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Error-independent effect of sensory uncertainty on motor learning when both feedforward and feedback control processes are engaged

Integrating sensory information during movement and adapting motor plans over successive movements are both essential for accurate, flexible motor behaviour. When an ongoing movement is off target, feedback control mechanisms update the descending motor commands to counter the sensed error. Over lon...

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Detalles Bibliográficos
Autores principales: Hewitson, Christopher L., Kaplan, David M., Crossley, Matthew J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10522034/
https://www.ncbi.nlm.nih.gov/pubmed/37683013
http://dx.doi.org/10.1371/journal.pcbi.1010526
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author Hewitson, Christopher L.
Kaplan, David M.
Crossley, Matthew J.
author_facet Hewitson, Christopher L.
Kaplan, David M.
Crossley, Matthew J.
author_sort Hewitson, Christopher L.
collection PubMed
description Integrating sensory information during movement and adapting motor plans over successive movements are both essential for accurate, flexible motor behaviour. When an ongoing movement is off target, feedback control mechanisms update the descending motor commands to counter the sensed error. Over longer timescales, errors induce adaptation in feedforward planning so that future movements become more accurate and require less online adjustment from feedback control processes. Both the degree to which sensory feedback is integrated into an ongoing movement and the degree to which movement errors drive adaptive changes in feedforward motor plans have been shown to scale inversely with sensory uncertainty. However, since these processes have only been studied in isolation from one another, little is known about how they are influenced by sensory uncertainty in real-world movement contexts where they co-occur. Here, we show that sensory uncertainty may impact feedforward adaptation of reaching movements differently when feedback integration is present versus when it is absent. In particular, participants gradually adjust their movements from trial-to-trial in a manner that is well characterised by a slow and consistent envelope of error reduction. Riding on top of this slow envelope, participants exhibit large and abrupt changes in their initial movement vectors that are strongly correlated with the degree of sensory uncertainty present on the previous trial. However, these abrupt changes are insensitive to the magnitude and direction of the sensed movement error. These results prompt important questions for current models of sensorimotor learning under uncertainty and open up new avenues for future exploration in the field.
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spelling pubmed-105220342023-09-27 Error-independent effect of sensory uncertainty on motor learning when both feedforward and feedback control processes are engaged Hewitson, Christopher L. Kaplan, David M. Crossley, Matthew J. PLoS Comput Biol Research Article Integrating sensory information during movement and adapting motor plans over successive movements are both essential for accurate, flexible motor behaviour. When an ongoing movement is off target, feedback control mechanisms update the descending motor commands to counter the sensed error. Over longer timescales, errors induce adaptation in feedforward planning so that future movements become more accurate and require less online adjustment from feedback control processes. Both the degree to which sensory feedback is integrated into an ongoing movement and the degree to which movement errors drive adaptive changes in feedforward motor plans have been shown to scale inversely with sensory uncertainty. However, since these processes have only been studied in isolation from one another, little is known about how they are influenced by sensory uncertainty in real-world movement contexts where they co-occur. Here, we show that sensory uncertainty may impact feedforward adaptation of reaching movements differently when feedback integration is present versus when it is absent. In particular, participants gradually adjust their movements from trial-to-trial in a manner that is well characterised by a slow and consistent envelope of error reduction. Riding on top of this slow envelope, participants exhibit large and abrupt changes in their initial movement vectors that are strongly correlated with the degree of sensory uncertainty present on the previous trial. However, these abrupt changes are insensitive to the magnitude and direction of the sensed movement error. These results prompt important questions for current models of sensorimotor learning under uncertainty and open up new avenues for future exploration in the field. Public Library of Science 2023-09-08 /pmc/articles/PMC10522034/ /pubmed/37683013 http://dx.doi.org/10.1371/journal.pcbi.1010526 Text en © 2023 Hewitson et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Hewitson, Christopher L.
Kaplan, David M.
Crossley, Matthew J.
Error-independent effect of sensory uncertainty on motor learning when both feedforward and feedback control processes are engaged
title Error-independent effect of sensory uncertainty on motor learning when both feedforward and feedback control processes are engaged
title_full Error-independent effect of sensory uncertainty on motor learning when both feedforward and feedback control processes are engaged
title_fullStr Error-independent effect of sensory uncertainty on motor learning when both feedforward and feedback control processes are engaged
title_full_unstemmed Error-independent effect of sensory uncertainty on motor learning when both feedforward and feedback control processes are engaged
title_short Error-independent effect of sensory uncertainty on motor learning when both feedforward and feedback control processes are engaged
title_sort error-independent effect of sensory uncertainty on motor learning when both feedforward and feedback control processes are engaged
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10522034/
https://www.ncbi.nlm.nih.gov/pubmed/37683013
http://dx.doi.org/10.1371/journal.pcbi.1010526
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