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. While gating mechanisms might be at play to avoid interference on dreaming activity, a total disconnection would prevent the sleeper from promptly responding to informative events (e.g., threat signals). In fact, a whole range of neural responses to external events are preserved, at least partially, during REM sleep. Thus, it remains unsettled whether external inputs are either integrated or conversely gated during REM sleep. Here, we sought to disentangle this issue by studying the impact of eye movements (EMs) on the processing of informative signals. EMs constitute a reliable predictor of reporting a dream upon awakening and induce a higher arousal threshold to external stimuli. We hypothesized that although sleepers might continue responding to external events, periods of EMs would be associated with the gating of informative signals in order to reduce interference with dreaming activity. By reconstructing perceived speech in a multi-talker, cocktail-party environment from electrophysiological responses, we show that informative speech is selectively amplified over meaningless speech during REM sleep. However, we show that at the precise timing of EMs, informative speech is, on the contrary, selectively suppressed. Importantly, this suppression did not affect the processing of non-informative signals, revealing a selective mechanism of gating for informative contents rather than a general decline in sensory encoding. These results reveal flexible mechanisms of amplification/suppression of external inputs during REM sleep, and demonstrate the impact of EMs on the selective gating of informative stimuli.
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)
We found that informative speech and Jabberwocky speech are differently affected across wakefulness and REM sleep (t(677.35) = À4.41, p < 0.001 for the interaction informative versus Jabberwocky 3 wake versus REM sleep)
Such results are consistent with previous reports showing that responses to auditory stimulation and deviant tones are reduced in the presence of eye movements (EMs) during REM sleep [20, 21], as well as the elevation of arousal thresholds during phasic compared to tonic REM sleep [12]
Summary
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]
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