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Epidural and Transcutaneous Spinal Cord Stimulation Strategies for Motor Recovery After Spinal Cord Injury

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Neuroprosthetics and Brain-Computer Interfaces in Spinal Cord Injury

Abstract

Recent studies combining spinal cord stimulation (SCS) with intense neurorehabilitation training have demonstrated unprecedented improvements of motor function in individuals with chronic, severe spinal cord injury (SCI). Invasive and non-invasive methods for SCS have emerged, all with the goal to augment functional activity of spared spinal circuits distal to the lesion. Here we provide background information on the development and function of these SCS techniques and give a detailed and critical view on contemporary studies that have shaped a new era of neurorehabilitation in SCI. Epidural lumbar SCS using conventional technology has enabled intentional movement of paralyzed legs, standing, and overground stepping with training when SCS was applied and participants actively contributed. A novel strategy of spatiotemporal epidural SCS interfaced with leg-kinematic feedback has induced unparalleled recovery of motor function lasting even without stimulation. Skin-surface electrode based methods for non-invasive lumbar SCS, with conventional or Russian currents, have produced qualitatively similar improvements like those seen with epidural stimulation. Early studies of cervical SCS in tetraplegic patients found augmented upper extremity motor function and increased grip strength. Together, these neuromodulation therapies provide various perspectives for recovery of motor function in chronic patients in whom limited improvement is expected with standard-of-care rehabilitative options.

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References

  • Al’joboori Y, Massey S, Donaldson N, Duffell L (2018) Frequency dependent facilitation of motor evoked potentials with transcutaneous spinal stimulation. Abstract book, 22. Annual conference of the international functional electrical society. Nottwil, p 78–81

    Google Scholar 

  • Anderson KD (2004) Targeting recovery: priorities of the spinal cord-injured population. J Neurotrauma 21:1371–1383

    Article  PubMed  Google Scholar 

  • Angeli CA, Edgerton VR, Gerasimenko YP, Harkema SJ (2014) Altering spinal cord excitability enables voluntary movements after chronic complete paralysis in humans. Brain 137:1394–1409

    Article  PubMed  PubMed Central  Google Scholar 

  • Angeli CA, Boakye M, Morton RA, Vogt J, Benton K, Chen Y et al (2018) Recovery of over-ground walking after chronic motor complete spinal cord injury. N Engl J Med 379:1244–1250

    Article  PubMed  Google Scholar 

  • Barolat G, Myklebust JB, Wenninger W (1986) Enhancement of voluntary motor function following spinal cord stimulation—case study. Appl Neurophysiol 49:307–314

    CAS  PubMed  Google Scholar 

  • Barolat G, Myklebust JB, Wenninger W (1988) Effects of spinal cord stimulation on spasticity and spasms secondary to myelopathy. Appl Neurophysiol 51:29–44

    CAS  PubMed  Google Scholar 

  • Barolat-Romana G, Myklebust JB, Hemmy DC, Myklebust B, Wenninger W (1985) Immediate effects of spinal cord stimulation in spinal spasticity. J Neurosurg 62:558–562

    Article  CAS  PubMed  Google Scholar 

  • Barra B, Roux C, Kaeser M, Schiavone G, Lacour SP, Bloch J et al (2018) Selective recruitment of arm motoneurons in nonhuman primates using epidural electrical stimulation of the cervical spinal cord. In: 2018 40th annual international conference of the IEEE engineering in medicine and biology society (EMBC). IEEE, pp 1424–1427

    Google Scholar 

  • Burke D (2016) Clinical uses of H reflexes of upper and lower limb muscles. Clin Neurophysiol Pract 1:9–17

    Article  PubMed  PubMed Central  Google Scholar 

  • Calvert JS, Grahn PJ, Zhao KD, Lee KH (2019) Emergence of epidural electrical stimulation to facilitate sensorimotor network functionality after spinal cord injury. Neuromodulation 22:244–252

