Excitatory components of the mammalian locomotor CPG

Brain Research Reviews

Volumn 57, Issue 1, 2008, Pages 56-63

  Kiehn, Ole ^a   Quinlan, Katharina A ^a   Restrepo, Carlos Ernesto ^a   Lundfald, Line ^a   Borgius, Lotta ^a   Talpalar, Adolfo E ^a   Endo, Toshiaki ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Commissural interneuron; Locomotion; Motor neuron; Spinal cord; Transcription factor

Indexed keywords

CELL INTERACTION; INTERNEURON; LOCOMOTION; MAMMAL; MOTONEURON; MUSCLE CONTRACTION; NERVE CELL NETWORK; NERVE FUNCTION; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPINAL CORD; SYNAPTIC TRANSMISSION;

ANIMALS; HUMANS; INSTINCT; INTERNEURONS; LOCOMOTION; MOTOR NEURONS; NERVE NET; SPINAL CORD; SYNAPTIC TRANSMISSION;

EID: 36749008469     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2007.07.002     Document Type: Review

References (90)

1. Angel M.J., Guertin P., Jimenez T., and McCrea D.A. Group I extensor afferents evoke disynaptic EPSPs in cat hindlimb extensor motorneurones during fictive locomotion. J. Physiol. 494 Pt. 3 (1996) 851-861
2. Angel M.J., Jankowska E., and McCrea D.A. Candidate interneurones mediating group I disynaptic EPSPs in extensor motoneurones during fictive locomotion in the cat. J. Physiol. 563 (2005) 597-610
3. Arber S., Han B., Mendelsohn M., Smith M., Jessell T.M., and Sockanathan S. Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 23 (1999) 659-674
4. Bannatyne B.A., Edgley S.A., Hammar I., Jankowska E., and Maxwell D.J. Networks of inhibitory and excitatory commissural interneurons mediating crossed reticulospinal actions. Eur. J. Neurosci. 18 (2003) 2273-2284
5. Beato M., Bracci E., and Nistri A. Contribution of NMDA and non-NMDA glutamate receptors to locomotor pattern generation in the neonatal rat spinal cord. Proc. Biol. Sci. 264 (1997) 877-884
6. Berg R.W., Alaburda A., and Hounsgaard J. Balanced inhibition and excitation drive spike activity in spinal half-centers. Science 315 (2007) 390-393
7. Berkinblit M.B., Deliagina T.G., Orlovsky G.N., and Feldman A.G. Activity of motoneurons during fictitious scratch reflex in the cat. Brain Res. 193 (1980) 427-438
8. 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
9. Bracci E., Ballerini L., and Nistri A. Spontaneous rhythmic bursts induced by pharmacological block of inhibition in lumbar motoneurons of the neonatal rat spinal cord. J. Neurophysiol. 75 (1996) 640-647
10. Bracci E., Beato M., and Nistri A. Extracellular K+ 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
11. Brownstone R.M., and Wilson J.M. Strategies for delineating spinal locomotor rhythm generating networks and the possible role of Hb9 interneurons in rhythmogenesis. Brain Res. Rev. (2007) 10.1016/j.brainresrev.2007.06.025
12. Butt S.J., and Kiehn O. Functional identification of interneurons responsible for left-right coordination of hindlimbs in mammals. Neuron 38 6 (2003) 953-963
13. Butt S.J., Harris-Warrick R.M., and Kiehn O. Firing properties of identified interneuron populations in the mammalian hindlimb central pattern generator. J. Neurosci. 22 (2002) 9961-9971
14. Butt S.J., Lebret J.M., and Kiehn O. Organization of left-right coordination in the mammalian locomotor network. Brain Res. Brain Res. Rev. 40 (2002) 107-117
15. Butt S.J., Lundfald L., and Kiehn O. EphA4 defines a class of excitatory locomotor-related interneurons. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 14098-14103
16. Cangiano L., and Grillner S. Fast and slow locomotor burst generation in the hemi-spinal cord of the lamprey. Abstract Society for Neuroscience (2002) 65.61
17. Cazalets J.R., Borde M., and Clarac F. The synaptic drive from the spinal locomotor network to motoneurons in the newborn rat. J. Neurosci. 16 (1996) 298-306
18. Coonan J.R., Greferath U., Messenger J., Hartley L., Murphy M., Boyd A.W., Dottori M., Galea M.P., and Bartlett P.F. Development and reorganization of corticospinal projections in EphA4 deficient mice. J. Comp. Neurol. 436 (2001) 248-262
19. Crone, S., Quinlan, K., Droho, S., Lundfald, L., Selak, J., Kiehn, O., Sharma, K., 2007. Selective ablation of ipsilateral excitatory interneurons decouples left-right locomotor coordination (submitted for publication).
