Multi-system neurorehabilitative strategies to restore motor functions following severe spinal cord injury

Experimental Neurology

Volumn 235, Issue 1, 2012, Pages 100-109

  Musienko, Pavel ^a,b,c   Heutschi, Janine ^a,b   Friedli, Lucia ^a,b   den Brand, Rubia van ^a,b   Courtine, Grégoire ^a,b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b Rehabilitation Initiative and Technology Platform Zurich (RITZ)   (Switzerland)

^c PAVLOV INSTITUTE OF PHYSIOLOGY   (Russian Federation)

Author keywords

Locomotion; Neuroprosthetic; Neurorehabilitation; Plasticity; SCI

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; QUIPAZINE; SEROTONIN AGONIST;

DISEASE SEVERITY; ELECTROMYOGRAM; ELECTROSTIMULATION THERAPY; FACILITATION; FUNCTIONAL STATUS; HUMAN; LEARNING; LOCOMOTION; MONOAMINERGIC SYSTEM; MOTONEURON; MOTOR CONTROL; MOTOR COORDINATION; MOTOR PERFORMANCE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROREHABILITATION; NONHUMAN; PRIORITY JOURNAL; REHABILITATION; REVIEW; SPINAL CORD INJURY; TREADMILL EXERCISE; WEIGHT BEARING;

ANIMALS; HUMANS; MOTOR ACTIVITY; NERVE NET; NEURONAL PLASTICITY; SPINAL CORD; SPINAL CORD INJURIES;

EID: 84859923506     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.08.025     Document Type: Review

References (74)

