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Dexterous Object Manipulation Requires Context-Dependent Sensorimotor Cortical Interactions in Humans

Dexterous object manipulation is a hallmark of human evolution and a critical skill for everyday activities. A previous work has used a grasping context that predominantly elicits memory-based control of digit forces by constraining where the object should be grasped. For this “constrained” grasping...

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Autores principales: Parikh, Pranav J, Fine, Justin M, Santello, Marco
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7197080/
https://www.ncbi.nlm.nih.gov/pubmed/31845726
http://dx.doi.org/10.1093/cercor/bhz296
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author Parikh, Pranav J
Fine, Justin M
Santello, Marco
author_facet Parikh, Pranav J
Fine, Justin M
Santello, Marco
author_sort Parikh, Pranav J
collection PubMed
description Dexterous object manipulation is a hallmark of human evolution and a critical skill for everyday activities. A previous work has used a grasping context that predominantly elicits memory-based control of digit forces by constraining where the object should be grasped. For this “constrained” grasping context, the primary motor cortex (M1) is involved in storage and retrieval of digit forces used in previous manipulations. In contrast, when choice of digit contact points is allowed (“unconstrained” grasping), behavioral studies revealed that forces are adjusted, on a trial-to-trial basis, as a function of digit position. This suggests a role of online feedback of digit position for force control. However, despite the ubiquitous nature of unconstrained hand–object interactions in activities of daily living, the underlying neural mechanisms are unknown. Using noninvasive brain stimulation, we found the role of primary motor cortex (M1) and somatosensory cortex (S1) to be sensitive to grasping context. In constrained grasping, M1 but not S1 is involved in storing and retrieving learned digit forces and position. In contrast, in unconstrained grasping, M1 and S1 are involved in modulating digit forces to position. Our findings suggest that the relative contribution of memory and online feedback modulates sensorimotor cortical interactions for dexterous manipulation.
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spelling pubmed-71970802020-05-07 Dexterous Object Manipulation Requires Context-Dependent Sensorimotor Cortical Interactions in Humans Parikh, Pranav J Fine, Justin M Santello, Marco Cereb Cortex Original Article Dexterous object manipulation is a hallmark of human evolution and a critical skill for everyday activities. A previous work has used a grasping context that predominantly elicits memory-based control of digit forces by constraining where the object should be grasped. For this “constrained” grasping context, the primary motor cortex (M1) is involved in storage and retrieval of digit forces used in previous manipulations. In contrast, when choice of digit contact points is allowed (“unconstrained” grasping), behavioral studies revealed that forces are adjusted, on a trial-to-trial basis, as a function of digit position. This suggests a role of online feedback of digit position for force control. However, despite the ubiquitous nature of unconstrained hand–object interactions in activities of daily living, the underlying neural mechanisms are unknown. Using noninvasive brain stimulation, we found the role of primary motor cortex (M1) and somatosensory cortex (S1) to be sensitive to grasping context. In constrained grasping, M1 but not S1 is involved in storing and retrieving learned digit forces and position. In contrast, in unconstrained grasping, M1 and S1 are involved in modulating digit forces to position. Our findings suggest that the relative contribution of memory and online feedback modulates sensorimotor cortical interactions for dexterous manipulation. Oxford University Press 2020-05 2019-12-14 /pmc/articles/PMC7197080/ /pubmed/31845726 http://dx.doi.org/10.1093/cercor/bhz296 Text en © The Author(s) 2019. Published by Oxford University Press. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Original Article
Parikh, Pranav J
Fine, Justin M
Santello, Marco
Dexterous Object Manipulation Requires Context-Dependent Sensorimotor Cortical Interactions in Humans
title Dexterous Object Manipulation Requires Context-Dependent Sensorimotor Cortical Interactions in Humans
title_full Dexterous Object Manipulation Requires Context-Dependent Sensorimotor Cortical Interactions in Humans
title_fullStr Dexterous Object Manipulation Requires Context-Dependent Sensorimotor Cortical Interactions in Humans
title_full_unstemmed Dexterous Object Manipulation Requires Context-Dependent Sensorimotor Cortical Interactions in Humans
title_short Dexterous Object Manipulation Requires Context-Dependent Sensorimotor Cortical Interactions in Humans
title_sort dexterous object manipulation requires context-dependent sensorimotor cortical interactions in humans
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7197080/
https://www.ncbi.nlm.nih.gov/pubmed/31845726
http://dx.doi.org/10.1093/cercor/bhz296
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