The "beneficial" effects of locomotor training after various types of spinal lesions in cats and rats

Progress in Brain Research

Volumn 218, Issue , 2015, Pages 173-198

  Rossignol, Serge ^a,b   Martinez, Marina ^a,b   Escalona, Manuel ^a   Kundu, Aritra ^a   Delivet Mongrain, Hugo ^a   Alluin, Olivier ^a,b   Gossard, Jean Pierre ^a,b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b CANADIAN INSTITUTES OF HEALTH RESEARCH   (Canada)

Author keywords

Cats; Electromyography; Fictive locomotion; Kinematics; Locomotion; Locomotor training; Rats; Reflexes; Spinal cord injury

Indexed keywords

CAT; CENTRAL PATTERN GENERATOR; CONVALESCENCE; COORDINATION; HINDLIMB; INTERNEURON; LOCOMOTION; MOTONEURON; NONHUMAN; PRIORITY JOURNAL; RAT; REVIEW; RUBROSPINAL TRACT; SPINAL CORD INJURY; SPINAL CORD LESION; SPINAL CORD TRANSSECTION; TREADMILL; ANIMAL; ANIMAL EXPERIMENT; CLASSIFICATION; DISEASE MODEL; HEMISPHERIC DOMINANCE; NERVE CELL PLASTICITY; PHYSIOLOGY; SPINAL CORD INJURIES;

ANIMALS; CATS; DISEASE MODELS, ANIMAL; FUNCTIONAL LATERALITY; LOCOMOTION; NEURONAL PLASTICITY; PHYSICAL CONDITIONING, ANIMAL; RATS; RECOVERY OF FUNCTION; SPINAL CORD INJURIES;

EID: 84955683198     PISSN: 00796123     EISSN: 18757855     Source Type: Book Series    
DOI: 10.1016/bs.pbr.2014.12.009     Document Type: Chapter

References (110)

1. Alluin, O., Karimi-Abdolrezaee, S., Delivet-Mongrain, H., Leblond, H., Fehlings, M.G., Rossignol, S., 2011. Kinematic study of locomotor recovery after spinal cord clip compression injury in rats. J. Neurotrauma 28, 1963-1981.
2. Alluin, O., Delivet-Mongrain, H., Gauthier, M.K., Fehlings, M.G., Rossignol, S., Karimi-Abdolrezaee, S., 2014. Examination of the combined effects of chondroitinase ABC, growth factors and locomotor training following compressive spinal cord injury on neuroanatomical plasticity and kinematics. PLoS One 9, e111072.
3. Antri, M., Mouffle, C., Orsal, D., Barthe, J.Y., 2003. 5-HT1A receptors are involved in shortand long-term processes responsible for 5-HT-induced locomotor function recovery in chronic spinal rat. Eur. J. Neurosci. 18, 1963-1972.
4. Antri, M., Barthe, J.Y., Mouffle, C., Orsal, D., 2005. Long-lasting recovery of locomotor function in chronic spinal rat following chronic combined pharmacological stimulation of serotonergic receptors with 8-OHDPAT and quipazine. Neurosci. Lett. 384, 162-167.
5. Armstrong, D.M., Marple-Horvat, D.E., 1996. Role of the cerebellum and motor cortex in the regulation of visually controlled locomotion. Can. J. Physiol. Pharmacol. 74, 443-455.
6. Aymard, C., Katz, R., Lafitte, C., Lo, E., Penicaud, A., Pradat-Diehl, P., Raoul, S., 2000. Presynaptic inhibition and homosynaptic depression: a comparison between lower and upper limbs in normal human subjects and patients with hemiplegia. Brain 123 (Pt. 8), 1688-1702.
7. Baker, L.L., Chandler, S.H., 1987. Characterization of hindlimb motoneuron membrane properties in acute and chronic spinal cats. Brain Res. 420, 333-339.
