Effects of acute aerobic exercise on multiple aspects of executive function in preadolescent children

Psychology of Sport and Exercise 15 (2014) 627e636

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Psychology of Sport and Exercise journal homepage: www.elsevier.com/locate/psychsport

Effects of acute aerobic exercise on multiple aspects of executive function in preadolescent children Ai-Guo Chen a, Jun Yan a, Heng-Chan Yin b, Chien-Yu Pan c, Yu-Kai Chang d, * a

College of Physical Education, Yangzhou University, Yangzhou, Jiangsu, People's Republic of China School of Physical Education and Sports Science, Beijing Normal University, Beijing, People's Republic of China c Department of Physical Education, National Kaohsiung Normal University, Kaohsiung, Taiwan, People's Republic of China d Graduate Institute of Athletics and Coaching Science, National Taiwan Sport University, Taoyuan County, Taiwan, People's Republic of China b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 26 January 2014 Received in revised form 14 June 2014 Accepted 14 June 2014 Available online 28 June 2014

Objective: The current study assessed the effects of acute exercise on three core executive functions in preadolescents and controlled for the moderating role of age. Design: A true experimental design. Methods: Thirty-four third-grade children and 53 fifth-grade preadolescents were randomly assigned into either an acute exercise group or a control group. The exercise protocol was designed for ecological validity and involved group jogging at moderate intensity for 30 min. Participants completed inhibition, working memory, and shifting-related executive function tasks prior to and following the treatment. Results: Acute exercise facilitated performance in three executive function tasks in children in both grade groups; nevertheless, better performance was observed among the fifth graders in inhibition and working memory, but not in shifting, when compared with the third graders. Conclusion: These findings suggest that acute exercise benefited three primary aspects of executive function in general, regardless of the preadolescent age group, whereas the distinct components of executive function had different developmental trajectories. © 2014 Elsevier Ltd. All rights reserved.

Keywords: Acute exercise Inhibition Preadolescence Shifting Working memory

Researchers have long been interested in how acute bouts of exercise influence cognitive function (Tomporowski, 2003). Although some inconsistent findings have been reported, early narrative reviews have generally revealed that acute exercise benefits cognitive performance (McMorris & Graydon, 2000; Tomporowski, 2003). This positive effect of acute exercise on cognition is consistent with recent meta-analyses indicating that acute exercise facilitates cognitive function, particularly after (as opposed to during) the bout, with a small to large effect (effect sizes range from 0.10 to 1.41) (Chang, Labban, Gapin, & Etnier, 2012; Lambourne & Tomporowski, 2010; McMorris, Sproule, Turner, & € nigs, Scherder, & Oosterlaan, 2014). Hale, 2011; Verburgh, Ko Despite the more solid consensus regarding the positive effects of exercise, heterogeneity in the reported magnitudes of the effect sizes as well as the later moderation analyses of these meta-analyses suggest that certain factors may moderate the relationship between

* Corresponding author. Graduate Institute of Athletics and Coaching Science, National Taiwan Sport University, No.250, Wenhua 1st Rd., Guishan Township, Taoyuan County 333, Taiwan, People's Republic of China. E-mail address: [email protected] (Y.-K. Chang). http://dx.doi.org/10.1016/j.psychsport.2014.06.004 1469-0292/© 2014 Elsevier Ltd. All rights reserved.

acute exercise and cognition. Further research is necessary to explore the potential involvement of such factors. The majority of research into acute exercise and cognition focuses on young adults (Audiffren, Tomporowski, & Zagrodnik, 2008, 2009; Chang, Chi, et al., 2014; Lambourne, Audiffren, & Tomporowski, 2010; Pesce & Audiffren, 2011), middle-aged adults (Chang, Ku, Tomporowski, Chen, & Huang, 2012; Chang, Tsai, Huang, Wang, & Chu, 2014), or old adults (Pesce & Audiffren, 2011; Pesce, Cereatti, Forte, Crova, & Casella, 2011). The results of these studies typically indicate that moderate-intensity aerobic exercise for approximately 30 min facilitates cognitive performance and that exercise-induced physiological arousal is a potential mechanism by which these beneficial effects are mediated (Audiffren et al., 2008; Lambourne et al., 2010; Pesce & Audiffren, 2011; Pesce et al., 2011). Similarly, Chang and colleagues have indicated that acute bouts of resistance exercise also increase cognitive performance and that a moderate intensity (i.e., 70% of the 10 repetition maximum, RM) leads to greater effects than light and vigorous intensities (i.e., 40% and 100% of the 10 RM, respectively), which indicates an inverted-U doseeresponse relationship between acute exercise and cognitive function (Chang, Chu, Chen, & Wang, 2011; Chang & Etnier, 2009). These findings suggest that acute,

