Sleep-like cortical OFF-periods disrupt causality and complexity in the brain of unresponsive wakefulness syndrome patients

Rosanova, Mario; Fecchio, M.; Casarotto, Silvia; Sarasso, Simone; Casali, A. G.; Pigorini, A.; Comanducci, A.; Seregni, F.; Devalle, G.; Citerio, Giuseppe; BODART, Olivier; Boly, Mélanie; Gosseries, Olivia; Laureys, Steven; Massimini, Marcello

doi:10.1038/s41467-018-06871-1

Article (Périodiques scientifiques)

Sleep-like cortical OFF-periods disrupt causality and complexity in the brain of unresponsive wakefulness syndrome patients

Rosanova, Mario; Fecchio, M.; Casarotto, Silvia et al.

2018 • In Nature Communications, 9 (1)

Peer reviewed vérifié par ORBi

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https://hdl.handle.net/2268/231468

DOI
10.1038/s41467-018-06871-1

PubMed
30356042

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Résumé :

[en] Unresponsive wakefulness syndrome (UWS) patients may retain intact portions of the thalamocortical system that are spontaneously active and reactive to sensory stimuli but fail to engage in complex causal interactions, resulting in loss of consciousness. Here, we show that loss of brain complexity after severe injuries is due to a pathological tendency of cortical circuits to fall into silence (OFF-period) upon receiving an input, a behavior typically observed during sleep. Spectral and phase domain analysis of EEG responses to transcranial magnetic stimulation reveals the occurrence of OFF-periods in the cortex of UWS patients (N = 16); these events never occur in healthy awake individuals (N = 20) but are similar to those detected in healthy sleeping subjects (N = 8). Crucially, OFF-periods impair local causal interactions, and prevent the build-up of global complexity in UWS. Our findings link potentially reversible local events to global brain dynamics that are relevant for pathological loss and recovery of consciousness. © 2018, The Author(s).

Disciplines :

Neurologie

Auteur, co-auteur :

Rosanova, Mario ^✱; Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Milan, 20157, Italy, Fondazione Europea per la Ricerca Biomedica Onlus, Milan, 20063, Italy, Neurointensive Care Unit, ASTT Grande Ospedale Metropolitano Niguarda, Milan, 20162, Italy

Fecchio, M. ^✱; Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Milan, 20157, Italy

Casarotto, Silvia; Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Milan, 20157, Italy, IRCCS Fondazione Don Gnocchi, Milan, 20149, Italy

Sarasso, Simone; Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Milan, 20157, Italy

Casali, A. G.; Instituto de Ciência e Tecnologia, Universidade Federal de São Paulo, Sao Jose dos Campos, 12231-280, Brazil

Pigorini, A.; Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Milan, 20157, Italy

Comanducci, A.; Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Milan, 20157, Italy

Seregni, F.; Department of Paediatrics, Cambridge University Hospital NHS Foundation Trust, Cambridge, CB2 0QQ, United Kingdom

Devalle, G.; IRCCS Fondazione Don Gnocchi, Milan, 20149, Italy

Citerio, Giuseppe; Scuola di Medicina e Chirurgia, University of Milan Bicocca, Milan, 20126, Italy

Plus d'auteurs (5 en +)

^✱ Ces auteurs ont contribué de façon équivalente à la publication.

Langue du document :

Anglais

Titre :

Sleep-like cortical OFF-periods disrupt causality and complexity in the brain of unresponsive wakefulness syndrome patients

Date de publication/diffusion :

2018

Titre du périodique :

Nature Communications

eISSN :

2041-1723

Maison d'édition :

Nature

Volume/Tome :

Fascicule/Saison :

Peer reviewed :