    Article  PubMed  Google Scholar 

  • Capogrosso M, Wenger N, Raspopovic S, Musienko P, Beauparlant J, Bassi Luciani L et al (2013) A computational model for epidural electrical stimulation of spinal sensorimotor circuits. J Neurosci 33:19326–19340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Capogrosso M, Milekovic T, Borton D, Wagner F, Moraud EM, Mignardot J-B et al (2016) A brain–spine interface alleviating gait deficits after spinal cord injury in primates. Nature 539:284–288

    Article  PubMed  PubMed Central  Google Scholar 

  • Capogrosso M, Wagner FB, Gandar J, Moraud EM, Wenger N, Milekovic T et al (2018) Configuration of electrical spinal cord stimulation through real-time processing of gait kinematics. Nat Protoc 13:2031–2061

    Article  CAS  PubMed  Google Scholar 

  • Cook AW, Weinstein SP (1973) Chronic dorsal column stimulation in multiple sclerosis. Preliminary report. N Y State J Med 73:2868–2872

    CAS  PubMed  Google Scholar 

  • Courtine G, Sofroniew MV (2019) Spinal cord repair: advances in biology and technology. Nat Med 25:898–908

    Article  CAS  PubMed  Google Scholar 

  • Courtine G, Harkema SJ, Dy CJ, Gerasimenko YP, Dyhre-Poulsen P (2007) Modulation of multisegmental monosynaptic responses in a variety of leg muscles during walking and running in humans. J Physiol 582:1125–1139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Danner SM, Hofstoetter US, Ladenbauer J, Rattay F, Minassian K (2011) Can the human lumbar posterior columns be stimulated by transcutaneous spinal cord stimulation? A modeling study. Artif Organs 35:257–262

    Article  PubMed  PubMed Central  Google Scholar 

  • Danner SM, Hofstoetter US, Freundl B, Binder H, Mayr W, Rattay F et al (2015) Human spinal locomotor control is based on flexibly organized burst generators. Brain 138:577–588

    Article  PubMed  PubMed Central  Google Scholar 

  • Davis R, Gray E, Kudzma J (1981) Beneficial augmentation following dorsal column stimulation in some neurological diseases. Appl Neurophysiol 44:37–49

    CAS  PubMed  Google Scholar 

  • De Ridder D, Vanneste S, Plazier M, van der Loo E, Menovsky T (2010) Burst spinal cord stimulation: toward paresthesia-free pain suppression. Neurosurgery 66:986–990

    Article  PubMed  Google Scholar 

  • Dimitrijevic MR, Dimitrijevic MM, Faganel J, Sherwood AM (1984) Suprasegmentally induced motor unit activity in paralyzed muscles of patients with established spinal cord injury. Ann Neurol 16:216–221

    Article  CAS  PubMed  Google Scholar 

  • Dimitrijevic MM, Dimitrijevic MR, Illis LS, Nakajima K, Sharkey PC, Sherwood AM (1986) Spinal cord stimulation for the control of spasticity in patients with chronic spinal cord injury: I. clinical observations. Cent Nerv Syst trauma J Am Paralys Assoc 3:129–144

    CAS  Google Scholar 

  • Dimitrijevic MR, Gerasimenko Y, Pinter MM (1998) Evidence for a spinal central pattern generator in humans. Ann N Y Acad Sci 860:360–376

    Article  CAS  PubMed  Google Scholar 

  • Dy CJ, Gerasimenko YP, Edgerton VR, Dyhre-Poulsen P, Courtine G, Harkema SJ (2010) Phase-dependent modulation of percutaneously elicited multisegmental muscle responses after spinal cord injury. J Neurophysiol 103:2808–2820

    Article  PubMed  PubMed Central  Google Scholar 

  • Estes SP, Iddings JA, Field-Fote EC (2017) Priming neural circuits to modulate spinal reflex excitability. Front Neurol 8:17

