Fiber length distribution characterizes the brain network maturation during early school-age

Abstract

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.