22 annotated bibliographies AMA style

Effects of Aerobic Exercise on Cognitive Performance Among Young Adults in a Higher Education Setting Sebastian Ludyga , Markus Gerber , Serge Brand, Uwe Pühse, and Flora Colledge

University of Basel

ABSTRACT Purpose: Acute benefits of aerobic exercise on executive functioning have been reported frequently under laboratory conditions. However, to date, a beneficial effect on long-term memory has been less well supported and no data are available regarding nonlaboratory conditions in young adults. The aim of the current study was to investigate acute effects of aerobic exercise on cognitive functioning in a university classroom setting. Method: Using a cross-over design, 51 participants performed a bout of moderately intense running (RUN) and read an article while seated (CON). Afterwards, they completed free-recall tests, followed by a Flanker task and an n-back task. Results: Participants in the RUN condition compared with those in the CON condition showed shorter reaction time on the inhibition task, F(1, 50) = 5.59, p = .022, η2 = .101, and recalled more words in the immediate- and delayed-recall tests, F(1, 50) = 8.40, p = .006, η2 = .144. Conclusion: The present findings suggest that a moderately intense bout of aerobic exercise benefits verbal short-term and long-term memory as well as inhibitory control among students in a classroom setting.

ARTICLE HISTORY Received 2 June 2017 Accepted 31 January 2018

KEYWORDS Cognition; free recall; inhibitory control; working memory

The brain has a capability for functional and structural changes in response to internal and external demands, thus ensuring adaptability, robustness, and diverse func- tionality (Park & Friston, 2013). A body of human and animal studies has shown that a period of regular exercise promotes this plasticity (Thomas, Dennis, Bandettini, & Johansen-Berg, 2012). While many studies have there- fore focused on chronic effects of exercise, potential tran- sient benefits of acute bouts of exercise for brain function and cognition have also become prominent targets in exer- cise psychology. Based on a meta-analytical examination of experimental studies, Chang, Labban, Gapin, and Etnier (2012) reported a small effect of a single exercise session on overall cognitive performance, which was more pro- nounced for aerobic activities compared with resistance exercise. A closer examination of different cognitive domains revealed that improved performance was found only for executive function tasks both during and after exercise.

Executive functions encompass higher-order cogni- tive processes responsible for organizing and controlling goal-directed behavior (Banich, 2009). Although there is still debate on the organization of executive control, response inhibition, working memory, and task switch- ing are generally considered its core components (Diamond, 2013). Combining effect sizes from

experimental studies, Verburgh, Konigs, Scherder, and Oosterlaan (2014) reported a moderate improvement of inhibitory control in adolescents and young adults, but no change in working memory after a single aerobic exercise session. According to McMorris and Hale (2012), the intensity of exercise has been found to influ- ence these effects in an inverted-U manner, suggesting that moderate aerobic activities lead to greater improve- ments in executive functions than aerobic exercise does at low- or high-intensity levels. Focusing on moderately intense exercise only, a recent meta-analysis showed small improvements in reaction time and accuracy on executive function tasks after aerobic exercise (Ludyga, Gerber, Brand, Holsboer-Trachsler, & Pühse, 2016). Whereas those benefits were not different between inhi- bition, task switching, and working memory, the parti- cipants’ age had an influence on the magnitude of the effects. In this respect, the authors found exercise- induced improvements to be small in young adults and moderate in preadolescent children and older adults. Additionally, physical fitness has been confirmed as a moderator of the interactive relationship between exer- cise and cognition, so highly active and physically fit individuals seem to benefit most from a single aerobic exercise session (Chang et al., 2012). However, Pesce (2009) suggested that the influence of physical fitness is

CONTACT Sebastian Ludyga [email protected] Department of Sport, Exercise and Health, Sport Science Section, University of Basel, Birsstrasse 320 B, Basel, CH-4052, Switzerland.

RESEARCH QUARTERLY FOR EXERCISE AND SPORT 2018, VOL. 89, NO. 2, 164–172 https://doi.org/10.1080/02701367.2018.1438575

© 2018 SHAPE America

less pronounced when cognitive testing is performed after exercise than during exercise.

