187– 194, 2013. attention-inhibition. eTh improvement is observed immedi- [12] S. Mojtahedi, M. R. Kordi, S. E. Hosseini,S.F.Omran,and ately aeft r less than 30 min of aerobic exercise. Little or no M. Soleimani, “Eeff ct of treadmill running on the expression improvement is observed for the nonexercise control group of genes that are involved in neuronal differentiation in the aer ft similar period of sedentary resting. hippocampus of adult male rats,” Cell Biology International, Conflict of Interests [13] E.B.Beall,M.J.Lowe, J. L. Albertsetal.,“eTh eeff ctof forced-exercise therapy for Parkinson’s disease on motor cortex eTh author conrm fi ed that there is no direct n fi ancial relation functional connectivity,” Brain Connect, vol. 3, pp. 190–198, 2013. with any commercial identities that might lead to a conflict of [14] P. J. Smith, J. A. Blumenthal, B. M. Hoffman et al., “Aerobic exer- interests. cise and neurocognitive performance: a meta-analytic review of randomized controlled trials,” Psychosomatic Medicine,vol.72, no.3,pp. 239–252, 2010. Acknowledgment [15] T.W.Robbins, “Dissociatingexecutive functionsofthe pre- frontal cortex,” Philosophical Transactions of the Royal Society eTh author greatly appreciates Ms. Krista Smith for the B,vol.351,pp. 1463–1470, 1996. helpful suggestions and for proofreading the paper. [16] G. O’Malley, “Aerobic exercise enhances executive function and academic achievement in sedentary, overweight children aged 7–11 years,” Journal of Physiotherapy,vol.57, no.4,p.255,2011. References [17] C. L. Davis, P. D. Tomporowski, J. E. McDowell et al., “Exercise [1] L. J. B. Hill,J.H.G.Williams,L.Aucott, J. oTh mson,and improves executive function and achievement and alters brain M. Mon-Williams, “How does exercise benefit performance activation in overweight children: a randomized, controlled on cognitive tests in primary-school pupils?” Developmental trial,” Health Psychology, vol. 30, no. 1, pp. 91–98, 2011. Medicine and Child Neurology,vol.53, no.7,pp. 630–635, 2011. [18] B. Rattray and D. Smee, “Exercise improves reaction time [2] J. E. Donnelly and K. Lambourne, “Classroom-based physi- without compromising accuracy in a novel easy-to-administer cal activity, cognition, and academic achievement,” Preventive tablet-based cognitive task,” JournalofScience andMedicinein Medicine, vol. 52, supplement 1, pp. S36–S42, 2011. Sport,2013. fift 6 Cardiovascular Psychiatry and Neurology [19] Y. K. Chang, S. Liu, H. H. Yu, and Y. H. Lee, “Eeff ct of acute exercise on executive function in children with attention deficit hyperactivity disorder,” Archives of Clinical Neuropsychology, vol. 27, pp. 225–237, 2012. [20] S. J. Lucas, P. N. Ainslie, C. J. Murrell, K. N. Thomas, E. A. Franz, and J. D. Cotter, “Eeff ct of age on exercise-induced alterations in cognitive executive function: relationship to cerebral perfusion,” Experimental Gerontology,vol.47, pp.541– 551, 2012. [21] J. R. Stroop, “Factors aeff cting speed in serial verbal reactions,” Psychological Monographs: General and Applied, vol. 50, pp. 38– 48, 1938. [22] A. R. Jensen and W. D. Rohwer Jr., “The stroop color-word test: a review,” Acta Psychologica,vol.25, pp.36–93,1966. [23] J. R. Stroop, “Studies of interference in serial verbal reactions,” Journal of Experimental Psychology,vol.18, no.6,pp. 643–662, [24] C. R. Alves, B. Gualano, P. P. Takao et al., “Ee ff cts of acute physical exercise on executive functions: a comparison between aerobic and strength exercise,” Journal of Sport & Exercise Psychology,vol.34, no.4,pp. 539–549, 2012. [25] J. R. Best, “Exergaming immediately enhances children’s execu- tive function,” Developmental Psychology,vol.48,no.5,pp.1501– 1510, 2012. [26] M. R. Rueda, J. Fan, B. D. McCandliss et al., “Development of attentional networks in childhood,” Neuropsychologia,vol.42, no. 8, pp. 1029–1040, 2004. [27] M. R. Rueda, M. I. Posner, M. K. Rothbart, and C. P. Davis- Stober, “Development of the time course for processing conflict: an event-related potentials study with 4 year olds and adults,” BMC Neuroscience,vol.5,article 39,2004. [28] F. Huertas, J. Zahonero, D. Sanabria, and J. Lupia´n, ˜ “Function- ing of the attentional networks at rest vs. during acute bouts of aerobic exercise,” JournalofSport andExercisePsychology,vol. 33,no. 5, pp.649–665,2011. 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Improvement of Processing Speed in Executive Function Immediately following an Increase in Cardiovascular Activity

