Abstract

Sleep leads to a disconnection from the external world. Even when sleepers regain consciousness during rapid eye movement (REM) sleep, little, if any, external information is incorporated into dream content [1-3]. While gating mechanisms might be at play to avoid interference on dreaming activity [4], a total disconnection from an ever-changing environment may prevent the sleeper from promptly responding to informative events (e.g., threat signals). In fact, a whole range of neural responses to external events turns out to be preserved during REM sleep [5-9]. Thus, it remains unclear whether external inputs are either processed or, conversely, gated during REM sleep. One way to resolve this issue is to consider the specific impact of eye movements (EMs) characterizing REM sleep. EMs are a reliable predictor of reporting a dream upon awakening [10, 11], and their absence is associated with a lower arousal threshold to external stimuli [12]. We thus hypothesized that the presence of EMs would selectively prevent the processing of informative stimuli, whereas periods of REM sleep devoid of EMs would be associated with the monitoring of external signals. By reconstructing speech in a multi-talker environment from electrophysiological responses, we show that informative speech is amplified over meaningless speech during REM sleep. Yet, at the precise timing of EMs, informative speech is, on the contrary, selectively suppressed. These results demonstrate the flexible amplification and suppression of sensory information during REM sleep and reveal the impact of EMs on the selective gating of informative stimuli during sleep.

Highlights

  • We first found that both informative speech and Jabberwocky speech could be reconstructed across wakefulness, light NREM sleep, and rapid eye movement (REM) sleep, revealing preserved auditory encoding across vigilance states (Figure 2A; p < 0.05 for all conditions corrected for multiple comparisons)

  • Participants were asked to focus only on informative speech and ignore Jabberwocky speech (Figure 1). They first performed this task in wakefulness and were allowed to sleep during a morning nap, at times of high rapid eye movement (REM) sleep pressure (STAR Methods)

  • When participants are instructed to focus only on the informative stream and enter non-REM (NREM) sleep, EEG markers reveal that informative speech is overall still enhanced, but it is suppressed during sleep slow waves, a hallmark of NREM sleep [15]

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Summary

Methods

METHOD DETAILSStimuli Stimuli used for this study were identical to Legendre and colleagues [15]. Eighty meaningful (informative) and meaningless (Jabberwocky) stories, i.e., texts for which content words (e.g., nouns and verbs) were replaced by French pseudo-words, and matched in length, syntax, word-frequency and phonemic properties. Using the IRCAMTRAX module of Logic Pro software (Apple), we manipulated the voice to generate two copies of each audio story, one pronounced by a low-pitched voice and one by a high-pitched voice. For the Training phase, the same text was played in both ears. For the Test phase, a pair of Jabberwocky and informative stories were played each in a different ear and in a different pitch. The side of the stimulation (left or right ear) and the pitch of the voice (low and high pitch) of the informative speech was randomized trial-by-trial and counterbalanced for each pair across participants. The volume of the stimulation was set around 50 dB and adapted to participant’s preferences, in line with previous studies [9, 15]

Results
Discussion
Conclusion
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