The Neural Bases of Social Motivation in Autism Spectrum Disorder during a Real-Time Peer Interaction

Background:  Difficulties with social communication and social interaction, including reduced interest in both approaching and sharing information with peers, are core features of autism spectrum disorder (ASD). Some hypothesize that reduced social motivation in ASD is one cause of these social communication deficits. However, functional magnetic resonance imaging (fMRI) studies investigating the neural correlates of social motivation in ASD reveal inconsistent findings. Critically, these past paradigms do not involve social interactions, which is a core area of dysfunction in ASD. Rather, participants are asked to passively and independently view images (e.g., static photos of smiling faces), which may not approximate real-world social communicative contexts. This lack of reciprocal social interaction and real-world applicability is troubling since individuals with ASD have the most difficulty in interactive social communicative contexts but may perform within normal limits on non-interactive laboratory tasks related to social cognition (Schilbach et al., 2013; Senju et al., 2009).

Objectives:  The purpose of this study was to utilize a real-world interactive fMRI paradigm to investigate neural circuitry underlying social motivation in ASD.

Methods:  Twelve children with ASD (ages 9-14, one female) and eleven gender-matched NT children (ages 8-12) were informed they would be chatting online both with a peer and a computer. The chat was simulated, but all children believed that the peer was real. Each trial had two phases: Initiation, in which participants disclosed information about themselves (e.g., “I like sushi”) and Reply, in which participants received feedback from the peer (“Me too/neither!”) or computer (“Matched!”).

Results:  During the Initiation period, neither NT nor ASD participants showed differences in activation between initiating a conversation with a peer versus a computer at the whole brain level (all whole-brain results are given at p<0.01, k = 20), potentially due to the high reward value of self-disclosure regardless of recipient. However, during the Reply period, NT participants showed greater activation in amygdala, ventral striatum (VS), orbitofrontal cortex (OFC), medial prefrontal cortex (mPFC), superior temporal sulcus (STS), and temporoparietal junction (TPJ) when they believed they were receiving a reply from a peer versus a computer, while participants with ASD showed no significant differences to peer versus computer replies. Between-group (NT versus ASD) whole-brain and region of interest (VS and amygdala) analyses revealed no significant differences between groups in neural activation to peer versus computer in either the Initiation or Reply phases; however, this may have been due to the current small sample size. These findings are preliminary, and data collection is ongoing.

Conclusions:  In summary, preliminary results suggest that neurotypical children, but not children with ASD, show greater activation in classic reward and social cognitive brain regions when interacting with a same-aged peer (versus a computer control). The investigation of neural and behavioral correlates of social motivation within real-time social interactive contexts will help us better understand the core social deficits in ASD as well as typically developing children’s drive to orient to and interact with the social world.