Characterization of the Temporal Stability of ToM and Pain Functional Brain Networks Carry Distinct Developmental Signatures during Naturalistic Viewing

Abstract

A temporally stable functional brain network pattern among coordinated brain regions is fundamental to stimulus selectivity and functional specificity during the critical period of brain development. Brain networks that are recruited in time to process internal states of others’ bodies (like hunger and pain) versus internal mental states (like beliefs, desires, and emotions) of others’ minds allow us to ask whether a quantitative characterization of the stability of these networks carry meaning during early development and constrain cognition in a specific way. Previous research provides critical insight into the early development of the ToM network and its segregation from the Pain network throughout normal development using functional connectivity. However, a quantitative characterization of the temporal stability of ToM networks from early childhood to adulthood remains unexplored. In this work, using a large sample of children (n=122, 3–12 years) and adults (n=33), we addressed this question based on their fMRI data during a short and engaging naturalistic movie-watching task. The movie highlights the characters’ bodily sensations (often pain) and mental states (beliefs, desires, emotions), and is a feasible experiment for young children. Our results tracked the change in temporal stability using an unsupervised characterization of ToM and Pain networks dFC patterns using Angular and Mahalanobis distance between dominant dynamic functional connectivity subspaces. Our findings reveal that both ToM and Pain networks exhibit lower temporal stability as early as 3 years and gradually stabilize by 5 years, which continues till adolescence and late adulthood (often sharing similarity with adult dFC stability patterns). Further, we find that the temporal stability of ToM brain networks is predictive of participants’ task performance in the false-belief task to access mentalization at an early age. Interestingly, higher temporal stability is predictive of the pass group, and similarly, moderate and low temporal stability are predictive of the inconsistent group and the fail group. Our findings open an avenue for applying the temporal stability of dFC subspaces of large-scale functional brain networks during cortical development to act as a biomarker for multiple developmental disorders concerning impairment and discontinuity in the neural basis of social cognition.