1. Agnati L.F., Guidolin D., Guescini M., Genedani S., Fuxe K. Understanding wiring and volume transmission. Brain Res. Rev. 2010, 64:137-159.
2. Barbeau H., Rossignol S. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res. 1987, 412:84-95.
3. Barbeau H., Ladouceur M., Norman K.E., Pepin A., Leroux A. Walking after spinal cord injury: evaluation, treatment, and functional recovery. Arch. Phys. Med. Rehabil. 1999, 80:225-235.
4. Barriere G., Leblond H., Provencher J., Rossignol S. Prominent role of the spinal central pattern generator in the recovery of locomotion after partial spinal cord injuries. J. Neurosci. 2008, 28:3976-3987.
5. Barthelemy D., Leblond H., Rossignol S. Characteristics and mechanisms of locomotion induced by intraspinal microstimulation and dorsal root stimulation in spinal cats. J. Neurophysiol. 2007, 97:1986-2000.
6. Behrman A.L., Harkema S.J. Locomotor training after human spinal cord injury: a series of case studies. Phys. Ther. 2000, 80:688-700.
7. Beres-Jones J.A., Harkema S.J. The human spinal cord interprets velocity-dependent afferent input during stepping. Brain 2004, 127:2232-2246.
8. Burke R.E. Sir Charles Sherrington's the integrative action of the nervous system: a centenary appreciation. Brain 2007, 130:887-894.
9. Cai L.L., Courtine G., Fong A.J., Burdick J.W., Roy R.R., Edgerton V.R. Plasticity of functional connectivity in the adult spinal cord. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2006, 361:1635-1646.
10. Calancie B., Alexeeva N., Broton J.G., Molano M.R. Interlimb reflex activity after spinal cord injury in man: strengthening response patterns are consistent with ongoing synaptic plasticity. Clin. Neurophysiol. 2005, 116:75-86.
11. Courtine G., Harkema S.J., Dy C.J., Gerasimenko Y.P., Dyhre-Poulsen P. Modulation of multisegmental monosynaptic responses in a variety of leg muscles during walking and running in humans. J. Physiol. 2007, 582:1125-1139.
12. Courtine G., Song B., Roy R.R., Zhong H., Herrmann J.E., Ao Y., Qi J., Edgerton V.R., Sofroniew M.V. Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat. Med. 2008, 14:69-74.
13. Courtine G., Gerasimenko Y., van den Brand R., Yew A., Musienko P., Zhong H., Song B., Ao Y., Ichiyama R.M., Lavrov I., Roy R.R., Sofroniew M.V., Edgerton V.R. Transformation of nonfunctional spinal circuits into functional states after the loss of brain input. Nat. Neurosci. 2009, 12:1333-1342.
14. De Leon R.D., Hodgson J.A., Roy R.R., Edgerton V.R. Full weight-bearing hindlimb standing following stand training in the adult spinal cat. J. Neurophysiol. 1998, 80:83-91.
15. Dietz V. Body weight supported gait training: from laboratory to clinical setting. Brain Res. Bull. 2009, 78:I-VI.
16. Dietz V. Behavior of spinal neurons deprived of supraspinal input. Nat. Rev. Neurol. 2010, 6:167-174.
17. Dietz V., Harkema S.J. Locomotor activity in spinal cord-injured persons. J. Appl. Physiol. 2004, 96:1954-1960.
18. Dietz V., Colombo G., Jensen L. Locomotor activity in spinal man. Lancet 1994, 344:1260-1263.
19. Dietz V., Grillner S., Trepp A., Hubli M., Bolliger M. Changes in spinal reflex and locomotor activity after a complete spinal cord injury: a common mechanism?. Brain 2009, 132:2196-2205.
20. Dobkin B., Barbeau H., Deforge D., Ditunno J., Elashoff R., Apple D., Basso M., Behrman A., Harkema S., Saulino M., Scott M. The evolution of walking-related outcomes over the first 12weeks of rehabilitation for incomplete traumatic spinal cord injury: the multicenter randomized Spinal Cord Injury Locomotor Trial. Neurorehabil. Neural Repair 2007, 21:25-35.
21. Edgerton V.R., Courtine G., Gerasimenko Y.P., Lavrov I., Ichiyama R.M., Fong A.J., Cai L.L., Otoshi C.K., Tillakaratne N.J., Burdick J.W., Roy R.R. Training locomotor networks. Brain Res. Rev. 2008, 57:241-254.
22. Fong A.J., Cai L.L., Otoshi C.K., Reinkensmeyer D.J., Burdick J.W., Roy R.R., Edgerton V.R. Spinal cord-transected mice learn to step in response to quipazine treatment and robotic training. J. Neurosci. 2005, 25:11738-11747.
23. Fong A.J., Roy R.R., Ichiyama R.M., Lavrov I., Courtine G., Gerasimenko Y., Tai Y.C., Burdick J., Edgerton V.R. Recovery of control of posture and locomotion after a spinal cord injury: solutions staring us in the face. Prog. Brain Res. 2009, 175:393-418.
24. Fuentes R., Petersson P., Siesser W.B., Caron M.G., Nicolelis M.A. Spinal cord stimulation restores locomotion in animal models of Parkinson's disease. Science 2009, 323:1578-1582.
