Fiber length distribution characterizes the brain network maturation during early school-age
Environmental and social changes during early school age have a profound impact on brain development. However, it remains unclear how the brains of typically-developing children adjust white matter to optimize network topology during this period. This study proposes fiber length distribution as a no...
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| Language: | English |
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Elsevier
2025-03-01
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| Series: | NeuroImage |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811925000680 |
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| author | Yanlin Yu Qing Cai Longnian Lin Chu-Chung Huang |
| author_facet | Yanlin Yu Qing Cai Longnian Lin Chu-Chung Huang |
| author_sort | Yanlin Yu |
| collection | DOAJ |
| description | Environmental and social changes during early school age have a profound impact on brain development. However, it remains unclear how the brains of typically-developing children adjust white matter to optimize network topology during this period. This study proposes fiber length distribution as a novel nodal metric to capture the continuous maturation of brain network. We acquired dMRI data from N = 30 typically developing children in their first year of primary school and a one-year follow-up. We assessed the longitudinal changes in fiber length distribution, characterized by the median length of connected fibers for each brain region. The length median was positively correlated with degree and betweenness centrality, while negatively correlated with clustering coefficient and local efficiency. From ages 7 to 8, we observed significant decreases in length median in the temporal, superior parietal, anterior cingulate, and medial prefrontal cortices, accompanied by a reduction in long-range connections and an increase in short-range connections. Meta-analytic decoding revealed that the widespread decrease in length median occurred in regions responsible for sensory processing, whereas a more localized increase in length median was observed in regions involved in memory and cognitive control. Finally, simulation tests on healthy adults further supported that the decrease in long-range connections and increase in short-range connections contributed to enhanced network segregation and integration, respectively. Our results suggest that the dual process of short- and long-range fiber changes reflects a cost-efficient strategy for optimizing network organization during this critical developmental stage. |
| format | Article |
| id | doaj-art-6f877e096f4b4f1c90727caf566faad0 |
| institution | Kabale University |
| issn | 1095-9572 |
| language | English |
| publishDate | 2025-03-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj-art-6f877e096f4b4f1c90727caf566faad02025-02-04T04:10:19ZengElsevierNeuroImage1095-95722025-03-01308121066Fiber length distribution characterizes the brain network maturation during early school-ageYanlin Yu0Qing Cai1Longnian Lin2Chu-Chung Huang3Shanghai Key Laboratory of Brain Functional Genomics (Ministry of Education), Institute of Brain and Education Innovation, School of Psychology and Cognitive Science, East China Normal University, Shanghai, ChinaShanghai Key Laboratory of Brain Functional Genomics (Ministry of Education), Institute of Brain and Education Innovation, School of Psychology and Cognitive Science, East China Normal University, Shanghai, China; Shanghai Center for Brain Science and Brain-Inspired Technology, Shanghai, China; NYU-ECNU Institute of Brain and Cognitive Science, New York University Shanghai, Shanghai, China; Corresponding authors at: Shanghai Key Laboratory of Brain Functional Genomics (Ministry of Education), Institute of Brain and Education Innovation, School of Psychology and Cognitive Science, East China Normal University, Shanghai, China.Shanghai Key Laboratory of Brain Functional Genomics (Ministry of Education), Institute of Brain and Education Innovation, School of Psychology and Cognitive Science, East China Normal University, Shanghai, China; Shanghai Center for Brain Science and Brain-Inspired Technology, Shanghai, China; NYU-ECNU Institute of Brain and Cognitive Science, New York University Shanghai, Shanghai, China; School of Life Science Department, East China Normal University, Shanghai 200062, China; Corresponding authors at: School of Life Science Department, East China Normal University, 3663 N. Zhongshan Road, Shanghai 200062, China.Shanghai Key Laboratory of Brain Functional Genomics (Ministry of Education), Institute of Brain and Education Innovation, School of Psychology and Cognitive Science, East China Normal University, Shanghai, China; Shanghai Center for Brain Science and Brain-Inspired Technology, Shanghai, China; NYU-ECNU Institute of Brain and Cognitive Science, New York University Shanghai, Shanghai, China; Corresponding authors at: Shanghai Key Laboratory of Brain Functional Genomics (Ministry of Education), Institute of Brain and Education Innovation, School of Psychology and Cognitive Science, East China Normal University, Shanghai, ChinaEnvironmental and social changes during early school age have a profound impact on brain development. However, it remains unclear how the brains of typically-developing children adjust white matter to optimize network topology during this period. This study proposes fiber length distribution as a novel nodal metric to capture the continuous maturation of brain network. We acquired dMRI data from N = 30 typically developing children in their first year of primary school and a one-year follow-up. We assessed the longitudinal changes in fiber length distribution, characterized by the median length of connected fibers for each brain region. The length median was positively correlated with degree and betweenness centrality, while negatively correlated with clustering coefficient and local efficiency. From ages 7 to 8, we observed significant decreases in length median in the temporal, superior parietal, anterior cingulate, and medial prefrontal cortices, accompanied by a reduction in long-range connections and an increase in short-range connections. Meta-analytic decoding revealed that the widespread decrease in length median occurred in regions responsible for sensory processing, whereas a more localized increase in length median was observed in regions involved in memory and cognitive control. Finally, simulation tests on healthy adults further supported that the decrease in long-range connections and increase in short-range connections contributed to enhanced network segregation and integration, respectively. Our results suggest that the dual process of short- and long-range fiber changes reflects a cost-efficient strategy for optimizing network organization during this critical developmental stage.http://www.sciencedirect.com/science/article/pii/S1053811925000680Early-school ageLongitudinal studyFiber length distributionNetwork topologyWhite matter development |
| spellingShingle | Yanlin Yu Qing Cai Longnian Lin Chu-Chung Huang Fiber length distribution characterizes the brain network maturation during early school-age NeuroImage Early-school age Longitudinal study Fiber length distribution Network topology White matter development |
| title | Fiber length distribution characterizes the brain network maturation during early school-age |
| title_full | Fiber length distribution characterizes the brain network maturation during early school-age |
| title_fullStr | Fiber length distribution characterizes the brain network maturation during early school-age |
| title_full_unstemmed | Fiber length distribution characterizes the brain network maturation during early school-age |
| title_short | Fiber length distribution characterizes the brain network maturation during early school-age |
| title_sort | fiber length distribution characterizes the brain network maturation during early school age |
| topic | Early-school age Longitudinal study Fiber length distribution Network topology White matter development |
| url | http://www.sciencedirect.com/science/article/pii/S1053811925000680 |
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