Neurorehabilitation Based on Spinal Cord Stimulation and Motor Training

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Abstract

—The review presents recent data on the recovery of motor functions after spinal injuries: on spontaneous neuroplasticity; about plasticity, depending on physical activity; about the results of using epidural and transcutaneous electrical stimulation of the spinal cord to restore movement control; on neurophysiological changes and mechanisms initiated by spinal electrical stimulation that may contribute to functional recovery after spinal cord injury.

About the authors

Y. K. Stolbkov

Pavlov Institute of Physiology of Russian Academy of Sciences

Author for correspondence.
Email: stolbkovyk@infran.ru
Russia, 199034, St.-Petersburg

Yu. P. Gerasimenko

Pavlov Institute of Physiology of Russian Academy of Sciences

Author for correspondence.
Email: gerasimenko@infran.ru
Russia, 199034, St.-Petersburg

References

  1. Виссарионов С.В., Солохина И.Ю., Икоева Г.А. и др. Двигательная реабилитация пациента с последствиями позвоночно-спинномозговой травмы методом неинвазивной электростимуляции спинного мозга в сочетании с механотерапией // Хирургия позвоночника. 2016. Т. 13. № 1. С. 8–12.
  2. Городничев Р.М., Пивоварова Е.А., Пухов А. и др. Чрескожная электрическая стимуляция спинного мозга: нвазивный способ активации генераторов шагательных движений у человека // Физиология человека. 2012. Т. 38. № 2. С. 46–56.
  3. Минаков А.Н., Чернов А.С., Асютин Д.С. и др. Экспериментальное моделирование травмы спинного мозга у лабораторных крыс // Acta Naturae. 2018. Т. 10. № 3(38). С. 4–10.
  4. Новосёлова И.Н. Этиология и клиническая эпидемиология позвоночно-спинномозговой травмы (литературный обзор) // Российский нейрохирургический журн. им. профессора А.Л. Поленова. 2019. Т. 11. № 4. С. 84–92.
  5. Павлов К.И., Мухин В.Н. Физиологические механизмы нейропластичности как основа психических процессов и социально-профессиональной адаптации (часть 1) // Психология. Психофизиология. 2021. Т. 14. № 3. С. 119–136.
  6. Прудникова О.Г., Качесова А.А., Рябых С.О. Реабилитация пациентов в отдаленном периоде травмы спинного мозга: метаанализ литературных данных // Хирургия позвоночника. 2019. Т. 16. № 3. С. 8–16.
  7. Смирнов В.А., Гринь А.А. Регенеративные методы лечения травмы спинного мозга. Обзор литературы. Часть 4 // Нейрохирургия. 2020. Т. 22. № 1. С. 83–92.
  8. Abualait T.S., Ibrahim A.I. Spinal direct current stimulation with locomotor training in chronic spinal cord injury // Saudi. Med. J. 2020. V. 41. P. 88–93.
  9. Al’joboori Y.D., Edgerton V.R., Ichiyama R.M. Effects of rehabilitation on perineural nets and synaptic plasticity following spinal cord transaction // Brain Sci. 2020. V. 10. Article 824.
  10. Alam M., Ling Y.T., Wong A.Y. et al. Reversing 21 years of chronic paralysis via non-invasive spinal cord neuromodulation: a case study // Ann. Clin. Transl. Neurol. 2020. V. 7. P. 829–838.
  11. Angeli C.A., Boakye M., Morton R.A. et al. Recovery of over-ground walking after chronic motor complete spinal cord injury // N. Engl. J. Med. 2018. V. 379. P. 1244–1250.
  12. Angeli C.A., Edgerton V.R., Gerasimenko Y.P., Harkema S.J. Altering spinal cord excitability enables voluntary movements after chronic complete paralysis in humans // Brain. 2014. V. 137. P. 1394-409.
  13. Angeli C.A., Gerasimenko Y. Combined cervical transcutaneous with lumbosacral epidural stimulation improves voluntary control of stepping movements in spinal cord injured individuals// Front. Bioeng. Biotechnol. 2023. V. 11. Article 1073716.
  14. Asboth L., Friedli L., Beauparlant J. et al. Cortico–reticulo–spinal circuit reorganization enables functional recovery after severe spinal cord contusion // Nat. Neurosci. 2018. V. 21. № 4. P. 576–88.
  15. Barss T.S., Parhizi B., Mushahwar V.K. Transcutaneous spinal cord stimulation of the cervical cord modulates lumbar networks // J. Neurophysiol. 2020. V. 123. P. 158–166.
