Compensatory adaptation of parallel motor pathways promotes skilled forelimb recovery after spinal cord injury
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, r...
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| Vydáno v: | iScience Ročník 27; číslo 12; s. 111371 |
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| Hlavní autoři: | , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
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Elsevier Inc
20.12.2024
Elsevier |
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| ISSN: | 2589-0042, 2589-0042 |
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| Abstract | 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.
[Display omitted]
•Rehabilitation after dorsal funicular lesions promotes recovery of skilled reaching•Partial recovery is mediated by either rubrospinal or C3/C4 propriospinal tracts•Silencing both these tracts eliminates rehabilitation mediated recovery•Rehabilitation induces CST sprouting into the red nucleus and C3/C4 spinal cord
Natural sciences; Biological sciences; Neuroscience; Systems neuroscience |
|---|---|
| AbstractList | 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.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. 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. 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. •Rehabilitation after dorsal funicular lesions promotes recovery of skilled reaching•Partial recovery is mediated by either rubrospinal or C3/C4 propriospinal tracts•Silencing both these tracts eliminates rehabilitation mediated recovery•Rehabilitation induces CST sprouting into the red nucleus and C3/C4 spinal cord Natural sciences; Biological sciences; Neuroscience; Systems neuroscience 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. [Display omitted] •Rehabilitation after dorsal funicular lesions promotes recovery of skilled reaching•Partial recovery is mediated by either rubrospinal or C3/C4 propriospinal tracts•Silencing both these tracts eliminates rehabilitation mediated recovery•Rehabilitation induces CST sprouting into the red nucleus and C3/C4 spinal cord Natural sciences; Biological sciences; Neuroscience; Systems neuroscience |
| ArticleNumber | 111371 |
| Author | Li, Chen Junker, Ian P. Keefe, Kathleen M. Smith, George M. Kirby, Lynn G. Sheikh, Imran S. Xu, Xiao-Ming Chen, Jie Sterling, Noelle A. |
| Author_xml | – sequence: 1 givenname: Imran S. surname: Sheikh fullname: Sheikh, Imran S. organization: Department 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 – sequence: 2 givenname: Kathleen M. surname: Keefe fullname: Keefe, Kathleen M. organization: Department 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 – sequence: 3 givenname: Noelle A. surname: Sterling fullname: Sterling, Noelle A. organization: Department 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 – sequence: 4 givenname: Ian P. surname: Junker fullname: Junker, Ian P. organization: Department 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 – sequence: 5 givenname: Chen surname: Li fullname: Li, Chen organization: Department of Anatomy and Cell Biology, Center for Substance Abuse Research, Lewis Katz School of Medicine at Temple University, Philadelphia, PA 19140, USA – sequence: 6 givenname: Jie surname: Chen fullname: Chen, Jie organization: Department 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 – sequence: 7 givenname: Xiao-Ming surname: Xu fullname: Xu, Xiao-Ming organization: Spinal Cord and Brain Injury Research Group, Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN 46202, USA – sequence: 8 givenname: Lynn G. surname: Kirby fullname: Kirby, Lynn G. organization: Department of Anatomy and Cell Biology, Center for Substance Abuse Research, Lewis Katz School of Medicine at Temple University, Philadelphia, PA 19140, USA – sequence: 9 givenname: George M. orcidid: 0000-0002-2614-1624 surname: Smith fullname: Smith, George M. email: george.smith@temple.edu organization: Department 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 |
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