Diminished social reward anticipation in the broad autism phenotype as revealed by event-related brain potentials

Abstract

Diminished responsivity to reward incentives is a key contributor to the social-communication problems seen in autism spectrum disorders (ASDs). Social motivation theories suggest that individuals with ASD do not experience social interactions as rewarding, leading to negative consequences for the development of brain circuitry subserving social information. In this study, we examined neural responses to social and non-social reward anticipation in 35 typically developing young adults, examining modulation of reward sensitivity by level of autistic traits. Using an Event-related potential incentive-delay task incorporating novel, more ecologically valid forms of reward, higher expression of autistic traits was associated with an attenuated P3 response to the anticipation of social (simulated real-time video feedback from an observer), but not non-social (candy), rewards. Exploratory analyses revealed that this was unrelated to mentalizing ability. The P3 component reflects motivated attention to reward signals, suggesting attenuated motivation allocation specific to social incentives. The study extends prior findings of atypical reward anticipation in ASD, demonstrating that attenuated social reward responsiveness extends to autistic traits in the range of typical functioning. Results support the development of innovative paradigms for investigating social and non-social reward responsiveness. Insight into vulnerabilities in reward processing is critical for understanding social function in ASD.

Common and distinct modulation of electrophysiological indices of feedback processing by autistic and psychopathic traits

“…As in our prior work (Cox et al, 2015; McPartland et al, 2012), the current study found individuals with higher levels of autistic traits displayed typical patterns of neural responsiveness to feedback presented in a non-social context; however, the neural response was attenuated for feedback presented in social contexts. As FRN amplitude is dependent upon task involvement and has been proposed to reflect a neural index of the motivational salience of outcomes (Yeung et al, 2005), these results suggest that individuals with high levels of autistic traits found social feedback less salient.…”

“…In support of this hypothesis, individuals with ASD display atypical neural response to social feedback both for social reward (e.g., smiling faces; Scott-Van Zeeland, Dapretto, Ghahremani, Poldrack, & Bookheimer, 2010; Dichter, Richey, Rittenberg, Sabatino, & Bodfish, 2012) and social loss (e.g., social exclusion; Masten et al, 2011; McPartland, Crowley, et al, 2011a). This pattern of selectively decreased sensitivity extends to the broad autism phenotype, with decreased neural activity found during anticipation of social rewards, but not non-social rewards, in individuals with high levels of autistic traits (Cox et al, 2015). Electrophysiological studies of feedback processing focus upon the feedback related negativity (FRN), a negative event-related potential component (ERP) found 200–300ms after feedback delivery over the frontal lobes.…”

Late Positive Potential ERP Responses to Social and Nonsocial Stimuli in Youth with Autism Spectrum Disorder

“…These studies have generally found longer N170 latencies to faces (but not objects) in ASD (Cygan, Tacikowski, Ostaszewski, Chojnicka, & Nowicka, 2014; Dalton, Holsen, Abbeduto, & Davidson, 2008; McPartland et al, 2011), a lack of N170 modulation by directed attention to faces in ASD (Gunji, Inagaki, Inoue, Takeshima, & Kaga, 2009), diminished N170 amplitude in the right hemisphere to faces and lack of P300 amplitude differences between self and other faces in ASD (Gunji et al, 2009), and greater P100 and N170 amplitude to faces versus houses and lack of differentiation of responses to upright vs inverted faces (Webb et al, 2012). More recent work has found attenuated P3 response during the anticipation of social, but not non-social, rewards in typically developing young adults with high levels of autistic traits (Cox et al, 2015). …”

Divergent relationship of depression severity to social reward responses among patients with bipolar versus unipolar depression

“…Fourth, we used a facial affective feedback task to assess responses to social rewards. More interactive and complex social reward paradigms that utilize faces with verbal praise or even live interactions via hyperscanning can be applied in future studies to develop and evaluate models of social reward processing (Scott-Van Zeeland et al 2010; Bilek et al, 2015; Cox et al, 2015). Finally, we did not assess real-world social function, and future work would benefit from the inclusion of social and other functional outcome measures.…”