Incomplete spinal cord injury promotes durable functional changes within the spinal locomotor circuitry

Journal of Neurophysiology

Volumn 108, Issue 1, 2012, Pages 124-134

  Martinez, Marina ^a   Delivet Mongrain, Hugo ^a   Leblond, Hugues ^a   Rossignol, Serge ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Central pattern generator; Cycle; Dual lesion paradigm; Kinematics; Plasticity

Indexed keywords

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; KINEMATICS; LOCOMOTION; MALE; NERVE CELL; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; PATTERN GENERATOR; PRIORITY JOURNAL; SPINAL CORD HEMISECTION; SPINAL CORD INJURY; WALKING;

ADAPTATION, PHYSIOLOGICAL; ANALYSIS OF VARIANCE; ANIMALS; BIOMECHANICS; CATS; DISEASE MODELS, ANIMAL; ELECTROMYOGRAPHY; FEMALE; FUNCTIONAL LATERALITY; LOCOMOTION; MALE; RECOVERY OF FUNCTION; SPINAL CORD; SPINAL CORD INJURIES; SPINE; TIME FACTORS;

EID: 84863325761     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00073.2012     Document Type: Article

References (58)

1. Armstrong DM. The supraspinal control of mammalian locomotion. J Physiol 405: 1-37, 1988.
2. Barbeau H, Rossignol S. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res 412: 84-95, 1987.
3. Barrière G, Frigon A, Leblond H, Provencher J, Rossignol S. Dual spinal lesion paradigm in the cat: evolution of the kinematic locomotor pattern. J Neurophysiol 104: 1119-1133, 2010.
4. Barrière 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 28: 3976-3987, 2008.
5. Bouyer LJ, Rossignol S. Contribution of cutaneous inputs from the hindpaw to the control of locomotion: 1. Intact cats. J Neurophysiol 90: 3625-3639, 2003a.
6. Bouyer LJ, Rossignol S. Contribution of cutaneous inputs from the hindpaw to the control of locomotion: 2. Spinal cats. J Neurophysiol 90: 3640-3653, 2003b.
7. Bretzner F, Drew T. Contribution of the motor cortex to the structure and the timing of hindlimb locomotion in the cat: a microstimulation study. J Neurophysiol 94: 657-672, 2005.
8. Brown TG. The intrinsic factors in the act of progression in the mammal. Proc R Soc Lond B Biol Sci 84: 308-319, 1911.
9. Brustein E, Rossignol S. Recovery of locomotion after ventral and ventrolateral spinal lesions in the cat. I. Deficits and adaptive mechanisms. J Neurophysiol 80: 1245-1267, 1998.
10. Chen XY, Carp JS, Chen L, Wolpaw JR. Corticospinal tract transection prevents operantly conditioned H-reflex increase in rats. Exp Brain Res 144: 88-94, 2002.
11. Chen XY, Wolpaw JR. Probable corticospinal tract control of spinal cord plasticity in the rat. J Neurophysiol 87: 645-652, 2002.
12. Drew T. The role of the motor cortex in the control of gait modification in the cat. In: Neurobiological Basis of Human Locomotion, edited by Shimamura M, Grillner S, Edgerton VR. Tokyo: Japan Scientific Societies, p. 201-212, 1991.
13. Dubuc R, Cabelguen JM, Rossignol S. Rhythmic fluctuations of dorsal root potentials and antidromic discharges of single primary afferents during fictive locomotion in the cat. J Neurophysiol 60: 2014-2036, 1988.
14. Forssberg H, Grillner S. The locomotion of the acute spinal cat injected with clonidine i.v. Brain Res 50: 184-186, 1973.
15. Forssberg H, Grillner S, Halbertsma J, Rossignol S. The locomotion of the low spinal cat: II. Interlimb coordination. Acta Physiol Scand 108: 283-295, 1980.
16. Frigon A, Barriere G, Leblond H, Rossignol S. Asymmetric changes in cutaneous reflexes after a partial spinal lesion and retention following spinalization during locomotion in the cat. J Neurophysiol 102: 2667-2680, 2009.