8. Barbeau, H., Rossignol, S., 1987. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res. 412, 84-95.
9. Barbeau, H., Julien, C., Rossignol, S., 1987. The effects of clonidine and yohimbine on locomotion and cutaneous reflexes in the adult chronic spinal cat. Brain Res. 437, 83-96.
10. Barbeau, H., Rossignol, S., 1990. The effects of serotonergic drugs on the locomotor pattern and on cutaneous reflexes of the adult chronic spinal cat. Brain Res. 514, 55-67.
11. Barbeau, H., Rossignol, S., 1994. Enhancement of locomotor recovery following spinal cord injury. Curr. Opin. Neurol. 7, 517-524.
12. Barrière, G., Leblond, H., Provencher, J., Rossignol, S., 2008. Prominent role of the spinal central pattern generator in the recovery of locomotion after partial spinal cord injuries. J. Neurosci. 28, 3976-3987.
13. Barrière, G., Frigon, A., Leblond, H., Provencher, J., Rossignol, S., 2010. Dual spinal lesion paradigm in the cat: evolution of the kinematic locomotor pattern. J. Neurophysiol. 104, 1119-1133.
14. Barthelemy, D., Leblond, H., Provencher, J., Rossignol, S., 2006. Non-locomotor and locomotor hindlimb responses evoked by electrical microstimulation of the lumbar cord in spinalized cats. J. Neurophysiol. 96, 3273-3292.
15. Barthelemy, D., Leblond, H., Rossignol, S., 2007. Characteristics and mechanisms of locomotion induced by intraspinal microstimulation and dorsal root stimulation in spinal cats. J. Neurophysiol. 97, 1986-2000.
16. Bélanger, M., Drew, T., Provencher, J., Rossignol, S., 1996. A comparison of treadmill locomotion in adult cats before and after spinal transection. J. Neurophysiol. 76, 471-491.
17. Beloozerova, I.N., Sirota, M.G., 1988. Role of motor cortex in control of locomotion. In: Gurfinkel, V.S., Ioffe, M.E., Massion, J., Roll, J.P. (Eds.), Stance and Motion. Facts and Concepts. Plenum Press, New York, pp. 163-176.
18. Beloozerova, I.N., Sirota, M.G., 1993a. The role of the motor cortex in the control of accuracy of locomotor movements in the cat. J. Physiol. 461, 1-25.
19. Beloozerova, I.N., Sirota, M.G., 1993b. The role of the motor cortex in the control of vigour of locomotor movements in the cat. J. Physiol. 461, 27-46.
20. Beloozerova, I.N., Farrell, B.J., Sirota, M.G., Prilutsky, B.I., 2010. Differences in movement mechanics, electromyographic, and motor cortex activity between accurate and nonaccurate stepping. J. Neurophysiol. 103, 2285-2300.
21. Bouyer, L.J.G., Rossignol, S., 2003. Contribution of cutaneous inputs from the hindpaw to the control of locomotion. II. Spinal cats. J. Neurophysiol. 90, 3640-3653.
22. Brustein, E., Rossignol, S., 1998. Recovery of locomotion after ventral and ventrolateral spinal lesions in the cat. I. Deficits and adaptive mechanisms. J. Neurophysiol. 80, 1245-1267.
23. Caudle, K.L., Brown, E.H., Shum-Siu, A., Burke, D.A., Magnuson, T.S., Voor, M.J., Magnuson, D.S., 2011. Hindlimb immobilization in a wheelchair alters functional recovery following contusive spinal cord injury in the adult rat. Neurorehabil. Neural Repair 28, 7370-7375.
24. Chau, C., Barbeau, H., Rossignol, S., 1998a. Early locomotor training with clonidine in spinal cats. J. Neurophysiol. 79, 392-409.
25. Chau, C., Barbeau, H., Rossignol, S., 1998b. Effects of intrathecal α1-and α2-noradrenergic agonists and norepinephrine on locomotion in chronic spinal cats. J. Neurophysiol. 79, 2941-2963.
