Affective neural response to restricted interests in autism spectrum disorders

Abstract

Background Restricted interests are a class of repetitive behavior in autism spectrum disorders (ASD) whose intensity and narrow focus often contribute to significant interference with daily functioning. While numerous neuroimaging studies have investigated executive circuits as putative neural substrates of repetitive behavior, recent work implicates affective neural circuits in restricted interests. We sought to explore the role of affective neural circuits and determine how restricted interests are distinguished from hobbies or interests in typical development. Methods We compared a group of children with ASD to a typically developing (TD) group of children with strong interests or hobbies, employing parent report, an operant behavioral task, and functional imaging with personalized stimuli based on individual interests. Results While performance on the operant task was similar between the two groups, parent report of intensity and interference of interests was significantly higher in the ASD group. Both the ASD and TD groups showed increased BOLD response in widespread affective neural regions to pictures of their own interest. When viewing pictures of other children's interests, the TD group showed a similar pattern, whereas BOLD response in the ASD group was much more limited. Increased BOLD response in the insula and anterior cingulate cortex distinguished the ASD from the TD group, and parent report of the intensity and interference with daily life of the child's restricted interest predicted insula response. Conclusions While affective neural network response and operant behavior are comparable in typical and restricted interests, the narrowness of focus that clinically distinguishes restricted interests in ASD is reflected in more interference in daily life and aberrantly enhanced insula and anterior cingulate response to individuals’ own interests in the ASD group. These results further support the involvement of affective neural networks in repetitive behaviors in ASD.

Social Orienting and Attention Is Influenced by the Presence of Competing Nonsocial Information in Adolescents with Autism

“…Enhanced nonsocial motivation has been found in individuals with ASD using behavioral measures (Damiano et al, 2012; Sasson et al, 2012; Watson et al, 2015) and other eye-tracking paradigms (Sasson et al, 2008, 2011; Elison et al, 2012; Sasson and Touchstone, 2014). These object preference findings are important to consider in light of neuroimaging studies that show enhanced activation of reward circuitry in ASD in response to nonsocial information (Dichter et al, 2012; Cascio et al, 2014). We also found evidence that decreased social attention may be related to increases in nonsocial preference in ASD.…”

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

“…RIs are, by definition, idiosyncratic and person-specific, and idiosyncratic RIs have been used in prior ASD studies (Cascio et al, 2014); nonetheless, the use of a standardized set of images allowed for increased internal validity because stimuli viewed by different participants did not differ in semantic content or visual features (e.g., luminance, contrast, etc.) and did not contain any depictions of faces.…”

“…Additionally, results are consistent with prior findings that certain types of nonsocial stimuli may be highly salient for individuals with ASD (Klin et al, 2003; Klin et al, 2002). This “nonsocial bias” may be mechanistically related to the development of RIs in ASD and may interfere with social development (Cascio et al, 2014; Klin et al, 2007; Turner-Brown et al, 2011). It may be the case that intensive behavioral interventions for children with ASD should expand their focus from increasing the salience and reward value of social interactions to also targeting the effects of RIs in ASD on social communicative skills (Boyd, Conroy, Mancil, Nakao, & Alter, 2007).…”

“…Additionally, whereas the social motivation theory of ASD suggests that neural systems supporting motivation and attention may be hyporesponsive to social stimuli in ASD (Delmonte et al, 2012; Scott-Van Zeeland, Dapretto, Ghahremani, Poldrack, & Bookheimer, 2010; Yirmiya, Kasari, Sigman, & Mundy, 1989), these same neural systems may be hyperresponsive to certain classes of nonsocial stimuli in ASD (Cascio et al, 2014). This mechanistic account of RIs in ASD explains why individuals with ASD may exhibit positive affect in response to specific nonsocial aspects of the environment (Attwood, 2003; Sasson, Dichter, & Bodfish, 2012) and may even engage in increased joint attention (Vismara & Lyons, 2007) and eye contact (Nadig, Lee, Singh, Bosshart, & Ozonoff, 2010) when such RIs are incorporated into social interactions.…”

Brain imaging research in autism spectrum disorders

“…The similarity is activation of bilateral amygdala, and the difference is significantly increased activation of the left anterior insula and anterior cingulate gyrus in ASD in response to pictures of one’s own interest [4 ▪ ]. The anterior insula and anterior cingulate gyrus are key nodes of the salience neural network, which appears spatially restricted at the structural level [5] and overconnected within itself at the functional level in ASD [6].…”