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Effects of Acute Exercise on Sensory and Executive Processing Tasks

LAMBOURNE, KATE1; AUDIFFREN, MICHEL2; TOMPOROWSKI, PHILLIP D.1

Medicine & Science in Sports & Exercise: July 2010 - Volume 42 - Issue 7 - p 1396-1402
doi: 10.1249/MSS.0b013e3181cbee11
Applied Sciences

Purpose: The immediate and delayed effects of a single bout of steady-state aerobic exercise on 19 young adults' (mean = 21.1 yr) sensory sensitivity (critical flicker fusion, CFF) and executive function (modified Paced Auditory Serial Addition Task, PASAT) were assessed.

Methods: Tests were performed before exercise, five times during 40 min of ergometer cycling at 90% ventilatory threshold, and three times during a 30-min postexercise period. In a separate control session, each participant performed the same sequence of tests while seated on the ergometer without pedaling.

Results: ANOVA were performed separately on CFF and PASAT scores, which compared performance during exercise and nonexercise conditions at nine time points. Planned ANOVA of CFF scores revealed that the participants' sensory discrimination increased during exercise and then quickly returned to baseline levels immediately after exercise. PASAT scores did not change during or after exercise.

Conclusions: Exercise-induced arousal facilitates sensory processes involved in stimulus detection but does not influence the updating component of executive processing.

1University of Georgia, Athens, GA; and 2University of Poitiers, Poitiers, FRANCE

Address for correspondence: Phillip D. Tomporowski, Ph.D., Department of Kinesiology, University of Georgia, 330 River Road, Athens, GA 30602-6554; E-mail: ptomporo@uga.edu.

Submitted for publication August 2009.

Accepted for publication November 2009.

The changes in adult human physiology that take place during the transition from rest to steady-state aerobic exercise are well known (8). Less well understood are the changes in mental functioning that accompany the transition. Although numerous experiments have addressed the relation between acute exercise and cognition, the results remain equivocal. The ambiguity among research findings has been explained in terms of the intensity and/or duration of the exercise bout, the type of mental task performed, and when measures of cognitive function are obtained (21,31). Some researchers have used acute exercise protocols designed to lead to voluntary exhaustion under the supposition that fatigue will impair cognition, whereas other researchers have selected aerobic submaximal exercise protocols led by the assumption that cortical arousal will facilitate mental function. The results of both research approaches have not been consistent and are suggestive that exercise effects may be task dependent. Exercise-induced arousal has been hypothesized to facilitate lower-level information processing but interfere with high-level executive functions (14). However, clear support for the task-complexity hypothesis is lacking. Compounding the difficulty in interpreting the acute exercise literature are potential differences in cognitive function when measured during, as opposed to immediately after, exercise (32).

The present experiment is one of a series we have conducted that track changes in mental processing during a 40-min period as young adults transition from rest to steady-state aerobic exercise and during a 30-min postexercise period. The intensity and duration of the cycling protocol were selected on the basis of previous research reporting facilitation of simple and complex cognitive processing during exercise (24-26). The goal of our studies has been to conduct a fine-grain, time course analysis of cognitive performance during and immediately after a single, controlled exercise bout. The results of our previous studies provide some insight into the complex interaction that exists between exercise-induced physical activity and various types of mental processing. Audiffren et al. (2) used additive factors logic and EMG to isolate the effects of a 40-min bout of ergometer cycling on young adults' auditory choice response time, which was measured at nine time points. Cycling at 90% ventilatory threshold was found to result in a gradual reduction in the participants' CRT, which reached asymptote after approximately 19 min of exercise. The facilitating effects of exercise decreased immediately after cessation of physical activity. This pattern of results, together with the EMG data obtained, is consistent with the results of several studies that have reported improvements in young adults' rapid decision making during exercise-induced arousal (20).