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short-term bouts of exercise at moderate intensity improve cognitive function in both young and old adult populations. Notably, compared with studies examining adult populations, relatively few studies have been conducted with preadolescent children. Nonetheless, improvements in cognitive function following acute bouts of exercise have been demonstrated in children (Sibley & Etnier, 2003; Verburgh et al., 2014). For example, acute combined aerobic and resistance exercise for 15 min improved concentration in fourth-grade children (Caterino & Polak, 1999). Additionally, better choices and reduced response times following acute aerobic ^nes, 2010) as well as exercise (Ellemberg & St-Louis-Desche improved free recall memory after acute bouts of exercise involving circuit training and group games (Pesce, Crova, Cereatti, Casella, & Bellucci, 2009) have been observed in children aged 7e12 years. Nevertheless, empirical studies have also yielded disparate findings. Specifically, only physical fitness, not acute exercise, has been shown to impact cognitive performance and neuroelectric activity in children aged 13e15 years (Stroth et al., 2009). Furthermore, improved cognition was only observed in children in the fourth grade, not in children in the second or third grade (Caterino & Polak, 1999). Importantly, previous studies have examined children over wide ranges of the developmental period spanning from middle childhood (i.e., 5e8 years) to all of preadolescence (i.e., 9e14 years) (Corsaro, 2005). These inconsistent findings suggest that the developmental period may modulate the effects of acute exercise on cognitive function. Studies that isolate the factor of age are needed to further explore this possibility. Therefore, the first aim of our study was to determine the effects of acute exercise on cognition by focusing on children in early (i.e., 9 year olds in third grade) and mid- (11 year olds in fifth grade) preadolescence; these periods were specifically chosen to minimize the potential confounding factor in previous studies that included preadolescents across different stages of maturation (e.g., 13e15 years old). Additionally, the type of cognition assessed should be considered when examining the effects of acute exercise (Chang, Labban, et al., 2012; Lambourne & Tomporowski, 2010; McMorris et al., 2011). While early acute exercise studies examined performance in cognitive tasks that included simple and choice reaction times, perception, short-term memory, and free-recall memory (Tomporowski, 2003), a growing body of recent studies has focused on complex cognitive tasks that involve executive function (Etnier & Chang, 2009). Executive function refers to higher and metalevels of cognitive processes that regulate and organize purposeful and goal-directed behaviors (Lezak, Howieson, Loring, Hannay, & Fischer, 2004). Executive functions enable individuals to address novel events, override habitual or automatic actions, and respond properly to the environment or external context (Banich, 2009; Zelazo, Craik, & Booth, 2004). Hillman, Snook, and Jerome (2003) have reported that acute exercise leads to greater performance benefits for the incongruent condition of the flanker task compared with the congruent condition. Given that the performance of the incongruent condition of the task requires a greater amount of executive control compared with the congruent condition, this result suggests that acute exercise has a preferential benefit for executive function. Notably, executive function is a multi-faceted process that involves distinguishable sub-functions, including inhibition, working memory, scheduling, and planning (Kramer et al., 1999). A prominent framework based on the factor analysis technique and proposed by Miyake et al. (2000) argues that executive function consists of three foundational domains: inhibition, updating of working memory, and shifting. This framework has been confirmed €rvi, Kooistra, & Pulkkinen, 2003). Etnier and in children (Lehto, Juuja Chang (2009) argued that acute exercise likely has a selective

influence on specific types of executive function and that further research is needed to clarify this issue. Since then, several studies have examined specific aspects of executive function following acute exercise, including inhibition (Chang, Tsai, Huang, et al., 2014), planning (Chang, Ku, et al., 2012; Chang, Tsai, Hung, et al., 2011), shifting (Chang, Liu, Yu, & Lee, 2012), and working memory (Pontifex, Hillman, Fernhall, Thompson, & Valentini, 2009). These studies have generally demonstrated that acute exercise has supportive effects in adult populations. The positive effect of acute exercise on executive function could be extended to children. For example, 20-min bouts of aerobic exercise that induced heart rates that were 60% of the maximum resulted in greater performance enhancements in the incongruent condition compared with the congruent condition of the flanker task in healthy preadolescents (Hillman et al., 2009). A similar positive acute exercise effect using exergaming has also been observed on the performance of the flanker task in children with a wide age range (i.e., 6e9 years) (Best, 2012). Recently, a metaanalysis conducted by Verburgh et al. (2014) indicated a larger overall effect of acute exercise on executive function in children (effect size ¼ 0.52) compared with other meta-analyses that targeted younger adults or populations of all ages (effect sizes ranging from 0.10 to 0.20) (Chang, Labban, et al., 2012; Lambourne & Tomporowski, 2010). These studies suggest that children can receive benefits in executive function from acute exercise. However, few studies have examined the relationship between acute exercise and specific aspects of executive function in children, and those studies have produced ambiguous findings. For example, while some studies have shown that acute exercise enhances inhibition (Best, 2012; Hillman et al., 2009) and shifting (Chang, Liu, et al., 2012), two other studies failed to find effects of acute exercise on inhibition (Stroth et al., 2009) or switching (Tomporowski, Davis, Lambourne, Gregoski, & Tkacz, 2008). Additionally, no studies have investigated the effects of acute exercise on the theorized multiple aspects of executive function in children. While these specific components of executive function do not fully mature until after adolescence, cognitive abilities begin to develop in early childhood and are significantly enhanced in the school years (Romine & Reynolds, 2005). Small changes in executive function during these periods lead to large alterations in behavior, emotional regulation, and social interactions later in life (Anderson, 2002; Best, Miller, & Jones, 2009). Therefore, the second objective of the present study was to empirically and simultaneously examine the three core components of executive function proposed by Miyake et al. (2000) in preadolescent children. The overarching purpose of the present work was to determine the effects of acute exercise on cognition in preadolescent children. Specifically, we attempted to clarify whether acute bouts of exercise influence the proposed core domains of executive function (i.e., inhibition, working memory, and shifting) in children in early and mid-preadolescence. We predicted that our study would both replicate previous research demonstrating that acute aerobic exercise facilitates specific aspects of executive function and extend our current understanding of this process to cover a variety of cognitive aspects and differential enhancements between two preadolescent age groups. Methods Participants Ninety-eight preadolescents in four classes were selected from third- (n ¼ 40) and fifth-grade (n ¼ 58) classes in an elementary school in the Miyun district, Beijing. All participants were instructed by the experimenter to complete several questionnaires to