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Copyright © 2013 Nicoladie D. Tam. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Hindawi Publishing Corporation Cardiovascular Psychiatry and Neurology Volume 2013, Article ID 212767, 6 pages http://dx.doi.org/10.1155/2013/212767 Research Article Improvement of Processing Speed in Executive Function Immediately following an Increase in Cardiovascular Activity Nicoladie D. Tam Department of Biological Sciences, University of North Texas, Denton, TX 76023, USA Correspondence should be addressed to Nicoladie D. Tam; nicoladie.tam@unt.edu Received 30 June 2013; Accepted 7 August 2013 Academic Editor: Koichi Hirata Copyright © 2013 Nicoladie D. Tam. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. This study aims to identify the acute eeff cts of physical exercise on specific cognitive functions immediately following an increase in cardiovascular activity. Stair-climbing exercise is used to increase the cardiovascular output of human subjects. The color-naming Stroop Test was used to identify the cognitive improvements in executive function with respect to processing speed and error rate. The study compared the Stroop results before and immediately aer ft exercise and before and aer ft nonexercise, as a control. eTh results show that there is a significant increase in processing speed and a reduction in errors immediately aer ft less than 30 min of aerobic exercise. eTh improvements are greater for the incongruent than for the congruent color tests. This suggests that physical exercise induces a better performance in a task that requires resolving conflict (or interference) than a task that does not. er Th e is no significant improvement for the nonexercise control trials. is Th demonstrates that an increase in cardiovascular activity has significant acute effects on improving the executive function that requires conflict resolution (for the incongruent color tests) immediately following aerobic exercise more than similar executive functions that do not require conflict resolution or involve the attention-inhibition process (for the congruent color tests). 1. Introduction mild cognitive impairment (MCI) [9]. Treadmill exercise has been shown to enhance memory plasticity function in Physical exercise is known to improve brain functions based hippocampus through (brain-derived neurotrophic factors on a large body of evidence, ranging from the improvement BDNF) upregulation (in rats), which is potentiated by antide- in academic performance in children to the improvement in pressant treatment [10]. It reverses stress-induced changes cognitive function in both healthy subjects and patients with by establishing functional reconnection of hippocampal mental disorders. Numerous studies have shown that exercise synapses that is mediated by antidepressant actions [11]. These is linked to an improvement in academic achievement for changes have been shown to be related to gene expression schoolchildren [1–5]. The improvement in academic perfor- in the hippocampus resulted from treadmill exercise [12]. mance is greater for physically tfi children than for obese Exercise can improve motor functions in Parkinson’s patients children [6]. Exercise has shown to improve brain processing by enhancing motor circuitry connectivity based on the func- speed by decreasing the event-related brain potential P300 in tional connectivity MRI (fcMRI) brain imaging studies [13]. healthy subjects with sedentary lifestyles [7]. Brain imaging These long-term eeff cts of exercise on brain functions are well studies also showed that exercise improves cognitive func- establishedinbothchildrenand adults,inphysicallyfitand tions by altering the efficiency of the neural circuitry based overweight individuals, in both healthy subjects and patients, on functional magnetic imaging (fMRI) data, especially for and in individual trials and randomized-control trials [14]. overweight children [8]. In this study, we will focus on immediate eects ff of Physical activities can improve memory and cognitive impairment in Alzheimer’s patients and motor functions in exercise on executive function, instead of long-term effects. Executive control is one of the essential cognitive processes Parkinson’s patients. It improves the logical memory and in higher animals to assess and evaluate information, so they reduces the whole brain cortical atrophy in older adults with 2 Cardiovascular Psychiatry and Neurology can make an appropriate decision in response to the stimuli. Red Yellow Blue Green Black It is the higher-level cognitive function that requires selective Pink Orange Brown Gray Purple attention, judgment, anticipation, planning, and reasoning Green Gray Black Blue Yellow to perform the crucial decision-making functions [15]. But Gray Brown Pink Orange Blue when conflicts arise, an appropriate decision is needed to choose one out of many options in order to resolve such Yellow Red