Compensatory adaptation of parallel motor pathways promotes skilled forelimb recovery after spinal cord injury

Summary: Skilled forelimb patterning is regulated by the corticospinal tract (CST) with support from brainstem regions. When the CST is lesioned, there is a loss of forelimb function; however, if indirect pathways remain intact, rehabilitative training can facilitate recovery. Following spinal cord...

Full description

Saved in:
Bibliographic Details
Main Authors: Imran S. Sheikh, Kathleen M. Keefe, Noelle A. Sterling, Ian P. Junker, Chen Li, Jie Chen, Xiao-Ming Xu, Lynn G. Kirby, George M. Smith
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:iScience
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2589004224025963
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850244635600879616
author Imran S. Sheikh
Kathleen M. Keefe
Noelle A. Sterling
Ian P. Junker
Chen Li
Jie Chen
Xiao-Ming Xu
Lynn G. Kirby
George M. Smith
author_facet Imran S. Sheikh
Kathleen M. Keefe
Noelle A. Sterling
Ian P. Junker
Chen Li
Jie Chen
Xiao-Ming Xu
Lynn G. Kirby
George M. Smith
author_sort Imran S. Sheikh
collection DOAJ
description Summary: Skilled forelimb patterning is regulated by the corticospinal tract (CST) with support from brainstem regions. When the CST is lesioned, there is a loss of forelimb function; however, if indirect pathways remain intact, rehabilitative training can facilitate recovery. Following spinal cord injury, rehabilitation is thought to enhance the reorganization and plasticity of spared supraspinal-propriospinal circuits, aiding functional recovery. This study focused on the roles of cervical propriospinal interneurons (PNs) and rubrospinal neurons (RNs) in the recovery of reaching and grasping behaviors in rats with bilateral lesions of the CST and dorsal columns at C5. The lesions resulted in a 50% decrease in pellet retrieval, which normalized over four weeks of training. Silencing PNs or RNs after recovery resulted in reduced retrieval success. Notably, silencing both pathways corresponded to greater functional loss, underscoring their parallel contributions to recovery, alongside evidence of CST fiber sprouting in the spinal cord and red nucleus.
format Article
id doaj-art-0b70d7ce4e8b45c0a2f083bd2ec1ac7b
institution OA Journals
issn 2589-0042
language English
publishDate 2024-12-01
publisher Elsevier
record_format Article
series iScience
spelling doaj-art-0b70d7ce4e8b45c0a2f083bd2ec1ac7b2025-08-20T01:59:40ZengElsevieriScience2589-00422024-12-01271211137110.1016/j.isci.2024.111371Compensatory adaptation of parallel motor pathways promotes skilled forelimb recovery after spinal cord injuryImran S. Sheikh0Kathleen M. Keefe1Noelle A. Sterling2Ian P. Junker3Chen Li4Jie Chen5Xiao-Ming Xu6Lynn G. Kirby7George M. Smith8Department of Neuroscience, Shriners Hospitals Pediatric Research Center, Center for Neural Rehabilitation and Repair, Lewis Katz School of Medicine at Temple University, Philadelphia, PA 19140, USADepartment of Neuroscience, Shriners Hospitals Pediatric Research Center, Center for Neural Rehabilitation and Repair, Lewis Katz School of Medicine at Temple University, Philadelphia, PA 19140, USADepartment of Neuroscience, Shriners Hospitals Pediatric Research Center, Center for Neural Rehabilitation and Repair, Lewis Katz School of Medicine at Temple University, Philadelphia, PA 19140, USADepartment of Neuroscience, Shriners Hospitals Pediatric Research Center, Center for Neural Rehabilitation and Repair, Lewis Katz School of Medicine at Temple University, Philadelphia, PA 19140, USADepartment of Anatomy and Cell Biology, Center for Substance Abuse Research, Lewis Katz School of Medicine at Temple University, Philadelphia, PA 19140, USADepartment of Neuroscience, Shriners Hospitals Pediatric Research Center, Center for Neural Rehabilitation and Repair, Lewis Katz School of Medicine at Temple University, Philadelphia, PA 19140, USASpinal