Developmental organization of neural dynamics supporting social processing: Evidence from naturalistic fMRI in children and adults

The development of social cognition underpins significant implications for diagnosing and treating neurodevelopmental disorders such as autism spectrum disorder. This study investigates the dynamic neural organization of social cognition in children ( n = 60, ages 3-10) and adults ( n = 55) using a naturalistic fMRI paradigm that tracks continuous brain activity during real-world social interactions. We identify four distinct co-activation patterns (CAP) that reflect a functional hierarchy, ranging from basic sensory processing to complex social-cognitive integration. These brain state dynamics reveal significant developmental differences: children exhibit immature transitions, often bypassing intermediate states (e.g., salience-driven filtering, State 3) and prematurely shifting from early sensory encoding (State 1) to internally-directed integration (State 2). Moreover, during mentalizing and pain events, children show reduced modulation of sensory and perceptual brain states, indicating limited cognitive flexibility that is essential for social interaction. Structural equation modeling reveals a developmental cascade linking the maturation of sensory (State 1), perceptual filtering (State 3), and social-cognitive (State 2) processing states. This pathway is mediated by individual differences in Theory of Mind (ToM) development and further predicts empathic abilities. These findings advance our understanding of how brain state reorganization supports social cognitive maturation and offer new insights into neurodevelopmental disorders. ● Identified hierarchical brain states during naturalistic social processing, highlighting neurodevelopmental differences between children and adults. ● Children exhibit immature neural transitions, bypassing critical processing states in social cognition. ● Event-driven CAP modulation during ToM and pain events reveals age-related differences, with children showing reduced modulation of perceptual and sensory states. ● A developmental cascade links the maturation of sensory, perceptual, and social-cognitive states throughout children's development.