[en] When subjects become unconscious, there is a characteristic change in the way the cerebral cortex responds to perturbations, as can be assessed using transcranial magnetic stimulation and electroencephalography (TMS-EEG). For instance, compared to wakefulness, during non-rapid eye movement (NREM) sleep TMS elicits a larger positive-negative wave, fewer phase-locked oscillations, and an overall simpler response. However, many physiological variables also change when subjects go from wake to sleep, anesthesia, or coma. To avoid these confounding factors, we focused on NREM sleep only and measured TMS-evoked EEG responses before awakening the subjects and asking them if they had been conscious (dreaming) or not. As shown here, when subjects reported no conscious experience upon awakening, TMS evoked a larger negative deflection and a shorter phase-locked response compared to when they reported a dream. Moreover, the amplitude of the negative deflection-a hallmark of neuronal bistability according to intracranial studies-was inversely correlated with the length of the dream report (i.e., total word count). These findings suggest that variations in the level of consciousness within the same physiological state are associated with changes in the underlying bistability in cortical circuits.
Disciplines :
Neurosciences & comportement
Auteur, co-auteur :
Nieminen, Jaakko O. ✱
Gosseries, Olivia ✱; Université de Liège - ULiège > Centre de recherches du cyclotron
Massimini, Marcello
Saad, Elyana
Sheldon, Andrew D.
Boly, Melanie
Siclari, Francesca
Postle, Bradley R.
Tononi, Giulio
✱ Ces auteurs ont contribué de façon équivalente à la publication.
Langue du document :
Anglais
Titre :
Consciousness and cortical responsiveness: a within-state study during non-rapid eye movement sleep.
Koch, C., Massimini, M., Boly, M., Tononi, G. Neural correlates of consciousness: progress and problems. Nat. Rev. Neurosci. 17, 307-321 (2016).
Casali, A. G. et al. A theoretically based index of consciousness independent of sensory processing and behavior. Sci. Transl. Med. 5, 198ra105 (2013).
Massimini, M. et al. Breakdown of cortical effective connectivity during sleep. Science 309, 2228-2232 (2005).
Rosanova, M. et al. Natural frequencies of human corticothalamic circuits. J. Neurosci. 29, 7679-7685 (2009).
Massimini, M. et al. Cortical reactivity and effective connectivity during REM sleep in humans. Cogn. Neurosci. 1, 176-183 (2010).
Sarasso, S. et al. Consciousness and complexity during unresponsiveness induced by propofol, xenon, and ketamine. Curr. Biol. 25, 3099-3105 (2015).
Rosanova, M. et al. Recovery of cortical effective connectivity and recovery of consciousness in vegetative patients. Brain 135, 1308-1320 (2012).
Ragazzoni, A. et al. Vegetative versus minimally conscious states: A study using TMS-EEG, sensory and event-related potentials. PLoS One 8, e57069 (2013).
Ferrarelli, F. et al. Breakdown in cortical effective connectivity during midazolam-induced loss of consciousness. Proc. Natl. Acad. Sci. USA 107, 2681-2686 (2010).
Massimini, M. et al. Triggering sleep slow waves by transcranial magnetic stimulation. Proc. Natl. Acad. Sci. USA 104, 8496-8501 (2007).
Gosseries, O. et al. On the cerebral origin of EEG responses to TMS: Insights from severe cortical lesions. Brain Stimul. 8, 142-149 (2015).
Pigorini, A. et al. Bistability breaks-off deterministic responses to intracortical stimulation during non-REM sleep. Neuroimage 112, 105-113 (2015).
Massimini, M., Ferrarelli, F., Sarasso, S., Tononi, G. Cortical mechanisms of loss of consciousness: insight from TMS/EEG studies. Arch. Ital. Biol. 150, 44-55 (2012).
Tononi, G., Massimini, M. Why does consciousness fade in early sleep? Ann. N. Y. Acad. Sci. 1129, 330-334 (2008).
Siclari, F., LaRocque, J. J., Postle, B. R., Tononi, G. Assessing sleep consciousness within subjects using a serial awakening paradigm. Front. Psychol. 4, 542 (2013).
McNamara, P. et al. REM and NREM sleep mentation. Int. Rev. Neurobiol. 92, 69-86 (2010).
Nir, Y., Tononi, G. Dreaming and the brain: from phenomenology to neurophysiology. Trends Cogn. Sci. 14, 88-100 (2010).
Foulkes, W. D. Dream reports from different stages of sleep. J. Abnorm. Soc. Psychol. 65, 14-25 (1962).
Noreika, V. et al. Consciousness lost and found: subjective experiences in an unresponsive state. Brain Cogn. 77, 327-334 (2011).
Siclari, F. LaRocque, J. J., Bernardi, G., Postle, B. R., Tononi, G. The neural correlates of consciousness in sleep: A no-task, withinstate paradigm. bioRxiv doi: 10.1101/012443 (2014).