    Article  PubMed  PubMed Central  Google Scholar 

  • Formento E, Minassian K, Wagner F, Mignardot JB, Le Goff-Mignardot CG, Rowald A et al (2018) Electrical spinal cord stimulation must preserve proprioception to enable locomotion in humans with spinal cord injury. Nat Neurosci 21:1728–1741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freyvert Y, Yong NA, Morikawa E, Zdunowski S, Sarino ME, Gerasimenko Y et al (2018) Engaging cervical spinal circuitry with non-invasive spinal stimulation and buspirone to restore hand function in chronic motor complete patients. Sci Rep 8:15546

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gad P, Gerasimenko Y, Zdunowski S, Turner A, Sayenko D, Lu DC et al (2017) Weight bearing over-ground stepping in an exoskeleton with non-invasive spinal cord neuromodulation after motor complete paraplegia. Front Neurosci 11:333

    Article  PubMed  PubMed Central  Google Scholar 

  • Gad P, Lee S, Terrafranca N, Zhong H, Turner A, Gerasimenko Y et al (2018) Non-invasive activation of cervical spinal networks after severe paralysis. J Neurotrauma 35:2145–2158

    Article  PubMed  PubMed Central  Google Scholar 

  • Gerasimenko YP, Lavrov IA, Courtine G, Ichiyama RM, Dy CJ, Zhong H et al (2006) Spinal cord reflexes induced by epidural spinal cord stimulation in normal awake rats. J Neurosci Methods 157:253–263

    Article  PubMed  Google Scholar 

  • Gerasimenko Y, Gorodnichev R, Moshonkina T, Sayenko D, Gad P, Reggie EV (2015a) Transcutaneous electrical spinal-cord stimulation in humans. Ann Phys Rehabil Med 58:225–231

    Article  PubMed  PubMed Central  Google Scholar 

  • Gerasimenko Y, Lu D, Modaber M, Zdunowski S, Gad P, Sayenko D et al (2015b) Noninvasive reactivation of motor descending control after paralysis. J Neurotrauma 32:1968–1980

    Article  PubMed  PubMed Central  Google Scholar 

  • Gildenberg P (2009) Neuromodulation: a historical perspective. In: Krames E, Peckham P, Rezai A (eds) Neuromodulation. Elsevier-Academic, London, pp 9–20

    Chapter  Google Scholar 

  • Gill ML, Grahn PJ, Calvert JS, Linde MB, Lavrov IA, Strommen JA et al (2018) Neuromodulation of lumbosacral spinal networks enables independent stepping after complete paraplegia. Nat Med 24:1677–1682

    Article  CAS  PubMed  Google Scholar 

  • Grahn PJ, Lavrov IA, Sayenko DG, Van Straaten MG, Gill ML, Strommen JA et al (2017) Enabling task-specific volitional motor functions via spinal cord neuromodulation in a human with paraplegia. Mayo Clin Proc 92:544–554

    Article  PubMed  Google Scholar 

  • Greiner N, Capogrosso M (2019) Anatomically realistic computational model to assess the specificity of epidural electrical stimulation of the cervical spinal cord. In: Masia L, Micera S, Akay M, Pons J (eds) Converging clinical and engineering research on neurorehabilitation III ICNR 2018 biosystems & biorobotics. Springer, New York, pp 44–48

    Google Scholar 

  • Guertin PA (2013) Central pattern generator for locomotion: anatomical, physiological, and pathophysiological considerations. Front Neurol 3:183

    Article  PubMed  PubMed Central  Google Scholar 

  • Harkema S, Gerasimenko Y, Hodes J, Burdick J, Angeli C, Chen Y et al (2011) Effect of epidural stimulation of the lumbosacral spinal cord on voluntary movement, standing, and assisted stepping after motor complete paraplegia: a case study. Lancet 377:1938–1947

    Article  PubMed  PubMed Central  Google Scholar 

  • Hofstoetter US, Minassian K, Hofer C, Mayr W, Rattay F, Dimitrijevic MR (2008) Modification of reflex responses to lumbar posterior root stimulation by motor tasks in healthy subjects. Artif Organs 32:644–648