26. Collins III, W.F., Davis, B.M., Mendell, L.M., 1986. Amplitude modulation of EPSPs in motoneurons in response to a frequency-modulated train in single la afferent fibers. J. Neurosci. 6, 1463-1468.
27. Cote, M.P., Gossard, J.P., 2004. Step training-dependent plasticity in spinal cutaneous pathways. J. Neurosci. 24, 11317-11327.
28. Cote, M.P., Menard, A., Gossard, J.P., 2003. Spinal cats on the treadmill: changes in load pathways. J. Neurosci. 23, 2789-2796.
29. Cote, M.P., Azzam, G.A., Lemay, M.A., Zhukareva, V., Houle, J.D., 2011. Activity-dependent increase in neurotrophic factors is associated with an enhanced modulation of spinal reflexes after spinal cord injury. J. Neurotrauma 28, 299-309.
30. Courtine, G., Song, B., Roy, R.R., Zhong, H., Herrmann, J.E., Ao, Y., Qi, J., Edgerton, V.R., Sofroniew, M.V., 2008. Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat. Med. 14, 69-74.
31. Courtine, G., Gerasimenko, Y., van den, B.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., 2009. Transformation of nonfunctional spinal circuits into functional states after the loss of brain input. Nat. Neurosci. 12, 1333-1342.
32. de Leon, R.D., Hodgson, J.A., Roy, R.R., Edgerton, V.R., 1998a. Full weight-bearing hindlimb standing following stand training in the adult spinal cat. J. Neurophysiol. 80, 83-91.
33. de Leon, R.D., Hodgson, J.A., Roy, R.R., Edgerton, V.R., 1998b. Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats. J. Neurophysiol. 79, 1329-1340.
34. de Leon, R.D., Hodgson, J.A., Roy, R.R., Edgerton, V.R., 1999. Retention of hindlimb stepping ability in adult spinal cats after the cessation of step training. J. Neurophysiol. 81, 85-94.
35. de Leon, R.D., Kubasak, M.D., Phelps, P.E., Timoszyk, W.K., Reinkensmeyer, D.J., Roy, R.R., Edgerton, V.R., 2002. Using robotics to teach the spinal cord to walk. Brain Res. Brain Res. Rev. 40, 267-273.
36. Drew, T., Andujar, J.E., Lajoie, K., Yakovenko, S., 2008. Cortical mechanisms involved in visuomotor coordination during precision walking. Brain Res. Rev. 57, 199-211.
37. Edgerton, V.R., Tillakaratne, N.J., Bigbee, A.J., de Leon, R.D., Roy, R.R., 2004. Plasticity of the spinal neural circuitry after injury. Annu. Rev. Neurosci. 27, 145-167.
38. Feraboli-Lohnherr, D., Barthe, J.-Y., Orsal, D., 1999. Serotonin-induced activation of the network for locomotion in adult spinal rats. J. Neurosci. Res. 55, 87-98.
39. Fong, A.J., Cai, L.L., Otoshi, C.K., Reinkensmeyer, D.J., Burdick, J.W., Roy, R.R., Edgerton, V.R., 2005. Spinal cord-transected mice learn to step in response to quipazine treatment and robotic training. J. Neurosci. 25, 11738-11747.
40. Forssberg, H., Grillner, S., 1973. The locomotion of the acute spinal cat injected with clonidine i.v. Brain Res. 50, 184-186.
41. Forssberg, H., Grillner, S., Halbertsma, J., 1980a. The locomotion of the low spinal cat. I. Coordination within a hindlimb. Acta Physiol. Scand. 108, 269-281.
42. Forssberg, H., Grillner, S., Halbertsma, J., Rossignol, S., 1980b. The locomotion of the low spinal cat. II. Interlimb coordination. Acta Physiol. Scand. 108, 283-295.
