Augmentation of Voluntary Locomotor Activity by Transcutaneous Spinal Cord Stimulation in Motor-Incomplete Spinal Cord-Injured Individuals

The level of sustainable excitability within lumbar spinal cord circuitries is one of the factors determining the functional outcome of locomotor therapy after motor‐incomplete spinal cord injury. Here, we present initial data using noninvasive transcutaneous lumbar spinal cord stimulation (tSCS) to...

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Published inArtificial organs Vol. 39; no. 10; pp. E176 - E186
Main Authors Hofstoetter, Ursula S., Krenn, Matthias, Danner, Simon M., Hofer, Christian, Kern, Helmut, McKay, William B., Mayr, Winfried, Minassian, Karen
Format Journal Article
LanguageEnglish
Published United States Blackwell Publishing Ltd 01.10.2015
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Abstract The level of sustainable excitability within lumbar spinal cord circuitries is one of the factors determining the functional outcome of locomotor therapy after motor‐incomplete spinal cord injury. Here, we present initial data using noninvasive transcutaneous lumbar spinal cord stimulation (tSCS) to modulate this central state of excitability during voluntary treadmill stepping in three motor‐incomplete spinal cord‐injured individuals. Stimulation was applied at 30 Hz with an intensity that generated tingling sensations in the lower limb dermatomes, yet without producing muscle reflex activity. This stimulation changed muscle activation, gait kinematics, and the amount of manual assistance required from the therapists to maintain stepping with some interindividual differences. The effect on motor outputs during treadmill‐stepping was essentially augmentative and step‐phase dependent despite the invariant tonic stimulation. The most consistent modification was found in the gait kinematics, with the hip flexion during swing increased by 11.3° ± 5.6° across all subjects. This preliminary work suggests that tSCS provides for a background increase in activation of the lumbar spinal locomotor circuitry that has partially lost its descending drive. Voluntary inputs and step‐related feedback build upon the stimulation‐induced increased state of excitability in the generation of locomotor activity. Thus, tSCS essentially works as an electrical neuroprosthesis augmenting remaining motor control.
AbstractList The level of sustainable excitability within lumbar spinal cord circuitries is one of the factors determining the functional outcome of locomotor therapy after motor‐incomplete spinal cord injury. Here, we present initial data using noninvasive transcutaneous lumbar spinal cord stimulation (t SCS ) to modulate this central state of excitability during voluntary treadmill stepping in three motor‐incomplete spinal cord‐injured individuals. Stimulation was applied at 30 Hz with an intensity that generated tingling sensations in the lower limb dermatomes, yet without producing muscle reflex activity. This stimulation changed muscle activation, gait kinematics, and the amount of manual assistance required from the therapists to maintain stepping with some interindividual differences. The effect on motor outputs during treadmill‐stepping was essentially augmentative and step‐phase dependent despite the invariant tonic stimulation. The most consistent modification was found in the gait kinematics, with the hip flexion during swing increased by 11.3° ± 5.6° across all subjects. This preliminary work suggests that t SCS provides for a background increase in activation of the lumbar spinal locomotor circuitry that has partially lost its descending drive. Voluntary inputs and step‐related feedback build upon the stimulation‐induced increased state of excitability in the generation of locomotor activity. Thus, t SCS essentially works as an electrical neuroprosthesis augmenting remaining motor control.
The level of sustainable excitability within lumbar spinal cord circuitries is one of the factors determining the functional outcome of locomotor therapy after motor‐incomplete spinal cord injury. Here, we present initial data using noninvasive transcutaneous lumbar spinal cord stimulation (tSCS) to modulate this central state of excitability during voluntary treadmill stepping in three motor‐incomplete spinal cord‐injured individuals. Stimulation was applied at 30 Hz with an intensity that generated tingling sensations in the lower limb dermatomes, yet without producing muscle reflex activity. This stimulation changed muscle activation, gait kinematics, and the amount of manual assistance required from the therapists to maintain stepping with some interindividual differences. The effect on motor outputs during treadmill‐stepping was essentially augmentative and step‐phase dependent despite the invariant tonic stimulation. The most consistent modification was found in the gait kinematics, with the hip flexion during swing increased by 11.3° ± 5.6° across all subjects. This preliminary work suggests that tSCS provides for a background increase in activation of the lumbar spinal locomotor circuitry that has partially lost its descending drive. Voluntary inputs and step‐related feedback build upon the stimulation‐induced increased state of excitability in the generation of locomotor activity. Thus, tSCS essentially works as an electrical neuroprosthesis augmenting remaining motor control.