Using the same exercise protocol, Audiffren et al. (3) observed a different pattern of cognitive performance when young adults performed a random number generation (RNG) task, which is a complex executive processing task that draws heavily on working memory abilities (4). In the RNG task used, participants were instructed to say a number between 1 and 9 every second and attempt to make the order of the numbers as random as possible. There are a variety of indices available to analyze RNG performance, which reflect the operation of specific executive functions (22,34). Inhibitory processes, which are used to suppress stereotyped responses, were affected by exercise. Compared with a rest condition, participants used less effortful RNG strategies, but only during the initial phase of exercise. The participants' RNG performance during the last 7 min of exercise and 30 min after the termination of exercise did not differ from their performance after a rest condition. The results were interpreted as evidence for dual-task interference that emerges when individuals concurrently adjust to changes in resistive exercise loads and perform complex mental tasks. Interference abates as cycling cadence becomes established. Similar views have been presented by Kurosawa (18) and Brisswalter et al. (7).

The present experiment used methods used by Audiffren et al. (2,3) to assess the time course of aerobic exercise on two mental processes: sensory discrimination and executive function. The tasks were selected to address specific hypotheses concerning the manner in which exercise-induced arousal influences mental functions. Both one-dimensional (16) and multidimensional (14) theories of attention and effort predict that arousal will alter the responsiveness of sensory systems to environmental stimulation. A critical flicker fusion (CFF) task was selected for the present experiment as an index of overall central nervous activity. The CFF is a visual sensory-discrimination task that measures the point at which an individual perceives that a flickering light has become fused, and the point at which a fused light begins to flicker. The CFF has been used by researchers in two studies that used steady-state aerobic exercise protocols. Davranche and Audiffren (9) reported that the CFF sensitivity of highly trained young adults increased significantly after 20 min of exercise performed at 50% V˙O2max but not after 20% V˙O2max or a rest condition. Several experiments, conducted with the expectation that fatigue would impair sensory processing, have assessed the impact of exhaustive exercise on young adults' CFF performance. In two studies, facilitative results were obtained. Presland et al. (27) found that CFF discrimination increased immediately after a strenuous bout of cycling and returned gradually to baseline levels during a 30-min postexercise rest period. Likewise, Davranche and Pichon (10) measured adults' CFF threshold before and immediately after a bout of exhausting exercise and also observed increased sensory sensitivity. These findings are consistent with the hypothesis that exercise modulates arousal and activation during exercise, which remain temporarily elevated immediately after exercise and return to baseline levels during recovery. To our knowledge, no study has examined the time course of change in CFF both during and after an acute bout of steady-state exercise.

The Paced Auditory Serial Addition Task (PASAT) was selected to measure the updating processes of executive function. Performance on the PASAT has been shown to be impaired during steady-state exercise (12) and explained in terms of the hypofrontality hypothesis (11), which predicts that the neural activity involved in the activation and control of motor movements draws resources from prefrontal cortical networks. PASAT performance has been shown to improve after the termination of exercise (33) and be explained by exercise-induced arousal. On the basis of our previous research (2), the participants' performance on the CFF task was predicted to improve gradually during the course of 40 min of exercise and then return gradually to baseline levels during a 30-min recovery period. On the basis of the hypofrontality hypothesis, PASAT performance was predicted to be impaired during exercise and improve after exercise attributable to heightened central arousal.

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METHODS

Participants.

Nineteen young adults (mean ± SD; age = 21.1 ± 1.7 yr) were recruited from undergraduate university classes to participate in this study. The physical characteristics of the participants are described in Table 1. Participants underwent an initial screening in which a medical history questionnaire was completed to identify contraindications to strenuous exercise. The study was reviewed and approved by the university's institutional review board.

TABLE 1

TABLE 1

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Procedures.

Each participant completed three sessions that were approximately 7 d apart and occurred at the same time of the day. During the first session, details of the study were explained to the participant, and each read and signed an informed consent document approved by the university's institutional review board. The medical history questionnaire was used to identify potential risk factors that might contraindicate participation in physical activity (e.g., disease states, medication, neurological deficits). A physical activity questionnaire was also administered and was used to ensure that the participants who were selected exercised on a regular basis (three or more times per week). None of the volunteers was excluded from the study.

