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Distinct neural components of visually guided grasping during planning and execution

Distinct neural components of visually guided grasping during planning and execution
Distinct neural components of visually guided grasping during planning and execution

Selecting suitable grasps on three-dimensional objects is a challenging visuomotor 3 computation, which involves combining information about an object (e.g., its shape, 4 size, and mass) with information about the actor’s body (e.g., the optimal grasp 5 aperture and hand posture for comfortable manipulation). Here we used functional 6 magnetic resonance imaging to investigate brain networks associated with these 7 distinct aspects during grasp planning and execution. Human participants 8 of either sex viewed and then executed preselected grasps on L-shaped objects 9 made of wood and/or brass. By leveraging a computational approach that accurately 10 predicts human grasp locations, we selected grasp points that disentangled the role 11 of multiple grasp-relevant factors: grasp axis, grasp size, and object mass. 12 Representational Similarity Analysis revealed that grasp axis was encoded along 13 dorsal-stream regions during grasp planning. Grasp size was first encoded in 14 ventral-stream areas during grasp planning, then in premotor regions during grasp 15 execution. Object mass was encoded in ventral-stream and (pre)motor regions only 16 during grasp execution. Premotor regions further encoded visual predictions of grasp 17 comfort, whereas the ventral stream encoded grasp comfort during execution, 18 suggesting its involvement in haptic evaluation. These shifts in neural 19 representations thus capture the sensorimotor transformations that allow humans to 20 grasp objects.

0270-6474
8504-8514
Klein, Lina K.
647f7604-4630-4cf1-9ae4-c0b84d28e97e
Maiello, Guido
c122b089-1bbc-4d3e-b178-b0a1b31a5295
Stubbs, Kevin
cfae5785-4317-4136-bc8c-e442d9206b9f
Proklova, Daria
7e496e25-a65c-412c-b68d-9298bd635ada
Chen, Juan
7587df42-e115-4f99-9639-eaf97d29d983
Paulun, Vivian C.
1f6ebb55-bae1-4c6b-87ba-46d2e2313b8e
Culham, Jody C.
540f9ada-1544-4fdc-8b86-600cf4abc445
Fleming, Roland W.
f9a60356-03e6-4931-a332-f3a7aa9f9915
Klein, Lina K.
647f7604-4630-4cf1-9ae4-c0b84d28e97e
Maiello, Guido
c122b089-1bbc-4d3e-b178-b0a1b31a5295
Stubbs, Kevin
cfae5785-4317-4136-bc8c-e442d9206b9f
Proklova, Daria
7e496e25-a65c-412c-b68d-9298bd635ada
Chen, Juan
7587df42-e115-4f99-9639-eaf97d29d983
Paulun, Vivian C.
1f6ebb55-bae1-4c6b-87ba-46d2e2313b8e
Culham, Jody C.
540f9ada-1544-4fdc-8b86-600cf4abc445
Fleming, Roland W.
f9a60356-03e6-4931-a332-f3a7aa9f9915

Klein, Lina K., Maiello, Guido, Stubbs, Kevin, Proklova, Daria, Chen, Juan, Paulun, Vivian C., Culham, Jody C. and Fleming, Roland W. (2023) Distinct neural components of visually guided grasping during planning and execution. Journal of Neuroscience, 43 (49), 8504-8514. (doi:10.1523/JNEUROSCI.0335-23.2023).

Record type: Article

Abstract

Selecting suitable grasps on three-dimensional objects is a challenging visuomotor 3 computation, which involves combining information about an object (e.g., its shape, 4 size, and mass) with information about the actor’s body (e.g., the optimal grasp 5 aperture and hand posture for comfortable manipulation). Here we used functional 6 magnetic resonance imaging to investigate brain networks associated with these 7 distinct aspects during grasp planning and execution. Human participants 8 of either sex viewed and then executed preselected grasps on L-shaped objects 9 made of wood and/or brass. By leveraging a computational approach that accurately 10 predicts human grasp locations, we selected grasp points that disentangled the role 11 of multiple grasp-relevant factors: grasp axis, grasp size, and object mass. 12 Representational Similarity Analysis revealed that grasp axis was encoded along 13 dorsal-stream regions during grasp planning. Grasp size was first encoded in 14 ventral-stream areas during grasp planning, then in premotor regions during grasp 15 execution. Object mass was encoded in ventral-stream and (pre)motor regions only 16 during grasp execution. Premotor regions further encoded visual predictions of grasp 17 comfort, whereas the ventral stream encoded grasp comfort during execution, 18 suggesting its involvement in haptic evaluation. These shifts in neural 19 representations thus capture the sensorimotor transformations that allow humans to 20 grasp objects.

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Accepted/In Press date: 6 September 2023
e-pub ahead of print date: 17 October 2023
Published date: 6 December 2023

Identifiers

Local EPrints ID: 490205
URI: http://eprints.soton.ac.uk/id/eprint/490205
ISSN: 0270-6474
PURE UUID: 6c189b42-b60c-4012-93e4-322000455af7
ORCID for Guido Maiello: ORCID iD orcid.org/0000-0001-6625-2583

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Date deposited: 20 May 2024 16:30
Last modified: 06 Jun 2024 02:17

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Contributors

Author: Lina K. Klein
Author: Guido Maiello ORCID iD
Author: Kevin Stubbs
Author: Daria Proklova
Author: Juan Chen
Author: Vivian C. Paulun
Author: Jody C. Culham
Author: Roland W. Fleming

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