The level of sustainable excitability within lumbar spinal cord circuitries is one of the factors determining the functional outcome of locomotor therapy after motor-incomplete spinal cord injury. Here, we present initial data using noninvasive transcutaneous lumbar spinal cord stimulation (tSCS) to modulate this central state of excitability during voluntary treadmill stepping in three motor-incomplete spinal cord-injured individuals. Stimulation was applied at 30 Hz with an intensity that generated tingling sensations in the lower limb dermatomes, yet without producing muscle reflex activity. This stimulation changed muscle activation, gait kinematics, and the amount of manual assistance required from the therapists to maintain stepping with some interindividual differences. The effect on motor outputs during treadmill-stepping was essentially augmentative and step-phase dependent despite the invariant tonic stimulation. The most consistent modification was found in the gait kinematics, with the hip flexion during swing increased by 11.3° ± 5.6° across all subjects. This preliminary work suggests that tSCS provides for a background increase in activation of the lumbar spinal locomotor circuitry that has partially lost its descending drive. Voluntary inputs and step-related feedback build upon the stimulation-induced increased state of excitability in the generation of locomotor activity. Thus, tSCS essentially works as an electrical neuroprosthesis augmenting remaining motor control.The level of sustainable excitability within lumbar spinal cord circuitries is one of the factors determining the functional outcome of locomotor therapy after motor-incomplete spinal cord injury. Here, we present initial data using noninvasive transcutaneous lumbar spinal cord stimulation (tSCS) to modulate this central state of excitability during voluntary treadmill stepping in three motor-incomplete spinal cord-injured individuals. Stimulation was applied at 30 Hz with an intensity that generated tingling sensations in the lower limb dermatomes, yet without producing muscle reflex activity. This stimulation changed muscle activation, gait kinematics, and the amount of manual assistance required from the therapists to maintain stepping with some interindividual differences. The effect on motor outputs during treadmill-stepping was essentially augmentative and step-phase dependent despite the invariant tonic stimulation. The most consistent modification was found in the gait kinematics, with the hip flexion during swing increased by 11.3° ± 5.6° across all subjects. This preliminary work suggests that tSCS provides for a background increase in activation of the lumbar spinal locomotor circuitry that has partially lost its descending drive. Voluntary inputs and step-related feedback build upon the stimulation-induced increased state of excitability in the generation of locomotor activity. Thus, tSCS essentially works as an electrical neuroprosthesis augmenting remaining motor control.
The level of sustainable excitability within lumbar spinal cord circuitries is one of the factors determining the functional outcome of locomotor therapy after motor-incomplete spinal cord injury. Here, we present initial data using noninvasive transcutaneous lumbar spinal cord stimulation (tSCS) to modulate this central state of excitability during voluntary treadmill stepping in three motor-incomplete spinal cord-injured individuals. Stimulation was applied at 30Hz with an intensity that generated tingling sensations in the lower limb dermatomes, yet without producing muscle reflex activity. This stimulation changed muscle activation, gait kinematics, and the amount of manual assistance required from the therapists to maintain stepping with some interindividual differences. The effect on motor outputs during treadmill-stepping was essentially augmentative and step-phase dependent despite the invariant tonic stimulation. The most consistent modification was found in the gait kinematics, with the hip flexion during swing increased by 11.3°±5.6° across all subjects. This preliminary work suggests that tSCS provides for a background increase in activation of the lumbar spinal locomotor circuitry that has partially lost its descending drive. Voluntary inputs and step-related feedback build upon the stimulation-induced increased state of excitability in the generation of locomotor activity. Thus, tSCS essentially works as an electrical neuroprosthesis augmenting remaining motor control.
Author McKay, William B.