  16. Beck L., Veith D., Linde M. et al. Impact of long-term epidural electrical stimulation enabled task-specific training on secondary conditions of chronic paraplegia in two humans // J. Spinal Cord Med. 2021. V. 44. P. 800–805.
  17. Behrman A.L., Argetsinger L.C., Roberts M.T. et al. Activity-based therapy targeting neuromuscular capacity after pediatric-onset spinal cord injury //Top. Spinal Cord. Inj. Rehabil. 2019. V. 25. №. 2. P. 132-149.
  18. Benavides F.D., Jo H.J., Lundell H. et al. Cortical and subcortical effects of transcutaneous spinal cord stimulation in humans with tetraplegia // J. Neurosci. 2020. V. 40. P. 2633–2643.
  19. Beverungen H., Klaszky S.C., Klaszky M., Côté M.P. Rehabilitation decreases spasticity by restoring chloride homeostasis through the brain-derived neurotrophic factor-KCC2 pathway after spinal cord injury // J. Neurotrauma. 2020. V. 37. P. 846–859.
  20. Bilchak J.N., Caron G., Côté M.P. Exercise-induced plasticity in signaling pathways involved in motor recovery after spinal cord injury // Int. J. Mol. Sci. 2021. V. 22. № 9. Article 4858.
  21. Brown A.R., Martinez M. From cortex to cord: motor circuit plasticity after spinal cord injury // Neural Regen. Res. 2019. V. 14. № 12. P. 2054–2062.
  22. Burns A.S., Marino R.J., Kalsi-Ryan S. et al. Type and timing of rehabilitation following acute and subacute spinal cord injury: a systematic review // Glob. Spine J. 2017. V. 7. P. 175s–194s.
  23. Côté M.P., Murray M., Lemay M.A. Rehabilitation strategies after spinal cord injury: inquiry into the mechanisms of success and failure // J. Neurotrauma. 2017. V. 34. № 10. P.1841–1857.
  24. Courtine G., Gerasimenko Y., van den Brand R. et al. Transformation of nonfunctional spinal circuits into functional states after the loss of brain input // Nat. Neurosci. 2009. V. 12. № 10. P. 1333–42.
  25. Courtine G., Sofroniew M.V. Spinal cord repair: advances in biology and technology // Nat. Med. 2019. V. 25. P. 898–908.
  26. Darrow D., Balser D., Netoff T.I. et al. Epidural spinal cord stimulation facilitates immediate restoration of dormantmotor and autonomic supraspinal pathways after chronic neurologically complete spinal cord injury // J. Neurotrauma. 2019. V. 36. P. 2325–2336.
  27. de Freitas R.M., Sasaki A., Sayenko D.G. et al. Selectivity and excitability of upper-limb muscle activation during cervical transcutaneous spinal cord stimulation in humans // J. Appl. Physiol. 2021. P. 131. № 2. P. 746–59.
  28. Diaz-Rıos M., Guertin P.A., Rivera-Oliver M. Neuromodulation of spinal locomotor networks in rodents // Curr. Pharm. Des. 2017. V. 23. P. 1741–1752.
  29. DiMarco A.F., Geertman R.T., Tabbaa K. et al. Effects of lower thoracic spinal cord stimulation on bowel management in individuals with spinal cord injury // Arch. Phys. Med. Rehabil. 2021. V. 102. P. 1155–1164.
  30. Dimitrijevic M.R., Gerasimenko Y., Pinter M.M. Evidence for Spinal Central Pattern Generator in Humans // Annals of the New York Academy of Sciences. 1998. V. 860. P. 360–376.
  31. Dimitrijevic M.R., Kakulas B.A. Spinal cord injuries, human neuropathology and neurophysiology // Acta Myol. 2020. V. 39. № 4. P. 353–358.
  32. Estes S., Zarkou A., Hope J.M. et al. Combined transcutaneous spinal stimulation and locomotor training to improve walking function and reduce spasticity in subacute spinal cord injury: a randomized study of clinical feasibility and efficacy // J. Clin. Med. 2021. V. 10. Article 1167.
  33. Evans R.W., Shackleton C.L., West S. et al. Robotic locomotor training leads to cardiovascular changes in individuals with incomplete spinal cord injury over a 24-week rehabilitation period: a randomized controlled pilot study // Arch. Phys. Med. Rehabil. 2021. V. 102. P. 1447–1456.
  34. Filipp M.E., Travis B.J., Henry S.S. et al. Differences in neuroplasticity after spinal cord injury in varying animal models and humans // Neural. Regen. Res. 2019. V. 14. P. 7–19.
