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

Abstract

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.

Keywords: Autism; Social interaction; Social reward; Ventral striatum; fMRI.

Fig. 1

Social-interactive reward task design. During the initiation period, participants sent messages about their interests (e.g., “I like cookies”) to a perceived peer or a computer partner. During the reply period, participants received engaged (e.g., “Me too!”/“Matched!”) or disengaged (e.g., “I’m away”/“Disconnected”) responses.

Fig. 2

Youth in the AUT group (n = 43) and youth in the TD group (n = 43) both liked chatting with (A) and wanted to see responses from (B) the peer more than the computer. Youth in the AUT group did not differ from youth in the TD group in overall enjoyment of chatting with the scanner peer as measured across a composite of seven questions assessing peer enjoyment (C).

Fig. 3

Results of whole-brain analysis for the reply period for the AUT group (n = 43).

Fig. 4

Results of whole-brain analysis for the reply period for the TD group (n = 43).

Fig. 5

Results of ROI analyses for the nucleus accumbens and ventral caudate (n = 43 AUT, n = 43 TD). Error bars are ± standard error.

Fig. 6

Enjoyment of the peer in the scanner task significantly predicts variation in nucleus accumbens (NAcc) sensitivity to social interaction (n = 114).

Fig. 7

Nucleus accumbens (NAcc) sensitivity to social interaction significantly predicts desire to interact with the same partner again (A; n = 58), but does not significantly predict self-reported interaction quality (B; n = 71) during a twenty-five minute face-to-face interaction with a novel peer. Relations were marginally stronger in the TD group (grey) compared to the AUT group (orange) for desire to interact with the same partner again.