Mayr, Winfried
Krenn, Matthias
Hofstoetter, Ursula S.
Hofer, Christian
Kern, Helmut
Danner, Simon M.
Minassian, Karen
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  organization: Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna, Austria
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  fullname: Mayr, Winfried
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  organization: Center for Medical Physics and Biomedical Engineering, Medical University of Vienna, Vienna, Austria
– sequence: 8
  givenname: Karen
  surname: Minassian
  fullname: Minassian, Karen
  organization: Center for Medical Physics and Biomedical Engineering, Medical University of Vienna, Vienna, Austria
BackLink https://www.ncbi.nlm.nih.gov/pubmed/26450344$$D View this record in MEDLINE/PubMed
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Keywords Human
Transcutaneous spinal cord stimulation
Spinal cord injury
Neuromodulation
Locomotor training
Language English
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October 2015
2015-10-00
2015-Oct
20151001
PublicationDateYYYYMMDD 2015-10-01
PublicationDate_xml – month: 10
  year: 2015
  text: 2015-10
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: Geesthacht
PublicationTitle Artificial organs
PublicationTitleAlternate Artificial Organs
PublicationYear 2015
Publisher Blackwell Publishing Ltd
Wiley Subscription Services, Inc
Publisher_xml – name: Blackwell Publishing Ltd
– name: Wiley Subscription Services, Inc
References Dimitrijevic MR, Gerasimenko Y, Pinter MM. Evidence for a spinal central pattern generator in humans. Ann N Y Acad Sci 1998;860:360-376.
Sherwood AM, McKay WB, Dimitrijevic MR. Motor control after spinal cord injury: assessment using surface EMG. Muscle Nerve 1996;19:966-979.
Rattay F. The basic mechanism for the electrical stimulation of the nervous system. Neuroscience 1999;89:335-346.
Hofstoetter US, Hofer C, Kern H, et al. Effects of transcutaneous spinal cord stimulation on voluntary locomotor activity in an incomplete spinal cord injured individual. Biomed Tech (Berl) 2013 doi: 10.1515/bmt-2013-4014; [Epub 2013 Sep 7].
Curt A, Van Hedel HJ, Klaus D, Dietz V. EM-SCI study group. Recovery from a spinal cord injury: significance of compensation, neural plasticity, and repair. J Neurotrauma 2008;25:677-685.
Hofstoetter US, McKay WB, Tansey KE, Mayr W, Kern H, Minassian K. Modification of spasticity by transcutaneous spinal cord stimulation in individuals with incomplete spinal cord injury. J Spinal Cord Med 2014;37:202-211.
Pinter MM, Gerstenbrand F, Dimitrijevic MR. Epidural electrical stimulation of posterior structures of the human lumbosacral cord: 3. Control of spasticity. Spinal Cord 2000;38:524-531.
Minassian K, Persy I, Rattay F, Dimitrijevic MR. Effect of peripheral afferent and central afferent input to the human lumbar spinal cord isolated from brain control. Biocybernetics Biomed Eng 2005;25:11-29.
Hunter JP, Ashby P. Segmental effects of epidural spinal cord stimulation in humans. J Physiol 1994;474:407-419.
Harkema SJ. Plasticity of interneuronal networks of the functionally isolated human spinal cord. Brain Res Rev 2008;57:255-264.
Herman R, He J, D'Luzansky S, Willis W, Dilli S. Spinal cord stimulation facilitates functional walking in a chronic, incomplete spinal cord injured. Spinal Cord 2002;40:65-68.
Harkema SJ, Hurley SL, Patel UK, Requejo PS, Dobkin BH, Edgerton VR. Human lumbosacral spinal cord interprets loading during stepping. J Neurophysiol 1997;77:797-811.
Barolat G, Massaro F, He J, Zeme S, Ketcik B. Mapping of sensory responses to epidural stimulation of the intraspinal neural structures in man. J Neurosurg 1993;78:233-239.
Hofstoetter US, Minassian K, Hofer C, Mayr W, Rattay F, Dimitrijevic MR. Modification of reflex responses to lumbar posterior root stimulation by motor tasks in healthy subjects. Artif Organs 2008;32:644-648.