43. Fouad, K., Metz, G.A., Merkler, D., Dietz, V., Schwab, M.E., 2000. Treadmill training in incomplete spinal cord injured rats. Behav. Brain Res. 115, 107-113.
44. Frigon, A., Gossard, J.P., 2009. Asymmetric control of cycle period by the spinal locomotor rhythm generator in the adult cat. J. Physiol. 587, 4617-4628.
45. Frigon, A., Rossignol, S., 2006. Functional plasticity following spinal cord lesions. Prog. Brain Res. 157, 231-260.
46. Frigon, A., Rossignol, S., 2007. Plasticity of reflexes from the foot during locomotion after denervating ankle extensors in intact cats. J. Neurophysiol. 98, 2122-2132.
47. Frigon, A., Rossignol, S., 2008a. Adaptive changes of the locomotor pattern and cutaneous reflexes during locomotion studied in the same cats before and after spinalization. J. Physiol. 586, 2927-2945.
48. Frigon, A., Rossignol, S., 2008b. Locomotor and reflex adaptation after partial denervation of ankle extensors in chronic spinal cats. J. Neurophysiol. 100, 1513-1522.
49. Frigon, A., Barriere, G., Leblond, H., Rossignol, S., 2009. Asymmetric changes in cutaneous reflexes after a partial spinal lesion and retention following spinalization during locomotion in the cat. J. Neurophysiol. 102, 2667-2680.
50. Gerasimenko, Y.P., Ichiyama, R.M., Lavrov, I.A., Courtine, G., Cai, L., Zhong, H., Roy, R.R., Edgerton, V.R., 2007. Epidural spinal cord stimulation plus quipazine administration enable stepping in complete spinal adult rats. J. Neurophysiol. 98, 2525-2536.
51. Giroux, N., Brustein, E., Chau, C., Barbeau, H., Reader, T.A., Rossignol, S., 1998. Differential effects of the noradrenergic agonist clonidine on the locomotion of intact, partially and completely spinalized adult cats. In: Kiehn, O., Harris-Warrick, R.M., Jordan, L.M., Hulborn, H., Kudo, N. (Eds.), Neuronal Mechanisms for Generating Locomotor Activity. Annals of the New York Academy of Sciences, New York, pp. 517-520.
52. Giroux, N., Rossignol, S., Reader, T.A., 1999. Autoradiographic study of α1-, α2-noradrenergic and serotonin 1A receptors in the spinal cord of normal and chronically transected cats. J. Comp. Neurol. 406, 402-414.
53. Giroux, N., Chau, C., Barbeau, H., Reader, T.A., Rossignol, S., 2003. Effects of intrathecal glutamatergic drugs on locomotion. II. NMDA and AP-5 in intact and late spinal cats. J. Neurophysiol. 90, 1027-1045.
54. Goldshmit, Y., Lythgo, N., Galea, M.P., Turnley, A.M., 2008. Treadmill training after spinal cord hemisection in mice promotes axonal sprouting and synapse formation and improves motor recovery. J. Neurotrauma 25, 449-465.
55. Grillner, S., 1973. Locomotion in the spinal cat. In: Stein, R.B., Pearson, K.G., Smith, R.S., Redford, J.B. (Eds.), Control of Posture and Locomotion. In: Advances in Behavioral Biology, vol. 7. Plenum Press, New York, pp. 515-535.
56. Grillner, S., 1981. Control of locomotion in bipeds, tetrapods, and fish. In: Brookhart, J.M., Mountcastle, V.B. (Eds.), Handbook of Physiology. In: The Nervous System, vol. II. American Physiological Society, Bethesda, MD, pp. 1179-1236.
57. Grillner, S., Zangger, P., 1979. On the central generation of locomotion in the low spinal cat. Exp. Brain Res. 34, 241-261.
