Brain structural and functional connectivity converge prenatally but diverge after birth

Abstract

Brain anatomical architecture supports its functional activity and complex cognitive processes. However, how the structure–function (SF) relationship establishes and develops during early life, as well as its underlying mechanisms, remain largely unclear. To address these questions, we leveraged multimodal MRI data from two large-scale public databases, the developing Human Connectome Project (dHCP) and the Baby Connectome Project (BCP), to characterize the spatiotemporal dynamics of SF coupling from the perinatal period to toddlerhood. Our results revealed that SF coupling at birth exhibited a spatial variation along the sensorimotor-association cortical axis. During the perinatal period (26–44 postmenstrual weeks), SF coupling strengthened drastically and followed three distinct developmental trajectories across the cortex, with sensorimotor and visual areas showing the fastest growth and the earliest plateau. After birth, SF coupling shifted toward a weakening pattern across the cortex during infancy and toddlerhood (1–28 months). These developmental changes of SF coupling were more strongly associated with the maturation of functional connectivity, which first converged toward the local structural architecture prenatally and then diverged postnatally through the expansion of global inter-modular pathways. Furthermore, SF coupling at birth, the developmental transition point, exhibited a significant association with individual differences in cognition and language outcomes at 18 months of age. Collectively, these findings offer valuable insights into the organizational principles underlying structural and functional network development during early life as well as the complex evolving relationship between them.