Muting, not fragmentation, of functional brain networks under general anesthesia

Changes in resting-state functional connectivity (rs-FC) under general anesthesia have been widely studied with the goal of identifying neural signatures of consciousness. This work has commonly revealed an apparent fragmentation of whole-brain network structure during unconsciousness, which has bee...

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Main Authors: Corson N. Areshenkoff, Joseph Y. Nashed, R. Matthew Hutchison, Melina Hutchison, Ron Levy, Douglas J. Cook, Ravi S. Menon, Stefan Everling, Jason P. Gallivan
Format: Article
Language:English
Published: Elsevier 2021-05-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811921001075
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author Corson N. Areshenkoff
Joseph Y. Nashed
R. Matthew Hutchison
Melina Hutchison
Ron Levy
Douglas J. Cook
Ravi S. Menon
Stefan Everling
Jason P. Gallivan
author_facet Corson N. Areshenkoff
Joseph Y. Nashed
R. Matthew Hutchison
Melina Hutchison
Ron Levy
Douglas J. Cook
Ravi S. Menon
Stefan Everling
Jason P. Gallivan
author_sort Corson N. Areshenkoff
collection DOAJ
description Changes in resting-state functional connectivity (rs-FC) under general anesthesia have been widely studied with the goal of identifying neural signatures of consciousness. This work has commonly revealed an apparent fragmentation of whole-brain network structure during unconsciousness, which has been interpreted as reflecting a break-down in connectivity and a disruption of the brain’s ability to integrate information. Here we show, by studying rs-FC under varying depths of isoflurane-induced anesthesia in nonhuman primates, that this apparent fragmentation, rather than reflecting an actual change in network structure, can be simply explained as the result of a global reduction in FC. Specifically, by comparing the actual FC data to surrogate data sets that we derived to test competing hypotheses of how FC changes as a function of dose, we found that increases in whole-brain modularity and the number of network communities – considered hallmarks of fragmentation – are artifacts of constructing FC networks by thresholding based on correlation magnitude. Taken together, our findings suggest that deepening levels of unconsciousness are instead associated with the increasingly muted expression of functional networks, an observation that constrains current interpretations as to how anesthesia-induced FC changes map onto existing neurobiological theories of consciousness.
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spelling doaj.art-a76c38f0abcc430fa33ed236ed373f4b2022-12-21T18:48:15ZengElsevierNeuroImage1095-95722021-05-01231117830Muting, not fragmentation, of functional brain networks under general anesthesiaCorson N. Areshenkoff0Joseph Y. Nashed1R. Matthew Hutchison2Melina Hutchison3Ron Levy4Douglas J. Cook5Ravi S. Menon6Stefan Everling7Jason P. Gallivan8Corresponding author at: Centre for Neuroscience Studies, Queens University, Kingston, ON, Canada.; Centre for Neuroscience Studies, Queens University, Kingston, ON, Canada; Department of Psychology, Queens University, Kingston, ON, CanadaCentre for Neuroscience Studies, Queens University, Kingston, ON, CanadaBiogen, Cambridge, MA, USAMassachusetts Eye and Ear Infirmary, Boston, MA, USACentre for Neuroscience Studies, Queens University, Kingston, ON, Canada; Department of Surgery, Queens University, Kingston, ON, CanadaCentre for Neuroscience Studies, Queens University, Kingston, ON, Canada; Department of Surgery, Queens University, Kingston, ON, CanadaRobarts Research Institute, University of Western Ontario, London, ON, CanadaRobarts Research Institute, University of Western Ontario, London, ON, Canada; Department of Physiology and Pharmacology, University of Western Ontario, London, ON, CanadaCentre for Neuroscience Studies, Queens University, Kingston, ON, Canada; Department of Psychology, Queens University, Kingston, ON, CanadaChanges in resting-state functional connectivity (rs-FC) under general anesthesia have been widely studied with the goal of identifying neural signatures of consciousness. This work has commonly revealed an apparent fragmentation of whole-brain network structure during unconsciousness, which has been interpreted as reflecting a break-down in connectivity and a disruption of the brain’s ability to integrate information. Here we show, by studying rs-FC under varying depths of isoflurane-induced anesthesia in nonhuman primates, that this apparent fragmentation, rather than reflecting an actual change in network structure, can be simply explained as the result of a global reduction in FC. Specifically, by comparing the actual FC data to surrogate data sets that we derived to test competing hypotheses of how FC changes as a function of dose, we found that increases in whole-brain modularity and the number of network communities – considered hallmarks of fragmentation – are artifacts of constructing FC networks by thresholding based on correlation magnitude. Taken together, our findings suggest that deepening levels of unconsciousness are instead associated with the increasingly muted expression of functional networks, an observation that constrains current interpretations as to how anesthesia-induced FC changes map onto existing neurobiological theories of consciousness.http://www.sciencedirect.com/science/article/pii/S1053811921001075Brain networkFunctional connectivityConsciousnessAnesthesia
spellingShingle Corson N. Areshenkoff
Joseph Y. Nashed
R. Matthew Hutchison
Melina Hutchison
Ron Levy
Douglas J. Cook
Ravi S. Menon
Stefan Everling
Jason P. Gallivan
Muting, not fragmentation, of functional brain networks under general anesthesia
NeuroImage
Brain network
Functional connectivity
Consciousness
Anesthesia
title Muting, not fragmentation, of functional brain networks under general anesthesia
title_full Muting, not fragmentation, of functional brain networks under general anesthesia
title_fullStr Muting, not fragmentation, of functional brain networks under general anesthesia
title_full_unstemmed Muting, not fragmentation, of functional brain networks under general anesthesia
title_short Muting, not fragmentation, of functional brain networks under general anesthesia
title_sort muting not fragmentation of functional brain networks under general anesthesia
topic Brain network
Functional connectivity
Consciousness
Anesthesia
url http://www.sciencedirect.com/science/article/pii/S1053811921001075
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