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NeuroscienceNature Communications
Peer-reviewed journal article

Developmental Variations in Recurrent Spatiotemporal Brain Propagations from Childhood to Adulthood

Kyoungseob ByeoniD, Hyunjin ParkiD, Shinwon ParkiD, Jon Cluce, Kahini P. MehtaiD, Matthew CieslakiD, Zaixu CuiiD, Seok‐Jun HongiD, Catie E. ChangiD, Jonathan SmallwoodiD, Theodore Daniel SatterthwaiteiD, Michael Peter MilhamiD, Ting XuiD

Abstract

The brain undergoes profound structural and functional transformations from childhood to adolescence. Convergent evidence suggests that neurodevelopment proceeds in a hierarchical manner, characterized by heterogeneous maturation patterns across brain regions and networks. However, the maturation of the intrinsic spatiotemporal propagations of brain activity remains largely unexplored. This study aims to bridge this gap by delineating spatiotemporal propagations from childhood to early adulthood. By leveraging a recently developed approach that captures time-lag dynamic propagations, we characterized intrinsic dynamic propagations along three axes: sensory-association (S-A), task-positive to default networks (TP-D), and somatomotor-visual (SM-V) networks, which progress towards adult-like brain dynamics from childhood to early adulthood. Importantly, we demonstrated that as participants mature, there is a prolonged occurrence of the S-A and TP-D propagation states, indicating that they spend more time in these states. Conversely, the prevalence of SM-V propagation states declines during development. Notably, top-down propagations along the S-A axis exhibited an age-dependent increase in occurrence, serving as a superior predictor of cognitive scores compared to bottom-up S-A propagation. These findings were replicated across two independent cohorts (N = 677 in total), emphasizing the robustness and generalizability of these findings. Our results provide new insights into the emergence of adult-like functional dynamics during youth and their role in supporting cognition.

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