Chellappa, S. L., Frey, S., Knoblauch, V., Cajochen, C. Cortical activation patterns herald successful dream recall after NREM and REM sleep. Biol. Psychol. 87, 251-256 (2011).
Horikawa, T., Tamaki, M., Miyawaki, Y., Kamitani, Y. Neural decoding of visual imagery during sleep. Science 340, 639-642 (2013).
Fosse, R., Stickgold, R., Hobson, J. A. Brain-mind states: Reciprocal variation in thoughts and hallucinations. Psychol. Sci. 12, 30-36 (2011).
Noreika, V., Valli, K., Lahtela, H., Revonsuo, A. Early-night serial awakenings as a new paradigm for studies on NREM dreaming. Int. J. Psychophysiol. 74, 14-18 (2009).
Nielsen, T. A. A review of mentation in REM and NREM sleep: "Covert" REM sleep as a possible reconciliation of two opposing models. Behav. Brain Sci. 23, 851-866 (2000).
Palva, J. M., Palva, S., Kaila, K. Phase synchrony among neuronal oscillations in the human cortex. J. Neurosci. 25, 3962-3972 (2005).
Steriade, M., Timofeev, I., Grenier, F. Natural waking and sleep states: A view from inside neocortical neurons. J. Neurophysiol. 85, 1969-1985 (2001).
Sanchez-Vives, M. V., McCormick, D. A. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 3, 1027-1034 (2000).
Oizumi, M., Albantakis, L., Tononi, G. From the phenomenology to the mechanisms of consciousness: Integrated information theory 3.0. PLoS Comput. Biol. 10, e1003588 (2014).
Tononi, G. Integrated information theory of consciousness: an updated account. Arch. Ital. Biol. 150, 293-329 (2012).
van Kerkoerle, T. et al. Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex. Proc. Natl. Acad. Sci. USA 111, 14332-14341 (2014).
Michalareas, G. et al. Alpha-beta and gamma rhythms subserve feedback and feedforward influences among human visual cortical areas. Neuron 89, 384-397 (2016).
Lamme, V. A. F. How neuroscience will change our view on consciousness. Cogn. Neurosci. 1, 204-220 (2010).
Siclari, F. et al. Two distinct synchronization processes in the transition to sleep: A high-density electroencephalographic study. Sleep 37, 1621-1637 (2014).
Massimini, M., Huber, R., Ferrarelli, F., Hill, S., Tononi, G. The sleep slow oscillation as a traveling wave. J. Neurosci. 24, 6862-6870 (2004).
Bergmann, T. O. et al. EEG-guided transcranial magnetic stimulation reveals rapid shifts in motor cortical excitability during the human sleep slow oscillation. J. Neurosci. 32, 243-253 (2012).
Buysse, D. J., Reynolds III, C. F., Monk, T. H., Berman, S. R., Kupfer, D. J. The Pittsburgh Sleep Quality Index: A new instrument for psychiatric practice and research. Psychiatry Res. 28, 193-213 (1989).
World Medical Association. World Medical Association Declaration of Helsinki: Ethical principles for medical research involving human subjects. JAMA 310, 2191-2194 (2013).
Iber, C., Ancoli-Israel, S., Chesson Jr. A. L., Quan, S. F. The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications. American Academy of Sleep Medicine, Westchester, IL, USA (2007).
Cavanna, A. E. The precuneus and consciousness. CNS Spectr. 12, 545-552 (2007).
Hagmann, P. et al. Mapping the structural core of human cerebral cortex. PLoS Biol. 6, e159 (2008).
Mutanen, T., Mäki, H., Ilmoniemi, R. J. The effect of stimulus parameters on TMS-EEG muscle artifacts. Brain Stimul. 6, 371-376 (2013).
Casarotto, S. et al. EEG responses to TMS are sensitive to changes in the perturbation parameters and repeatable over time. PLoS One 5, e10281 (2010).
Nieminen, J. O., Koponen, L. M., Ilmoniemi, R. J. Experimental characterization of the electric field distribution induced by TMS devices. Brain Stimul. 8, 582-589 (2015).
Wassermann, E. M. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. Electroencephalogr. Clin. Neurophysiol. 108, 1-16 (1998).
Nikouline, V., Ruohonen, J., Ilmoniemi, R. J. The role of the coil click in TMS assessed with simultaneous EEG. Clin. Neurophysiol. 110, 1325-1328 (1999).
Delorme, A., Makeig, S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 134, 9-21 (2004).
Mutanen, T. P. et al. Recovering TMS-evoked EEG responses masked by muscle artifacts. Neuroimage 139, 157-166 (2016).
Maris, E., Oostenveld, R. Nonparametric statistical testing of EEG-and MEG-data. J. Neurosci. Methods 164, 177-190 (2007).
Waterman, D. É., Elton, M., Kenemans, J. L. Methodological issues affecting the collection of dreams. J. Sleep Res. 2, 8-12 (1993).
