[en] Falling asleep is a dynamical process that is poorly defined. The period preceding sleep, characterized by the progressive alteration of behavioral responses to the environment, which may last several minutes, has no electrophysiological definition, and is embedded in the first stage of sleep (N1). We aimed at better characterizing this drowsiness period looking for neurophysiological predictors of responsiveness using electro and magneto-encephalography. Healthy participants were recorded when falling asleep, while they were presented with continuous auditory stimulations and asked to respond to deviant sounds. We analysed brain responses to sounds and markers of ongoing activity, such as information and connectivity measures, in relation to rapid fluctuations of brain rhythms observed at sleep onset and participants' capabilities to respond. Results reveal a drowsiness period distinct from wakefulness and sleep, from alpha rhythms to the first sleep spindles, characterized by diverse and transient brain states that come on and off at the scale of a few seconds and closely reflects, mainly through neural processes in alpha and theta bands, decreasing probabilities to be responsive to external stimuli. Results also show that the global P300 was only present in responsive trials, regardless of vigilance states. A better consideration of the drowsiness period through a formalized classification and its specific brain markers such as described here should lead to significant advances in vigilance assessment in the future, in medicine and ecological environments.
Disciplines :
Radiology, nuclear medicine & imaging Neurosciences & behavior
Author, co-author :
Strauss, Mélanie; Cognitive Neuroimaging Unit, CEA DSV/I2BM, INSERM, NeuroSpin Center, Université Paris-Sud, Université Paris-Saclay, Gif-sur-Yvette, France, Neuropsychology and Functional Imaging Research Group (UR2NF), Center for Research in Cognition and Neurosciences (CRCN), Université Libre de Bruxelles, B-1050 Brussels, Belgium, Departments of Neurology, Psychiatry and Sleep Medicine, Cliniques Universitaires de Bruxelles, Hôpital Erasme, Université Libre de Bruxelles, B-1070 Brussels, Belgium. Electronic address: melanie.strauss@erasme.ulb.ac.be
Sitt, Jacobo D; Institut du Cerveau et de la Moelle épinière, ICM, PICNIC Lab, F-75013 Paris, France, Inserm U 1127, F-75013 Paris, France
Naccache, Lionel; Institut du Cerveau et de la Moelle épinière, ICM, PICNIC Lab, F-75013 Paris, France, Department of Neurophysiology, Hôpital de la Pitié-Salpêtrière, AP-HP, F-75013 Paris, France
Raimondo, Federico ; Université de Liège - ULiège > GIGA > GIGA Consciousness - Coma Science Group
Language :
English
Title :
Predicting the loss of responsiveness when falling asleep in humans.
We are grateful to Stanislas Dehaene for his essential support in data acquisition and for helpful comments, to Bernadette Martins and the Neurospin staff for administrative support, to nurses Laurence Laurier, Véronique Joly-Testault, and Gaëlle Mediouni for their help in recruitment and data acquisition and to Kaustubh Patil for his feedback on predictive modelling. This work was supported by grants from Institut National de la Santé et de la Recherche Médicale (INSERM) and Journées de Neurologie de Langue Française (to M.S.), Stic-Amsud “RTBRAIN” (to J.D.S.) and Wallonia-Bruxelles International IN Excellence Grant (to F.R.). The Neurospin MEG facility is sponsored by grants from INSERM, CEA, Fondation pour la Recherche Médicale, the Bettencourt-Schueller Foundation, and the Région île-de-France. This study was supported by the European Union's Horizon 2020 Research and Innovation Programme Grant Agreement No. 945539 (HBP SGA3).We are grateful to Stanislas Dehaene for his essential support in data acquisition and for helpful comments, to Bernadette Martins and the Neurospin staff for administrative support, to nurses Laurence Laurier, V?ronique Joly-Testault, and Ga?lle Mediouni for their help in recruitment and data acquisition and to Kaustubh Patil for his feedback on predictive modelling. This work was supported by grants from Institut National de la Sant? et de la Recherche M?dicale (INSERM) and Journ?es de Neurologie de Langue Fran?aise (to M.S.), Stic-Amsud ?RTBRAIN? (to J.D.S.) and Wallonia-Bruxelles International IN Excellence Grant (to F.R.). The Neurospin MEG facility is sponsored by grants from INSERM, CEA, Fondation pour la Recherche M?dicale, the Bettencourt-Schueller Foundation, and the R?gion i?le-de-France. This study was supported by the European Union's Horizon 2020 Research and Innovation Programme Grant Agreement No. 945539 (HBP SGA3). M.S. made contributions to the conception of the work, study design, data acquisition, analysis and interpretation, and have drafted the manuscript. J.D.S. and L.N. made contributions to the conception of the work, study design, and revised the manuscript. F.R. made contributions to the conception of the work, data analysis and interpretation, and have drafted the manuscript.