Whereas meta-analyses have provided compelling evi- dence for improvements in executive function after mod- erate aerobic exercise, it is less clear whether or not those effects can be extended to other cognitive domains, such as verbal short-term and long-term memory. These cognitive functions allow for the acquisition and retention of newly acquired information, and some studies have also con- firmed their sensitivity to aerobic exercise (Chang et al., 2012; Lambourne & Tomporowski, 2010; Roig, Nordbrandt, Geertsen, & Nielsen, 2013). Based on the timing of the exercise bout, aerobic activity can have dis- tinct effects on memory encoding and consolidation. However, the results of a recent meta-analysis indicated that performing aerobic exercise before exposure to infor- mation had the greatest benefits for long-term memory (Roig et al., 2013), probably due to the facilitation of encod- ing processes (Labban & Etnier, 2011). In line with this finding, previous studies have confirmed increased perfor- mance on delayed verbal recall tasks rather than immediate verbal recall tasks, when exposure was preceded by an aerobic exercise session (Coles & Tomporowski, 2008; Pesce, Crova, Cereatti, Casella, & Bellucci, 2009).

Although a strategic scheduling of exercise is promising, the evidence for improvements in verbal short-term and long-term memory is not as strong as it is for executive function (Chang et al., 2012). However, these cognitive domains are highly relevant for educational settings. Executive control influences cognitive, social, and psycho- logical development, and this cognitive domain is also strongly related to academic success (Diamond, 2013). The ability to acquire and retain information has a high impact on the success of factual learning, so explicit mem- ory is essential for building a pool of knowledge (Barry, 2006; Paas & Ayres, 2014). So far, exercise-induced improvements on these cognitive functions have mainly been investigated in the laboratory (Guiney & Machado, 2013), although studies with children and adolescents showed that such benefits for executive control could be replicated in a school setting (Jäger, Schmidt, Conzelmann, & Roebers, 2014; Kubesch et al., 2009; Pirrie & Lodewyk, 2012). In contrast, it remains unclear whether or not aero- bic exercise similarly improves young adults’ higher-order cognitive function in a classroom setting, so the external validity and practical relevance are still questionable (Mitchell, 2012).

Therefore, the present study aimed to compare the effect of antecedent aerobic exercise versus reading an academic text on young adults’ inhibitory control, working memory, and verbal short-term as well as long-term memory in a

classroom setting. Based on the current state of the litera- ture, we expected that participants would show increased performance on working-memory and inhibitory control tasks in particular after a single moderately intense running bout compared to a physically inactive control condition. Additionally, we hypothesized that exercise before encod- ing would benefit verbal short-term and long-term memory.

Methods

Participants

As recommended by Faul, Erdfelder, Buchner, and Lang (2009), sample size was calculated a priori using G*Power 3.1. Based on previous studies investigating acute effects of exercise on cognitive performance in an educational setting (Jäger et al., 2014; Kubesch et al., 2009; Pirrie & Lodewyk, 2012), a moderate effect size was expected. With an alpha level set to .05, the initial power analysis indicated that 17 participants were required to reach 85% statistical power.

On the university campus, male and female students with high physical activity levels and corrected-to-normal or normal vision were recruited to attend two experimental sessions separated by 1 week. High physical activity was fulfilled when participants reported vigorous-intensity activity for at least 3 days (accumulating at least 1,500 meta- bolic equivalent [MET] minutes/week) or 7 or more days of any combination of walking or moderate-intensity or vigorous-intensity activities achieving a minimum of at least 3,000 MET minutes/week on the International Physical Activity Questionnaire (IPAQ; Craig et al., 2003). Participants meeting one or more of the following criteria were excluded from the study: (a) existence of an acute or chronic disease, which is a contraindication for exercise; (b) any injury or disease affecting the functionality of the left or right hand; and (c) not willing or able to sign the written and informed consent.

