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

M. Rosanova, M. Fecchio, S. Casarotto, S. Sarasso, A. G. Casali, A. Pigorini, A. Comanducci, F. Seregni, G. Devalle, G. Citerio, O. Bodart, M. Boly, O. Gosseries, S. Laureys, M. Massimini

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

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.

Original languageEnglish
Article number4427
JournalNature Communications
Volume9
Issue number1
DOIs
Publication statusPublished - Dec 1 2018

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wakefulness
sleep
Wakefulness
Causality
consciousness
brain
Brain
Sleep
Unconsciousness
Medical Errors
electroencephalography
Transcranial Magnetic Stimulation
cortexes
Electroencephalography
stimulation
stimuli
Healthy Volunteers
tendencies
recovery
interactions

ASJC Scopus subject areas

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

Cite this

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

In: Nature Communications, Vol. 9, No. 1, 4427, 01.12.2018.

Research output: Contribution to journalArticle

Rosanova, M, Fecchio, M, Casarotto, S, Sarasso, S, Casali, AG, Pigorini, A, Comanducci, A, Seregni, F, Devalle, G, Citerio, G, Bodart, O, Boly, M, Gosseries, O, Laureys, S & Massimini, M 2018, 'Sleep-like cortical OFF-periods disrupt causality and complexity in the brain of unresponsive wakefulness syndrome patients', Nature Communications, vol. 9, no. 1, 4427. https://doi.org/10.1038/s41467-018-06871-1
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. / Sleep-like cortical OFF-periods disrupt causality and complexity in the brain of unresponsive wakefulness syndrome patients. In: Nature Communications. 2018 ; Vol. 9, No. 1.
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