Spinal Cord Imaging Markers and Recovery of Volitional Leg Movement With Spinal Cord Epidural Stimulation in Individuals With Clinically Motor Complete Spinal Cord Injury

Previous studies have shown that epidural stimulation of the lumbosacral spinal cord (scES) can re-enable lower limb volitional motor control in individuals with chronic, clinically motor complete spinal cord injury (SCI). This observation entails that residual supraspinal connectivity to the lumbos...

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Main Authors: Enrico Rejc, Andrew C. Smith, Kenneth A. Weber, Beatrice Ugiliweneza, Robert J. Bert, Mohammadjavad Negahdar, Maxwell Boakye, Susan J. Harkema, Claudia A. Angeli
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-10-01
Series:Frontiers in Systems Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnsys.2020.559313/full
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author Enrico Rejc
Enrico Rejc
Andrew C. Smith
Kenneth A. Weber
Beatrice Ugiliweneza
Beatrice Ugiliweneza
Robert J. Bert
Mohammadjavad Negahdar
Maxwell Boakye
Maxwell Boakye
Susan J. Harkema
Susan J. Harkema
Susan J. Harkema
Susan J. Harkema
Claudia A. Angeli
Claudia A. Angeli
Claudia A. Angeli
spellingShingle Enrico Rejc
Enrico Rejc
Andrew C. Smith
Kenneth A. Weber
Beatrice Ugiliweneza
Beatrice Ugiliweneza
Robert J. Bert
Mohammadjavad Negahdar
Maxwell Boakye
Maxwell Boakye
Susan J. Harkema
Susan J. Harkema
Susan J. Harkema
Susan J. Harkema
Claudia A. Angeli
Claudia A. Angeli
Claudia A. Angeli
Spinal Cord Imaging Markers and Recovery of Volitional Leg Movement With Spinal Cord Epidural Stimulation in Individuals With Clinically Motor Complete Spinal Cord Injury
Frontiers in Systems Neuroscience
epidural stimulation
spinal cord injury
voluntary movement
spinal cord MRI
spinal cord lesion
spinal tracts
author_facet Enrico Rejc
Enrico Rejc
Andrew C. Smith
Kenneth A. Weber
Beatrice Ugiliweneza
Beatrice Ugiliweneza
Robert J. Bert
Mohammadjavad Negahdar
Maxwell Boakye
Maxwell Boakye
Susan J. Harkema
Susan J. Harkema
Susan J. Harkema
Susan J. Harkema
Claudia A. Angeli
Claudia A. Angeli
Claudia A. Angeli
author_sort Enrico Rejc
title Spinal Cord Imaging Markers and Recovery of Volitional Leg Movement With Spinal Cord Epidural Stimulation in Individuals With Clinically Motor Complete Spinal Cord Injury
title_short Spinal Cord Imaging Markers and Recovery of Volitional Leg Movement With Spinal Cord Epidural Stimulation in Individuals With Clinically Motor Complete Spinal Cord Injury
title_full Spinal Cord Imaging Markers and Recovery of Volitional Leg Movement With Spinal Cord Epidural Stimulation in Individuals With Clinically Motor Complete Spinal Cord Injury
title_fullStr Spinal Cord Imaging Markers and Recovery of Volitional Leg Movement With Spinal Cord Epidural Stimulation in Individuals With Clinically Motor Complete Spinal Cord Injury
title_full_unstemmed Spinal Cord Imaging Markers and Recovery of Volitional Leg Movement With Spinal Cord Epidural Stimulation in Individuals With Clinically Motor Complete Spinal Cord Injury
title_sort spinal cord imaging markers and recovery of volitional leg movement with spinal cord epidural stimulation in individuals with clinically motor complete spinal cord injury
publisher Frontiers Media S.A.
series Frontiers in Systems Neuroscience
issn 1662-5137
publishDate 2020-10-01
description Previous studies have shown that epidural stimulation of the lumbosacral spinal cord (scES) can re-enable lower limb volitional motor control in individuals with chronic, clinically motor complete spinal cord injury (SCI). This observation entails that residual supraspinal connectivity to the lumbosacral spinal circuitry still persisted after SCI, although it was non-detectable when scES was not provided. In the present study, we aimed at exploring further the mechanisms underlying scES-promoted recovery of volitional lower limb motor control by investigating neuroimaging markers at the spinal cord lesion site via magnetic resonance imaging (MRI). Spinal cord MRI was collected prior to epidural stimulator implantation in 13 individuals with chronic, clinically motor complete SCI, and the spared tissue of specific regions of the spinal cord (anterior, posterior, right, left, and total cord) was assessed. After epidural stimulator implantation, and prior to any training, volitional motor control was evaluated during left and right lower limb flexion and ankle dorsiflexion attempts. The ability to generate force exertion and movement was not correlated to any neuroimaging marker. On the other hand, spared tissue of specific cord regions significantly and importantly correlated with some aspects of motor control that include activation amplitude of antagonist (negative correlation) muscles during left ankle dorsiflexion, and electromyographic coordination patterns during right lower limb flexion. The fact that amount and location of spared spinal cord tissue at the lesion site were not related to the ability to generate volitional lower limb movements may suggest that supraspinal inputs through spared spinal cord regions that differ across individuals can result in the generation of lower limb volitional motor output prior to any training when epidural stimulation is provided.