The recruitment and study implementation were per- formed in two waves (first wave, October 2015, N = 18; second wave, October 2017, N = 33). In total, 21 male and 30 female students (Mage = 21.8 ± 1.3 years; Mheight = 1.72 ± 0.08 m; Mbody mass = 68.6 ± 9.8 kg; Mbody mass index = 23.2 ± 1.8; MIPAQ = 4,456.7 ± 1,652.8 MET minutes/ week) were deemed eligible and received information on the testing procedures as well as information on possible risks and benefits. Informed consent was obtained from all participants. All procedures were in line with the Declaration of Helsinki, and the local ethics committee approved the study protocol as complying with the ethical guidelines for nonclinical trials.

EXERCISE, EXECUTIVE FUNCTION, AND MEMORY 165

Design

Using a cross-over design, participants attended an experimental session in a seminar room after a running exercise (RUN) and after a physically inactive control condition (CON), which involved reading an academic text. The order of the conditions was counterbalanced and randomly assigned across participants with gender included as stratification factor. For optimal supervision, the participants were divided into two groups (for each recruitment and study implementation wave), and the groups completed identical procedures consecutively (see Figure 1). Following exercise or reading, partici- pants were provided with a word list and completed the immediate-recall test in a large seminar room. Afterwards, they listened to a 20-min lecture on exercise addiction. Previously, participants were told that they would be asked to remember key words mentioned in the lecture. Following the recall of those key words, they completed the delayed-recall task. Additionally, all par- ticipants performed a n-back task and a Flanker task while sitting in front of a computer. The order of those tests was counterbalanced across participants to elimi- nate order effects.

Conditions

All participants were provided with a heart rate monitor (Polar, RS 400, Espoo, Finland). Prior to the running exercise, heart rate targets corresponding to moderate intensity were calculated individually for each participant. Moderately intense exercise was defined as 70% of the maximum heart rate (Norton, Norton, & Sadgrove, 2010), which was calculated using the equation 208 − 0.7 × Age (Tanaka, Monahan, & Seals, 2001). Running exercise was performed on a predefined route in the city and in small groups up to 10 people. Environmental temperature was 13.7 ± 0.8°C during the experimental sessions. The exer- cise protocol included a 3-min warm-up, 15 min of mod- erate running, and a 2-min cool-down period. During exercise, participants were required to individually adjust their running velocity to match the predefined target heart rate.

In the physically inactive control condition, partici- pants were provided with an academic text, which was related to the lecture. In a group setting, they were asked to read the text and then identify and write down the key statements within 20 min. During the reading task, par- ticipants remained seated in an upright position. This task was chosen for better comparability with previous studies as many researchers have compared the acute effects of exercise on cognition to the effects of reading (Ludyga et al., 2016).

Cognitive testing

Following running exercise or reading the academic text, participants performed computer-based cognitive tests in a seminar room. As two groups were completing the experimental session consecutively, assessments were performed with up to 10 participants at a time. All tasks were administered with E-Prime 2.0 (Psychology Software Tools, Pittsburgh, PA), and participants were therefore seated in front of a laptop. Brightness of the display and viewing distance were standardized. Prior to testing, the investigator provided instructions. Additionally, relevant information was also presented on the screen to make sure that participants understood the tasks. After the instruction, participants were told to keep silent to reduce noise to a minimum.

Inhibitory control

To assess inhibitory control as a marker of executive function, a modified Flanker task was applied (Eriksen & Eriksen, 1974). The task required participants to respond to the direction of a centrally presented target stimulus. In congruent trials, five arrows were facing the same direction, whereas in incongruent trials, the centrally presented target stimulus was facing in the opposite direction of the flanking arrows. During the task, participants were required to respond by pressing a button corresponding to the direction of the target stimulus. In the first block of the computer-based test, participants completed 20 practice trials. Following the practice round, three test blocks with 40 trials were

Flanker task

nBack task

Immediate Recall

Delayed Recall

20-min lecture

Presentation of word list

20-min running (70% HRmax)

20-min reading task

OR

Study procedures Assessment of cognitive outcomes

Figure 1. Overview of experimental procedures. Note. HRmax = maximal heart rate.