Peer reviewed vérifié par ORBi

Disponible sur ORBi :

depuis le 15 janvier 2019

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citations Scopus^®

112

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Bibliographie

Laureys, S. et al. Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med. 8, 68 (2010)
Laureys, S., Owen, A. M. & Schiff, N. D. Brain function in coma, vegetative state, and related disorders. Lancet Neurol. 3, 537–546 (2004)
Schiff, N. D. et al. Residual cerebral activity and behavioural fragments can remain in the persistently vegetative brain. Brain 125, 1210–1234 (2002)
Stender, J. et al. Diagnostic precision of PET imaging and functional MRI in disorders of consciousness: a clinical validation study. Lancet 384, 514–522 (2014)
Boly, M. et al. Cerebral processing of auditory and noxious stimuli in severely brain injured patients: differences between VS and MCS. Neuropsychol. Rehabil. 15, 283–289 (2005)
Fischer, C., Luaute, J. & Morlet, D. Event-related potentials (MMN and novelty P3) in permanent vegetative or minimally conscious states. Clin. Neurophysiol. 121, 1032–1042 (2010)
Casarotto, S. et al. Stratification of unresponsive patients by an independently validated index of brain complexity. Ann. Neurol. 80, 718–729 (2016)
Massimini, M. et al. Breakdown of cortical effective connectivity during sleep. Science 309, 2228–2232 (2005)
Casali, A. G. et al. A theoretically based index of consciousness independent of sensory processing and behavior. Sci. Transl. Med. 5, 198ra105–198ra105 (2013)
Pigorini, A. et al. Bistability breaks-off deterministic responses to intracortical stimulation during non-REM sleep. Neuroimage 112, 105–113 (2015)
Usami, K. et al. Sleep modulates cortical connectivity and excitability in humans: direct evidence from neural activity induced by single-pulse electrical stimulation. Hum. Brain Mapp. 36, 4714–4729 (2015)
Steriade, M., Nuñez, A. & Amzica, F. A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci. 13, 3252–3265 (1993)
Timofeev, I., Grenier, F. & Steriade, M. Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study. Proc. Natl Acad. Sci. USA 98, 1924–1929 (2001)
Sanchez-Vives, M. V. & McCormick, D. A. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 3, 1027–1034 (2000)
Compte, A., Sanchez-Vives, M. V., McCormick, D. A. & Wang, X.-J. Cellular and network mechanisms of slow oscillatory activity (<1 Hz) and wave propagations in a cortical network model. J. Neurophysiol. 89, 2707–2725 (2003)
Funk, C. M. et al. Role of somatostatin-positive cortical interneurons in the generation of sleep slow waves. J. Neurosci. 37, 9132–9148 (2017)
Zucca, S. et al. An inhibitory gate for state transition in cortex. eLife 6, e26177 (2017)
Sanchez-Vives, M. V., Massimini, M. & Mattia, M. Shaping the default activity pattern of the cortical network. Neuron 94, 993–1001 (2017)
Mann, E. O., Kohl, M. M. & Paulsen, O. Distinct roles of GABA(A) and GABA(B) receptors in balancing and terminating persistent cortical activity. J. Neurosci. 29, 7513–7518 (2009)
Timofeev, I., Grenier, F., Bazhenov, M., Sejnowski, T. J. & Steriade, M. Origin of slow cortical oscillations in deafferented cortical slabs. Cereb. Cortex 10, 1185–1199 (2000)
Giacino, J. T., Kalmar, K. & Whyte, J. The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. Arch. Phys. Med. Rehabil. 85, 2020–2029 (2004)
Mukovski, M., Chauvette, S., Timofeev, I. & Volgushev, M. Detection of active and silent states in neocortical neurons from the field potential signal during slow-wave sleep. Cereb. Cortex 17, 400–414 (2007)
Cash, S. S. et al. The human K-complex represents an isolated cortical down-state. Science 324, 1084–1087 (2009)
Piantoni, G. et al. Modulation of γ and spindle-range power by slow oscillations in scalp sleep EEG of children. Int. J. Psychophysiol. 89, 252–258 (2013)
