Neural Hyperresponsivity During the Anticipation of Tangible Social and Nonsocial Rewards in Autism Spectrum Disorder: A Concurrent Neuroimaging and Facial Electromyography Study

Abstract

Background: Atypical anticipation of social reward has been shown to lie at the core of the social challenges faced by individuals with autism spectrum disorder (ASD). However, previous research has yielded inconsistent results and has often overlooked crucial characteristics of stimuli. Here, we investigated ASD reward processing using social and nonsocial tangible stimuli, carefully matched on several key dimensions.

Methods: We examined the anticipation and consumption of social (interpersonal touch) and nonsocial (flavored milk) rewards in 25 high-functioning individuals with ASD and 25 neurotypical adult individuals. In addition to subjective ratings of wanting and liking, we measured physical energetic expenditure to obtain the rewards, brain activity with neuroimaging, and facial reactions through electromyography on a trial-by-trial basis.

Results: Participants with ASD did not exhibit reduced motivation for social or nonsocial rewards; their subjective ratings, motivated efforts, and facial reactions were comparable to those of neurotypical participants. However, anticipation of higher-value rewards increased neural activation in lateral parietal cortices, sensorimotor regions, and the orbitofrontal cortex. Moreover, participants with ASD exhibited hyperconnectivity between frontal medial regions and occipital regions and the thalamus.

Conclusions: Individuals with ASD who experienced rewards with tangible characteristics, whether social or nonsocial, displayed typical subjective and objective motivational and hedonic responses. Notably, the observed hyperactivations in sensory and attentional nodes during anticipation suggest atypical sensory overprocessing of forthcoming rewards rather than decreased reward value. While these atypicalities may not have manifested in observable behavior here, they could impact real-life social interactions that require nuanced predictions, potentially leading to the misperception of reduced interest in rewarding social stimuli in ASD.

Keywords: Food; Liking; Reward processing; Social motivation theory; Touch; Wanting.