Pupil dynamics during very light exercise predict benefits to prefrontal cognition

Kuwamizu, Ryuta; Yamazaki, Yudai; Aoike, Naoki; Hiraga, Taichi; Hata, Toshiaki; Yassa, Michael A.; Soya, Hideaki · 2023 · DOAJ

DOI: 10.1016/j.neuroimage.2023.120244

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Summary

This study investigates the neural mechanisms underlying the cognitive benefits of very-light-intensity exercise, specifically addressing how such exercise enhances prefrontal executive function. While previous research established that stress-free, very-light exercise (e.g., yoga, slow running) improves executive performance, the specific neural substrates triggering this enhancement remained unidentified. The authors hypothesized that pupil-linked brain dynamics, associated with locus coeruleus (LC) activation and arousal, mediate these benefits. To test this, they examined whether pupil dilation during exercise predicts subsequent improvements in prefrontal cognition. The study employed a crossover design with 24 healthy young adults who underwent two conditions: a resting control (CTL) and a very-light-intensity exercise (EX) session involving 10 minutes of cycling at 30% of peak oxygen uptake ($\dot{V}O_2peak$). Executive function was assessed using a color-word Stroop task before and after each condition, with performance measured via inverse efficiency scores (IES). Prefrontal cortical activation during the task was monitored using multichannel functional near-infrared spectroscopy (fNIRS), focusing on regions such as the dorsolateral prefrontal cortex (DLPFC). Concurrently, pupil diameter was recorded via eye-tracking during the exercise period to serve as a noninvasive marker of arousal and LC activity. Statistical analyses included repeated measures ANOVA for pupil dynamics, paired t-tests for cognitive and neural changes, and causal mediation analysis to determine if pupil dilation mediated the relationship between exercise and cognitive performance. The results demonstrated that very-light-intensity exercise significantly increased pupil diameter compared to the resting control. This physiological change was associated with improved Stroop task performance, evidenced by a significant reduction in Stroop interference IES. fNIRS data revealed that exercise potentiated task-related activation in the left DLPFC. Crucially, the magnitude of pupil dilation during exercise positively predicted the magnitude of improvement in Stroop performance. Causal mediation analysis confirmed that pupil dilation robustly mediated the effect of exercise on Stroop performance, indicating that the arousal-linked neural state reflected by pupil changes is a key mechanism for cognitive enhancement. However, pupil dilation did not significantly mediate the exercise-induced increase in DLPFC activation. These findings suggest that pupil-linked mechanisms, likely tied to locus coeruleus activation, serve as a primary pathway through which very-light exercise enhances prefrontal executive function. The study identifies pupillometry as a valuable tool for interpreting the real-time neural impacts of exercise on cognition. By establishing a causal link between exercise-induced arousal markers and cognitive benefits, the research provides insight into the neurophysiological basis of exercise-induced cognitive potentiation, supporting the use of low-intensity physical activity for brain health without the stress responses associated with higher intensities.

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