Abraham, A., Pedregosa, F., Eickenberg, M., Gervais, P., Mueller, A., Kossaifi, J., Gramfort, A., Thirion, B., Varoquaux, G., Machine learning for neuroimaging with scikit-learn. Front. Neuroinformatics, 8, 2014, 10.3389/fninf.2014.00014.
American Academy of Sleep Medicine Iber, C., The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications. 2007, American Academy of Sleep Medicine.
Andrillon, T., Burns, A., Mackay, T., Windt, J., Tsuchiya, N., Predicting lapses of attention with sleep-like slow waves. Nat. Commun., 12, 2021, 3657, 10.1038/s41467-021-23890-7.
Atienza, M., L Cantero, J., Gómez, C.M., The mismatch negativity component reveals the sensory memory during REM sleep in humans. Neurosci. Lett. 237 (1997), 21–24.
Bandt, C., Pompe, B., Permutation Entropy: A Natural Complexity Measure for Time Series. Phys. Rev. Lett., 88, 2002, 10.1103/PhysRevLett.88.174102 174102–174102.
Bareham, C.A., Manly, T., Pustovaya, O.V., Scott, S.K., Bekinschtein, T.A., Losing the left side of the world: Rightward shift in human spatial attention with sleep onset. Sci. Rep., 4, 2014, 10.1038/srep05092.
Bekinschtein, T.A., Dehaene, S., Rohaut, B., Tadel, F., Cohen, L., Naccache, L., Neural signature of the conscious processing of auditory regularities. Proc. Natl. Acad. Sci. 106 (2009), 1672–1677.
Bonnet, M.H., Moore, S.E., The threshold of sleep: Perception of sleep as a function of time asleep and auditory threshold. Sleep J. Sleep Res. Sleep Med. 5 (1982), 267–276.
Bourdillon, P., Hermann, B., Guénot, M., Bastuji, H., Isnard, J., King, J.-R., Sitt, J., Naccache, L., Brain-scale cortico-cortical functional connectivity in the delta-theta band is a robust signature of conscious states: an intracranial and scalp EEG study. Sci. Rep., 10, 2020, 10.1038/s41598-020-70447-7.
Buzsáki, G., Theta Oscillations in the Hippocampus. Neuron 33 (2002), 325–340, 10.1016/S0896-6273(02)00586-X.
Casagrande, M., De Gennaro, L., Violani, C., Braibanti, P., Bertini, M., A finger-tapping task and a reaction time task as behavioral measures of the transition from wakefulness to sleep: which task interferes less with the sleep onset process. Sleep 20 (1997), 301–312.
Chen, B., Sun, P., Fu, S., Consciousness modulates the automatic change detection of masked emotional faces: Evidence from visual mismatch negativity. Neuropsychologia, 107459, 2020, 10.1016/j.neuropsychologia.2020.107459.
Comsa, I.M., Bekinschtein, T.A., Chennu, S., Transient Topographical Dynamics of the Electroencephalogram Predict Brain Connectivity and Behavioural Responsiveness During Drowsiness. Brain Topogr, 2018, 10.1007/s10548-018-0689-9.
Dehaene, S., Changeux, J.-P., Experimental and Theoretical Approaches to Conscious Processing. Neuron 70 (2011), 200–227, 10.1016/j.neuron.2011.03.018.
