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Interlimb Transfer of Reach Adaptation Does Not Require an Intact Corpus Callosum: Evidence from Patients with Callosal Lesions and Agenesis

Generalization of sensorimotor adaptation across limbs, known as interlimb transfer, is a well-demonstrated phenomenon in humans, yet the underlying neural mechanisms remain unclear. Theoretical models suggest that interlimb transfer is mediated by interhemispheric transfer of information via the co...

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Autores principales: Tilsley, Penelope A., Romaiguère, Patricia, Tramoni, Eve, Felician, Olivier, Sarlegna, Fabrice R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8318344/
https://www.ncbi.nlm.nih.gov/pubmed/33632816
http://dx.doi.org/10.1523/ENEURO.0190-20.2021
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author Tilsley, Penelope A.
Romaiguère, Patricia
Tramoni, Eve
Felician, Olivier
Sarlegna, Fabrice R.
author_facet Tilsley, Penelope A.
Romaiguère, Patricia
Tramoni, Eve
Felician, Olivier
Sarlegna, Fabrice R.
author_sort Tilsley, Penelope A.
collection PubMed
description Generalization of sensorimotor adaptation across limbs, known as interlimb transfer, is a well-demonstrated phenomenon in humans, yet the underlying neural mechanisms remain unclear. Theoretical models suggest that interlimb transfer is mediated by interhemispheric transfer of information via the corpus callosum. We thus hypothesized that lesions of the corpus callosum, especially to its midbody connecting motor, supplementary motor, and premotor areas of the two cerebral hemispheres, would impair interlimb transfer of sensorimotor adaptation. To test this hypothesis, we recruited three patients: two rare stroke patients with recent, extensive callosal lesions including the midbody and one patient with complete agenesis. A prismatic adaptation paradigm involving unconstrained arm reaching movements was designed to assess interlimb transfer from the prism-exposed dominant arm (DA) to the unexposed non-dominant arm (NDA) for each participant. Baseline results showed that spatial performance of each patient did not significantly differ from controls, for both limbs. Further, each patient adapted to the prismatic perturbation, with no significant difference in error reduction compared with controls. Crucially, interlimb transfer was found in each patient. The absolute magnitude of each patient’s transfer did not significantly differ from controls. These findings show that sensorimotor adaptation can transfer across limbs despite extensive lesions or complete absence of the corpus callosum. Therefore, callosal pathways connecting homologous motor, premotor, and supplementary motor areas are not necessary for interlimb transfer of prismatic reach adaptation. Such interlimb transfer could be mediated by transcallosal splenium pathways (connecting parietal, temporal and visual areas), ipsilateral cortico-spinal pathways or subcortical structures such as the cerebellum.
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spelling pubmed-83183442021-07-29 Interlimb Transfer of Reach Adaptation Does Not Require an Intact Corpus Callosum: Evidence from Patients with Callosal Lesions and Agenesis Tilsley, Penelope A. Romaiguère, Patricia Tramoni, Eve Felician, Olivier Sarlegna, Fabrice R. eNeuro Research Article: New Research Generalization of sensorimotor adaptation across limbs, known as interlimb transfer, is a well-demonstrated phenomenon in humans, yet the underlying neural mechanisms remain unclear. Theoretical models suggest that interlimb transfer is mediated by interhemispheric transfer of information via the corpus callosum. We thus hypothesized that lesions of the corpus callosum, especially to its midbody connecting motor, supplementary motor, and premotor areas of the two cerebral hemispheres, would impair interlimb transfer of sensorimotor adaptation. To test this hypothesis, we recruited three patients: two rare stroke patients with recent, extensive callosal lesions including the midbody and one patient with complete agenesis. A prismatic adaptation paradigm involving unconstrained arm reaching movements was designed to assess interlimb transfer from the prism-exposed dominant arm (DA) to the unexposed non-dominant arm (NDA) for each participant. Baseline results showed that spatial performance of each patient did not significantly differ from controls, for both limbs. Further, each patient adapted to the prismatic perturbation, with no significant difference in error reduction compared with controls. Crucially, interlimb transfer was found in each patient. The absolute magnitude of each patient’s transfer did not significantly differ from controls. These findings show that sensorimotor adaptation can transfer across limbs despite extensive lesions or complete absence of the corpus callosum. Therefore, callosal pathways connecting homologous motor, premotor, and supplementary motor areas are not necessary for interlimb transfer of prismatic reach adaptation. Such interlimb transfer could be mediated by transcallosal splenium pathways (connecting parietal, temporal and visual areas), ipsilateral cortico-spinal pathways or subcortical structures such as the cerebellum. Society for Neuroscience 2021-07-26 /pmc/articles/PMC8318344/ /pubmed/33632816 http://dx.doi.org/10.1523/ENEURO.0190-20.2021 Text en Copyright © 2021 Tilsley et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article: New Research
Tilsley, Penelope A.
Romaiguère, Patricia
Tramoni, Eve
Felician, Olivier
Sarlegna, Fabrice R.
Interlimb Transfer of Reach Adaptation Does Not Require an Intact Corpus Callosum: Evidence from Patients with Callosal Lesions and Agenesis
title Interlimb Transfer of Reach Adaptation Does Not Require an Intact Corpus Callosum: Evidence from Patients with Callosal Lesions and Agenesis
title_full Interlimb Transfer of Reach Adaptation Does Not Require an Intact Corpus Callosum: Evidence from Patients with Callosal Lesions and Agenesis
title_fullStr Interlimb Transfer of Reach Adaptation Does Not Require an Intact Corpus Callosum: Evidence from Patients with Callosal Lesions and Agenesis
title_full_unstemmed Interlimb Transfer of Reach Adaptation Does Not Require an Intact Corpus Callosum: Evidence from Patients with Callosal Lesions and Agenesis
title_short Interlimb Transfer of Reach Adaptation Does Not Require an Intact Corpus Callosum: Evidence from Patients with Callosal Lesions and Agenesis
title_sort interlimb transfer of reach adaptation does not require an intact corpus callosum: evidence from patients with callosal lesions and agenesis
topic Research Article: New Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8318344/
https://www.ncbi.nlm.nih.gov/pubmed/33632816
http://dx.doi.org/10.1523/ENEURO.0190-20.2021
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