20. Dale N., and Grillner S. Dual-component synaptic potentials in the lamprey mediated by excitatory amino acid receptors. J. Neurosci. 6 (1986) 2653-2661
21. Dale N., and Roberts A. Dual-component amino-acid-mediated synaptic potentials: excitatory drive for swimming in Xenopus embryos. J. Physiol. 363 (1985) 35-59
22. Deliagina T.G., and Orlovsky G.N. Activity of Ia inhibitory interneurons during fictitious scratch reflex in the cat. Brain Res. 193 (1980) 439-447
23. Dottori M., Hartley L., Galea M., Paxinos G., Polizzotto M., Kilpatrick T., Bartlett P.F., Murphy M., Kontgen F., and Boyd A.W. EphA4 (Sek1) receptor tyrosine kinase is required for the development of the corticospinal tract. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 13248-13253
24. 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
25. Droho S., Crone C., Lundfald L., Quinlan K., Viemary J., McDonald J., Setlak J., Kiehn O., and Sharma K. Genetic analysis of motor function: role of V2a neurons in locomotion. Society for Neuroscience Abstract (2006)
26. Dubuc R., Brocard F., Myriam A., Fenelon K., Gariepy J.F., Smetana R., Menard A., Le Ray D., Viana di Prisco G., Pearlstein E., Sirota M.G., Derjean D., St-Pierre M., Zielinsky B., Brocard F., and Veilleux D. Initiation of locomotion in lampreys. Brain Res. Rev. (2007) 10.1016/j.brainresrev.2007.07.016
27. Edgley S.A., and Jankowska E. An interneuronal relay for group I and II muscle afferents in the midlumbar segments of the cat spinal cord. J. Physiol. 389 (1987) 647-674
28. Edgley S.A., Jankowska E., and Hammar I. Ipsilateral actions of feline corticospinal tract neurons on limb motoneurons. J. Neurosci. 24 (2004) 7804-7813
29. Edgley S.A., Jankowska E., Krutki P., and Hammar I. Both dorsal horn and lamina VIII interneurones contribute to crossed reflexes from feline group II muscle afferents. J. Physiol. 552 (2003) 961-974
30. Endo T., and Kiehn O. Conductance measurements of synaptic inputs to mammalian motor neurons during locomotion. Society for Neuroscience, Abstract (2007)
31. Fenaux F., Corio M., Palisses R., and Viala D. Effects of an NMDA-receptor antagonist, MK-801, on central locomotor programming in the rabbit. Exp. Brain Res. 86 (1991) 393-401
32. Gosgnach S., Lanuza G.M., Butt S.J., Saueressig H., Zhang Y., Velasquez T., Riethmacher D., Callaway E.M., Kiehn O., and Goulding M. V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature 440 (2006) 215-219
33. Goulding M., Lanuza G., Sapir T., and Narayan S. The formation of sensorimotor circuits. Curr. Opin. Neurobiol. 12 (2002) 508-515
34. Goulding M., and Pfaff S.L. Development of circuits that generate simple rhythmic behaviors in vertebrates. Curr. Opin. Neurobiol. 15 (2005) 14-20
35. Grillner S. The motor infrastructure: from ion channels to neuronal networks. Nat. Rev. Neurosci. 4 (2003) 573-586
36. Hammar I., Bannatyne B.A., Maxwell D.J., Edgley S.A., and Jankowska E. The actions of monoamines and distribution of noradrenergic and serotoninergic contacts on different subpopulations of commissural interneurons in the cat spinal cord. Eur. J. Neurosci. 19 (2004) 1305-1316
37. 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
38. Hinckley C.A., and Ziskind-Conhaim L. Electrical coupling between locomotor-related excitatory interneurons in the mammalian spinal cord. J. Neurosci. 26 (2006) 8477-8483
39. Hochman S., and Schmidt B.J. Whole cell recordings of lumbar motoneurons during locomotor-like activity in the in vitro neonatal rat spinal cord. J. Neurophysiol. 79 (1998) 743-752
40. Jankowska E., Hammar I., Slawinska U., Maleszak K., and Edgley S.A. Neuronal basis of crossed actions from the reticular formation on feline hindlimb motoneurons. J. Neurosci. 23 (2003) 1867-1878
41. Jankowska E., Edgley S.A., Krutki P., and Hammar I. Functional differentiation and organization of feline midlumbar commissural interneurones. J. Physiol. 565 (2005) 645-658
42. Jankowska E., Krutki P., and Matsuyama K. Relative contribution of Ia inhibitory interneurones to inhibition of feline contralateral motoneurones evoked via commissural interneurones. J. Physiol. 598 (2005) 617-628
43. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1 (2000) 20-29
44. Jordan L.M., Liu J., Hedlund P., and Akay T. Descending command systems for the initiation of locomotion in mammals. Brain Res. Rev. (2007) 10.1016/j.brainresrev.2007.07.019