Green Black Gray conflicts. Conflicts arise when there are multiple competing Black Brown Purple Orange Pink options to choose from, but only one of the options can be Purple Black Yellow Red Green selected. aTh t is, a person must choose one but not both at the Orange Pink Brown Gray Purple same time. Choosing one option effectively conflicts with the other options, resulting in nullifying the competing options— Figure 1: An example Stroop Test for congruent colors and words. that is, the dilemma created by “wanting to have the cake, andeat it too.”Ifthe conflictisnot resolved,itwillresult in a deadlock, thus preventing a decision from being made, Red Yellow Blue Green Black when the desire is to want both, but it is impossible to have both. us, Th unresolved conflict interferes with the decision- Pink Orange Brown Gray Purple making process. To resolve a conflict, it requires an attention- Green Gray Black Blue Yellow inhibition process to break the deadlock. It is resolved by Gray Brown Pink Orange Blue suppressing one of the choices, in order to select the alterna- Yellow Red Green Black Gray tive option to make a decision. Insufficient inhibition oen ft Black Brown Purple Orange Pink leads to impulsivity, by choosing the inappropriate action instead of the appropriate one. Impulsivity arises when the Purple Black Yellow Red Green inappropriate action cannot be overridden by the appropriate Orange Pink Brown Gray Purple one, due to a lack of inhibition to the inappropriate choice. Numerous studies have shown that long-term exercise Figure 2: An example Stroop Test for incongruent colors and words. programs can improve the executive function in school-aged children [16]. These improvements are related to an increased bilateral prefrontal cortex activity and a reduced bilateral wrong color. It is one of the many classic cognitive tests posterior parietal cortex activity based on fMRI studies [17]. for identifying the impulsivity of the subjects that requires Exercise can improve reaction time, without compromising executive control by the prefrontal cortex [15]. Using the accuracy [18]. Acuteexerciseimprovesexecutive function example illustrated above in the naming of the color of the in (attention deficit hyperactivity disorder ADHD) children, word “RED,” thesubject hastosuppresswhatthe word says using Wisconsin Card Sorting Test (WCST), regardless of (which says red), in order to identify the color as “blue” not age [19], while the associated increase in the middle cerebral red. eTh tendency is to read the word as “red” impulsively artery blood flow velocity (MCAv) is related to cognition at rather than saying it is “blue.” In order to resolve this color rest (not during exercise). The relationship between different conflict, the task requires the attention-inhibition process hemodynamics measures becomes uncoupled during exer- in the prefrontal cortex to suppress the word-recognition cise in terms of global cerebral blood flow, regional cortical process, so that the color-recognition process can supersede oxygenation, and cortical hemodynamics blood volume [20]. the impulsivity to read the word instead of identifying the Toward the goal to determine the immediate effects of color. exercise on brain function, we will design an experiment to identify the cognitive improvements immediately aeft r physical activities. One of the classic psychophysics tests is 2. Methods the Stroop Test [21–23] that addresses this executive function by invoking an attention-inhibition process to resolve the Healthyhuman subjects (bothmaleand female college conflicting interference. It is a simple name-that-color test students) were recruited in this study to perform the Stroop that requires a human subject to name the color of a word, Test before and aeft r physical exercise. eTh Stroop Test was instead of reading the color name. When the word (color administered on a computer screen using two sets of ran- name) matches the color in which the word is printed on, domized color-recognition tests—one for congruent words such as “RED,” no conflict occurs. But when the word (color and colors (Figure 1) and the other for incongruent words name) does not match the color in which the word is printed and colors (Figure 2). Subjects were asked to perform 20 on,suchas“RED,”aconflictiselicited,becausethesubjecthas randomized Stroop Tests before exercise and 20 randomized to choose whethertonamethe color(blue)orreadthe color Stroop Tests immediately following an aerobic exercise that name (red), but not both. This causes the classic interference increases the cardiovascular activity. eTh timing and the in the executive control, when the color-naming process errors were recorded for