Descending command systems for the initiation of locomotion in mammals

Brain Research Reviews

Volumn 57, Issue 1, 2008, Pages 183-191

  Jordan, Larry M ^a   Liu, Jun ^a   Hedlund, Peter B ^b   Akay, Turgay ^c   Pearson, Keir G ^d  

^a UNIVERSITY OF MANITOBA   (Canada)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c Columbia University ^*  (United States)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

5 Hydroxytryptamine; Adult mouse; Brainstem; Central pattern generator; Dopamine; EMG; Excitatory amino acids; Isolated spinal cord; Locomotion; Noradarenaline; Spinal cord

Indexed keywords

SEROTONIN 2A RECEPTOR; SEROTONIN 7 RECEPTOR;

BRAIN REGION; BRAIN STEM; DOPAMINERGIC SYSTEM; DRUG ACTIVITY; DRUG MECHANISM; EXCITATORY POSTSYNAPTIC POTENTIAL; LOCOMOTION; LUMBAR SPINAL CORD; MAMMAL; MOTONEURON; NERVE CELL; NONHUMAN; NORADRENERGIC SYSTEM; ONCOGENE C FOS; PRIORITY JOURNAL; REVIEW; SEROTONINERGIC SYSTEM;

ANIMALS; DOPAMINE; EFFERENT PATHWAYS; GLUTAMATES; HUMANS; LOCOMOTION; MAMMALS; NOREPINEPHRINE; SEROTONIN;

EID: 36749061303     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2007.07.019     Document Type: Review

References (83)

