Closed-loop neuromodulation of spinal sensorimotor circuits controls refined locomotion after complete spinal cord injury

Science Translational Medicine

Volumn 6, Issue 255, 2014, Pages

  Wenger, Nikolaus ^a   Moraud, Eduardo Martin ^a,b   Raspopovic, Stanisa ^a,c   Bonizzato, Marco ^a   DiGiovanna, Jack ^a   Musienko, Pavel ^a,d   Morari, Manfred ^b   Micera, Silvestro ^a,c   Courtine, Grégoire ^a  

^a EPFL   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c SCUOLA SUPERIORE SANT ANNA   (Italy)

^d PAVLOV INSTITUTE OF PHYSIOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CLIMBING; CONCEPTUAL FRAMEWORK; CONTROLLED STUDY; FEEDBACK SYSTEM; FOOT; KINEMATICS; LEG MOVEMENT; LOCOMOTION; MOTOR CONTROL; MOTOR SYSTEM; NEUROMODULATION; NEUROPROSTHESIS; NONHUMAN; POLICY; POSITIVE FEEDBACK; RAT; SENSORIMOTOR CIRCUIT; SENSORY SYSTEM; SPINAL CORD; SPINAL CORD INJURY; TECHNOLOGY; ANIMAL; BIOMECHANICS; CONVALESCENCE; DEVICES; DISEASE MODEL; FEMALE; GAIT; INNERVATION; LEWIS RAT; LIMB; MOTONEURON; MUSCLE FATIGUE; NEUROFEEDBACK; PATHOPHYSIOLOGY; PROSTHESIS DESIGN; SENSORY FEEDBACK; SPINAL CORD INJURIES; SPINAL NERVE; TIME FACTOR;

ANIMALS; BIOMECHANICAL PHENOMENA; DISEASE MODELS, ANIMAL; EXTREMITIES; FEEDBACK, SENSORY; FEMALE; GAIT; LOCOMOTION; MOTOR NEURONS; MUSCLE FATIGUE; NEURAL PROSTHESES; NEUROFEEDBACK; PROSTHESIS DESIGN; RATS, INBRED LEW; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; SPINAL NERVES; TIME FACTORS;

EID: 84908377656     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3008325     Document Type: Article

References (44)