    Article  PubMed  Google Scholar 

  • Hofstoetter US, Hofer C, Kern H, Danner SM, Mayr W, Dimitrijevic MR et al (2013) Effects of transcutaneous spinal cord stimulation on voluntary locomotor activity in an incomplete spinal cord injured individual. Biomed Tech 58

    Google Scholar 

  • Hofstoetter US, McKay WB, Tansey KE, Mayr W, Kern H, Minassian K (2014) Modification of spasticity by transcutaneous spinal cord stimulation in individuals with incomplete spinal cord injury. J Spinal Cord Med 37:202–211

    Article  PubMed  PubMed Central  Google Scholar 

  • Hofstoetter US, Danner SM, Freundl B, Binder H, Mayr W, Rattay F et al (2015a) Periodic modulation of repetitively elicited monosynaptic reflexes of the human lumbosacral spinal cord. J Neurophysiol 114:400–410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hofstoetter US, Danner SM, Minassian K (2015b) Paraspinal magnetic and transcutaneous electrical stimulation. In: Jaeger D, Jung R (eds) Encyclopedia of computational neuroscience. Springer, New York, pp 2194–2212

    Google Scholar 

  • Hofstoetter US, Krenn M, Danner SM, Hofer C, Kern H, McKay WB et al (2015c) Augmentation of voluntary locomotor activity by transcutaneous spinal cord stimulation in motor-incomplete spinal cord-injured individuals. Artif Organs 39:E176–E186

    Article  PubMed  Google Scholar 

  • Hofstoetter US, Knikou M, Guertin PA, Minassian K (2017) Probing the human spinal locomotor circuits by phasic step-induced feedback and by tonic electrical and pharmacological neuromodulation. Curr Pharm Des 23:1805–1820

    Article  CAS  PubMed  Google Scholar 

  • Hofstoetter US, Freundl B, Binder H, Minassian K (2018) Common neural structures activated by epidural and transcutaneous lumbar spinal cord stimulation: elicitation of posterior root-muscle reflexes. PLoS One 13:e0192013

    Google Scholar 

  • Hofstoetter U, Freundl B, Danner S, Krenn M, Mayr W, Binder H et al (2020) Transcutaneous spinal cord stimulation induces temporary attenuation of spasticity in individuals with spinal cord injury. J Neurotrauma 37:481–493

    Google Scholar 

  • Illis LS, Oygar AE, Sedgwick EM, Awadalla MA (1976) Dorsal-column stimulation in the rehabilitation of patients with multiple sclerosis. Lancet 1:1383–1386

    Article  CAS  PubMed  Google Scholar 

  • Illis LS, Sedgwick EM, Tallis RC (1980) Spinal cord stimulation in multiple sclerosis: clinical results. J Neurol Neurosurg Psychiatry 43:1–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Illis LS, Read DJ, Sedgwick EM, Tallis RC (1983) Spinal cord stimulation in the United Kingdom. J Neurol Neurosurg Psychiatry 46:299–304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inanici F, Samejima S, Gad P, Edgerton VR, Hofstetter CP, Moritz CT (2018) Transcutaneous electrical spinal stimulation promotes long-term recovery of upper extremity function in chronic tetraplegia. IEEE Trans Neural Syst Rehabil Eng 26:1272–1278

    Article  PubMed  PubMed Central  Google Scholar 

  • Jilge B, Minassian K, Rattay F, Pinter MM, Gerstenbrand F, Binder H et al (2004) Initiating extension of the lower limbs in subjects with complete spinal cord injury by epidural lumbar cord stimulation. Exp Brain Res 154:308–326

    Article  CAS  PubMed  Google Scholar 

  • Kakulas A (1988) The applied neurobiology of human spinal cord injury: a review. Paraplegia 26:371–379

