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Initial action output and feedback-guided motor behaviors in autism spectrum disorder
BACKGROUND: Sensorimotor issues are common in autism spectrum disorder (ASD), related to core symptoms, and predictive of worse functional outcomes. Deficits in rapid behaviors supported primarily by feedforward mechanisms, and continuous, feedback-guided motor behaviors each have been reported, but...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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BioMed Central
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8272343/ https://www.ncbi.nlm.nih.gov/pubmed/34246292 http://dx.doi.org/10.1186/s13229-021-00452-8 |
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author | Unruh, Kathryn E. McKinney, Walker S. Bojanek, Erin K. Fleming, Kandace K. Sweeney, John A. Mosconi, Matthew W. |
author_facet | Unruh, Kathryn E. McKinney, Walker S. Bojanek, Erin K. Fleming, Kandace K. Sweeney, John A. Mosconi, Matthew W. |
author_sort | Unruh, Kathryn E. |
collection | PubMed |
description | BACKGROUND: Sensorimotor issues are common in autism spectrum disorder (ASD), related to core symptoms, and predictive of worse functional outcomes. Deficits in rapid behaviors supported primarily by feedforward mechanisms, and continuous, feedback-guided motor behaviors each have been reported, but the degrees to which they are distinct or co-segregate within individuals and across development are not well understood. METHODS: We characterized behaviors that varied in their involvement of feedforward control relative to feedback control across skeletomotor (precision grip force) and oculomotor (saccades) control systems in 109 individuals with ASD and 101 age-matched typically developing controls (range: 5–29 years) including 58 individuals with ASD and 57 controls who completed both grip and saccade tests. Grip force was examined across multiple force (15, 45, and 85% MVC) and visual gain levels (low, medium, high). Maximum grip force also was examined. During grip force tests, reaction time, initial force output accuracy, variability, and entropy were examined. For the saccade test, latency, accuracy, and trial-wise variability of latency and accuracy were examined. RESULTS: Relative to controls, individuals with ASD showed similar accuracy of initial grip force but reduced accuracy of saccadic eye movements specific to older ages of our sample. Force variability was greater in ASD relative to controls, but saccade gain variability (across trials) was not different between groups. Force entropy was reduced in ASD, especially at older ages. We also find reduced grip strength in ASD that was more severe in dominant compared to non-dominant hands. LIMITATIONS: Our age-related findings rely on cross-sectional data. Longitudinal studies of sensorimotor behaviors and their associations with ASD symptoms are needed. CONCLUSIONS: We identify reduced accuracy of initial motor output in ASD that was specific to the oculomotor system implicating deficient feedforward control that may be mitigated during slower occurring behaviors executed in the periphery. Individuals with ASD showed increased continuous force variability but similar levels of trial-to-trial saccade accuracy variability suggesting that feedback-guided refinement of motor commands is deficient specifically when adjustments occur rapidly during continuous behavior. We also document reduced lateralization of grip strength in ASD implicating atypical hemispheric specialization. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13229-021-00452-8. |
format | Online Article Text |
id | pubmed-8272343 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-82723432021-07-12 Initial action output and feedback-guided motor behaviors in autism spectrum disorder Unruh, Kathryn E. McKinney, Walker S. Bojanek, Erin K. Fleming, Kandace K. Sweeney, John A. Mosconi, Matthew W. Mol Autism Research BACKGROUND: Sensorimotor issues are common in autism spectrum disorder (ASD), related to core symptoms, and predictive of worse functional outcomes. Deficits in rapid behaviors supported primarily by feedforward mechanisms, and continuous, feedback-guided motor behaviors each have been reported, but the degrees to which they are distinct or co-segregate within individuals and across development are not well understood. METHODS: We characterized behaviors that varied in their involvement of feedforward control relative to feedback control across skeletomotor (precision grip force) and oculomotor (saccades) control systems in 109 individuals with ASD and 101 age-matched typically developing controls (range: 5–29 years) including 58 individuals with ASD and 57 controls who completed both grip and saccade tests. Grip force was examined across multiple force (15, 45, and 85% MVC) and visual gain levels (low, medium, high). Maximum grip force also was examined. During grip force tests, reaction time, initial force output accuracy, variability, and entropy were examined. For the saccade test, latency, accuracy, and trial-wise variability of latency and accuracy were examined. RESULTS: Relative to controls, individuals with ASD showed similar accuracy of initial grip force but reduced accuracy of saccadic eye movements specific to older ages of our sample. Force variability was greater in ASD relative to controls, but saccade gain variability (across trials) was not different between groups. Force entropy was reduced in ASD, especially at older ages. We also find reduced grip strength in ASD that was more severe in dominant compared to non-dominant hands. LIMITATIONS: Our age-related findings rely on cross-sectional data. Longitudinal studies of sensorimotor behaviors and their associations with ASD symptoms are needed. CONCLUSIONS: We identify reduced accuracy of initial motor output in ASD that was specific to the oculomotor system implicating deficient feedforward control that may be mitigated during slower occurring behaviors executed in the periphery. Individuals with ASD showed increased continuous force variability but similar levels of trial-to-trial saccade accuracy variability suggesting that feedback-guided refinement of motor commands is deficient specifically when adjustments occur rapidly during continuous behavior. We also document reduced lateralization of grip strength in ASD implicating atypical hemispheric specialization. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13229-021-00452-8. BioMed Central 2021-07-10 /pmc/articles/PMC8272343/ /pubmed/34246292 http://dx.doi.org/10.1186/s13229-021-00452-8 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Unruh, Kathryn E. McKinney, Walker S. Bojanek, Erin K. Fleming, Kandace K. Sweeney, John A. Mosconi, Matthew W. Initial action output and feedback-guided motor behaviors in autism spectrum disorder |
title | Initial action output and feedback-guided motor behaviors in autism spectrum disorder |
title_full | Initial action output and feedback-guided motor behaviors in autism spectrum disorder |
title_fullStr | Initial action output and feedback-guided motor behaviors in autism spectrum disorder |
title_full_unstemmed | Initial action output and feedback-guided motor behaviors in autism spectrum disorder |
title_short | Initial action output and feedback-guided motor behaviors in autism spectrum disorder |
title_sort | initial action output and feedback-guided motor behaviors in autism spectrum disorder |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8272343/ https://www.ncbi.nlm.nih.gov/pubmed/34246292 http://dx.doi.org/10.1186/s13229-021-00452-8 |
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