166 S. LUDYGA ET AL.

administered. The blocks were interspersed by a 10-s resting period, and the order of the trials was rando- mized. The congruency (congruent, incongruent) and the directionality (left, right) of the stimuli were equi- probable. The stimuli subtended a 1.8° visual angle in height, and they were presented focally for 250 ms on a white background with a response window of 1,000 ms. The interstimulus interval varied randomly from 900 ms to 1,400 ms. Task performance was assessed by calculating the mean reaction time for correct responses as well as mean accuracy separately for con- gruent and incongruent trials. The Flanker task has been found to have adequate to good convergent and discriminant validity (Zelazo et al., 2014), and it is suitable for repeated measures, as Wöstmann et al. (2013) confirmed accurate 4-week test–retest reliability of performance on a Flanker task consisting of 120 trials (congruent stimuli, intraclass correlation coeffi- cient [ICC] = .89; incongruent stimuli, ICC = .94).

Working memory

Working-memory performance was assessed using the n-back task, which requires storage, manipulation, and updating of information (Jonides et al., 1997). In the present study, participants completed a computer-based version of the n-back task, which was already used by Ruiz-Contreras et al. (2013). The task involved the pre- sentation of a sequence of letters, and participants had to detect whether or not the current letter matched the letter presented 1 or 2 trials earlier in the series. For each trial, they were asked to respond by pressing a button corre- sponding to yes or no. The participants completed the task on two difficulty levels (one-back and two-back). For each difficulty, there was one practice block with 20 trials, followed by two blocks with 60 trials each. A short break of 10 s was provided between blocks. The stimuli were dark gray letters (vertical visual angle = 0.7°) presented on a light gray background. Each letter in the sequence was displayed for 500 ms, and a response window of 1,500 ms was provided. The interstimulus interval was set at 1,000 ms. In each block, targets (letter matching the letter presented n trials earlier) occurred with a probability of 20%. Task performance was assessed by averaging the mean reaction time for correct responses separately in the one-back and two-back trials. Additionally, the adjusted hit rate was calculated by dividing the hit rate (Number of Correct Responses for Targets / Total Number of Targets) by the error rate (Number of Errors for Nontargets / Total Number of Nontargets; Ruiz- Contreras et al., 2013). Thus, the adjusted hit rate could take on values from −1 to 1, with 1 denoting that the participant performed correctly in all trials and −1

meaning that the participant performed incorrectly on all the trials. Hockey and Geffen (2004) previously showed that the n-back task is a reliable measure of work- ing memory as performance across the difficulty levels did not change from baseline to retest after 1 week (one-back, r = .79; two-back, r = .72). Due to its moderate correlation with other measures (r = .45), the n-back task has been found to be a valid measure of working-memory function (Shelton, Elliott, Hill, Calamia, & Gouvier, 2009).

Verbal short-term and long-term memory

The free-recall task assesses the modulation of memory storage processes (Nielson, Radtke, & Jensen, 1996) and has previously been used to study possible benefits of acute exercise on verbal short-term and long-term memory (Coles & Tomporowski, 2008; Pesce et al., 2009). Free-recall tasks have been found to be stable and reliable measures of verbal memory (r = .75–.77; Waters & Caplan, 2003). Following a standardized protocol (Nielson et al., 1996), two 20-item word lists were created from the nor- mative list of Paivio, Yuille, and Madigan (1968). Therefore, only nouns rating 6.40 or higher on imagery and concreteness (range = 1–7) were selected. Those words were translated into German and were back-translated into English by a native speaker. Nouns not matching the original form after the back translation were excluded. A linguist then controlled the words remaining on the list for frequency of usage in the German language. Finally, 4 words were repeatedly matched by concreteness, imagery, and frequency of usage and were randomly assigned to the two word lists until 20 items were reached. For the free- recall task, each word from the list (vertical visual angle = 1.3°) was presented for a period of 5 s, equaling a total presentation time of 100 s. Afterwards, participants were allowed (but not specifically encouraged) to rehearse the word list during a 100-s consolidation period. Then a sentence displayed on the screen asked participants to recall and write down as many words as possible in any order. The time limit for the immediate recall was 180 s. Afterwards, they listened to a 20-min lecture, which served as a distractor task administered to keep participants from rehearsing the word list. Two lectures on the same topic were prepared, so participants listened to Version A during the first experimental session and Version B during the second experimental session. Following the lecture, parti- cipants were again asked to write down any words they remembered to assess delayed recall. For the evaluation of correctly recalled words, minor spelling errors and plural– singular substitutions were ignored. Performance on the memory task was assessed by the total number of correctly recalled words in the immediate (short-term memory) and delayed (long-term memory) versions of the task.

