Altered reward system reactivity for personalized circumscribed interests in autism

Abstract

BackgroundNeurobiological 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).MethodsWe 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.ResultsCompared 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.ConclusionsThe 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.Electronic supplementary materialThe online version of this article (10.1186/s13229-018-0195-7) contains supplementary material, which is available to authorized users.

Evaluation of the Social Motivation Hypothesis of Autism

“…As predicted by the social motivation hypothesis, a metaanalysis of 7 studies with social stimuli revealed significant large clusters of reward circuitry hypoactivation in the ASD group in bilateral caudate (−12, Supplement), and, after controlling for sample age, bilateral anterior cingulate (eTable 4 in the Supplement). The nucleus accumbens showed both hypoactivation in the left hemisphere and hyperactivation in the right hemisphere, consistent with findings from both Cascio et al 33 and Kohls et al 28 ; the third study in this meta-analysis reported no significant results in this region. 36 Other areas with significant hypoactivation included the left hippocampus, central opercular cortex, and parietal operculum cortex (eTable 4 and eFigure 3 in the Supplement).…”

“…Hyperactivation was observed in the right temporal occipital fusiform cortex and the left superior temporal gyrus/planum temporale (eTable 2 in the Supplement). Jackknife sensitivity analysis showed robustness of all striatal findings and most other regions; several smaller clusters were no longer significant after removing 1 of 2 studies16,28 (eTable 2 in the Supplement). The Egger test (bias = −2.11, t 5 = −0.23; P = .41) and funnel plots (eFigures 3-6 in the Supplement) gave no evidence of publication bias.Decreased Activation to Nonsocial RewardsA meta-analysis of 10 studies with nonsocial stimuli revealed reward circuitry hypoactivation in the ASD group in bilateral caudate (−8, 2, 26; d = −0.22; 95% CI, −0.42 to −0.02; P < .0001), bilateral nucleus accumbens (−2, 16, −4; d = −0.21; 95% CI, −0.40 to −0.02; P < .0001), anterior cingulate cortex (−8, 2, 26; d = −0.22; 95% CI, −0.42 to −0.02; P < .0001), and right insula (38, −4, 16; d = −0.19; 95% CI, −0.33 to −0.04; P < .001) (Figure 1, Figure 2B, eFigure 5 in the Supplement).…”

Mapping social reward and punishment processing in the human brain: A voxel-based meta-analysis of neuroimaging findings using the Social Incentive Delay task

“…However, a clear picture of the brain circuits underpinning social reward and punishment processing in the human brain is still missing due to inconsistencies in the areas identified across individual studies. This lack of consistency makes it difficult to inform targeted hypotheses about potentially disrupted areas in neuropsychiatric disorders, based on our understanding of the neural underpinnings of social reward/punishment processing in healthy individuals (Cremers et al, 2015;Delmonte et al, 2012;Kohls et al, 2018).…”

Gender differences in restricted and repetitive behaviors and interests in youth with autism

“…Moreover, “knowledge of factual information” about interests was less reported in affected girls than boys [Mandy et al, ]. Taken together, these findings suggest greater circumscribed interests in affected boys, which in turn may be related to both underlying reward and executive function processes [Anthony et al, ; Dichter et al, ; Kohls, Antezana, Mosner, Schultz, & Yerys, ].…”