Recovery of locomotion has been considered unattainable following a clinically complete or severe incomplete spinal cord injury even after conventional therapy. However, the locomotion of spinal animals can be improved by training that provides complex temporal patterns of sensory information related to stepping that is interpreted by the spinal cord. This review discusses the evidence that suggests human spinal networks can integrate and interpret complex sensory signals to produce functional efferent output and adapt to repetitive training. Locomotor training, a new rehabilitative approach, is based on principles that promote the movement of limbs and trunk to generate sensory information consistent with locomotion to improve the potential for the recovery of walking after neurologic injury.
Andersson O, Grillner S. 1983. Peripheral control of the cat’s step cycle: II. Entrainment of the central pattern generators for locomotion by sinusoidal hip movements during “fictive locomotion.” Acta Physiol Scand118:229-239.
2.
Barbeau H, Blunt R. 1991. A novel interactive locomotor approach using body weight support to retrain gait in spastic paretic subjects. In: Wernig A, editor. Plasticity of motorneuronal connections. Amsterdam, the Netherlands: Elsevier Science. p 461-474.
3.
Barbeau H, Chau C, Rossignol S. 1993. Noradrenergic agonists and locomotor training affect locomotor recovery after cord transection in adult cats. Brain Res Bull30:387-393.
4.
Barbeau H, Rossignol S. 1987. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res412:84-95.
5.
Barbeau H, Wainberg M, Finch L. 1987. Description and application of a system for locomotor rehabilitation. Med Biol Eng Comput25:341-344.
6.
Behrman A, Harkema S. 2000. Locomotor training after human spinal cord injury: a series of case studies. Phys Ther80:688-700.
7.
Beres JA, Johnson TD, Harkema SJ. 2001. Clonus after human spinal cord injury cannot be attributed solely to recurrent muscle-tendon stretch. J Neurophysiol. Submitted.
8.
Bussel B, Roby-Brami A, Azouvi P, Biraben A, Yakovleff A, Held P. 1988. Myoclonus in a patient with spinal cord transection. Brain111:1235-1245.
9.
Bussel B, Roby-Brami A, Yakovleff A, Bennis N. 1989. Late flexion reflex in paraplegic patients. Evidence for spinal stepping generator. Brain Res Bull22:53-56.
Capaday C, Stein RB. 1986. Amplitude modulation of the soleus H-reflex in the human during standing and walking. J Neurosci6:1308-1313.
12.
Conrad B, Benecke R, Meinck HM. 1985. Gait disturbances in para-spastic patients. In: Delwaide PJ, Young R, editors. Clinical neurophysiology in spasticity. Amsterdam, the Netherlands: Elsevier. p 155-174.
13.
Conway BA, Hultborn H, Kiehn O. 1987. Proprioceptive input resets central locomotor rhythm in the spinal cat. Exp Brain Res68:643-656.
14.
Crenna P, Frigo C. 1987. Excitability of the soleus H-reflex arc during walking and stepping in man. Exp Brain Res66:49-60.
15.
de Leon RD, Hodgson JA, Roy RR, Edgerton VR. 1998a. Full weight-bearing hindlimb standing following stand training in the adult spinal cat. J Neurophysiol80:83-91.
16.
de Leon RD, Hodgson JA, Roy RR, Edgerton VR. 1998b. Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats. J Neurophysiol79:1329-1340.
17.
de Leon RD, Hodgson JA, Roy RR, Edgerton VR. 1999. Retention of hindlimb stepping abililty in adult spinal cats after the cessation of step training. J Neurophysiol81:85-94.
18.
Dietz V, Colombo G, Jensen L. 1994. Locomotor activity in spinal man. Lancet344:1260-1263.
19.
Dietz V, Colombo G, Jensen L, Baumgartner L. 1995. Locomotor capacity of spinal cord in paraplegic patients. Ann Neurol37:574-582.
20.
