Sleepers Selectively Suppress Informative Inputs during Rapid Eye Movements

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 [1Dement W. Wolpert E.A. The relation of eye movements, body motility, and external stimuli to dream content.J. Exp. Psychol. 1958; 55: 543-553Crossref PubMed Scopus (207) Google Scholar, 2Rechtschaffen A. Foulkes D. Effect of visual stimuli on dream content.Percept. Mot. Skills. 1965; 20: 1149-1160Crossref PubMed Scopus (32) Google Scholar, 3Berger R.J. Experimental modification of dream content by meaningful verbal stimuli.Br. J. Psychiatry. 1963; 109: 722-740Crossref PubMed Scopus (64) Google Scholar]. While gating mechanisms might be at play to avoid interference on dreaming activity [4Nir Y. Tononi G. Dreaming and the brain: from phenomenology to neurophysiology.Trends Cogn. Sci. 2010; 14: 88-100Abstract Full Text Full Text PDF PubMed Scopus (311) Google Scholar], 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 [5Issa E.B. Wang X. Sensory responses during sleep in primate primary and secondary auditory cortex.J. Neurosci. 2008; 28: 14467-14480Crossref PubMed Scopus (81) Google Scholar, 6Nir Y. Vyazovskiy V.V. Cirelli C. Banks M.I. Tononi G. Auditory responses and stimulus-specific adaptation in rat auditory cortex are preserved across NREM and REM sleep.Cereb. Cortex. 2015; 25: 1362-1378Crossref PubMed Scopus (62) Google Scholar, 7Perrin F. García-Larrea L. Mauguière F. Bastuji H. A differential brain response to the subject’s own name persists during sleep.Clin. Neurophysiol. 1999; 110: 2153-2164Crossref PubMed Scopus (219) Google Scholar, 8Blume C. Del Giudice R. Wislowska M. Heib D.P.J. Schabus M. Standing sentinel during human sleep: continued evaluation of environmental stimuli in the absence of consciousness.Neuroimage. 2018; 178: 638-648Crossref PubMed Scopus (18) Google Scholar, 9Strauss M. Sitt J.D. King J.R. Elbaz M. Azizi L. Buiatti M. Naccache L. van Wassenhove V. Dehaene S. Disruption of hierarchical predictive coding during sleep.Proc. Natl. Acad. Sci. USA. 2015; 112: E1353-E1362Crossref PubMed Scopus (106) Google Scholar]. 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 [10Dement W. Kleitman N. The relation of eye movements during sleep to dream activity: an objective method for the study of dreaming.J. Exp. Psychol. 1957; 53: 339-346Crossref PubMed Scopus (509) Google Scholar, 11Goodenough D.R. Shapiro A. Holden M. Steinschriber L. A comparison of” dreamers” and” nondreamers”: Eye movements, electroencephalograms, and the recall of dreams.J. Abnorm. Soc. Psychol. 1959; 59: 295Crossref Scopus (58) Google Scholar], and their absence is associated with a lower arousal threshold to external stimuli [12Ermis U. Krakow K. Voss U. Arousal thresholds during human tonic and phasic REM sleep.J. Sleep Res. 2010; 19: 400-406Crossref PubMed Scopus (77) Google Scholar]. 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.

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