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Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation

Sensorimotor memory built through previous hand-object interactions allows subjects to plan grasp forces. The memory-based mechanism is particularly effective when contact points on the object do not change across multiple manipulations, thus allowing subjects to generate the same forces in a feedfo...

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Detalles Bibliográficos
Autores principales: Davare, Marco, Parikh, Pranav J., Santello, Marco
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Physiological Society 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6485741/
https://www.ncbi.nlm.nih.gov/pubmed/30726158
http://dx.doi.org/10.1152/jn.00800.2018
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author Davare, Marco
Parikh, Pranav J.
Santello, Marco
author_facet Davare, Marco
Parikh, Pranav J.
Santello, Marco
author_sort Davare, Marco
collection PubMed
description Sensorimotor memory built through previous hand-object interactions allows subjects to plan grasp forces. The memory-based mechanism is particularly effective when contact points on the object do not change across multiple manipulations, thus allowing subjects to generate the same forces in a feedforward fashion. However, allowing subjects to choose where to grasp an object causes trial-to-trial variability in fingertip positioning, suggesting a decreased ability to predict where the object will be grasped. In this scenario, subjects modulate forces on a trial-to-trial basis as a function of fingertip positioning. We suggested that this fingertip force-to-position modulation could be implemented by transforming feedback of digit placement into an accurate distribution of fingertip forces. Thus, decreasing certainty of fingertip position on an object would cause a shift from predominantly memory- to feedback-based force control mechanisms. To gain further insight into these sensorimotor transformation mechanisms, we asked subjects to grasp and lift an object with an asymmetrical center of mass while preventing it from tilting. To isolate the effect of digit placement uncertainty, we designed two experimental conditions that differed in terms of predictability of fingertip position but had similar average fingertip positioning and force distribution. We measured corticospinal excitability to probe possible changes in sensorimotor processing associated with digit placement uncertainty. We found a differential effect of sensorimotor uncertainty after but not before object contact. Our results suggest that sensorimotor integration is rapidly tuned after object contact based on different processing demands for memory versus feedback mechanisms underlying the control of manipulative forces. NEW & NOTEWORTHY The relative contribution of predictive and feedback mechanisms for scaling digit forces to position during dexterous manipulation depends on the predictability of where the object will be grasped. We found that corticospinal excitability shortly after contact was sensitive to digit position predictability. This supports the proposition that distinct sensorimotor integration processes are engaged, depending on the role of feedback about digit placement versus sensorimotor memory in controlling manipulative forces.
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spelling pubmed-64857412019-04-30 Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation Davare, Marco Parikh, Pranav J. Santello, Marco J Neurophysiol Research Article Sensorimotor memory built through previous hand-object interactions allows subjects to plan grasp forces. The memory-based mechanism is particularly effective when contact points on the object do not change across multiple manipulations, thus allowing subjects to generate the same forces in a feedforward fashion. However, allowing subjects to choose where to grasp an object causes trial-to-trial variability in fingertip positioning, suggesting a decreased ability to predict where the object will be grasped. In this scenario, subjects modulate forces on a trial-to-trial basis as a function of fingertip positioning. We suggested that this fingertip force-to-position modulation could be implemented by transforming feedback of digit placement into an accurate distribution of fingertip forces. Thus, decreasing certainty of fingertip position on an object would cause a shift from predominantly memory- to feedback-based force control mechanisms. To gain further insight into these sensorimotor transformation mechanisms, we asked subjects to grasp and lift an object with an asymmetrical center of mass while preventing it from tilting. To isolate the effect of digit placement uncertainty, we designed two experimental conditions that differed in terms of predictability of fingertip position but had similar average fingertip positioning and force distribution. We measured corticospinal excitability to probe possible changes in sensorimotor processing associated with digit placement uncertainty. We found a differential effect of sensorimotor uncertainty after but not before object contact. Our results suggest that sensorimotor integration is rapidly tuned after object contact based on different processing demands for memory versus feedback mechanisms underlying the control of manipulative forces. NEW & NOTEWORTHY The relative contribution of predictive and feedback mechanisms for scaling digit forces to position during dexterous manipulation depends on the predictability of where the object will be grasped. We found that corticospinal excitability shortly after contact was sensitive to digit position predictability. This supports the proposition that distinct sensorimotor integration processes are engaged, depending on the role of feedback about digit placement versus sensorimotor memory in controlling manipulative forces. American Physiological Society 2019-04-01 2019-02-06 /pmc/articles/PMC6485741/ /pubmed/30726158 http://dx.doi.org/10.1152/jn.00800.2018 Text en Copyright © 2019 the American Physiological Society http://creativecommons.org/licenses/by/4.0/deed.en_US Licensed under Creative Commons Attribution CC-BY 4.0 (http://creativecommons.org/licenses/by/4.0/deed.en_US) : © the American Physiological Society.
spellingShingle Research Article
Davare, Marco
Parikh, Pranav J.
Santello, Marco
Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation
title Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation
title_full Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation
title_fullStr Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation
title_full_unstemmed Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation
title_short Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation
title_sort sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6485741/
https://www.ncbi.nlm.nih.gov/pubmed/30726158
http://dx.doi.org/10.1152/jn.00800.2018
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