25. Gerasimenko Y.P., Lavrov I.A., Courtine G., Ichiyama R.M., Dy C.J., Zhong H., Roy R.R., Edgerton V.R. Spinal cord reflexes induced by epidural spinal cord stimulation in normal awake rats. J. Neurosci. Methods 2006, 157:253-263.
26. Gerasimenko Y.P., Ichiyama R.M., Lavrov I.A., Courtine G., Cai L., Zhong H., Roy R.R., Edgerton V.R. Epidural spinal cord stimulation plus quipazine administration enable stepping in complete spinal adult rats. J. Neurophysiol. 2007, 98:2525-2536.
27. 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. 2008, 209:417-425.
28. Giszter S., Patil V., Hart C. Primitives, premotor drives, and pattern generation: a combined computational and neuroethological perspective. Prog. Brain Res. 2007, 165:323-346.
29. Graham-Brown T. The intrinsic factors in the act of progression in the mammal. Proc. R. Soc. Lond. B Biol. Sci. 1911, 308-319.
30. Grillner S. Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 2006, 52:751-766.
31. Grillner S., Zangger P. The effect of dorsal root transection on the efferent motor pattern in the cat's hindlimb during locomotion. Acta Physiol. Scand. 1984, 120:393-405.
32. Guertin P.A. Recovery of locomotor function with combinatory drug treatments designed to synergistically activate specific neuronal networks. Curr. Med. Chem. 2009, 16:1366-1371.
33. Hagglund M., Borgius L., Dougherty K.J., Kiehn O. Activation of groups of excitatory neurons in the mammalian spinal cord or hindbrain evokes locomotion. Nat. Neurosci. 2010, 13:246-252.
34. Harkema S.J. Neural plasticity after human spinal cord injury: application of locomotor training to the rehabilitation of walking. Neuroscientist 2001, 7:455-468.
35. Harkema S.J. Plasticity of interneuronal networks of the functionally isolated human spinal cord. Brain Res. Rev. 2008, 57:255-264.
36. Harkema S.J., Hurley S.L., Patel U.K., Requejo P.S., Dobkin B.H., Edgerton V.R. Human lumbosacral spinal cord interprets loading during stepping. J. Neurophysiol. 1997, 77:797-811.
37. Harkema S.J., Gerasimenko Y., Hodes J., Burdick J., Angeli C., Chen Y., Ferreira C.K., Rejc E., Edgerton V.R. Sensory control of standing and stepping enabled by epidural stimulation after a human motor complete spinal cord injury. 2010 Neuroscience Meeting Planner, San Diego, CA 2010, pp. Program No. 259.251. Neuroscience, S. f. (Ed.).
38. Hebb D.O. The Organization of Behavior: A neuropsychological Theory 1949, Wiley, New York.
39. Hentall I.D., Pinzon A., Noga B.R. Spatial and temporal patterns of serotonin release in the rat's lumbar spinal cord following electrical stimulation of the nucleus raphe magnus. Neuroscience 2006, 142:893-903.
40. Hiersemenzel L.P., Curt A., Dietz V. From spinal shock to spasticity: neuronal adaptations to a spinal cord injury. Neurology 2000, 54:1574-1582.
41. Holsheimer J. Computer modelling of spinal cord stimulation and its contribution to therapeutic efficacy. Spinal Cord 1998, 36:531-540.
42. Hou S., Duale H., Cameron A.A., Abshire S.M., Lyttle T.S., Rabchevsky A.G. Plasticity of lumbosacral propriospinal neurons is associated with the development of autonomic dysreflexia after thoracic spinal cord transection. J. Comp. Neurol. 2008, 509:382-399.
43. Hultborn H. State-dependent modulation of sensory feedback. J. Physiol. 2001, 533:5-13.
44. Hultborn H. Spinal reflexes, mechanisms and concepts: from Eccles to Lundberg and beyond. Prog. Neurobiol. 2006, 78:215-232.
45. Ichiyama R.M., Gerasimenko Y.P., Zhong H., Roy R.R., Edgerton V.R. Hindlimb stepping movements in complete spinal rats induced by epidural spinal cord stimulation. Neurosci. Lett. 2005, 383:339-344.
46. Ichiyama R.M., Courtine G., Gerasimenko Y.P., Yang G.J., van den Brand R., Lavrov I.A., Zhong H., Roy R.R., Edgerton V.R. Step training reinforces specific spinal locomotor circuitry in adult spinal rats. J. Neurosci. 2008, 28:7370-7375.
47. Jordan L.M., Liu J., Hedlund P.B., Akay T., Pearson K.G. Descending command systems for the initiation of locomotion in mammals. Brain Res. Rev. 2008, 57:183-191.
48. Landry E.S., Lapointe N.P., Rouillard C., Levesque D., Hedlund P.B., Guertin P.A. Contribution of spinal 5-HT1A and 5-HT7 receptors to locomotor-like movement induced by 8-OH-DPAT in spinal cord-transected mice. Eur. J. Neurosci. 2006, 24:535-546.
