Prefrontal oxygenation and the acoustic startle eyeblink response during exercise: A test of the dual‐mode model

Abstract

The interplay between the prefrontal cortex and amygdala is proposed to explain the regulation of affective responses (pleasure/displeasure) during exercise as outlined in the dual-mode model. However, due to methodological limitations the dual-mode model has not been fully tested. In this study, prefrontal oxygenation (using near-infrared spectroscopy) and amygdala activity (reflected by eyeblink amplitude using acoustic startle methodology) were recorded during exercise standardized to metabolic processes: 80% of ventilatory threshold (below VT), at the VT, and at the respiratory compensation point (RCP). Self-reported tolerance of the intensity of exercise was assessed prior to, and affective responses recorded during exercise. The results revealed that, as the intensity of exercise became more challenging (from below VT to RCP), prefrontal oxygenation was larger and eyeblink amplitude and affective responses were reduced. Below VT and at VT, larger prefrontal oxygenation was associated with larger eyeblink amplitude. At the RCP, prefrontal oxygenation was greater in the left than right hemisphere, and eyeblink amplitude explained significant variance in affective responses (with prefrontal oxygenation) and self-reported tolerance. These findings highlight the role of the prefrontal cortex and potentially the amygdala in the regulation of affective (particularly negative) responses during exercise at physiologically challenging intensities (above VT). In addition, a psychophysiological basis of self-reported tolerance is indicated. This study provides some support of the dual-mode model and insight into the neural basis of affective responses during exercise.

Aerobic Exercise Decreases Negative Affect by Modulating Orbitofrontal-Amygdala Connectivity in Adolescents

“…The aforementioned evidence has demonstrated that physical exercise could exert influences on the functions of both amygdala and OFC. The dual-mode theory postulates that affective responses to exercise are determined by the continuous interplay between cognitive parameters (from PFC to the amygdala) and interoceptive cues (from subcortical homeostatic afferents to amygdala) [ 20 ]. A greater ability to down-regulate negative emotions means a greater amygdala attenuation and greater inverse OFC/dlPFC-amygdala FC [ 41 ].…”

“…Lateral OFC activity was associated with down-regulation of emotional responses, and a functional coupling of the amygdala during the negative appraisal process [ 42 ]. The prefrontal control system influences the amygdala activity in the emotional system [ 43 ] by combating the sensory input to the amygdala [ 20 ] and then affect the emotional response. On the other hand, exercise could directly decrease the activity of amygdala.…”

“…Moreover, the results of our research may be restricted by the small sample size, as neuroimaging requires powerful statistical power; therefore, future study with larger sample size is encouraged. In addition, some previous studies have explored the relationship between acute exercise intensity and mood regulation [ 20 ], which found that high-intensity physical activity resulted in significantly more negative affect than either light or moderate-intensity physical activity [ 47 ]. Although we have confirmed in this study that moderate-intensity acute exercise can reduce negative affect, we could not generalize this effect and neural mechanism to all exercise intensity, which needs to be assessed in further investigation.…”

“…Furthermore, a recent functional magnetic resonance imaging (fMRI) study examined the neural mechanism underlying the effect of a 15-min moderate to high-intensity treadmill running on the perception of emotional faces, which found that compared with walking, running produced significant anxiolytic effects, indicating the underlying neural mechanisms might be related to amygdala reactivity and its connectivity with the orbitofrontal cortex and insula [ 19 ]. Similarly, a functional near-infrared spectroscopy study also observed the crucial role of the amygdala and prefrontal cortex in regulating negative emotional responses during acute exercise [ 20 ]. These studies consistently observed increased functional activity of prefrontal cortex.…”

Affective and Enjoyment Responses to Sprint Interval Exercise at Different Hypoxia Levels

“…Individual differences in physical (e.g., physical activity level [39]), psychological status (e.g., exercise preference and tolerance of intensity) [40,41], and macronutrient intake (e.g., low-carbohydrate diets) [42] also account for the discrepancy. From the aspect of the neural system, the interplay of prefrontal cortex and amygdala have been revealed to regulate affective responses during exercise [43][44][45]. For example, individual differences in the ability to maintain prefrontal cortex involvement, indicated by self-reported tolerance, are possibly associated with feelings of pleasure or displeasure [41,44].…”