Elsevier

NeuroImage

Volume 50, Issue 4, 1 May 2010, Pages 1702-1710
NeuroImage

Acute moderate exercise elicits increased dorsolateral prefrontal activation and improves cognitive performance with Stroop test

https://doi.org/10.1016/j.neuroimage.2009.12.023Get rights and content

Abstract

A growing number of human studies have reported the beneficial influences of acute as well as chronic exercise on cognitive functions. However, neuroimaging investigations into the neural substrates of the effects of acute exercise have yet to be performed. Using multichannel functional near-infrared spectroscopy (fNIRS), we sought cortical activation related to changes in the Stroop interference test, elicited by an acute bout of moderate exercise, in healthy volunteers (N = 20). The compactness and portability of fNIRS allowed on-site cortical examination in a laboratory with a cycle ergometer, enabling strict control of the exercise intensity of each subject by assessing their peak oxygen intake (V·o2peak). We defined moderate exercise intensity as 50% of a subject's peak oxygen uptake (50%V·o2peak). An acute bout of moderate exercise caused significant improvement of cognitive performance reflecting Stroop interference as measured by reaction time. Consistent with previous functional neuroimaging studies, we detected brain activation due to Stroop interference (incongruent minus neutral) in the lateral prefrontal cortices in both hemispheres. This Stroop-interference-related activation was significantly enhanced in the left dorsolateral prefrontal cortex due to the acute bout of moderate exercise. The enhanced activation significantly coincided with the improved cognitive performance. This suggests that the left dorsolateral prefrontal cortex is likely the neural substrate for the improved Stroop performance elicited by an acute bout of moderate exercise. fNIRS, which allows physiological monitoring and functional neuroimaging to be combined, proved to be an effective tool for examining the cognitive effects of exercise.

Introduction

A body of human and animal studies have reported the beneficial influence of exercise on cognitive and brain functions. Accordingly, exercise is drawing increasing research attention as a possible lifestyle factor for improving neurocognitive functions, and preventing or delaying dementia (Cotman et al., 2007, Hillman et al., 2008).

So far, the majority of studies have focused on the chronic effects of exercise, while studies on acute exercise effects on cognition have only started to draw growing attention (Tomporowski, 2003). Recent studies provide evidence that an acute bout of moderate aerobic exercise improves cognitive performance in a choice reaction task (Chmura et al., 1998), a simple reaction time task (Collardeau et al., 2001), as well as confliction tasks such as Eriksen flanker and Stroop tasks (Hogervorst et al., 1996, Kamijo et al., 2004, Kamijo et al., 2007).

Keeping pace with the examination of the cognitive effects of acute exercise, the search for their neural substrates has been accelerated mainly in the field of event-related potential (ERP) research. P300 (or P3) is a component believed to indicate the brain activity required to maintain working memory when the mental model of the stimulus environment is updated (Donchin & Coles, 1988), and is thus regarded as an appropriate neural substrate for improved cognitive performance. Several studies have generally demonstrated increased amplitude and shortened latency of P300 components in relation to the performance improvements caused by an acute bout of exercise (Hillman et al., 2003, Hillman et al., 2008, Kamijo et al., 2004, Kamijo et al., 2007, Magnie et al., 2000, Nakamura et al., 1999, Polich and Lardon, 1997).

ERP provides high temporal information about brain activities, but it provides only rough information regarding where in the brain the effect was originated. In order to examine which brain regions change activation in response to exercise, the application of different neuroimaging techniques would be beneficial. As a promising neuroimaging technique for investigating the acute effects of exercise on cognition, we introduced functional near-infrared spectroscopy (fNIRS): an optical method that non-invasively monitors cerebral hemodynamics by measuring changes in the attenuation of near-infrared light passing through tissue (Koizumi et al., 2003, Obrig and Villringer, 2003, Villringer and Chance, 1997). In many studies, fNIRS has proven to be effective in assessing oxygenation changes in response to cortical activities, utilizing the tight coupling between neuronal activity and regional cerebral blood flow. In contrast to other neuroimaging methods, fNIRS requires only compact experimental systems, is portable, and can be easily installed in a gym (Timinkul et al., 2008) (Fig. 1). This is advantageous for our study as exercise intensity can be strictly controlled using gym facilities, and on-site neuroimaging allows precise control of the interval between exercise and brain measurement. Moreover, since fNIRS allows for the least restrictive measuring environment among neuroimaging modalities, possible influences on cognitive tasks can be kept minimal.

An important factor that needed to be controlled for this study was the exercise intensity for each subject. Behavioral studies and recent ERP studies have shown that the effects of acute exercise on cognitive performance and brain response differ depending on the exercise intensity: The best improvements are generally achieved with a moderate intensity (Kamijo et al., 2004, Kamijo et al., 2007). Nevertheless, the same degree of difficulty of a physical task will have different impacts on each subject depending on an individual's fitness level. Therefore, we assessed the peak oxygen intake (V·o2peak) for each subject and defined a moderate exercise intensity as 50% of a given subject's V·o2peak (50%V·o2peak).

