DOI: 10.1113/jp290737 ISSN: 0022-3751

Breathing‐evoked potentials in humans during wakefulness and sleep

Léo Grassion, Thomas Andrillon, Marie‐Cécile Niérat, Nicolas Wattiez, Maxime Patout, Jessica Njlagni Voutsa, Delphine Oudiette, Isabelle Arnulf, Jésus Gonzalez‐Bermejo, Thomas Similowski

Abstract

Breathing modulates cortical activities and cognitive functions, but the neurophysiological basis of the brain–breathing relationship is incompletely understood. We aimed to determine whether breathing at rest evokes scalp EEG‐detectable potentials (as inspiratory occlusions do in the respiratory‐related evoked potential model), whether these signatures persist during sleep and whether they are linked to sleep‐organizing processes. We examined recordings from 729 participants in the Cleveland Family Study to identify cortical activity time‐locked to inspiration during wakefulness and sleep, with a median of 7871 respiratory cycles analysed per participant. Breathing‐related cortical responses were assessed in the time and frequency domains. Quiet breathing evoked a reproducible sequence of cortical potentials during wakefulness, including a pre‐inspiratory component ∼300 ms before inspiration and several post‐inspiratory peaks ≤3 s after. These responses persisted during non‐rapid eye movement stages 2 and 3 (N2 and N3) and rapid eye movement (REM) sleep, in which they showed simplified morphology resembling K‐complexes and co‐occurred with increased spindle‐range activity. The pattern was present irrespective of body mass index and was qualitatively unchanged in the 203 participants free of sleep‐disordered breathing, arguing against obesity or sleep apnoea as its origin. Scalp EEG can detect breathing‐evoked potentials during quiet breathing in awake humans. These potentials persist during sleep with a morphology that resembles cortical activities previously associated with sleep stabilization. Further studies are needed to determine the physiological and clinical significance of these observations in health and disease. image

Key points

Spontaneous breathing at rest evokes reproducible breathing‐related cortical potentials detectable with scalp EEG.

These potentials persist during sleep.

They are associated with time‐locked modulation of cortical oscillatory activity.

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