The first session also involved familiarization with the cognitive tasks and assessment of cardiorespiratory function. The participant was led to the testing area and seated on the cycle ergometer. A small table constructed to hold the CFF device was positioned over the ergometer between the seat and the handlebars. The table allowed the participant to support his/her arms while performing the CFF task. After eye dominance was assessed, the participant was instructed to place the response switch of the Lafayette Instrument 12021 Flicker Fusion apparatus (Lafayette, ID) in the ipsilateral hand and place his/her face into the mask of the device. A single light was presented in the visual field of the dominant eye. The participant was instructed to make a response by depressing a switch when the flicker appeared to fuse (ascending threshold) and when a fused light appeared to flicker (descending threshold). The flicker frequencies ranged between 0 and 100 Hz. Measurement began at 0 Hz for ascending trials and 100 Hz for descending trials. Light frequency changed at a rate of 4 Hz·s−1. There was a 4-s delay between trials. Following instructions, the participant performed 40 trials consisting of 20 ascending and 20 descending sequences.

After completion of the CFF task, the participant dismounted the ergometer, took a seat at a computer station, and was given instructions for the adapted PASAT. In this task, the participant was presented a random series of single-digit numbers aurally via headphones. The task required the participant to add pairs of numbers such that each number was added to the number that immediately preceded it on the list. This requires the ability to inhibit the verbal response and attend only to the digits that were presented in the series. Performance was measured as the proportion of digit pairs correctly added and reported. The test was adapted from the original PASAT (19). During training, a series of 40 numbers from 1 to 9 were presented to the participant in a randomized order. Each series of 40 numbers constituted a trial, and participants performed 14 practice trials. During the first six trials, the 40 stimuli were presented at intervals of 1.6 s per digit. If the participant had higher than 90% accuracy by the sixth trial, the interstimulus interval was reduced to 1.2 s for the remaining and subsequent testing trials. If the participant's accuracy was between 60% and 90%, he/she was tested with a 1.6-s interstimulus interval, and if accuracy was lower than 60%, 2-s interstimulus intervals were used. Eleven of the participants were tested at a 1.2-s interstimulus interval, four participants were tested at a 1.6-s interstimulus interval, and three participants were tested at a 2-s interval. The manipulation of the interstimulus interval was used to equate for interindividual differences in processing speed.

After familiarization with the CFF and PASAT tasks, the participant completed a test of maximal oxygen consumption (V˙O2peak) on a braked cycle ergometer (Corival model No. 906900; Lode BV, Groningen, The Netherlands). The table for the CFF device was removed from the testing area, and the seat and handlebars of the cycle were adjusted to fit the participant. A Polar T61 HR monitor was placed around the chest, and instructions were given regarding the procedures and RPE. Perceived exertion was measured using the Borg 15-point category scale (6). The test began with a 5-min warm-up at 24 W and increased to 50 W as the graded exercise phase started. The wattage increased continuously at a rate of 23 W·min−1 thereafter. Respiratory gases were sampled continuously using open-circuit spirometry (TrueOne 2400 Metabolic Measurement System; Parvo Medics, Sandy, UT). The test was administered at room temperature (21°C-23°C). During the test, HR and RPE were obtained every 60 s. A visual scale for RPE was provided to allow the participant to point to the number that corresponded with his/her perceived exertion. The test was terminated when the participant could not maintain a cadence of 40 rpm or when he/she acknowledged voluntary exhaustion. Verbal encouragement was provided throughout the test, particularly once the participant reported an RPE of 17 or higher. V˙O2peak (mL·kg−1·min−1) was defined by reaching two of the following three criteria: 1) RER ≥ 1.15, 2) RPE ≥ 18, or 3) a failure to increase oxygen intake with further exercise intensity. After completion of the graded exercise test, the session was complete.

A second session consisted of a 40-min bout of steady-state cycling on the cycle ergometer. Before the cycling bout, the participant was provided practice on the CFF and PASAT tasks. A series of six ascending and descending CFF trials was completed while the participant was seated on the ergometer. Next, the participant completed three practice PASAT trials that consisted of 40 numbers.