For the cognitive task, we chose the color–word matching Stroop task, a classical measure of prefrontal cortex (PFC) function (MacLeod, 1991), because it has been studied extensively using many neuroimaging techniques including fNIRS (Ehlis et al., 2005, Schroeter et al., 2002, Schroeter et al., 2003, 2004b), and the brain regions associated with the task are well known. In the color–word matching Stroop task, subjects observe the names of colors presented in various ink colors, and are instructed to name the presented ink color (Fig. 2A). Color names are presented in non-matching ink colors (e.g., the word green presented in red ink) in the incongruent condition, color names are presented in matching ink colors (e.g., the word green presented in green ink) in the congruent condition, and non-color letters are presented in any ink color (e.g., the letters XXXX presented in red ink) in the neutral condition. During the incongruent condition, the two conflicting sources of color information cause a competing effect known as Stroop interference, which is most typically observed as a prolonged reaction time compared to the neutral or congruent conditions (Laird et al., 2005).

Stroop interference is consistently associated with the anterior cingulate cortex (ACC) and the lateral prefrontal cortex (LPFC), especially the dorsolateral prefrontal cortex (DLPFC), where the ACC is considered to be susceptible to conflict, and the DLPFC is purported to implement cognitive control (Carter et al., 2000, Leung et al., 2000). Although fNIRS cannot monitor the cortical activation in the ACC because its measurement is limited to lateral cortical surfaces, it has successfully monitored the activation of the LPFC associated with Stroop interference (Ehlis et al., 2005, Schroeter et al., 2002, Schroeter et al., 2003, 2004b), and some of these studies have also demonstrated LPFC activation related to Stroop task performance (Carter et al., 1995, Carter et al., 2000, Leung et al., 2000, Pardo et al., 1990, Taylor et al., 1997, Zysset et al., 2001). In addition, it has been observed that the color–word matching Stroop task does not always involve ACC activation (Zysset et al., 2001). Therefore we focused our analyses on the LPFC, and set fNIRS probes to cover the region.

In this way, we aimed to examine where in the LPFC activation related to Stroop interference changes due to an acute bout of moderate exercise. Using an event-related multichannel fNIRS targeting the LPFC, we compared the cortical activation pattern during the color–word matching Stroop task before and after the acute bout of moderate physical exercise. Together, we will provide the first experimental evidence that the improved cognitive performance after an acute bout of exercise has relevant neural substrates in specific regions of the LPFC.

Section snippets

Materials and methods

The overall procedure consisted of three major steps. First, in Pilot Study 1, we determined the V·o2peak to find the appropriate level of exercise for each subject. Second, in Pilot Study 2, we examined the effects of non-cortically derived physiological signals evoked by exercise on fNIRS measurements (skin blood flow etc.). Finally, we assessed the effects of an acute bout of exercise on cortical activation during a color–word matching Stroop task. Details of Pilot Studies 1 and 2 are

Results

The subjects underwent two fNIRS experiments: exercise (EX) and control (CTL) experiments, each with two sessions (Fig. 2B). In EX experiments, subjects performed the Stroop task before (pre-session) and 15 min after (post-session) the acute exercise bout. In the CTL experiment, subjects rested during the interval between pre- and post-sessions instead of performing any exercise. Brain activity was monitored with fNIRS while subjects performed the Stroop task. The two experiments were performed

fNIRS results

Fig. 5A illustrates patterns of cortical activation during Stroop tasks in the EX condition represented by [peak period–baseline period] contrasts for the oxy-Hb signal. Examples of one-channel timeline data for oxy-Hb and deoxy-Hb signals are also exhibited. First, we observed more stable event-related oxy-Hb signals than deoxy-Hb signals. Thus, oxy-Hb signals are more appropriate for our experimental conditions. Second, cortical activation was generally greater in incongruent conditions than

Discussion

In this study, we have for the first time applied fNIRS measurements to assess the neural substrates underlying the cognitive effect of an acute bout of moderate exercise. fNIRS measurements in a laboratory enabled strict control of the exercise intensity across subjects to be set at 50%V·o2peak. Since most of the ERP studies performed thus far have not applied strict criteria related to physical fitness, the current study is valuable in that it couples physiological monitoring with functional

Acknowledgments

This work was supported in part by a grant of the 21st Center of Excellence (COE) program from the Japanese Ministry of Education, Culture, Sports, Science, and Technology, the Program for Promotion of Basic Research Activities for Innovative Bioscience, and Health and Labor Sciences Research Grants, Research on Psychiatric and Neurological Diseases and Mental Health.

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