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 the 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.

Keywords: Autism; fMRI; insula; repetitive behavior; restricted interests; reward; salience.

Figure 1

fMRI task design for a single sample run, and example stimuli for a participant whose restricted interest is trains (Own image block). Within each of the 5 runs, blocks of each condition were arranged in a pseudorandom sequence (random except that each began and ended with a visual baseline block) that was fixed across participants.

Figure 2

Behavioral keypress results. Viewing time for the ASD (dark bars) and TD (light bars) groups, for their own personalized stimuli (left) versus other children's stimuli (right). Viewing time results directly from participant effort expenditure to increase or decrease viewing duration from the default value of 5 sec.

Figure 3

Parent-report data from the YSII for the ASD (dark bars) and TD (light bars) groups. The Y-axis represents the severity score from the YSII measuring the intensity and interference of the interest in multiple domains of daily life.

Figure 4

One sample maps depicting significant clusters (uncorrected p<.005; cluster size ≥ 10) in the “Own” interest (top panel) and “Other” interest (bottom panel) conditions, relative to the visual baseline condition, for the ASD (left) and TD (right) groups. Clusters that remained after correction for multiple comparisons are highlighted with red arrows.

Figure 5

Maps of the most stringent contrast (Own-Other). A. One sample map showing significantly active clusters in the ASD (left) and TD (right) groups for this contrast. None of these clustered remained after correction for multiple comparisons. B. Two sample maps showing clusters that were significantly more active in the ASD than the TD group. Clusters that remained after correction for multiple comparisons are highlighted with red arrows. There were no clusters that were significantly more active in the TD than ASD group in this contrast.

Figure 6

Correlation (for the ASD group only) between parent report of interest severity from the YSII and percent signal change in the left insula that was significantly more active in the ASD group for the Own-Other contrast.