Intrinsic Visual-Motor Synchrony Correlates With Social Deficits in Autism

Abstract

Background: Imitation, which is impaired in children with autism spectrum disorder (ASD) and critically depends on the integration of visual input with motor output, likely impacts both motor and social skill acquisition in children with ASD; however, it is unclear what brain mechanisms contribute to this impairment. Children with ASD also exhibit what appears to be an ASD-specific bias against using visual feedback during motor learning. Does the temporal congruity of intrinsic activity, or functional connectivity, between motor and visual brain regions contribute to ASD-associated deficits in imitation, motor, and social skills?

Methods: We acquired resting-state functional magnetic resonance imaging scans from 100 8- to 12-year-old children (50 ASD). Group independent component analysis was used to estimate functional connectivity between visual and motor systems. Brain-behavior relationships were assessed by regressing functional connectivity measures with social deficit severity, imitation, and gesture performance scores.

Results: We observed increased intrinsic asynchrony between visual and motor systems in children with ASD and replicated this finding in an independent sample from the Autism Brain Imaging Data Exchange. Moreover, children with more out-of-sync intrinsic visual-motor activity displayed more severe autistic traits, while children with greater intrinsic visual-motor synchrony were better imitators.

Conclusions: Our twice replicated findings confirm that visual-motor functional connectivity is disrupted in ASD. Furthermore, the observed temporal incongruity between visual and motor systems, which may reflect diminished integration of visual consequences with motor output, was predictive of the severity of social deficits and may contribute to impaired social-communicative skill development in children with ASD.

Keywords: Autism; Functional connectivity; Imitation; Independent component analysis; Symptom severity; Visual-motor integration.

Figure 1. Intrinsic visual-motor synchronization in the KKI sample

A) Topography of visual and motor networks estimated from the fMRI data using group independent component analysis (37). The motor system was represented by two components reflecting the separation of dorsomedial lower limb areas (“LL”, blue) from more lateral upper limb areas (“UL”, red) within the pre and post central gyri. The visual system was represented by three components. Two (“VC1”, green, and “VC2”, purple) were localized to early visual processing areas, while the third (“VC3”, pink) was situated mainly in the lateral occipital cortex. These maps are the result of entering participant-specific motor and visual components into one-sample t-tests. B) Dot plots and 95% confidence intervals of the intrinsic synchronization of each pair of participant-specific motor and visual networks for each group. Typically developing children (TD, N=50) are in blue; children with autism (ASD, N=50) are in red. Synchronization was calculated as the Pearson correlation between component time courses and converted to a z-score using Fisher's transform. Confidence intervals are based on comparing the mean of each group to 0. VC3-UL was the only visual-motor pair with a significant group difference in connectivity (t = 3.923, p < .001, non-overlapping confidence intervals).

Figure 2. Intrinsic visual-motor synchronization in the UM_1 sample

A) Topography of estimated visual and motor networks. B) Dot plots and 95% confidence intervals of the intrinsic synchronization of each pair of participant-specific motor and visual networks by group. Typically developing children (TD, N=25) are in blue; children with autism (ASD, N=25) are in red. Confidence intervals are based on comparing the mean of each group to 0. VC3-UL was the only visual-motor pair with a significant group difference in connectivity (t = 3.673, p = .006).

Figure 3. Intrinsic visual-motor synchronization as a predictor of social, imitation and overall gesture ability

A) The Social Responsiveness Scale (SRS), a measure of social engagement in naturalistic settings, was scored for all of the typically developing (TD) children and most of the children with autism (ASD, 49 of 50). The inset shows upper limb motor and higher order visual processing areas included in the UL (red) and VC3 (pink) networks, respectively. The x axes represent the intrinsic synchronization between UL and VC3. B) Imitation ability was assessed by asking the child to mimic a series of 34 actions (performed one at a time). C) Overall gesture ability (praxis) was assessed by asking the child to perform a series of 25 gestures to verbal command and 17 gestures using a common tool in addition to the 34 imitated. All TD children and 43 out of 50 children with ASD completed the praxis exam.