Configuration of electrical spinal cord stimulation through real-time processing of gait kinematics

Abstract

Epidural electrical stimulation (EES) of the spinal cord and real-time processing of gait kinematics are powerful methods for the study of locomotion and the improvement of motor control after injury or in neurological disorders. Here, we describe equipment and surgical procedures that can be used to acquire chronic electromyographic (EMG) recordings from leg muscles and to implant targeted spinal cord stimulation systems that remain stable up to several months after implantation in rats and nonhuman primates. We also detail how to exploit these implants to configure electrical spinal cord stimulation policies that allow control over the degree of extension and flexion of each leg during locomotion. This protocol uses real-time processing of gait kinematics and locomotor performance, and can be configured within a few days. Once configured, stimulation bursts are delivered over specific spinal cord locations with precise timing that reproduces the natural spatiotemporal activation of motoneurons during locomotion. These protocols can also be easily adapted for the safe implantation of systems in the vicinity of the spinal cord and to conduct experiments involving real-time movement feedback and closed-loop controllers.

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Fig. 1: Conceptual and technological framework underlying spatiotemporal neuromodulation.
Fig. 2: Spatially selective spinal implants tailored to the anatomy of the spinal cord.
Fig. 3: Procedure for implantation of chronic EMG leads in rats.
Fig. 4: Procedure for implantation of the spinal implant in rats.
Fig. 5: Spatial and functional specificity of spinal implants.
Fig. 6: Spatiotemporal neuromodulation of the lumbar spinal cord.
Fig. 7: Real-time detection of gait events.
Fig. 8: Amplitude and frequency modulation of kinematic and EMG activity during walking enabled by spatiotemporal neuromodulation.
Fig. 9: Enhanced functional specificity of spatiotemporal neuromodulation during walking.

References

  1. 1.

    Bizzi, E., Giszter, S. F., Loeb, E., Mussa-Ivaldi, F. A. & Saltiel, P. Modular organization of motor behavior in the frog’s spinal cord. Trends Neurosci. 18, 442–446 (1995).

    Article  PubMed  CAS  Google Scholar 

  2. 2.

    Levine, A. J. et al. Identification of a cellular node for motor control pathways. Nat. Neurosci. 17, 586–593 (2014).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  3. 3.

    van den Brand, R. et al. Restoring voluntary control of locomotion after paralyzing spinal cord injury. Science 336, 1182–1185 (2012).

    Article  PubMed  CAS  Google Scholar 

  4. 4.

    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 137, 1394–1409 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Harkema, S. 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 377, 1938–1947 (2011).

  6. 6.

    Danner, S. M. et al. Human spinal locomotor control is based on flexibly organized burst generators. Brain 138, 577–588 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Courtine, G. et al. Transformation of nonfunctional spinal circuits into functional states after the loss of brain input. Nat. Neurosci. 12, 1333–1342 (2009).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  8. 8.

    Capogrosso, M. et al. A brain–spine interface alleviating gait deficits after spinal cord injury in primates. Nature 539, 284–288 (2016).

  9. 9.

    Grahn, P. J. et al. Enabling task-specific volitional motor functions via spinal cord neuromodulation in a human with paraplegia. Mayo Clin. Proc. 92, 544–554 (2017).

    Article  PubMed  Google Scholar 

  10. 10.

    Capogrosso, M. et al. A computational model for epidural electrical stimulation of spinal sensorimotor circuits. J. Neurosci. 33, 19326–19340 (2013).

    Article  PubMed  CAS  Google Scholar 

  11. 11.

    Moraud, E. M. et al. Mechanisms underlying the neuromodulation of spinal circuits for correcting gait and balance deficits after spinal cord injury. Neuron 89, 814–828 (2016).

    Article  PubMed  CAS  Google Scholar 

  12. 12.

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

  13. 13.

    Gerasimenko, Y. P. et al. Spinal cord reflexes induced by epidural spinal cord stimulation in normal awake rats. J. Neurosci. Methods 157, 253–263 (2006).

    Article  PubMed  Google Scholar 

  14. 14.

    Minassian, K. et al. Human lumbar cord circuitries can be activated by extrinsic tonic input to generate locomotor-like activity. Hum. Mov. Sci. 26, 275–295 (2007).

    Article  PubMed  CAS  Google Scholar 

  15. 15.

    Taccola, G., Sayenko, D., Gad, P., Gerasimenko, Y. & Edgerton, V. R. And yet it moves: recovery of volitional control after spinal cord injury. Prog. Neurobiol. 160, 64–81 (2018).

  16. 16.

