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Post-ischemic reorganization of sensory responses in cerebral cortex

INTRODUCTION: Sensorimotor integration is critical for generating skilled, volitional movements. While stroke tends to impact motor function, there are also often associated sensory deficits that contribute to overall behavioral deficits. Because many of the cortico-cortical projections participatin...

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Autores principales: Hayley, P., Tuchek, C., Dalla, S., Borrell, J., Murphy, M. D., Nudo, R. J., Guggenmos, D. J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10272353/
https://www.ncbi.nlm.nih.gov/pubmed/37332854
http://dx.doi.org/10.3389/fnins.2023.1151309
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author Hayley, P.
Tuchek, C.
Dalla, S.
Borrell, J.
Murphy, M. D.
Nudo, R. J.
Guggenmos, D. J.
author_facet Hayley, P.
Tuchek, C.
Dalla, S.
Borrell, J.
Murphy, M. D.
Nudo, R. J.
Guggenmos, D. J.
author_sort Hayley, P.
collection PubMed
description INTRODUCTION: Sensorimotor integration is critical for generating skilled, volitional movements. While stroke tends to impact motor function, there are also often associated sensory deficits that contribute to overall behavioral deficits. Because many of the cortico-cortical projections participating in the generation of volitional movement either target or pass-through primary motor cortex (in rats, caudal forelimb area; CFA), any damage to CFA can lead to a subsequent disruption in information flow. As a result, the loss of sensory feedback is thought to contribute to motor dysfunction even when sensory areas are spared from injury. Previous research has suggested that the restoration of sensorimotor integration through reorganization or de novo neuronal connections is important for restoring function. Our goal was to determine if there was crosstalk between sensorimotor cortical areas with recovery from a primary motor cortex injury. First, we investigated if peripheral sensory stimulation would evoke responses in the rostral forelimb area (RFA), a rodent homologue to premotor cortex. We then sought to identify whether intracortical microstimulation-evoked activity in RFA would reciprocally modify the sensory response. METHODS: We used seven rats with an ischemic lesion of CFA. Four weeks after injury, the rats’ forepaw was mechanically stimulated under anesthesia and neural activity was recorded in the cortex. In a subset of trials, a small intracortical stimulation pulse was delivered in RFA either individually or paired with peripheral sensory stimulation. RESULTS: Our results point to post-ischemic connectivity between premotor and sensory cortex that may be related to functional recovery. Premotor recruitment during the sensory response was seen with a peak in spiking within RFA after the peripheral solenoid stimulation despite the damage to CFA. Furthermore, stimulation in RFA modulated and disrupted the sensory response in sensory cortex. DISCUSSION: The presence of a sensory response in RFA and the sensitivity of S1 to modulation by intracortical stimulation provides additional evidence for functional connectivity between premotor and somatosensory cortex. The strength of the modulatory effect may be related to the extent of the injury and the subsequent reshaping of cortical connections in response to network disruption.
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spelling pubmed-102723532023-06-17 Post-ischemic reorganization of sensory responses in cerebral cortex Hayley, P. Tuchek, C. Dalla, S. Borrell, J. Murphy, M. D. Nudo, R. J. Guggenmos, D. J. Front Neurosci Neuroscience INTRODUCTION: Sensorimotor integration is critical for generating skilled, volitional movements. While stroke tends to impact motor function, there are also often associated sensory deficits that contribute to overall behavioral deficits. Because many of the cortico-cortical projections participating in the generation of volitional movement either target or pass-through primary motor cortex (in rats, caudal forelimb area; CFA), any damage to CFA can lead to a subsequent disruption in information flow. As a result, the loss of sensory feedback is thought to contribute to motor dysfunction even when sensory areas are spared from injury. Previous research has suggested that the restoration of sensorimotor integration through reorganization or de novo neuronal connections is important for restoring function. Our goal was to determine if there was crosstalk between sensorimotor cortical areas with recovery from a primary motor cortex injury. First, we investigated if peripheral sensory stimulation would evoke responses in the rostral forelimb area (RFA), a rodent homologue to premotor cortex. We then sought to identify whether intracortical microstimulation-evoked activity in RFA would reciprocally modify the sensory response. METHODS: We used seven rats with an ischemic lesion of CFA. Four weeks after injury, the rats’ forepaw was mechanically stimulated under anesthesia and neural activity was recorded in the cortex. In a subset of trials, a small intracortical stimulation pulse was delivered in RFA either individually or paired with peripheral sensory stimulation. RESULTS: Our results point to post-ischemic connectivity between premotor and sensory cortex that may be related to functional recovery. Premotor recruitment during the sensory response was seen with a peak in spiking within RFA after the peripheral solenoid stimulation despite the damage to CFA. Furthermore, stimulation in RFA modulated and disrupted the sensory response in sensory cortex. DISCUSSION: The presence of a sensory response in RFA and the sensitivity of S1 to modulation by intracortical stimulation provides additional evidence for functional connectivity between premotor and somatosensory cortex. The strength of the modulatory effect may be related to the extent of the injury and the subsequent reshaping of cortical connections in response to network disruption. Frontiers Media S.A. 2023-06-02 /pmc/articles/PMC10272353/ /pubmed/37332854 http://dx.doi.org/10.3389/fnins.2023.1151309 Text en Copyright © 2023 Hayley, Tuchek, Dalla, Borrell, Murphy, Nudo and Guggenmos. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Hayley, P.
Tuchek, C.
Dalla, S.
Borrell, J.
Murphy, M. D.
Nudo, R. J.
Guggenmos, D. J.
Post-ischemic reorganization of sensory responses in cerebral cortex
title Post-ischemic reorganization of sensory responses in cerebral cortex
title_full Post-ischemic reorganization of sensory responses in cerebral cortex
title_fullStr Post-ischemic reorganization of sensory responses in cerebral cortex
title_full_unstemmed Post-ischemic reorganization of sensory responses in cerebral cortex
title_short Post-ischemic reorganization of sensory responses in cerebral cortex
title_sort post-ischemic reorganization of sensory responses in cerebral cortex
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10272353/
https://www.ncbi.nlm.nih.gov/pubmed/37332854
http://dx.doi.org/10.3389/fnins.2023.1151309
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