Published October 24, 2018 | Version v1
Journal article Open

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

  • 1. 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.
  • 2. Department of Biomedical and Clinical Sciences "L. Sacco", University of Milan, Milan, 20157, Italy.
  • 3. Department of Biomedical and Clinical Sciences "L. Sacco", University of Milan, Milan, 20157, Italy. IRCCS Fondazione Don Gnocchi, Milan, 20149, Italy.
  • 4. Instituto de Ciência e Tecnologia, Universidade Federal de São Paulo, Sao Jose dos Campos, 12231-280, Brazil.
  • 5. Department of Paediatrics, Cambridge University Hospital NHS Foundation Trust, Cambridge, CB2 0QQ, UK.
  • 6. IRCCS Fondazione Don Gnocchi, Milan, 20149, Italy.
  • 7. Scuola di Medicina e Chirurgia, University of Milan Bicocca, Milan, 20126, Italy.
  • 8. GIGA-consciousness, Coma Science Group, University and University Hospital of Liège, Liège, 4000, Belgium.
  • 9. Department of Neurology, University of Wisconsin, Madison, WI, 53705, USA. Department of Psychiatry, University of Wisconsin, Madison, WI, 53719, USA.
  • 10. Department of Biomedical and Clinical Sciences "L. Sacco", University of Milan, Milan, 20157, Italy. marcello.massimini@unimi.it. IRCCS Fondazione Don Gnocchi, Milan, 20149, Italy.

Description

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.

Files

Rosanova et al. - 2018 - Sleep-like cortical OFF-periods disrupt causality .pdf

Additional details

Funding

LUMINOUS – Studying, Measuring and Altering Consciousness through information theory in the electrical brain 686764
European Commission