each Stroop Test. conflicts with the word-recognition process in the brain. The exercise was stairs climbing for 15–30 min to increase In order to name the color, the word-recognition process the cardiac output to approximately 50–70% of the maximal has to be suppressed; otherwise, the word-recognition will heart rate of the subject. We chose the stair-climbing exercise supersede the color recognition, resulting in naming the to increase cardiovascular output in this study for multiple Cardiovascular Psychiatry and Neurology 3 reasons. It provides an objective measure of the actual total energy expenditure (and power consumption) by computing the potential energy (energy used to lift the body mass against gravity by the height traveled for the exercise duration), without using any estimation or indirect measures of energy and power. It is a purely physical exercise, without any specific mental or cognitive engagement, so that the results would not be confounded by the added cognitive variables in performing the exercise. Heart rate, breathing rate, and partial pressure of oxygen saturation in hemoglobin were recorded before and aeft r the exercise. In order to compare the effects of exercise versus 10 nonexercise on executive function, the subjects were also asked to perform the same 2 sets of randomized Stroop Tests Exercise Nonexercise Exercise Nonexercise before and aeft r nonexercise (i.e., 15–30 min of resting period) Heart rate (%) Breathing rate (%) on a different day. This would eliminate any practice eeff cts (not associated with exercise) due to the extra practices on the Figure 3: Change in heartrateand breathingratebeforeand Stroop Test for posttests compared to the pretests. A typical aer ft exercise (for exercise versus nonexercise trials). eTh error bar experiment lasted for an hour, with 15 min of Stroop Test represents standard error of the mean. (pretest), 30 min of exercise (or nonexercise), and another 15 min of Stroop Test (posttest). The study protocol was approved by the Institutional Review Board. Exercise Nonexercise Congruent Incongruent Congruent Incongruent color test color test color test color test 3. Results −5 A total of sixty-five voluntary subjects were included in this study, with the average age of22.4±3.9 (mean± standard deviation), average weight of166.5±44.7 pounds, average −10 height of58.03 ±3.8 , and average (body mass index BMI) of24.8±5.1. eTh average duration of exercise was 18.8± 6.3min. eTh totalheightofstairsclimbed was 151.4±66.8 −15 vertical meters (i.e.,496±219 ft, or 34±15 floors) in less than 30 min. −20 Note that because of the individual differences in the resting heart rate, the breathing rate, and the time spent to complete the Stroop Test, it is important to use the percentage −25 change as a metric to compare the difference between the Figure 4: Percentage change in the time spent on completing the pre- and posttests for the same subject, so that the results are Stroop Tests for the congruent and incongruent color tests (for not confounded by the individual differences. In other words, exercise versus nonexercise trials). the results are normalized relative to the individual subject, so that the improvements for that subject can be identiefi d independent of the individual differences in the baseline or the resting rate. time spent to complete the Stroop Test decreased by 10.2% for Figure 3 shows the aerobic exercise signicfi antly increased the exercise trials but only by 5.8% for the nonexercise trials. the heart rate by 68% and the breathing rate by 58% imme- It shows that there is a 4.4% improvement in processing speed diately aeft r the exercise, compared to the nonexercise trials. for the simple name-that-color test with congruent colors The hemoglobin partial pressure of oxygen ( 𝑃 )dropped and words (which does not involve the attention-inhibition from the average of a 96.4% saturation to a 94.6% level. This process). indicates that the subjects experienced a high oxygen demand In contrast, for the incongruent color test (which requires during and aeft r exercise, when the 𝑃 level dropped below conflict resolution of color interference), the time spent 96%. Normal nonhypoxic 𝑃 level is 96–99%. Any level to complete the Stroop Test decreased by 20.6% for the below𝑃 indicates a hypoxic condition. This occurs when exercise trials but only by 8.1% for the nonexercise trials. the oxygen extraction exceeds oxygen delivery, resulting in a This illustrates that exercise does produce a significant 12.5% decrease in the hemodynamic𝑃 measurement. (𝑃 < 0.01 ) improvement in processing speed for resolving Figure 4 shows the percentage change in the time spent to color interference conflicts in executive