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Multilayer network switching rate predicts brain performance

Large-scale brain dynamics are characterized by repeating spatiotemporal connectivity patterns that reflect a range of putative different brain states that underlie the dynamic repertoire of brain functions. The role of transition between brain networks is poorly understood, and whether switching be...

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Autores principales: Pedersen, Mangor, Zalesky, Andrew, Omidvarnia, Amir, Jackson, Graeme D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6310789/
https://www.ncbi.nlm.nih.gov/pubmed/30545918
http://dx.doi.org/10.1073/pnas.1814785115
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author Pedersen, Mangor
Zalesky, Andrew
Omidvarnia, Amir
Jackson, Graeme D.
author_facet Pedersen, Mangor
Zalesky, Andrew
Omidvarnia, Amir
Jackson, Graeme D.
author_sort Pedersen, Mangor
collection PubMed
description Large-scale brain dynamics are characterized by repeating spatiotemporal connectivity patterns that reflect a range of putative different brain states that underlie the dynamic repertoire of brain functions. The role of transition between brain networks is poorly understood, and whether switching between these states is important for behavior has been little studied. Our aim was to model switching between functional brain networks using multilayer network methods and test for associations between model parameters and behavioral measures. We calculated time-resolved fMRI connectivity in 1,003 healthy human adults from the Human Connectome Project. The time-resolved fMRI connectivity data were used to generate a spatiotemporal multilayer modularity model enabling us to quantify network switching, which we define as the rate at which each brain region transits between different networks. We found (i) an inverse relationship between network switching and connectivity dynamics, where the latter was defined in terms of time-resolved fMRI connections with variance in time that significantly exceeded phase-randomized surrogate data; (ii) brain connectivity was lower during intervals of network switching; (iii) brain areas with frequent network switching had greater temporal complexity; (iv) brain areas with high network switching were located in association cortices; and (v) using cross-validated elastic net regression, network switching predicted intersubject variation in working memory performance, planning/reasoning, and amount of sleep. Our findings shed light on the importance of brain dynamics predicting task performance and amount of sleep. The ability to switch between network configurations thus appears to be a fundamental feature of optimal brain function.
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spelling pubmed-63107892019-01-04 Multilayer network switching rate predicts brain performance Pedersen, Mangor Zalesky, Andrew Omidvarnia, Amir Jackson, Graeme D. Proc Natl Acad Sci U S A Biological Sciences Large-scale brain dynamics are characterized by repeating spatiotemporal connectivity patterns that reflect a range of putative different brain states that underlie the dynamic repertoire of brain functions. The role of transition between brain networks is poorly understood, and whether switching between these states is important for behavior has been little studied. Our aim was to model switching between functional brain networks using multilayer network methods and test for associations between model parameters and behavioral measures. We calculated time-resolved fMRI connectivity in 1,003 healthy human adults from the Human Connectome Project. The time-resolved fMRI connectivity data were used to generate a spatiotemporal multilayer modularity model enabling us to quantify network switching, which we define as the rate at which each brain region transits between different networks. We found (i) an inverse relationship between network switching and connectivity dynamics, where the latter was defined in terms of time-resolved fMRI connections with variance in time that significantly exceeded phase-randomized surrogate data; (ii) brain connectivity was lower during intervals of network switching; (iii) brain areas with frequent network switching had greater temporal complexity; (iv) brain areas with high network switching were located in association cortices; and (v) using cross-validated elastic net regression, network switching predicted intersubject variation in working memory performance, planning/reasoning, and amount of sleep. Our findings shed light on the importance of brain dynamics predicting task performance and amount of sleep. The ability to switch between network configurations thus appears to be a fundamental feature of optimal brain function. National Academy of Sciences 2018-12-26 2018-12-13 /pmc/articles/PMC6310789/ /pubmed/30545918 http://dx.doi.org/10.1073/pnas.1814785115 Text en Copyright © 2018 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Pedersen, Mangor
Zalesky, Andrew
Omidvarnia, Amir
Jackson, Graeme D.
Multilayer network switching rate predicts brain performance
title Multilayer network switching rate predicts brain performance
title_full Multilayer network switching rate predicts brain performance
title_fullStr Multilayer network switching rate predicts brain performance
title_full_unstemmed Multilayer network switching rate predicts brain performance
title_short Multilayer network switching rate predicts brain performance
title_sort multilayer network switching rate predicts brain performance
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6310789/
https://www.ncbi.nlm.nih.gov/pubmed/30545918
http://dx.doi.org/10.1073/pnas.1814785115
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