58. Hancock, J., 1985. Motor cortical discharges and locomotion in the cat. J. Physiol. 364, 28P.
59. Helgren, M.E., Goldberger, M.E., 1993. 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.
60. Heng, C., de Leon, R.D., 2009. Treadmill training enhances the recovery of normal stepping patterns in spinal cord contused rats. Exp. Neurol. 216, 139-147.
61. Hou, J., Nelson, R., Nissim, N., Parmer, R., Thompson, F.J., Bose, P., 2014. Effect of combined treadmill training and magnetic stimulation on spasticity and gait impairments after cervical spinal cord injury. J. Neurotrauma 31, 1088-1106.
62. Hounsgaard, J., Hultborn, H., Jespersen, J., Kiehn, O., 1988. Bistability of alphamotoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan. J. Physiol. 405, 345-367.
63. Hultborn, H., Malmsten, J., 1983a. 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.
64. Hultborn, H., Malmsten, J., 1983b. Changes in segmental reflexes following chronic spinal cord hemisection in the cat. II. Conditioned monosynaptic test reflexes. Acta Physiol. Scand. 119, 423-433.
65. Hultborn, H., Denton, M.E., Wienecke, J., Nielsen, J.B., 2003. Variable amplification of synaptic input to cat spinal motoneurones by dendritic persistent inward current. J. Physiol. 552, 945-952.
66. Ichiyama, R.M., Gerasimenko, Y.P., Zhong, H., Roy, R.R., Edgerton, V.R., 2005. Hindlimb stepping movements in complete spinal rats induced by epidural spinal cord stimulation. Neurosci. Lett. 383, 339-344.
67. 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., 2008. Step training reinforces specific spinal locomotor circuitry in adult spinal rats. J. Neurosci. 28, 7370-7375.
68. Ichiyama, R., Potuzak, M., Balak, M., Kalderon, N., Edgerton, V.R., 2009.Enhancedmotor function by training in spinal cord contused rats following radiation therapy. PLoS One 4, e6862.
69. Ilha, J., Centenaro, L.A., Broetto, C.N., de Souza, D.F., Jaeger, M., do Nascimento, P.S., Kolling, J., Ben, J., Marcuzzo, S., Wyse, A.T., Gottfried, C., Achaval, M., 2011. The beneficial effects of treadmill step training on activity-dependent synaptic and cellular plasticity markers after complete spinal cord injury. Neurochem. Res. 36, 1046-1055.
70. Jiang, W., Drew, T., 1996. 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.
71. Karimi-Abdolrezaee, S., Eftekharpour, E., Wang, J., Schut, D., Fehlings, M.G., 2010. Synergistic effects of transplanted adult neural stem/progenitor cells, chondroitinase, and growth factors promote functional repair and plasticity of the chronically injured spinal cord. J. Neurosci. 30, 1657-1676.
72. Kato, M., 1992. Walking of cats on a grid: performance of locomotor task in spinal intact and hemisected cats. Neurosci. Lett. 145, 129-132.
73. Leblond, H., L'Espérance, M., Orsal, D., Rossignol, S., 2003. Treadmill locomotion in the intact and spinal mouse. J. Neurosci. 23, 11411-11419.
74. Lev-Tov, A., Pinter, M.J., Burke, R.E., 1983. Posttetanic potentiation of group Ia EPSPs: possible mechanisms for differential distribution among medial gastrocnemius motoneurons. J. Neurophysiol. 50, 379-398.
75. Li, Y., Bennett, D.J., 2003. Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J. Neurophysiol. 90, 857-869.
76. Liu, H., Skinner, R.D., Arfaj, A., Yates, C., Reese, N.B., Williams, K., Garcia-Rill, E., 2010. L-Dopa effect on frequency-dependent depression of the H-reflex in adult rats with complete spinal cord transection. Brain Res. Bull. 83, 262-265.
