[en] 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.
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Bibliography
Dement, W., Wolpert, E.A., The relation of eye movements, body motility, and external stimuli to dream content. J. Exp. Psychol. 55 (1958), 543–553.
Rechtschaffen, A., Foulkes, D., Effect of visual stimuli on dream content. Percept. Mot. Skills 20 (1965), 1149–1160.
Berger, R.J., Experimental modification of dream content by meaningful verbal stimuli. Br. J. Psychiatry 109 (1963), 722–740.
Nir, Y., Tononi, G., Dreaming and the brain: from phenomenology to neurophysiology. Trends Cogn. Sci. 14 (2010), 88–100.
Issa, E.B., Wang, X., Sensory responses during sleep in primate primary and secondary auditory cortex. J. Neurosci. 28 (2008), 14467–14480.
Nir, 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 25 (2015), 1362–1378.
Perrin, F., García-Larrea, L., Mauguière, F., Bastuji, H., A differential brain response to the subject's own name persists during sleep. Clin. Neurophysiol. 110 (1999), 2153–2164.
Blume, 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 178 (2018), 638–648.
Strauss, 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 112 (2015), E1353–E1362.
Dement, W., Kleitman, N., The relation of eye movements during sleep to dream activity: an objective method for the study of dreaming. J. Exp. Psychol. 53 (1957), 339–346.
Goodenough, 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., 59, 1959, 295.
Ermis, U., Krakow, K., Voss, U., Arousal thresholds during human tonic and phasic REM sleep. J. Sleep Res. 19 (2010), 400–406.
Mesgarani, N., Chang, E.F., Selective cortical representation of attended speaker in multi-talker speech perception. Nature 485 (2012), 233–236.
O'Sullivan, J.A., Power, A.J., Mesgarani, N., Rajaram, S., Foxe, J.J., Shinn-Cunningham, B.G., Slaney, M., Shamma, S.A., Lalor, E.C., Attentional selection in a cocktail party environment can be decoded from single-trial EEG. Cereb. Cortex 25 (2015), 1697–1706.
Legendre, G., Andrillon, T., Koroma, M., Kouider, S., Sleepers track informative speech in a multitalker environment. Nat. Hum. Behav. 3 (2019), 274–283.
Spreng, L.F., Johnson, L.C., Lubin, A., Autonomic correlates of eye movement bursts during stage REM sleep. Psychophysiology 4 (1968), 311–323.
Arnulf, I., The ‘scanning hypothesis’ of rapid eye movements during REM sleep: a review of the evidence. Arch. Ital. Biol. 149 (2011), 367–382.
Bastuji, H., Perrin, F., Garcia-Larrea, L., Semantic analysis of auditory input during sleep: studies with event related potentials. Int. J. Psychophysiol. 46 (2002), 243–255.
Tamaki, M., Sasaki, Y., Surveillance during REM sleep for the first-night effect. Front. Neurosci., 13, 2019, 1161.
Sallinen, M., Kaartinen, J., Lyytinen, H., Processing of auditory stimuli during tonic and phasic periods of REM sleep as revealed by event-related brain potentials. J. Sleep Res. 5 (1996), 220–228.
Wehrle, R., Kaufmann, C., Wetter, T.C., Holsboer, F., Auer, D.P., Pollmächer, T., Czisch, M., Functional microstates within human REM sleep: first evidence from fMRI of a thalamocortical network specific for phasic REM periods. Eur. J. Neurosci. 25 (2007), 863–871.
McCormick, D.A., Bal, T., Sensory gating mechanisms of the thalamus. Curr. Opin. Neurobiol. 4 (1994), 550–556.
Esser, S.K., Hill, S., Tononi, G., Breakdown of effective connectivity during slow wave sleep: investigating the mechanism underlying a cortical gate using large-scale modeling. J. Neurophysiol. 102 (2009), 2096–2111.
Andrillon, T., Kouider, S., The vigilant sleeper: neural mechanisms of sensory (de) coupling during sleep. Curr. Opin. Physiol., 2019, 10.1016/j.cophys.2019.12.002 Published online 13 December 2019.