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ensure that they met the inclusion criteria. The Physical Activity Readiness Questionnaire (PAR-Q), the Wechsler Intelligence Scale for Children-IV-Chinese Version (WISC-IV-C) (Zhang, 2009), the Attention Deficit/Hyperactivity Disorder Rating Scale-IV-Parent Version (ADHDRS-IV-P) (DuPaul, Power, Anastopoulos, & Reid, 1998) (the information was provided by the children's guardians), and the Symptom Checklist-90-Chinese Version (SCL-90-C) (Jin, & Zhang, 1986) were used to ensure that exercise could be performed safely (PAR-Q ¼ 6), that participants were of normal intelligence (WISC-IV-C > 90), that no participants had attention deficit/hyperactivity disorder (defined as scores of 2 or 3 on six of the nine inattention items and/or scores of 2 or 3 on six of the nine hyperactivity/impulsivity items), and that no participants had an otherwise altered mental status (SCL-90-C > 160). For eligibility, participants were also required to be right handed, to have normal or corrected-to-normal vision, to not be color-blind, and to not be taking psychoactive medications. After the screening processes, 34 third-grade children (boys: n ¼ 18; girls: n ¼ 16) and 53 fifth-grade children (boys: n ¼ 27; girls: n ¼ 26) were included in the study. All participants and their guardians provided written consent, and the protocol was approved by the institutional review board of Beijing Normal University. The participants were then randomly assigned into either a control or an exercise group after employing stratification methods regarding grade and gender by lottery. The

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samples sizes for the exercise group in the third and fifth grades were 17 and 27, respectively, and the sample sizes for the control group in the third and fifth grades were 17 and 26, respectively. Four participants in the fifth-grade control group were absent on the test day, leaving 22 children in this group (Fig. 1). Executive function and related assessments Three computer-based neuropsychological assessments were used to assess the inhibition, working memory, and shifting aspects of executive function. The stimulus presentation and response data collection were performed with E-prime software 1.1 (Psychology Software Tools Inc., Pittsburgh, USA). Inhibition A modified Eriksen flanker task was employed to examine the inhibitory control aspect of executive function (Eriksen & Eriksen, 1974). This task has been found to be sensitive to acute exercise (Hillman et al., 2003, 2009). The flanker task involved two types of trials, congruent and incongruent. The congruent trials consisted of a horizontally arranged array of the same five letters (e.g., LLLLL or FFFFF); the incongruent trials consisted of a horizontally arranged array of five letters in which the middle letter was different

Fig. 1. Flow diagram of participant selection and assignment.

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(e.g., LLFLL or FFLFF). During the flanker task, the participant was asked to press the “F” or “L” with their left or right index finger, respectively, based on the middle letter presented in the trial. A fixation cross (þ) was first presented for 500 ms at the center of the screen to attract the participant's attention. Then, either a congruent or an incongruent letter set was displayed for 1000 ms. The stimulus-onset asynchrony was set at 2000 ms. All stimuli were presented on a black background. The participants were instructed to react to each trial as quickly and accurately as possible. Pressing the wrong button and failing to respond within 150 mse1000 ms were each considered incorrect responses. Participants were asked to perform 12 practice trials and then complete two blocks of 48 trials each, with a 1-min rest interval between the blocks. The congruent and incongruent trials were presented in a random order with equal probability in each block. The total task duration was approximately 6 min. The response times in the congruent and incongruent trials were recorded and used to create an index of inhibition, defined as the response time difference between incongruent and congruent trials. Shorter response time differences reflected better performance. Working memory A modified visual “N-back” (2-back) task that has been used extensively to assess the updating of the working memory aspect of executive function was employed. The 2-back task consists of a series of quickly changing letters displayed on the center of the computer screen (i.e., B, D, L, Y, O). All letters were presented on a black background for 2000 ms each, and the stimulus-onset asynchrony was set at 3000 ms. For the 2-back task, the participants were instructed to monitor each letter and to identify whether the letter was identical to the one that appeared two trials ago. When the current letter matched the letter presented two trials previously, the participants pressed the “F” key with their left index finger to indicate “yes”; they were asked to press the “L” key with their right index finger to indicate a “no” response. “Yes” and “no” trials each accounted for 50% of the trials. Pressing the wrong button and failing to respond within 300 mse1500 ms were each considered incorrect responses. Participants performed 12 practice trials and then completed two blocks of 25 trials each, with a 1-min rest interval between the blocks. The total duration of the task was approximately 7 min. The response times on correct trials were recorded and averaged as the main behavioral index, wherein shorter response times reflected better performance. Shifting A more-odd task adapted from Hillman, Kramer, Belopolsky, and Smith (2006); Salthouse, Fristoe, McGuthry, and Hambrick (1998) was employed to investigate the shifting aspect of executive function. The more-odd task consists of a series of numeric digits from either 1 to 4 or 6 to 9 displayed in the center of the screen. All digits were displayed for 2000 ms, and the stimulus-onset asynchrony was set at 3000 ms. The task consisted of three types of blocks. The A block involved 16 homogeneous trials in which the digits were printed in black. The participants were instructed to press the “F” or the “L” key with their left or right index finger to indicate whether the presented digit was greater than or less than 5, respectively. The B block involved 16 homogeneous trials in which the digits were printed in green. The participants were instructed to press the “F” or “L” key with their left or right index finger to indicate whether the presented digit was odd or even, respectively. The C block consisted of 32 heterogeneous trials that included both A- and

