Abstract
BackgroundIt is unclear whether and how elite athletes process physiological or psychological challenges differently than healthy comparison subjects. In general, individuals optimize exercise level as it relates to differences between expected and experienced exertion, which can be conceptualized as a body prediction error. The process of computing a body prediction error involves the insular cortex, which is important for interoception, i.e. the sense of the physiological condition of the body. Thus, optimal performance may be related to efficient minimization of the body prediction error. We examined the hypothesis that elite athletes, compared to control subjects, show attenuated insular cortex activation during an aversive interoceptive challenge.Methodology/Principal FindingsElite adventure racers (n = 10) and healthy volunteers (n = 11) performed a continuous performance task with varying degrees of a non-hypercapnic breathing load while undergoing functional magnetic resonance imaging. The results indicate that (1) non-hypercapnic inspiratory breathing load is an aversive experience associated with a profound activation of a distributed set of brain areas including bilateral insula, dorsolateral prefrontal cortex and anterior cingulated; (2) adventure racers relative to comparison subjects show greater accuracy on the continuous performance task during the aversive interoceptive condition; and (3) adventure racers show an attenuated right insula cortex response during and following the aversive interoceptive condition of non-hypercapnic inspiratory breathing load.Conclusions/SignificanceThese findings support the hypothesis that elite athletes during an aversive interoceptive condition show better performance and an attenuated insular cortex activation during the aversive experience. Interestingly, differential modulation of the right insular cortex has been found previously in elite military personnel and appears to be emerging as an important brain system for optimal performance in extreme environments.
Highlights
The neuroscience underlying optimal performance in extreme environments is in its infancy [1]
The breathing load resulted in an aversive experience, there were no differences in the degree of unpleasantness between adventure racers and comparison subjects
We examined the hypothesis that elite athletes show attenuated neural processing of aversive interoceptive stimulation in the insular cortex by testing the behavioral and neural processing response of elite athletes during an aversive interoceptive nonhypercapnic breathing load
Summary
The neuroscience underlying optimal performance in extreme environments is in its infancy [1]. The U.S Navy SEALs showed selectively greater activation to angry target faces relative to fearful or happy target faces in both right and left insula [4] These individuals show greater insula activation when anticipating a change in interoceptive state from the current state, but reduced insula activation to aversive images relative to comparison subjects (Simmons, in prep). Taken together, these results are consistent with the hypothesis that elite performers deploy processing resources that are more focused on specific task demands, and they are better able to respond to external stimuli that perturb internal homeostasis. We examined the hypothesis that elite athletes, compared to control subjects, show attenuated insular cortex activation during an aversive interoceptive challenge
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