Dietz V, Müller R, Colombo G. Locomotor activity in spinal man: significance of afferent input from joint and load receptors. Brain 2002;125:2626-2634.
Minassian K, Persy I, Rattay F, Pinter MM, Kern H, Dimitrijevic MR. Human lumbar cord circuitries can be activated by extrinsic tonic input to generate locomotor-like activity. Hum Mov Sci 2007;26:275-295.
Minassian K, Hofstoetter U, Tansey K, Mayr W. Neuromodulation of lower limb motor control in restorative neurology. Clin Neurol Neurosurg 2012;114:489-497.
Burns S, Biering-Sørensen F, Donovan W, et al. International standards for neurological classification of spinal cord injury, revised 2011. Top Spinal Cord Inj Rehabil 2012;18:85-99.
Danner SM, Hofstoetter US, Ladenbauer J, Rattay F, Minassian K. Can the human lumbar posterior columns be stimulated by transcutaneous spinal cord stimulation? A modeling study. Artif Organs 2011;35:257-262.
Huang H, He J, Herman R, Carhart MR. Modulation effects of epidural spinal cord stimulation on muscle activities during walking. IEEE Trans Neural Syst Rehabil Eng 2006;14:14-23.
Harkema S, Gerasimenko Y, Hodes J, et al. Effect of epidural stimulation of the lumbosacral spinal cord on voluntary movement, standing, and assisted stepping after motor complete paraplegia: a case study. Lancet 2011;377:1938-1947.
Minassian K, Jilge B, Rattay F, et al. Stepping-like movements in humans with complete spinal cord injury induced by epidural stimulation of the lumbar cord: electromyographic study of compound muscle action potentials. Spinal Cord 2004;42:401-416.
Ranck JB. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 1975;98:417-440.
Harkema S, Behrman A, Barbeau H. Evidence-based therapy for recovery of function after spinal cord injury. Handb Clin Neurol 2012;109:259-274.
Wernig A, Müller S. Laufband locomotion with body weight support improved walking in persons with severe spinal cord injuries. Paraplegia 1992;30:229-238.
Barolat G, Myklebust JB, Wenninger W. Enhancement of voluntary motor function following spinal cord stimulation-case study. Appl Neurophysiol 1986;49:307-314.
Ladenbauer J, Minassian K, Hofstoetter US, Dimitrijevic MR, Rattay F. Stimulation of the human lumbar spinal cord with implanted and surface electrodes: a computer simulation study. IEEE Trans Neural Syst Rehabil Eng 2010;18:637-645.
Lloyd DCP. Reflex action in relation to pattern and peripheral source of afferent stimulation. J Neurophysiol 1943;6:111-120.
Holsheimer J. Which neuronal elements are activated directly by spinal cord stimulation. Neuromodulation 2002;5:25-31.
Morganti B, Scivoletto G, Ditunno P, Ditunno JF, Molinari M. Walking index for spinal cord injury (WISCI): criterion validation. Spinal Cord 2005;43:27-33.
Minassian K, Persy I, Rattay F, Dimitrijevic MR, Hofer C, Kern H. Posterior root-muscle reflexes elicited by transcutaneous stimulation of the human lumbosacral cord. Muscle Nerve 2007;35:327-336.
Sedgwick EM, Illis LS, Tallis RC, et al. Evoked potentials and contingent negative variation during treatment of multiple sclerosis with spinal cord stimulation. J Neurol Neurosurg Psychiatry 1980;43:15-24.
Roy FD, Gibson G, Stein RB. Effect of percutaneous stimulation at different spinal levels on the activation of sensory and motor roots. Exp Brain Res 2012;223:281-289.
Hubli M, Dietz V. The physiological basis of neurorehabilitation-locomotor training after spinal cord injury. J Neuroeng Rehabil 2013;10:5.
Rattay F, Minassian K, Dimitrijevic MR. Epidural electrical stimulation of posterior structures of the human lumbosacral cord: 2. quantitative analysis by computer modeling. Spinal Cord 2000;38:473-489.
Beres-Jones JA, Harkema SJ. The human spinal cord interprets velocity-dependent afferent input during stepping. Brain 2004;127:2232-2246.