topic epidural stimulation
spinal cord injury
voluntary movement
spinal cord MRI
spinal cord lesion
spinal tracts
url https://www.frontiersin.org/articles/10.3389/fnsys.2020.559313/full
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spelling doaj-d1262d81f35e4c67a00ff2fdfe9369242020-11-25T03:44:30ZengFrontiers Media S.A.Frontiers in Systems Neuroscience1662-51372020-10-011410.3389/fnsys.2020.559313559313Spinal Cord Imaging Markers and Recovery of Volitional Leg Movement With Spinal Cord Epidural Stimulation in Individuals With Clinically Motor Complete Spinal Cord InjuryEnrico Rejc0Enrico Rejc1Andrew C. Smith2Kenneth A. Weber3Beatrice Ugiliweneza4Beatrice Ugiliweneza5Robert J. Bert6Mohammadjavad Negahdar7Maxwell Boakye8Maxwell Boakye9Susan J. Harkema10Susan J. Harkema11Susan J. Harkema12Susan J. Harkema13Claudia A. Angeli14Claudia A. Angeli15Claudia A. Angeli16Kentucky Spinal Cord Injury Research Center, University of Louisville, Louisville, KY, United StatesDepartment of Neurological Surgery, University of Louisville, Louisville, KY, United StatesUniversity of Colorado School of Medicine, Department of Physical Medicine and Rehabilitation, Physical Therapy Program, Aurora, CO, United StatesDepartment of Anethesiology, Perioperative and Pain Medicine, Stanford University School of Medicine, Palo Alto, CA, United StatesKentucky Spinal Cord Injury Research Center, University of Louisville, Louisville, KY, United StatesDepartment of Neurological Surgery, University of Louisville, Louisville, KY, United StatesDepartment of Radiology, University of Louisville, Louisville, KY, United StatesDepartment of Radiology, University of Louisville, Louisville, KY, United StatesKentucky Spinal Cord Injury Research Center, University of Louisville, Louisville, KY, United StatesDepartment of Neurological Surgery, University of Louisville, Louisville, KY, United StatesKentucky Spinal Cord Injury Research Center, University of Louisville, Louisville, KY, United StatesDepartment of Neurological Surgery, University of Louisville, Louisville, KY, United StatesFrazier Rehabilitation Institute, University of Louisville Health, Louisville, KY, United StatesDepartment of Bioengineering, University of Louisville, Louisville, KY, United StatesKentucky Spinal Cord Injury Research Center, University of Louisville, Louisville, KY, United StatesFrazier Rehabilitation Institute, University of Louisville Health, Louisville, KY, United StatesDepartment of Bioengineering, University of Louisville, Louisville, KY, United StatesPrevious studies have shown that epidural stimulation of the lumbosacral spinal cord (scES) can re-enable lower limb volitional motor control in individuals with chronic, clinically motor complete spinal cord injury (SCI). This observation entails that residual supraspinal connectivity to the lumbosacral spinal circuitry still persisted after SCI, although it was non-detectable when scES was not provided. In the present study, we aimed at exploring further the mechanisms underlying scES-promoted recovery of volitional lower limb motor control by investigating neuroimaging markers at the spinal cord lesion site via magnetic resonance imaging (MRI). Spinal cord MRI was collected prior to epidural stimulator implantation in 13 individuals with chronic, clinically motor complete SCI, and the spared tissue of specific regions of the spinal cord (anterior, posterior, right, left, and total cord) was assessed. After epidural stimulator implantation, and prior to any training, volitional motor control was evaluated during left and right lower limb flexion and ankle dorsiflexion attempts. The ability to generate force exertion and movement was not correlated to any neuroimaging marker. On the other hand, spared tissue of specific cord regions significantly and importantly correlated with some aspects of motor control that include activation amplitude of antagonist (negative correlation) muscles during left ankle dorsiflexion, and electromyographic coordination patterns during right lower limb flexion. The fact that amount and location of spared spinal cord tissue at the lesion site were not related to the ability to generate volitional lower limb movements may suggest that supraspinal inputs through spared spinal cord regions that differ across individuals can result in the generation of lower limb volitional motor output prior to any training when epidural stimulation is provided.https://www.frontiersin.org/articles/10.3389/fnsys.2020.559313/fullepidural stimulationspinal cord injuryvoluntary movementspinal cord MRIspinal cord lesionspinal tracts