Breathing in Waves: Understanding Respiratory-Brain Coupling as a Gradient of Predictive Oscillations

Abstract

Breathing exerts significant influence on perceptual and cognitive processes by modulating the amplitude and synchronisation of neural oscillations. Previous studies report that respiratory rhythms control an array of behavioural effects spanning cognitive, affective, and perceptual domains. Similarly, respiratory modulated brain oscillations have been reported in multiple mammalian model systems and across a variety of frequency profiles. However, an overarching framework for understanding these diverse phenomena is still missing. Here, we integrate these findings to propose a neural gradient of respiratory modulated brain oscillations. We further review recent computational models of neural oscillations to map breath-brain interaction onto a hierarchical cascade of precision weighted prediction errors. Understanding the computational mechanisms underlying respiratory control of these processes may offer new avenues for targeted intervention in respiratory-brain and psychiatric disorders.

Respiratory modulations of cortical excitability and interictal spike timing in focal epilepsy - a case report

“…In a non-clinical context, we and others have previously discussed such pH-related changes as one potential driver of respiration-related modulations in neural activity [33,34]. At this point, mechanistic considerations are critically informed by the distinction of nasal vs oral breathing pathways: Respiratory coupling of neural oscillations is dependent on initial oscillatory activity in the olfactory bulb (see [23]), as evident from the absence of coupling in bulbectomised animals [35]. Accordingly, respiratory modulations of brain oscillations dissipate during oral breathing in humans [36].…”

“…One recurrent motif is the apparent systematic relationship between respiration and transient states of cortical excitability [20]. Extending previous findings of body-brain interactions in psychopathology (see [21] for review), there is an increasing number of accounts suggesting respiratory involvement in neuropsychiatric disorders [22,23]: By modulating disease-specific neural activity, respiration (and other physiological rhythms) may play a role in the course of certain disorders, particularly when they include alterations of excitability like schizophrenia or epilepsy.…”

The respiratory cycle modulates distinct dynamics of affective and perceptual decision-making

“…Other studies have found that inspiration increases the speed of emotional processing (Zelano et al, 2016), and that participants make more volitional movements during expiration (Park et al, 2020). These and many more recent reports suggest that respiratory rhythms play a fundamental role in shaping exteroceptive, affective (Bagur et al, 2021;Mizuhara & Nittono, 2023;Zelano et al, 2016), and cognitive behaviour (for reviews, see Allen et al, 2022;Azzalini et al, 2019;Braendholt et al, 2023;Heck et al, 2022).…”

“…The respiratory cycle modulates distinct dynamics Braendholt et al 2023 of affective and perceptual decision-making boundaries (e.g., reporting a happy or an angry face), and additional latencies not related to the decision process itself. Fitting this model to choices, reaction times, and respiratory states allowed us to investigate whether the observed coupling effects were most effectively accounted for by changes in the rate of evidence accumulation (drift rate, v), participants' biases towards particular with observed changes in speed and accuracy described above.…”

“…Indeed, until recently, breathing in the brain was thought to be largely constrained to basic processes concerning only the maintenance of respiratory drive and gas exchange (Heck et al, 2017;Herrero et al, 2017). This idea has recently been challenged by novel neurophysiological and behavioural discoveries (for reviews see, Allen et al, 2022;Braendholt et al, 2023). These studies have shown that respiratory rhythms drive alterations in both neural oscillations and behaviour across numerous tasks and animal models.…”