Efron, Bradley, Tibshirani, Robert, An introduction to the bootstrap. 1994, Chapman & Hall.
Engemann, Denis A., Raimondo, F., King, J.-R., Rohaut, B., Louppe, G., Faugeras, F., Annen, J., Cassol, H., Gosseries, O., Fernandez-Slezak, D., Laureys, S., Naccache, L., Dehaene, S., Sitt, J.D., Robust EEG-based cross-site and cross-protocol classification of states of consciousness. Brain 141 (2018), 3179–3192, 10.1093/brain/awy251.
Engemann, Denis A, Raimondo, F., King, J.-R., Rohaut, B., Louppe, G., Faugeras, F., Annen, J., Cassol, H., Gosseries, O., Fernandez-Slezak, D., Laureys, S., Naccache, L., Dehaene, S., Sitt, J.D., Robust EEG-based cross-site and cross-protocol classification of states of consciousness. Brain 141 (2018), 3179–3192, 10.1093/brain/awy251.
Fischer, C., Morlet, D., Bouchet, P., Luaute, J., Jourdan, C., Salord, F., Mismatch negativity and late auditory evoked potentials in comatose patients. Clin. Neurophysiol. 110 (1999), 1601–1610, 10.1016/S1388-2457(99)00131-5.
Foulkes, D., Vogel, G., Mental Activity at Sleep Onset. J. Abnorm. Psychol. 70 (1965), 231–243.
Gibbs, F.A., Gibbs, joint author. Erna L. (Erna Leonhardt), 1950. Atlas of electroencephalography.
Goupil, L., Bekinschtein, T., Cognitive processing during the transition to sleep. Arch. Ital. Biol. 150 (2012), 140–154, 10.4449/aib.v150i2.1247.
Gramfort, A., Luessi, M., Larson, E., Engemann, D.A., Strohmeier, D., Brodbeck, C., Goj, R., Jas, M., Brooks, T., Parkkonen, L., Hämäläinen, M.S., MEG and EEG data analysis with MNE-Python. Front. Neurosci., 7, 2013, 10.3389/fnins.2013.00267 267–267.
Heinke, W., Kenntner, R., Gunter, T.C., Sammler, D., Olthoff, D., Koelsch, S., Sequential effects of increasing propofol sedation on frontal and temporal cortices as indexed by auditory event-related potentials. Anesthesiology 100 (2004), 617–625.
Hermans, L.W.A., Leufkens, T.R., van Gilst, M.M., Weysen, T., Ross, M., Anderer, P., Overeem, S., Vermeeren, A., Sleep EEG characteristics associated with sleep onset misperception. Sleep Med 57 (2019), 70–79, 10.1016/j.sleep.2019.01.031.
Hertig-Godeschalk, A., Skorucak, J., Malafeev, A., Achermann, P., Mathis, J., Schreier, D.R., Microsleep episodes in the borderland between wakefulness and sleep. Sleep zsz163, 2019, 10.1093/sleep/zsz163.
Hori, T., Changes of EEG patterns and reaction time during hypnagogic state. Sleep Res, 20, 1991, 20.
Hori, T., Hayashi, M., Morikawa, T., Topographical EEG changes and the hypnagogic experience. Ogilvie RD Harsh JR Ed. Sleep Onset Norm. Abnorm. Process. Wash. DC Am. Psychol. Assoc., 1994, 237–253.
Imperatori, L.S., Cataldi, J., Betta, M., Ricciardi, E., Ince, R.A.A., Siclari, F., Bernardi, G., Cross-participant prediction of vigilance stages through the combined use of wPLI and wSMI EEG functional connectivity metrics. Sleep, 44, 2021, 10.1093/sleep/zsaa247.
Jagannathan, S.R., Ezquerro-Nassar, A., Jachs, B., Pustovaya, O.V., Bareham, C.A., Bekinschtein, T.A., Tracking wakefulness as it fades: Micro-measures of alertness. NeuroImage 176 (2018), 138–151, 10.1016/j.neuroimage.2018.04.046.