  35. Freyvert Y., Yong N.A., Morikawa E. et al. Engaging cervical spinal circuitry with non-invasive spinal stimulation and buspirone to restore hand function in chronic motor complete patients // Sci. Rep. 2018. V. 8. Article 15546.
  36. Gad P., Gerasimenko Y., Zdunowski S. et al. Weight bearing over-ground stepping in an exoskeleton with non-invasive spinal cord neuromodulation after motor complete paraplegia // Front. Neurosci. 2017. V. 11. Article 333.
  37. Gallegos C., Carey M., Zheng Y. et al. Reaching and grasping training improves functional recovery after chronic cervical spinal cord injury // Front. Cell Neurosci. 2020. V. 14. Article 110.
  38. Gerasimenko Y., Gorodnichev R., Moshonkina T. et al. Transcutaneous electrical spinal-cord stimulation in humans // Ann. Phys. Rehabil. Med. 2015. V. 58. № 4. P. 225–231.
  39. Gerasimenko Y., Moshonkina T., Savochin A. et al. Initiation and modulation of locomotor circuitry output with multisite transcutaneous electrical stimulation of the spinal cord in noninjured humans // J. Neurophysiol. 2015. V. 113. № 3. P. 834–842.
  40. Gerasimenko Y., Daniel O., Regnaux J. et al. Mechanisms of locomotor activity generation under epidural spinal cord stimulation //NATO Science Series Sub Series I Life and Behavioural Sciences. 2001. V. 326. P. 164–171.
  41. Gerasimenko Y.P., Lu D.C., Modaber M. et al. Noninvasive reactivation of motor descending control after paralysis // Neurotrauma. 2015. V. 32. № 24. P. 1968–1980.
  42. Gill M.L., Grahn P.J., Calvert J.S. et al. Neuromodulation of lumbosacral spinal networks enables independent stepping after complete paraplegia // Nat. Med. 2018. V. 24. P. 1677–1682.
  43. Gill M.L., Linde M.B., Hale R.F. et al. Alterations of spinal epidural stimulationenabled stepping by descending intentional motor commands and proprioceptive inputs in humans with spinal cord injury // Front. Syst. Neurosci. 2021. V. 14. Article 590231.
  44. Goldhardt M.G., Andreia A., Dorneles G.P. et al. Does a single bout of exercise impacts BDNF, oxidative stress and epigenetic markers in spinal cord injury patients? // Funct. Neurol. 2019. V. 34. P. 158–166.
  45. Greiner N., Barra B., Schiavone G. et al. Recruitment of upper-limb motoneurons with epidural electrical stimulation of the cervical spinal cord // Nat. Commun. 2021. V. 12. Article 435.
  46. Guiho T., Baker S.N., Jackson A. Epidural and transcutaneous spinal cord stimulation facilitates descending inputs to upper-limb motoneurons in monkeys // J. Neural. Eng. 2021. V. 18. № 4. Article 046011.
  47. Harkema S., Angeli C., Gerasimenko Y. Historical development and contemporary use of neuromodulation in human spinal cord injury // Curr. Opin. Neurol. 2022. V. 35. № 4. P. 536–543.
  48. 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. V. 377. P. 1938–1947.
  49. Harkema S., Hillyer J., Schmidt-Read M. et al. Locomotor training: as a treatment of spinal cord injury and in the progression of neurologic rehabilitation //Arch. Phys. Med. Rehabil. 2012. V. 93. № 9. P. 1588–97.
  50. Harmsen I.E., Hasanova D., Elias G.J. et al. Trends in clinical trials for spinal cord stimulation // Stereotact. Funct. Neurosurg. 2021. V. 99. P. 123–134.
  51. Herman R., He J., D’Luzansky S. et al. Spinal cord stimulation facilitates functional walking in a chronic, incomplete spinal cord injured // Spinal Cord. 2002. V. 40. P. 65–68.
  52. Hilton B.J., Tetzlaff W. A brainstem bypass for spinal cord injury // Nat. Neurosci. 2018. V. 21. P. 457–458.
  53. Hofer A.S., Schwab M.E. Enhancing rehabilitation and functional recovery after brain and spinal cord trauma with electrical neuromodulation // Curr. Opin. Neurol. 2019. V. 32. № 6. P. 828–835.
  54. Hofstoetter U.S., Freundl B., Binder H., Minassian K. Common neural structures activated by epidural and transcutaneous lumbar spinal cord stimulation: Elicitation of posterior root-muscle reflexes // PloS One. 2018. V. 13. № 1. P. e0192013-e0192013
