Intrinsic visual-motor synchrony correlates with social deficits in autism

Mary Beth Nebel, Ani Eloyan, Carrie A. Nettles, Kristie L. Sweeney, Katarina Ament, Rebecca E. Ward, Ann Choe, Anita D. Barber, James J Pekar, Stewart H Mostofsky

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
Pages (from-to)633-641
Number of pages9
JournalBiological Psychiatry
Volume79
Issue number8
DOIs
StatePublished - Apr 15 2016

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Autistic Disorder
Motor Skills
Brain
Autism Spectrum Disorder
Sensory Feedback
Gestures
Child Development
Neuroimaging
Motor Activity
Magnetic Resonance Imaging
Learning

Keywords

  • Autism
  • Functional connectivity
  • Imitation
  • Independent component analysis
  • Symptom severity
  • Visual-motor integration

ASJC Scopus subject areas

  • Biological Psychiatry

Cite this

Nebel, M. B., Eloyan, A., Nettles, C. A., Sweeney, K. L., Ament, K., Ward, R. E., ... Mostofsky, S. H. (2016). Intrinsic visual-motor synchrony correlates with social deficits in autism. Biological Psychiatry, 79(8), 633-641. https://doi.org/10.1016/j.biopsych.2015.08.029

Intrinsic visual-motor synchrony correlates with social deficits in autism. / Nebel, Mary Beth; Eloyan, Ani; Nettles, Carrie A.; Sweeney, Kristie L.; Ament, Katarina; Ward, Rebecca E.; Choe, Ann; Barber, Anita D.; Pekar, James J; Mostofsky, Stewart H.

In: Biological Psychiatry, Vol. 79, No. 8, 15.04.2016, p. 633-641.

Research output: Contribution to journalArticle

Nebel, MB, Eloyan, A, Nettles, CA, Sweeney, KL, Ament, K, Ward, RE, Choe, A, Barber, AD, Pekar, JJ & Mostofsky, SH 2016, 'Intrinsic visual-motor synchrony correlates with social deficits in autism', Biological Psychiatry, vol. 79, no. 8, pp. 633-641. https://doi.org/10.1016/j.biopsych.2015.08.029
Nebel MB, Eloyan A, Nettles CA, Sweeney KL, Ament K, Ward RE et al. Intrinsic visual-motor synchrony correlates with social deficits in autism. Biological Psychiatry. 2016 Apr 15;79(8):633-641. https://doi.org/10.1016/j.biopsych.2015.08.029
Nebel, Mary Beth ; Eloyan, Ani ; Nettles, Carrie A. ; Sweeney, Kristie L. ; Ament, Katarina ; Ward, Rebecca E. ; Choe, Ann ; Barber, Anita D. ; Pekar, James J ; Mostofsky, Stewart H. / Intrinsic visual-motor synchrony correlates with social deficits in autism. In: Biological Psychiatry. 2016 ; Vol. 79, No. 8. pp. 633-641.
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N2 - 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.

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