Visual imaging as a predictor of neurodegeneration in experimental autoimmune demyelination and multiple sclerosis

Abstract Thalamic volume is associated with clinical disability in multiple sclerosis (MS) and is vulnerable to secondary neurodegeneration due to its extensive connectivity throughout the central nervous system (CNS). Using a model of autoimmune demyelination that exhibits CNS-infiltrating immune c...

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Main Authors: Gabrielle M. Mey, Kirsten S. Evonuk, McKenzie K. Chappell, Laura M. Wolfe, Rupesh Singh, Julia C. Batoki, Minzhong Yu, Neal S. Peachey, Bela Anand-Apte, Robert Bermel, Daniel Ontaneda, Kunio Nakamura, Kedar R. Mahajan, Tara M. DeSilva
Format: Article
Language:English
Published: BMC 2022-06-01
Series:Acta Neuropathologica Communications
Online Access:https://doi.org/10.1186/s40478-022-01391-y
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author Gabrielle M. Mey
Kirsten S. Evonuk
McKenzie K. Chappell
Laura M. Wolfe
Rupesh Singh
Julia C. Batoki
Minzhong Yu
Neal S. Peachey
Bela Anand-Apte
Robert Bermel
Daniel Ontaneda
Kunio Nakamura
Kedar R. Mahajan
Tara M. DeSilva
author_facet Gabrielle M. Mey
Kirsten S. Evonuk
McKenzie K. Chappell
Laura M. Wolfe
Rupesh Singh
Julia C. Batoki
Minzhong Yu
Neal S. Peachey
Bela Anand-Apte
Robert Bermel
Daniel Ontaneda
Kunio Nakamura
Kedar R. Mahajan
Tara M. DeSilva
author_sort Gabrielle M. Mey
collection DOAJ
description Abstract Thalamic volume is associated with clinical disability in multiple sclerosis (MS) and is vulnerable to secondary neurodegeneration due to its extensive connectivity throughout the central nervous system (CNS). Using a model of autoimmune demyelination that exhibits CNS-infiltrating immune cells in both spinal cord white matter and optic nerve, we sought to evaluate neurodegenerative changes due to lesions affecting the spino- and retino-thalamic pathways. We found comparable axonal loss in spinal cord white matter and optic nerve during the acute phase of disease consistent with synaptic loss, but not neuronal cell body loss in the thalamic nuclei that receive input from these discrete pathways. Loss of spinal cord neurons or retinal ganglion cells retrograde to their respective axons was not observed until the chronic phase of disease, where optical coherence tomography (OCT) documented reduced inner retinal thickness. In patients with relapsing–remitting MS without a history of optic neuritis, OCT measures of inner retinal volume correlated with retino-thalamic (lateral geniculate nucleus) and spino-thalamic (ventral posterior nucleus) volume as well as neuroperformance measures. These data suggest retinal imaging may serve as an important noninvasive predictor of neurodegeneration in MS.
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spelling doaj.art-d1f51e11e09742c58a6739f3748c0f612022-12-22T00:28:01ZengBMCActa Neuropathologica Communications2051-59602022-06-0110111810.1186/s40478-022-01391-yVisual imaging as a predictor of neurodegeneration in experimental autoimmune demyelination and multiple sclerosisGabrielle M. Mey0Kirsten S. Evonuk1McKenzie K. Chappell2Laura M. Wolfe3Rupesh Singh4Julia C. Batoki5Minzhong Yu6Neal S. Peachey7Bela Anand-Apte8Robert Bermel9Daniel Ontaneda10Kunio Nakamura11Kedar R. Mahajan12Tara M. DeSilva13Department of Neurosciences, Lerner Research Institute, Cleveland Clinic Foundation, and Case Western Reserve UniversityDepartment of Neurosciences, Lerner Research Institute, Cleveland Clinic Foundation, and Case Western Reserve UniversityDepartment of Neurosciences, Lerner Research Institute, Cleveland Clinic Foundation, and Case Western Reserve UniversityDepartment of Neurosciences, Lerner Research Institute, Cleveland Clinic Foundation, and Case Western Reserve UniversityCole Eye Institute, Cleveland Clinic FoundationCole Eye Institute, Cleveland Clinic FoundationCole Eye Institute, Cleveland Clinic FoundationCole Eye Institute, Cleveland Clinic FoundationCole Eye Institute, Cleveland Clinic FoundationMellen Center for MS Treatment and Research, Neurological Institute, Cleveland Clinic FoundationMellen Center for MS Treatment and Research, Neurological Institute, Cleveland Clinic FoundationDepartment of Biomedical Engineering, Lerner Research Institute, Cleveland Clinic FoundationDepartment of Neurosciences, Lerner Research Institute, Cleveland Clinic Foundation, and Case Western Reserve UniversityDepartment of Neurosciences, Lerner Research Institute, Cleveland Clinic Foundation, and Case Western Reserve UniversityAbstract Thalamic volume is associated with clinical disability in multiple sclerosis (MS) and is vulnerable to secondary neurodegeneration due to its extensive connectivity throughout the central nervous system (CNS). Using a model of autoimmune demyelination that exhibits CNS-infiltrating immune cells in both spinal cord white matter and optic nerve, we sought to evaluate neurodegenerative changes due to lesions affecting the spino- and retino-thalamic pathways. We found comparable axonal loss in spinal cord white matter and optic nerve during the acute phase of disease consistent with synaptic loss, but not neuronal cell body loss in the thalamic nuclei that receive input from these discrete pathways. Loss of spinal cord neurons or retinal ganglion cells retrograde to their respective axons was not observed until the chronic phase of disease, where optical coherence tomography (OCT) documented reduced inner retinal thickness. In patients with relapsing–remitting MS without a history of optic neuritis, OCT measures of inner retinal volume correlated with retino-thalamic (lateral geniculate nucleus) and spino-thalamic (ventral posterior nucleus) volume as well as neuroperformance measures. These data suggest retinal imaging may serve as an important noninvasive predictor of neurodegeneration in MS.https://doi.org/10.1186/s40478-022-01391-y
spellingShingle Gabrielle M. Mey
Kirsten S. Evonuk
McKenzie K. Chappell
Laura M. Wolfe
Rupesh Singh
Julia C. Batoki
Minzhong Yu
Neal S. Peachey
Bela Anand-Apte
Robert Bermel
Daniel Ontaneda
Kunio Nakamura
Kedar R. Mahajan
Tara M. DeSilva
Visual imaging as a predictor of neurodegeneration in experimental autoimmune demyelination and multiple sclerosis
Acta Neuropathologica Communications
title Visual imaging as a predictor of neurodegeneration in experimental autoimmune demyelination and multiple sclerosis
title_full Visual imaging as a predictor of neurodegeneration in experimental autoimmune demyelination and multiple sclerosis
title_fullStr Visual imaging as a predictor of neurodegeneration in experimental autoimmune demyelination and multiple sclerosis
title_full_unstemmed Visual imaging as a predictor of neurodegeneration in experimental autoimmune demyelination and multiple sclerosis
title_short Visual imaging as a predictor of neurodegeneration in experimental autoimmune demyelination and multiple sclerosis
title_sort visual imaging as a predictor of neurodegeneration in experimental autoimmune demyelination and multiple sclerosis
url https://doi.org/10.1186/s40478-022-01391-y
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