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Visual information following object grasp supports digit position variability and swift anticipatory force control

Anticipatory force control underlying dexterous manipulation has historically been understood to rely on visual object properties and on sensorimotor memories associated with previous experiences with similar objects. However, it is becoming increasingly recognized that anticipatory force control al...

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Detalles Bibliográficos
Autores principales: Bland, Joshua T., Davare, Marco, Marneweck, Michelle
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Physiological Society 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10259848/
https://www.ncbi.nlm.nih.gov/pubmed/37162174
http://dx.doi.org/10.1152/jn.00104.2023
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author Bland, Joshua T.
Davare, Marco
Marneweck, Michelle
author_facet Bland, Joshua T.
Davare, Marco
Marneweck, Michelle
author_sort Bland, Joshua T.
collection PubMed
description Anticipatory force control underlying dexterous manipulation has historically been understood to rely on visual object properties and on sensorimotor memories associated with previous experiences with similar objects. However, it is becoming increasingly recognized that anticipatory force control also relies on how an object is grasped. Experiments that allow unconstrained grasp contact points when preventing tilting an object with an off-centered mass show trial-to-trial variations in digit position and subsequent scaling of lift forces, all before feedback of object properties becomes available. Here, we manipulated the availability of visual information before reach onset and after grasp contact (with no vision during the reach) to determine the contribution and timing of visual information processing to the scaling of fingertip forces during dexterous manipulation at flexible contact points. Results showed that anticipatory force control was similarly successful, quantified as an appropriate compensatory torque at lift onset that counters the external torque of an object with a left and right center of mass, irrespective of the timing and availability of visual information. However, the way in which anticipatory force control was achieved varied depending on the availability of visual information. Visual information following grasp contact was associated with greater use of an asymmetric thumb and index finger grasp configuration to generate a compensatory torque and digit position variability, together with faster fingertip force scaling and sensorimotor learning. This result supports the hypothesis that visual information at a critical and functionally relevant time point following grasp contact supports variable and swift digit-based force control for dexterous object manipulation. NEW & NOTEWORTHY Humans excel in dexterous object manipulation by precisely coordinating grasp points and fingertip forces, highlighted in scenarios requiring countering object torques in advance, e.g., lifting a teacup without spilling will demand a unique digit force pattern based on the grip configuration at lift onset. Here, we show that visual information following grasp contact, a critical and functionally relevant time point, supports digit position variability and swift anticipatory force control to achieve a dexterous motor goal.
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spelling pubmed-102598482023-06-13 Visual information following object grasp supports digit position variability and swift anticipatory force control Bland, Joshua T. Davare, Marco Marneweck, Michelle J Neurophysiol Research Article Anticipatory force control underlying dexterous manipulation has historically been understood to rely on visual object properties and on sensorimotor memories associated with previous experiences with similar objects. However, it is becoming increasingly recognized that anticipatory force control also relies on how an object is grasped. Experiments that allow unconstrained grasp contact points when preventing tilting an object with an off-centered mass show trial-to-trial variations in digit position and subsequent scaling of lift forces, all before feedback of object properties becomes available. Here, we manipulated the availability of visual information before reach onset and after grasp contact (with no vision during the reach) to determine the contribution and timing of visual information processing to the scaling of fingertip forces during dexterous manipulation at flexible contact points. Results showed that anticipatory force control was similarly successful, quantified as an appropriate compensatory torque at lift onset that counters the external torque of an object with a left and right center of mass, irrespective of the timing and availability of visual information. However, the way in which anticipatory force control was achieved varied depending on the availability of visual information. Visual information following grasp contact was associated with greater use of an asymmetric thumb and index finger grasp configuration to generate a compensatory torque and digit position variability, together with faster fingertip force scaling and sensorimotor learning. This result supports the hypothesis that visual information at a critical and functionally relevant time point following grasp contact supports variable and swift digit-based force control for dexterous object manipulation. NEW & NOTEWORTHY Humans excel in dexterous object manipulation by precisely coordinating grasp points and fingertip forces, highlighted in scenarios requiring countering object torques in advance, e.g., lifting a teacup without spilling will demand a unique digit force pattern based on the grip configuration at lift onset. Here, we show that visual information following grasp contact, a critical and functionally relevant time point, supports digit position variability and swift anticipatory force control to achieve a dexterous motor goal. American Physiological Society 2023-06-01 2023-05-10 /pmc/articles/PMC10259848/ /pubmed/37162174 http://dx.doi.org/10.1152/jn.00104.2023 Text en Copyright © 2023 The Authors. https://creativecommons.org/licenses/by/4.0/Licensed under Creative Commons Attribution CC-BY 4.0 (https://creativecommons.org/licenses/by/4.0/) . Published by the American Physiological Society.
spellingShingle Research Article
Bland, Joshua T.
Davare, Marco
Marneweck, Michelle
Visual information following object grasp supports digit position variability and swift anticipatory force control
title Visual information following object grasp supports digit position variability and swift anticipatory force control
title_full Visual information following object grasp supports digit position variability and swift anticipatory force control
title_fullStr Visual information following object grasp supports digit position variability and swift anticipatory force control
title_full_unstemmed Visual information following object grasp supports digit position variability and swift anticipatory force control
title_short Visual information following object grasp supports digit position variability and swift anticipatory force control
title_sort visual information following object grasp supports digit position variability and swift anticipatory force control
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10259848/
https://www.ncbi.nlm.nih.gov/pubmed/37162174
http://dx.doi.org/10.1152/jn.00104.2023
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