1. Akay T., Acharya H.J., Fouad K., and Pearson K.G. Behavioral and electromyographic characterization of mice lacking EphA4 receptors. J. Neurophysiol. 96 (2006) 642-651
2. Alford S., Schwartz E., and Viana di Prisco G. The pharmacology of vertebrate spinal central pattern generators. Neuroscientist 9 (2003) 217-228
3. Atsuta Y., Garcia-Rill E., and Skinner R.D. Electrically induced locomotion in the in vitro brainstem-spinal cord preparation. Dev. Brain Res. 42 (1988) 309-312
4. Atsuta Y., Garcia-Rill E., and Skinner R.D. Characteristics of electrically induced locomotion in rat in vitro brain stem-spinal cord preparation. J. Neurophysiol. 64 (1990) 727-735
5. Atsuta Y., Garcia-Rill E., and Skinner R.D. Control of locomotion in vitro: I. Deafferentation. Somatosens. Motor Res. 8 (1991) 45-53
6. Barbeau H., and Rossignol S. Initiation and modulation of the locomotor pattern in the adult chronic spinal cat by noradrenergic, serotonergic and dopaminergic drugs. Brain Res. 546 (1991) 250-260
7. Barbeau H., Julien C., and Rossignol S. The effects of clonidine and yohimbine on locomotion and cutaneous reflexes in the adult chronic spinal cat. Brain Res. 437 (1987) 83-96
8. 1 receptor class. Proc. R. Soc. Lond., B Biol. Sci. 265 (1998) 2073-2080
9. Björklund A., and Skagerberg G. Evidence for a major spinal cord projection from the diencephalic A11 dopamine cell group in the rat using transmitter-specific fluorescent retrograde tracing. Brain Res. 177 (1979) 170-175
10. Bonnot A., Whelan P.J., Mentis G.Z., and O'Donovan M.J. Locomotor-like activity generated by the neonatal mouse spinal cord. Brain Res. Brain Res. Rev. 40 (2002) 141-151
11. + induces locomotor-like patterns in the rat spinal cord in vitro: Comparison with NMDA or 5-HT induced activity. J. Neurophysiol. 79 (1998) 2643-2652
12. Carlin K.P., Dai Y., and Jordan L.M. Cholinergic and serotonergic excitation of ascending commissural neurons in the thoraco-lumbar spinal cord of the neonatal mouse. J. Neurophysiol. 95 (2006) 1278-1284
13. Cazalets J.R., Grillner P., Menard I., Cremieux J., and Clarac F. Two types of motor rhythm induced by NMDA and amines in an in vitro spinal cord preparation of neonatal rat. Neurosci. Lett. 111 (1990) 116-121
14. Cazalets J.R., Sqalli-Houssaini Y., and Clarac F. Activation of the central pattern generators for locomotion by serotonin and excitatory amino acids in neonatal rat. J. Physiol. (Lond) 455 (1992) 187-204
15. Cazalets J.R., Borde M., and Clarac F. Localization and organization of the central pattern generator for hindlimb locomotion in newborn rat. J. Neurosci. 15 (1995) 4943-4951
16. Chau C., Barbeau H., and Rossignol S. Early locomotor training with clonidine in spinal cats. J. Neurophysiol. 79 (1998) 392-409
17. Chau C., Barbeau H., and Rossignol S. Effects of intrathecal alpha-1 and alpha-2-noradrenergic agonists and norepinephrine on locomotion in chronic spinal cats. J. Neurophysiol. 79 (1998) 2841-2963
18. Chau C., Giroux N., Barbeau H., Jordan L., and Rossignol S. Effects of intrathecal glutamatergic drugs on locomotion I. NMDA in short-term spinal cats. J. Neurophysiol. 88 (2002) 3032-3045
19. Clarac F., Pearlstein E., Pflieger J.F., and Vinay L. The in vitro neonatal rat spinal cord preparation: a new insight into mammalian locomotor mechanisms. J. Comp. Physiol., A Sens. Neural Behav. Physiol. 190 (2004) 343-357
20. Clark F.M., and Proudfit H.K. The projections of noradrenergic neurons in the A5 catecholamine cell group to the spinal cord in the rat: anatomical evidence that A5 neurons modulate nociception. Brain Res. 616 (1993) 200-210
21. Cowley K.C., and Schmidt B.J. A comparison of motor patterns induced by N-methyl-d-aspartate, acetylcholine and serotonin in the in vitro neonatal rat spinal cord. Neurosci. Lett. 171 (1994) 147-150
22. Cowley K.C., and Schmidt B.J. Regional distribution of the locomotor pattern-generating network in the neonatal rat spinal cord. J. Neurophysiol. 77 (1997) 247-259