1. A. M. Lozano, N. Lipsman, Probing and regulating dysfunctional circuits using deep brain stimulation. Neuron 77, 406-424 (2013).
2. D. Borton, S. Micera, R. Millán Jdel, G. Courtine, Personalized neuroprosthetics. Sci. Transl. Med. 5, 210rv212 (2013).
3. P. Krack, A. Batir, N. Van Blercom, S. Chabardes, V. Fraix, C. Ardouin, A. Koudsie, P. D. Limousin, A. Benazzouz, J. F. LeBas, A. L. Benabid, P. Pollak, Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N. Engl. J. Med. 349, 1925-1934 (2003).
4. B. Rosin, M. Slovik, R. Mitelman, M. Rivlin-Etzion, S. N. Haber, Z. Israel, E. Vaadia, H. Bergman, Closed-loop deep brain stimulation is superior in ameliorating parkinsonism. Neuron 72, 370-384 (2011).
5. P. A. Tass, L. Qin, C. Hauptmann, S. Dovero, E. Bezard, T. Boraud, W. G. Meissner, Coordinated reset has sustained aftereffects in Parkinsonian monkeys. Ann. Neurol. 72, 816-820 (2012).
6. D. T. Brocker, B. D. Swan, D. A. Turner, R. E. Gross, S. B. Tatter, M. M. Koop, H. Bronte-Stewart, W. M. Grill, Improved efficacy of temporally non-regular deep brain stimulation in Parkinson's disease. Exp. Neurol. 239, 60-67 (2013).
7. R. van den Brand, J. Heutschi, Q. Barraud, J. DiGiovanna, K. Bartholdi, M. Huerlimann, L. Friedli, I. Vollenweider, E. M. Moraud, S. Duis, N. Dominici, S. Micera, P. Musienko, G. Courtine, Restoring voluntary control of locomotion after paralyzing spinal cord injury. Science 336, 1182-1185 (2012).
8. S. Harkema, Y. Gerasimenko, J. Hodes, J. Burdick, C. Angeli, Y. Chen, C. Ferreira, A. Willhite, E. Rejc, R. G. Grossman, V. R. Edgerton, 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).
9. B. J. Holinski, D. G. Everaert, V. K. Mushahwar, R. B. Stein, Real-time control of walking using recordings from dorsal root ganglia. J. Neural Eng. 10, 056008 (2013).
10. R. Fuentes, P. Petersson, W. B. Siesser, M. G. Caron, M. A. Nicolelis, Spinal cord stimulation restores locomotion in animal models of Parkinson's disease. Science 323, 1578-1582 (2009).
11. G. Fénelon, C. Goujon, J. M. Gurruchaga, P. Cesaro, B. Jarraya, S. Palfi, J. P. Lefaucheur, Spinal cord stimulation for chronic pain improved motor function in a patient with Parkinson's disease. Parkinsonism Relat. Disord. 18, 213-214 (2012).
12. J. T. Paz, T. J. Davidson, E. S. Frechette, B. Delord, I. Parada, K. Peng, K. Deisseroth, J. R. Huguenard, Closed-loop optogenetic control of thalamus as a tool for interrupting seizures after cortical injury. Nat. Neurosci. 16, 64-70 (2013).
13. K. Minassian, B. Jilge, F. Rattay, M. M. Pinter, H. Binder, F. Gerstenbrand, M. R. Dimitrijevic, 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 (2004).
14. G. Courtine, Y. Gerasimenko, R. van den Brand, A. Yew, P. Musienko, H. Zhong, B. Song, Y. Ao, R. M. Ichiyama, I. Lavrov, R. R. Roy, M. V. Sofroniew, V. R. Edgerton, Transformation of non G. Courtine, Y. Gerasimenko, R. van den Brand, A. Yew, P. Musienko, H. Zhong, B. Song, Y. Ao, R. M. Ichiyama, I. Lavrov, R. R. Roy, M. V. Sofroniew, V. R. Edgerton, Transformation of non-functional spinal circuits into functional states after the loss of brain input. Nat. Neurosci. 12, 1333-1342 (2009).
15. V. F. Lyalka, L. J. Hsu, A. Karayannidou, P. V. Zelenin, G. N. Orlovsky, T. G. Deliagina, Facilitation of postural limb reflexes in spinal rabbits by serotonergic agonist administration, epidural electrical stimulation, and postural training. J. Neurophysiol. 106, 1341-1354 (2011).
16. P. Afshar, A. Khambhati, S. Stanslaski, D. Carlson, R. Jensen, D. Linde, S. Dani, M. Lazarewicz, P. Cong, J. Giftakis, P. Stypulkowski, T. Denison, A translational platform for prototyping closed-loop neuromodulation systems. Front. Neural Circuits 6, 117 (2013).
17. M. Capogrosso, N. Wenger, S. Raspopovic, P. Musienko, J. Beauparlant, L. Bassi Luciani, G. Courtine, S. Micera, A computational model for epidural electrical stimulation of spinal sensorimotor circuits. J. Neurosci. 33, 19326-19340 (2013).
18. P. Gad, I. Lavrov, P. Shah, H. Zhong, R. R. Roy, V. R. Edgerton, Y. Gerasimenko, Neuromodulation of motor-evoked potentials during stepping in spinal rats. J. Neurophysiol. 110, 1311-1322 (2013).
19. I. Lavrov, C. J. Dy, A. J. Fong, Y. Gerasimenko, G. Courtine, H. Zhong, R. R. Roy, V. R. Edgerton, Epidural stimulation induced modulation of spinal locomotor networks in adult spinal rats. J. Neurosci. 28, 6022-6029 (2008).
20. J. Ladenbauer, K. Minassian, U. S. Hofstoetter, M. R. Dimitrijevic, F. Rattay, 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 (2010).
21. V. Dietz, R. Müller, Degradation of neuronal function following a spinal cord injury: Mechanisms and countermeasures. Brain 127, 2221-2231 (2004).
