Hierarchical maturation of structural brain connectomes from birth to childhood.

Abstract

The postnatal white matter connectome undergoes profound reorganization, yet the topological principles governing its spatiotemporal maturation remain largely unknown. Using connectome mapping, machine learning, and neurobiological annotation, we show hierarchical network development from birth to childhood and its association with neurobiological signatures. We identify two cardinal topological transformations that change rapidly during infancy and continue to refine into childhood, as characterized by nonlinear global increases in network efficiency and robustness to nodal attack, and regional reorganization with accelerated hub consolidation and prolonged modular reconfiguration, predominantly involving the prefrontal and insular cortices. Early developmental trajectories of these association cortices predict late childhood network architecture through local microstructural maturation of connected white matter tracts. These patterns align with well-established multiscale cortical hierarchies, including anatomical, evolutionary, and energy metabolism axes. Our findings reveal critical neurotopological milestones after postnatal development and establish a unified multiscale framework linking macroscale network dynamics to biologically constrained rules.