    CAS  PubMed  Google Scholar 

  • Kapural L, Yu C, Doust MW, Gliner BE, Vallejo R, Sitzman BT et al (2015) Novel 10-kHz high-frequency therapy (HF10 therapy) is superior to traditional low-frequency spinal cord stimulation for the treatment of chronic Back and leg pain. Anesthesiology 123:851–860

    Article  PubMed  Google Scholar 

  • Krames E, Rezai A, Peckham P, Aboelsaad F (2009) What is neuromodulation? In: Krames E, Peckham P, Rezai A (eds) Neuromodulation. Elsevier-Academic Press, London, pp 3–8

    Chapter  Google Scholar 

  • Ladenbauer J, Minassian K, Hofstoetter US, Dimitrijevic MR, Rattay F (2010) Stimulation of the human lumbar spinal cord with implanted and surface electrodes: a computer simulation study. IEEE Trans Neural Syst Rehabil Eng 18:637–645

    Article  PubMed  Google Scholar 

  • Lu DC, Edgerton VR, Modaber M, AuYong N, Morikawa E, Zdunowski S et al (2016) Engaging cervical spinal cord networks to Reenable volitional control of hand function in tetraplegic patients. Neurorehabil Neural Repair 30:951–962

    Article  PubMed  PubMed Central  Google Scholar 

  • Maertens de Noordhout A, Rothwell JC, Thompson PD, Day BL, Marsden CD (1988) Percutaneous electrical stimulation of lumbosacral roots in man. J Neurol Neurosurg Psychiatry 51:174–181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maynard FM, Karunas RS, Waring WP (1990) Epidemiology of spasticity following traumatic spinal cord injury. Arch Phys Med Rehabil 71:566–569

    CAS  PubMed  Google Scholar 

  • McCrimmon CM, Wang PT, Heydari P, Nguyen A, Shaw SJ, Gong H et al (2018) Electrocorticographic encoding of human gait in the leg primary motor cortex. Cereb Cortex 28:2752–2762

    Article  PubMed  Google Scholar 

  • Melzack R, Wall PD (1965) Pain mechanisms: a new theory. Science 150:971–979

    Article  CAS  PubMed  Google Scholar 

  • Milosevic M, Masugi Y, Sasaki A, Sayenko DG, Nakazawa K (2019) On the reflex mechanisms of cervical transcutaneous spinal cord stimulation in human subjects. J Neurophysiol 121:1672–1679

    Article  PubMed  Google Scholar 

  • Minassian K, Hofstoetter US (2016) Spinal cord stimulation and augmentative control strategies for leg movement after spinal paralysis in humans. CNS Neurosci Ther 22:262–270

    Article  PubMed  PubMed Central  Google Scholar 

  • Minassian K, Jilge B, Rattay F, Pinter MM, Binder H, Gerstenbrand F et al (2004) 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 42:401–416

    Article  CAS  PubMed  Google Scholar 

  • Minassian K, Persy I, Rattay F, Pinter MM, Kern H, Dimitrijevic MR (2007a) Human lumbar cord circuitries can be activated by extrinsic tonic input to generate locomotor-like activity. Hum Mov Sci 26:275–295

    Article  CAS  PubMed  Google Scholar 

  • Minassian K, Persy I, Rattay F, Dimitrijevic MR, Hofer C, Kern H (2007b) Posterior root-muscle reflexes elicited by transcutaneous stimulation of the human lumbosacral cord. Muscle Nerve 35:327–336

    Article  PubMed  Google Scholar 

  • Minassian K, Hofstoetter U, Tansey K, Rattay F, Mayr W, Dimitrijevic M (2010) Transcutaneous stimulation of the human lumbar spinal cord: facilitating locomotor output in spinal cord injury. Neuroscience Meeting Planner. San Diego, 2010. Program No 286.19

    Google Scholar 

  • Minassian K, Hofstoetter U, Rattay F (2011) Transcutaneous lumbar posterior root stimulation for motor control studies and modification of motor activity after spinal cord injury. In: Dimitrijevic M, Kakulas B, McKay W (eds) Restorative neurology in spinal cord injury. Oxford University Press, New York, pp 226–255

