Watching Together, Yet Feeling Apart: Interpersonal Neural Synchronization as a Marker of Symptom Severity in Children With Autism Spectrum Disorder During Naturalistic Viewing

Social interaction impairments in autism spectrum disorder (ASD) have been widely attributed to deficits in empathy, including both cognitive and affective components. However, the underlying neural mechanisms remain incompletely understood. In the current study, we used functional near-infrared spectroscopy (fNIRS) hyperscanning to simultaneously measure brain activities in children with ASD or typical development (TD) and their mothers while they co-viewed the animated film Partly Cloudy. Results revealed that compared to TD children, children with ASD exhibited significantly reduced interpersonal neural synchronization (INS), that is, desynchronization, in the frontopolar area and right dorsolateral prefrontal cortex (DLPFC) during scenes involving theory of mind (ToM) and pain-related events. Notably, TD children showed enhanced INS in the right DLPFC, with significant group differences. Moreover, the right DLPFC INS negatively correlated with ASD symptom severity and mediated the relationship between group and symptom severity. Inter-brain functional connectivity analysis revealed that, during empathy-related events, children's frontopolar area/right DLPFC and maternal brain regions were reduced in ASD but enhanced in TD dyads, with significant group-level contrasts. Finally, using support vector machine (SVM) classification, we found that INS features in the right DLPFC during empathy scenes could accurately distinguish between ASD and TD children. This study offers novel insights into the neural basis of empathy deficits in ASD by examining mother-child INS in a naturalistic setting. These findings provide preliminary insights into the neural mechanisms of INS in ASD and may inform future research on parent-child neural synchrony and its potential relevance for intervention strategies.