17. Frigon A, Gossard JP. Asymmetric control of cycle period by the spinal locomotor rhythm generator in the adult cat. J Physiol 587: 4617-4628, 2009.
18. Frigon A, Rossignol S. Experiments and models of sensorimotor interactions during locomotion. Biol Cybern 95: 607-627, 2006.
19. Frigon A, Rossignol S. Locomotor and reflex adaptation after partial denervation of ankle extensors in chronic spinal cats. J Neurophysiol 100: 1513-1522, 2008.
20. Frigon A, Sirois J, Gossard JP. The effects of ankle and hip muscle afferent inputs on rhythm generation during fictive locomotion. J Neurophysiol 103: 1591-1605, 2010.
21. Gorska T, Majczynski H, Bem T, Zmyslowski W. Hindlimb swing, stance and step relationships during unrestrained walking in cats with lateral funicular lesion. Acta Neurobiol Exp (Warsz) 53: 133-142, 1993.
22. Goslow GE, Reinking RM, Stuart DG. The cat step cycle: hind limb joint angles and muscle lengths during unrestrained locomotion. J Morphol 141: 1-42, 1973.
23. Grillner S. Locomotion in vertebrates: central mechanisms and reflex interaction. Physiol Rev 55: 247-304, 1975.
24. Grillner S, Halbertsma J, Nillsson J, Thorstensson A. The adaptation to speed in human locomotion. Brain Res 165: 177-182, 1979.
25. Halbertsma JM. The stride cycle of the cat: the modelling of locomotion by computerized analysis of automatic recordings. Acta Physiol Scand Suppl 521: 1-75, 1983.
26. Helgren ME, Goldberger ME. The recovery of postural reflexes and locomotion following low thoracic hemisection in adult cats involves compensation by undamaged primary afferent pathways. Exp Neurol 123: 17-34, 1993.
27. Hultborn H, Malmsten J. Changes in segmental reflexes following chronic spinal cord hemisection in the cat. I. Increased monosynaptic and polysynaptic ventral root discharges. Acta Physiol Scand 119: 405-422, 1983a.
28. Hultborn H, Malmsten J. Changes in segmental reflexes following chronic spinal cord hemisection in the cat. II. Conditioned monosynaptic test reflexes. Acta Physiol Scand 119: 423-433, 1983b.
29. Jiang W, Drew T. Effects of bilateral lesions of the dorsolateral funiculi and dorsal columns at the level of the low thoracic spinal cord on the control of locomotion in the adult cat: I. Treadmill walking. J Neurophysiol 76: 849-866, 1996.
30. Kiehn O. Locomotor circuits in the mammalian spinal cord. Annu Rev Neurosci 29: 279-306, 2006.
31. Kuhtz-Buschbeck JP, Boczek-Funcke A, Mautes A, Nacimiento W, Weinhardt C. Recovery of locomotion after spinal cord hemisection: an X-ray study of the cat hindlimb. Exp Neurol 137: 212-224, 1996.
32. Leblond H, Gossard JP. Supraspinal and segmental signals can be transmitted through separate spinal cord pathways to enhance locomotor activity in extensor muscles in the cat. Exp Brain Res 114: 188-192, 1997.
33. Lovely RG, Gregor RJ, Roy RR, Edgerton VR. Weight-bearing hindlimb stepping in treadmill-exercised adult spinal cat. Brain Res 514: 206-218, 1990.
34. Malmsten J. Time course of segmental reflex changes after chronic spinal cord hemisection in the rat. Acta Physiol Scand 119: 435-443, 1983.
35. Martinez M, Delivet-Mongrain H, Leblond H, Rossignol S. Changes in cycle structure after an incomplete spinal cord injury and then a complete spinalization in the cat. Soc Neurosci Abstr 705.25/TT27, 2011a.
36. Martinez M, Delivet-Mongrain H, Leblond H, Rossignol S. Recovery of hindlimb locomotion after incomplete spinal cord injury in the cat involves spontaneous compensatory changes within the spinal locomotor circuitry. J Neurophysiol 106: 1969-1984, 2011b.
