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

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...

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Main Authors: Zheng Wang, Yan Wang, John A. Sweeney, Qiyong Gong, Su Lui, Matthew W. Mosconi
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-05-01
Series:Frontiers in Integrative Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnint.2019.00017/full
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language English
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author Zheng Wang
Yan Wang
John A. Sweeney
John A. Sweeney
Qiyong Gong
Su Lui
Matthew W. Mosconi
Matthew W. Mosconi
Matthew W. Mosconi
spellingShingle Zheng Wang
Yan Wang
John A. Sweeney
John A. Sweeney
Qiyong Gong
Su Lui
Matthew W. Mosconi
Matthew W. Mosconi
Matthew W. Mosconi
Resting-State Brain Network Dysfunctions Associated With Visuomotor Impairments in Autism Spectrum Disorder
Frontiers in Integrative Neuroscience
autism spectrum disorder
resting-state functional MRI
visuomotor control
precision grip
cortical–cerebellar connectivity
amplitude of low-frequency fluctuations
author_facet Zheng Wang
Yan Wang
John A. Sweeney
John A. Sweeney
Qiyong Gong
Su Lui
Matthew W. Mosconi
Matthew W. Mosconi
Matthew W. Mosconi
author_sort Zheng Wang
title Resting-State Brain Network Dysfunctions Associated With Visuomotor Impairments in Autism Spectrum Disorder
title_short Resting-State Brain Network Dysfunctions Associated With Visuomotor Impairments in Autism Spectrum Disorder
title_full Resting-State Brain Network Dysfunctions Associated With Visuomotor Impairments in Autism Spectrum Disorder
title_fullStr Resting-State Brain Network Dysfunctions Associated With Visuomotor Impairments in Autism Spectrum Disorder
title_full_unstemmed Resting-State Brain Network Dysfunctions Associated With Visuomotor Impairments in Autism Spectrum Disorder
title_sort resting-state brain network dysfunctions associated with visuomotor impairments in autism spectrum disorder
publisher Frontiers Media S.A.
series Frontiers in Integrative Neuroscience
issn 1662-5145
publishDate 2019-05-01
description 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.
topic autism spectrum disorder
resting-state functional MRI
visuomotor control
precision grip
cortical–cerebellar connectivity
amplitude of low-frequency fluctuations
url https://www.frontiersin.org/article/10.3389/fnint.2019.00017/full
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spelling doaj-6fc91ff2d41544548f35224de73a947c2020-11-24T22:10:04ZengFrontiers Media S.A.Frontiers in Integrative Neuroscience1662-51452019-05-011310.3389/fnint.2019.00017451023Resting-State Brain Network Dysfunctions Associated With Visuomotor Impairments in Autism Spectrum DisorderZheng Wang0Yan Wang1John A. Sweeney2John A. Sweeney3Qiyong Gong4Su Lui5Matthew W. Mosconi6Matthew W. Mosconi7Matthew W. Mosconi8Department of Occupational Therapy, University of Florida, Gainesville, FL, United StatesHuaxi Magnetic Resonance Research Center, Department of Radiology, West China Hospital of Sichuan University, Chengdu, ChinaHuaxi Magnetic Resonance Research Center, Department of Radiology, West China Hospital of Sichuan University, Chengdu, ChinaDepartment of Psychiatry and Behavioral Neuroscience, University of Cincinnati College of Medicine, Cincinnati, OH, United StatesHuaxi Magnetic Resonance Research Center, Department of Radiology, West China Hospital of Sichuan University, Chengdu, ChinaHuaxi Magnetic Resonance Research Center, Department of Radiology, West China Hospital of Sichuan University, Chengdu, ChinaSchiefelbusch Institute for Life Span Studies, University of Kansas, Lawrence, KS, United StatesClinical Child Psychology Program, University of Kansas, Lawrence, KS, United StatesKansas Center for Autism Research and Training, University of Kansas, Lawrence, KS, United StatesBackground: 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.https://www.frontiersin.org/article/10.3389/fnint.2019.00017/fullautism spectrum disorderresting-state functional MRIvisuomotor controlprecision gripcortical–cerebellar connectivityamplitude of low-frequency fluctuations