B-type trials (16 trials each) that switched from one to the other every two trials. The participants were required to press the “F” or “L” key to identify whether the digit was greater or less than 5 when the digit was presented in black and whether the digit was odd or even when the digit was presented in green. Pressing the wrong button and failing to respond within 150 mse1000 ms for homogeneous trials or within 300 mse1500 ms for heterogeneous trials were each considered incorrect responses. For practice, the participants performed eight A- and B-type trials (16 trials in total). Participants then completed six blocks (in the following order: ABCCBA) with 1-min rest intervals between the blocks. The total duration of the task was approximately 12 min. The shifting index used in the present study was the global switch cost, which was calculated as the response time difference between the heterogeneous (i.e., the average of the C blocks) and homogeneous (i.e., the average of the A and B blocks) blocks. Experimental procedure Children in four classes (2 third-grade classes and 2 fifth-grade classes) were instructed to come to a specific classroom on two separate days. The first day was used to screen participants based on the inclusion criteria. All potential participants in the four classes were briefly introduced to the study and then asked to provide demographic information and complete the following four questionnaires: PAR-Q, WISC-IV-C, ADHDRS-IV-P, and SCL-90-C. Eligible participants in each grade were then randomly assigned to either the exercise or control group based on gender. Participants were then given the informed consent form and asked to return it on the second testing day. The four groups were led by the same instructor on separate days. For the third-grade exercise group, the participants' heart rates were measured before beginning the exercise (pre-HR). The participants then entered a group-specific computer room (each participant had his/her own space of approximately 1.5 m squared) and were instructed to complete the modified Eriksen flanker task, the 2-back task, and the more-odd task, in that order, as a pre-test. Participants received instructions prior to each task and fully understood the tasks. The participants in the exercise group then jogged in the groups at a moderate intensity for 30 min on a playing field. Exercise intensity was monitored by portable heart rate monitors that were attached to six participants (three boys and three girls) throughout the experiment. Each of these six participants was asked to lead his/her own sub-group (n ¼ 3e5) and to adjust running speed based on their heart rates. The exercise intensity was set at moderate intensity (60e70% of the predicted maximal heart rate), which has been shown to benefit cognition (Hillman et al., 2009). After the exercise protocol, all participants were taken back to the same computer room and allowed to rest until their HRs returned to within 10% of their preexercise levels (heart rate data were measured based upon the six participants, and the duration of recovery was approximately 20e25 min). All participants were then asked to perform the same cognitive tasks as a post-test. The same experimental process was applied to the fifth-grade group. While all participants were subjected to similar experimental protocols in terms of the cognitive tasks, the participants in the third- and fifthgrade control groups were instructed to read exercise-related books provided by the instructor for 30 min while sitting quietly in the classroom. Additional heart rate recordings were taken at 10, 20, and 30 min during the exercise and reading treatments and prior to conducting the cognitive post-test. The entire experimental process of the second day required approximately 2.5 h to complete.

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maximal heart rate suggest that the consideration of the exercise manipulation of moderate exercise intensity was appropriate.

Statistical analysis The present study had a true experimental and mixed design with group and grade as between-subject factors and time point as a within-subject factor. Independent t-tests and the chi-square test were first conducted where appropriate to examine the significance of differences between means of demographic variables for the two treatment groups in each grade. Descriptive data were also evaluated to determine the appropriateness of the exercise intensity manipulation. Regarding the performance of the executive function tasks, 2 (treatment: exercise versus control)  2 (grade: third versus fifth)  2 (time point: pre-test versus post-test) ANOVAs were conducted separately for the inhibition, working memory, and shifting indices (i.e., duration index). Post-hoc analyses were conducted with planned pairwise comparisons when significant main and interaction effects were revealed. Additional independent t-tests were separately conducted to examine differences in accuracy between the means of the exercise and control groups for the inhibition, working memory, and shifting indices. Bonferroni adjustments were applied to control for the inflation of type I error. Effect sizes are presented as partial etasquared (h2) values. The alpha level for statistical significance was set at 0.05 prior to Bonferroni adjustment. Results Participant characteristics The participants' demographic details are presented in Table 1. Independent t-tests revealed no significant differences between the control and exercise groups among the third-grade children in terms of gender (chi-square ¼ 0.12, p ¼ 0.73), age, education, height, weight, or BMI (ts' (32) ¼ 0.82 to 0.88, p ¼ 0.42 to 0.64), suggesting that the two groups had similar demographic backgrounds. Similarly, no differences between the two treatment groups regarding gender (chi-square ¼ 0.18, p ¼ 0.67), age, education, height, weight, and BMI (ts' (51) ¼ 0.1.81 to 0.37, p ¼ 0.25 to 0.89) were found for the fifth-grade children.

Executive function assessment The summary statistics for the executive function performances are presented in Table 2. Inhibition A three-way mixed ANOVA revealed main effects for grade (F(1, 79) ¼ 17.36, p < 0.001, partial h2 ¼ 0.18) and group (F(1, 79) ¼ 16.45, p < .001, partial h2 ¼ 0.17). Pairwise comparisons revealed that the inhibition response time differences were shorter for the fifthgrade group than for the third-grade group. Shorter response time differences were also found in the exercise group compared with the control group (Fig. 2a). The interaction of time point and group was also significant (F (1, 79) ¼ 12.98, p < 0.001, partial h2 ¼ 0.14). A follow-up analysis deconstructing the interaction revealed no pre-test differences between the exercise and control groups, but the post-test inhibition response time differences were shorter than the pre-test inhibition response time differences in the exercise group. This difference was not present in the control group (Fig. 3a). The main effects for time (p ¼ 0.09, partial h2 ¼ 0.04), the interaction of time point and grade (p ¼ 0.67, partial h2 ¼ 0.002), the interaction between grade and group (p ¼ 0.55, partial h2 ¼ 0.001), and the three-way interaction (p ¼ .24, partial h2 ¼ 0.02) failed to reach significance. Regarding accuracy, no differences were observed between the exercise and control groups for the congruent block (pre-test, p ¼ 0.58; post-test, p ¼ 0.44) or incongruent block (pre-test, p ¼ 0.68; post-test, p ¼ 0.85) in the third-grade group. Similarly, no differences were observed for the congruent block (pre-test, p ¼ 0.94; post-test, p ¼ 0.35) or incongruent block (pre-test, p ¼ 0.97; post-test, p ¼ 0.90) in the fifth-grade group.

