From pigeon holes to descending spirals: a paradigm of physiology, cognitive performance and behaviour in extreme environments

Abstract

Few physiologists dedicate their research careers to understanding the crucial integration between physiology, cognitive science, psychology and behaviour. Even whole-body integrative human physiologists do not often go as far as including the brain and cognition performance. Has the tradition of reductionist learning, within increasing specialisation (‘pigeon-holing’) meant that we have lost sight of a critical bigger picture? In separating physiology from cognition, we risk missing the impact of cognitive impairment and behavioural change on the subsequent physiological state. The first major organ to be deleteriously affected by hypoxia, hypoand hyperthermia is the brain. Executive function, memory and decision-making become impaired and risk-taking behaviour is altered, often resulting in greater physiological strain. This ‘descending spiral’, or deleterious feedback loop is under-researched by physiologists, but given the environments in which these situations occur it can pose mortal risk. Here, we consider a paradigm (Figure 1) developed to demonstrate how, as Da Vinci described it, ‘everything connects to everything else’ when humans are exposed to an extreme environment such as terrestrial altitude or reduced oxygen. It is well established that the brain, in particular the centres responsible for cardiorespiratory control, responds rapidly to homeostatic perturbations such as hypoxia (Bailey et al., 2009; Gibbons et al., 2020) and increases or decreases in temperature (Caldwell et al., 2020; Gibbons et al, 2020, 2021). In turn, the subsequent detrimental effects of hypoxia on cognitive performance have also been well-studied (see McMorris et al., 2017 and Ando et al., 2020 for a review). This decrement appears to occur regardless of the type of cognitive task(s) examined, e.g., central executive, non-central executive, perception/attention, or short-term working memory. It also appears likely that the arterial partial pressure of oxygen (PaO2 ) is the key predictor of the change in cognitive performance (McMorris et al., 2017). This hypothesis is corroborated by recent work demonstrating that reductions in cerebral oxygenation and peripheral oxygen saturation are correlated with the decrease in cognitive performance during normobaric hypoxia (Williams et al., 2019). However, the exact aetiology or physiological mechanism(s) responsible for a reduction in cognitive performance following hypoxia have yet to be fully elucidated. Some of the proposed mechanisms for a decrement in cognitive performance after acute (<2 h) hypo-