37. Martinez M, Rossignol S. Changes in CNS structures after spinal cord lesions implications for BMI. Prog Brain Res 194: 191-202, 2011.
38. McCrea DA. Spinal circuitry of sensorimotor control of locomotion. J Physiol 533: 41-50, 2001.
39. McCrea DA, Rybak IA. Organization of mammalian locomotor rhythm and pattern generation. Brain Res Rev 57: 134-146, 2008.
40. Muir GD, Katz SL, Gosline JM, Steeves JD. Asymmetric bipedal locomotion-an adaptive response to incomplete spinal injury in the chick. Exp Brain Res 122: 275-282, 1998.
41. Murray M, Goldberger ME. Restitution of function and collateral sprouting in the cat spinal cord: the partially hemisected animal. J Comp Neurol 158: 19-36, 1974.
42. Naito A, Shimizu Y, Handa Y. Analyses of treadmill locomotion in adult spinal dogs. Neurosci Res 8: 281-290, 1990.
43. Pearson KG. Common principles of motor control in vertebrates and invertebrates. Annu Rev Neurosci 16: 265-297, 1993.
44. Pearson KG. Neural adaptation in the generation of rhythmic behavior. Annu Rev Physiol 62: 723-753, 2000.
45. Pearson KG. Role of sensory feedback in the control of stance duration in walking cats. Brain Res Rev 57: 222-227, 2008.
46. Pearson KG, Rossignol S. Fictive motor patterns in chronic spinal cats. J Neurophysiol 66: 1874-1887, 1991.
47. Philippson M. L'autonomie et la centralisation dans le système nerveux des animaux. Trav Lab Physiol Inst Solvay (Bruxelles) 7: 1-208, 1905.
48. Prochazka A, Mushahwar V, Yakovenko S. Activation and coordination of spinal motoneuron pools after spinal cord injury. Prog Brain Res 137: 1099-124, 2002.
49. Rossignol S, Dubuc R, Gossard JP. Dynamic sensorimotor interactions in locomotion. Physiol Rev 86: 89-154, 2006.
50. Rossignol S, Lund JP, Drew T. The role of sensory inputs in regulating patterns of rhythmical movements in higher vertebrates. A comparison between locomotion, respiration and mastication. In: Neural Control of Rhythmic Movements in Vertebrates, edited by Cohen A, Rossignol S, and Grillner S. New York: Wiley, p. 201-253, 1988.
51. Sakurai A, Katz PS. Functional recovery after lesion of a central pattern generator. J Neurosci 29: 13115-13125, 2009.
52. Saltiel P, Rossignol S. Critical points in the forelimb fictive locomotor cycle and motor coordination: effects of phasic retractions and protractions of the shoulder in the cat. J Neurophysiol 92: 1342-1356, 2004.
53. Wetzel MC, Atwater AE, Stuart DG. Movements of the hindlimb during locomotion of the cat. In: Neural Control of Locomotion, edited by Herman R, Grillner S, Stein P, and Stuart DG. New York: Plenum, p. 99-135, 1976.
54. Wetzel MC, Atwater AE, Wait JV, Stuart GG. Neural implications of different profiles between treadmill and overground locomotion timings in cats. J Neurophysiol 38: 492-501, 1975.
55. Whelan PJ, Hiebert GW, Pearson KG. Stimulation of the group I extensor afferents prolongs the stance phase in walking cats. Exp Brain Res 103: 20-30, 1995.
56. Wolpaw JR, Lee CL. Memory traces in primate spinal cord produced by operant conditioning of H-reflex. J Neurophysiol 61: 563-572, 1989.
57. Yakovenko S, McCrea DA, Stecina K, Prochazka A. Control of locomotor cycle durations. J Neurophysiol 94: 1057-1065, 2005.
58. Yang JF, Lamont EV, Pang MY. Split-belt treadmill stepping in infants suggests autonomous pattern generators for the left and right leg in humans. J Neurosci 25: 6869-6876, 2005.