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Movement predictability modulates sensorimotor processing

INTRODUCTION: An important factor for optimal sensorimotor control is how well we are able to predict sensory feedback from internal and external sources during movement. If predictability decreases due to external disturbances, the brain is able to adjust muscle activation and the filtering of inco...

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Autores principales: Altermatt, Miriam, Thomas, Felix Alexander, Wenderoth, Nicole
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10694232/
http://dx.doi.org/10.3389/fnhum.2023.1237407
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author Altermatt, Miriam
Thomas, Felix Alexander
Wenderoth, Nicole
author_facet Altermatt, Miriam
Thomas, Felix Alexander
Wenderoth, Nicole
author_sort Altermatt, Miriam
collection PubMed
description INTRODUCTION: An important factor for optimal sensorimotor control is how well we are able to predict sensory feedback from internal and external sources during movement. If predictability decreases due to external disturbances, the brain is able to adjust muscle activation and the filtering of incoming sensory inputs. However, little is known about sensorimotor adjustments when predictability is increased by availability of additional internal feedback. In the present study we investigated how modifications of internal and external sensory feedback influence the control of muscle activation and gating of sensory input. METHODS: Co-activation of forearm muscles, somatosensory evoked potentials (SEP) and short afferent inhibition (SAI) were assessed during three object manipulation tasks designed to differ in the predictability of sensory feedback. These included manipulation of a shared object with both hands (predictable coupling), manipulation of two independent objects without (uncoupled) and with external interference on one of the objects (unpredictable coupling). RESULTS: We found a task-specific reduction in co-activation during the predictable coupling compared to the other tasks. Less sensory gating, reflected in larger subcortical SEP amplitudes, was observed in the unpredictable coupling task. SAI behavior was closely linked to the subcortical SEP component indicating an important function of subcortical sites in predictability related SEP gating and their direct influence on M1 inhibition. DISCUSSION: Together, these findings suggest that the unpredictable coupling task cannot only rely on predictive forward control and is compensated by enhancing co-activation and increasing the saliency for external stimuli by reducing sensory gating at subcortical level. This behavior might serve as a preparatory step to compensate for external disturbances and to enhance processing and integration of all incoming external stimuli to update the current sensorimotor state. In contrast, predictive forward control is accurate in the predictable coupling task due to the integrated sensory feedback from both hands where sensorimotor resources are economized by reducing muscular co-activation and increasing sensory gating.
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spelling pubmed-106942322023-12-05 Movement predictability modulates sensorimotor processing Altermatt, Miriam Thomas, Felix Alexander Wenderoth, Nicole Front Hum Neurosci Neuroscience INTRODUCTION: An important factor for optimal sensorimotor control is how well we are able to predict sensory feedback from internal and external sources during movement. If predictability decreases due to external disturbances, the brain is able to adjust muscle activation and the filtering of incoming sensory inputs. However, little is known about sensorimotor adjustments when predictability is increased by availability of additional internal feedback. In the present study we investigated how modifications of internal and external sensory feedback influence the control of muscle activation and gating of sensory input. METHODS: Co-activation of forearm muscles, somatosensory evoked potentials (SEP) and short afferent inhibition (SAI) were assessed during three object manipulation tasks designed to differ in the predictability of sensory feedback. These included manipulation of a shared object with both hands (predictable coupling), manipulation of two independent objects without (uncoupled) and with external interference on one of the objects (unpredictable coupling). RESULTS: We found a task-specific reduction in co-activation during the predictable coupling compared to the other tasks. Less sensory gating, reflected in larger subcortical SEP amplitudes, was observed in the unpredictable coupling task. SAI behavior was closely linked to the subcortical SEP component indicating an important function of subcortical sites in predictability related SEP gating and their direct influence on M1 inhibition. DISCUSSION: Together, these findings suggest that the unpredictable coupling task cannot only rely on predictive forward control and is compensated by enhancing co-activation and increasing the saliency for external stimuli by reducing sensory gating at subcortical level. This behavior might serve as a preparatory step to compensate for external disturbances and to enhance processing and integration of all incoming external stimuli to update the current sensorimotor state. In contrast, predictive forward control is accurate in the predictable coupling task due to the integrated sensory feedback from both hands where sensorimotor resources are economized by reducing muscular co-activation and increasing sensory gating. Frontiers Media S.A. 2023-11-20 /pmc/articles/PMC10694232/ http://dx.doi.org/10.3389/fnhum.2023.1237407 Text en Copyright © 2023 Altermatt, Thomas and Wenderoth. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Altermatt, Miriam
Thomas, Felix Alexander
Wenderoth, Nicole
Movement predictability modulates sensorimotor processing
title Movement predictability modulates sensorimotor processing
title_full Movement predictability modulates sensorimotor processing
title_fullStr Movement predictability modulates sensorimotor processing
title_full_unstemmed Movement predictability modulates sensorimotor processing
title_short Movement predictability modulates sensorimotor processing
title_sort movement predictability modulates sensorimotor processing
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10694232/
http://dx.doi.org/10.3389/fnhum.2023.1237407
work_keys_str_mv AT altermattmiriam movementpredictabilitymodulatessensorimotorprocessing
AT thomasfelixalexander movementpredictabilitymodulatessensorimotorprocessing
AT wenderothnicole movementpredictabilitymodulatessensorimotorprocessing