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Dynamic changes in brain lateralization correlate with human cognitive performance

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Wu, Xinran, Kong, Xiangzhen, Vatansever, Deniz, Liu, ZhaoWen, Zhang, Kai, Sahakian, Barbara J., Robbins, Trevor W., Feng, Jianfeng, Thompson, Paul and Zhang, Jie (2022) Dynamic changes in brain lateralization correlate with human cognitive performance. PLoS Biology, 20 (3). e3001560. doi:10.1371/journal.pbio.3001560

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Official URL: https://doi.org/10.1371/journal.pbio.3001560

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Abstract

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.

Item Type: Journal Article
Subjects: B Philosophy. Psychology. Religion > BF Psychology
Q Science > QP Physiology
Divisions: Faculty of Science, Engineering and Medicine > Science > Computer Science
SWORD Depositor: Library Publications Router
Library of Congress Subject Headings (LCSH): Cerebral dominance, Cerebral hemispheres, Brain , Cognition, Brain -- Localization of functions, Laterality
Journal or Publication Title: PLoS Biology
Publisher: Public Library of Science
ISSN: 1545-7885
Official Date: 17 March 2022
Dates:
DateEvent
17 March 2022Published
31 January 2022Accepted
Volume: 20
Number: 3
Article Number: e3001560
DOI: 10.1371/journal.pbio.3001560
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
2021ZD0200204 (Science and Technology Innovation 2030 - Brain Science and Brain-Inspired Intelligence Project)Chinese academy of scienceshttps://english.cas.cn/
2018SHZDZX01Science and Technology Commission of Shanghai Municipalityhttp://dx.doi.org/10.13039/501100003399
32171031[NSFC] National Natural Science Foundation of Chinahttp://dx.doi.org/10.13039/501100001809
UNSPECIFIEDZJLabUNSPECIFIED
2021XZZX006Fundamental Research Funds for the Central Universitieshttp://dx.doi.org/10.13039/501100012226
UNSPECIFIEDZhejiang Universityhttp://dx.doi.org/10.13039/501100004835
31950410541[NSFC] National Natural Science Foundation of Chinahttp://dx.doi.org/10.13039/501100001809
2018SHZDZX01Science and Technology Commission of Shanghai Municipalityhttp://dx.doi.org/10.13039/501100003399
U54 EB020403National Institutes of Healthhttp://dx.doi.org/10.13039/100000002
B18015Higher Education Discipline Innovation Projecthttp://dx.doi.org/10.13039/501100013314
16JC1420402Shanghai Science and Technology Development Foundationhttp://dx.doi.org/10.13039/100012543
2018YFC1312900National Science and Technology Infrastructure Programhttp://dx.doi.org/10.13039/501100012167
NSFC 91630314[NSFC] National Natural Science Foundation of Chinahttp://dx.doi.org/10.13039/501100001809
UNSPECIFIEDShanghai Rising-Star Programhttp://dx.doi.org/10.13039/501100013105
Contributors:
ContributionNameContributor ID
UNSPECIFIEDRushworth, Matthew F. S.UNSPECIFIED

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