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...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2022-03-01
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| Series: | PLoS Biology |
| Online Access: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8929635/?tool=EBI |
| _version_ | 1818281339924774912 |
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| author | Xinran Wu Xiangzhen Kong Deniz Vatansever Zhaowen Liu Kai Zhang Barbara J. Sahakian Trevor W. Robbins Jianfeng Feng Paul Thompson Jie Zhang |
| author_facet | Xinran Wu Xiangzhen Kong Deniz Vatansever Zhaowen Liu Kai Zhang Barbara J. Sahakian Trevor W. Robbins Jianfeng Feng Paul Thompson Jie Zhang |
| author_sort | Xinran Wu |
| collection | DOAJ |
| 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. Hemispheric lateralization constitutes a core architectural principle of human brain organization, often argued to represent a stable, trait-like feature, but how does this fit with our increasing appreciation of the inherently dynamic nature of brain networks? This neuroimaging study reveals the dynamic nature of functional brain lateralization at resting-state and its relationship with language function and cognitive flexibility. |
| first_indexed | 2024-12-13T00:03:33Z |
| format | Article |
| id | doaj.art-96dabbe60bd34f92885a6e1b9c681b0e |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-12-13T00:03:33Z |
| publishDate | 2022-03-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-96dabbe60bd34f92885a6e1b9c681b0e2022-12-22T00:06:20ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852022-03-01203Dynamic changes in brain lateralization correlate with human cognitive performanceXinran WuXiangzhen KongDeniz VatanseverZhaowen LiuKai ZhangBarbara J. SahakianTrevor W. RobbinsJianfeng FengPaul ThompsonJie ZhangHemispheric 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. Hemispheric lateralization constitutes a core architectural principle of human brain organization, often argued to represent a stable, trait-like feature, but how does this fit with our increasing appreciation of the inherently dynamic nature of brain networks? This neuroimaging study reveals the dynamic nature of functional brain lateralization at resting-state and its relationship with language function and cognitive flexibility.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8929635/?tool=EBI |
| spellingShingle | Xinran Wu Xiangzhen Kong Deniz Vatansever Zhaowen Liu Kai Zhang Barbara J. Sahakian Trevor W. Robbins Jianfeng Feng Paul Thompson Jie Zhang Dynamic changes in brain lateralization correlate with human cognitive performance PLoS Biology |
| 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 |
| url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8929635/?tool=EBI |
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