  55. Imai T., Katoh H., Suyama K. et al. Amiloride promotes oligodendrocyte survival and remyelination after spinal cord injury in rats // J. Clin. Med. 2018. V. 7. № 3. Article 46.
  56. Inanici F., Brighton L.N., Samejima S. et al. Transcutaneous spinal cord stimulation restores hand and arm function after spinal cord injury // IEEE Trans. Neural. Syst. Rehabil. Eng. 2021. V. 29. P. 310–319.
  57. Inanici F., Samejima S., Gad P. et al. Transcutaneous electrical spinal stimulation promotes long-term recovery of upper extremity function in chronic tetraplegia // IEEE Trans. Neural. Syst. Rehab. Eng. 2018. V. 26. P. 1272–1278.
  58. James N.D., McMahon S.B., Field-Fote E.C., Bradbury E.J. Neuromodulation in the restoration of function after spinal cord injury // Lancet. Neurology. 2018. V. 17. P. 905–917.
  59. Jankowska E., Hammar I. The plasticity of nerve fibers: the prolonged effects of polarization of afferent fibers // J. Neurophysiol. 2021. V. 126. P. 1568–1591.
  60. Khalki L., Sadlaoud K., Lerond J. et al. Changes in innervation of lumbar motoneurons and organization of premotor network following training of transected adult rats // Exp. Neurol. 2018. V. 299. P. 1–14.
  61. Knikou M., Murray L.M. Repeated transspinal stimulation decreases soleus H-reflex excitability and restores spinal inhibition in human spinal cord injury // PLoS One. 2019. V. 14. № 9. Article e0223135.
  62. Leech K.A., Hornby T.G. High-intensity locomotor exercise increases brain-derived neurotrophic factor in individuals with incomplete spinal cord injury // J. Neurotrauma. 2017. V. 34. P. 1240–1248.
  63. Li X., Wang Q., Ding J. et al. Exercise training modulates glutamic acid decarboxylase-65/67 expression through TrkB signaling to ameliorate neuropathic pain in rats with spinal cord injury // Mol. Pain. 2020. V. 16. P. 1–12.
  64. Li X., Wu Q., Xie C. et al. Blocking of BDNF-TrkB signaling inhibits the promotion effect of neurological function recovery after treadmill training in rats with spinal cord injury // Spinal Cord. 2019. V. 57. P. 65–74.
  65. Li G., Fan Z.K., Gu G.F. et al. Epidural spinal cord stimulation promotes motor functional recovery by enhancing oligodendrocyte survival and differentiation and by protecting myelin after spinal cord injury in rats // Neurosci. Bull. 2020. V. 36. P. 372–384.
  66. Loy K., Bareyre F.M. Rehabilitation following spinal cord injury: how animal models can help our understanding of exercise-induced neuroplasticity // Neural. Regen. Res. 2019. V. 14. P. 405–412.
  67. Loy K., Schmalz A., Hoche T. et al. Enhanced voluntary exercise improves functional recovery following spinal cord injury by impacting the local neuroglial injury response and supporting the rewiring of supraspinal circuits // J. Neurotrauma. 2018. V. 35. P. 2904–2915.
  68. Lu D.C., Edgerton V.R. Modaber M. et al. Engaging cervical spinal cord networks to reenable volitional control of hand function in tetraplegic patients // Neurorehabilit. Neural Repair. 2016. V. 30. № 10. P. 951–962.
  69. Manson G., Atkinson D.A., Shi Z. et al. Transcutaneous spinal stimulation alters cortical and subcortical activation patterns during mimicked-standing: A proof-of-concept fMRI study //Neuroimage Rep. 2022. V. 2. № 2. Article 100090.
  70. Manson G.A., Calvert J.S., Ling J. et al. The relationship between maximum tolerance and motor activation during transcutaneous spinal stimulation is unaffected by the carrier frequency or vibration // Phys. Rep. 2020. V. 8. Article e14397.
  71. McHugh L.V., Miller A.A., Leech K.A. et al. Feasibility and utility of transcutaneous spinal cord stimulation combined with walking-based therapy for people with motor incomplete spinal cord injury // Spinal Cord. Ser. Cases. 2020. V. 6. Article 104.
  72. Mesbah S., Gonnelli F., Angeli C.A. et al. Neurophysiological markers predicting recovery of standing in humans with chronic motor complete spinal cord injury // Sci. Rep. 2019. V. 9.Article 14474.