1943; 6
2011; 377
1994; 474
2004; 42
2004; 127
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2000; 38
1997; 77
2013; 10
2002; 40
2002; 125
2008; 25
1986; 49
2014; 37
2013
2012; 114
1998; 860
2007; 26
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References_xml – reference: Hubli M, Dietz V. The physiological basis of neurorehabilitation-locomotor training after spinal cord injury. J Neuroeng Rehabil 2013;10:5.
– reference: Hofstoetter US, Hofer C, Kern H, et al. Effects of transcutaneous spinal cord stimulation on voluntary locomotor activity in an incomplete spinal cord injured individual. Biomed Tech (Berl) 2013 doi: 10.1515/bmt-2013-4014; [Epub 2013 Sep 7].
– reference: Beres-Jones JA, Harkema SJ. The human spinal cord interprets velocity-dependent afferent input during stepping. Brain 2004;127:2232-2246.
– reference: Sherwood AM, McKay WB, Dimitrijevic MR. Motor control after spinal cord injury: assessment using surface EMG. Muscle Nerve 1996;19:966-979.
– reference: Dimitrijevic MR, Gerasimenko Y, Pinter MM. Evidence for a spinal central pattern generator in humans. Ann N Y Acad Sci 1998;860:360-376.
– reference: Ranck JB. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 1975;98:417-440.
– reference: Rattay F. The basic mechanism for the electrical stimulation of the nervous system. Neuroscience 1999;89:335-346.
– reference: Sedgwick EM, Illis LS, Tallis RC, et al. Evoked potentials and contingent negative variation during treatment of multiple sclerosis with spinal cord stimulation. J Neurol Neurosurg Psychiatry 1980;43:15-24.
– reference: Morganti B, Scivoletto G, Ditunno P, Ditunno JF, Molinari M. Walking index for spinal cord injury (WISCI): criterion validation. Spinal Cord 2005;43:27-33.
– reference: Dietz V, Müller R, Colombo G. Locomotor activity in spinal man: significance of afferent input from joint and load receptors. Brain 2002;125:2626-2634.
– reference: Hofstoetter US, Minassian K, Hofer C, Mayr W, Rattay F, Dimitrijevic MR. Modification of reflex responses to lumbar posterior root stimulation by motor tasks in healthy subjects. Artif Organs 2008;32:644-648.
– reference: Herman R, He J, D'Luzansky S, Willis W, Dilli S. Spinal cord stimulation facilitates functional walking in a chronic, incomplete spinal cord injured. Spinal Cord 2002;40:65-68.
– reference: Harkema S, Behrman A, Barbeau H. Evidence-based therapy for recovery of function after spinal cord injury. Handb Clin Neurol 2012;109:259-274.
– reference: Danner SM, Hofstoetter US, Ladenbauer J, Rattay F, Minassian K. Can the human lumbar posterior columns be stimulated by transcutaneous spinal cord stimulation? A modeling study. Artif Organs 2011;35:257-262.
– reference: Burns S, Biering-Sørensen F, Donovan W, et al. International standards for neurological classification of spinal cord injury, revised 2011. Top Spinal Cord Inj Rehabil 2012;18:85-99.
– reference: Minassian K, Hofstoetter U, Tansey K, Mayr W. Neuromodulation of lower limb motor control in restorative neurology. Clin Neurol Neurosurg 2012;114:489-497.
– reference: Harkema SJ. Plasticity of interneuronal networks of the functionally isolated human spinal cord. Brain Res Rev 2008;57:255-264.
– reference: Harkema SJ, Hurley SL, Patel UK, Requejo PS, Dobkin BH, Edgerton VR. Human lumbosacral spinal cord interprets loading during stepping. J Neurophysiol 1997;77:797-811.
– reference: Holsheimer J. Which neuronal elements are activated directly by spinal cord stimulation. Neuromodulation 2002;5:25-31.
– reference: Ladenbauer J, Minassian K, Hofstoetter US, Dimitrijevic MR, Rattay F. Stimulation of the human lumbar spinal cord with implanted and surface electrodes: a computer simulation study. IEEE Trans Neural Syst Rehabil Eng 2010;18:637-645.