    Stein, R. B. & Capaday, C. The modulation of human reflexes during functional motor tasks. Trends Neurosci. 11, 328–332 (1988).

    Article  PubMed  CAS  Google Scholar 

  17. 17.

    Dy, C. J. et al. Phase-dependent modulation of percutaneously elicited multisegmental muscle responses after spinal cord injury. J. Neurophysiol. 103, 2808–2820 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Sayenko, D. G., Angeli, C., Harkema, S. J., Edgerton, V. R. & Gerasimenko, Y. P. Neuromodulation of evoked muscle potentials induced by epidural spinal-cord stimulation in paralyzed individuals. J. Neurophysiol. 111, 1088–1099 (2014).

    Article  PubMed  Google Scholar 

  19. 19.

    Wenger, N. et al. Closed-loop neuromodulation of spinal sensorimotor circuits controls refined locomotion after complete spinal cord injury. Sci. Transl. Med. 6, 255ra133 (2014).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  20. 20.

    Wenger, N. et al. Spatiotemporal neuromodulation therapies engaging muscle synergies improve motor control after spinal cord injury. Nat. Med. 22, 138–145 (2016).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  21. 21.

    Yakovenko, S., Mushahwar, V., VanderHorst, V., Holstege, G. & Prochazka, A. Spatiotemporal activation of lumbosacral motoneurons in the locomotor step cycle. J. Neurophysiol. 87, 1542–1553 (2002).

    Article  PubMed  Google Scholar 

  22. 22.

    Ivanenko, Y. P. et al. Temporal components of the motor patterns expressed by the human spinal cord reflect foot kinematics. J. Neurophysiol. 90, 3555–3565 (2003).

    Article  PubMed  Google Scholar 

  23. 23.

    Wenger, N. et al. Closed-loop neuromodulation of spinal sensorimotor circuits controls refined locomotion after complete spinal cord injury. Sci. Transl. Med. 6, 255ra133 (2014).

  24. 24.

    Courtine, G. et al. Transformation of nonfunctional spinal circuits into functional states after the loss of brain input. Nat. Neurosci. 12, 1333–1342 (2009).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  25. 25.

    Minev, I. R. et al. Electronic dura mater for long-term multimodal neural interfaces. Science 347, 159–163 (2015).

    Article  PubMed  CAS  Google Scholar 

  26. 26.

    Capogrosso, M. et al. Advantages of soft subdural implants for the delivery of electrochemical neuromodulation therapies to the spinal cord. J. Neural Eng. 15, 026024 (2018).

    Article  PubMed  Google Scholar 

  27. 27.

    Cheriyan, T. et al. Spinal cord injury models: a review. Spinal Cord 52, 588–595 (2014).

    Article  PubMed  CAS  Google Scholar 

  28. 28.

    Lukovic, D. et al. Complete rat spinal cord transection as a faithful model of spinal cord injury for translational cell transplantation. Sci. Rep. 5, 9640 (2015).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  29. 29.

    Courtine, G. et al. Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat. Med. 14, 69–74 (2008).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  30. 30.

    Courtine, G. et al. Can experiments in nonhuman primates expedite the translation of treatments for spinal cord injury in humans? Nat. Med. 13, 561–566 (2007).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  31. 31.

    Capogrosso, M. et al. A brain–spine interface alleviating gait deficits after spinal cord injury in primates. Nature 539, 284–288 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Freund, P. et al. Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates. Nat. Med. 12, 790–792 (2006).

    Article  PubMed  CAS  Google Scholar 

  33. 33.

    Slotkin, J. R. et al. Biodegradable scaffolds promote tissue remodeling and functional improvement in non-human primates with acute spinal cord injury. Biomaterials 123, 63–76 (2017).

    Article  PubMed  CAS  Google Scholar 

  34. 34.

    Rosenzweig, E. S. et al. Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat. Neurosci. 13, 1505–1510 (2010).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  35. 35.

    Salegio, E. A. et al. A unilateral cervical spinal cord contusion injury model in non-human primates (Macaca mulatta). J. Neurotrauma 33, 439–459 (2016).

  36. 36.

    Reeve, C. & Reeve, D. The Spinal Cord (Elsevier, New York, 2008).

  37. 37.

    Coburn, B. A theoretical study of epidural electrical stimulation of the spinal cord—Part II: effects on long myelinated fibers. IEEE Trans. Biomed. Eng. 32, 978–986 (1985).

  38. 38.

    Holsheimer, J. Which neuronal elements are activated directly by spinal cord stimulation. Neuromodulation 5, 25–31 (2002).

    Article  PubMed  Google Scholar 

  39. 39.

