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Post-Ischemic Reorganization of Sensory Responses in Cerebral Cortex

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 gener...

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Autores principales: Hayley, P, Tuchek, C, Dalla, S, Borrell, J, Murphy, MD, Nudo, RJ, Guggenmos, DJ
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9882270/
https://www.ncbi.nlm.nih.gov/pubmed/36711682
http://dx.doi.org/10.1101/2023.01.18.524583
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author Hayley, P
Tuchek, C
Dalla, S
Borrell, J
Murphy, MD
Nudo, RJ
Guggenmos, DJ
author_facet Hayley, P
Tuchek, C
Dalla, S
Borrell, J
Murphy, MD
Nudo, RJ
Guggenmos, DJ
author_sort Hayley, P
collection PubMed
description 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. 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. 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 evoked activity in RFA modulated and disrupted the sensory response in sensory cortex, providing additional evidence for the transmission of premotor activity to sensory cortex and the sensitivity of sensory cortex to premotor cortex’s influence. 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-98822702023-01-28 Post-Ischemic Reorganization of Sensory Responses in Cerebral Cortex Hayley, P Tuchek, C Dalla, S Borrell, J Murphy, MD Nudo, RJ Guggenmos, DJ bioRxiv Article 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. 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. 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 evoked activity in RFA modulated and disrupted the sensory response in sensory cortex, providing additional evidence for the transmission of premotor activity to sensory cortex and the sensitivity of sensory cortex to premotor cortex’s influence. 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. Cold Spring Harbor Laboratory 2023-01-20 /pmc/articles/PMC9882270/ /pubmed/36711682 http://dx.doi.org/10.1101/2023.01.18.524583 Text en https://creativecommons.org/licenses/by/4.0/This work is licensed under a Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/) , which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format, so long as attribution is given to the creator. The license allows for commercial use.
spellingShingle Article
Hayley, P
Tuchek, C
Dalla, S
Borrell, J
Murphy, MD
Nudo, RJ
Guggenmos, DJ
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 Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9882270/
https://www.ncbi.nlm.nih.gov/pubmed/36711682
http://dx.doi.org/10.1101/2023.01.18.524583
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