– reference: Harkema S, Gerasimenko Y, Hodes J, et al. Effect of epidural stimulation of the lumbosacral spinal cord on voluntary movement, standing, and assisted stepping after motor complete paraplegia: a case study. Lancet 2011;377:1938-1947.
– reference: Barolat G, Myklebust JB, Wenninger W. Enhancement of voluntary motor function following spinal cord stimulation-case study. Appl Neurophysiol 1986;49:307-314.
– reference: Minassian K, Persy I, Rattay F, Pinter MM, Kern H, Dimitrijevic MR. Human lumbar cord circuitries can be activated by extrinsic tonic input to generate locomotor-like activity. Hum Mov Sci 2007;26:275-295.
– reference: Rattay F, Minassian K, Dimitrijevic MR. Epidural electrical stimulation of posterior structures of the human lumbosacral cord: 2. quantitative analysis by computer modeling. Spinal Cord 2000;38:473-489.
– reference: Barolat G, Massaro F, He J, Zeme S, Ketcik B. Mapping of sensory responses to epidural stimulation of the intraspinal neural structures in man. J Neurosurg 1993;78:233-239.
– reference: Huang H, He J, Herman R, Carhart MR. Modulation effects of epidural spinal cord stimulation on muscle activities during walking. IEEE Trans Neural Syst Rehabil Eng 2006;14:14-23.
– reference: Roy FD, Gibson G, Stein RB. Effect of percutaneous stimulation at different spinal levels on the activation of sensory and motor roots. Exp Brain Res 2012;223:281-289.
– reference: Minassian K, Jilge B, Rattay F, et al. Stepping-like movements in humans with complete spinal cord injury induced by epidural stimulation of the lumbar cord: electromyographic study of compound muscle action potentials. Spinal Cord 2004;42:401-416.
– reference: Lloyd DCP. Reflex action in relation to pattern and peripheral source of afferent stimulation. J Neurophysiol 1943;6:111-120.
– reference: Wernig A, Müller S. Laufband locomotion with body weight support improved walking in persons with severe spinal cord injuries. Paraplegia 1992;30:229-238.
– reference: Minassian K, Persy I, Rattay F, Dimitrijevic MR. Effect of peripheral afferent and central afferent input to the human lumbar spinal cord isolated from brain control. Biocybernetics Biomed Eng 2005;25:11-29.
– reference: Hofstoetter US, McKay WB, Tansey KE, Mayr W, Kern H, Minassian K. Modification of spasticity by transcutaneous spinal cord stimulation in individuals with incomplete spinal cord injury. J Spinal Cord Med 2014;37:202-211.
– reference: Minassian K, Persy I, Rattay F, Dimitrijevic MR, Hofer C, Kern H. Posterior root-muscle reflexes elicited by transcutaneous stimulation of the human lumbosacral cord. Muscle Nerve 2007;35:327-336.
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– reference: Pinter MM, Gerstenbrand F, Dimitrijevic MR. Epidural electrical stimulation of posterior structures of the human lumbosacral cord: 3. Control of spasticity. Spinal Cord 2000;38:524-531.
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Snippet The level of sustainable excitability within lumbar spinal cord circuitries is one of the factors determining the functional outcome of locomotor therapy after...
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SubjectTerms Adult
Biomechanical Phenomena
Electromyography
Female
Gait - physiology
Human
Humans
Locomotor training
Lumbosacral Region
Male
Muscle, Skeletal - physiopathology
Neuromodulation
Spinal Cord - physiopathology
Spinal Cord Injuries - therapy
Spinal cord injury
Spinal Cord Stimulation
Transcutaneous spinal cord stimulation
Walking - physiology
Title Augmentation of Voluntary Locomotor Activity by Transcutaneous Spinal Cord Stimulation in Motor-Incomplete Spinal Cord-Injured Individuals
URI https://api.istex.fr/ark:/67375/WNG-N1X3ZNN4-C/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Faor.12615
https://www.ncbi.nlm.nih.gov/pubmed/26450344
https://www.proquest.com/docview/1722353060
https://www.proquest.com/docview/1722928499
Volume 39
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