The first test block was performed on the ergometer before the participant began exercise. Each test block consisted of performing the CFF and PASAT tasks. The CFF test consisted of three ascending and descending trials during which the participant's response was recorded and stored automatically via computer software. The mean CFF threshold for test blocks was determined for the three trials as recommended by Kranda (17). The PASAT consisted of the presentation of 40 numbers, during which the participant's auditory responses were recorded on a tape recorder and a response checklist. The CFF task was always performed first because the PASAT task is known to produce test anxiety and increased arousal in some individuals (30).

After the first block of cognitive tasks, the participant completed a 5-min warm-up at 30% of the participant's V˙O2peak. The exercise phase consisted of pedaling against a resistance that elicited 90% of the participant's ventilatory threshold (VT) as estimated by the V˙O2peak test. In the present study, VT was estimated by using the V-slope method (5). The second through sixth testing blocks occurred at 8, 14, 22, 28, and 34 min after pedaling began. The final three trials occurred 1 min after exercise and again at 15 and 30 min after exercise. Water was provided ad libitum. HR was recorded after each test block, and RPE was obtained. The mean ± SD workload during exercise was 208.9 ± 46 W, which resulted in a mean ± SD HR of 143 ± 13 bpm and a mean ± SD RPE of 13 ± 1. See Figure 1 for a schematic of the experimental sessions.

FIGURE 1

FIGURE 1

A third session consisted of a resting control condition. The protocol was the same as the exercise condition, except for the exercise. The participant first practiced the cognitive tasks and then performed the test blocks at the same time intervals during the 70-min session duration. The participants' mean ± HR was 84 ± 11 bpm, and the mean ± SD RPE was 6 ± 0.2. The order of the rest and exercise conditions was counterbalanced across participants and separated by approximately 7 ± 2 d. The participant was debriefed about hypotheses related to the study at the completion of the third session.

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Statistical analysis.

A within-participant repeated-measures design was used, with counterbalanced order of interventions. The participants' CFF and PASAT scores were analyzed separately using a 2 (condition: exercise or no exercise) × 9 (test block: 1 to 9) ANOVA with repeated measures on both factors. Significant omnibus tests were followed by planned two-way ANOVA conducted on performance during the pretest and the first five test blocks performed during exercise to assess the immediate effects of exercise on cognitive function. The short-term after effects of exercise on cognitive function were measured via two planned comparisons: 1) a two-way ANOVA was conducted on performance during the final exercise block and the three postexercise test blocks and 2) a two-way ANOVA was performed to analyze the preexercise test scores and the scores from the three postexercise test blocks. Trend analyses were conducted to examine test performance before and during exercise, as well as performance during the final period of exercise and the postexercise phase. Violations of sphericity were corrected by adjusting the degrees of freedom according to the Greenhouse-Geisser test. An α of 0.05 was used for ANOVA and trend tests. Estimates of effect size (ηp 2) were reported for significant main effects and interactions. Post hoc paired-sample t-tests were conducted for each test block using a Bonferroni correction for multiple comparisons. Paired-sample t-tests were also used to compare preexercise test performance to each postexercise test block. Reliability of test scores was assessed by computing an intraclass correlation coefficient (ICC) for the scores obtained during the control condition using a two-way random consistency model.