Exercise intensity manipulation

Working memory

The heart rates for the third-grade control and exercise groups were 41.57% and 64.29% of the maximal heart rate, respectively (t (10) ¼ 18.48, p < .001). The heart rates for the fifth-grade control and exercise groups were 42.78% and 64.40% of the maximal heart rate, respectively (t (10) ¼ 29.11, p < 0.001). The different heart rates between the two treatment groups as well as the percentages of the

A three-way mixed ANOVA revealed the main effects for grade (F(1, 79) ¼ 39.76, p < 0.001, partial h2 ¼ 0.34) and group (F(1, 79) ¼ 28.97, p < 0.001, partial h2 ¼ 0.27). Pairwise comparisons revealed that the working memory response times were shorter for the fifth-grade group than for the third-grade group. Shorter working memory response times

Table 1 Participant demographics and treatment-induced heart rates (mean ± standard deviation). Variables

n Female/Male Age (yrs) Height (cm) Weight (kg) BMI (kg/m2) Heart rate (HR) na Female/Male HR at pre-test HR during treatment HR at post-test

Third grade

Fifth grade

Control group

Exercise group

Control group

Exercise group

17 8/9 9.12 ± 0.33 136.43 ± 4.53 32.31 ± 3.76 17.34 ± 1.63

17 8/9 9.24 ± 0.44 137.21 ± 5.05 31.89 ± 3.55 16.91 ± 1.39

27 13/14 11.14 ± 0.35 151.46 ± 7.93 42.50 ± 6.22 18.41 ± 1.23

22 13/9 11.07 ± 0.27 150.33 ± 7.49 42.74 ± 5.86 18.82 ± 1.18

6 3/3 79.17 ± 6.88 87.67 ± 4.80 82.00 ± 5.66

6 3/3 81.67 ± 6.15 135.50 ± 4.15 85.83 ± 6.24

6 3/3 75.67 ± 5.12 89.39 ± 2.14 82.00 ± 3.69

6 3/3 76.00 ± 5.87 134.56 ± 3.14 80.33 ± 4.72

Note. BMI ¼ Body mass index; HR at pre-test ¼ averaged heart rate assessed before cognitive task at pre-test and treatment; HR during treatment ¼ averaged heart rate of three points assessed during treatment at 10 min, 20 min and 30 min; HR at post-test ¼ averaged heart rate assessed following treatment and before the cognitive task at posttest. a Heart rate value was presented by six participants in each group.

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Table 2 Performance results for three fundamental aspects of executive function, segregated by grade, treatment, and time point (mean ± standard deviation). Third grade

Fifth grade

Control group Pre-test

Exercise group Post-test

Pre-test

Control group Post-test

Duration (ms)

Pre-test

Exercise group Post-test

Pre-test

Post-test

Duration (ms)

Inhibition Congruent 591.37 ± 55.95 561.99 ± 62.59 604.80 ± 63.39 577.38 ± 52.34 Incongruent 624.12 ± 48.99 601.39 ± 68.53 630.07 ± 66.54 590.99 ± 52.28 Inhibitory control 32.75 ± 15.19 39.40 ± 14.10 25.27 ± 11.01 13.61 ± 17.35 Working Memory 2-back 1081.76 ± 117.36 1125.45 ± 113.19 1054.50 ± 145.82 935.79 ± 75.38 Shifting Homogeneous 665.32 ± 106.18 704.84 ± 98.54 691.82 ± 132.66 697.39 ± 114.31 Heterogeneous 1030.67 ± 85.28 1099.45 ± 128.91 1069.49 ± 112.50 986.00 ± 131.67 G switch cost 365.34 ± 66.40 394.61 ± 78.97 377.66 ± 48.30 288.61 ± 70.05 Accuracy (%) Inhibition Congruent 92.57 ± 0.07 95.06 ± 0.05 93.62 ± 0.04 96.34 ± 0.05 Incongruent 92.70 ± 0.07 93.32 ± 0.06 93.48 ± 0.04 93.66 ± 0.04 Working Memory 2-back 76.12 ± 0.07 76.35 ± 0.07 77.53 ± 0.09 77.76 ± 0.09 Shifting Homogeneous 92.46 ± 0.04 92.61 ± 0.04 93.81 ± 0.04 93.86 ± 0.04 Heterogeneous 89.08 ± 0.01 89.11 ± 0.01 88.43 ± 0.04 89.11 ± 0.02

524.64 ± 52.96 543.44 ± 51.51 18.80 ± 21.87

508.69 ± 39.70 527.99 ± 51.28 19.30 ± 22.32

524.60 ± 90.34 535.73 ± 92.66 11.14 ± 19.03

507.07 ± 55.49 509.45 ± 52.13 2.38 ± 17.71

977.66 ± 91.35

979.71 ± 94.86

930.05 ± 89.75

860.60 ± 93.46

544.78 ± 137.53 677.73 ± 90.38 577.94 ± 126.80 664.25 ± 91.96 901.22 ± 123.43 1045.30 ± 101.51 901.75 ± 124.29 947.83 ± 103.44 356.44 ± 77.54 367.57 ± 79.58 323.81 ± 70.09 283.58 ± 85.42 Accuracy (%) 94.50 ± 0.05 94.19 ± 0.04

