Subjecting elite athletes to inspiratory breathing load reveals behavioral and neural signatures of optimal performers in extreme environments

“Several personality and symptom assessment questionnaires were administered including the Sensation Seeking Scale [34], the Barratt Impulsiveness Scale [BIS-11, 35], the Brief Symptom Inventory (BSI), a brief psychological self-report symptom scale [36], and the Connor Davidson Resiliency Scale CD-RISC [37].”

“All subject-level structural and functional image processing was done with the Analysis of Functional Neuroimages (AFNI) software package [40].”

“[6] within the context of ongoing activities, and the initiation of”

“Several personality and symptom assessment questionnaires were administered including the Sensation Seeking Scale [34], the Barratt Impulsiveness Scale [BIS-11, 35], the Brief Symptom Inventory (BSI), a brief psychological self-report symptom scale [36], and the Connor Davidson Resiliency Scale CD-RISC [37].”

“condition of the body [5], the representation of this internal state”

“leading to altered error processing in the anterior cingulate”

“The relationship between self-rated unpleasantness and the degree of activation in ventral anterior cingulate, left anterior insular and lateral inferior frontal gyrus supports the notion that brain structures which are important for regulating subjective mood states [54,55] are also critical for modulating optimal pe…”

“To that end, a 0–1 reference function of the particular time interval was convolved with a gamma variate function [44] modeling a prototypical hemodynamic response (6–8 second delay [45]) and to account for the temporal dynamics of the hemodynamic response (typically 12–16 seconds) [46].”

“The relationship between self-rated unpleasantness and the degree of activation in ventral anterior cingulate, left anterior insular and lateral inferior frontal gyrus supports the notion that brain structures which are important for regulating subjective mood states [54,55] are also critical for modulating optimal pe…”

“These investigators have argued that the a centrally generated corollary discharge of the brain is critical for optimal effort [70], and that mental fatigue affects performance via altered perception of effort rather than afferent and body originating cardiorespiratory and musculoenergetic mechanisms [71].”

“Finally, it is also unclear whether optimal performers generate different learning signals (similar to reward prediction error [64]), as part of the interactions between the insula and the basolateral amygdala [65] and the ventral striatum [66].”

“Since the insula cortex is important in generating body prediction errors [33], then one would hypothesize that elite athletes show attenuated neural processing in the insular cortex of afferent aversive interoceptive stimuli.”

“This notion is consistent with findings that elite athletes pay close attention to bodily signals [9] and may be particularly adept in generating anticipatory prediction errors [10].”

“Optimal performers are able to more quickly adapt to both bottom-up interoceptive afferents and top-down cognitive control brain areas that modulate mood and anxiety [67] in regulating one’s response to an aversive interoceptive perturbation.”

“Optimal performers may generate different context-dependent valuation of the interoceptive states within the orbitofrontal cortex [60] leading to altered error processing in the anterior cingulate [61] and selection of different actions [62].”

“To that end, a 0–1 reference function of the particular time interval was convolved with a gamma variate function [44] modeling a prototypical hemodynamic response (6–8 second delay [45]) and to account for the temporal dynamics of the hemodynamic response (typically 12–16 seconds) [46].”

“To that end, a 0–1 reference function of the particular time interval was convolved with a gamma variate function [44] modeling a prototypical hemodynamic response (6–8 second delay [45]) and to account for the temporal dynamics of the hemodynamic response (typically 12–16 seconds) [46].”

“As pointed out by others, this approach may help to explain sporting skill at the highest levels of performance [1].”

“Recently this model has been extended by Tucker and colleagues [11] based on prior formulations by Hampson [12].”

“In addition to chemoreceptors that form reflex feedback mechanisms for respiratory motor activities [16], breathing is also influenced by internal and external environmental changes, which is termed behavioral breathing.”

“Therefore, both insula and anterior cingulate may process the individual’s sense of effort or exertion with and without the need for peripheral afferents [49].”

“The multivariate regressor approach detailed below was used to relate changes in EPI intensity to differences in task characteristics [41].”

“Specifically, an individual’s expectation of effort perception during exercise is the basis for an ongoing interpretation of perceived exertion, and is due to both efferent feed-forward and afferent feedback signals [12].”

“contribute to athletic performance [49,50].”

“This has been shown to increase power in detecting task-related activation [43].”

“Finally, it is also unclear whether optimal performers generate different learning signals (similar to reward prediction error [64]), as part of the interactions between the insula and the basolateral amygdala [65] and the ventral striatum [66].”