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RESULTS

The two-way ANOVA conducted on CFF scores that were measured before, during, and after exercise yielded a significant interaction between test condition and test block, F 8,144 = 5.98, P < 0.001, ηp 2 = 0.25. The planned two-way ANOVA that assessed the immediate effects of exercise on CFF scores also yielded a significant interaction, F 5,90 = 8.82, P < 0.001, ηp 2 = 0.33. The CFF scores differed significantly between exercise and control conditions at the fifth test block (minute 28), t = 2.93, P = 0.009, and the sixth test block (minute 34), t = 2.96, P = 0.008. CFF scores during exercise increased from baseline at each time point, eventually leveling off (Fig. 2). The trend analysis revealed both a significant linear trend, F 1,18 = 20.85, P < 0.001, ηp 2 = 0.54, and a significant quadratic trend, F 1,18 = 21.44, P < 0.001, ηp 2 = 0.54. The planned two-way ANOVA conducted on performance during the last exercise block and the three postexercise test blocks yielded a significant interaction, F 3,54 = 4.62, P = 0.006, ηp 2 = 0.20. There was a significant difference in CFF scores between exercise and control conditions during the last exercise block, t = 2.96, P = 0.008, but this difference did not remain when the CFF threshold was tested 1 min after exercise, t = 0.88, P = 0.39. Comparisons between the final two postexercise test blocks (15 and 30 min after exercise) revealed no difference between the exercise and control conditions. The CFF scores dropped immediately after the cessation of exercise and followed a decreasing linear trend, F 1,18 = 16.34, P = 0.001, ηp 2 = 0.48. The planned ANOVA conducted on preintervention and postintervention test scores yielded a significant main effect for time, F 3,54 = 3.37, P = 0.03, ηp 2 = 0.16, and the interaction between time and condition approached statistical significance, F 3,54 = 2.57, P = 0.06, ηp 2 = 0.13. The ICC analysis of the participants' CFF scores revealed that they were stable within the control condition (α = 0.99).

FIGURE 2

FIGURE 2

The two-way ANOVA conducted on PASAT scores that were measured before, during, and after exercise did not yield significant main effects or interactions. There were no significant interactions or main effects for the PASAT scores in the comparison between the last exercise block and the three postexercise test blocks or the preexercise and postexercise test scores. The participants' performance is shown in Table 2. The ICC analysis of the participants' PASAT scores during the control condition revealed that they were stable throughout the session (α = 0.95).

TABLE 2

TABLE 2

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DISCUSSION

Young adults' sensory sensitivity and their executive processing performance were measured five times during the course of 40 min of cycling at a moderate aerobic level and three times during a 30-min postexercise period. As predicted, there was a gradual improvement in the participants' sensory sensitivity during exercise. The increase in sensory sensitivity paralleled closely the facilitation of young adults' CRT performance observed by Audiffren et al. (2). It seems that moderate steady-state exercise, like other agents that increase central nervous system arousal (e.g., psychostimulant drugs), enhances performance by making the individual more receptive to sensory stimulation and by increasing the speed of late motor processes. Importantly, the facilitation of young adults' performance is a gradual process, which apparently peaks after exercising submaximally for periods of 15-20 min. After the termination of exercise, there was a rapid decrease in sensory sensitivity to baseline levels. The rate of decline in CFF was more rapid than reported by Presland et al. (27), who observed a gradual decrease in CFF during successive 10-min intervals after the termination of exercise. However, in the study of Presland et al. (27), CFF measures were obtained after an exhaustive incremental exercise bout. It remains to be determined whether the duration and the intensity of exercise influence the maintenance of sensory sensitivity after exercise. Nevertheless, the findings of the present experiment, together with those obtained by Audiffren et al. (2), have implications for applied sport psychologists and human factors researchers interested in optimizing operational performance. Audiffren et al. (2) reported a reduction in CRT on the order of 17 ms, and in the present experiment, we report an improvement of sensory sensitivity, which may determine either success or failure in many sports contexts (e.g., track events, tennis, or baseball batting). Thus, gains in performance may be linked to preevent warm-up exercise activities of specific duration and intensity.

The results obtained are consistent with historical and contemporary views of arousal, activation, and effort (16,29). In Sanders' model (29), arousal is conceptualized as a construct that differentially affects cognitive processes. Arousal is linked to involuntary attentional control and is thought to be a temporary, phasic, reflexive-like response to a stimulus input. Activation is the tonic component of the involuntary mode of attentional control and is a stable, generalized readiness to respond. The coordination of the two components of involuntary control is accomplished through the regulation of effort, which, in turn, regulates the voluntary mode of attentional control. Increases in arousal resulting from exercise may benefit sensory-type tasks such as the CFF by priming an individual to respond to incoming stimuli. The results obtained are also in concert with the view that acute bouts of exercise influence the release of neuromodulators, thereby facilitating cognitive processes in a fashion similar to some psychostimulant drugs (1). Exercise-induced changes in catecholamines and monoamines may improve the ability to discriminate between sensory information by altering the neurological signal-to-noise ratio. Several experiments conducted in animals showed that an increase in brain noradrenergic transmission improves the signal-to-noise ratio of evoked responses to environmental stimuli, by enhancing evoked responses, by suppressing "background activity," or by a combination of these two effects. This occurs in several cortical terminal regions, whatever the sensory modality (15,23).