Menicucci, D. et al. Fragments of wake-like activity frame down-states of sleep slow oscillations in humans: new vistas for studying homeostatic processes during sleep. Int. J. Psychophysiol. 89, 151–157 (2013)
Rosanova, M. et al. Recovery of cortical effective connectivity and recovery of consciousness in vegetative patients. Brain 135, 1308–1320 (2012)
Gosseries, O. et al. On the cerebral origin of EEG responses to TMS: insights from severe cortical lesions. Brain Stimul. 8, 142–149 (2015)
Bodart, O. et al. Measures of metabolism and complexity in the brain of patients with disorders of consciousness. Neuroimage Clin. 14, 354–362 (2017)
Moruzzi, G. & Magoun, H. W. Brain stem reticular formation and activation of the EEG. Electroencephalogr. Clin. Neurophysiol. 1, 455–473 (1949)
Steriade, M., Datta, S., Paré, D., Oakson, G. & Curró Dossi, R. C. Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J. Neurosci. 10, 2541–2559 (1990)
McCormick, D. A. & Williamson, A. Convergence and divergence of neurotransmitter action in human cerebral cortex. Proc. Natl Acad. Sci. USA 86, 8098–8102 (1989)
Edlow, B. L. et al. Neuroanatomic connectivity of the human ascending arousal system critical to consciousness and its disorders. J. Neuropathol. Exp. Neurol. 71, 531–546 (2012)
Hill, S. & Tononi, G. Modeling sleep and wakefulness in the thalamocortical system. J. Neurophysiol. 93, 1671–1698 (2005)
Gloor, P., Ball, G. & Schaul, N. Brain lesions that produce delta waves in the EEG. Neurology 27, 326–333 (1977)
Ball, G. J., Gloor, P. & Schaul, N. The cortical electromicrophysiology of pathological delta waves in the electroencephalogram of cats. Electroencephalogr. Clin. Neurophysiol. 43, 346–361 (1977)
Meythaler, J. M., Peduzzi, J. D., Eleftheriou, E. & Novack, T. A. Current concepts: diffuse axonal injury-associated traumatic brain injury. Arch. Phys. Med. Rehabil. 82, 1461–1471 (2001)
Schwindt, P. C., Spain, W. J. & Crill, W. E. Long-lasting reduction of excitability by a sodium-dependent potassium current in cat neocortical neurons. J. Neurophysiol. 61, 233–244 (1989)
Nita, D. A., Cissé, Y., Timofeev, I. & Steriade, M. Waking-sleep modulation of paroxysmal activities induced by partial cortical deafferentation. Cereb. Cortex 17, 272–283 (2007)
Lemieux, M., Chen, J.-Y., Lonjers, P., Bazhenov, M. & Timofeev, I. The impact of cortical deafferentation on the neocortical slow oscillation. J. Neurosci. 34, 5689–5703 (2014)
Lőrincz, M. L. et al. A distinct class of slow (~0.2-2 Hz) intrinsically bursting layer 5 pyramidal neurons determines UP/DOWN state dynamics in the neocortex. J. Neurosci. 35, 5442–5458 (2015)
Fanciullacci, C. et al. Delta power is higher and more symmetrical in ischemic stroke patients with cortical involvement. Front. Hum. Neurosci. 11, 385 (2017)
Schaul, N. The fundamental neural mechanisms of electroencephalography. Electroencephalogr. Clin. Neurophysiol. 106, 101–107 (1998)
Schiff, N. D. Recovery of consciousness after brain injury: a mesocircuit hypothesis. Trends Neurosci. 33, 1–9 (2010)
Fridman, E. A., Beattie, B. J., Broft, A., Laureys, S. & Schiff, N. D. Regional cerebral metabolic patterns demonstrate the role of anterior forebrain mesocircuit dysfunction in the severely injured brain. Proc. Natl Acad. Sci. USA 111, 6473–6478 (2014)
McCormick, D. A. & Bal, T. Sleep and arousal: thalamocortical mechanisms. Annu. Rev. Neurosci. 20, 185–215 (1997)
Crunelli, V. & Hughes, S. W. The slow (<1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators. Nat. Neurosci. 13, 9–17 (2010)
Leon-Carrion, J., Martin-Rodriguez, J. F., Damas-Lopez, J., Barroso y Martin, J. M. & Dominguez-Morales, M. R. Brain function in the minimally conscious state: a quantitative neurophysiological study. Clin. Neurophysiol. 119, 1506–1514 (2008)
Lehembre, R. et al. Resting-state EEG study of comatose patients: a connectivity and frequency analysis to find differences between vegetative and minimally conscious states. Funct. Neurol. 27, 41–47 (2012)