Ding, N., Simon, J.Z., Emergence of neural encoding of auditory objects while listening to competing speakers. Proc. Natl. Acad. Sci. USA 109 (2012), 11854–11859.
Hong, C.C.H., Fallon, J.H., Friston, K.J., Harris, J.C., Rapid eye movements in sleep furnish a unique probe into consciousness. Front. Psychol., 9, 2018, 2087.
Leclair-Visonneau, L., Oudiette, D., Gaymard, B., Leu-Semenescu, S., Arnulf, I., Do the eyes scan dream images during rapid eye movement sleep? Evidence from the rapid eye movement sleep behaviour disorder model. Brain 133 (2010), 1737–1746.
Doricchi, F., Iaria, G., Silvetti, M., Figliozzi, F., Siegler, I., The “ways” we look at dreams: evidence from unilateral spatial neglect (with an evolutionary account of dream bizarreness). Exp. Brain Res. 178 (2007), 450–461.
Hong, C.C.H., Harris, J.C., Pearlson, G.D., Kim, J.S., Calhoun, V.D., Fallon, J.H., Golay, X., Gillen, J.S., Simmonds, D.J., van Zijl, P.C.M., et al. fMRI evidence for multisensory recruitment associated with rapid eye movements during sleep. Hum. Brain Mapp. 30 (2009), 1705–1722.
Miyauchi, S., Misaki, M., Kan, S., Fukunaga, T., Koike, T., Human brain activity time-locked to rapid eye movements during REM sleep. Exp. Brain Res. 192 (2009), 657–667.
Andrillon, T., Nir, Y., Cirelli, C., Tononi, G., Fried, I., Single-neuron activity and eye movements during human REM sleep and awake vision. Nat. Commun., 6, 2015, 7884.
Ogawa, K., Nittono, H., Hori, T., Brain potentials before and after rapid eye movements: an electrophysiological approach to dreaming in REM sleep. Sleep 28 (2005), 1077–1082.
Siclari, F., Larocque, J.J., Postle, B.R., Tononi, G., Assessing sleep consciousness within subjects using a serial awakening paradigm. Front. Psychol., 4, 2013, 542.
Stickgold, R., Malia, A., Fosse, R., Propper, R., Hobson, J.A., Brain-mind states: I. Longitudinal field study of sleep/wake factors influencing mentation report length. Sleep 24 (2001), 171–179.
Siclari, F., Baird, B., Perogamvros, L., Bernardi, G., LaRocque, J.J., Riedner, B., Boly, M., Postle, B.R., Tononi, G., The neural correlates of dreaming. Nat. Neurosci. 20 (2017), 872–878.
Chow, H.M., Horovitz, S.G., Carr, W.S., Picchioni, D., Coddington, N., Fukunaga, M., Xu, Y., Balkin, T.J., Duyn, J.H., Braun, A.R., Rhythmic alternating patterns of brain activity distinguish rapid eye movement sleep from other states of consciousness. Proc. Natl. Acad. Sci. USA 110 (2013), 10300–10305.
Llinás, R.R., Paré, D., Of dreaming and wakefulness. Neuroscience 44 (1991), 521–535.
Formby, D., Maternal recognition of infant's cry. Dev. Med. Child Neurol. 9 (1967), 293–298.
Obin, N., MeLos: analysis and modelling of speech prosody and speaking style. PhD thesis (Université Pierre et Marie Curie - Paris VI). 2011.
Oostenveld, R., Fries, P., Maris, E., Schoffelen, J.M., FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput. Intell. Neurosci., 2011, 2011, 156869.
Delorme, A., Makeig, S., EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 134 (2004), 9–21.
Krekelberg, K., bayesFactor. 2019 GitHub https://www.github.com/klabhub/bayesFactor.
Iber, C., Iber, C., The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications. Volume 1, 2007, American Academy of Sleep Medicine.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.