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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| Vydáno v: | Nature communications Ročník 9; číslo 1; s. 4427 - 10 |
|---|---|
| Hlavní autoři: | , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
| Vydáno: |
London
Nature Publishing Group UK
24.10.2018
Nature Publishing Group Nature Portfolio |
| Témata: | |
| ISSN: | 2041-1723, 2041-1723 |
| On-line přístup: | Získat plný text |
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| 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.
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. |
|---|---|
| AbstractList | 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. 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. 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. 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.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. 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). 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. 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. |
| ArticleNumber | 4427 |
| Author | Laureys, S. Massimini, M. Comanducci, A. Boly, M. Casali, A. G. Casarotto, S. Citerio, G. Devalle, G. Bodart, O. Rosanova, M. Fecchio, M. Pigorini, A. Seregni, F. Gosseries, O. Sarasso, S. |
| Author_xml | – sequence: 1 givenname: M. orcidid: 0000-0001-7486-7617 surname: Rosanova fullname: Rosanova, M. organization: Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, Fondazione Europea per la Ricerca Biomedica Onlus, Neurointensive Care Unit, ASTT Grande Ospedale Metropolitano Niguarda – sequence: 2 givenname: M. orcidid: 0000-0002-0347-8531 surname: Fecchio fullname: Fecchio, M. organization: Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan – sequence: 3 givenname: S. orcidid: 0000-0002-7548-7664 surname: Casarotto fullname: Casarotto, S. organization: Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, IRCCS Fondazione Don Gnocchi – sequence: 4 givenname: S. orcidid: 0000-0001-9984-4710 surname: Sarasso fullname: Sarasso, S. organization: Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan – sequence: 5 givenname: A. G. surname: Casali fullname: Casali, A. G. organization: Instituto de Ciência e Tecnologia, Universidade Federal de São Paulo – sequence: 6 givenname: A. surname: Pigorini fullname: Pigorini, A. organization: Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan – sequence: 7 givenname: A. surname: Comanducci fullname: Comanducci, A. organization: Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan – sequence: 8 givenname: F. surname: Seregni fullname: Seregni, F. organization: Department of Paediatrics, Cambridge University Hospital NHS Foundation Trust – sequence: 9 givenname: G. surname: Devalle fullname: Devalle, G. organization: IRCCS Fondazione Don Gnocchi – sequence: 10 givenname: G. orcidid: 0000-0002-5374-3161 surname: Citerio fullname: Citerio, G. organization: Scuola di Medicina e Chirurgia, University of Milan Bicocca – sequence: 11 givenname: O. orcidid: 0000-0003-1188-5484 surname: Bodart fullname: Bodart, O. organization: GIGA-consciousness, Coma Science Group, University and University Hospital of Liège – sequence: 12 givenname: M. surname: Boly fullname: Boly, M. organization: Department of Neurology, University of Wisconsin, Department of Psychiatry, University of Wisconsin – sequence: 13 givenname: O. surname: Gosseries fullname: Gosseries, O. organization: GIGA-consciousness, Coma Science Group, University and University Hospital of Liège – sequence: 14 givenname: S. surname: Laureys fullname: Laureys, S. organization: GIGA-consciousness, Coma Science Group, University and University Hospital of Liège – sequence: 15 givenname: M. surname: Massimini fullname: Massimini, M. email: marcello.massimini@unimi.it organization: Department of Biomedical and Clinical Sciences “L. Sacco”, University of Milan, IRCCS Fondazione Don Gnocchi |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30356042$$D View this record in MEDLINE/PubMed |
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| Copyright | The Author(s) 2018 2018. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
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| DOI | 10.1038/s41467-018-06871-1 |
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| Snippet | Unresponsive wakefulness syndrome (UWS) patients may retain intact portions of the thalamocortical system that are spontaneously active and reactive to sensory... Unresponsive wakefulness syndrome (UWS) patients may retain intact portions of the thalamocortical system that are spontaneously active and reactive to sensory... Many brain-injured patients retain large cortical islands that are intact, active and reactive but blocked in a state of low complexity, leading to... |
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| Title | Sleep-like cortical OFF-periods disrupt causality and complexity in the brain of unresponsive wakefulness syndrome patients |
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