function. complete theStroopTest, before andaeft rexercise(forexer- The color-recognition processing speed is doubled for ciseversusnonexercisetrials).Itshowsthat,forthecongruent the executive process that resolves color conflicts (20.6%) color test (that does not elicit conflict or interference), the compared to theexecutive processthatdoesnot require Change in time (%) Change (%) 󸀠󸀠 󸀠󸀠 4 Cardiovascular Psychiatry and Neurology As an informal observation, the subjects oeft n reported it took a lot of mental eo ff rts to complete the incongruent color test compared to the congruent color test. They also reported (aeft r the exercise experiment) that they could complete the Stroop Test so much faster, as if time flied without knowing it. Most interestingly, they were surprised that the incongruent color test became so much easier without any extra mental −5 efforts aer ft the exercise. Thissuggeststhatcardiovascularexercisehas an immedi- −10 ate eeff ct on improving the executive function for both con- gruent and incongruent color Stroop Tests. eTh improvement −15 in processing speed is doubled for the highly demanding task that requires resolving color conflict or interference −20 (incongruent color test) compared to the less demanding Exercise Nonexercise task that does not require resolution of color conflict (the Congruent Incongruent Congruent Incongruent congruent color test). That is, aerobic exercise can improve color test color test color test color test performance by suppressing the impulsivity that interferes with conflict resolution, immediately following an increase Figure 5: Percentage change in errors made during the Stroop Test in cardiovascular activity. It improves the performance by for the congruent and incongruent color tests (for exercise versus increasing the processing speed and by reducing the errors nonexercise trials). made in resolving the color conflict in the Stroop Test. eTh se n fi dings are consistent with those of other studies that reported aerobic exercise accelerated reaction time com- resolve any color conflicts (10.2%). eTh difference in process- pared with the rest condition. The improvement is specific ing speed improvement between incongruent color (8.1%) to Stroop Test that requires conflict resolution in both acute and congruent color tests (5.8%) is not statistically sig- aerobic and strength exercises but not in the Trail Making Test nificant for the nonexercise trials. This differentiates the (for testing visual attention and task switching, which does specific improvements in cognitive functions induced by not require conflict resolution skills) [ 24]. Our results are also the increased cardiovascular activity. eTh processing speed consistent with the n fi dings that the improvement is related to improvement is doubled for a task that requires the attention- cardiovascular activities but not cognitive engagement. Using inhibition process to suppress impulsivity (incongruent color exergaming as the physical activity, other studies have shown test) compared to the speed improvement for a task that does that exercise enhanced children’s speed to resolve interference not require the attention-inhibition process (congruent color from conflicting visuospatial stimuli, but cognitive engage- test). ment (of the exercise game) had no effect on any aspect of Figure 5 shows the percentage change in the errors made task performance [25]. In order to further identify the neural in the Stroop Tests before and aeft r exercise (for exercise circuitryinvolvedinthe executivefunction, Ruedaetal. [26] versus nonexercise trials). It shows a 15% reduction (𝑃< had developed an integrated Attention Network Test (ANT) 0.01) in the errors made for the incongruent color tests aeft r using flanker task [ 27]tomeasure theecffi iencyofthree the exercise trials, whereas there is no statistical significant networks in adults. It showed that moderate aerobic exercise change in errors made aer ft the nonexercise trials. Note modulated the functioning of phasic alertness by increasing that there is little or no change in the congruent color tests the general state of tonic vigilance [28], but aerobic exercise because most subjects did not make any errors when the did not modulate the functioning of either the orienting or color matched the word. It is only when the color did not the executive control attentional networks. This may account match the word that subjects made errors if they did not for the dissimilar results based on other executive function pay attention. This shows that an increase in cardiovascular tests, because these tests tap into the selective attention and activity reduced the error rate following exercise but not aer