    Chapter  Google Scholar 

  • Minassian K, Hofstoetter U, Tansey K, Mayr W (2012) Neuromodulation of lower limb motor control in restorative neurology. Clin Neurol Neurosurg 114:489–497

    Article  PubMed  PubMed Central  Google Scholar 

  • Minassian K, McKay WB, Binder H, Hofstoetter US (2016a) Targeting lumbar spinal neural circuitry by epidural stimulation to restore motor function after spinal cord injury. Neurotherapeutics 13:284–294

    Article  PubMed  PubMed Central  Google Scholar 

  • Minassian K, Hofstoetter US, Danner SM, Mayr W, Bruce JA, McKay WB et al (2016b) Spinal rhythm generation by step-induced feedback and transcutaneous posterior root stimulation in complete spinal cord-injured individuals. Neurorehabil Neural Repair 30:233–243

    Article  PubMed  Google Scholar 

  • Minassian K, Hofstoetter US, Dzeladini F, Guertin PA, Ijspeert A (2017) The human central pattern generator for locomotion: does it exist and contribute to walking? Neurosci 23:649–663

    Google Scholar 

  • Moraud EM, Capogrosso M, Formento E, Wenger N, DiGiovanna J, Courtine G et al (2016) Mechanisms underlying the neuromodulation of spinal circuits for correcting gait and balance deficits after spinal cord injury. Neuron 89:814–828

    Article  CAS  PubMed  Google Scholar 

  • Murg M, Binder H, Dimitrijevic MR (2000) Epidural electric stimulation of posterior structures of the human lumbar spinal cord: 1. Muscle twitches - a functional method to define the site of stimulation. Spinal Cord 38:394–402

    Article  CAS  PubMed  Google Scholar 

  • Nagel SJ, Wilson S, Johnson MD, Machado A, Frizon L, Chardon MK et al (2017) Spinal cord stimulation for spasticity: historical approaches, current status, and future directions. Neuromodulation 20:307–321

    Article  PubMed  Google Scholar 

  • Nielsen J, Willerslev-Olsen M, Lorentzen J (2018) Pathophysiology of spasticity. In: Pandyan A, Hermens H, Conway B (eds) Neurological rehabilitation spasticity and contractures in clinical practice and research. CRC, Boca Raton, pp 25–57

    Chapter  Google Scholar 

  • Pinter MM, Gerstenbrand F, Dimitrijevic MR (2000) Epidural electrical stimulation of posterior structures of the human lumbosacral cord: 3. Control of spasticity. Spinal Cord 38:524–531

    Article  CAS  PubMed  Google Scholar 

  • Rattay F, Minassian K, Dimitrijevic MR (2000) Epidural electrical stimulation of posterior structures of the human lumbosacral cord: 2. Quantitative analysis by computer modeling. Spinal Cord 38:473–489

    Article  CAS  PubMed  Google Scholar 

  • Rejc E, Angeli C, Harkema S (2015) Effects of lumbosacral spinal cord epidural stimulation for standing after chronic complete paralysis in humans. PLoS One 10:e0133998

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rejc E, Angeli CA, Atkinson D, Harkema SJ (2017) Motor recovery after activity-based training with spinal cord epidural stimulation in a chronic motor complete paraplegic. Sci Rep 7:13476

    Article  PubMed  PubMed Central  Google Scholar 

  • Richardson RR, McLone DG (1978) Percutaneous epidural neurostimulation for paraplegic spasticity. Surg Neurol 9:153–155

    CAS  PubMed  Google Scholar 

  • Richardson RR, Cerullo LJ, McLone DG, Gutierrez FA, Lewis V (1979a) Percutaneous epidural neurostimulation in modulation of paraplegic spasticity. Six case reports. Acta Neurochir 49:235–243

    Article  CAS  PubMed  Google Scholar 

  • Richardson RR, Cerullo LJ, Meyer PR (1979b) Autonomic hyper-reflexia modulated by percutaneous epidural neurostimulation: a preliminary report. Neurosurgery 4:517–520