94.59 ± 0.05 94.05 ± 0.04

94.24 ± 0.06 94.14 ± 0.06

93.45 ± 0.04 94.14 ± 0.06

78.00 ± 0.07

77.91 ± 0.06

77.33 ± 0.09

77.52 ± 0.09

94.16 ± 0.04 89.30 ± 0.02

93.78 ± 0.04 89.57 ± 0.02

94.14 ± 0.05 89.49 ± 0.02

93.95 ± 0.04 89.30 ± 0.03

Note. Inhibitory control ¼ response time difference between incongruent and congruent condition; G switch cost ¼ global switch cost represent the response time difference between non-shift and shift condition.

were also found in the exercise group compared with the control group (Fig. 2b). There was a significant interaction between time point and group (F(1, 79) ¼ 16.50, p < 0.001, partial h2 ¼ 0.17). A follow-up analysis deconstructing this interaction revealed no differences in pre-test scores between the exercise and control groups. However, the post-test working memory response times were shorter than the pre-test working memory response times in the exercise group, but not in the control group (Fig. 3b). The main effects for time (p ¼ 0.02, partial h2 ¼ 0.07), the interaction between time point and grade (p ¼ 0.90, partial h2 ¼ 0.000), the interaction between grade and group (p ¼ .48, partial h2 ¼ 0.01), and the three-way interaction (p ¼ .12, partial h2 ¼ 0.03) failed to reach significance. Regarding accuracy, no differences were observed between the exercise and control groups for working memory (pre-test, p ¼ 0.62; post-test, p ¼ .60) in the third-grade group. Similarly, no differences were observed for working memory (pre-test, p ¼ 0.83; post-test, p ¼ 0.90) in the fifth-grade group. Shifting A three-way mixed ANOVA revealed a main effect for group (F(1, 79) ¼ 17.03, p < 0.001, partial h2 ¼ 0.17). Pairwise comparisons revealed shorter response time differences in the exercise group compared with the control group (Fig. 3c). Similar to the indices for inhibition and working memory, there was an interaction between time point and group (F(1, 79) ¼ 16.21, p < 0.001, partial h2 ¼ 0.17). There were no differences in pre-test scores across groups. However, the exercise group had shorter shifting response times post-test relative to pre-test. This pre- versus post-test difference was not observed in the control group (Fig. 3c). The main effects for grade and time point (ps' ¼ 0.04 to. 07, partial h2 ¼ 0.04 to 0.05), the interaction between grade and group (p ¼ .65, partial h2 ¼ 0.003), and the three-way interaction (p ¼ 0.12) failed to reach significance. Regarding accuracy, no differences were observed between the exercise and control groups for the homogeneous block (pre-test,

p ¼ 0.36; post-test, p ¼ 0.37) or heterogeneous block (pre-test, p ¼ 0.49; post-test, p ¼ 1.00) in the third-grade group. Similarly, no differences were observed for the homogeneous block (pre-test, p ¼ 0.82; post-test, p ¼ 0.91) or heterogeneous block (pre-test, p ¼ 0.80; post-test, p ¼ 0.50) in the fifth-grade group. Discussion Given that few studies of acute exercise and cognition have included children, the aim of the current study was to determine the effects of an acute bout of group-based aerobic exercise on three core aspects of executive function and whether this relationship would be moderated by the stage of preadolescence. Our results support the hypotheses that acute exercise facilitates multiple aspects of executive function when group assignments and exercise manipulations are appropriate and that this facilitation is independent of the stage of preadolescence. Specifically, improved executive functions were found in both grades in the exercise group. Additionally, we found main effects of age for the inhibition and working memory aspects of executive function, with the fifthgrade group performing better, but no effect was observed for shifting, suggesting different developmental trends between the ages examined. Our findings regarding the general benefits of exercise on the performance of three specific aspects of executive function corroborate previous studies targeting inhibition and shifting (Chang, Liu, et al., 2012; Hillman et al., 2009) and add to the knowledge of the effect of acute exercise on working memory in children. Interestingly, while the three tasks were administered in order, improvement between post- and pre-test was only observed in the exercise group, not the control group, regardless of grouping by grade, suggesting that the effect of acute exercise predominately affected executive function, even if order and fatigue effects were present. These findings are in contrast to those of studies suggesting that acute exercise has no effect on inhibition in 13- to 15year-old children (Stroth et al., 2009) or shifting in overweight children (Tomporowski et al., 2008). Because the age and body mass of the subjects varied across these studies, it is possible that the effects of acute exercise on various executive functions are

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Fig. 2. Performance for specific aspects of executive function as functions of grade (third versus fifth) and treatment group (exercise versus control group): a) inhibition, b) working memory, and c) shifting. *significant difference (p < .05). The data are presented as the mean and the SEM.