EXERCISE, EXECUTIVE FUNCTION, AND MEMORY 167

Data analysis

In advance, Gaussian distribution of the collected data was checked by visual inspection of normality plots and by applying the Shapiro-Wilk test. Student’s t test was conducted to control if the mean heart rate during exercise was different from the predefined target heart rate. Analysis of variance (ANOVA) was used for com- parison of cognitive performance between conditions. The effect of exercise on inhibitory control was ana- lyzed by applying a 2 (condition: exercise, reading) × 2 (congruency: congruent, incongruent) ANOVA for reaction time on the Flanker task. As accuracy data followed a non-normal distribution, Wilcoxon signed- rank tests were used to compare accuracy between conditions and trial types. To examine the effect of exercise on hit rate and reaction time on the n-back task, a 2 (condition: exercise, reading) × 2 (difficulty: one-back, two-back) ANOVA was employed. Moreover, within-subject differences in verbal memory performance were analyzed using a 2 (condition: exer- cise, reading) × 2 (time of recall: immediate, delayed) ANOVA on the total number of correctly recalled words. When nonsphericity was confirmed, the Greenhouse-Geisser correction was applied. Within- subject effects as well as interactions were reported. For all statistical analyses, the level of significance was set at p < .05. The statistical analysis of collected data was performed with SPSS Version 22.0 (IBM Corporation, Armonk NY) for Windows.

Results

In the exercise condition, participants’ heart rate (135.6 ± 6.0 min−1) was not significantly different from the prescribed target heart rate, T(50) = 0.78, p = .441.

Regarding cognitive outcomes, a main effect of condi- tion on reaction time in the Flanker task was observed, F(1, 50) = 5.59, p = .022, η2 = .101. Participants’ reaction time to both congruent and incongruent stimuli was lower follow- ing exercise than after reading an academic text (see

Table 1). For incongruent trials, accuracy rates were higher after exercise (Mdn = .95) compared with the physically inactive control condition (Mdn = .92), Z = 1.97, p = .049, r = .275. In contrast, accuracy rates on congruent trials were not significantly different between conditions, Z = 0.72, p = .469, r = .101. Furthermore, the statistical analysis revealed a main effect of congruency on Flanker task reaction time, F(1, 50) = 159.09, p < .001, η2 = .761, so that participants showed higher reaction time on incon- gruent trials compared with congruent trials. Additionally, statistical analysis revealed higher accuracy on congruent (Mdn = .98) relative to incongruent trials (Mdn = 0.93), Z = 5.95, p < .001, r = .833.

In contrast to the effect of exercise on Flanker task performance, reaction time, F(1, 50) = 2.17, p = .147, η2 = .042, and hit rate on the n-back tasks, F(1, 50) = .03, p = .859, η2 = .001, were not influenced by condition. However, there was a main effect of difficulty (see Table 1) on reaction time, F(1, 50) = 66.10, p < .001, η2 = .569, and the adjusted hit rate, F(1, 50) = 81.05, p < .001, η2 = .618. In comparison with one-back trials, participants showed a lower hit rate and higher reaction time on two-back trials.

Regarding free recall, main effects of condition, F(1, 50) = 8.40, p = .006, η2 = .144, and time of recall, F(1, 50) = 18.24, p < .001, η2 = .267, on the number of correctly recalled words were found. Compared with participants in the physically inactive control condition, participants in the exercise condition recalled more words from the list (see Figure 2). Furthermore, more words were recalled in immediate recall than delayed recall.

