Neural Mechanisms of Social and Nonsocial Reward Prediction Errors in Adolescents with Autism Spectrum Disorder

Abstract

Autism spectrum disorder (ASD) is characterized by impaired predictive abilities; however, the neural mechanisms subsuming reward prediction errors in ASD are poorly understood. In the current study, we investigated neural responses during social and nonsocial reward prediction errors in 22 adolescents with ASD (ages 12-17) and 20 typically developing control adolescents (ages 12-18). Participants performed a reward prediction error task using both social (i.e., faces) and nonsocial (i.e., objects) rewards during a functional magnetic resonance imaging scan. Reward prediction errors were defined in two ways: (a) the signed prediction error, the difference between the experienced and expected reward; and (b) the thresholded unsigned prediction error, the difference between expected and unexpected outcomes regardless of magnitude. During social reward prediction errors, the ASD group demonstrated the following differences relative to the TD group: (a) signed prediction error: decreased activation in the right precentral gyrus and increased activation in the right frontal pole; and (b) thresholded unsigned prediction error: increased activation in the right anterior cingulate gyrus and bilateral precentral gyrus. Groups did not differ in brain activation during nonsocial reward prediction errors. Within the ASD group, exploratory analyses revealed that reaction times and social-communication impairments were related to precentral gyrus activation during social prediction errors. These findings elucidate the neural mechanisms of social reward prediction errors in ASD and suggest that ASD is characterized by greater neural atypicalities during social, relative to nonsocial, reward prediction errors in ASD.

A Simultaneous [11C]Raclopride Positron Emission Tomography and Functional Magnetic Resonance Imaging Investigation of Striatal Dopamine Binding in Autism

“…Though the present study did not investigate reward learning, this pattern of impaired dorsal striatal DA release in the ASD group is consistent with the well-documented deficits in learning [61, 62] and flexible responses to environmental contingencies [63] in ASD that may result from atypical computation of prediction errors [64, 65]. The neuroimaging literature addressing reward learning in ASD has found decreased frontostriatal activity during both implicit and explicit social reward learning tasks [15, 66, 67], underscoring the potential relevance of impaired reward learning to core ASD symptoms.…”

Prediction in Autism Spectrum Disorder: A Systematic Review of Empirical Evidence

“…Four studies gave participants explicit information about probabilistic or deterministic stimulus contingencies (e.g., “X will follow Y 80% of the time”) upon which to base their predictions. These studies found differences between the groups in fMRI activity related to social (but not nonsocial) reward prediction error [Kinard et al, 2020], fewer spontaneous anticipatory saccades toward the predictable target [Greene et al, 2019], a range of differences in predictability‐related RT and EEG differences [Thillay et al, 2016], and differences in accuracy and fMRI correlates of predictions made from the perspective of another [Balsters et al, 2017].…”

“…One study used non‐social learned outcome expectancies [Mosner et al, 2019], and two used social conditions [Balsters et al, 2017; Kinard et al, 2020]. The social conditions within these studies were quite different; they included stimuli that were social (smiling face) and non‐social (preferred objects) [Kinard et al, 2020] and a theory of mind task with first and third person perspective taking [Balsters et al, 2017]. All three studies showed differences in the frontostriatal prediction error signal between the ASD group and the NT group.…”

“…All three studies showed differences in the frontostriatal prediction error signal between the ASD group and the NT group. One study found the neural differences during social, but not non‐social, reward conditions for adolescents with ASD [Kinard et al, 2020].…”

A simultaneous [11C]raclopride positron emission tomography and functional magnetic resonance imaging investigation of striatal dopamine binding in autism

“…contingencies 59 in ASD that may result from atypical computation of prediction errors 60,61 . The neuroimaging literature addressing reward learning in ASD has found decreased frontostriatal activity during both implicit and explicit social reward learning tasks 8,62,63 , underscoring the potential relevance of impaired reward learning to core ASD symptoms. fMRI functional connectivity with PET-derived striatal seed regions was evaluated with a GFC approach.…”