“The subjects were asked to rate their experience on a 10 cm Visual Analog Scale which was anchored from ‘‘not at all’’ to ‘‘extremely’’ on the following 16 dimensions: pleasant; unpleasant; intense; tingling; fear of losing control; faintness; fear of dying; unreality; hot/cold flushes; trembling; choking; abdominal d…”

“Consistent with this idea, Williamson and colleagues suggest that the neural circuitry underlying central regulation of performance includes the insular and anterior cingulate cortex that interact with thalamic and brainstem structures which are important for cardiovascular integration [49] as well as for the central…”

“Several personality and symptom assessment questionnaires were administered including the Sensation Seeking Scale [34], the Barratt Impulsiveness Scale [BIS-11, 35], the Brief Symptom Inventory (BSI), a brief psychological self-report symptom scale [36], and the Connor Davidson Resiliency Scale CD-RISC [37].”

“These investigators found that under these conditions, changes in rCBF in left and right insular cortex as well as anterior cingulate cortex correlated with perceived exertion, but not with changes in heart rate or blood pressure [56].”

“observed during active, but not passive, cycling [52].”

“perceived cycling intensity [53] and with individual blood pressure”

“, via contextual associations from memory), which are processed in insular cortex via connections to temporal and parietal cortex to generate body states based on conditioned associations [58].”

“Measures of mood states have been used to predict athletic injury [48], but much less is known about the central nervous system contribution to optimal performance.”

“Optimal performers may generate different context-dependent valuation of the interoceptive states within the orbitofrontal cortex [60] leading to altered error processing in the anterior cingulate [61] and selection of different actions [62].”

“The basic experimental approach was similar to that of a recently published study by our group involving human touch [39].”

“We have previously proposed that optimal performance may be related to the ability to effectively minimize the body prediction error [8], which allows individuals to better adjust to environmental perturbations.”

“EPI images were co-registered using a 3Dcoregistration algorithm [42] that was developed to minimize the amount of image translation and rotation relative to all other images.”

“Finally, it is also unclear whether optimal performers generate different learning signals (similar to reward prediction error [64]), as part of the interactions between the insula and the basolateral amygdala [65] and the ventral striatum [66].”

“Optimal performers may also differentially integrate interoceptive states within the insular cortex (which shows a clear gradient from the dorsal-posterior to ventral-anterior part) to provide an increasingly ‘‘contextualized’’ representation of the interoceptive state [59].”

“Moreover, resistive loads generate pre-motor potentials that reflect the involvement of higher cortical motor areas [27], they decrease systolic blood pressure [28], they differ for males and females [29], they are perceived less intense in older individuals [30], they generate load-dependent increases of unpleasantne…”

“These sensations are the result of both subcortical and cortical processes [18], which include discriminative processing (the awareness of the spatial, temporal and intensity components of the respiratory input) and affective processing (the evaluative and emotional components of the respiratory input).”

“restricted inspiration, was first introduced by Lopata [19] and Gottfried [20], and is an airflow-dependent load [21] and a simple but powerful experimental approach to induce an altered interoceptive state.”

“comparison subjects [3].”

“These results are consistent with those of Hilty and colleagues [63] who reported that individuals who perform a handgrip exercise prior to task failure show increased activation in both the mid/anterior insular cortex and the thalamus.”

“Inspiratory breathing loads can be used to examine breathing difficulty and generate respiratoryrelated evoked potentials with several peaks that indicate the transition from an early sensory component to a later cognitive aspect [23,24,25,26].”

“The subjects were asked to rate their experience on a 10 cm Visual Analog Scale which was anchored from ‘‘not at all’’ to ‘‘extremely’’ on the following 16 dimensions: pleasant; unpleasant; intense; tingling; fear of losing control; faintness; fear of dying; unreality; hot/cold flushes; trembling; choking; abdominal d…”

“Inspiratory breathing loads can be used to examine breathing difficulty and generate respiratoryrelated evoked potentials with several peaks that indicate the transition from an early sensory component to a later cognitive aspect [23,24,25,26].”

“Moreover, resistive loads generate pre-motor potentials that reflect the involvement of higher cortical motor areas [27], they decrease systolic blood pressure [28], they differ for males and females [29], they are perceived less intense in older individuals [30], they generate load-dependent increases of unpleasantne…”

“Inspiratory breathing loads can be used to examine breathing difficulty and generate respiratoryrelated evoked potentials with several peaks that indicate the transition from an early sensory component to a later cognitive aspect [23,24,25,26].”

“Resistive load, i.e. restricted inspiration, was first introduced by Lopata [19] and Gottfried [20], and is an airflow-dependent load [21] and a simple but powerful experimental approach to induce an altered interoceptive state.”

