Long ascending propriospinal neurons are heterogenous and subject to spinal cord injury induced anatomic plasticity
Long ascending propriospinal neurons (LAPNs) are a subset of spinal interneurons that provide direct connectivity between distant spinal segments. Here, we focus specifically on an anatomically defined population of “inter-enlargement” LAPNs with cell bodies at L2/3 and terminals at C5/6. Previous s...
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| Published in | Experimental neurology Vol. 373; p. 114631 |
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| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.03.2024
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| Subjects | |
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| Abstract | Long ascending propriospinal neurons (LAPNs) are a subset of spinal interneurons that provide direct connectivity between distant spinal segments. Here, we focus specifically on an anatomically defined population of “inter-enlargement” LAPNs with cell bodies at L2/3 and terminals at C5/6. Previous studies showed that silencing LAPNs in awake and freely moving animals disrupted interlimb coordination of the hindlimbs, forelimbs, and heterolateral limb pairs. Surprisingly, despite a proportion of LAPNs being anatomically intact post- spinal cord injury (SCI), silencing them improved locomotor function but only influenced coordination of the hindlimb pair. Given the functional significance of LAPNs pre- and post-SCI, we characterized their anatomy and SCI-induced anatomical plasticity. This detailed anatomical characterization revealed three morphologically distinct subsets of LAPNs that differ in soma size, neurite complexity and/or neurite orientation. Following a mild thoracic contusive SCI there was a marked shift in neurite orientation in two of the LAPN subsets to a more dorsoventral orientation, and collateral densities decreased in the cervical enlargement but increased just caudal to the injury epicenter. These post-SCI anatomical changes potentially reflect maladaptive plasticity and an effort to establish new functional inputs from sensory afferents that sprout post-SCI to achieve circuitry homeostasis.
•Dual-viral labeling allows for large volume single neuron reconstructions•Long ascending propriospinal neurons have three distinct morphologies•Spinal cord injury results in shifts in neurite orientation•Long ascending propriospinal neurons' axon targets change post-spinal cord injury |
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| AbstractList | Long ascending propriospinal neurons (LAPNs) are a subset of spinal interneurons that provide direct connectivity between distant spinal segments. Here, we focus specifically on an anatomically defined population of "inter-enlargement" LAPNs with cell bodies at L2/3 and terminals at C5/6. Previous studies showed that silencing LAPNs in awake and freely moving animals disrupted interlimb coordination of the hindlimbs, forelimbs, and heterolateral limb pairs. Surprisingly, despite a proportion of LAPNs being anatomically intact post- spinal cord injury (SCI), silencing them improved locomotor function but only influenced coordination of the hindlimb pair. Given the functional significance of LAPNs pre- and post-SCI, we characterized their anatomy and SCI-induced anatomical plasticity. This detailed anatomical characterization revealed three morphologically distinct subsets of LAPNs that differ in soma size, neurite complexity and/or neurite orientation. Following a mild thoracic contusive SCI there was a marked shift in neurite orientation in two of the LAPN subsets to a more dorsoventral orientation, and collateral densities decreased in the cervical enlargement but increased just caudal to the injury epicenter. These post-SCI anatomical changes potentially reflect maladaptive plasticity and an effort to establish new functional inputs from sensory afferents that sprout post-SCI to achieve circuitry homeostasis. Long ascending propriospinal neurons (LAPNs) are a subset of spinal interneurons that provide direct connectivity between distant spinal segments. Here, we focus specifically on an anatomically defined population of "inter-enlargement" LAPNs with cell bodies at L2/3 and terminals at C5/6. Previous studies showed that silencing LAPNs in awake and freely moving animals disrupted interlimb coordination of the hindlimbs, forelimbs, and heterolateral limb pairs. Surprisingly, despite a proportion of LAPNs being anatomically intact post- spinal cord injury (SCI), silencing them improved locomotor function but only influenced coordination of the hindlimb pair. Given the functional significance of LAPNs pre- and post-SCI, we characterized their anatomy and SCI-induced anatomical plasticity. This detailed anatomical characterization revealed three morphologically distinct subsets of LAPNs that differ in soma size, neurite complexity and/or neurite orientation. Following a mild thoracic contusive SCI there was a marked shift in neurite orientation in two of the LAPN subsets to a more dorsoventral orientation, and collateral densities decreased in the cervical enlargement but increased just caudal to the injury epicenter. These post-SCI anatomical changes potentially reflect maladaptive plasticity and an effort to establish new functional inputs from sensory afferents that sprout post-SCI to achieve circuitry homeostasis.Long ascending propriospinal neurons (LAPNs) are a subset of spinal interneurons that provide direct connectivity between distant spinal segments. Here, we focus specifically on an anatomically defined population of "inter-enlargement" LAPNs with cell bodies at L2/3 and terminals at C5/6. Previous studies showed that silencing LAPNs in awake and freely moving animals disrupted interlimb coordination of the hindlimbs, forelimbs, and heterolateral limb pairs. Surprisingly, despite a proportion of LAPNs being anatomically intact post- spinal cord injury (SCI), silencing them