Cord and Brain Injury Research Group, Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN 46202, USADepartment of Anatomy and Cell Biology, Center for Substance Abuse Research, Lewis Katz School of Medicine at Temple University, Philadelphia, PA 19140, USADepartment of Neuroscience, Shriners Hospitals Pediatric Research Center, Center for Neural Rehabilitation and Repair, Lewis Katz School of Medicine at Temple University, Philadelphia, PA 19140, USA; Corresponding authorSummary: Skilled forelimb patterning is regulated by the corticospinal tract (CST) with support from brainstem regions. When the CST is lesioned, there is a loss of forelimb function; however, if indirect pathways remain intact, rehabilitative training can facilitate recovery. Following spinal cord injury, rehabilitation is thought to enhance the reorganization and plasticity of spared supraspinal-propriospinal circuits, aiding functional recovery. This study focused on the roles of cervical propriospinal interneurons (PNs) and rubrospinal neurons (RNs) in the recovery of reaching and grasping behaviors in rats with bilateral lesions of the CST and dorsal columns at C5. The lesions resulted in a 50% decrease in pellet retrieval, which normalized over four weeks of training. Silencing PNs or RNs after recovery resulted in reduced retrieval success. Notably, silencing both pathways corresponded to greater functional loss, underscoring their parallel contributions to recovery, alongside evidence of CST fiber sprouting in the spinal cord and red nucleus.http://www.sciencedirect.com/science/article/pii/S2589004224025963Natural sciencesBiological sciencesNeuroscienceSystems neuroscience
spellingShingle Imran S. Sheikh
Kathleen M. Keefe
Noelle A. Sterling
Ian P. Junker
Chen Li
Jie Chen
Xiao-Ming Xu
Lynn G. Kirby
George M. Smith
Compensatory adaptation of parallel motor pathways promotes skilled forelimb recovery after spinal cord injury
iScience
Natural sciences
Biological sciences
Neuroscience
Systems neuroscience
title Compensatory adaptation of parallel motor pathways promotes skilled forelimb recovery after spinal cord injury
title_full Compensatory adaptation of parallel motor pathways promotes skilled forelimb recovery after spinal cord injury
title_fullStr Compensatory adaptation of parallel motor pathways promotes skilled forelimb recovery after spinal cord injury
title_full_unstemmed Compensatory adaptation of parallel motor pathways promotes skilled forelimb recovery after spinal cord injury
title_short Compensatory adaptation of parallel motor pathways promotes skilled forelimb recovery after spinal cord injury
title_sort compensatory adaptation of parallel motor pathways promotes skilled forelimb recovery after spinal cord injury
topic Natural sciences
Biological sciences
Neuroscience
Systems neuroscience
url http://www.sciencedirect.com/science/article/pii/S2589004224025963
work_keys_str_mv AT imranssheikh compensatoryadaptationofparallelmotorpathwayspromotesskilledforelimbrecoveryafterspinalcordinjury
AT kathleenmkeefe compensatoryadaptationofparallelmotorpathwayspromotesskilledforelimbrecoveryafterspinalcordinjury
AT noelleasterling compensatoryadaptationofparallelmotorpathwayspromotesskilledforelimbrecoveryafterspinalcordinjury
AT ianpjunker compensatoryadaptationofparallelmotorpathwayspromotesskilledforelimbrecoveryafterspinalcordinjury
AT chenli compensatoryadaptationofparallelmotorpathwayspromotesskilledforelimbrecoveryafterspinalcordinjury
AT jiechen compensatoryadaptationofparallelmotorpathwayspromotesskilledforelimbrecoveryafterspinalcordinjury
AT xiaomingxu compensatoryadaptationofparallelmotorpathwayspromotesskilledforelimbrecoveryafterspinalcordinjury
AT lynngkirby compensatoryadaptationofparallelmotorpathwayspromotesskilledforelimbrecoveryafterspinalcordinjury
AT georgemsmith compensatoryadaptationofparallelmotorpathwayspromotesskilledforelimbrecoveryafterspinalcordinjury