    Cuellar, C. A. et al. The role of functional neuroanatomy of the lumbar spinal cord in effect of epidural stimulation. Front. Neuroanat. 11, 82 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Gad, P. et al. Development of a multi-electrode array for spinal cord epidural stimulation to facilitate stepping and standing after a complete spinal cord injury in adult rats. J. Neuroeng. Rehabil. 10, 2 (2013).

    PubMed  PubMed Central  Google Scholar 

  41. 41.

    Merrill, D. R., Bikson, M. & Jefferys, J. G. Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J. Neurosci. Methods 141, 171–198 (2005).

    Article  PubMed  Google Scholar 

  42. 42.

    Cogan, S. F. Neural stimulation and recording electrodes. Annu. Rev. Biomed. Eng. 10, 275–309 (2008).

    Article  PubMed  CAS  Google Scholar 

  43. 43.

    de Jongste, M. J. et al. Stimulation characteristics, complications, and efficacy of spinal cord stimulation systems in patients with refractory angina: a prospective feasibility study. Pacing Clin. Electrophysiol. 17, 1751–1760 (1994).

    Article  PubMed  Google Scholar 

  44. 44.

    Alo, K. et al. Factors affecting impedance of percutaneous leads in spinal cord stimulation. Neuromodulation 9, 128–135 (2006).

    Article  PubMed  Google Scholar 

  45. 45.

    Hofstoetter, U. S. et al. Periodic modulation of repetitively elicited monosynaptic reflexes of the human lumbosacral spinal cord. J. Neurophysiol. 114, 400–410 (2015).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  46. 46.

    Segev, I., Fleshman, J. W. Jr. & Burke, R. E. Computer simulation of group Ia EPSPs using morphologically realistic models of cat α-motoneurons. J. Neurophysiol. 64, 648–660 (1990).

  47. 47.

    Gerasimenko, Y. P. et al. Spinal cord reflexes induced by epidural spinal cord stimulation in normalawakerats. J. Neurosci. Methods. 157, 253–263 (2006).

    Article  PubMed  Google Scholar 

  48. 48.

    Edgerton, V. R. et al. Training locomotor networks. Brain Res. Rev. 57, 241–254 (2008).

    Article  PubMed  Google Scholar 

  49. 49.

    Holinski, B. J. et al. Intraspinal microstimulation produces over-ground walking in anesthetized cats. J. Neural Eng. 13, 056016 (2016).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  50. 50.

    Hehenberger, L., Seeber, M. & Scherer, R. Estimation of gait parameters from EEG source oscillations. IEEE International Conference on Systems, Man, and Cybernetics (SMC) 004182-004187, https://doi.org/10.1109/SMC.2016.7844888 (2016).

  51. 51.

    Presacco, A., Goodman, R., Forrester, L. & Contreras-Vidal, J. L. Neural decoding of treadmill walking from noninvasive electroencephalographic signals. J. Neurophysiol. 106, 1875–1887 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Presacco, A., Forrester, L. W. & Contreras-Vidal, J. L. Decoding intra-limb and inter-limb kinematics during treadmill walking from scalp electroencephalographic (EEG) signals. IEEE Trans. Neural Syst. Rehabil. Eng. 20, 212–219 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Artoni, F. et al. Unidirectional brain to muscle connectivity reveals motor cortex control of leg muscles during stereotyped walking. Neuroimage 159, 403–416 (2017).

    Article  PubMed  Google Scholar 

  54. 54.

    Rouse, A. G., Williams, J. J., Wheeler, J. J. & Moran, D. W. Cortical adaptation to a chronic micro-electrocorticographic brain computer interface. J. Neurosci. 33, 1326–1330 (2013).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  55. 55.

    McCrimmon, C. M. et al. Electrocorticographic encoding of human gait in the leg primary motor cortex. Cereb. Cortex 28, 2752–2762 (2018).

  56. 56.

    Fitzsimmons, N. A., Lebedev, M. A., Peikon, I. D. & Nicolelis, M. A. Extracting kinematic parameters for monkey bipedal walking from cortical neuronal ensemble activity. Front. Integr. Neurosci. 3, 3 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Ma, X. et al. Decoding lower limb muscle activity and kinematics from cortical neural spike trains during monkey performing stand and squat movements. Front. Neurosci. 11, 44 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  58. 58.

    Waldert, S. et al. A review on directional information in neural signals for brain–machine interfaces. J. Physiol. Paris 103, 244–254 (2009).

  59. 59.

    Yin, M. et al. Wireless neurosensor for full-spectrum electrophysiology recordings during free behavior. Neuron 84, 1170–1182 (2014).

    Article  PubMed  CAS  Google Scholar 

  60. 60.

