Breathing-evoked potentials in humans during wakefulness and sleep

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. 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.