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Dynamic changes in brain lateralization correlate with human cognitive performance

Hemispheric lateralization constitutes a core architectural principle of human brain organization underlying cognition, often argued to represent a stable, trait-like feature. However, emerging evidence underlines the inherently dynamic nature of brain networks, in which time-resolved alterations in...

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Autores principales: Wu, Xinran, Kong, Xiangzhen, Vatansever, Deniz, Liu, Zhaowen, Zhang, Kai, Sahakian, Barbara J., Robbins, Trevor W., Feng, Jianfeng, Thompson, Paul, Zhang, Jie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8929635/
https://www.ncbi.nlm.nih.gov/pubmed/35298460
http://dx.doi.org/10.1371/journal.pbio.3001560
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author Wu, Xinran
Kong, Xiangzhen
Vatansever, Deniz
Liu, Zhaowen
Zhang, Kai
Sahakian, Barbara J.
Robbins, Trevor W.
Feng, Jianfeng
Thompson, Paul
Zhang, Jie
author_facet Wu, Xinran
Kong, Xiangzhen
Vatansever, Deniz
Liu, Zhaowen
Zhang, Kai
Sahakian, Barbara J.
Robbins, Trevor W.
Feng, Jianfeng
Thompson, Paul
Zhang, Jie
author_sort Wu, Xinran
collection PubMed
description Hemispheric lateralization constitutes a core architectural principle of human brain organization underlying cognition, often argued to represent a stable, trait-like feature. However, emerging evidence underlines the inherently dynamic nature of brain networks, in which time-resolved alterations in functional lateralization remain uncharted. Integrating dynamic network approaches with the concept of hemispheric laterality, we map the spatiotemporal architecture of whole-brain lateralization in a large sample of high-quality resting-state fMRI data (N = 991, Human Connectome Project). We reveal distinct laterality dynamics across lower-order sensorimotor systems and higher-order associative networks. Specifically, we expose 2 aspects of the laterality dynamics: laterality fluctuations (LF), defined as the standard deviation of laterality time series, and laterality reversal (LR), referring to the number of zero crossings in laterality time series. These 2 measures are associated with moderate and extreme changes in laterality over time, respectively. While LF depict positive association with language function and cognitive flexibility, LR shows a negative association with the same cognitive abilities. These opposing interactions indicate a dynamic balance between intra and interhemispheric communication, i.e., segregation and integration of information across hemispheres. Furthermore, in their time-resolved laterality index, the default mode and language networks correlate negatively with visual/sensorimotor and attention networks, which are linked to better cognitive abilities. Finally, the laterality dynamics are associated with functional connectivity changes of higher-order brain networks and correlate with regional metabolism and structural connectivity. Our results provide insights into the adaptive nature of the lateralized brain and new perspectives for future studies of human cognition, genetics, and brain disorders.
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spelling pubmed-89296352022-03-18 Dynamic changes in brain lateralization correlate with human cognitive performance Wu, Xinran Kong, Xiangzhen Vatansever, Deniz Liu, Zhaowen Zhang, Kai Sahakian, Barbara J. Robbins, Trevor W. Feng, Jianfeng Thompson, Paul Zhang, Jie PLoS Biol Research Article Hemispheric lateralization constitutes a core architectural principle of human brain organization underlying cognition, often argued to represent a stable, trait-like feature. However, emerging evidence underlines the inherently dynamic nature of brain networks, in which time-resolved alterations in functional lateralization remain uncharted. Integrating dynamic network approaches with the concept of hemispheric laterality, we map the spatiotemporal architecture of whole-brain lateralization in a large sample of high-quality resting-state fMRI data (N = 991, Human Connectome Project). We reveal distinct laterality dynamics across lower-order sensorimotor systems and higher-order associative networks. Specifically, we expose 2 aspects of the laterality dynamics: laterality fluctuations (LF), defined as the standard deviation of laterality time series, and laterality reversal (LR), referring to the number of zero crossings in laterality time series. These 2 measures are associated with moderate and extreme changes in laterality over time, respectively. While LF depict positive association with language function and cognitive flexibility, LR shows a negative association with the same cognitive abilities. These opposing interactions indicate a dynamic balance between intra and interhemispheric communication, i.e., segregation and integration of information across hemispheres. Furthermore, in their time-resolved laterality index, the default mode and language networks correlate negatively with visual/sensorimotor and attention networks, which are linked to better cognitive abilities. Finally, the laterality dynamics are associated with functional connectivity changes of higher-order brain networks and correlate with regional metabolism and structural connectivity. Our results provide insights into the adaptive nature of the lateralized brain and new perspectives for future studies of human cognition, genetics, and brain disorders. Public Library of Science 2022-03-17 /pmc/articles/PMC8929635/ /pubmed/35298460 http://dx.doi.org/10.1371/journal.pbio.3001560 Text en © 2022 Wu et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://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
Wu, Xinran
Kong, Xiangzhen
Vatansever, Deniz
Liu, Zhaowen
Zhang, Kai
Sahakian, Barbara J.
Robbins, Trevor W.
Feng, Jianfeng
Thompson, Paul
Zhang, Jie
Dynamic changes in brain lateralization correlate with human cognitive performance
title Dynamic changes in brain lateralization correlate with human cognitive performance
title_full Dynamic changes in brain lateralization correlate with human cognitive performance
title_fullStr Dynamic changes in brain lateralization correlate with human cognitive performance
title_full_unstemmed Dynamic changes in brain lateralization correlate with human cognitive performance
title_short Dynamic changes in brain lateralization correlate with human cognitive performance
title_sort dynamic changes in brain lateralization correlate with human cognitive performance
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8929635/
https://www.ncbi.nlm.nih.gov/pubmed/35298460
http://dx.doi.org/10.1371/journal.pbio.3001560
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