Discussion

As the external validity of exercise-induced benefits for cognitive performance has only been investigated in children and adolescents (Jäger et al., 2014; Kubesch et al., 2009; Pirrie & Lodewyk, 2012), the present study aimed to replicate the effects of moderately intense aerobic exercise on young adults’ executive function and verbal memory in a classroom setting.

Table 1. Comparison of participants’ (n = 51) n-back and Flanker task performance between the antecedent running (RUN) and control (CON) conditions.

RUN CON

Task Trials Measures M SD M SD

Flanker Congruent Reaction time (ms) 342.1* 36.4 349.7 35.4 Accuracy 0.98 0.03 0.97 0.03

Incongruent Reaction time (ms) 368.7*,# 39.7 377.1# 39.4 Accuracy 0.93*,# 0.07 0.91# 0.07

n-back One-back Reaction time (ms) 368.2 49.2 377.2 66.2 Adjusted hit rate 0.71 0.28 0.72 0.23

Two-back Reaction time (ms) 417.5# 75.9 439.4# 103.8 Adjusted hit rate 0.43# 0.23 0.42# 0.25

* p < .05 compared with CON. # p < .05 compared with congruent trials (in the Flanker task) or one-back trials (in the n-back task)

168 S. LUDYGA ET AL.

Previous meta-analyses have shown improved execu- tive control after a single aerobic exercise session (Chang et al., 2012; Verburgh et al., 2014). This finding was partly supported by the present results as adjacent run- ning compared with reading an academic text signifi- cantly increased speed of processing and the inhibitory aspect of executive control. A recent review combining findings from behavioral and neuropsychological research indicated that such improvements are partly due to an increased allocation of attentional resources toward the task as well as reduced stimulus classification or evaluation time after aerobic exercise (Hillman, Kamijo, & Scudder, 2011). Benefits on inhibition have a high practical relevance in learning environments, because inhibitory control involves the ability to control one’s attention, behavior, and thoughts to override an internal predisposition or ignore external stimuli (Diamond, 2013). Particularly for group learning, sup- pression of disturbing behavior and resistance to dis- tractor interference are necessary to successfully focus attention on relevant information. As the present study replicated exercise-induced improvements in inhibitory control in a classroom setting, it is very likely that such temporary benefits may contribute to improved learning behavior in real-life situations.

In contrast to inhibition, working-memory perfor- mance was not different between the exercise condition and the physically inactive control condition. This finding is in conflict with the results of McMorris, Sproule, Turner, and Hale (2011), who found a strong positive effect of moderate exercise on speed of response in working-mem- ory tasks. In a more recent meta-analysis, Ludyga et al.

(2016) found that improvements in reaction time and accuracy on executive function tasks after moderately intense aerobic exercise were not influenced by the com- ponent assessed with the task. However, the majority of findings included for quantitative synthesis were obtained from laboratory studies, whereas the present results were based on cognitive assessments in a classroom setting. Therefore, the setting might have an influence on the effect of aerobic exercise on working memory, particularly when cognitive tests are administered in groups. Moreover, the impact of exercise on cognitive performance is not uniform across all individuals (Pesce, 2009), so the selection of students with high physical activity levels might have biased the results. In this respect, Sibley and Beilock (2007) found that participants with the lowest working- memory performance benefited most from a moderate aerobic exercise session. As students with high physical activity levels showed higher working-memory perfor- mance than students with low physical activity levels (Lambourne, 2006), a ceiling effect might explain why an impact of exercise on working memory could not be observed in the present study.

Regarding short- and long-term memory functions, running compared with reading enhanced young adults’ performance on the free-recall task. Consequently, a short exercise bout led to facilitation of memory functions, which do not involve (frequent) manipulation of the acquired information (Diamond, 2013). This result is in line with meta-analyses that have shown acute benefits of aerobic exercise for memory (Lambourne & Tomporowski, 2010) and the verbal-auditory subtype in particular (Roig et al., 2013). From a practical perspective, such exercise-induced improvements on verbal short- and long-term memory are interesting, because these cognitive functions are key com- ponents of successful learning (Paas & Ayres, 2014). It is also worth noting that running improved delayed recall, although the group setting and the distractor task may have affected different memory processes. However, it is possi- ble that inhibitory control contributed to increased mem- ory performance through an improved ability to suppress extraneous thoughts and resist proactive interference (Blumenfeld & Ranganath, 2007; Unsworth & Engle, 2007). This is important for encoding in particular as maintaining focus on the items to be remembered is a prerequisite for the acquisition of information (Diamond, 2013).