49. Lapointe N.P., Guertin P.A. Synergistic effects of D1/5 and 5-HT1A/7 receptor agonists on locomotor movement induction in complete spinal cord-transected mice. J. Neurophysiol. 2008, 100:160-168.
50. Lavrov I., Courtine G., Dy C.J., van den Brand R., Fong A.J., Gerasimenko Y., Zhong H., Roy R.R., Edgerton V.R. Facilitation of stepping with epidural stimulation in spinal rats: role of sensory input. J. Neurosci. 2008, 28:7774-7780.
51. Lavrov I., Dy C.J., Fong A.J., Gerasimenko Y., Courtine G., Zhong H., Roy R.R., Edgerton V.R. Epidural stimulation induced modulation of spinal locomotor networks in adult spinal rats. J. Neurosci. 2008, 28:6022-6029.
52. Lovely R.G., Gregor R.J., Roy R.R., Edgerton V.R. Effects of training on the recovery of full-weight-bearing stepping in the adult spinal cat. Exp. Neurol. 1986, 92:421-435.
53. Maegele M., Muller S., Wernig A., Edgerton V.R., Harkema S.J. Recruitment of spinal motor pools during voluntary movements versus stepping after human spinal cord injury. J. Neurotrauma 2002, 19:1217-1229.
54. Minassian K., Jilge B., Rattay F., Pinter M.M., Binder H., Gerstenbrand F., Dimitrijevic M.R. 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.
55. Mushahwar V.K., Horch K.W. Muscle recruitment through electrical stimulation of the lumbo-sacral spinal cord. IEEE Trans. Rehabil. Eng. 2000, 8:22-29.
56. Mushahwar V.K., Guevremont L., Saigal R. Could cortical signals control intraspinal stimulators? A theoretical evaluation. IEEE Trans. Neural Syst. Rehabil. Eng. 2006, 14:198-201.
57. Mushahwar V.K., Jacobs P.L., Normann R.A., Triolo R.J., Kleitman N. New functional electrical stimulation approaches to standing and walking. J. Neural Eng. 2007, 4:S181-S197.
58. Musienko P.E., Bogacheva I.N., Gerasimenko Iu P. Significance of peripheral feedback in stepping movement generation under epideral spinal cord stimulation. Ross. Fiziol. Zh. Im. I. M. Sechenova 2005, 91:1407-1420.
59. Musienko P.E., Bogacheva I.N., Gerasimenko Y.P. Significance of peripheral feedback in the generation of stepping movements during epidural stimulation of the spinal cord. Neurosci. Behav. Physiol. 2007, 37:181-190.
60. Musienko P.E., Gerasimenko Iu P., Van den Brand R., Roy R.R., Zhong H., Edgerton V., Courtine G. Monoaminergic modulation of locomotion facilitated by epidural stimulation (ES) in spinal rats 2008, Society for Neuroscience, Washington, DC, pp. Program No 573.572.
61. 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. 2009, 56:2707-2711.
62. Musienko P.E., Zelenin P.V., Orlovsky G.N., Deliagina T.G. Facilitation of postural limb reflexes with epidural stimulation in spinal rabbits. J. Neurophysiol. 2010, 103:1080-1092.
63. Pearson K.G. Generating the walking gait: role of sensory feedback. Prog. Brain Res. 2004, 143:123-129.
64. Philippson M. L'autonomie et la centrilasation dans le système nerveux des animaux. Trav. Lab. Physiol. Inst. Solvay. (Bruxelle) 1905, 7:1-208.
65. Prochazka A., Mushahwar V.K., McCreery D.B. Neural prostheses. J. Physiol. 2001, 533:99-109.
66. 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 2000, 38:473-489.
67. Rossignol S., Giroux N., Chau C., Marcoux J., Brustein E., Reader T.A. Pharmacological aids to locomotor training after spinal injury in the cat. J. Physiol. 2001, 533:65-74.
68. Rossignol S., Dubuc R., Gossard J.P. Dynamic sensorimotor interactions in locomotion. Physiol. Rev. 2006, 86:89-154.
69. Schomburg E.D., Steffens H., Kniffki K.D. Contribution of group III and IV muscle afferents to multisensorial spinal motor control in cats. Neurosci. Res. 1999, 33:195-206.
70. Sherrington C. Flexion-reflex of the limb, crossed extension reflex, and reflex stepping and standing. J. Physiol. (Lond) 1910, 40:28-121.
71. Tillakaratne N.J., de Leon R.D., Hoang T.X., Roy R.R., Edgerton V.R., Tobin A.J. Use-dependent modulation of inhibitory capacity in the feline lumbar spinal cord. J. Neurosci. 2002, 22:3130-3143.
72. Van de Crommert H.W., Mulder T., Duysens J. Neural control of locomotion: sensory control of the central pattern generator and its relation to treadmill training. Gait Posture 1998, 7:251-263.
73. Vrieseling E., Arber S. Target-induced transcriptional control of dendritic patterning and connectivity in motor neurons by the ETS gene Pea3. Cell 2006, 127:1439-1452.
74. Wernig A., Muller S. Laufband locomotion with body weight support improved walking in persons with severe spinal cord injuries. Paraplegia 1992, 30:229-238.