23. Dale N., and Roberts A. Excitatory amino acid receptors in Xenopus embryo spinal cord and their role in the activation of swimming. J. Physiol. 348 (1984) 527-543
24. Dean C., Marson L., and Kampine J.P. Distribution and co-localization of 5-hydroxytryptamine, thyrotropin-releasing hormone and substance P in the cat medulla. Neuroscience 57 (1993) 811-822
25. Degtyarenko A.M., Simon E.S., and Burke R.E. Locomotor modulation of disynaptic EPSPs from the mesencephalic locomotor region in cat motoneurons. J. Neurophysiol. 80 (1998) 3284-3296
26. Douglas J.R., Noga B.R., Dai X., and Jordan L.M. The effects of intrathecal administration of excitatory amino-acid agonists and antagonists on the initiation of locomotion in the adult cat. J. Neurosci. 13 (1993) 990-1000
27. Feraboli-Lohnherr D., Barthe J.-Y., and Orsal D. Serotonin-induced activation of the network for locomotion in adult spinal rats. J. Neurosci. Res. 55 (1999) 87-98
28. Forssberg H., and Grillner S. The locomotion of the acute spinal cat injected with clonidine i.v. Brain Res. 50 (1973) 184-186
29. Gabbay H., and Lev-Tov A. Alpha-1 adrenoceptor agonists generate a "fast" NMDA receptor-independent motor rhythm in the neonatal rat spinal cord. J. Neurophysiol. 92 (2004) 997-1010
30. Gilmore J., and Fedirchuk B. The excitability of lumbar motoneurons in the neonatal rat is increased by a hyperpolarization of their voltage threshold for activation by descending serotonergic fibers. J. Physiol. 558.1 (2004) 213-224
31. Gimenez y Ribotta M., Provencher J., Feraboli-Lohnherr D., Rossignol S., Privat A., and Orsal D. Activation of locomotion in adult chronic spinal rats is achieved by transplantation of embryonic raphe cells reinnervating a precise lumbar level. J. Neurosci. 20 (2000) 5144-5152
32. Giroux N., Reader T.A., and Rossignol S. Comparison of the effect of intrathecal administration of clonidine and yohimbine on the locomotion of intact and spinal cats. J. Neurophysiol. 85 (2001) 2516-2536
33. Giroux N., Chau C., Barbeau H., Reader T.A., and Rossignol S. Effects of intrathecal glutamatergic drugs on locomotion. II. NMDA and AP-5 in intact and late spinal cats. J. Neurophysiol. 90 (2003) 1027-1045
34. Grillner, S., 1981 Control of locomotion in bipeds, tetrapods, and fish. Handbook of Physiology - The Nervous System. 2(Part 2), 1179-1236. 81. Baltimore, MD, Waverly Press. S.R. Geiger, V.B. Brooks J.M. Brookhart and V.B. Mountcastle.
35. Grillner S., and Zangger P. On the central generation of locomotion in the low spinal cat. Exp. Brain Res. 34 (1979) 241-261
36. Grillner S., Georgopoulos A.P., and Jordan L.M. Selection and initiation of motor behavior. In: Stein P.S.G., Grillner S., Selverston A.I., and Stuart D.G. (Eds). Neurons, Networks, and Motor Behavior (1997), MIT Press, Cambridge, Ma 3-19
37. Grillner S., McClellan A., Sigvardt K., Wallen P., and Wilen M. Activation of NMDA-receptors elicits 'fictive locomotion' in lamprey spinal cord in vitro. Acta Physiol. Scand. 133 (1981) 549-551
38. Gunnar S., and Olle L. Organization of diencephalic dopamine neurons projecting to the spinal cord in the rat. Brain Res. 342 (1985) 340-351
39. Harding A., Paximos G., and Halliday G. The serotonin and tachykinin systems. In: Paximos G. (Ed). The Rat Nervous System. 3rd edition (2004), Elsevier Academic Press, New York 1205-1256
40. Hedlund P.B., Danielson P.E., Thomas E.A., Slanina K., Carson M.J., and Sutcliffe J.G. No hypothermic response to serotonin in 5-HT7 receptor knockout mice. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 1375-1380
41. Hinckley C.A., Hartley R., Wu L., Todd A., and Ziskind-Conhaim L. Locomotor-like rhythms in a genetically distinct cluster of interneurons in the mammalian spinal cord. J. Neurophysiol. 93 (2005) 1439-1449
42. Hochman S., Jordan L., and MacDonald J. N-methyl-d-aspartate receptor-mediated voltage oscillations in neurons surrounding the central canal in slices of rat spinal cord. J. Neurophysiol. 72 (1994) 565-577
