Respiration aligns perception with neural excitability.

Daniel S Kluger,Joachim Gross,Niko A Busch,Elio Balestrieri

doi:10.7554/elife.70907

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 behavior. We acquired respiration and human magnetoencephalography 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 versus undetected targets underscored the behavioral benefits of heightened excitability. Notably, respiration-locked excitability changes were maximized at a respiration phase lag of around -30° 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.

Highlights

Human respiration at rest is a continuous, rhythmic sequence of active inspiration and passive expiration (Fleming et al, 2011)
Whole-head MEG, and performance measures from thirty human participants in a spatial detection task to address the questions introduced earlier: First, we investigated whether respiration cyclically affects sensitivity towards near-threshold stimuli and how this link develops over the respiration cycle
Since the previous analysis had established a significant relationship between respiration and perceptual performance, we addressed the question if this relationship is mediated by a respiration-induced change of the individual psychometric function that relates stimulus contrast to perceptual performance

Summary

Introduction

Human respiration at rest is a continuous, rhythmic sequence of active inspiration and passive expiration (Fleming et al, 2011). While it is admittedly easier to imagine the high-frequency sniffing and whisking of mice as an active sampling of sensory stimuli, a similar case can be made for human respiration from the perspective of predictive processing (Mumford, 1992): In temporally coordinating the breathing act and internal brain dynamics (i.e., heightened excitability), the sampling of bottom-up sensory information can be aligned with top-down predictive streams (Arnal and Giraud, 2012) This active view of respiration is corroborated by reports that human participants spontaneously inhale at trial onset in a self-paced cognitive task (Perl et al, 2019), effectively aligning stimulus processing with the inspiration phase. We aimed to illuminate the overarching link between respiration-excitability and respiration-performance modulations

Results

Discussion

Methods