    Borton, D. A., Yin, M., Aceros, J. & Nurmikko, A. An implantable wireless neural interface for recording cortical circuit dynamics in moving primates. J. Neural Eng. 10, 026010 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Foster, J. D. et al. A freely-moving monkey treadmill model. J. Neural Eng. 11, 046020 (2014).

    Article  PubMed  Google Scholar 

  62. 62.

    Schwarz, D. A. et al. Chronic, wireless recordings of large-scale brain activity in freely moving rhesus monkeys. Nat. Methods 11, 670–676 (2014).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  63. 63.

    Suner, S., Fellows, M. R., Vargas-Irwin, C., Nakata, G. K. & Donoghue, J. P. Reliability of signals from a chronically implanted, silicon-based electrode array in non-human primate primary motor cortex. IEEE Trans. Neural Syst. Rehabil. Eng. 13, 524–541 (2005).

    Article  PubMed  Google Scholar 

  64. 64.

    Barrese, J. C. et al. Failure mode analysis of silicon-based intracortical microelectrode arrays in non-human primates. J. Neural Eng. 10, 066014 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  65. 65.

    Simeral, J. D., Kim, S. P., Black, M. J., Donoghue, J. P. & Hochberg, L. R. Neural control of cursor trajectory and click by a human with tetraplegia 1000 days after implant of an intracortical microelectrode array. J. Neural Eng. 8, 025027 (2011).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  66. 66.

    Chestek, C. A. et al. Long-term stability of neural prosthetic control signals from silicon cortical arrays in rhesus macaque motor cortex. J. Neural Eng. 8, 045005 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  67. 67.

    Milekovic, T., Ball, T., Schulze-Bonhage, A., Aertsen, A. & Mehring, C. Detection of error related neuronal responses recorded by electrocorticography in humans during continuous movements. PLoS ONE 8, e55235 (2013).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  68. 68.

    Flouty, O. E. et al. Intracranial somatosensory responses with direct spinal cord stimulation in anesthetized sheep. PLoS ONE 8, e56266 (2013).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  69. 69.

    Musienko, P., van den Brand, R., Maerzendorfer, O., Larmagnac, A. & Courtine, G. Combinatory electrical and pharmacological neuroprosthetic interfaces to regain motor function after spinal cord injury. IEEE Trans. Biomed. Eng. 56, 2707–2711 (2009).

    Article  PubMed  Google Scholar 

  70. 70.

    Moritz, C. T., Lucas, T. H., Perlmutter, S. I. & Fetz, E. E. Forelimb movements and muscle responses evoked by microstimulation of cervical spinal cord in sedated monkeys. J. Neurophysiol. 97, 110–120 (2007).

    Article  PubMed  Google Scholar 

  71. 71.

    Sunshine, M. D. et al. Cervical intraspinal microstimulation evokes robust forelimb movements before and after injury. J. Neural Eng. 10, 036001 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  72. 72.

    Zimmermann, J. B., Seki, K. & Jackson, A. Reanimating the arm and hand with intraspinal microstimulation. J. Neural Eng. 8, 054001 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  73. 73.

    Calixto, R. & Mushahwar, V. Understanding the mechanisms and sites of action of intraspinal microstimulation. in P roceedings of the 12th Annual Conference of the International Functional Electrical Stimulation Society.

  74. 74.

    Rattay, F. Analysis of models for external stimulation of axons. IEEE Trans. Biomed. Eng. 33, 974–977 (1986).

    Article  PubMed  CAS  Google Scholar 

  75. 75.

    McIntyre, C. C. & Grill, W. M. Extracellular stimulation of central neurons: influence of stimulus waveform and frequency on neuronal output. J. Neurophysiol. 88, 1592–1604 (2002).

    Article  PubMed  Google Scholar 

  76. 76.

    Gaunt, R. A., Prochazka, A., Mushahwar, V. K., Guevremont, L. & Ellaway, P. H. Intraspinal microstimulation excites multisegmental sensory afferents at lower stimulus levels than local α- motoneuron responses. J. Neurophysiol. 96, 2995–3005 (2006).

    Article  PubMed  CAS  Google Scholar 

  77. 77.

    Iles, J. F. Central terminations of muscle afferents on motoneurones in the cat spinal cord. J. Physiol. 262, 91–117 (1976).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  78. 78.

    Brown, A. G. & Fyffe, R. E. The morphology of group Ia afferent fibre collaterals in the spinal cord of the cat. J. Physiol. 274, 111–127 (1978).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  79. 79.

    Burke, R. E. & Glenn, L. L. Horseradish peroxidase study of the spatial and electrotonic distribution of group Ia synapses on type-identified ankle extensor motoneurons in the cat. J. Comp. Neurol. 372, 465–485 (1996).

