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

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 a...

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Bibliographic Details
Published in:Nature communications Vol. 9; no. 1; pp. 4427 - 10
Main Authors: Rosanova, M., Fecchio, M., Casarotto, S., Sarasso, S., Casali, A. G., Pigorini, A., Comanducci, A., Seregni, F., Devalle, G., Citerio, G., Bodart, O., Boly, M., Gosseries, O., Laureys, S., Massimini, M.
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 24.10.2018
Nature Publishing Group
Nature Portfolio
Subjects:
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Brain
Brain - physiology
Brain injury
Cerebral cortex
Complexity
Consciousness
EEG
Electroencephalography
Head injuries
Human health sciences
Humanities and Social Sciences
Humans
Magnetic fields
multidisciplinary
Neurologie
Neurology
Patients
Persistent Vegetative State - physiopathology
Science
Science (multidisciplinary)
Sciences de la santé humaine
Sensory stimuli
Sleep
Sleep - physiology
Sleep and wakefulness
Somatosensory cortex
Thalamus
Transcranial magnetic stimulation
Wakefulness
Wakefulness - physiology
ISSN:2041-1723, 2041-1723
Online Access:Get full text
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Summary: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. Many brain-injured patients retain large cortical islands that are intact, active and reactive but blocked in a state of low complexity, leading to unconsciousness. Here, the authors show that this loss of complexity is due to the pathological engagement of sleep-like neuronal mechanisms.
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scopus-id:2-s2.0-85055463200
ISSN:2041-1723
2041-1723
DOI:10.1038/s41467-018-06871-1