particularly sensitive in healthy children within the early to midpreadolescent period. Considered together with studies examining sub-components of executive function only in the early (Hillman et al., 2009) or middle to late preadolescent periods (Pesce et al., 2009; Stroth et al., 2009), the present study completes the early to middle developmental picture, as recommended by Best et al. (2009), regarding acute exercise and multiple facets of executive function in healthy preadolescent children. Acute exercise-induced attention has been proposed to be a potential mechanism underlying these effects. Previous studies have indicated that acute exercise elicits greater P3 amplitude or shorter P3 latency neuroelectric measures during inhibitionrelated tasks in young adults (Hillman et al., 2003; Kamijo et al., 2009). Given that P3 amplitudes and latencies are associated with attentional allocation and the efficiency of stimulus classification, respectively, in a given task (Polich, 2007), these neuroelectric indices suggest that acute exercise provides increased cognitive capacity to allocate attentional resources and hastens information processing compared with resting conditions during stimulation engagement. Partially in line with the results for younger adults, superior P3 amplitudes have also been observed during trials that require inhibition in preadolescent children, suggesting that the

attention-related mechanism could extend from young adults to children (Drollette et al., 2014; Hillman et al., 2009). While the potential attention-related mechanisms proposed by the abovementioned studies were specifically emphasized regarding inhibition, other potential mechanisms, such as exerciseinduced brain states and regional cerebral blood flow, could also presumably explain the changes in separate aspects of executive function. An electroencephalography study indicated that acute exercise may facilitate performance in multiple tasks by inducing a better-prepared brain state. Schneider, Vogt, Frysch, Guardiera, and Strüder (2009) reported increased alpha activity and decreased beta relative to baseline conditions following 15 min of aerobic exercise in children. While this study did not assess cognitive performance, these altered neuroelectric activities reflect the overall physical relaxation that may increase concentration and alter available processing capacity, which may enhance cognitive performance (Schneider et al., 2009). A variety of demands that engage executive functions have been linked to the prefrontal cortex. For example, young adults and children exhibit similar activation locations in the prefrontal cortex during inhibitory tasks, although children exhibit greater volumes of activation, which implies that inhibition is related to the

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Fig. 3. Performance in specific aspects of executive function as functions of treatment group (exercise versus control group) and time point (pre- versus post-test condition): a) inhibition, b) working memory, and c) shifting. *significant difference between pre-test and post-test (p < .05). # significant difference between control and exercise groups (p < .05). The data are presented as the mean and SEM.

prefrontal brain region and that children are less efficient at performing the task (Casey et al., 1997). Recently, D’Ardenne et al. (2012) investigated the relationship between working memory and the prefrontal cortex in two stages. These researchers first identified the working memory-related areas of the prefrontal cortex using functional MRI and then applied single-pulse transcranial magnetic stimulation (TMS) to the right dorsolateral prefrontal cortex during a working memory task. Decreases in working memory were observed after TMS, suggesting a somewhat strong relationship between the prefrontal cortex and working memory. Similar to inhibition and working memory, shifting is also associated with the prefrontal cortex, particularly the inferior prefrontal cortex, where adult-like activation during shifting tasks has been found in preschool-age children (Moriguchi & Hiraki, 2009). Notably, acute exercise elevates the activation of the prefrontal cortex and may thereby influence executive function. Indeed, acute exercise-induced increases in cerebral blood flow have been found to improve both the activity of the left dorsolateral prefrontal cortex and performance on inhibitory tasks; these findings have led to the claim that the changes in the prefrontal cortex induced by acute exercise are the neural basis of the improvement in inhibitory performance (Endo et al., 2013; Yanagisawa et al., 2010). No studies have examined alterations of prefrontal cortical activation in response to acute exercise during working memory and shifting

tasks. However, because these core aspects of executive function involve similar cortical regions and acute exercise enhances brain activity during inhibitory tasks, it has been postulated that acute exercise facilitates multiple executive functions by elevating the activation of the prefrontal cortex. Further research should explore this proposition. Regardless of the effects of acute exercise, there were differences in the sub-components of executive function between the early and mid-preadolescent periods. The fifth-grade group exhibited better performance on the inhibition and working memory tasks but not on the shifting task. These findings suggest that the developmental time courses of the three fundamental aspects of executive function may be different. Our findings corroborate those of Best et al. (2009), who indicated that different executive functions develop following distinct time courses. During childhood, inhibition develops first and is followed by working memory and shifting (Brocki & Bohlin, 2004). While previous studies in line with our own results have observed that inhibition and working memory develop rapidly between 7 and 11 years of age (Brocki & Bohlin, 2004; Huizinga, Dolan, & van der Molen, 2006), developmental research examining shifting has produced discrepant findings: improvements, reductions, and an absence of differences have all been reported in children aged 6e13 years (Davidson, Amso, Anderson, & Diamond, 2006). These

