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

Universidad Europea de Madrid, Spain
PLoS ONE (Impact Factor: 3.23). 02/2012; 7(1):e29394. DOI: 10.1371/journal.pone.0029394
Source: PubMed


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.
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 inspiratory breathing load.
These 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.

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    • "In particular, aversive body state signals may reduce an individual's propensity to engage in risky activities such as drug use. In comparison, engaging in risky activities such as drug taking may result from attenuated insular processing of potentially aversive states, which—in turn—results in inadequate cognitive control modulation implemented by DLPFC (Paulus et al., 2009; Verdejo-Garcia & Bechara, 2009; Verdejo-Garcia et al., 2012). As of yet, however, few studies have employed interoceptive manipulations to examine neural changes as a function of stages of stimulant use. "
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    ABSTRACT: Inability to appropriately process afferent interoceptive stimuli may contribute to initiation and/or escalation of substance use. An aversive interoceptive stimulus probed neural processing in problem stimulant users (PSU; n = 19), 18 desisted stimulant users (DSU; n = 18), and healthy comparison subjects (CTL; n = 21). Participants completed a continuous performance task while they anticipated and experienced 40 cm H2O/L/sec inspiratory breathing loads during fMRI. PSU exhibited lower left dorsolateral prefrontal cortex and inferior frontal gyrus (IFG) activation than DSU and CTL across trials. Greater lifetime drug use due to stimulants was also linked to lower activation in these regions. In addition, PSU displayed lower right IFG and insula activation during breathing load than DSU and CTL. Findings suggest that transition to stimulant use disorders is marked by weakened attentional salience of aversive stimuli.
    Psychophysiology 10/2014; 52(2). DOI:10.1111/psyp.12303 · 2.99 Impact Factor
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    • "ator of feelings of " fatigue " and " effort " ( Amann et al . 2010 ; Hilty et al . 2011 ) . Individuals who are more aware of their homeostatic condition self - regulate their energy consumption more efficiently , and highly trained ath - letes and warriors use interoceptive sensory activity to produce optimal performance ( Herbert et al . 2007 ; Paulus et al . 2010 ; 2012 ) ."
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    ABSTRACT: Kurzban et al. make a convincing case against the idea that willpower is a depleting resource. However, they do not advance a positive account of willpower. Rather than treating “willpower” as a synonym of “executive function,” we argue that the term willpower should be designated for mechanisms individuals deploy to reduce dynamic inconsistency in their behavior.
    Behavioral and Brain Sciences 12/2013; 36(6):700-1. DOI:10.1017/S0140525X1300112X · 20.77 Impact Factor
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    • "A twochoice prediction task with fluctuating error rates was employed to examine decision making in response to rewarding, uncertain, and punishing outcomes. In addition, an inspiratory breathing load shown to activate insula and PFC during decision making was used as an aversive interoceptive manipulation (Paulus et al., 2012) during the two-choice prediction task. Five specific hypotheses were tested in this investigation. "
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    ABSTRACT: Problems associated with stimulant use have been linked to frontocingulate, insular, and thalamic dysfunction during decision making and alterations in interoceptive processing. However, little is known about how interoception and decision making interact and contribute to dysfunctions that promote the transition from recreational drug use to abuse or dependence. Here, we investigate brain activation in response to reward, punishment, and uncertainty during an aversive interoceptive challenge in current and former stimulant (cocaine and amphetamine) users using functional magnetic resonance imaging (fMRI). Young adults previously identified as recreational users (n = 184) were followed up 3 years later. Of these, 18 individuals progressed to problem stimulant use (PSU), whereas 15 desisted stimulant use (DSU). PSU, DSU, and 14 healthy comparison subjects (CTL) performed a two-choice prediction task at three fixed error rates (20% = reward, 50% = uncertainty, 80% = punishment) during which they anticipated and experienced episodes of inspiratory breathing load. Although groups did not differ in insula activation or subjective breathing load ratings, PSU exhibited lower right inferior frontal gyrus (IFG) and bilateral anterior cingulate (ACC) activation than DSU and CTL during aversive interoceptive processing as well as lower right IFG in response to decision making involving uncertainty. However, PSU exhibited greater bilateral IFG activation than DSU and CTL while making choices within the context of punishing feedback, and both PSU and DSU showed lower thalamic activation during breathing load than CTL. Findings suggest that frontocingulate attenuation, reflecting reduced resources devoted to goal maintenance and action selection in the presence of uncertainty and interoceptive perturbations, may be a biomarker for susceptibility to PSU.
    Frontiers in Systems Neuroscience 11/2013; 7:89. DOI:10.3389/fnsys.2013.00089
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