Kayser, J., Tenke, C.E., Principal components analysis of Laplacian waveforms as a generic method for identifying ERP generator patterns: I. Evaluation with auditory oddball tasks. Clin. Neurophysiol. 117 (2006), 348–368, 10.1016/j.clinph.2005.08.034.
Kimura, M., Widmann, A., Schröger, E., Top-down attention affects sequential regularity representation in the human visual system. Int. J. Psychophysiol. Off. J. Int. Organ. Psychophysiol. 77 (2010), 126–134, 10.1016/j.ijpsycho.2010.05.003.
King, J.R., Sitt, J.D., Faugeras, F., Rohaut, B., El Karoui, I., Cohen, L., Naccache, L., Dehaene, S., Information sharing in the brain indexes consciousness in noncommunicative patients. Curr. Biol. 23 (2013), 1914–1919, 10.1016/j.cub.2013.07.075.
Lindsay, J.J., Anderson, C.A., From Antecedent Conditions to Violent Actions: A General Affective Aggression Model. Pers. Soc. Psychol. Bull. 26 (2000), 533–547, 10.1177/0146167200267002.
Magnin, M., Rey, M., Bastuji, H., Guillemant, P., Mauguiere, F., Garcia-Larrea, L., Thalamic deactivation at sleep onset precedes that of the cerebral cortex in humans. Proc. Natl. Acad. Sci. 107 (2010), 3829–3833, 10.1073/pnas.0909710107.
Naccache, L., Puybasset, L., Gaillard, R., Serve, E., Willer, J.-C., Auditory mismatch negativity is a good predictor of awakening in comatose patients: a fast and reliable procedure. Clin. Neurophysiol. 116 (2005), 988–989, 10.1016/j.clinph.2004.10.009.
Nittono, H., Momose, D., Hori, T., The vanishing point of the mismatch negativity at sleep onset. Clin. Neurophysiol. 112 (2001), 732–739, 10.1016/S1388-2457(01)00491-6.
Noreika, V., Canales-Johnson, A., Harrison, W.J., Johnson, A., Arnatkevičiūtė, A., Koh, J., Chennu, S., Bekinschtein, T.A., 2017. Wakefulness state modulates conscious access: Suppression of auditory detection in the transition to sleep. https://doi.org/10.1101/155705.
Noreika, V., Kamke, M.R., Canales-Johnson, A., Chennu, S., Bekinschtein, T.A., Mattingley, J.B., Alertness fluctuations when performing a task modulate cortical evoked responses to transcranial magnetic stimulation. NeuroImage, 223, 2020, 117305, 10.1016/j.neuroimage.2020.117305.
Nunez, P.L., Wingeier, B.M., Silberstein, R.B., Spatial-temporal structures of human alpha rhythms: Theory, microcurrent sources, multiscale measurements, and global binding of local networks. Hum. Brain Mapp. 13 (2001), 125–164, 10.1002/hbm.1030.
Ogilvie, R.D., The process of falling asleep. Sleep Med. Rev. 5 (2001), 247–270, 10.1053/smrv.2001.0145.
Ogilvie, R.D., Wilkinson, R.T., Allison, S., The detection of sleep onset: behavioral, physiological, and subjective convergence. Sleep 12 (1989), 458–474.
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), 1–9, 10.1155/2011/156869.
Page, E.B., Ordered Hypotheses for Multiple Treatments: A Significance Test for Linear Ranks. J. Am. Stat. Assoc., 58, 1963, 216, 10.2307/2282965.
Pedregosa, F., Varoquaux, G., Gramfort, A., Michel, V., Thirion, B., Grisel, O., Blondel, M., Prettenhofer, P., Weiss, R., Dubourg, V., Vanderplas, J., Passos, A., Cournapeau, D., Brucher, M., Perrot, M., Duchesnay, É., Scikit-learn: Machine Learning in Python. J. Mach. Learn. Res. 12 (2012), 2825–2830, 10.1007/s13398-014-0173-7.2.
