The brain selectively tunes to unfamiliar voices during sleep

Abstract

The 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 of sleep. We detected K-complexes, sleep spindles, and micro-arousals, and then assessed event-related potentials, oscillatory power as well as inter-trial 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.

Item-specific memory reactivation during sleep supports memory consolidation in humans

“…The copyright holder for this preprint this version posted January 26, 2023. ; https://doi.org/10.1101/2023.01.25.525599 doi: bioRxiv preprint process meaningful auditory stimuli such as participants' own names (Perrin et al, 1999), voices (Ameen et al, 2022), lexical sounds (Kouider et al, 2014), continuous speech (Legendre et al, 2019), and new semantic associations (Xia et al, 2022;Züst et al, 2019). At the neural level, auditory stimulation during NREM sleep is manifested by increased EEG power in both the lowfrequency range (2-10 Hz) and sigma band (11-16 Hz) immediately following auditory stimuli (Andrillon et al, 2016;Wislowska et al, 2022).…”

“…For example, non-human primate and rodent studies have shown that the neuronal responses of the primary auditory cortex are well preserved during sleep with little modulation by different vigilance states (Issa & Wang, 2008; Nir et al, 2015). Human research shows that the sleeping brain can process meaningful auditory stimuli such as participants’ own names (Perrin et al, 1999), voices (Ameen et al, 2022), lexical sounds (Kouider et al, 2014), continuous speech (Legendre et al, 2019), and new semantic associations (Xia et al, 2022; Züst et al, 2019). At the neural level, auditory stimulation during NREM sleep is manifested by increased EEG power in both the low-frequency range (2-10 Hz) and sigma band (11-16 Hz) immediately following auditory stimuli (Andrillon et al, 2016; Wislowska et al, 2022).…”

Item-specific memory reactivation supports overnight memory consolidation

“…For example, non-human primate and rodent studies have shown that the neuronal responses of the primary auditory cortex are well preserved during sleep with little modulation by different vigilance states 42,43 . Human research shows that the sleeping brain can process meaningful auditory stimuli such as participants' own names 44 , voices 45 , lexical sounds 46 , continuous speech 47 , and new semantic associations 48,49 . At the neural level, auditory stimulation during NREM sleep is manifested by increased EEG power in both the low-frequency range (2-10 Hz) and sigma band (11-16 Hz) immediately following auditory stimuli 34,50 .…”