    Article  PubMed  CAS  Google Scholar 

  80. 80.

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

    Article  PubMed  PubMed Central  Google Scholar 

  81. 81.

    Ethier, C., Oby, E. R., Bauman, M. J. & Miller, L. E. Restoration of grasp following paralysis through brain-controlled stimulation of muscles. Nature 485, 368–371 (2012).

  82. 82.

    Bouton, C. E. et al. Restoring cortical control of functional movement in a human with quadripleaturgia. Nature 533, 247–250 (2016).

  83. 83.

    Ajiboye, A. B. et al. Restoration of reaching and grasping movements through brain-controlled muscle stimulation in a person with tetraplegia: a proof-of-concept demonstration. Lancet 389, 1821–1830 (2017).

  84. 84.

    Giat, Y., Mizrahi, J. & Levy, M. A musculotendon model of the fatigue profiles of paralyzed quadriceps muscle under FES. IEEE Trans. Biomed. Eng. 40, 664–674 (1993).

    Article  PubMed  CAS  Google Scholar 

  85. 85.

    Popovic, M. R., Popovic, D. B. & Keller, T. Neuroprostheses for grasping. Neurol. Res. 24, 443–452 (2002).

    Article  PubMed  Google Scholar 

  86. 86.

    House, P. A., MacDonald, J. D., Tresco, P. A. & Normann, R. A. Acute microelectrode array implantation into human neocortex: preliminary technique and histological considerations. Neurosurg. Focus 20, 1–4 (2006).

    Article  Google Scholar 

  87. 87.

    Gerasimenko, Y., Roy, R. R. & Edgerton, V. R. Epidural stimulation: comparison of the spinal circuits that generate and control locomotion in rats, cats and humans. Exp. Neurol. 209, 417–425 (2008).

    Article  PubMed  Google Scholar 

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Acknowledgements

The illustration in Fig. 1 was created by C. Beach. N.W. is a participant in the Charité Clinical Scientist Program funded by the Charité–Universitätsmedizin Berlin and the Berlin Institute of Health. This work was supported by Medtronic, the European Community’s Seventh Framework Programme (CP-IP 258654, NeuWALK), the International Paraplegic foundation (IRP), a Consolidator Grant from the European Research Council (ERC-2015-CoG HOW2WALKAGAIN 682999), the Wyss Center in Geneva, the Russian Science Foundation (RSF grant 14-15-00788, P.M.), a Wings for Life Fellowship to G.C., Marie Curie COFUND EPFL fellowships to F.B.W. and T.M., and a Morton Cure Paralysis Fund fellowship to T.M., as well as by the Swiss National Science Foundation, including a Bonus of Excellence (310030B_166674), the National Center of Competence in Research (NCCR) Robotics, the Sino-Swiss Science and Technology Cooperation (IZLCZ3_156331), the NanoTera.ch program (SpineRepair) and the Sinergia program (CRSII3_160696).

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M.C., F.B.W., J.G., E.M.M., N.W., T.M. and G.C. developed the methods to control the stimulation and optimize the electrode placement. P.S., N.P., P.M., J.B. and G.C. developed the surgical procedures. M.C., F.B.W., J.G., E.M.M. and T.M. performed the experiments in monkeys. N.W., E.M.M., J.G. and M.C. performed the experiments in rats. E.B. and G.C. supervised the experiments and animal procedures. M.C., F.B.W., J.G., E.M.M., N.W. and T.M. analyzed the data. M.C., F.B.W. and J.G. created the figures. M.C., F.B.W. and G.C. wrote the manuscript.

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Correspondence to Grégoire Courtine.

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Competing interests

G.C., M.C., E.M.M., N.W., T.M., F.B.W., J.G. and J.B. hold various patents related to the present work. E.B. reports receipt of personal fees from Motac Neuroscience Ltd. UK and is a shareholder of Motac Holding, UK, and Plenitudes SARL, France. G.C. and J.B. are founders and shareholders of GTX Medical BV. The other authors declare no competing interests.

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Key references using this protocol

1. Wenger, N. et al. Nat. Med. 22, 138–145 (2016) https://doi.org/10.1038/nm.4025

2. Capogrosso, M. et al. Nature 539, 284–288 (2016) https://doi.org/10.1038/nature20118

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Capogrosso, M., Wagner, F.B., Gandar, J. et al. Configuration of electrical spinal cord stimulation through real-time processing of gait kinematics . Nat Protoc 13, 2031–2061 (2018). https://doi.org/10.1038/s41596-018-0030-9

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