Sitt, J. D. et al. Large scale screening of neural signatures of consciousness in patients in a vegetative or minimally conscious state. Brain 137, 2258–2270 (2014)
Mattia, M. & Sanchez-Vives, M. V. Exploring the spectrum of dynamical regimes and timescales in spontaneous cortical activity. Cogn. Neurodyn 6, 239–250 (2012)
Tartaglia, E. M. & Brunel, N. Bistability and up/down state alternations in inhibition-dominated randomly connected networks of LIF neurons. Sci. Rep. 7, 11916 (2017)
Freyer, F., Aquino, K., Robinson, P. A., Ritter, P. & Breakspear, M. Bistability and non-Gaussian fluctuations in spontaneous cortical activity. J. Neurosci. 29, 8512–8524 (2009)
Jercog, D. et al. UP-DOWN cortical dynamics reflect state transitions in a bistable network. eLife 6, e22425 (2017)
Rosanova, M. et al. Natural frequencies of human corticothalamic circuits. J. Neurosci. 29, 7679–7685 (2009)
Lumer, E. D., Edelman, G. M. & Tononi, G. Neural dynamics in a model of the thalamocortical system. II. The role of neural synchrony tested through perturbations of spike timing. Cereb. Cortex 7, 228–236 (1997)
Tononi, G., Boly, M., Massimini, M. & Koch, C. Integrated information theory: from consciousness to its physical substrate. Nat. Rev. Neurosci. 17, 450–461 (2016)
Fernández-Espejo, D. et al. A role for the default mode network in the bases of disorders of consciousness. Ann. Neurol. 72, 335–343 (2012)
Lutkenhoff, E. S. et al. Thalamic and extrathalamic mechanisms of consciousness after severe brain injury. Ann. Neurol. 78, 68–76 (2015)
Voss, H. U. et al. Possible axonal regrowth in late recovery from the minimally conscious state. J. Clin. Invest. 116, 2005–2011 (2006)
Sidaros, A. et al. Diffusion tensor imaging during recovery from severe traumatic brain injury and relation to clinical outcome: a longitudinal study. Brain 131, 559–572 (2008)
Laureys, S. et al. Restoration of thalamocortical connectivity after recovery from persistent vegetative state. Lancet 355, 1790–1791 (2000)
Schiff, N. D. et al. Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature 448, 600–603 (2007)
Monti, M. M., Schnakers, C., Korb, A. S., Bystritsky, A. & Vespa, P. M. Non-invasive ultrasonic thalamic stimulation in disorders of consciousness after severe brain injury: a first-in-man report. Brain Stimul. 9, 940–941 (2016)
D’Andola, M. et al. Bistability, causality, and complexity in cortical networks: an in vitro perturbational study. Cereb. Cortex 28, 2233–2242 (2018)
Giacino, J. T. et al. Placebo-controlled trial of amantadine for severe traumatic brain injury. N. Engl. J. Med. 366, 819–826 (2012)
Sutton, J. A. & Clauss, R. P. A review of the evidence of zolpidem efficacy in neurological disability after brain damage due to stroke, trauma and hypoxia: a justification of further clinical trials. Brain Inj. 31, 1019–1027 (2017)
Thibaut, A., Bruno, M.-A., Ledoux, D., Demertzi, A. & Laureys, S. tDCS in patients with disorders of consciousness: sham-controlled randomized double-blind study. Neurology 82, 1112–1118 (2014)
Corazzol, M. et al. Restoring consciousness with vagus nerve stimulation. Curr. Biol. 27, R994–R996 (2017)
Silber, M. H. et al. The visual scoring of sleep in adults. J. Clin. Sleep Med. 3, 121–131 (2007)
Massimini, M. et al. Triggering sleep slow waves by transcranial magnetic stimulation. Proc. Natl Acad. Sci. USA 104, 8496–8501 (2007)
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)
Forgacs, P. B. et al. Preservation of electroencephalographic organization in patients with impaired consciousness and imaging-based evidence of command-following. Ann. Neurol. 76, 869–879 (2014)
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)
Grandchamp, R. & Delorme, A. Single-trial normalization for event-related spectral decomposition reduces sensitivity to noisy trials. Front. Psychol. 2, 236 (2011)
Palva, S., Linkenkaer-Hansen, K., Näätänen, R. & Palva, J. M. Early neural correlates of conscious somatosensory perception. J. Neurosci. 25, 5248–5258 (2005)