The brain selectively tunes to unfamiliar voices during sleep

AbstractThe brain continues to respond selectively to environmental stimuli even during sleep. However, the functional role of such responses, and whether they reflect information processing or rather sensory inhibition is not fully understood.Here, we presented 17 human sleepers (14 females) with their own name and two unfamiliar first names, spoken by either a familiar voice (FV) or an unfamiliar voice (UFV), while recording polysomnography during a full night’s sleep. We detected K-complexes, sleep spindles, and micro-arousals, and then assessed event-related potentials, oscillatory power as well as intertrial phase synchronization in response to the different stimuli presented during non-rapid eye movement (NREM) sleep.We show that UFVs evoke more K-complexes and micro-arousals than FVs. When both stimuli evoke a K-complex, we observed larger evoked potentials, higher oscillatory power in the high beta (>16Hz) frequency range, and stronger time-locking in the delta band (1-4 Hz) in response to UFVs relative to FVs. Crucially, these differences in brain responses disappear when no K-complexes are evoked by the auditory stimuli.Our findings highlight discrepancies in brain responses to auditory stimuli based on their relevance to the sleeper and propose a key role for K-complexes in the modulation of sensory processing during sleep. We argue that such content-specific, dynamic reactivity to external sensory information enables the brain to enter a ‘sentinel processing mode’ in which it engages in the many important processes that are ongoing during sleep while still maintaining the ability to process vital information in the surrounding.Significance statementPrevious research has shown that sensory processing continues during sleep. Here, we studied the capacity of the sleeping brain to extract and process relevant sensory information. We presented sleepers with their own names and unfamiliar names spoken by either a familiar (FV) or an unfamiliar voice (UFV). During non-rapid eye movement (NREM) sleep, UFVs elicited more K-complexes and micro-arousals than FVs. By contrasting stimuli which evoked K-complexes, we demonstrate that UFVs triggered larger evoked potentials, stronger time-locking in the delta (1-4Hz) band, and higher oscillatory power (>16Hz) relative to FVs. These differences in brain responses disappeared when no K-complexes were evoked. Our results suggest a pivotal role for K-complexes in the selective processing of relevant information during NREM sleep.