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

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.

Towards a three-dimensional framework of centrally regulated and goal-directed exercise behaviour: a narrative review

“…Supportive evidence for a crucial role of this putative pathway described above comes from increased activation of the IC after fatiguing cycling exercise,107 108 fatiguing handgrip task108 109 and during increased inspiratory breathing load 110. Interestingly, the subjective perceptions are more accurate and less aversive in elite athletes suggesting a critical role for the IC in the complex integration of physiological, affective and cognitive components underpinning exercise behaviour and performance 110.…”

“…Interestingly, the subjective perceptions are more accurate and less aversive in elite athletes suggesting a critical role for the IC in the complex integration of physiological, affective and cognitive components underpinning exercise behaviour and performance 110. Furthermore, non-invasive stimulation of the left temporal and insular cortices integrating predominantly information from the parasympathetic branch of the autonomic nervous system reduces heart rate and perceived exertion during submaximal, but not maximal, exercise intensities 111…”

Dyspnoea: a multidimensional and multidisciplinary approach

“…The affective processing of respiratory sensations is thought to involve a cortical pathway or pathways parallel to respiratory somatosensation; the responses are related to the type and quality of the respiratory afferent stimuli [15]. The affective processing responsible for the unpleasantness qualities implies the activation of limbic cortical structures for air hunger and work/effort [25][26][27][28][29]. Affective activation by respiratory stimuli can evoke distress and motivate cognitive behaviour.…”

Altered interoceptive activation before, during, and after aversive breathing load in women remitted from anorexia nervosa

“…We studied remitted participants to avoid confounding effects of malnutrition on neural function. The well-validated task has been shown to activate regions of the insula, PFC, striatum, and anterior cingulate (Berk et al 2015; Galli et al 2013; Paulus et al 2012; Stewart et al 2014). The majority of prior data from this paradigm suggest that less healthy or less resilient individuals tend to show reduced activation during anticipation and increased activation during breathing load (Berk et al 2015; Haase et al 2015; Haase et al 2016; Haase et al 2014; Paulus et al 2012; see Table S1 for summary).…”