From a neurobiological perspective, exercise-induced increases in catecholamines and neurotrophins have been discussed as underlying mechanisms for the elicitation of transient changes in cognition (Roig et al., 2013). Elevated brain-derived neurotrophic factor (BDNF) levels in par- ticular have been shown to enhance the encoding, reten- tion, and retrieval of information (Bekinschtein,

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Figure 2. Performance on the immediate- and delayed-recall tasks after running (RUN) and in the physically inactive control condition (CON). * p < .05 immediate versus delayed recall; # p < .05 RUN versus CON.

EXERCISE, EXECUTIVE FUNCTION, AND MEMORY 169

Cammarota, Izquierdo, & Medina, 2008). Although BDNF signaling was not assessed in the present study, the exercise dose was greater than the minimal duration required for an increased expression (Tang, Chu, Hui, Helmeste, & Law, 2008). Moreover, findings from animal studies have provided evidence for increased dopamine and noradrenaline concentrations during exercise, which may facilitate cognitive functions in a dose-dependent matter (McMorris, Turner, Hale, & Sproule, 2016). Whereas a low to moderate release of these catecholamines has been related to improvements in inhibition and attention regulation, higher concentrations impaired executive control due to severe neural traffic (Arnsten, 2011; Arnsten & Li, 2005). McGaugh and Roozendaal (2002) also supported an enhancement of memory storage processes by facilitation of the release of noradrenaline and the activation of β-adrenoceptors within the basolateral amygdala. However, McMorris et al. (2016) suggested that high exercise intensity is necessary to increase noradrenaline to a certain level, at which it has a beneficial effect for long-term memory. In summary, a body of evidence has suggested that the exercise-induced improvements in memory functions and inhibitory control in the present study might partly be due to elevated BDNF levels and a moderate release of catecholamines, respectively.

As possible exercise benefits on specific cognitive domains were investigated using field testing, some limita- tions have to be taken into account for interpretation of the results. First, the present study design did not allow for a differentiation between maintenance and enhancement of cognitive performance by antecedent exercise because assessments were performed after the experimental condi- tions only. Consequently, it is likely that inhibitory control decreased due to the reading task and the subsequent distractor task. In that case, maintenance rather than enhancement of inhibition might explain the difference between the RUN and CON conditions. However, Chang et al. (2011) observed a small positive effect of reading on measures related to working memory and inhibitory con- trol processes in healthy young adults. This finding is an indication that the RUN condition may have elicited greater improvements than the CON condition in the present study. Second, findings from laboratory studies were replicated in a classroom setting. This replication does not necessarily mean that all groups found in educa- tional settings should expect cognitive benefits from an aerobic exercise session as the present study only supports an exercise-induced enhancement in inhibition and verbal memory in students with high physical activity. However, a recent meta-analysis did not show an influence of aerobic fitness, which was associated with physical activity levels, on exercise-induced enhancements of executive function

(Ludyga et al., 2016). It is still likely that other variables, such as perceived stress, intelligence, or sleep had a mod- erating role in the interaction between exercise and execu- tive function in the present study.

Conclusions

The present study indicated that in young adults, a running bout of moderate intensity compared with a physically inactive condition benefited inhibitory control as well as verbal short-term and long-term memory in a classroom setting. Consequently, exercise-induced enhancements in cognition were not limited to executive functioning. Moreover, the acute effect of aerobic exercise on executive function seemed to be selective, because working memory was not facilitated by antecedent running. As short-term and long-term memories as well as inhibitory control are related to learning and academic success, benefits elicited by exercise encourage the implementation of short running bouts in higher education settings.

ORCID

Sebastian Ludyga http://orcid.org/0000-0002-3905-7894 Markus Gerber http://orcid.org/0000-0001-6140-8948

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