Cardio-audio synchronization elicits neural and cardiac surprise responses in human wakefulness and sleep

Abstract

The human brain can infer temporal regularities in auditory sequences with fixed sound-to-sound intervals and in pseudo-regular sequences where sound onsets are locked to cardiac inputs. Here, we investigated auditory and cardio-audio regularity encoding during sleep, when reduced vigilance may result in altered bodily and environmental stimulus processing. Using electroencephalography and electrocardiography in healthy volunteers (N=26) during wakefulness and sleep, we measured the response to unexpected sound omissions within three auditory regularity conditions: synchronous, where sound and heartbeat are temporally locked, isochronous, with fixed sound-to-sound intervals, and a control condition without specific regularity. During wakefulness and all sleep stages, the cardiac signal following sound omissions exhibited a deceleration over time in the synchronous condition only. At the neural level, both the synchronous and isochronous sequences gave rise to a neural omission response in wakefulness and N2 sleep. Regularity encoding in the synchronous and isochronous conditions was characterized by a modulation of the background oscillatory activity in N2 sleep, outlining a possible mechanism through which the brain aligns periods of high neuronal excitability to the expected sound onset. The violation of auditory and cardio-audio regularity elicits cardiac and neural surprise responses across vigilance stages. Significance StatementAcross vigilance states, the human brain can generate predictions about the future based on past sensory regularities. While this is evident for environmental stimuli, the role of bodily signals in forming sensory prediction remains unknown. Here, we show that the human brain utilizes the temporal relationship between cardiac and auditory inputs in order to anticipate upcoming sounds during wakefulness and sleep. After presenting sounds in synchrony with the ongoing heartbeat, a sound omission elicited both a heartbeat deceleration and a prediction error signal as measured by the electroencephalographic response. Heartbeat signals support auditory regularity encoding during sleep and wakefulness, highlighting one mechanism for optimizing the detection of unexpected stimuli by taking advantage of the continuously monitored cardiac signals.