    Article  CAS  PubMed  Google Scholar 

  • Roy FD, Gibson G, Stein RB (2012) Effect of percutaneous stimulation at different spinal levels on the activation of sensory and motor roots. Exp Brain Res 223:281–289

    Article  PubMed  Google Scholar 

  • Sayenko DG, Angeli C, Harkema SJ, Edgerton VR, Gerasimenko YP (2014) Neuromodulation of evoked muscle potentials induced by epidural spinal-cord stimulation in paralyzed individuals. J Neurophysiol 111:1088–1099

    Article  PubMed  Google Scholar 

  • Sayenko DG, Rath M, Ferguson AR, Burdick JW, Havton LA, Edgerton VR et al (2019) Self-assisted standing enabled by non-invasive spinal stimulation after spinal cord injury. J Neurotrauma 36:1435–1450

    Article  PubMed  PubMed Central  Google Scholar 

  • Shealy CN, Mortimer JT, Reswick JB (1967) Electrical inhibition of pain by stimulation of the dorsal columns: preliminary clinical report. Anesth Analg 46:489–491

    Article  CAS  PubMed  Google Scholar 

  • Siegfried J, Lazorthes Y, Broggi G (1981) Electrical spinal cord stimulation for spastic movement disorders. Appl Neurophysiol 44:77–92

    CAS  PubMed  Google Scholar 

  • Tator CH, Minassian K, Mushahwar VK (2012) Spinal cord stimulation. Handb Clin Neurol 109:283–296

    Article  PubMed  Google Scholar 

  • Troni W, Bianco C, Moja MC, Dotta M (1996) Improved methodology for lumbosacral nerve root stimulation. Muscle Nerve 19:595–604

    Article  CAS  PubMed  Google Scholar 

  • Vansteensel MJ, Pels EGM, Bleichner MG, Branco MP, Denison T, Freudenburg ZV et al (2016) Fully implanted brain–computer Interface in a locked-in patient with ALS. N Engl J Med 375:2060–2066

    Article  PubMed  PubMed Central  Google Scholar 

  • Wagner FB, Mignardot J-B, Le Goff-Mignardot CG, Demesmaeker R, Komi S, Capogrosso M et al (2018) Targeted neurotechnology restores walking in humans with spinal cord injury. Nature 563:65–71

    Article  CAS  PubMed  Google Scholar 

  • Waltz JM (1997) Spinal cord stimulation: a quarter century of development and investigation. A review of its development and effectiveness in 1,336 cases. Stereotact Funct Neurosurg 69:288–299

    Article  CAS  PubMed  Google Scholar 

  • Wenger N, Moraud EM, Raspopovic S, Bonizzato M, DiGiovanna J, Musienko P et al (2014) Closed-loop neuromodulation of spinal sensorimotor circuits controls refined locomotion after complete spinal cord injury. Sci Transl Med 6:255ra133

    Article  PubMed  CAS  Google Scholar 

  • Wenger N, Moraud EM, Gandar J, Musienko P, Capogrosso M, Baud L et al (2016) Spatiotemporal neuromodulation therapies engaging muscle synergies improve motor control after spinal cord injury. Nat Med 22:138–145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Starr A, Haldeman S, Chu JK, Sugerman RA (1998) Soleus H-reflex to S1 nerve root stimulation. Electroencephalogr Clin Neurophysiol 109:10–14

    Article  CAS  PubMed  Google Scholar 

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Minassian, K., Perret, I., Hofstoetter, U.S. (2021). Epidural and Transcutaneous Spinal Cord Stimulation Strategies for Motor Recovery After Spinal Cord Injury. In: Müller-Putz, G., Rupp, R. (eds) Neuroprosthetics and Brain-Computer Interfaces in Spinal Cord Injury. Springer, Cham. https://doi.org/10.1007/978-3-030-68545-4_7

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