Signature of consciousness in brain-wide synchronization patterns of monkey and human fMRI signals

During the sleep-wake cycle, the brain undergoes profound dynamical changes, which manifest subjectively as transitions between conscious experience and unconsciousness. Yet, neurophysiological signatures that can objectively distinguish different consciousness states based are scarce. Here, we show...

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Main Authors: Gerald Hahn, Gorka Zamora-López, Lynn Uhrig, Enzo Tagliazucchi, Helmut Laufs, Dante Mantini, Morten L Kringelbach, Bechir Jarraya, Gustavo Deco
Format: Article
Language:English
Published: Elsevier 2021-02-01
Series:NeuroImage
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811920309551
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author Gerald Hahn
Gorka Zamora-López
Lynn Uhrig
Enzo Tagliazucchi
Helmut Laufs
Dante Mantini
Morten L Kringelbach
Bechir Jarraya
Gustavo Deco
author_facet Gerald Hahn
Gorka Zamora-López
Lynn Uhrig
Enzo Tagliazucchi
Helmut Laufs
Dante Mantini
Morten L Kringelbach
Bechir Jarraya
Gustavo Deco
author_sort Gerald Hahn
collection DOAJ
description During the sleep-wake cycle, the brain undergoes profound dynamical changes, which manifest subjectively as transitions between conscious experience and unconsciousness. Yet, neurophysiological signatures that can objectively distinguish different consciousness states based are scarce. Here, we show that differences in the level of brain-wide signals can reliably distinguish different stages of sleep and anesthesia from the awake state in human and monkey fMRI resting state data. Moreover, a whole-brain computational model can faithfully reproduce changes in global synchronization and other metrics such as functional connectivity, structure-function relationship, integration and segregation across vigilance states. We demonstrate that the awake brain is close to a Hopf bifurcation, which naturally coincides with the emergence of globally correlated fMRI signals. Furthermore, simulating lesions of individual brain areas highlights the importance of connectivity hubs in the posterior brain and subcortical nuclei for maintaining the model in the awake state, as predicted by graph-theoretical analyses of structural data.
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spelling doaj.art-3c67bec061f14652b0bf85271bbb2d512022-12-21T18:19:51ZengElsevierNeuroImage1095-95722021-02-01226117470Signature of consciousness in brain-wide synchronization patterns of monkey and human fMRI signalsGerald Hahn0Gorka Zamora-López1Lynn Uhrig2Enzo Tagliazucchi3Helmut Laufs4Dante Mantini5Morten L Kringelbach6Bechir Jarraya7Gustavo Deco8Center for Brain and Cognition, Computational Neuroscience Group, Department of Information and Communication Technologies, Universitat Pompeu Fabra, Barcelona, Spain; Corresponding author.Center for Brain and Cognition, Computational Neuroscience Group, Department of Information and Communication Technologies, Universitat Pompeu Fabra, Barcelona, SpainCommissariat à l'Énergie Atomique et aux Énergies Alternatives, Direction de la Recherche Fondamentale, NeuroSpin Center, Gif-sur-Yvette, France; Cognitive Neuroimaging Unit, Institut National de la Santé et de la Recherche Médicale U992, Gif-sur-Yvette, FranceInstitute for Medical Psychology, Christian Albrechts University, Kiel, Germany; Department of Neurology and Brain Imaging Center, Goethe University, Frankfurt am Main, Germany; Department of Physics, University of Buenos Aires, Argentina; National Scientific and Technical Research Council (CONICET), Buenos Aires, ArgentinaDepartment of Neurology and Brain Imaging Center, Goethe University, Frankfurt am Main, Germany; Department of Neurology, Christian Albrechts University, Kiel, GermanyResearch Center for Motor Control and Neuroplasticity, KU Leuven, Leuven, Belgium; Brain Imaging and Neural Dynamics Research Group, IRCSS San Camillo Hospital, Venice, ItalyDepartment of Psychiatry, University of Oxford, Oxford, United Kingdom; Center for Music in the Brain, Department of Clinical Medicine, Aarhus University, Denmark; Centre for Eudaimonia and Human Flourishing, University of Oxford, UKCommissariat à l'Énergie Atomique et aux Énergies Alternatives, Direction de la Recherche Fondamentale, NeuroSpin Center, Gif-sur-Yvette, France; Cognitive Neuroimaging Unit, Institut National de la Santé et de la Recherche Médicale U992, Gif-sur-Yvette, France; University of Versailles Saint-Quentin-en-Yvelines, Université Paris-Saclay, Versailles, France; Neuromodulation Unit, Foch Hospital, Suresnes, FranceCenter for Brain and Cognition, Computational Neuroscience Group, Department of Information and Communication Technologies, Universitat Pompeu Fabra, Barcelona, Spain; Institució Catalana de la Recerca i Estudis Avançats, Barcelona, Spain; Department of Neuropsychology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany; School of Psychological Sciences, Turner Institute for Brain and Mental Health, Monash University, Melbourne, Clayton, AustraliaDuring the sleep-wake cycle, the brain undergoes profound dynamical changes, which manifest subjectively as transitions between conscious experience and unconsciousness. Yet, neurophysiological signatures that can objectively distinguish different consciousness states based are scarce. Here, we show that differences in the level of brain-wide signals can reliably distinguish different stages of sleep and anesthesia from the awake state in human and monkey fMRI resting state data. Moreover, a whole-brain computational model can faithfully reproduce changes in global synchronization and other metrics such as functional connectivity, structure-function relationship, integration and segregation across vigilance states. We demonstrate that the awake brain is close to a Hopf bifurcation, which naturally coincides with the emergence of globally correlated fMRI signals. Furthermore, simulating lesions of individual brain areas highlights the importance of connectivity hubs in the posterior brain and subcortical nuclei for maintaining the model in the awake state, as predicted by graph-theoretical analyses of structural data.http://www.sciencedirect.com/science/article/pii/S1053811920309551
spellingShingle Gerald Hahn
Gorka Zamora-López
Lynn Uhrig
Enzo Tagliazucchi
Helmut Laufs
Dante Mantini
Morten L Kringelbach
Bechir Jarraya
Gustavo Deco
Signature of consciousness in brain-wide synchronization patterns of monkey and human fMRI signals
NeuroImage
title Signature of consciousness in brain-wide synchronization patterns of monkey and human fMRI signals
title_full Signature of consciousness in brain-wide synchronization patterns of monkey and human fMRI signals
title_fullStr Signature of consciousness in brain-wide synchronization patterns of monkey and human fMRI signals
title_full_unstemmed Signature of consciousness in brain-wide synchronization patterns of monkey and human fMRI signals
title_short Signature of consciousness in brain-wide synchronization patterns of monkey and human fMRI signals
title_sort signature of consciousness in brain wide synchronization patterns of monkey and human fmri signals
url http://www.sciencedirect.com/science/article/pii/S1053811920309551
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