ft orientation responses rather than into the conflict resolution sedentary resting. process for interference. Taken together, these results show that aerobic exercise can increase the processing speed in resolving conflicting interference and reduce the error rates 4. Discussions that are related to the cardiovascular activity, without neces- eTh results show that there is a signicfi ant improvement in sarily being confounded by any mental cognitive engagement processing executive function aeft r less than 30 min of exer- while doing such exercise. This improvement in executive cise. An increase in cardiovascular activity is demonstrated function may be specific for resolving conflicts of interference to increase the processing speed of executive function and only but not necessary for improving visual attention or task switching processes. to decrease the error rate. eTh improvement in processing speed is doubled for the executive process that requires Note that this is one of the first experiments that identi- the attention-inhibition process to resolve color conflict or fied the specific cognitive improvements attributable to the immediate eeff cts following an increase in cardiovascular interference compared to the executive process that does not require such conflict resolution. activities. As the first phase in the experimental design, Change in errors (%) Cardiovascular Psychiatry and Neurology 5 the present study included a wide range of healthy subjects [3] J. Morales, M. Pellicer-Chenoll, X. Garc´ıa-Masso, ´ M. Gomis, and L.-M. Gonzalez, ´ “Relation between physical activity and (independent of the physical tfi ness level or mental capacity). academic performance in 3rd-year secondary education stu- The present sample in this study included a wide range of dents,” Perceptual and Motor Skills,vol.113,no. 2, pp.539–546, BMI, with an average of24.8±5.1. This suggests that the cognitive improvements were found in both physically tfi and [4] H. J. Syvaoja, M. T. Kantomaa, T. Ahonen, H. Hakonen, A. obese subjects. Given that we have demonstrated the acute Kankaanpaa, and T. H. Tammelin, “Physical activity, sedentary effects of cardiovascular activities on cognitive functions, behavior, and academic performance in Finnish Children,” the next phase in our experimental design will compare the Medicine and Science in Sports and Exercise,2013. specific cognitive improvements between physically active [5] R. A. Wittberg, K. L. Northrup, and L. A. Cottrell, “Children’s and sedentary subjects and between healthy and attention aerobic tfi ness and academic achievement: a longitudinal exam- deficit hyperactivity disorder (ADHD) subjects. Since the ination of students during their h and seventh grade years,” Stroop Test is oen ft used to identify the impulsivity of American Journal of Public Health,vol.102,no. 12,pp. 2303– the subjects, comparing the difference between ADHD and 2307, 2012. healthy subjects will provide specific evidence identifying [6] R. A. London and S. Castrechini, “A longitudinal examination of whetherphysicalexercisewillmakeADHDsubjectsbecome the link between youth physical tfi ness and academic achieve- more impulsive (an increase in both processing speed and ment,” JournalofSchoolHealth,vol.81, no.7,pp. 400–408, 2011. error rate) or pay more concentrated attention (an increase [7] N.Kumar,M.Singh,S.Sood et al., “Eeff ct of acutemoder- in processing speed but a reduction in error rate). Future ate exercise on cognitive P300 in persons having sedentary experiments will identify whether sedentary subjects will lifestyles,” International Journal of Applied and Basic Medical Research,vol.2,no. 1, pp.67–69,2012. benefit more than physically tfi subjects or ADHD subjects [8]C.E.Krafft, N. F. Schwarz, L. Chietal.,“An eightmonth will benefit more than normal subjects. randomized controlled exercise trial alters brain activation during cognitive tasks in overweight children,” Obesity,2013. 5. Summary [9] S.Balsamo,J.M.Willardson,S.Frederico et al., “Eeff ctiveness of exercise on cognitive impairment and Alzheimer’s disease,” This study has demonstrated that an increase in cardiovas- International Journal of General Medicine,vol.6,pp. 387–391, cular activity could have immediate eeff cts on increasing the processing speed and reducing the errors in executive [10] T. Suzuki, H. Shimada, H. Makizako et al., “A randomized control. It doubles the executive function processing speed of controlled trial of multicomponent exercise in older adults with the highly demanding task to resolve conflict or interference mild cognitive impairment,” PLoS One,vol.8,no. 4, ArticleID compared to the less demanding task that does not require e61483, 2013. resolving