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Rapid and Bihemispheric Reorganization of Neuronal Activity in Premotor Cortex after Brain Injury

Brain injuries cause hemodynamic changes in several distant, spared areas from the lesion. Our objective was to better understand the neuronal correlates of this reorganization in awake, behaving female monkeys. We used reversible inactivation techniques to “injure” the primary motor cortex, while c...

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Autores principales: Moreau-Debord, Ian, Serrano, Éléonore, Quessy, Stephan, Dancause, Numa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8570830/
https://www.ncbi.nlm.nih.gov/pubmed/34556488
http://dx.doi.org/10.1523/JNEUROSCI.0196-21.2021
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author Moreau-Debord, Ian
Serrano, Éléonore
Quessy, Stephan
Dancause, Numa
author_facet Moreau-Debord, Ian
Serrano, Éléonore
Quessy, Stephan
Dancause, Numa
author_sort Moreau-Debord, Ian
collection PubMed
description Brain injuries cause hemodynamic changes in several distant, spared areas from the lesion. Our objective was to better understand the neuronal correlates of this reorganization in awake, behaving female monkeys. We used reversible inactivation techniques to “injure” the primary motor cortex, while continuously recording neuronal activity of the ventral premotor cortex in the two hemispheres, before and after the onset of behavioral impairments. Inactivation rapidly induced profound alterations of neuronal discharges that were heterogeneous within each and across the two hemispheres, occurred during movements of either the affected or nonaffected arm, and varied during different phases of grasping. Our results support that extensive, and much more complex than expected, neuronal reorganization takes place in spared areas of the bihemispheric cortical network involved in the control of hand movements. This broad pattern of reorganization offers potential targets that should be considered for the development of neuromodulation protocols applied early after brain injury. SIGNIFICANCE STATEMENT It is well known that brain injuries cause changes in several distant, spared areas of the network, often in the premotor cortex. This reorganization is greater early after the injury and the magnitude of early changes correlates with impairments. However, studies to date have used noninvasive brain imaging approaches or have been conducted in sedated animals. Therefore, we do not know how brain injuries specifically affect the activity of neurons during the generation of movements. Our study clearly shows how a lesion rapidly impacts neurons in the premotor cortex of both hemispheres. A better understanding of these complex changes can help formulate hypotheses for the development of new treatments that specifically target neuronal reorganization induced by lesions in the brain.
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spelling pubmed-85708302021-11-08 Rapid and Bihemispheric Reorganization of Neuronal Activity in Premotor Cortex after Brain Injury Moreau-Debord, Ian Serrano, Éléonore Quessy, Stephan Dancause, Numa J Neurosci Research Articles Brain injuries cause hemodynamic changes in several distant, spared areas from the lesion. Our objective was to better understand the neuronal correlates of this reorganization in awake, behaving female monkeys. We used reversible inactivation techniques to “injure” the primary motor cortex, while continuously recording neuronal activity of the ventral premotor cortex in the two hemispheres, before and after the onset of behavioral impairments. Inactivation rapidly induced profound alterations of neuronal discharges that were heterogeneous within each and across the two hemispheres, occurred during movements of either the affected or nonaffected arm, and varied during different phases of grasping. Our results support that extensive, and much more complex than expected, neuronal reorganization takes place in spared areas of the bihemispheric cortical network involved in the control of hand movements. This broad pattern of reorganization offers potential targets that should be considered for the development of neuromodulation protocols applied early after brain injury. SIGNIFICANCE STATEMENT It is well known that brain injuries cause changes in several distant, spared areas of the network, often in the premotor cortex. This reorganization is greater early after the injury and the magnitude of early changes correlates with impairments. However, studies to date have used noninvasive brain imaging approaches or have been conducted in sedated animals. Therefore, we do not know how brain injuries specifically affect the activity of neurons during the generation of movements. Our study clearly shows how a lesion rapidly impacts neurons in the premotor cortex of both hemispheres. A better understanding of these complex changes can help formulate hypotheses for the development of new treatments that specifically target neuronal reorganization induced by lesions in the brain. Society for Neuroscience 2021-11-03 /pmc/articles/PMC8570830/ /pubmed/34556488 http://dx.doi.org/10.1523/JNEUROSCI.0196-21.2021 Text en Copyright © 2021 Moreau-Debord 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 Articles
Moreau-Debord, Ian
Serrano, Éléonore
Quessy, Stephan
Dancause, Numa
Rapid and Bihemispheric Reorganization of Neuronal Activity in Premotor Cortex after Brain Injury
title Rapid and Bihemispheric Reorganization of Neuronal Activity in Premotor Cortex after Brain Injury
title_full Rapid and Bihemispheric Reorganization of Neuronal Activity in Premotor Cortex after Brain Injury
title_fullStr Rapid and Bihemispheric Reorganization of Neuronal Activity in Premotor Cortex after Brain Injury
title_full_unstemmed Rapid and Bihemispheric Reorganization of Neuronal Activity in Premotor Cortex after Brain Injury
title_short Rapid and Bihemispheric Reorganization of Neuronal Activity in Premotor Cortex after Brain Injury
title_sort rapid and bihemispheric reorganization of neuronal activity in premotor cortex after brain injury
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8570830/
https://www.ncbi.nlm.nih.gov/pubmed/34556488
http://dx.doi.org/10.1523/JNEUROSCI.0196-21.2021
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