Subjecting Elite Athletes to Inspiratory Breathing Load Reveals Behavioral and Neural Signatures of Optimal Performers in Extreme Environments

Background: It 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 Findings: Elite 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 inspirator

Personality and symptom assessment of elite athletes and comparison subjects.

<p>Personality and symptom assessments show that elite athletes score higher on sensation seeking and perseverance than comparison subjects.</p

Main effect of task, i.e. brain changes as a consequence of inspiratory breathing load in both comparison subjects and elite athletes.

<p>Activation increases primarily during the breathing load and post-breathing load condition.</p

Group×Task Interaction, right middle insula showed significantly greater activation during breathing load and post-breathing load condition in comparison subjects relative to elite athletes.

<p>Group×Task Interaction, right middle insula showed significantly greater activation during breathing load and post-breathing load condition in comparison subjects relative to elite athletes.</p

Task by group interaction: Elite athletes relative to comparison subjects differentially activated the right insula cortex.

<p>Volume (µL), center of mass coordinate, and brain area based on the voxel-wise mixed model task by group interaction. There were significant differences in the right insula cortex between adventure racers and comparison subjects.</p

Visual Analog Rating during Baseline (no load) and 40 cm H2O/L/sec inspiratory breathing load in comparison subjects and elite athletes, respectively.

<p>Both groups showed increased unpleasantness during the 40 cm H2O/L/sec load condition.</p

Behavioral performance (latency and accuracy) during the continuous performance task in both comparison subjects and athletes (left) and separately for each group (right).

<p>Behavioral performance (latency and accuracy) during the continuous performance task in both comparison subjects and athletes (left) and separately for each group (right).</p

Main effect of breathing restriction on brain activation in comparison subjects and elite athletes.

<p>Volume (µL), center of mass coordinate, and brain area based on the voxel-wise mixed model main effect of breathing load. These areas showed brain activation related to loaded breathing for both comparison subjects and elite athletes.</p