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. Autism Res 2020, 13: 715-728. © 2020 International Society for Autism Research, Wiley Periodicals, Inc. LAY SUMMARY: We used brain imaging to evaluate differences in brain activation in adolescents with autism while they performed tasks that involved learning about social and nonsocial information. We found no differences in brain responses during the nonsocial condition, but differences during the social condition of the learning task. This study provides evidence that autism may involve different patterns of brain activation when learning about social information.

Keywords: autism spectrum disorder; fMRI; reward prediction error; social; social-communication.

© 2020 International Society for Autism Research, Wiley Periodicals, Inc.

Figures

Figure 1.

Prediction Error Task. The task consisted of a cue phase, which lasted 2 seconds (first two columns above), and an outcome phase, which lasted 1 second (last column above). During the cue phase, participants were shown one of two cues (Pattern A in row 1 or Pattern B in row 2). Participants selected one of two options: (1) a “check mark” to predict that a reward would appear next (i.e., an unscrambled image); or (2) an “X” to predict that a non-reward would appear next (i.e., a scrambled image). There were two versions of the task: (1) a social version, where the reward was an unscrambled image of a smiling face; and (2) a nonsocial version, where the reward was an unscrambled image of a nonsocial object previously identified as highly pleasing to individuals with ASD (see text for details).

Figure 2.

Regions of Activation for the Social Task. Clusters that revealed group differences in voxel-wise analyses during the social version of the task are shown for the following contrasts: (1) SPE contrast: (a) ASD TD, RH Frontal Pole; (2) tUPE contrast: (a) ASD > TD, RH Anterior Cingulate Gyrus, (b) ASD > TD, RH Precentral Gyrus, (c) ASD > TD, Left Hemisphere (LH) Precentral Gyrus; and (3) Main Effect of Reward: (a) ASD > TD, RH Precentral Gyrus. TD = typical development; ASD = autism spectrum disorder.

Figure 3.

Correlation between reaction times for the social condition in the ASD group and the ASD>TD cluster in the left precentral gyrus during the social thresholded unsigned prediction error (tUPE) contrast in the ASD group.

Figure 4.

Correlations between the Pragmatic Rating Scale—School Age (PRS-SA) and brain activation in the right hemisphere (RH) precentral gyrus during the Social Task in the ASD group. Left panel: PRS-SA Degree of Pragmatic Impairment and brain activation during the signed prediction error (SPE) contrast; Right panel: PRS-SA Paralinguistic subdomain score and brain activation during the thresholded unsigned prediction error (tUPE) contrast.