Neural Theory-of-Mind Mechanisms and Their Relations to Children’s Social Functioning

Background: Theory of mind (ToM), the ability to reason about others’ mental states, is a core facet of social cognition implicated in autism spectrum disorder (ASD). Neuroimaging evidence indicates that adolescents and adults with ASD show atypical activation in the neural ToM network during mental state reasoning. In addition, a recent study suggests that activation in the right temporoparietal junction (rTPJ), a key node of the ToM network, is linked to ASD symptom severity. Although influential developmental theories posit that ToM is central to social understanding and functioning, the relations between neural ToM mechanisms and the broad spectrum of empathy and social ability observed across typical (TD) and atypical child development remain unclear.

Objectives: This study aimed to (a) identify neural activation specifically elicited by ToM reasoning and to (b) elucidate relations between these neural ToM mechanisms and individual variation in children’s socioemotional functioning. We predicted that TD children would demonstrate enhanced activation at key nodes of the ToM network (i.e., bilateral TPJ and precuneus) during mental state reasoning. Moreover, we hypothesized that the strength of this activation would be associated with individual variation in children’s empathy and social functioning.

Methods: Participants were 32 TD children between 9 and 13 years old. Functional neuroimaging (fMRI) data were collected on a 3T scanner while participants completed a false belief task developed for children. In the experimental (ToM) condition, children listened to vignettes describing social scenarios and then evaluated characters’ beliefs. In the control condition, they listened to non-social scenarios and then made inferences about physical causality. Children also completed a behavioral measure of empathy (Interpersonal Reactivity Index), and parents completed measures assessing multiple facets of their children’s social abilities (Social Responsiveness Scale, 2^ndedition) and competence (Child Behavior Checklist).

Results:  Whole-brain analyses indicated enhanced activation to ToM reasoning versus the control task at key nodes of the ToM network, including the bilateral temporoparietal junction (rTPJ and lTPJ) and precuneus (p<.05, FWE-corrected). Controlling for age, greater activity in the bilateral TPJ correlated with reduced empathic concern for others (rTPJ: ρ=-0.46, p=0.01; lTPJ: ρ=-0.46, p=0.01) and poorer social competence (rTPJ: ρ=-0.56, p=0.03; lTPJ: ρ=-0.52; p=0.04). In addition, greater activity in the precuneus (ρ=0.48, p=0.02) and lTPJ (ρ=0.41, p=0.06) correlated with diminished social awareness.

Conclusions: During mental state reasoning, children engaged a distributed ToM network previously identified in adults. Moreover, greater activation in the TPJ and precuneus was associated with poorer socioemotional functioning, suggesting that reduced efficiency of ToM regions is linked to difficulties in empathy and social functioning among school-age children. These findings have important translational implications for understanding social deficits in children with ASD: dysregulation of ToM network activation may be a core neural mechanism underlying impaired social understanding and interaction. Our results also indicate that neural ToM mechanisms index individual variation in socioemotional behavior, demonstrating value as a biological metric of functional heterogeneity in social development. Ongoing connectivity analyses explore relations between functional integration of the ToM network during mental state reasoning and variation in children’s social cognition and functioning.