Social cognition develops in the context of reciprocal social interaction. However, most neuroimaging studies of mentalizing have used noninteractive tasks that may fail to capture important aspects of real-world mentalizing. In adults, social-interactive context modulates activity in regions linked to social cognition and reward, but few interactive studies have been done with children. The current fMRI study examines children aged 8-12 using a novel paradigm in which children believed they were interacting online with a peer. We compared mental and non-mental state reasoning about a live partner (Peer) versus a story character (Character), testing the effects of mentalizing and social interaction in a 2 × 2 design. Mental versus Non-Mental reasoning engaged regions identified in prior mentalizing studies, including the temporoparietal junction, superior temporal sulcus, and dorsomedial prefrontal cortex. Moreover, peer interaction, even in conditions without explicit mentalizing demands, activated many of the same mentalizing regions. Peer interaction also activated areas outside the traditional mentalizing network, including the reward system. Our results demonstrate that social interaction engages multiple neural systems during middle childhood and contribute further evidence that social-interactive paradigms are needed to fully capture how the brain supports social processing in the real world.

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Successful social interactions are assumed to depend on theory of mind—the ability to represent others’ mental states—yet most studies of the relation between theory of mind and social-interactive success rely on non-interactive tasks that do not adequately capture the spontaneous engagement of theory of mind, a crucial component of everyday social interactions. We addressed this gap by establishing a novel observational rating scale to measure the spontaneous use of theory of mind (or lack thereof) within naturalistic conversations ( conversational ToM; cToM). In 50 age- and gender-matched dyads of autistic and typically developing youth aged 8–16 years (three dyad types: autistic–typically developing, typically developing–typically developing, autistic–autistic), we assessed cToM during 5-min unstructured conversations. We found that ratings on the cToM Negative scale, reflecting theory-of-mind-related violations of neurotypical conversational norms, were negatively associated with two forms of non-interactive theory of mind: visual-affective and spontaneous. In contrast, the cToM Positive scale, reflecting explicit mental state language and perspective-taking, was not associated with non-interactive theory of mind. Furthermore, autistic youth were rated higher than typically developing youth on cToM Negative, but the groups were rated similarly on cToM Positive. Together, these findings provide insight into multiple aspects of theory of mind in conversation and reveal a nuanced picture of the relative strengths and difficulties among autistic youth. Lay abstract Conversation is a key part of everyday social interactions. Previous studies have suggested that conversational skills are related to theory of mind, the ability to think about other people’s mental states, such as beliefs, knowledge, and emotions. Both theory of mind and conversation are common areas of difficulty for autistic people, yet few studies have investigated how people, including autistic people, use theory of mind during conversation. We developed a new way of measuring cToM using two rating scales: cToM Positive captures behaviors that show consideration of a conversation partner’s mental states, such as referring to their thoughts or feelings, whereas cToM Negative captures behaviors that show a lack of theory of mind through violations of neurotypical conversational norms, such as providing too much, too little, or irrelevant information. We measured cToM in 50 pairs of autistic and typically developing children (ages 8–16 years) during 5-min “getting to know you” conversations. Compared to typically developing children, autistic children displayed more frequent cToM Negative behaviors but very similar rates of cToM Positive behaviors. Across both groups, cToM Negative (but not Positive) ratings were related to difficulties in recognizing emotions from facial expressions and a lower tendency to talk about others’ mental states spontaneously (i.e., without being instructed to do so), which suggests that both abilities are important for theory of mind in conversation. Altogether, this study highlights both strengths and difficulties among autistic individuals, and it suggests possible avenues for further research and for improving conversational skills.

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