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divergent results may be attributable to the shifting tasks that were utilized (e.g., the dot task and the Wisconsin card sorting test), the shifting indices that were calculated (e.g., global or local switch costs), the ages chosen for study (e.g., 6 to 13 and 7e21 years old), and the strategies used by participants (e.g., the speedaccuracy tradeoff is used differentially by participants of different ages) (Davidson et al., 2006; Garon, Bryson, & Smith, 2008; Huizinga et al., 2006). While replication studies are needed, the current study, along with previous works, suggests that the maturation rate of shifting is different from the linearly improving rates of inhibition and working memory between the early and mid-preadolescent periods. One significant aspect of the present study is that the exercise protocol we utilized has high ecological validity. Rather than utilizing treadmills or cycle ergometers in the laboratory, as has been performed in the majority of studies (Lambourne & Tomporowski, 2010), the present study utilized group exercise in a field, which gave the children greater opportunities to experience social interactions and cognitive demands (e.g., adjust their speed or distance relative to that of other individuals within the group). It is possible that exercise involving greater social interaction or cognitive demands produces an additional beneficial effect on cognition. Pesce et al. (2009) utilized exercise protocols that involved similar exercise intensities and observed that exercise had greater effects on immediate recall in children who participated in an acute bout of a group game compared with children who participated in circuit training. Similar results have been found for selective attention in children who participated in an exercise group compared with those who participated in circuit training (Budde, Voelcker-Rehage, Pietrabyk-Kendziorra, Ribeiro, & Tidow, 2008). Recently, Pesce (2012) argued that researchers interested in the exerciseecognition interaction should shift their attention away from the quantitative aspects of exercise (e.g., intensity, duration) and toward the qualitative aspects of exercise (e.g., exercises with different movement task complexities and cognitive demands) because exercise that requires highly coordinated, strategic, and socially interactive behaviors may reciprocally regulate executive function, which in turn may lead to stronger effects on executive function, particularly in children with enhanced brain plasticity capacities. Several unavoidable limitations to the interpretation of these results may guide future research directions. Because the same instructor was utilized and the experimental process was not blinded, it is possible that the instructor consciously or unconsciously provided information (e.g., tone of voice, instructions, or encouragement) differently to participants in each group, which is particularly difficult to control for in group testing. Further study is also suggested to assess the heart rate during exercise as well as to collect data regarding a subjective index (e.g., Rating of Perceived Exertion) for all participants rather than data on only a small set of selected individuals to refine the monitoring of exercise intensity. Furthermore, while the present study applied the most prominent theoretical framework for executive function (Miyake et al., 2000), other frameworks, particularly several focused on children, have also been proposed. For example, the executive function development model proposed by Anderson (2002) involves the dimensions of cognitive flexibility, goal setting, attentional control, and information processing, and planning is recognized as an essential subconstruct. Further investigations should determine whether these facilitatory effects extend to these specific aspects of executive function. While the inclusion of field conditions in our study was a strength, as it increased ecological validity, this approach may have introduced other confounding factors (e.g., following the pace set by someone else in front may be a stressor), and it is therefore recommended that such confounders be considered in future

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research. Future studies should also emphasize the inclusion of children with clinical disorders associated with reduced executive functioning, such as attention deficit hyperactivity disorder (ADHD) and obesity. Indeed, acute bouts of exercise have been shown to enhance inhibition and shifting in children with ADHD (Chang, Liu, et al., 2012), but no facilitatory effect of acute exercise on switching performance has been found in overweight children (Tomporowski et al., 2008). These results suggest that children with different conditions will exhibit different relationships between acute exercise and specific executive functions. Finally, our interpretation may be compromised by the small sample size, and further study is recommended to consider this issue. In summary, to the best of our knowledge, the present study is the first to examine the effects of acute exercise on three primary aspects of executive function in healthy preadolescent children, with special attention paid to age as a moderating factor. Our findings suggest that in both early and mid-preadolescence, acute bouts of ecologically valid group exercise facilitate executive function regardless of the fundamental component of executive function assessed. These findings extend current knowledge and have implications for both public health and educational practices for preadolescents. Future research on this topic should consider the relationship between acute exercise and executive function in children using ecologically valid exercise protocols and should involve longitudinal designs, sub-constructs of executive function identified in other theoretical frameworks, and children with clinical disorders. Acknowledgment This research was supported in part by grants from the National Social Science Fund of China (CLA120162), the National Natural Science Foundation of China (31300863), and the Fok Ying Tung Education Foundation (141113) to Ai-Guo Chen; from the Ministry of Science and Technology in Taiwan to Yu-Kai Chang. (102-2410-H179-014-MY3; NSC 102-2918-I-179-001-). References Anderson, P. (2002). Assessment and development of executive function (EF) during childhood. Child Neuropsychology, 8, 71e82. http://dx.doi.org/10.1076/ chin.8.2.71.8724. Audiffren, M., Tomporowski, P. D., & Zagrodnik, J. (2008). Acute aerobic exercise and information processing: energizing motor processes during a choice reaction time task. Acta Psychologica, 129, 410e419. http://dx.doi.org/10.1016/ j.actpsy.2008.09.006. Audiffren, M., Tomporowski, P. D., & Zagrodnik, J. (2009). Acute aerobic exercise and information processing: modulation of executive control in a Random Number Generation task. Acta Psychologica, 132, 85e95. http://dx.doi.org/10.1016/ j.actpsy.2009.06.008. Banich, M. T. (2009). Executive function: the search for an integrated account. Current Directions in Psychological Science, 18, 89e94. http://dx.doi.org/10.1111/ j.1467-8721.2009.01615.x. Best, J. R. (2012). Exergaming immediately enhances children's executive function. Developmental Psychology, 48, 1501e1510. http://dx.doi.org/10.1037/a0026648. Best, J. R., Miller, P. H., & Jones, L. L. (2009). Executive functions after age 5: changes and correlates. Developmental Review, 29, 180e200. http://dx.doi.org/10.1016/ j.dr.2009.05.002. Brocki, K. C., & Bohlin, G. (2004). Executive functions in children aged 6 to 13: a dimensional and developmental study. Developmental Neuropsychology, 26, 571e593. Budde, H., Voelcker-Rehage, C., Pietrabyk-Kendziorra, S., Ribeiro, P., & Tidow, G. (2008). Acute coordinative exercise improves attentional performance in adolescents. Neuroscience Letters, 441, 219e223. http://dx.doi.org/10.1016/ j.neulet.2008.06.024. Casey, B., Trainor, R. J., Orendi, J. L., Schubert, A. B., Nystrom, L. E., Giedd, J. N., & Cohen, J. D. (1997). A developmental functional MRI study of prefrontal activation during performance of a go-no-go task. Journal of Cognitive Neuroscience, 9, 835e847. http://dx.doi.org/10.1162/jocn.1997.9.6.835. Caterino, M. C., & Polak, E. D. (1999). Effects of two types of activity on the performance of second-, third-, and fourth-grade students on a test of concentration. Perceptual and Motor Skills, 89, 245e248. http://dx.doi.org/10.2466/ pms.1999.89.1.245.

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