“Resistive load, i.e. restricted inspiration, was first introduced by Lopata [19] and Gottfried [20], and is an airflow-dependent load [21] and a simple but powerful experimental approach to induce an altered interoceptive state.”

“In this study we examine elite adventure racers who are non-military elite performers and who are often exposed to extreme environments [14].”

“Individuals participating in adventure racing experience significant physical and psychological stress during these competitions, which sometimes result in both significant injury and in mood-state disruption [13].”

“In contrast to expiratory breathing load which affects C02 [19], inspiratory breathing load results in stable, unchanged C02 levels [22].”

“In extension of the previous study that did not show performance accuracy or response latency differences between elite war fighters and comparison subjects [4], the current study shows that elite athletes demonstrate greater accuracy under challenging conditions.”

“Moreover, resistive loads generate pre-motor potentials that reflect the involvement of higher cortical motor areas [27], they decrease systolic blood pressure [28], they differ for males and females [29], they are perceived less intense in older individuals [30], they generate load-dependent increases of unpleasantne…”

“Moreover, resistive loads generate pre-motor potentials that reflect the involvement of higher cortical motor areas [27], they decrease systolic blood pressure [28], they differ for males and females [29], they are perceived less intense in older individuals [30], they generate load-dependent increases of unpleasantne…”

“This notion is consistent with findings that elite athletes pay close attention to bodily signals [9] and may be particularly adept in generating anticipatory prediction errors [10].”

“The sensation of breathing is a complex process that is modulated by numerous factors [15].”

“Moreover, resistive loads generate pre-motor potentials that reflect the involvement of higher cortical motor areas [27], they decrease systolic blood pressure [28], they differ for males and females [29], they are perceived less intense in older individuals [30], they generate load-dependent increases of unpleasantne…”

“To progress from a general description of interoceptive processing toward characterizing the wholesomeness of such processing requires a greater level of theoretical complexity, the beginnings to which we will attempt to address.”

“Studying the response of trained athletes and untrained volunteers to an aversive activity, Paulus et al. (2011) reported “profound” activation of the right and left insula, the dorsolateral prefrontal cortex, and the anterior cingulate gyrus in response to the unpleasant task.”

“With the exception of manipulations of inspiratory breathing load (Paulus et al., 2012), we presently lack non-invasive methods to do so, and new paradigms will need to be developed.”

“(19)], and a carbon dioxide inhalation task [as in Pine et al.”

“These include cardiac challenges with short-acting sympathomimetics (128), manipulating inspiratory breathing load or air composition (129,130), transcutaneous vagus nerve stimulation (131), baroreceptor stimulation (132), acute induction of in fl ammation by vaccination (133), or C-fi ber…”

“In the support of this proposal, we have previously shown that highly resilient individuals, such as elite adventure racers (Paulus et al., 2012) and US NAVY Sea, Air and Land Forces (Simmons et al.”

“The well-validated task has been shown to activate regions of the insula, PFC, striatum, and anterior cingulate (Paulus et al. 2012; Galli et al. 2013; Stewart et al. 2014; Berk et al. 2015).”

“For example, it appears that elite athletes, which have undergone extensive physical exercise have the ability to use predictive signals to modulate the insula response to an aversive interoceptive perturbation (127).”

“Given the assumed prominent role of the insular cortex in processing the affective qualities of perceived dyspnea [11, 16, 39, 40], we investigated the influence of brain activation during dyspnea anticipation on individual average right insular activation during the subsequent perception of resistiveload-induced dysp…”

“These areas of significant response are consistent with previous results using this task in healthy adults (for e.g., Paulus et al., 2012).”

“In humans, the involvement of this region of the insula in interoception is demonstrated in neuroimaging studies of direct visceral stimulation (Cameron, 2002; Paulus et al, 2012; Wang et al, 2008), as well as interoceptive attention to visceral signals (Simmons et al, 2013a).”

“This finding is supported by a recent study of an athlete population that revealed lower neural processing in the right insula during an aversive interoceptive event (Paulus et al., 2012).”

“This distinction is important to note because allocation of attention to continuously monitor the breath sensations promotes interoceptive and reappraisal-based processes.(2,9,14,26,27,32,36,43,60,61,63) Slow-breathing practices reliably reduce pain, 17, 47, 51, 82, 91 and endogenous opioids are engaged during volitio…”

“This could involve approaches like auricular (percutaneous or transcutaneous vagus nerve stimulation; 116), short-lived pharmacological (117) or immunological (118) interventions, or manipulations of cardiac and respiratory processes (119).”