43. Hochman S., Garraway S.M., Machacek D.W., and Shay B.L. 5-HT receptors and the neuromodulatory control of spinal cord function. In: Cope T.C. (Ed). Motor Neurobiology of the Spinal Cord (2001), CRC Press, New York 48-87
44. Jankowska E., Jukes M.G.M., Lund S., and Lundberg A. The effect of DOPA on the spinal cord: V. Reciprocal organization of pathways transmitting excitatory action to alpha motoneurones of flexors and extensors. Acta Physiol. Scand. 70 (1967) 369-388
45. Jankowska E., Jukes M.G.M., Lund S., and Lundberg A. The effect of DOPA on the spinal cord. VI. Half-centre organization of interneurones transmitting effects from the flexor reflex afferents. Acta Physiol. Scand. 70 (1967) 389-402
46. Jasmin L., Boudah A., and Ohara P.T. Long-term effects of decreased noradrenergic central nervous system innervation on pain behavior and opioid antinociception. J. Comp. Neurol. 460 (2003) 38-55
47. Jiang Z., Carlin K.P., and Brownstone R.M. An in vitro functionally mature mouse spinal cord preparation for the study of spinal motor networks. Brain Res. 816 (1999) 493-499
48. Jones S.L., and Light A.R. Serotoninergic medullary raphespinal projection to the lumbar spinal cord in the rat: a retrograde immunohistochemical study. J. Comp. Neurol. 322 (1992) 599-610
49. Jordan L.M. Brainstem and spinal cord mechanisms for the initiation of locomotion. In: Shimamura M., Grillner S., and Edgerton V.R. (Eds). Neurobiological Basis of Human Locomotion (1991), Japan Scientific Society Press 3-20
50. Jordan L.M. Initiation of locomotion in mammals. Ann. N. Y. Acad. Sci. 860 (1998) 83-93
51. Jordan L.M., and Schmidt B.J. Propriospinal neurons involved in the control of locomotion: potential targets for repair strategies?. Prog. Brain Res. 137 (2002) 125-139
52. Kiehn O., and Kjaerulff O. Spatiotemporal characteristics of 5-HT and dopamine-induced rhythmic hindlimb activity in the in vitro neonatal rat. J. Neurophysiol. 75 (1996) 1472-1482
53. Kiehn O., and Butt S.J. Physiological, anatomical and genetic identification of CPG neurons in the developing mammalian spinal cord. Prog. Neurobiol. 70 (2003) 347-361
54. Kiehn O., and Kjaerulff O. Distribution of central pattern generators for rhythmic motor outputs in the spinal cord of limbed vertebrates. Ann. N. Y. Acad. Sci. 860 (1998) 110-129
55. Kiehn O., Sillar K.T., Kjaerulff O., and McDearmid J.R. Effects of noradrenaline on locomotor rhythm-generating networks in the isolated neonatal rat spinal cord. J. Neurophysiol. 82 (1999) 741-746
56. Kinjo N., Atsuta Y., Webber M., Kyle R., Skinner R.D., and Garcia-Rill E. Medioventral medulla-induced locomotion. Brain Res. Bull. 24 (1990) 509-516
57. Kudo N., and Yamada T. N-methyl-d,l-aspartate-induced locomotor activity in a spinal cord-hindlimb muscles preparation of the newborn rat studied in vitro. Neurosci. Lett. 75 (1987) 43-48
58. Lafreniere-Roula M., and McCrea D.A. Effects of spontaneous deletions of nerve activity during fictive locomotion in the cat on MLR-evoked post-synaptic potentials in lumbar motoneurons. Soc. Neurosci. Abst. 648.12 (2006)
59. Liu J., and Jordan L.M. Stimulation of the parapyramidal region of the neonatal rat brain stem produces locomotor-like activity involving spinal 5-HT7 and 5-HT2A receptors. J. Neurophysiol. 94 (2005) 1392-1404
60. Madriaga M.A., McPhee L.C., Chersa T., Christie K.J., and Whelan P.J. Modulation of locomotor activity by multiple 5-HT and dopaminergic receptor subtypes in the neonatal mouse spinal cord. J. Neurophysiol. 92 (2004) 1566-1576
61. Marcoux J., and Rossignol S. Initiating or blocking locomotion in spinal cats by applying noradrenergic drugs to restricted lumbar spinal segments. J. Neurosci. 20 (2000) 8577-8585
62. Nishimaru H., Takizawa H., and Kudo N. 5-Hydroxytryptamine-induced locomotor rhythm in the neonatal mouse spinal cord in vitro. Neurosci. Lett. 280 (2000) 187-190