The participants' executive processing as measured by the PASAT was predicted to decrease during exercise and then to be facilitated during recovery. There were, however, no systematic changes in the participants' performance. The results failed to support predictions derived from both the hypofrontality (11) and arousal theories (14). The lack of agreement between the present study and the study conducted by Dietrich and Sparling (12) may be attributable to methodological differences. The PASAT stimuli lists used in the present experiment were shorter than those used by Dietrich and Sparling, and the stimulus-presentation rate was selected on the basis of each participant's processing speed. The failure to detect the predicted decrement in cognitive performance during exercise might have occurred because repeated performance of the PASAT resulted in near-ceiling performance level in several participants, and as a result, the test may not have been sensitive to change. Alternatively, as demonstrated by Audiffren et al. (3), the effects of acute exercise on executive function may be selective because, in that experiment, cycling modulated inhibitory but not updating processes. Parsing components of cognitive function that are influenced by acute exercise will require additional research that can isolate and measure basic mental processes. The results also failed to replicate the results of previous research, where a facilitation of PASAT performance was observed when tested 30 min after the termination of exercise (33). Again, the failure to observe improved PASAT performance may have been attributable to ceiling effects that allowed little room for improved performance.

A limitation of the present study, as well as many others, is the selection of executive function tasks that are sensitive to the effects of exercise interventions while maintaining acceptable levels of reliability and stability (13,28). The PASAT was selected, and attempts were made to address these issues in the present study; nevertheless, potential exercise-related changes were obfuscated by the ceiling effects. Future research on the effects of exercise on cognitive performance would benefit by the selection of executive processing tasks that do not suffer from floor or ceiling effects. In addition, the participants in the present study were active and physically fit; future research will be needed to address how exercise-induced arousal affects basic information processing in less fit younger adults.

Several researchers have commented on the challenges faced when attempting to demonstrate the effects of acute exercise on cognitive function (13,32). A task comparison approach was taken in our series of experiments (2,3). In each study, the exercise protocols were identical, with intensity and duration carefully chosen on the basis of previous research to increase the likelihood to observe a positive effect of exercise on cognitive processes. Audiffren et al. (2) observed a temporally linked facilitation on CRT that was similar to the temporal change in sensory sensitivity in the CFF task observed in the present study. Likewise, CRT and CFF performance returned to baseline conditions almost immediately after the cessation of exercise. These results confirm the close interrelationship between sensory processes and sustained information transfer processes. The effects of acute exercise on higher-level cognitive processes are unclear. Although exercise modulated inhibition processes during RNG tasks (3), it did not affect PASAT performance in the present study. The lack of agreement may be attributable to the aforementioned measurement sensitivity or it may be the case that exercise-induced arousal does not influence executive updating processes used in working memory tasks.

Acute bouts of moderate-intensity exercise influenced the performance of a sensory-dependent cognitive task. This effect increased throughout the exercise period but disappeared rapidly once exercise was terminated. This pattern of performance can be explained in terms of arousal theory, which predicts that exercise-induced arousal will affect attentional control processes that filter stimulus input. Complex executive processing measured in terms of working memory did not differ from control conditions either during or after the termination of exercise. Thus, the effects of exercise on complex, executive processing tasks remain to be elucidated.

No outside funding was received for this work.

The results of this study do not constitute endorsement by American College of Sports Medicine.

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Keywords:

COGNITION; CRITICAL FLICKER FUSION; PACED AUDITORY SERIAL ADDITION TASK; WORKING MEMORY

©2010The American College of Sports Medicine