77. Lovely, R.G., Gregor, R.J., Roy, R.R., Edgerton, V.R., 1986. Effects of training on the recovery of full-weight-bearing stepping in the adult spinal cat. Exp. Neurol. 92, 421-435.
78. Lovely, R.G., Gregor, R.J., Roy, R.R., Edgerton, V.R., 1990. Weight-bearing hindlimb stepping in treadmill-exercised adult spinal cat. Brain Res. 514, 206-218.
79. Maier, I.C., Schwab, M.E., 2006. Sprouting, regeneration and circuit formation in the injured spinal cord: factors and activity. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1611-1634.
80. Martinez, M., Rossignol, S., 2011. Changes in CNS structures after spinal cord lesions implications for BMI. Prog. Brain Res. 194, 191-202.
81. Martinez, M., Rossignol, S., 2013. A dual spinal cord lesion paradigm to study spinal locomotor plasticity in the cat. Ann. N. Y. Acad. Sci. 1279, 127-134.
82. Martinez, M., Brezun, J.M., Zennou-Azogui, Y., Baril, N., Xerri, C., 2009. Sensorimotor training promotes functional recovery and somatosensory cortical map reactivation following cervical spinal cord injury. Eur. J. Neurosci. 30, 2356-2367.
83. Martinez, M., Delivet-Mongrain, H., Leblond, H., Rossignol, S., 2011. 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.
84. Martinez, M., Delivet-Mongrain, H., Leblond, H., Rossignol, S., 2012a. Effect of locomotor training in completely spinalized cats previously submitted to a spinal hemisection. J. Neurosci. 32, 10961-10970.
85. Martinez, M., Delivet-Mongrain, H., Leblond, H., Rossignol, S., 2012b. Incomplete spinal cord injury promotes durable functional changes within the spinal locomotor circuitry. J. Neurophysiol. 108, 124-134.
86. Martinez, M., Delivet-Mongrain, H., Rossignol, S., 2013. Treadmill training promotes spinal changes leading to locomotor recovery after partial spinal cord injury in cats. J. Neurophysiol. 109, 2909-2922.
87. Multon, S., Franzen, R., Poirrier, A.L., Scholtes, F., Schoenen, J., 2003. The effect of treadmill training on motor recovery after a partial spinal cord compression-injury in the adult rat. J. Neurotrauma 20, 699-706.
88. Murray, M., Goldberger, M.E., 1974. Restitution of function and collateral sprouting in the cat spinal cord: the partially hemisected animal. J. Comp. Neurol. 158, 19-36.
89. Nielsen, J., Petersen, N., Ballegaard, M., Biering-Sorensen, F., Kiehn, O., 1993. H-reflexes are less depressed following muscle stretch in spastic spinal cord injured patients than in healthy subjects. Exp. Brain Res. 97, 173-176.
90. 2b receptors in the thoraco-lumbar spinal cord. J. Neurophysiol. 105, 1835-1849.
91. Norton, J.A., Mushahwar, V.K., 2010. Afferent inputs to mid-and lower-lumbar spinal segments are necessary for stepping in spinal cats. Ann. N. Y. Acad. Sci. 1198, 10-20.
92. Orsal, D., Barthe, J.Y., Antri, M., Feraboli-Lohnherr, D., Yakovleff, A., Ribotta, M., Privat, A., Provencher, J., Rossignol, S., 2002. Locomotor recovery in chronic spinal rat: long-term pharmacological treatment or transplantation of embryonic neurons? Prog. Brain Res. 137, 213-230.
93. Pearson, K.G., Rossignol, S., 1991. Fictive motor patterns in chronic spinal cats. J. Neurophysiol. 66, 1874-1887.
94. Ribotta, M.G., Provencher, J., Feraboli-Lohnherr, D., Rossignol, S., Privat, A., Orsal, D., 2000. Activation of locomotion in adult chronic spinal rats is achieved by transplantation of embryonic raphe cells reinnervating a precise lumbar level. J. Neurosci. 20, 5144-5152.
