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

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  • M. Rosanova

    (University of Milan
    Fondazione Europea per la Ricerca Biomedica Onlus
    ASTT Grande Ospedale Metropolitano Niguarda)

  • M. Fecchio

    (University of Milan)

  • S. Casarotto

    (University of Milan
    IRCCS Fondazione Don Gnocchi)

  • S. Sarasso

    (University of Milan)

  • A. G. Casali

    (Universidade Federal de São Paulo)

  • A. Pigorini

    (University of Milan)

  • A. Comanducci

    (University of Milan)

  • F. Seregni

    (Cambridge University Hospital NHS Foundation Trust)

  • G. Devalle

    (IRCCS Fondazione Don Gnocchi)

  • G. Citerio

    (University of Milan Bicocca)

  • O. Bodart

    (University and University Hospital of Liège)

  • M. Boly

    (University of Wisconsin
    University of Wisconsin)

  • O. Gosseries

    (University and University Hospital of Liège)

  • S. Laureys

    (University and University Hospital of Liège)

  • M. Massimini

    (University of Milan
    IRCCS Fondazione Don Gnocchi)

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.

Suggested Citation

  • 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. Massimin, 2018. "Sleep-like cortical OFF-periods disrupt causality and complexity in the brain of unresponsive wakefulness syndrome patients," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-06871-1
    DOI: 10.1038/s41467-018-06871-1
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    Cited by:

    1. Sarah L Eagleman & Divya Chander & Christina Reynolds & Nicholas T Ouellette & M Bruce MacIver, 2019. "Nonlinear dynamics captures brain states at different levels of consciousness in patients anesthetized with propofol," PLOS ONE, Public Library of Science, vol. 14(10), pages 1-26, October.
    2. Minji Lee & Leandro R. D. Sanz & Alice Barra & Audrey Wolff & Jaakko O. Nieminen & Melanie Boly & Mario Rosanova & Silvia Casarotto & Olivier Bodart & Jitka Annen & Aurore Thibaut & Rajanikant Panda &, 2022. "Quantifying arousal and awareness in altered states of consciousness using interpretable deep learning," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Marcello Massimini & Maurizio Corbetta & Maria V. Sanchez-Vives & Thomas Andrillon & Gustavo Deco & Mario Rosanova & Simone Sarasso, 2024. "Sleep-like cortical dynamics during wakefulness and their network effects following brain injury," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Andrea I. Luppi & Lynn Uhrig & Jordy Tasserie & Camilo M. Signorelli & Emmanuel A. Stamatakis & Alain Destexhe & Bechir Jarraya & Rodrigo Cofre, 2024. "Local orchestration of distributed functional patterns supporting loss and restoration of consciousness in the primate brain," Nature Communications, Nature, vol. 15(1), pages 1-22, December.

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