22. J. Beauparlant, R. van den Brand, Q. Barraud, L. Friedli, P. Musienko, V. Dietz, G. Courtine, Undirected compensatory plasticity contributes to neuronal dysfunction after severe spinal cord injury. Brain 136, 3347-3361 (2013).
23. C. A. Angeli, V. R. Edgerton, Y. P. Gerasimenko, S. J. Harkema, Altering spinal cord excitability enables voluntary movements after chronic complete paralysis in humans. Brain 137, 1394-1409 (2014).
24. H. Vallery, P. Lutz, J. von Zitzewitz, G. Rauter, M. Fritschi, C. Everarts, R. Ronsse, A. Curt, M. Bolliger, S. B. Pai, Multidirectional transparent support for overground gait training, IEEE International Conference on Rehabilitation Robotics (ICORR), Seattle, WA, 24 to 26 June 2013.
25. D. A. McCrea, Spinal circuitry of sensorimotor control of locomotion. J. Physiol. 533, 41-50 (2001).
26. Y. Gerasimenko, R. Gorodnichev, E. Machueva, E. Pivovarova, D. Semyenov, A. Savochin, R. R. Roy, V. R. Edgerton, Novel and direct access to the human locomotor spinal circuitry. J. Neurosci. 30, 3700-3708 (2010).
27. G. Courtine, S. J. Harkema, C. J. Dy, Y. P. Gerasimenko, P. Dyhre-Poulsen, Modulation of multisegmental monosynaptic responses in a variety of leg muscles during walking and running in humans. J. Physiol. 582, 1125-1139 (2007).
28. J. B. Zimmermann, K. Seki, A. Jackson, Reanimating the arm and hand with intraspinal microstimulation. J. Neural Eng. 8, 054001 (2011).
29. D. Kernell, Principles of force gradation in skeletal muscles. Neural Plast. 10, 69-76 (2003).
30. K. Minassian, I. Persy, F. Rattay, M. M. Pinter, H. Kern, M. R. Dimitrijevic, Human lumbar cord circuitries can be activated by extrinsic tonic input to generate locomotor-like activity. Hum. Mov. Sci. 26, 275-295 (2007).
31. Y. Gerasimenko, R. R. Roy, V. R. Edgerton, Epidural stimulation: Comparison of the spinal circuits that generate and control locomotion in rats, cats and humans. Exp. Neurol. 209, 417-425 (2008).
32. G. P. Braz, M. Russold, G. M. Davis, Functional electrical stimulation control of standing and stepping after spinal cord injury: A review of technical characteristics. Neuromodulation 12, 180-190 (2009).
33. C. L. Lynch, M. R. Popovic, Functional electrical stimulation. IEEE Contr. Syst. Mag. 28, 40-50 (2008).
34. E. C. Field-Fote, Combined use of body weight support, functional electric stimulation, and treadmill training to improve walking ability in individuals with chronic incomplete spinal cord injury. Arch. Phys. Med. Rehabil. 82, 818-824 (2001).
35. G. Bosco, R. E. Poppele, Proprioception from a spinocerebellar perspective. Physiol. Rev. 81, 539-568 (2001).
36. G. Courtine, R. R. Roy, J. Hodgson, H. McKay, J. Raven, H. Zhong, H. Yang, M. H. Tuszynski, V. R. Edgerton, Kinematic and EMG determinants in quadrupedal locomotion of a non-human primate (Rhesus). J. Neurophysiol. 93, 3127-3145 (2005).
37. Y. P. Ivanenko, A. d'Avella, R. E. Poppele, F. Lacquaniti, On the origin of planar covariation of elevation angles during human locomotion. J. Neurophysiol. 99, 1890-1898 (2008).
38. D. Borton, M. Bonizzato, J. Beauparlant, J. DiGiovanna, E. M. Moraud, N. Wenger, P. Musienko, I. R. Minev, S. P. Lacour, R. Millán Jdel, S. Micera, G. Courtine, Corticospinal neuroprostheses to restore locomotion after spinal cord injury. Neurosci. Res. 78, 21-29 (2014).
39. B. Mariani, S. Rochat, C. J. Büla, K. Aminian, Heel and toe clearance estimation for gait analysis using wireless inertial sensors. IEEE Trans. Biomed. Eng. 59, 3162-3168 (2012).
40. N. Dominici, U. Keller, H. Vallery, L. Friedli, R. van den Brand, M. L. Starkey, P. Musienko, R. Riener, G. Courtine, Versatile robotic interface to evaluate, enable and train locomotion and balance after neuromotor disorders. Nat. Med. 18, 1142-1147 (2012).
41. V. R. Edgerton, G. Courtine, Y. P. Gerasimenko, I. Lavrov, R. M. Ichiyama, A. J. Fong, L. L. Cai, C. K. Otoshi, N. J. K. Tillakaratne, J. W. Burdick, R. R. Roy, Training locomotor networks. Brain Res. Rev. 57, 241-254 (2008).
42. P. Musienko, R. van den Brand, O. Märzendorfer, R. R. Roy, Y. Gerasimenko, V. R. Edgerton, G. Courtine, Controlling specific locomotor behaviors through multidimensional monoaminergic modulation of spinal circuitries. J. Neurosci. 31, 9264-9278 (2011).
43. I. Steuer, P. Rouleau, P. A. Guertin, Pharmacological approaches to chronic spinal cord injury. Curr. Pharm. Des. 19, 4423-4436 (2013).
44. C. Ethier, E. R. Oby, M. J. Bauman, L. E. Miller, Restoration of grasp following paralysis through brain-controlled stimulation of muscles. Nature 485, 368-371 (2012).