Altered reward system reactivity for personalized circumscribed interests in autism

Abstract

Background: Neurobiological research in autism spectrum disorders (ASD) has paid little attention on brain mechanisms that cause and maintain restricted and repetitive behaviors and interests (RRBIs). Evidence indicates an imbalance in the brain's reward system responsiveness to social and non-social stimuli may contribute to both social deficits and RRBIs. Thus, this study's central aim was to compare brain responsiveness to individual RRBI (i.e., circumscribed interests), with social rewards (i.e., social approval), in youth with ASD relative to typically developing controls (TDCs).

Methods: We conducted a 3T functional magnetic resonance imaging (fMRI) study to investigate the blood-oxygenation-level-dependent effect of personalized circumscribed interest rewards versus social rewards in 39 youth with ASD relative to 22 TDC. To probe the reward system, we employed short video clips as reinforcement in an instrumental incentive delay task. This optimization increased the task's ecological validity compared to still pictures that are often used in this line of research.

Results: Compared to TDCs, youth with ASD had stronger reward system responses for CIs mostly within the non-social realm (e.g., video games) than social rewards (e.g., approval). Additionally, this imbalance within the caudate nucleus' responsiveness was related to greater social impairment.

Conclusions: The current data support the idea of reward system dysfunction that may contribute to enhanced motivation for RRBIs in ASD, accompanied by diminished motivation for social engagement. If a dysregulated reward system indeed supports the emergence and maintenance of social and non-social symptoms of ASD, then strategically targeting the reward system in future treatment endeavors may allow for more efficacious treatment practices that help improve outcomes for individuals with ASD and their families.

Keywords: Autism spectrum disorders; Caudate nucleus; Circumscribed interests; Functional magnetic resonance imaging; Motivation; Restricted and repetitive behaviors and interests; Reward; Reward system; Striatum.

Fig. 1

Illustration of the incentive delay task in a blocked fMRI design, including three different reward conditions: social reward (SR), interest reward (IR), and neutral (NR). To increase the ecological validity of the paradigm, static photos were replaced with short video clips (see text for more details)

Fig. 2

Z-statistic activation maps depict reward system activation across the entire sample separately for the two high-level contrasts social reward > neutral outcome (hot colors) and interest reward > neutral outcome (cool colors). Both social reward and interest reward (versus neutral outcome) strongly activated a widespread reward system, comprising ventral and dorsal striatum, thalamus, amygdala, medial prefrontal areas (ACC, vmPFC) as well as clusters with orbitofrontal cortex (OFC) and anterior insula. Maps were thresholded using clusters determined by a voxel-level of p ≤ 0.001 and an FWE-corrected cluster-significance threshold of p ≤ 0.05. Color bars indicate Z-scores

Fig. 3

ROI analyses revealed a significant group-by-reward type interaction effect in the caudate nucleus with greater dorsal striatum activation for interest reward (IR) than social reward (SR) in youth with ASD, while TDCs did not show significant differences—although a reverse direction—in their response pattern to both reward types. Bar graphs depict mean β values from the bilateral caudate cluster identified by the significant interaction effect. The ROI was anatomically defined based on the Harvard-Oxford structural probabilistic atlas. Results are FEW corrected at p ≤ 0.05 across this particular region. Color bar indicates t-statistics

Fig. 4

The magnitude of caudate activation that distinguished the two groups correlated positively with ASD symptom severity as assessed by the SRS-2 social communication and interaction sub-score (for the ASD group only). The stronger the caudate activation for personalized interest reward vs. social reward the greater the social impairment in the ASD group