color conflicts. It suggests that the improvement is [11] Z. H. Fang, C. H. Lee, M. K. Seo et al., “Eeff ct of treadmill more specicfi to enhancing the attention-inhibition process exercise on the BDNF-mediated pathway in the hippocampus than to the executive process that does not require such of stressed rats,” Neuroscience Research,vol.76, no.4,pp. 187– 194, 2013. attention-inhibition. eTh improvement is observed immedi- [12] S. Mojtahedi, M. R. Kordi, S. E. Hosseini,S.F.Omran,and ately aeft r less than 30 min of aerobic exercise. Little or no M. Soleimani, “Eeff ct of treadmill running on the expression improvement is observed for the nonexercise control group of genes that are involved in neuronal differentiation in the aer ft similar period of sedentary resting. hippocampus of adult male rats,” Cell Biology International, Conflict of Interests [13] E.B.Beall,M.J.Lowe, J. L. Albertsetal.,“eTh eeff ctof forced-exercise therapy for Parkinson’s disease on motor cortex eTh author conrm fi ed that there is no direct n fi ancial relation functional connectivity,” Brain Connect, vol. 3, pp. 190–198, 2013. with any commercial identities that might lead to a conflict of [14] P. J. Smith, J. A. Blumenthal, B. M. Hoffman et al., “Aerobic exer- interests. cise and neurocognitive performance: a meta-analytic review of randomized controlled trials,” Psychosomatic Medicine,vol.72, no.3,pp. 239–252, 2010. Acknowledgment [15] T.W.Robbins, “Dissociatingexecutive functionsofthe pre- frontal cortex,” Philosophical Transactions of the Royal Society eTh author greatly appreciates Ms. Krista Smith for the B,vol.351,pp. 1463–1470, 1996. helpful suggestions and for proofreading the paper. [16] G. O’Malley, “Aerobic exercise enhances executive function and academic achievement in sedentary, overweight children aged 7–11 years,” Journal of Physiotherapy,vol.57, no.4,p.255,2011. References [17] C. L. Davis, P. D. Tomporowski, J. E. McDowell et al., “Exercise [1] L. J. B. Hill,J.H.G.Williams,L.Aucott, J. oTh mson,and improves executive function and achievement and alters brain M. Mon-Williams, “How does exercise benefit performance activation in overweight children: a randomized, controlled on cognitive tests in primary-school pupils?” Developmental trial,” Health Psychology, vol. 30, no. 1, pp. 91–98, 2011. Medicine and Child Neurology,vol.53, no.7,pp. 630–635, 2011. [18] B. Rattray and D. Smee, “Exercise improves reaction time [2] J. E. Donnelly and K. Lambourne, “Classroom-based physi- without compromising accuracy in a novel easy-to-administer cal activity, cognition, and academic achievement,” Preventive tablet-based cognitive task,” JournalofScience andMedicinein Medicine, vol. 52, supplement 1, pp. S36–S42, 2011. Sport,2013. fift 6 Cardiovascular Psychiatry and Neurology [19] Y. K. Chang, S. Liu, H. H. Yu, and Y. H. Lee, “Eeff ct of acute exercise on executive function in children with attention deficit hyperactivity disorder,” Archives of Clinical Neuropsychology, vol. 27, pp. 225–237, 2012. [20] S. J. Lucas, P. N. Ainslie, C. J. Murrell, K. N. Thomas, E. A. Franz, and J. D. Cotter, “Eeff ct of age on exercise-induced alterations in cognitive executive function: relationship to cerebral perfusion,” Experimental Gerontology,vol.47, pp.541– 551, 2012. [21] J. R. Stroop, “Factors aeff cting speed in serial verbal reactions,” Psychological Monographs: General and Applied, vol. 50, pp. 38– 48, 1938. [22] A. R. Jensen and W. D. Rohwer Jr., “The stroop color-word test: a review,” Acta Psychologica,vol.25, pp.36–93,1966. [23] J. R. Stroop, “Studies of interference in serial verbal reactions,” Journal of Experimental Psychology,vol.18, no.6,pp. 643–662, [24] C. R. Alves, B. Gualano, P. P. Takao et al., “Ee ff cts of acute physical exercise on executive functions: a comparison between aerobic and strength exercise,” Journal of Sport & Exercise Psychology,vol.34, no.4,pp. 539–549, 2012. [25] J. R. Best, “Exergaming immediately enhances children’s execu- tive function,” Developmental Psychology,vol.48,no.5,pp.1501– 1510, 2012. [26] M. R. Rueda, J. Fan, B. D. McCandliss et al., “Development of attentional networks in childhood,” Neuropsychologia,vol.42, no. 8, pp. 1029–1040, 2004. [27] M. R. Rueda, M. I. Posner, M. K. Rothbart, and C. P. Davis- Stober, “Development of the time course for processing conflict: an event-related potentials study with 4 year olds and adults,” BMC Neuroscience,vol.5,article 39,2004. [28] F. Huertas, J. Zahonero, D. Sanabria, and J. Lupia´n, ˜ “Function- ing of the attentional networks at rest vs. during acute bouts of aerobic exercise,” JournalofSport andExercisePsychology,vol. 33,no. 5, pp.649–665,2011. 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