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Intrinsic somatosensory feedback supports motor control and learning to operate artificial body parts

Objective. Considerable resources are being invested to enhance the control and usability of artificial limbs through the delivery of unnatural forms of somatosensory feedback. Here, we investigated whether intrinsic somatosensory information from the body part(s) remotely controlling an artificial...

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Autores principales: Amoruso, E, Dowdall, L, Kollamkulam, M T, Ukaegbu, O, Kieliba, P, Ng, T, Dempsey-Jones, H, Clode, D, Makin, T R
Formato: Online Artículo Texto
Lenguaje:English
Publicado: IOP Publishing 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10431236/
https://www.ncbi.nlm.nih.gov/pubmed/34983040
http://dx.doi.org/10.1088/1741-2552/ac47d9
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author Amoruso, E
Dowdall, L
Kollamkulam, M T
Ukaegbu, O
Kieliba, P
Ng, T
Dempsey-Jones, H
Clode, D
Makin, T R
author_facet Amoruso, E
Dowdall, L
Kollamkulam, M T
Ukaegbu, O
Kieliba, P
Ng, T
Dempsey-Jones, H
Clode, D
Makin, T R
author_sort Amoruso, E
collection PubMed
description Objective. Considerable resources are being invested to enhance the control and usability of artificial limbs through the delivery of unnatural forms of somatosensory feedback. Here, we investigated whether intrinsic somatosensory information from the body part(s) remotely controlling an artificial limb can be leveraged by the motor system to support control and skill learning. Approach. We used local anaesthetic to attenuate somatosensory inputs to the big toes while participants learned to operate through pressure sensors a toe-controlled and hand-worn robotic extra finger. Motor learning outcomes were compared against a control group who received sham anaesthetic and quantified in three different task scenarios: while operating in isolation from, in synchronous coordination, and collaboration with, the biological fingers. Main results. Both groups were able to learn to operate the robotic extra finger, presumably due to abundance of visual feedback and other relevant sensory cues. Importantly, the availability of displaced somatosensory cues from the distal bodily controllers facilitated the acquisition of isolated robotic finger movements, the retention and transfer of synchronous hand-robot coordination skills, and performance under cognitive load. Motor performance was not impaired by toes anaesthesia when tasks involved close collaboration with the biological fingers, indicating that the motor system can close the sensory feedback gap by dynamically integrating task-intrinsic somatosensory signals from multiple, and even distal, body-parts. Significance. Together, our findings demonstrate that there are multiple natural avenues to provide intrinsic surrogate somatosensory information to support motor control of an artificial body part, beyond artificial stimulation.
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spelling pubmed-104312362023-08-17 Intrinsic somatosensory feedback supports motor control and learning to operate artificial body parts Amoruso, E Dowdall, L Kollamkulam, M T Ukaegbu, O Kieliba, P Ng, T Dempsey-Jones, H Clode, D Makin, T R J Neural Eng Paper Objective. Considerable resources are being invested to enhance the control and usability of artificial limbs through the delivery of unnatural forms of somatosensory feedback. Here, we investigated whether intrinsic somatosensory information from the body part(s) remotely controlling an artificial limb can be leveraged by the motor system to support control and skill learning. Approach. We used local anaesthetic to attenuate somatosensory inputs to the big toes while participants learned to operate through pressure sensors a toe-controlled and hand-worn robotic extra finger. Motor learning outcomes were compared against a control group who received sham anaesthetic and quantified in three different task scenarios: while operating in isolation from, in synchronous coordination, and collaboration with, the biological fingers. Main results. Both groups were able to learn to operate the robotic extra finger, presumably due to abundance of visual feedback and other relevant sensory cues. Importantly, the availability of displaced somatosensory cues from the distal bodily controllers facilitated the acquisition of isolated robotic finger movements, the retention and transfer of synchronous hand-robot coordination skills, and performance under cognitive load. Motor performance was not impaired by toes anaesthesia when tasks involved close collaboration with the biological fingers, indicating that the motor system can close the sensory feedback gap by dynamically integrating task-intrinsic somatosensory signals from multiple, and even distal, body-parts. Significance. Together, our findings demonstrate that there are multiple natural avenues to provide intrinsic surrogate somatosensory information to support motor control of an artificial body part, beyond artificial stimulation. IOP Publishing 2022-02-01 2022-01-24 /pmc/articles/PMC10431236/ /pubmed/34983040 http://dx.doi.org/10.1088/1741-2552/ac47d9 Text en © 2022 The Author(s). Published by IOP Publishing Ltd https://creativecommons.org/licenses/by/4.0/ Original content from this work may be used under the terms of the Creative Commons Attribution 4.0 license (https://creativecommons.org/licenses/by/4.0/) . Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.
spellingShingle Paper
Amoruso, E
Dowdall, L
Kollamkulam, M T
Ukaegbu, O
Kieliba, P
Ng, T
Dempsey-Jones, H
Clode, D
Makin, T R
Intrinsic somatosensory feedback supports motor control and learning to operate artificial body parts
title Intrinsic somatosensory feedback supports motor control and learning to operate artificial body parts
title_full Intrinsic somatosensory feedback supports motor control and learning to operate artificial body parts
title_fullStr Intrinsic somatosensory feedback supports motor control and learning to operate artificial body parts
title_full_unstemmed Intrinsic somatosensory feedback supports motor control and learning to operate artificial body parts
title_short Intrinsic somatosensory feedback supports motor control and learning to operate artificial body parts
title_sort intrinsic somatosensory feedback supports motor control and learning to operate artificial body parts
topic Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10431236/
https://www.ncbi.nlm.nih.gov/pubmed/34983040
http://dx.doi.org/10.1088/1741-2552/ac47d9
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