  73. Minassian K., McKay W.B., Binder H., Hofstoetter U.S. Targeting lumbar spinal neural circuitry by epidural stimulation to restore motor function after spinal cord injury // Neurotherapeutics. 2016. V. 13. № 2. P. 284–94.
  74. Moraud E.M., Capogrosso M., Formento E. et al. Mechanisms underlying the neuromodulation of spinal circuits for correcting gait and balance deficits after spinal cord injury // Neuron. 2016. V. 89. P. 814–828.
  75. Musienko P., van den Brand R., Märzendorfer O. et al. Controlling specific locomotor behaviors through multidimensional monoaminergic modulation of spinal circuitries // J. Neurosci. 2011. V. 31. № 25. P. 9264–78.
  76. Nagappan P.G., Chen H., Wang D.Y. Neuroregeneration and plasticity: a review of the physiological mechanisms for achieving functional recovery postinjury // Military Med. Res. 2020. V. 7. Article 30.
  77. Noble B.T., Brennan F.H., Wang Y. et al. Thoracic VGluT21 Spinal Interneurons Regulate Structural and Functional Plasticity of Sympathetic Networks after High-Level Spinal Cord Injury // J. Neuro-science. 2022. V. 42. № 17. P. 3659–75.
  78. Parhizi B., Barss T.S., Mushahwar V.K. Simultaneous cervical and lumbar spinal cord stimulation induces facilitation of both spinal and corticospinal circuitry in humans // Front. Neurosci. 2021. V. 15. Article 615103.
  79. Peña Pino I., Hoover C., Venkatesh S. et al. Long-Term Spinal Cord Stimulation After Chronic Complete Spinal Cord Injury Enables Volitional Movement in the Absence of Stimulation // Front. Syst. Neurosci. 2020. V. 14. Article 35.
  80. Phillips A.A., Squair J.W., Sayenko D.G. et al. An autonomic neuroprosthesis: noninvasive electrical spinal cord stimulation restores autonomic cardiovascular function in individuals with spinal cord injury // J. Neurotrauma. 2018. V. 35. P. 446–451.
  81. Quilgars C., Bertrand S. Activity-dependent synaptic dynamics in motor circuits of the spinal cord // Current Opinion Physiology. 2019. V. 8. P. 44–49.
  82. Rejc E., Angeli C.A., Atkinson D., Harkema S.J. Motor recovery after activity-based training with spinal cord epidural stimulation in a chronic motor complete paraplegic // Sci. Rep. 2017. V. 7. Article 13476.
  83. Rejc E., Angeli C.A. Ichiyama R.M. Editorial: Advances in Spinal Cord Epidural Stimulation for Motor and Autonomic Functions Recovery After Severe Spinal Cord Injury // Front. Syst. Neurosci. 2022. V. 15. Article 820913.
  84. Rejc E., Smith A.C., Weber K.A. et al. Spinal cord imaging markers and recovery of volitional leg movement with spinal cord epidural stimulation in individuals with clinically motor complete spinal cord injury // Front. Syst. Neurosci. 2020. V. 14. Article 559313.
  85. Rowald A., Komi S., Demesmaeker R. et al. Activity-dependent spinal cord neuromodulation rapidly restores trunk and leg motor functions after complete paralysis. Nat. Med. 2022. V. 28. P. 260–271.
  86. Sachdeva R., Nightingale T.E., Pawar K. et al. Noninvasive neuroprosthesis promotes cardiovascular recovery after spinal cord injury // Neurotherapeutics. 2021. V. 18. P. 1244–1256.
  87. Samejima S., Henderson R., Pradarelli J. et al. Activity-dependent plasticity and spinal cord stimulation for motor recovery following spinal cord injury // Exp. Neurol. 2022. V. 357. Article 114178.
  88. Samejima S., Caskey C.D., Inanici F. et al. Multisite transcutaneous spinal stimulation for walking and autonomic recovery in motor-incomplete tetraplegia: a single-subject design // Phys. Ther. 2022. V. 102. P. 1–12.
  89. Sanchez-Ventura J., Gimenez-Llort L., Penas C., Udina E. Voluntary wheel running preserves lumbar perineuronal nets, enhances motor functions and prevents hyperreflexia after spinal cord injury // Exp. Neurol. 2021. V. 336. Article 113533.
  90. Sayenko D.G., Rath M., Ferguson A.R. et al. Self-assisted standing enabled by non-invasive spinal stimulation after spinal cord injury // J. Neurotrauma. 2019. V. 36. № 9. P. 1435–50.