63. Noga B.R., Kriellaars D.J., Brownstone R.M., and Jordan L.M. Mechanism for activation of locomotor centers in the spinal cord by stimulation of the mesencephalic locomotor region. J. Neurophysiol. 90 (2003) 1464-1478
64. Pearlstein E., Mabrouk F.B., Pflieger J.F., and Vinay L. Serotonin refines the locomotor-related alternations in the in vitro neonatal rat spinal cord. Eur. J. Neurosci. 21 (2005) 1338-1346
65. Pearson S.A., Mouihate A., Pittman Q.J., and Whelan P.J. Peptidergic activation of locomotor pattern generators in the neonatal spinal cord. J. Neurosci. 23 (2003) 10154-10163
66. Pearson K.G., Acharya H., and Fouad K. A new electrode configuration for recording electromyographic activity in behaving mice. J. Neurosci. Methods 148 (2005) 36-42
67. Qu S., Ondo W.G., Zhang X., Xie W.J., Pan T.H., and Le W.D. Projections of diencephalic dopamine neurons into the spinal cord in mice. Exp. Brain Res. 168 (2006) 152-156
68. Rossignol S. Neural control of stereotypic limb movements. In: Rowell L., and Shepard J. (Eds). Integration of Motor, Circulatory, Respiratory and Metabolic Control During Exercise (1996), American Physiological Society 173-216
69. Rossignol S., Bouyer L., Barthelemy D., Langlet C., and Leblond H. Recovery of locomotion in the cat following spinal cord lesions. Brain Res. Brain Res. Rev. 40 (2002) 257-266
70. Schmidt B.J., and Jordan L.M. The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res. Bull. 53 (2000) 689-710
71. Shefchyk S.J., Jell R.M., and Jordan L.M. Reversible cooling of the brainstem reveals areas required for mesencephalic locomotor region evoked treadmill locomotion. Exp. Brain Res. 56 (1984) 257-262
72. Shefchyk S.J., and Jordan L.M. Excitatory and inhibitory postsynaptic potentials in alpha-motoneurons produced during fictive locomotion by stimulation of the mesencephalic locomotor region. J. Neurophysiol. 53 (1985) 1345-1355
73. Skagerberg G., Bjorklund A., and Lindvall O. Further studies on the use of the fluorescent retrograde tracer true blue in combination with monoamine histochemistry. J. Neurosci. Methods 14 (1985) 25-40
74. Smith J.C., and Feldman J.L. In vitro brainstem-spinal cord preparations for study of motor systems for mammalian respiration and locomotion. J. Neurosci. Methods 21 (1987) 321-333
75. Smith J.C., Feldman J.L., and Schmidt B.J. Neural mechanisms generating locomotion studied in mammalian brain stem-spinal cord in vitro. FASEB J. (1998) 2283-2288
76. Steeves J.D., Schmidt B.J., Skovgaard B.J., and Jordan L.M. Effect of noradrenaline and 5-hydroxytryptamine depletion on locomotion in the cat. Brain Res. 185 (1980) 349-362
77. VanderHorst V.G., and Ulfhake B. The organization of the brainstem and spinal cord of the mouse: relationships between monoaminergic, cholinergic, and spinal projection systems. J. Chem. Neuroanat. 31 (2006) 2-36
78. Whelan P. Control of locomotion in the decerebrate cat. Prog. Neurobiol. 49 (1996) 481-515
79. Whelan P., Bonnot A., and O'Donovan M.J. Properties of rhythmic activity generated by the isolated spinal cord of the neonatal mouse. J. Neurophysiol. 84 (2000) 2821-2833
80. Wilson J.M., Hartley R., Maxwell D.J., Todd A.J., Lieberam I., Kaltschmidt J.A., Yoshida Y., Jessell T.M., and Brownstone R.M. Conditional rhythmicity of ventral spinal interneurons defined by expression of the Hb9 homeodomain protein. J. Neurosci. 25 (2005) 5710-5719
81. Zaporozhets E., Cowley K.C., and Schmidt B.J. A reliable technique for the induction of locomotor-like activity in the in vitro neonatal rat spinal cord using brainstem electrical stimulation. J. Neurosci. Methods 139 (2004) 33-41
82. Zaporozhets E., Cowley K.C., and Schmidt B.J. Propriospinal neurons contribute to bulbospinal transmission of the locomotor command signal in the neonatal rat spinal cord. J. Physiol. 572 (2006) 443-458
83. Zhong G., Diaz-Rios M.E., and Harris-Warrick R.M. Serotonin modulates the properties of ascending commissural interneurons in the neonatal mouse spinal cord. J. Neurophysiol. 95 (2006) 1545-1555