Social reward network connectivity differs between autistic and neurotypical youth during social interaction.

A core feature of autism is difficulties with social interaction. Atypical social motivation is proposed to underlie these difficulties. However, prior work testing this hypothesis has shown mixed support and has been limited in its ability to understand real-world social-interactive processes in autism. We attempted to address these limitations by scanning neurotypical and autistic youth (n = 86) during a text-based reciprocal social interaction that mimics a "live" chat and elicits social reward processes. We focused on task-evoked functional connectivity (FC) of regions responsible for motivational-reward and mentalizing processes within the broader social reward circuitry. We found that task-evoked FC between these regions was significantly modulated by social interaction and receipt of social-interactive reward. Compared to neurotypical peers, autistic youth showed significantly greater task-evoked connectivity of core regions in the mentalizing network (e.g., posterior superior temporal sulcus) and the amygdala, a key node in the reward network. Furthermore, across groups, the connectivity strength between these mentalizing and reward regions was negatively correlated with self-reported social motivation and social reward during the scanner task. Our results highlight an important role of FC within the broader social reward circuitry for social-interactive reward. Specifically, greater context-dependent FC (i.e., differences between social engagement and non-social engagement) may indicate an increased "neural effort" during social reward and relate to differences in social motivation within autistic and neurotypical populations.

Social-interactive reward elicits similar neural response in autism and typical development and predicts future social experiences.

Challenges in initiating and responding to social-interactive exchanges are a key diagnostic feature of autism spectrum disorder, yet investigations into the underlying neural mechanisms of social interaction have been hampered by reliance on non-interactive approaches. Using an innovative social-interactive neuroscience approach, we investigated differences between youth with autism and youth with typical development in neural response to a chat-based social-interactive reward, as well as factors such as age and self-reported social enjoyment that may account for heterogeneity in that response. We found minimal group differences in neural and behavioral response to social-interactive reward, and variation within both groups was related to self-reported social enjoyment during the task. Furthermore, neural sensitivity to social-interactive reward predicted future enjoyment of a face-to-face social interaction with a novel peer. These findings have important implications for understanding the nature of social reward and peer interactions in typical development as well as for future research informing social interactions in individuals on the autism spectrum.

Theory of mind in naturalistic conversations between autistic and typically developing children and adolescents.

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.

Neural similarity between mentalizing and live social interaction during the transition to adolescence.

Social interactions are essential for human development, yet little neuroimaging research has examined their underlying neurocognitive mechanisms using socially interactive paradigms during childhood and adolescence. Recent neuroimaging research has revealed activity in the mentalizing network when children engage with a live social partner, even when mentalizing is not required. While this finding suggests that social-interactive contexts may spontaneously engage mentalizing, it is not a direct test of how similarly the brain responds to these two contexts. The current study used representational similarity analysis on data from 8- to 14-year-olds who made mental and nonmental judgments about an abstract character and a live interaction partner during fMRI. A within-subject, 2 (Mental/Nonmental) × 2 (Peer/Character) design enabled us to examine response pattern similarity between conditions, and estimate fit to three conceptual models of how the two contexts relate: (1) social interaction and mentalizing about an abstract character are represented similarly; (2) interactive peers and abstract characters are represented differently regardless of the evaluation type; and (3) mental and nonmental states are represented dissimilarly regardless of target. We found that the temporal poles represent mentalizing and peer interactions similarly (Model 1), suggesting a neurocognitive link between the two in these regions. Much of the rest of the social brain exhibits different representations of interactive peers and abstract characters (Model 2). Our findings highlight the importance of studying social-cognitive processes using interactive approaches, and the utility of pattern-based analyses for understanding how social-cognitive processes relate to each other.

Developmental differences in brain functional connectivity during social interaction in middle childhood.

The transition from childhood to adolescence is marked by significant changes in peer interactions. However, limited research has examined the brain systems (e.g., mentalizing and reward networks) involved in direct peer interaction, particularly during childhood and early adolescence. Here, we analyzed fMRI data from 50 children aged 8-12 years while they participated in a task in which they chatted with a peer (Peer) or answered questions about a story character (Character). Using a beta-series correlation analysis, we investigated how social interaction modulates functional connectivity within and between mentalizing and reward networks and whether this modulation changes with age. We observed effects of social interaction on functional connectivity were modulated by age within the mentalizing and reward networks. Further, greater connectivity within and between these networks during social interaction was related to faster reaction time to the Peer versus Character condition. Similar effects were found in the salience and mirror neuron networks. These findings provide insights into age-related differences in how the brain supports social interaction, and thus have the potential to advance our understanding of core social difficulties in social-communicative disorders, such as autism spectrum disorder.

Effects of social and emotional context on neural activation and synchrony during movie viewing.

Sharing emotional experiences impacts how we perceive and interact with the world, but the neural mechanisms that support this sharing are not well characterized. In this study, participants (N = 52) watched videos in an MRI scanner in the presence of an unfamiliar peer. Videos varied in valence and social context (i.e., participants believed their partner was viewing the same (joint condition) or a different (solo condition) video). Reported togetherness increased during positive videos regardless of social condition, indicating that positive contexts may lessen the experience of being alone. Two analysis approaches were used to examine both sustained neural activity averaged over time and dynamic synchrony throughout the videos. Both approaches revealed clusters in the medial prefrontal cortex that were more responsive to the joint condition. We observed a time-averaged social-emotion interaction in the ventromedial prefrontal cortex, although this region did not demonstrate synchrony effects. Alternatively, social-emotion interactions in the amygdala and superior temporal sulcus showed greater neural synchrony in the joint compared to solo conditions during positive videos, but the opposite pattern for negative videos. These findings suggest that positive stimuli may be more salient when experienced together, suggesting a mechanism for forming social bonds.

Explaining Variance in Social Symptoms of Children with Autism Spectrum Disorder.

The social symptoms of autism spectrum disorder are likely influenced by multiple psychological processes, yet most previous studies have focused on a single social domain. In school-aged autistic children (n = 49), we compared the amount of variance in social symptoms uniquely explained by theory of mind (ToM), biological motion perception, empathy, social reward, and social anxiety. Parent-reported emotional contagion-the aspect of empathy in which one shares another's emotion-emerged as the most important predictor, explaining 11-14% of the variance in social symptoms, with higher levels of emotional contagion predicting lower social symptom severity. Our findings highlight the role of mutual emotional experiences in social-interactive success, as well as the limitations of standard measures of ToM and social processing in general.

Social interaction recruits mentalizing and reward systems in middle childhood.

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.