Resting-State Brain Network Dysfunctions Associated With Visuomotor Impairments in Autism Spectrum Disorder.

Zheng Wang,Yan Wang,Matthew W Mosconi,John A Sweeney,Su Lui,Qiyong Gong

doi:10.3389/fnint.2019.00017

Abstract

Background: Individuals with autism spectrum disorder (ASD) show elevated levels of motor variability that are associated with clinical outcomes. Cortical–cerebellar networks involved in visuomotor control have been implicated in postmortem and anatomical imaging studies of ASD. However, the extent to which these networks show intrinsic functional alterations in patients, and the relationship between intrinsic functional properties of cortical–cerebellar networks and visuomotor impairments in ASD have not yet been clarified.Methods: We examined the amplitude of low-frequency fluctuation (ALFF) of cortical and cerebellar brain regions during resting-state functional MRI (rs-fMRI) in 23 individuals with ASD and 16 typically developing (TD) controls. Regions of interest (ROIs) with ALFF values significantly associated with motor variability were identified for for patients and controls respectively, and their functional connectivity (FC) to each other and to the rest of the brain was examined.Results: For TD controls, greater ALFF in bilateral cerebellar crus I, left superior temporal gyrus, left inferior frontal gyrus, right supramarginal gyrus, and left angular gyrus each were associated with greater visuomotor variability. Greater ALFF in cerebellar lobule VIII was associated with less visuomotor variability. For individuals with ASD, greater ALFF in right calcarine cortex, right middle temporal gyrus (including MT/V5), left Heschl's gyrus, left post-central gyrus, right pre-central gyrus, and left precuneus was related to greater visuomotor variability. Greater ALFF in cerebellar vermis VI was associated with less visuomotor variability. Individuals with ASD and TD controls did not show differences in ALFF for any of these ROIs. Individuals with ASD showed greater posterior cerebellar connectivity with occipital and parietal cortices relative to TD controls, and reduced FC within cerebellum and between lateral cerebellum and pre-frontal and other regions of association cortex.Conclusion: Together, these findings suggest that increased resting oscillations within visuomotor networks in ASD are associated with more severe deficits in controlling variability during precision visuomotor behavior. Differences between individuals with ASD and TD controls in the topography of networks showing relationships to visuomotor behavior suggest atypical patterns of cerebellar–cortical specialization and connectivity in ASD that underlies previously documented visuomotor deficits.

Highlights

Autism spectrum disorder (ASD) is characterized by difficulties in social interaction and communication, a restricted repertoire of interests and stereotypic behaviors (American Psychiatric Association, 2013)
region of interest (ROI) that were positively correlated with force variability for typically developing (TD) controls after corrections for multiple comparisons included left inferior frontal gyrus, right supramarginal gyrus, left angular gyrus, left superior temporal gyrus, and bilateral cerebellar crus I
Greater amplitude of low frequency fluctuations (ALFF) values of sensorimotor cortical and cerebellar brain regions were associated with greater force variability in ASD, whereas greater ALFF values in cortical and cerebellar brain regions that comprise higher-order association networks were related to greater force variability in TD controls

Summary

Introduction

Autism spectrum disorder (ASD) is characterized by difficulties in social interaction and communication, a restricted repertoire of interests and stereotypic behaviors (American Psychiatric Association, 2013). Our group has documented that individuals with ASD show increased force variability relative to typically developing (TD) controls during visually guided precision gripping (Mosconi et al, 2015; Wang et al, 2015) and isometric index finger abduction (Wang et al, 2017). Non-human primate and task-based functional magnetic resonance imaging (tb-fMRI) studies have delineated distinct cortical–cerebellar networks involved in reactively adjusting sustained precision motor behavior in response to visual information (Kelly and Strick, 2003; Vaillancourt et al, 2006; Coombes et al, 2010). The extent to which these networks show intrinsic functional alterations in patients, and the relationship between intrinsic functional properties of cortical–cerebellar networks and visuomotor impairments in ASD have not yet been clarified

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Discussion

Conclusion