Fiber Length Distribution Characterizes the Brain Network Maturation during Early School-age.

Neuroimage

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. Electronic address:

Published: January 2025

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 aims to propose the fiber length distribution as a novel nodal metric to capture the continuous maturation of brain network. We scanned dMRI among N=30 typically-developing children in their first year of primary school and 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 cortex, 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, simulations test on healthy adults further support that the decrease in long-range and increase in short-range connection contributed to increased 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.

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http://dx.doi.org/10.1016/j.neuroimage.2025.121066DOI Listing

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