Dietz V, Curt A, Colombo G. 1998. Locomotor pattern in paraplegic patients: training effects and recovery of spinal cord function. Spinal Cord36:380-390.
21.
Dietz V, Nakazawa K, Wirz M, Erni T. 1999. Level of spinal cord lesion determines locomotor activity in spinal man. Exp Brain Res128:405-409.
22.
Dietz V, Wirz M, Colombo G, Curt A. 1998. Locomotor capacity and recovery of spinal cord function in paraplegic patients: a clinical and electrophysiological evaluation. Electroencephalogr Clin Neurophysiol109:140-153.
23.
Dimitrijevic MR, Gerasimenko Y, Pinter MM. 1998. Evidence for a spinal central pattern generator in humans. Ann N Y Acad Sci860:360-376.
24.
Ditunno JF, Young W, Donovan WH, Creasey G. 1994. The international standards booklet for neurological and functional classification of spinal cord injury. Paraplegia32:70-80.
25.
Dobkin BH, Harkema SJ, Requejo PS, Edgerton VR. 1995. Modulation of locomotor-like EMG activity in subjects with complete and incomplete spinal cord injury. J Neurol Rehabil9:183-190.
26.
Duysens J, Pearson KG. 1980. Inhibition of flexor burst generation by loading ankle extensor muscle in walking cats. Brain Res187:321-332.
27.
Duysens J, Trippel M, Horstmann GA, Dietz V. 1990. Gating and reversal of reflexes in ankle muscles during human walking. Exp Brain Res82:351-358.
28.
Edgerton VR, Grillner S, Sjostrom A, Zangger P. 1976. Central generation of locomotion in vertebrates. In: Herman S, Grillner S, Stein P, Stuart DG, editors. Neural control of locomotion. New York: Plenum. p 439-464.
29.
Eidelberg E, Walden JG, Nguyen LH. 1981. Locomotor control in macaque monkeys. Brain104:647-663.
30.
Erni T, Colombo G. 1998. Locomotor training in paraplegic patients: a new approach to assess changes in leg muscle EMG patterns [published erratum appears in Electroencephalogr Clin Neurophysiol 1998 Aug;109(4):385]. Electroencephalogr Clin Neurophysiol109:135-139.
31.
Fedirchuk B, Nielsen J, Petersen N, Hultborn H. 1998. Pharmacologically evoked fictive motor patterns in the acutely spinalized marmoset minkey (Callithrix jacchus). Exp Brain Res122:351-361.
32.
Fung J, Barbeau H. 1989. A dynamic EMG profile index to quantify muscular activation disorder in spastic paretic gait. Electroencephalogr Clin Neurophysiol73:233-244.
33.
Fung J, Stewart JE, Barbeau H. 1990. The combined effects of clonidine and cyproheptadine with interactive training on the modulation of locomotion in spinal cord injured subjects. J Neurol Sci100:85-93.
34.
Gordon KE, Ferris DP, Beres JA, Roberton M, Harkema SJ. 2000. The importance of using an appropriate body weight support system in locomotor training. Soc Neurosci26:160.
35.
Gossard JP, Hultborn H. 1991. The organization of the spinal rhythm generation in locomotion. In: Wernig A, editor. Plasticity of motoneural connections. Amsterdam, the Netherlands: Elsevier Science. p 385-404.
36.
Grillner S. 1981. Control of locomotion in bipeds, tetrapods, and fish. In: Handbook of physiology: the nervous system II. Bestheda, MD: American Physiological Society. p 1179-1236.
37.
Grillner S. 1985. Neurobiological bases of rhythmic motor acts in vertebrates. Science228:143-149.
38.
Grillner S, Rossignol S. 1978. On the initiation of the swing phase of locomotion in chronic spinal cats. Brain Res146:269-277.
39.
Grillner S, Zangger P. 1975. How detailed is the central pattern generation for locomotion? Brain Res88:367-371.
40.
Grillner S, Zangger P. 1979. On the central generation of locomotion in the low spinal cat. Exp Brain Res34:241-261.
41.
Harkema SJ, Dobkin BH, Edgerton VR. 2000. Pattern generators in locomotion: implications for recovery of walking after spinal cord injury. Top Spinal Cord Injury Rehabil6:82-96.
Jankowska E, Jukes MG, Lund S, Lundberg A. 1967a. The effect of DOPA on the spinal cord: 5. Reciprocal organization of pathways transmitting excitatory action to alpha motoneurones of flexors and extensors. Acta Physiol Scand70:369-388.
44.
Jankowska E, Jukes MG, Lund S, Lundberg A. 1967b. The effect of DOPA on the spinal cord: 6. Half-centre organization of interneurones transmitting effects from the flexor reflex afferents. Acta Physiol Scand70:389-402.
45.
Lovely RG, Gregor R, Roy RR, Edgerton VR. 1986. Effects of training on the recovery of full-weight-bearing stepping in the adult spinal cat. Exp Neurol92:421-435.
46.
Maegele M, Müller S, Wernig A, Edgerton VR, Harkema SJ. 2001. Differential recruitment of spinal motor pools during voluntary attempts at lower limb movements versus load bearing stepping following human spinal cord injury. J Neurotrauma. Forthcoming.
47.
Maynard FM, Bracken MB, Creasey G, Ditunno JF, Donovan WH, Ducker TB, and others. 1997. International standards for neurological and functional classification of spinal cord injury. Spinal Cord35:266-274.
48.
Norman KE, Pepin A, Ladouceur M, Barbeau H. 1995. A treadmill apparatus and harness support for evaluation and rehabilitation of gait. Arch Phys Med Rehabil76:772-778.
49.
Patel UK, Dobkin BH, Edgerton VR, Harkema SJ. 1998. The response of neural locomotor circuits to changes in gait velocity. Soc Neurosci24:2104.
50.
Roby-Brami A, Bussel B. 1987. Long-latency spinal reflex in man after flexor reflex afferent stimulation. Brain110:707-725.
51.
Stewart JE, Barbeau H, Gauthter L. 1991. Modulation of locomotor patterns and spasticity with clonidine in spinal cord injured patients. Can J Neurol Sci18:321-332.
52.
Vilensky JA, Moore GP, Eidelberg E, Walden J. 1992. Recovery of locomotion in monkeys with spinal cord lesions. J Motor Behav24:288-296.
53.
Visintin M, Barbeau H. 1994. The effects of parallel bars, body weight support and speed on the modulation of the locomotor pattern of spastic paretic gait. A preliminary communication. Paraplegia32:540-553.
54.
Wernig A, Müller S. 1991. Improvement of walking in spinal cord injured persons after treadmill training. Amsterdam, the Netherlands: Elsevier Science. p 475-485.
55.
Wernig A, Müller S, Nanassy A, Cagol E. 1992. Laufband locomotion with body weight support improved walking in persons with severe spinal cord injuries. Paraplegia30:229-238.
56.
Wernig A, Müller S, Nanassy A, Cagol E. 1995. Laufband therapy based on “rules of spinal locomotion” is effective in spinal cord injured persons. Eur J Neurosci7:823-829.
57.
Wernig A, Nanassy A, Mueller WM. 1999. Laufband (treadmill) therapy in incomplete paraplegia and tetraplegia. J Neurotrauma16:719-726.
58.
Wernig A, Nanassy A, Müller S. 1998. Maintenance of locomotor abilities following Laufband (treadmill) therapy in para- and tetraplegic persons: follow-up studies. Spinal Cord36:744-749.
59.
Yang JF, Fung J, Edamura M, Blunt R, Stein RB, Barbeau H. 1991. H-reflex modulation during walking in spastic paretic subjects. Can J Neurol Sci18:443-452.