Rosenberg, R.S., Van Hout, S., The American Academy of Sleep Medicine Inter-scorer Reliability Program: Sleep Stage Scoring. J. Clin. Sleep Med. 09 (2013), 81–87, 10.5664/jcsm.2350.
Santamaria, J., Chiappa, K.H., The EEG of Drowsiness in Normal Adults. J. Clin. Neurophysiol., 4, 1987, 327.
Schlossmacher, I., Dellert, T., Pitts, M., Bruchmann, M., Straube, T., Differential Effects of Awareness and Task Relevance on Early and Late ERPs in a No-Report Visual Oddball Paradigm. J. Neurosci. 40 (2020), 2906–2913, 10.1523/JNEUROSCI.2077-19.2020.
Sergent, C., Baillet, S., Dehaene, S., Timing of the brain events underlying access to consciousness during the attentional blink. Nat. Neurosci. 8 (2005), 1391–1400, 10.1038/nn1549.
Siclari, F., Tononi, G., Local aspects of sleep and wakefulness. Curr. Opin. Neurobiol. 44 (2017), 222–227, 10.1016/j.conb.2017.05.008.
Sitt, J.D., King, J.-R., Karoui, I.E., Rohaut, B., Faugeras, F., Gramfort, A., Cohen, L., Sigman, M., Dehaene, S., Naccache, L., Large scale screening of neural signatures of consciousness in patients in a vegetative or minimally conscious state. Brain 137 (2014), 2258–2270, 10.1093/brain/awu141.
Skorucak, J., Hertig-Godeschalk, A., Achermann, P., Mathis, J., Schreier, D.R., Automatically Detected Microsleep Episodes in the Fitness-to-Drive Assessment. Front. Neurosci., 14, 2020, 10.3389/fnins.2020.00008.
Sokoliuk, R., Mayhew, S.D., Aquino, K.M., Wilson, R., Brookes, M.J., Francis, S.T., Hanslmayr, S., Mullinger, K.J., Two Spatially Distinct Posterior Alpha Sources Fulfill Different Functional Roles in Attention. J. Neurosci. 39 (2019), 7183–7194, 10.1523/JNEUROSCI.1993-18.2019.
Stevner, A.B.A., Vidaurre, D., Cabral, J., Rapuano, K., Nielsen, S.F.V., Tagliazucchi, E., Laufs, H., Vuust, P., Deco, G., Woolrich, M.W., Van Someren, E., Kringelbach, M.L., Discovery of key whole-brain transitions and dynamics during human wakefulness and non-REM sleep. Nat. Commun., 10, 2019, 1035, 10.1038/s41467-019-08934-3.
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, 2015, 201501026, 10.1073/pnas.1501026112.
Tan, S.H., The Correct Interpretation of Confidence Intervals. Proc. Singap. Healthc., 19, 2010, 3.
Tanaka, H., Hayashi, M., Hori, T., Statistical features of hypnagogic EEG measured by a new scoring system. Sleep 19 (1996), 731–738.
Wacongne, C., Labyt, E., van Wassenhove, V., Bekinschtein, T., Naccache, L., Dehaene, S., Evidence for a hierarchy of predictions and prediction errors in human cortex. Proc. Natl. Acad. Sci. 108 (2011), 20754–20759, 10.1073/pnas.1117807108.
Wei, J.-H., Chan, T.-C., Luo, Y.-J., A modified oddball paradigm “cross-modal delayed response” and the research on mismatch negativity. Brain Res. Bull. 57 (2002), 221–230, 10.1016/S0361-9230(01)00742-0.
Welch, P., The use of fast Fourier transform for the estimation of power spectra: A method based on time averaging over short, modified periodograms. IEEE Trans. Audio Electroacoustics 15 (1967), 70–73, 10.1109/TAU.1967.1161901.
Yang, C.-M., Han, H.-Y., Yang, M.-H., Su, W.-C., Lane, T., What subjective experiences determine the perception of falling asleep during sleep onset period?. Conscious. Cogn. 19 (2010), 1084–1092, 10.1016/j.concog.2009.12.017.
