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Transitions in information processing dynamics at the whole-brain network level are driven by alterations in neural gain
A key component of the flexibility and complexity of the brain is its ability to dynamically adapt its functional network structure between integrated and segregated brain states depending on the demands of different cognitive tasks. Integrated states are prevalent when performing tasks of high comp...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6793849/ https://www.ncbi.nlm.nih.gov/pubmed/31613882 http://dx.doi.org/10.1371/journal.pcbi.1006957 |
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author | Li, Mike Han, Yinuo Aburn, Matthew J. Breakspear, Michael Poldrack, Russell A. Shine, James M. Lizier, Joseph T. |
author_facet | Li, Mike Han, Yinuo Aburn, Matthew J. Breakspear, Michael Poldrack, Russell A. Shine, James M. Lizier, Joseph T. |
author_sort | Li, Mike |
collection | PubMed |
description | A key component of the flexibility and complexity of the brain is its ability to dynamically adapt its functional network structure between integrated and segregated brain states depending on the demands of different cognitive tasks. Integrated states are prevalent when performing tasks of high complexity, such as maintaining items in working memory, consistent with models of a global workspace architecture. Recent work has suggested that the balance between integration and segregation is under the control of ascending neuromodulatory systems, such as the noradrenergic system, via changes in neural gain (in terms of the amplification and non-linearity in stimulus-response transfer function of brain regions). In a previous large-scale nonlinear oscillator model of neuronal network dynamics, we showed that manipulating neural gain parameters led to a ‘critical’ transition in phase synchrony that was associated with a shift from segregated to integrated topology, thus confirming our original prediction. In this study, we advance these results by demonstrating that the gain-mediated phase transition is characterized by a shift in the underlying dynamics of neural information processing. Specifically, the dynamics of the subcritical (segregated) regime are dominated by information storage, whereas the supercritical (integrated) regime is associated with increased information transfer (measured via transfer entropy). Operating near to the critical regime with respect to modulating neural gain parameters would thus appear to provide computational advantages, offering flexibility in the information processing that can be performed with only subtle changes in gain control. Our results thus link studies of whole-brain network topology and the ascending arousal system with information processing dynamics, and suggest that the constraints imposed by the ascending arousal system constrain low-dimensional modes of information processing within the brain. |
format | Online Article Text |
id | pubmed-6793849 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-67938492019-10-25 Transitions in information processing dynamics at the whole-brain network level are driven by alterations in neural gain Li, Mike Han, Yinuo Aburn, Matthew J. Breakspear, Michael Poldrack, Russell A. Shine, James M. Lizier, Joseph T. PLoS Comput Biol Research Article A key component of the flexibility and complexity of the brain is its ability to dynamically adapt its functional network structure between integrated and segregated brain states depending on the demands of different cognitive tasks. Integrated states are prevalent when performing tasks of high complexity, such as maintaining items in working memory, consistent with models of a global workspace architecture. Recent work has suggested that the balance between integration and segregation is under the control of ascending neuromodulatory systems, such as the noradrenergic system, via changes in neural gain (in terms of the amplification and non-linearity in stimulus-response transfer function of brain regions). In a previous large-scale nonlinear oscillator model of neuronal network dynamics, we showed that manipulating neural gain parameters led to a ‘critical’ transition in phase synchrony that was associated with a shift from segregated to integrated topology, thus confirming our original prediction. In this study, we advance these results by demonstrating that the gain-mediated phase transition is characterized by a shift in the underlying dynamics of neural information processing. Specifically, the dynamics of the subcritical (segregated) regime are dominated by information storage, whereas the supercritical (integrated) regime is associated with increased information transfer (measured via transfer entropy). Operating near to the critical regime with respect to modulating neural gain parameters would thus appear to provide computational advantages, offering flexibility in the information processing that can be performed with only subtle changes in gain control. Our results thus link studies of whole-brain network topology and the ascending arousal system with information processing dynamics, and suggest that the constraints imposed by the ascending arousal system constrain low-dimensional modes of information processing within the brain. Public Library of Science 2019-10-15 /pmc/articles/PMC6793849/ /pubmed/31613882 http://dx.doi.org/10.1371/journal.pcbi.1006957 Text en © 2019 Li 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 (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Li, Mike Han, Yinuo Aburn, Matthew J. Breakspear, Michael Poldrack, Russell A. Shine, James M. Lizier, Joseph T. Transitions in information processing dynamics at the whole-brain network level are driven by alterations in neural gain |
title | Transitions in information processing dynamics at the whole-brain network level are driven by alterations in neural gain |
title_full | Transitions in information processing dynamics at the whole-brain network level are driven by alterations in neural gain |
title_fullStr | Transitions in information processing dynamics at the whole-brain network level are driven by alterations in neural gain |
title_full_unstemmed | Transitions in information processing dynamics at the whole-brain network level are driven by alterations in neural gain |
title_short | Transitions in information processing dynamics at the whole-brain network level are driven by alterations in neural gain |
title_sort | transitions in information processing dynamics at the whole-brain network level are driven by alterations in neural gain |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6793849/ https://www.ncbi.nlm.nih.gov/pubmed/31613882 http://dx.doi.org/10.1371/journal.pcbi.1006957 |
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