Atypical Associations between Gesture Processing, Performance and Social Symptoms in Autism Spectrum Disorder

Background: Individuals with autism spectrum disorder (ASD) demonstrate impairments in nonverbal communication, including diminished use of gestures, gesturing errors and difficulties with imitation. One potential explanation for these impairments is a deficit in perceiving biological motion (BM). Decreased visual sensitivity to BM may inhibit adequate processing of dynamic non-verbal social cues, like gestures. This perceptual dysfunction may impede learning and subsequent performance of these actions, resulting in nonverbal communication deficits and atypical social development in ASD.

Objectives: The goal of this study was to examine the brain-behavior relationships between neural activity during gesture processing, gesturing abilities and social symptoms to identify atypical mechanisms underlying perception-action coupling and how this abnormality may relate to compromised social development in ASD.

Methods: Participants included 15 children and adolescents with ASD and 16 typically-developing (TD) controls, ages 9 to 17. During the fMRI task, participants viewed animations (created by applying digitalized motion capture of actions performed by an actor to a 3D human model) of both functional (e.g. driving) and communicative (e.g. waving) gestures. Gesture performance was assessed outside the scanner using a charade-style paradigm, in which participants enacted a series of 15 familiar actions (e.g. brush teeth), which were double-coded by raters blind to diagnosis for quality of specific components (e.g. limb movement, hand posture). A parent-report measure of social functioning, the Social Responsiveness Scale (SRS-2), was also collected.

Results: In whole brain analyses, both groups showed activation of lateral occipital-temporal cortex (LOTC), a region sensitive to both body motion and form. Beta parameters were averaged from 6-mm radius spherical regions of interest (ROI) centered around individual peak coordinates in bilateral LOTC. This ROI analysis revealed that the ASD group had reduced activity in left LOTC compared to controls (p < .001). In order to explore this group difference in neural activity, we examined associations between activation, gesture performance and social symptomology. The TD group showed a negative correlation between left LOTC activity and SRS scores (r = -.49, p <.05), not present in the ASD group (r = -.09, p = .76). Gesture performance was also negatively correlated with SRS scores in both groups, significant only in the TD group (r = -.60, p <.05; ASD: r = -.57, p = .05). These associations demonstrate links between social impairment and both diminished processing and performance of gestures. In a subset of participants who completed both fMRI and behavioral components (8 ASD, 12 TD), activity in left LOTC was positively associated with gesture performance in the TD group (r = .65, p < .05) but not the ASD group (r = .08, p = .86).

Conclusions: These findings suggest that in typical development, increased neural processing of gestures is associated with better gesture performance and social functioning, supporting a link between perception of dynamic social cues, subsequent gesturing abilities and sociability. The absence of such relationships in the ASD group may reflect dysfunction in a perception-action coupling mechanism that leads to cascading effects on atypical social development.