Respiration aligns perception with neural excitability

Abstract

Recent studies from the field of interoception have highlighted the link between bodily and neural rhythms during action, perception, and cognition. The mechanisms underlying functional body-brain coupling, however, are poorly understood, as are the ways in which they modulate behaviour. We acquired respiration and human magnetoencephalography (MEG) data from a near-threshold spatial detection task to investigate the trivariate relationship between respiration, neural excitability, and performance. Respiration was found to significantly modulate perceptual sensitivity as well as posterior alpha power (8-13 Hz), a well-established proxy of cortical excitability. In turn, alpha suppression prior to detected vs undetected targets underscored the behavioural benefits of heightened excitability. Notably, respiration-locked excitability changes were maximised at a respiration phase lag of around -30 degrees and thus temporally preceded performance changes. In line with interoceptive inference accounts, these results suggest that respiration actively aligns sampling of sensory information with transient cycles of heightened excitability to facilitate performance.

Respiration, heartbeat, and conscious tactile perception

“…It is known that not only heart rate but also neural excitability changes during the respiratory cycle. In a recent study, the course of alpha power – known to be inversely related to excitability – across the respiratory cycle has been shown to have a minimum around expiration onset (Kluger et al, 2021) – the time period when in our study most stimuli were timed. Also for tactile stimuli, it has been shown that alpha power in central brain areas is related to conscious detection (Schubert et al, 2009; Nierhaus et al, 2015; Craddock et al, 2017; Forschack et al, 2020; Stephani et al, 2021).…”

Respiratory Rhythms of the Predictive Mind

“…While the neural mechanisms supporting the control of respiration have been studied extensively, the potential for respiratory rhythms to influence other domains of neural processing has largely been overlooked. Now, a rapidly growing number of studies demonstrate that respiration directly influences rhythmic brain activity to reshape neural activity and modulate behavior across sensory, affective, and cognitive domains [3][4][5][6][7][8][9][10][11][12].…”

“…These studies find, for example, that participants align the rhythm of respiration to the onset of exteroceptive stimuli [10], and that breath-by-breath parameters such as respiratory phase (see Glossary) modulate performance [3,5,9,13]. Neurophysiologically, respiratory rhythms exert a global, heterogenous influence on neuronal oscillations across all major brain frequencies, with a dominant role for hippocampal theta and sharp wave ripples, prefrontal alpha, and high-frequency gamma oscillations in primary sensory cortices [8,11,12].…”

“…Psychologically, we propose that this global mechanism helps to align local neural oscillations with endogenous, breath-driven fluctuations in neural excitation to improve goal-oriented cognition and perceptual target detection [9]. As such, the breath-by-breath control of noradrenaline further modulates the precision of prediction and prediction error signals in a non-specific fashion throughout the brain, and proffers a putative mechanistic explanation of effects whereby perceptual sensitivity or memory encoding varies as a function of the respiratory cycle [3][4][5].…”

“…Respiration via its influence on neuronal excitability and neuronal oscillations is likely to influence the brain's functional connectome at multiple time-scales. At shorter intervals, respiration modulates neuronal excitability and the power of neuronal oscillations including gamma oscillations [9,11,25], both of which have been linked to alterations in synaptic plasticity [98,99], suggesting that breathing can contribute to sustained changes in network topology and neurotransmission. The breath-by-breath modulation of locus coeruleus activity by respiration presents another route by which respiratory patterns can alter both sustained state-based neural activity and evoked responses to environmental stimuli [24].…”