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Spectral Signatures of Reorganised Brain Networks in Disorders of Consciousness

Theoretical advances in the science of consciousness have proposed that it is concomitant with balanced cortical integration and differentiation, enabled by efficient networks of information transfer across multiple scales. Here, we apply graph theory to compare key signatures of such networks in hi...

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Autores principales: Chennu, Srivas, Finoia, Paola, Kamau, Evelyn, Allanson, Judith, Williams, Guy B., Monti, Martin M., Noreika, Valdas, Arnatkeviciute, Aurina, Canales-Johnson, Andrés, Olivares, Francisco, Cabezas-Soto, Daniela, Menon, David K., Pickard, John D., Owen, Adrian M., Bekinschtein, Tristan A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4199497/
https://www.ncbi.nlm.nih.gov/pubmed/25329398
http://dx.doi.org/10.1371/journal.pcbi.1003887
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author Chennu, Srivas
Finoia, Paola
Kamau, Evelyn
Allanson, Judith
Williams, Guy B.
Monti, Martin M.
Noreika, Valdas
Arnatkeviciute, Aurina
Canales-Johnson, Andrés
Olivares, Francisco
Cabezas-Soto, Daniela
Menon, David K.
Pickard, John D.
Owen, Adrian M.
Bekinschtein, Tristan A.
author_facet Chennu, Srivas
Finoia, Paola
Kamau, Evelyn
Allanson, Judith
Williams, Guy B.
Monti, Martin M.
Noreika, Valdas
Arnatkeviciute, Aurina
Canales-Johnson, Andrés
Olivares, Francisco
Cabezas-Soto, Daniela
Menon, David K.
Pickard, John D.
Owen, Adrian M.
Bekinschtein, Tristan A.
author_sort Chennu, Srivas
collection PubMed
description Theoretical advances in the science of consciousness have proposed that it is concomitant with balanced cortical integration and differentiation, enabled by efficient networks of information transfer across multiple scales. Here, we apply graph theory to compare key signatures of such networks in high-density electroencephalographic data from 32 patients with chronic disorders of consciousness, against normative data from healthy controls. Based on connectivity within canonical frequency bands, we found that patient networks had reduced local and global efficiency, and fewer hubs in the alpha band. We devised a novel topographical metric, termed modular span, which showed that the alpha network modules in patients were also spatially circumscribed, lacking the structured long-distance interactions commonly observed in the healthy controls. Importantly however, these differences between graph-theoretic metrics were partially reversed in delta and theta band networks, which were also significantly more similar to each other in patients than controls. Going further, we found that metrics of alpha network efficiency also correlated with the degree of behavioural awareness. Intriguingly, some patients in behaviourally unresponsive vegetative states who demonstrated evidence of covert awareness with functional neuroimaging stood out from this trend: they had alpha networks that were remarkably well preserved and similar to those observed in the controls. Taken together, our findings inform current understanding of disorders of consciousness by highlighting the distinctive brain networks that characterise them. In the significant minority of vegetative patients who follow commands in neuroimaging tests, they point to putative network mechanisms that could support cognitive function and consciousness despite profound behavioural impairment.
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spelling pubmed-41994972014-10-21 Spectral Signatures of Reorganised Brain Networks in Disorders of Consciousness Chennu, Srivas Finoia, Paola Kamau, Evelyn Allanson, Judith Williams, Guy B. Monti, Martin M. Noreika, Valdas Arnatkeviciute, Aurina Canales-Johnson, Andrés Olivares, Francisco Cabezas-Soto, Daniela Menon, David K. Pickard, John D. Owen, Adrian M. Bekinschtein, Tristan A. PLoS Comput Biol Research Article Theoretical advances in the science of consciousness have proposed that it is concomitant with balanced cortical integration and differentiation, enabled by efficient networks of information transfer across multiple scales. Here, we apply graph theory to compare key signatures of such networks in high-density electroencephalographic data from 32 patients with chronic disorders of consciousness, against normative data from healthy controls. Based on connectivity within canonical frequency bands, we found that patient networks had reduced local and global efficiency, and fewer hubs in the alpha band. We devised a novel topographical metric, termed modular span, which showed that the alpha network modules in patients were also spatially circumscribed, lacking the structured long-distance interactions commonly observed in the healthy controls. Importantly however, these differences between graph-theoretic metrics were partially reversed in delta and theta band networks, which were also significantly more similar to each other in patients than controls. Going further, we found that metrics of alpha network efficiency also correlated with the degree of behavioural awareness. Intriguingly, some patients in behaviourally unresponsive vegetative states who demonstrated evidence of covert awareness with functional neuroimaging stood out from this trend: they had alpha networks that were remarkably well preserved and similar to those observed in the controls. Taken together, our findings inform current understanding of disorders of consciousness by highlighting the distinctive brain networks that characterise them. In the significant minority of vegetative patients who follow commands in neuroimaging tests, they point to putative network mechanisms that could support cognitive function and consciousness despite profound behavioural impairment. Public Library of Science 2014-10-16 /pmc/articles/PMC4199497/ /pubmed/25329398 http://dx.doi.org/10.1371/journal.pcbi.1003887 Text en © 2014 Chennu et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Chennu, Srivas
Finoia, Paola
Kamau, Evelyn
Allanson, Judith
Williams, Guy B.
Monti, Martin M.
Noreika, Valdas
Arnatkeviciute, Aurina
Canales-Johnson, Andrés
Olivares, Francisco
Cabezas-Soto, Daniela
Menon, David K.
Pickard, John D.
Owen, Adrian M.
Bekinschtein, Tristan A.
Spectral Signatures of Reorganised Brain Networks in Disorders of Consciousness
title Spectral Signatures of Reorganised Brain Networks in Disorders of Consciousness
title_full Spectral Signatures of Reorganised Brain Networks in Disorders of Consciousness
title_fullStr Spectral Signatures of Reorganised Brain Networks in Disorders of Consciousness
title_full_unstemmed Spectral Signatures of Reorganised Brain Networks in Disorders of Consciousness
title_short Spectral Signatures of Reorganised Brain Networks in Disorders of Consciousness
title_sort spectral signatures of reorganised brain networks in disorders of consciousness
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4199497/
https://www.ncbi.nlm.nih.gov/pubmed/25329398
http://dx.doi.org/10.1371/journal.pcbi.1003887
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