improved locomotor function but only influenced coordination of the hindlimb pair. Given the functional significance of LAPNs pre- and post-SCI, we characterized their anatomy and SCI-induced anatomical plasticity. This detailed anatomical characterization revealed three morphologically distinct subsets of LAPNs that differ in soma size, neurite complexity and/or neurite orientation. Following a mild thoracic contusive SCI there was a marked shift in neurite orientation in two of the LAPN subsets to a more dorsoventral orientation, and collateral densities decreased in the cervical enlargement but increased just caudal to the injury epicenter. These post-SCI anatomical changes potentially reflect maladaptive plasticity and an effort to establish new functional inputs from sensory afferents that sprout post-SCI to achieve circuitry homeostasis. Long ascending propriospinal neurons (LAPNs) are a subset of spinal interneurons that provide direct connectivity between distant spinal segments. Here, we focus specifically on an anatomically defined population of “inter-enlargement” LAPNs with cell bodies at L2/3 and terminals at C5/6. Previous studies showed that silencing LAPNs in awake and freely moving animals disrupted interlimb coordination of the hindlimbs, forelimbs, and heterolateral limb pairs. Surprisingly, despite a proportion of LAPNs being anatomically intact post- spinal cord injury (SCI), silencing them improved locomotor function but only influenced coordination of the hindlimb pair. Given the functional significance of LAPNs pre- and post-SCI, we characterized their anatomy and SCI-induced anatomical plasticity. This detailed anatomical characterization revealed three morphologically distinct subsets of LAPNs that differ in soma size, neurite complexity and/or neurite orientation. Following a mild thoracic contusive SCI there was a marked shift in neurite orientation in two of the LAPN subsets to a more dorsoventral orientation, and collateral densities decreased in the cervical enlargement but increased just caudal to the injury epicenter. These post-SCI anatomical changes potentially reflect maladaptive plasticity and an effort to establish new functional inputs from sensory afferents that sprout post-SCI to achieve circuitry homeostasis. •Dual-viral labeling allows for large volume single neuron reconstructions•Long ascending propriospinal neurons have three distinct morphologies•Spinal cord injury results in shifts in neurite orientation•Long ascending propriospinal neurons' axon targets change post-spinal cord injury |
| ArticleNumber | 114631 |
| Author | States, Gregory Anil, Neha Magnuson, David S.K. Brown, Brandon L. Whittemore, Scott R. |
| AuthorAffiliation | 2 Kentucky Spinal Cord Injury Research Center, University of Louisville, Louisville, KY, United States 4 Department of Bioengineering, J.B. Speed School of Engineering, University of Louisville, Louisville, KY, United States 5 Department of Neurological Surgery, School of Medicine, University of Louisville, Louisville, KY, United States 3 Department of Anatomical Sciences and Neurobiology, School of Medicine, University of Louisville, Louisville, KY, United States 1 Interdisciplinary Program in Translational Neuroscience, University of Louisville, Louisville, KY, United States |
| AuthorAffiliation_xml | – name: 5 Department of Neurological Surgery, School of Medicine, University of Louisville, Louisville, KY, United States – name: 3 Department of Anatomical Sciences and Neurobiology, School of Medicine, University of Louisville, Louisville, KY, United States – name: 1 Interdisciplinary Program in Translational Neuroscience, University of Louisville, Louisville, KY, United States – name: 2 Kentucky Spinal Cord Injury Research Center, University of Louisville, Louisville, KY, United States – name: 4 Department of Bioengineering, J.B. Speed School of Engineering, University of Louisville, Louisville, KY, United States |
| Author_xml | – sequence: 1 givenname: Brandon L. surname: Brown fullname: Brown, Brandon L. organization: Interdisciplinary Program in Translational Neuroscience, University of Louisville, Louisville, KY, United States – sequence: 2 givenname: Neha surname: Anil fullname: Anil, Neha organization: Kentucky Spinal Cord Injury Research Center, University of Louisville, Louisville, KY, United States – sequence: 3 givenname: Gregory surname: States fullname: States, Gregory organization: Kentucky Spinal Cord Injury Research Center, University of Louisville, Louisville, KY, United States – sequence: 4 givenname: Scott R. surname: Whittemore fullname: Whittemore, Scott R. organization: Interdisciplinary Program in Translational Neuroscience, University of Louisville, Louisville, KY, United States – sequence: 5 givenname: David S.K. surname: Magnuson fullname: Magnuson, David S.K. email: david.magnuson@louisville.edu organization: Interdisciplinary Program in Translational Neuroscience, University of Louisville, Louisville, KY, United States |
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| Keywords | Virus Spinal cord Injury Neuroanatomy Plasticity Propriospinal Tissue clearing Labeling Anatomy |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Current address: Department of Physical Medicine and Rehabilitation, Case Western Reserve University, 2500 MetroHealth Drive, Cleveland, Ohio 44109 Current address: Norton Neuroscience Institute, 224 E Broadway St., Suite 400, Louisville, KY Current address: Children’s Hospital of Philadelphia, 3501 Civic Center Boulevard, Philadelphia, PA, 19104 |
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| SubjectTerms | Anatomy Animals Hindlimb Injury Interneurons - physiology Labeling Neuroanatomy Neuronal Plasticity Neurons Plasticity Propriospinal Spinal Cord Spinal Cord Injuries Tissue clearing Virus |
| Title | Long ascending propriospinal neurons are heterogenous and subject to spinal cord injury induced anatomic plasticity |
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