  91. Seáñez I., Capogrosso M. Motor improvements enabled by spinal cord stimulation combined with physical training after spinal cord injury: review of experimental evidence in animals and humans // Bioelectronic Medicine. 2021. V. 7, Article 16.
  92. Shackleton C., Hodgkiss D., Samejima S. et al. When the whole is greater than the sum of its parts: Activity-based therapy paired with spinal cord stimulation following spinal cord injury // J. Neurophysiol. 2022. V. 128. P. 1292–1306.
  93. Shapkova E.Y., Pismennaya E.V., Emelyannikov D.V., Ivanenko Y. Exoskeleton walk training in paralyzed individuals benefits from transcutaneous lumbar cord tonic electrical stimulation // Front. Neurosci. 2020. V. 14. Article 416.
  94. Singh G., Lucas K., Keller A. et al. Transcutaneous Spinal Stimulation From Adults to Children: A Review // Top Spinal Cord Inj. Rehabil. 2023. V. 29. № 1. P. 16–32.
  95. Siu R., Brown E.H., Mesbah S. et al. Novel Noninvasive Spinal Neuromodulation Strategy Facilitates Recovery of Stepping after Motor Complete Paraplegia // J. Clin. Med. 2022. V. 11. № 13. Article 3670.
  96. Skinnider M.A., Squair J.W., Kathe C. et al. G. Cell type prioritization in single-cell data // Nat. Biotechnol. 2021. V. 39. P. 30–34.
  97. Taccola G., Sayenko D., Gad P. et al. And yet it moves: recovery of volitional control after spinal cord injury // Prog. Neurobiol. 2018. V. 160. P. 64–81.
  98. Takeoka A., Arber S. Functional local proprioceptive feedback circuits initiate and maintain locomotor recovery after spinal cord injury // Cell Reports. 2019. V. 27. Issue 1. P. 71–85e3.
  99. Tefertiller C., Rozwod M., VandeGriend E. et al. Transcutaneous electrical spinal cord stimulation to promote recovery in chronic spinal cord injury // Front. Rehabil. Sci. 2022. V. 2. Article 740307.
  100. Tharu N.S., Alam M., Ling Y.T. et al. Combined Transcutaneous Electrical Spinal Cord Stimulation and Task-Specific Rehabilitation Improves Trunk and Sitting Functions in People with Chronic Tetraplegia // Biomedicines. 2022. V. 11. № 1. Article 34.
  101. Urban L.S., Thornton M.A., Ingraham Dixie K.L. et al. Formation of a Novel Supraspinal-Spinal Connectome that Relearns the Same Motor Task after Complete Paralysis // J. Neurophysiol. 2021. V. 126. Issue 3. P. 957–966.
  102. Wagner F.B., Mignardot J-B., Le Goff-Mignardot C.G. et al. Targeted neurotechnology restores walking in humans with spinal cord injury // Nature. 2018. V. 563. P. 65–71.
  103. Wernig A., Müller S., Nanassy A., Cagol E. Laufband therapy based on ‘rules of spinal locomotion’ is effective in spinal cord injured persons // Eur. J. Neurosci. 1995. V. 7. P. 823–829.
  104. Ying X., Xie Q., Yu X. et al. Water treadmill training protects the integrity of the blood-spinal cord barrier following SCI via the BDNF/TrkB-CREB signalling pathway // Neurochem. Int. 2021. V. 143. Article 104945.
  105. Yu P., Zhang W., Liu Y. et al. The effects and potential mechanisms of locomotor training on improvements of functional recovery after spinal cord injury // Int. Rev. Neurobiol. 2019. V. 147. P. 199–217.
  106. Zavvarian M.M., Hong J. M.G. The functional role of spinal interneurons following traumatic spinal cord injury // Front. Cell. Neurosci. 2020. V. 14. Article 127.
  107. Zhang W., Yang B., Weng H. et al. Wheel running improves motor function and spinal cord plasticity in mice with genetic absence of the corticospinal tract // Front. Cell. Neurosci. 2019. V. 13. Article 106.
  108. Zholudeva L.V., Abraira V.E., Satkunendrarajah K. et al. Spinal interneurons as gatekeepers to neuroplasticity after injury or disease // J. Neurosci. 2021. V. 41. № 5. P. 845–854.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2.

Download (553KB)
Indexing metadata

Copyright (c) 2023 Ю.К. Столбков, Ю.П. Герасименко

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies