Neural control of locomotion; Part 1: The central pattern generator from cats to humans

Gait and Posture

Volumn 7, Issue 2, 1998, Pages 131-141

  Duysens, Jacques ^a   Van De Crommert, Henry W A A ^b  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b SINT MAARTENSKLINIEK   (Netherlands)

Author keywords

Cat; Central pattern generator (CPG); Human; Locomotion; Spinal cord; Spinal cord injury (SCI)

Indexed keywords

CAT; HUMAN; LOCOMOTION; MOTOR CONTROL; NONHUMAN; PATTERN GENERATOR; PRIORITY JOURNAL; REVIEW; SPINAL CORD INJURY;

EID: 0031976869     PISSN: 09666362     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0966-6362(97)00042-8     Document Type: Review

References (116)

1. Grillner S, Wallen P. Central pattern generators for locomotion, with special reference to vertebrates. Ann Rev Neurosci 1985;8:233-61.
2. Prochazka A, Stephens JA, Wand P. Muscle spindle discharge in normal and obstructed movements. J Physiol 1979;287:57-66.
3. Perret C, Cabelguen JM. Main characteristics of the hindlimb locomotor cycle in the decorticate cat with special reference to bifunctional muscles. Brain Res 1980;187:333-52.
4. Wisleder D, Zernicke RF, Smith JL. Speed-related changes in hindlimb intersegmental dynamics during the swing phase of cat locomotion. Exp Brain Res 1990;79:651-60.
5. Van de Crommert HWAA, Mulder T, Duysens J. Neural control of locomotion; Part 2: Sensory control of the locomotor CPG. Gait Pos (in press).
6. Grillner S. Neurobiological bases on rhythmic motor acts in vertebrates. Science 1985;228:143-9.
7. Weiss P. Central versus peripheral factors in the development of coordination. In: Bard P, editor. Patterns of Organization in the Central Nervous System. Chap. 1. Williams and Wilkins, 1952:2-23.
8. Forssberg H, Svartengren G. Hardwired locomotor network in cat revealed by a retained motor pattern to gastrocnemius after muscle transposition. Neurosci Lett 1983;42:283-8.
9. Gordon T, Stein RB, Thomas CK. Innervation and function of hind-limb muscles in the cat after cross-union of the tibial and peroneal nerves. J Physiol Lond 1986;374:429-41.
10. Sperry RW. The functional results of muscle transposition in the hindlimb of the rat. J Comp Neurol 1940;73:379-404.
11. Brown TG. The intinsic factors in the act of progression in the mammal. Proc R Soc Lond 1911;B84:308-19.
12. Brown TG. The factors in rhythmic activity of the nervous system. Proc R Soc London Ser 1912;B85:278-89.
13. Rossignol S. Neural control of stereotypic limb movements. In: Rowell, Sheperd JT, editors. Exercise: Regulation and Integration of Multiple Systems. Handbook of Physiology. Sec. 12. Bethseda: America Physiological Society, 1996:173-216.
14. Grillner S, Zangger P. How detailed is the central pattern generator for locomotion? Brain Res 1975;88:367-71.
15. Coggeshall RE, Coulter JD, Willis WD Jr. Unmyelinated fibers in the ventral root. Brain Res 1997;57(1):229-33.
16. Loeb GE. Ventral root projections of myelinated dorsal root ganglion cells in the cat. 1976;106:159-65.
17. 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.
18. Coggeshall RE. Law of separation of function of the spinal roots. Physiol Rev 1980;60:716-56.
19. Shik ML, Orlovsky GN. Neurophysiology of locomotor automatism. Physiol Rev 1976;55:465-501.
20. Shik ML, Orlovsky GN, Severin FV. Organization of locomotor synergism. Biophysics 1966a;11:1011-19.
21. Shik ML, Severin FV, Orlovsky GN. Control of walking and running by means of electrical stimulation of the mid-brain. Biophysics 1966b;11:756-65.
22. Shik ML, Orlovsky GN, Severin FV. Locomotion of the mesencephalic cat elicited by stimulation of the pyramids. Biophysics 1968;13:143-52.
23. Cruse H, Warnecke H. Coordination of the legs of a slow-walking cat. Exp Brain Res 1992;89:147-56.
24. Giuliani CA, Smith JL. Stepping behaviors in chronic spinal cats with one hindlimb deafferented. J Neurosci 1987;7:2537-46.
25. Forssberg H, Grillner S, Halbertsma J. The locomotion of the low spinal cat. I. Coordination within a hindlimb. Acta Physiol Scand 1980a;108:269-81.
26. Forssberg H, Grillner S, Halbertsma J, Rossignol S. The locomotion of the low spinal cat. II. Interlimb coordination. Acta Physiol Scand 1980b;108:283-95.
27. Barbeau H, Rossignol S. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res 1987;412:84-95.
28. Brown TG, Sherrington CS. The rule of reflex response in the limb reflexes of the mammal and its exceptions. J Physiol 1912;44:125-30.
29. Jankowska E, Jukes MGM, Lund S, Lundberg A. The effects of DOPA on the spinal cord. 5 Reciprocal organization of pathways transmitting excitatory action to alpha motoneuroned of flexors and extensors. Acta Physiol Scand 1967;70:369-88.
30. Lundberg A. Half centers revisited. In: Szentagothai J, Palkovits M, Hamori J, editors. Regulatory Functions of the CNS. Principles of Motion and Organization. Academiai Kiado, Budapest, Oxford: Pergamon, 1981:155-67.
31. Gossard JP, Brownstone RM, Barajon I, Hultborn H. Transmission in a locomotor-related group Ib pathway from hindlimb extensor muscles in the cat. Exp Brain Res 1994;98:213-28.
32. Chandler SH, Baker LL, Goldberg LJ. Characterization of synaptic potentials in hindlimb extensor motoneurons during L-DOPA-induced fictive locomotion in acute and chronic spinal cats. Brain Res 1984;303:91-100.
33. Fleshman JW, Lev-Tov A, Burke RE. Peripheral and central control of flexor digitorum longus and flexor hallucis longus motoneurons; the synaptic basis of functional diversity. Exp Brain Res 1984;54:133-49.
34. Floeter MK, Sholomenko GN, Gossard J-P, Burke TE. Disynaptic excitation from the medial longitudinal fasciculus to lumbosacral motoneurons: modulation by repetitive activation, descending pathways, and locomotion. Exp Brain Res 1993;92:407-19.
35. Miller S, Van der Burg J, Van der Meche FGA. Coordination of movements of the hindlimbs and forelimbs in different forms of locomotion in normal and decerebrate cats. Brain Res 1975;91:217-37.
36. Amemiya M, Yamaguchi T. Fictive locomotion of the forelimb evoked by stimulation of the mesencephalic locomotor region in the decerebrate cat. Neurosci Lett 1984;50:91-6.
37. Yamaguchi T. Muscle activity during forelimb stepping in decerebrate cats. Jpn J Physiol 1992;42:489-99.
38. Buford JA, Smith JL. Adaptive control for backward quadrupedal walking. III Stumbling corrective reactions and cutaneous reflex sensitivity. J Neurophysiol 1993;70:1102-14.
39. Pearson KG, Rossignol S. Fictive motor patterns in chronic spinal cats. J Neurophysiol 1991;66:1009-17.
40. Goldberger ME. Locomotor recovery after unilateral hindlimb deafferentation in cats. Brain Res 1977;123:59-74.
41. Smith JL. Hindlimb locomotion of the spinal cat: synergistic patterns, limb dynamics and novel blends. In: Gurfinkel VS, Ioffe ME, Massion J, Roll JP, editors. Stance and Motion. London: Plenum. 1986:185-97.
42. Smith JL, Chung SH, Zernicke RF. Gait-related motor pattern and hindlimb kinetics for the cat trot and gallop. Exp Brain Res 1993;94:308-22.
43. Grillner S. Control of locomotion in bipeds, tetrapods, and fish. In: Brookhart JM, Mountcastle VB, editors. Handbook of Physiology. American Physiological Society 1981:1179-236.
44. Rossignol S, Dubuc R. Spinal pattern generation. Curr Opin Neurobiol 1994;4:894-902.
45. Armstrong DM. The supraspinal control of mammalian locomotion. J Physiol Lond 1988;405:1-37.
46. Philippson M. L'autonomie et la centralisation dans le systéme nerveux des animaux. Trav Lab Physiol Inst Solvay (Brussels) 1905;7:1-208.
47. Eidelberg E. Consequences of spinal cord lesions upon motor function, with special reference to locomotor activity. Prog Neurobiol 1981a;17:185-202.
48. Vilensky JA, Moore AM, Eidelberg E, Walden JG. Recovery of locomotion in monkeys with spinal cord lesions. J Mot Behav 1992;24(3):288-96.
49. Vilensky JA, O'Connor BL. Stepping in humans with complete spinal cord transection: a phylogenetic evaluation. Mot Cont 1997;1:284-92.
50. Hultborn H, Petersen N, Brownstone P, Nielsen J. Evidence of fictive spinal locomotion in the marmoset (Callithrix Jacchus). Soc Neurosci Abstr 1993;19:539.
51. Roby-Brami A, Bussel B. Long latency spinal reflex in man after flexor reflex afferent stimulation. Brain 1987;110:707-25.
52. Roby-Brami A, Bussel B. Effects of flexor reflex afferent stimulation on the soleus H reflex in patients with a complete spinal cord lesion: evidence for a presynaptic inhibition of Ia transmission. Exp Brain Res 1990;81:593-601.
53. Roby-Brami A, Bussel B. Inhibitory effect on flexor reflexes in patients with a complete spinal cord section. Exp Brain Res 1992;90:201-8.
54. Bussel B, Roby-Brami A, Azouvi P. Organization of reflexes elicited by flexor reflex afferents in paraplegic man: evidence for a spinal stepping generator. In: Jami L, Pierrot-Deseilligny E, Zytnicki D, editors. Muscle Afferents and Spinal Control of Movement. Oxford: Pergamon, 1991:427.
55. Roby-Brami A, Bussel B. Late flexion reflex in paraplegic patients: evidence for a spinal stepping generator. In: Thilmann et al. (editors). Mechanisms and Management. Heidelberg: Springer, 1993:333-43.
56. Duysens J. Reflex control locomotion as revealed by stimulation of cutaneous afferents in spontaneously walking premammillary cats. J Neurophysiol 1977;140:737-51.
57. Lhermite J. La section totale de la moelle dorsal. Tardy Pigelet, Bourges, 1919.
58. Kuhn RA. Functional capacity of the isolated human spinal cord. Brain 1950;73:1-51.
59. Bussel B, Roby-Brami A, Azouvi P, Biraben A, Yakovleff A, Held JP. Myoclonus in a patient with a spinal cord transection. Possible involvement of the spinal stepping generator. Brain 1988;111:1235-45.
60. Bussel B, Roby-Brami A, Rémi Néris O, Yakovleff A. Evidence for a spinal stepping generator in man. Paraplegia 1996;34:91-2.
61. Schalow G, Blanc Y, Jeltsch W, Zäch GA. Electromyographic identification of spinal oscillator patterns and recouplings in a patient with incomplete spinal cord lesion: oscillator formation training as a method to improve motor activities. Gen Physiol Biophys 1996;15(1):121-220.
62. Calancie B, Needham-Shropshire B, Jacobs P, Willer K, Zych G, Green BA. Involuntary stepping after chronic spinal cord injury. Evidence for a central rhythm generator for locomotion in man. Brain 1994;117:1143-59.
63. Dobkin BH, Harkema S, Requejo P, Edgerton R. Modulation of locomotor-like EMG activity in subjects with complete and incomplete spinal cord injury. J Neuro Rehab 1995;9:183-90.
64. Hanna JP, Frank JI. Automatic stepping in the pontomedullary stage of central herniation. Neurology 1995;45:985-6.
65. Luys J. Le cerveau et ses fonctions. Paris, 1893:139-41.
66. Coleman RM, Pollak CP, Weitzman ED. Periodic movements in sleep (noctural myoclonus): relation to sleep disorders. Ann Neurol 1980;8:416-21.
67. Lugaresi E, Cirigotta F, Coccagna G, Montagna P. Nocturnal myoclonus and restless leg syndrome. Adv Neurol 1986;43:295-307.
68. Bixler EO, Kales A, Vela-Bueno A, Jacoby JA, Scarone S, Soldatos CR. Nocturnal myoclonus and nocturnal myoclonic activity in a normal population. Res Commun Chem Pathol Pharmacol 1982;36:129-40.
69. Yokota T, Hirose K, Tanabe H, Tsukagoshi H. Sleep-related periodic leg movements (nocturnal myoclonus) due to spinal cord lesion. J Neurol Sci 1991;104(1):13-8.
70. Lee MS, Choi YC, Lee LS, Lee SB. Sleep-related periodic leg movements assocoiated with spinal cord lesions. Move Disord 1996;11(6):719-22.
71. Dickel MJ, Renfrow SD, Moore PT, Berry RB. Rapid eye movement sleep periodic leg movements in patients with spinal cord injury. Sleep 1994;17(8):733-8.
72. Groen JHM, Kamphuisen HAC. Periodic nocturnal myoclonus in a patient with hyperekplexia (startle disease). J Neurol Sci 1978;38:207-13.
73. Koning-Tijssen MAJ de. Hyperekplexia - startle disease. Thesis, Leiden. 1997:1-173.
74. Avelev V, Anissimova N, Khoroshikh E, Gerasimenko Y. Activation of central pattern generator in cat by epidural spinal cord stimulation. In: Gurfinkel VS, Levik Yu S, editors. Proceedings of the International Symposium on Brain and Movement St. Petersburg, Moscow, 1997:26.
75. Rosenfeld JE, Sherwood AM, Halter JA, Dimitrijevic MR. Evidence of a pattern generator in paralyzed subject with spinal cord stimulation. Soc Neurosci Abstr 1995;21:688.
76. Gerasimenko YP, Makarovsky AN. Neurophysiological evaluation of the effects of spinal cord stimulation in spinal patients. In: Stuart DG, Gatchev GN, Gurfunkel VS, Wiesendangerr M, editors. Motor Control VII. Tucson: Motor Control. 1996a:153-7.
77. Gerasimenko Y, McKay WB, Pollo FE, Dimitrijevic MR. Stepping movements in paraplegic patients induced by epidural spinal cord stimulation. Soc Neurosci Abstr 1996b;22:1372.
78. Shapkova HY, Shapkov YT, Mushkin AY. Locomotor activity in paraplegic children induced by spinal cord stimulation. In: Gurfinkel VS, Levik Yu S, editors. Proceedings of the International Symposium on Brain and Movement. St. Petersburg, Moscow. 1997:170-1.
79. Dimitrijevic MR, Pinter M, Sherwood AM. The effect of reduced suprasegmental input as a result of spinal cord injury on stepping movement induced by epidural stimulation of the lumbar enlargement in humans. In: Gurfinkel VS, Levik Yu S, editors. Proceedings of the International Symposium on Brain and Movement, St. Petersburg, Moscow, 1997:59.
80. Dimitrijevic MR, Gerasimenko Y, Pollo FE. Sustained epidural electrical stimulation of the spinalized lumbar cord in humans can facilitate or suppress spinal reflex and central pattern generator activities. In: Gurfinkel VS, Levik Yu S, editors. Proceedings of the International Symposium on Brain and Movement, St. Petersburg, Moscow, 1997:60.
81. Gerasimenko Y, Avelev V, Anissimova N, Dubrovin V, Makaravsky A, Nikitin O. Motor control functions of the spinal cord in paraplegic patients and in cats with various lesions of CNS. In: Gurfinkel VS, Levik Yu S, editors. Proceedings of the International Symposium on Brain and Movement. St. Petersburg, Moscow, 1997:79.
82. Selionov VA, Kazennikov OV, Levik YS, Gurfinkel VS. Experimental investigation of locomotor-like movements elicited by vibration in human. In: Gurfinkel VS, Levik Yu S, editors. Proceedings of the International Symposium on Brain and Movement, St. Petersburg, Moscow, 1997:167.
83. Kazennikov O, Selionov V, Levik Y, Gurfinkel V. Sensory facilitation of the vibratory evoked air-stepping in human. In: Gurfinkel VS, Levik Yu S editors. Proceedings of the International Symposium on Brain and Movement. St. Petersburg, Moscow, 1997:104.
84. Robinson GA, Goldberger ME. The development and recovery of motor function in spinal cats. I. The infant lesion effect. Exp Brain Res 1986;62:373-86.
85. Patla AE. Neurobiomechanical bases for the control of human locomotion. In: Bronstein A, Brandt T, Wolloncott MH, editors. Clinical Disorders of Balance, Posture and Gait. London: Arnold, 1995:19-40.
86. Forssberg H. Ontogeny of human locomotor control. I. Infant stepping, supported locomotion and transition to independent locomotion. Exp Brain Res 1985;57(3):480-93.
87. Thelen E, Cooke DW. Relationship between newborn stepping and later walking: a new interpretation. Dev Med Child Neurol 1987;29(3):380-93.
88. Rayburn WF. Fetal movement monitoring. Clin Obstet Gynecol 1995;38(1):59-67.
89. Pearson KG. Common principles of motor control in vertebrates and invertebrates. Ann Rec Neurosci 1993;265-97.
90. Clarac F. Spatial and temporal co-ordination during walking in Crustacea. Trends Neurosci 1984;7:3293-8.
91. Buford JA, Smith JL. Adaptive control of backward quadriped walking. II Hindlimb muscle synergies. J Neurophysiol 1990;64:756-66.
92. Thorstensson A. How is the normal locomotor program modified to produce backward walking? Exp Brain Res 1986;61:644-68.
93. Perell KI, Gregor RJ, Buford JA, Smith JC. Adaptive control for backward quadrupedal walking. IV. Hindlimb kinetics during stance and swing. J Neurophysiol 1993;70:2226-40.
94. Vilensky JA, Gankiewicz E, Gehlsen GA. Kinematic comparison of backward and forward walking in humans. J Hum Move Stud 1987;13:29-50.
95. Winter DA, Pluck N, Yang JF. Backward walking a simple reversal of forward walking. J Mot Behav 1989;21:291-305.
96. Duysens J, Tax AAM, Murrer L, Dietz V. Backward and forward walking use different patterns of phase-dependent modulation of cutaneous reflexes in humans. J Neurophysiol 1996;76(1):301-10.
97. Whelan P. Control of locomotion in the decerebrate cat. Prog Neurobiol 1996;49:481-515.
98. Jordan LM, Pratt CA, Menzies JE. Locomotion evoked by brain stem stimulation: occurence without phasic segmental afferent input. Brain Res 1979;177:204-7.
99. Eidelberg E, Walden JG, Nguyen LH. Locomotor control in macaque monkeys. Brain 1981b;104:647-63.
100. Masdeu JC, Alampur U, Cavaliere R, Tavoulareas G. Astasia and gait failure with damage of the pontomescencephalic locomotor region. Ann Neurol 1994;35:619-21.
101. Budakova N. Stepping movements in the spinal cat due to DOPA administration. Fioziol Zh SSSR 1973;59:1190-8.
102. Forssberg H, Grillner S. The locomotion of the acute spinal cat injected with clonidine i.v. Brain Res 1973;50:184-6.
103. Grillner S, Zangger P. On the central generation of locomotion in the low spinal cat. Exp Brain Res 1979;34:241-61.
104. Barbeau H, Chau C, Rossignol S. Noradrenergic agonists and locomotor training affect locomotor recovery after cord transection in adult cats. Brain Res Bull 1993;30:387-93.
105. Barbeau H, Julien C, Rossignol S. The effects of clonidine and yohimbine on locomotion and cutaneous reflexes in the adult chronic spinal cat. Brain Res 1987;437(1):83-96.
106. Barbeau H, Rossignol S. Initiation and modulation of locomotor pattern in the adult chronic spinal cat by noradrenergic, serotonergic and dopaminergic drugs. Brain Res 1991;546:250-60.
107. Russel D, Zajac F. Effects of stimulating Deiter's nucleus and medial longitudinal fasciculus on the timing of the fictive locomotor rhythm induced in cats by DOPA. Brain Res 1979;177:588-92.
108. Dietz V, Colombo G, Jensen L. Locomotor activity in spinal man. Lancet 1994;344:1260-3.
109. Dietz V, Colombo G, Jensen L, Baumgartner L. Locomotor capacity of spinal cord in paraplegic patients. Ann Neurol 1995;37:574-82.
110. Dietz V. Human motor control of automatic functional movements: Interaction between central programs and afferent input. Physiol Rev 1992;72(1):33-69.
111. Duysens J, Tax AAM, Trippel M, Dietz V. Phase-dependent reversal of reflexly induced movements during human gait. Exp Brain Res 1992;90:404-14.
112. Edgerton VR, Grillner S, Sjostrom A, Zangger P. Central generation of locomotion in vertebrates. In: Herman RM, Grillner S, Stein P, Stuart DG, (editors). Neural Control of Locomotion. New York: Plenum, 1976:439-64.
113. Rossignol S, Barbeau H. Pharmacology of locomotion: an account of studies in spinal cats and spinal cord injured subjects. J Am Paraplegia Soc 1993;16(4):190-1966.
114. Sperry RW. The effect of crossing nerves to antagonistic muscles in the hind limb of the rat. J Comp Neurol 1941;75:1-19.
115. Sperry RW. Transplantation of motor nerves and muscles in the forelimb of the rat. J Comp Neurol 1942;76:283-321.
116. Van de Crommert HWAA, Faist M, Berger W, Duysens J. Biceps femoris tendon jerk reflexes are enhanced at the end of the swing phase. Brain Res 734:341-4