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Cortical reorganization of lower-limb motor representations in an elite archery athlete with congenital amputation of both arms

Despite their disabilities, top Paralympic athletes have better motor skills than able-bodied athletes. However, the neural underpinnings of these better motor skills remain unclear. We investigated the reorganization of the primary motor cortex (M1) in a Paralympic athlete with congenital amputatio...

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Autores principales: Nakagawa, Kento, Takemi, Mitsuaki, Nakanishi, Tomoya, Sasaki, Atsushi, Nakazawa, Kimitaka
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6970184/
https://www.ncbi.nlm.nih.gov/pubmed/31958685
http://dx.doi.org/10.1016/j.nicl.2019.102144
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author Nakagawa, Kento
Takemi, Mitsuaki
Nakanishi, Tomoya
Sasaki, Atsushi
Nakazawa, Kimitaka
author_facet Nakagawa, Kento
Takemi, Mitsuaki
Nakanishi, Tomoya
Sasaki, Atsushi
Nakazawa, Kimitaka
author_sort Nakagawa, Kento
collection PubMed
description Despite their disabilities, top Paralympic athletes have better motor skills than able-bodied athletes. However, the neural underpinnings of these better motor skills remain unclear. We investigated the reorganization of the primary motor cortex (M1) in a Paralympic athlete with congenital amputation of both arms who holds the world record for the farthest accurate shot in archery (Amputee Archer: AA). We recorded brain activity during contraction of right toe, ankle, knee, and hip joint muscles in the AA and 12 able-bodied control subjects using functional magnetic resonance imaging. The results revealed that M1 activation was more widespread in the AA compared with control subjects during all tasks, and shifted towards the lateral part of the M1 during contraction of toe and knee muscles. We also conducted a motor mapping experiment using navigated transcranial magnetic stimulation. The M1 area receiving stimulation elicited motor-evoked potentials from the toe, lower-leg, and thigh muscles, which were larger in the AA compared with 12 control subjects. Furthermore, the AA's motor maps were shifted towards the lateral side of M1. These results suggest an expansion of lower-limb M1 representation towards the lateral side of M1, including the trunk and upper-limb representations, and an expansion of the area of corticomotor neurons innervating the lower limb muscles in the AA. This unique M1 reorganization could underpin the AA's excellent archery performance in the absence of upper limbs. The current results suggest that Paralympic athletes may exhibit extreme M1 plasticity, which could arise through a combination of rigorous long-term motor training and compensatory M1 reorganization for missing body parts.
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spelling pubmed-69701842020-01-27 Cortical reorganization of lower-limb motor representations in an elite archery athlete with congenital amputation of both arms Nakagawa, Kento Takemi, Mitsuaki Nakanishi, Tomoya Sasaki, Atsushi Nakazawa, Kimitaka Neuroimage Clin Regular Article Despite their disabilities, top Paralympic athletes have better motor skills than able-bodied athletes. However, the neural underpinnings of these better motor skills remain unclear. We investigated the reorganization of the primary motor cortex (M1) in a Paralympic athlete with congenital amputation of both arms who holds the world record for the farthest accurate shot in archery (Amputee Archer: AA). We recorded brain activity during contraction of right toe, ankle, knee, and hip joint muscles in the AA and 12 able-bodied control subjects using functional magnetic resonance imaging. The results revealed that M1 activation was more widespread in the AA compared with control subjects during all tasks, and shifted towards the lateral part of the M1 during contraction of toe and knee muscles. We also conducted a motor mapping experiment using navigated transcranial magnetic stimulation. The M1 area receiving stimulation elicited motor-evoked potentials from the toe, lower-leg, and thigh muscles, which were larger in the AA compared with 12 control subjects. Furthermore, the AA's motor maps were shifted towards the lateral side of M1. These results suggest an expansion of lower-limb M1 representation towards the lateral side of M1, including the trunk and upper-limb representations, and an expansion of the area of corticomotor neurons innervating the lower limb muscles in the AA. This unique M1 reorganization could underpin the AA's excellent archery performance in the absence of upper limbs. The current results suggest that Paralympic athletes may exhibit extreme M1 plasticity, which could arise through a combination of rigorous long-term motor training and compensatory M1 reorganization for missing body parts. Elsevier 2019-12-24 /pmc/articles/PMC6970184/ /pubmed/31958685 http://dx.doi.org/10.1016/j.nicl.2019.102144 Text en © 2020 The Authors http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Regular Article
Nakagawa, Kento
Takemi, Mitsuaki
Nakanishi, Tomoya
Sasaki, Atsushi
Nakazawa, Kimitaka
Cortical reorganization of lower-limb motor representations in an elite archery athlete with congenital amputation of both arms
title Cortical reorganization of lower-limb motor representations in an elite archery athlete with congenital amputation of both arms
title_full Cortical reorganization of lower-limb motor representations in an elite archery athlete with congenital amputation of both arms
title_fullStr Cortical reorganization of lower-limb motor representations in an elite archery athlete with congenital amputation of both arms
title_full_unstemmed Cortical reorganization of lower-limb motor representations in an elite archery athlete with congenital amputation of both arms
title_short Cortical reorganization of lower-limb motor representations in an elite archery athlete with congenital amputation of both arms
title_sort cortical reorganization of lower-limb motor representations in an elite archery athlete with congenital amputation of both arms
topic Regular Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6970184/
https://www.ncbi.nlm.nih.gov/pubmed/31958685
http://dx.doi.org/10.1016/j.nicl.2019.102144
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