Structural connectome architecture shapes the maturation of cortical morphology from childhood to adolescence

Prior research indicates substantial refinements of regional cortical morphology in the transition period from childhood to adolescence. However, whether and how the spatial pattern of cortical maturation is shaped by underlying white matter connectome architecture remains largely unknown. Here, we address this issue by leveraging 521 longitudinal structural and diffusion magnetic resonance imaging scans from 314 typically developing individuals during childhood and adolescence (aged 6-14 years). We demonstrate widespread cortical thinning from childhood to adolescence predominantly distributed in bilateral frontoparietal heteromodal nodes, and this maturation pattern is structurally constrained by the white matter connectome architecture of the brain. Specifically, this constraint is first observed as a direct association of the cortical maturation extents between nodes and their anatomically connected neighbors. Using a network-level diffusion computational model, we further demonstrate that the spatial maturation of cortical thickness can be significantly predicted by using multiscale diffusion profiles of network links. Furthermore, these connectome-based constraints are primarily dominated by several core nodes located in bilateral frontoparietal regions, which exhibit differential gene expression profiles in microstructural neurodevelopment processes compared to non-dominant brain nodes. These findings are highly reproducible when using another independent neuroimaging dataset from the Lifespan Human Connectome Project in Development (aged 5-14 years). Our results highlight the importance of white matter network structure in shaping the coordinated maturation of regional cortical morphology and demonstrate the feasibility of using a network-based diffusion model to reveal the maturational principle of cortical morphology from childhood to adolescence. Significance Statement Cortical thinning is an important hallmark of the maturation of brain morphology during childhood and adolescence. However, the connectome-based wiring mechanism that underlies cortical maturation remains unclear. Using neuroimaging, connectome, transcriptome, and computational modeling, we mapped cortical thinning patterns primarily located in lateral frontal and parietal heteromodal nodes during childhood and adolescence, which is structurally constrained by white matter network architecture and is particularly represented using a network-based diffusion model. Furthermore, connectome-based constraints are regionally heterogeneous, with the largest constraints residing in frontoparietal nodes, and are associated with gene expression signatures of microstructural neurodevelopmental events. These findings advance our understanding of network-level mechanisms and the associated genetic basis that underlie the maturational process of cortical morphology during childhood and adolescence.