95. Rossignol, S., Frigon, A., 2011. Recovery of locomotion after spinal cord injury: some facts and mechanisms. Annu. Rev. Neurosci. 34, 413-440.
96. Rossignol, S., Giroux, N., Chau, C., Marcoux, J., Brustein, E., Reader, T.A., 2001. Pharmacological aids to locomotor training after spinal injury in the cat. J. Physiol. 533, 65-74.
97. Rossignol, S., Dubuc, R., Gossard, J.P., 2006. Dynamic sensorimotor interactions in locomotion. Physiol. Rev. 86, 89-154.
98. Rossignol, S., Barriere, G., Alluin, O., Frigon, A., 2009. Re-expression of locomotor function after partial spinal cord injury. Physiology (Bethesda) 24, 127-139.
99. Rossignol, S., Frigon, A., Barriere, G., Martinez, M., Barthelemy, D., Bouyer, L., Belanger, M., Provencher, J., Chau, C., Brustein, E., Barbeau, H., Giroux, N., Marcoux, J., Langlet, C., Alluin, O., 2011. Spinal plasticity in the recovery of locomotion. Prog. Brain Res. 188, 229-241.
100. Roy, R.R., Harkema, S.J., Edgerton, V.R., 2012. Basic concepts of activity-based interventions for improved recovery of motor function after spinal cord injury. Arch. Phys. Med. Rehabil. 93, 1487-1497.
101. Schindler-Ivens, S., Shields, R.K., 2000. Low frequency depression of H-reflexes in humans with acute and chronic spinal-cord injury. Exp. Brain Res. 133, 233-241.
102. Shields, R.K., Dudley-Javoroski, S., Oza, P.D., 2011. Low-frequency H-reflex depression in trained human soleus after spinal cord injury. Neurosci. Lett. 499, 88-92.
103. Singh, A., Balasubramanian, S., Murray, M., Lemay, M., Houle, J., 2011. Role of spared pathways in locomotor recovery after body-weight-supported treadmill training in contused rats. J. Neurotrauma 28, 2405-2416.
104. Slawinska, U., Majczynski, H., Djavadian, R., 2000. Recovery of hindlimb motor functions after spinal cord transection is enhanced by grafts of the embryonic raphe nuclei. Exp. Brain Res. 132, 27-38.
105. Slawinska, U., Miazga, K., Cabaj, A.M., Leszczynska, A., Majczynski, H., Nagy, J.I., Jordan, L.M., 2013. Grafting of fetal brainstem 5-HT neurons into the sublesional spinal cord of paraplegic rats restores coordinated hindlimb locomotion. Exp. Neurol. 247, 572-581.
106. Stevens, J.E., Liu, M., Bose, P., O'Steen, W.A., Thompson, F.J., Anderson, D.K., Vandenborne, K., 2006. Changes in soleus muscle function and fiber morphology with one week of locomotor training in spinal cord contusion injured rats. J. Neurotrauma 23, 1671-1681.
107. Thota, A., Carlson, S., Jung, R., 2001. Recovery of locomotor function after treadmill training of incomplete spinal cord injured rats. Biomed. Sci. Instrum. 37, 63-67.
108. Tillakaratne, N.J., de Leon, R.D., Hoang, T.X., Roy, R.R., Edgerton, V.R., Tobin, A.J., 2002. Use-dependent modulation of inhibitory capacity in the feline lumbar spinal cord. J. Neurosci. 22, 3130-3143.
109. Weber, E.D., Stelzner, D.J., 1977. Behavioral effects of spinal cord transection in the developing rat. Brain Res. 125, 241-255.
110. Yates, C., Garrison, K., Reese, N.B., Charlesworth, A., Garcia-Rill, E., 2011. Chapter 11-novel mechanism for hyperreflexia and spasticity. Prog. Brain Res. 188, 167-180.