“One could adopt a similar approach to evaluating respiratory interoception using different inspiratory breathing load perturbations (e.g., ranging from 5 to 40 cmH 2 O/l/s inspiratory resistance loads (as in [45]), or higher).”

“…present findings support the notion, that activation of the anterior insular cortex is particularly relevant for the perception of the affective dimension of aversive events in general (Seeley et al., 2007) and dyspnea unpleasantness in particular (von Leupoldt et al., 2008; Paulus et al., 2012).”

“Others include a change of serotonin concentration in the brain (2) or an insular processing loop proposed to regulate motor drive (3).”

“Whilst previous research had identified reduced anterior insula activity during loaded breathing in endurance athletes (Paulus et al., 2012), we have not reproduced these findings when employing more stringent fMRI statistics.”

“, 2010) and both ACC and DLPFC are active during interoceptive processing in healthy individuals, likely as a part of a monitoring and top-down inhibitory circuit regulating reactions to aversive stimuli (Critchley, Wiens, Rotschtein, Ohman, & Dolan, 2004; Paulus et al., 2012).”

“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.”

“The strength of activity in left insula has been previously associated with regulation of emotion and appetitive behavior (Craig, 2009; Kelly et al., 2012; Paulus et al., 2012).”

“Research has shown that all meditations included in mindfulness practices directly shape the anatomy and function of the insula and intero-ceptive network (IA) or salience network (SN) [23–26, 32, 40–45].”

“Paulus and colleagues [141] showed that adventure racing athletes have altered (insular) cortex activation during an aversive interoceptive challenge consisting of increased respiratory effort.”

“Recent research has highlighted a relationship between in-teroception and physical activity or experience level in sport athletes (Christensen, Gaigg, and Calvo-Merino 2018; Herbert, Ulbrich, and Schandry 2007; Li et al. 2021; Marcora 2008; Paulus et al. 2012, 2009; Wallman-Jones et al. 2022).”

“A breathing load of 40 cm H2O/L/s was selected based on previous research which has demonstrated that this load alters subjective symptoms without significantly affecting CO2 or O2 levels, and thereby does not impact the BOLD signal [48,49].”

“Inspiratorybreathing load is anaversiveexperience associated with activations of brain areas including bilateral insula, dorsolateral prefrontal cortex and ACC (Paulus et al., 2012; Stewart et al., 2015).”

“This experimental approach has been previously shown to effectively induce a substantial alteration in interoceptive state [2,5,6,21].”

“This level of resistance was chosen because of prior work demonstrating its effectiveness and feasibility [45]; we also con fi rmed that it induced moderate but tolerable (roughly 5 out of 10) levels of anxiety within our clinical sample in the initial sensitivity assessment (Supplementary Fig.”

“…reflected by the activation of insula as well as limbic activation, which is in accordance with the literature on the activation of insula (Paulus et al., 2010, 2012; Simmons et al., 2012) which reported more insula activation at the time of shifting from anticipating one emotion to…”

“Also, higher anterior insula activation was observed in the LR individuals in aversive interoceptive stimulus processing and emotion detection [15, 16].”

“Moreover, a recent study subjecting elite athletes to inspiratory breathing load revealed attenuated insular cortex activation (compared with controls) during and following the aversive interoceptive condition of inspiratory resistive load breathing (Paulus et al., 2012).”

“perior interoceptive function, which allows them to accurately anticipate and modulate the state of their bodies (11).”

“During one run of the task (counterbalanced order), participants were continuously exposed to a resistance level of 40 cmH2O/L/s, chosen to maintain a moderate (but tolerable) anxiety level (i.e., based on previous work using this paradigm [36] and con fi rmed by results of the sensitivity protocol).”

“…; Tracy et al., 2007; Yao et al., 2018 ; Zaki et al., 2012 ), followed by respiration/breathing ( n = 6; Farb et al., 2013 ; Haase et al., 2016 ; Paulus et al., 2012 ; Walter et al., 2020 ), gastrointestinal stimulation ( n = 5; Avery et al., 2015 ; Elsenbruch et al., 2010; Haruki & Ogawa, 2023…”

“Interestingly, our healthy controls reported lower resilience scores than other adult populations (72), which might explain the small but significant difference between people with IBD and healthy controls in the current study.”

“However, increasing body awareness and self-compassion during difficult experiences effectively reduces the negative impacts of stress [8, 9].”

“…RISC-10 scores reported are consistent with those of elite athletes and healthy U.S. adults (30.6 and 31.4, respectively) (Gonzalez et al., 2016; Paulus et al., 2012) as well as populations with frequent occupational stress, such as trauma surgeons (33.4) (Warren et al., 2013) and elevated…”