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Segregation, integration, and balance of large-scale resting brain networks configure different cognitive abilities

Diverse cognitive processes set different demands on locally segregated and globally integrated brain activity. However, it remains an open question how resting brains configure their functional organization to balance the demands on network segregation and integration to best serve cognition. Here...

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Autores principales: Wang, Rong, Liu, Mianxin, Cheng, Xinhong, Wu, Ying, Hildebrandt, Andrea, Zhou, Changsong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8201916/
https://www.ncbi.nlm.nih.gov/pubmed/34074762
http://dx.doi.org/10.1073/pnas.2022288118
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author Wang, Rong
Liu, Mianxin
Cheng, Xinhong
Wu, Ying
Hildebrandt, Andrea
Zhou, Changsong
author_facet Wang, Rong
Liu, Mianxin
Cheng, Xinhong
Wu, Ying
Hildebrandt, Andrea
Zhou, Changsong
author_sort Wang, Rong
collection PubMed
description Diverse cognitive processes set different demands on locally segregated and globally integrated brain activity. However, it remains an open question how resting brains configure their functional organization to balance the demands on network segregation and integration to best serve cognition. Here we use an eigenmode-based approach to identify hierarchical modules in functional brain networks and quantify the functional balance between network segregation and integration. In a large sample of healthy young adults ([Formula: see text] = 991), we combine the whole-brain resting state functional magnetic resonance imaging (fMRI) data with a mean-filed model on the structural network derived from diffusion tensor imaging and demonstrate that resting brain networks are on average close to a balanced state. This state allows for a balanced time dwelling at segregated and integrated configurations and highly flexible switching between them. Furthermore, we employ structural equation modeling to estimate general and domain-specific cognitive phenotypes from nine tasks and demonstrate that network segregation, integration, and their balance in resting brains predict individual differences in diverse cognitive phenotypes. More specifically, stronger integration is associated with better general cognitive ability, stronger segregation fosters crystallized intelligence and processing speed, and an individual’s tendency toward balance supports better memory. Our findings provide a comprehensive and deep understanding of the brain’s functioning principles in supporting diverse functional demands and cognitive abilities and advance modern network neuroscience theories of human cognition.
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spelling pubmed-82019162021-06-24 Segregation, integration, and balance of large-scale resting brain networks configure different cognitive abilities Wang, Rong Liu, Mianxin Cheng, Xinhong Wu, Ying Hildebrandt, Andrea Zhou, Changsong Proc Natl Acad Sci U S A Biological Sciences Diverse cognitive processes set different demands on locally segregated and globally integrated brain activity. However, it remains an open question how resting brains configure their functional organization to balance the demands on network segregation and integration to best serve cognition. Here we use an eigenmode-based approach to identify hierarchical modules in functional brain networks and quantify the functional balance between network segregation and integration. In a large sample of healthy young adults ([Formula: see text] = 991), we combine the whole-brain resting state functional magnetic resonance imaging (fMRI) data with a mean-filed model on the structural network derived from diffusion tensor imaging and demonstrate that resting brain networks are on average close to a balanced state. This state allows for a balanced time dwelling at segregated and integrated configurations and highly flexible switching between them. Furthermore, we employ structural equation modeling to estimate general and domain-specific cognitive phenotypes from nine tasks and demonstrate that network segregation, integration, and their balance in resting brains predict individual differences in diverse cognitive phenotypes. More specifically, stronger integration is associated with better general cognitive ability, stronger segregation fosters crystallized intelligence and processing speed, and an individual’s tendency toward balance supports better memory. Our findings provide a comprehensive and deep understanding of the brain’s functioning principles in supporting diverse functional demands and cognitive abilities and advance modern network neuroscience theories of human cognition. National Academy of Sciences 2021-06-08 2021-05-31 /pmc/articles/PMC8201916/ /pubmed/34074762 http://dx.doi.org/10.1073/pnas.2022288118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Wang, Rong
Liu, Mianxin
Cheng, Xinhong
Wu, Ying
Hildebrandt, Andrea
Zhou, Changsong
Segregation, integration, and balance of large-scale resting brain networks configure different cognitive abilities
title Segregation, integration, and balance of large-scale resting brain networks configure different cognitive abilities
title_full Segregation, integration, and balance of large-scale resting brain networks configure different cognitive abilities
title_fullStr Segregation, integration, and balance of large-scale resting brain networks configure different cognitive abilities
title_full_unstemmed Segregation, integration, and balance of large-scale resting brain networks configure different cognitive abilities
title_short Segregation, integration, and balance of large-scale resting brain networks configure different cognitive abilities
title_sort segregation, integration, and balance of large-scale resting brain networks configure different cognitive abilities
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8201916/
https://www.ncbi.nlm.nih.gov/pubmed/34074762
http://dx.doi.org/10.1073/pnas.2022288118
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