45. Kiehn O. Locomotor circuits in the mammalian spinal cord. Annu. Rev. Neurosci. 29 (2006) 279-306
46. 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
47. Kiehn O., Hounsgaard J., and Sillar K.T. Basic buildings blocks of vertebrate central pattern generators. In: Stein P.S.G., Grillner S., Selverston A., and Stuart D.G. (Eds). Neurons, Networks and Motor Behavior (1997), MIT Press, Cambridge 47-59
48. Kjaerulff O., and Kiehn O. Distribution of networks generating and coordinating locomotor activity in the neonatal rat spinal cord in vitro: a lesion study. J. Neurosci. 16 (1996) 5777-5794
49. Kimura Y., Okamura Y., and Higashijima S. alx, a zebrafish homolog of Chx10, marks ipsilateral descending excitatory interneurons that participate in the regulation of spinal locomotor circuits. J. Neurosci. 26 (2006) 5684-5697
50. Kjaerulff O., and Kiehn O. Crossed rhythmic synaptic input to motoneurons during selective activation of the contralateral spinal locomotor network. J. Neurosci. 17 (1997) 9433-9447
51. Krutki P., Jankowska E., and Edgley S.A. Are crossed actions of reticulospinal and vestibulospinal neurons on feline motoneurons mediated by the same or separate commissural neurons?. J. Neurosci. 23 (2003) 8041-8050
52. 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
53. Kullander K., Croll S.D., Zimmer M., Pan L., McClain J., Hughes V., Zabski S., DeChiara T.M., Klein R., Yancopoulos G.D., and Gale N.W. Ephrin-B3 is the midline barrier that prevents corticospinal tract axons from recrossing, allowing for unilateral motor control. Genes Dev. 15 (2001) 877-888
54. Kullander K., Mather N.K., Diella F., Dottori M., Boyd A.W., and Klein R. Kinase-dependent and kinase-independent functions of EphA4 receptors in major axon tract formation in vivo. Neuron 29 (2001) 73-84
55. Kullander K., Butt S.J., Lebret J.M., Lundfald L., Restrepo C.E., Rydstrom A., Klein R., and Kiehn O. Role of EphA4 and EphrinB3 in local neuronal circuits that control walking. Science 299 (2003) 1889-1892
56. Landry M., Bouali-Benazzouz R., El Mestikawy S., Ravassard P., and Nagy F. Expression of vesicular glutamate transporters in rat lumbar spinal cord, with a note on dorsal root ganglia. J. Comp. Neurol. 468 (2004) 380-394
57. Lanuza G.M., Gosgnach S., Pierani A., Jessell T.M., and Goulding M. Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements. Neuron 42 (2004) 375-386
58. Lee S.K., and Pfaff S.L. Transcriptional networks regulating neuronal identity in the developing spinal cord. Nat. Neurosci. 4 (2001) 1183-1191 Suppl
59. Lundfald, L., Restrepo, C.E., Butt, S.J.B., Peng, C.Y., Droho, S., Endo, T., Zeilhofer, H.U., Sharma, K., Kiehn, O., in press. Phenotype of V2 derived interneurons and their relationship to the axon guidance molecule EphA4 in the developing mouse spinal cord. Eur J. Neurosci.
60. Machacek D.W., and Hochman S. Noradrenaline unmasks novel self-reinforcing motor circuits within the mammalian spinal cord. J. Neurosci. 26 (2006) 5920-5928
61. Matsuyama K., and Jankowska E. Coupling between feline cerebellum (fastigial neurons) and motoneurons innervating hindlimb muscles. J. Neurophysiol. 91 (2004) 1183-1192
62. Mentis G.Z., Alvarez F.J., Bonnot A., Richards D.S., Gonzalez-Forero D., Zerda R., and O'Donovan M.J. Noncholinergic excitatory actions of motoneurons in the neonatal mammalian spinal cord. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 7344-7349
63. Moran-Rivard L., Kagawa T., Saueressig H., Gross M.K., Burrill J., and Goulding M. Evx1 is a postmitotic determinant of v0 interneuron identity in the spinal cord. Neuron 29 (2001) 385-399
64. Nishimaru H., and Kudo N. Formation of the central pattern generator for locomotion in the rat and mouse. Brain Res. Bull. 53 (2000) 661-669
65. Nishimaru H., Iizuka M., Ozaki S., and Kudo N. Spontaneous motoneuronal activity mediated by glycine and GABA in the spinal cord of rat fetuses in vitro. J. Physiol. 497 Pt. 1 (1996) 131-143
66. Nishimaru H., Restrepo C.E., Ryge J., Yanagawa Y., and Kiehn O. Mammalian motor neurons corelease glutamate and acetylcholine at central synapses. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 5245-5249
67. Oliveira A.L., Hydling F., Olsson E., Shi T., Edwards R.H., Fujiyama F., Kaneko T., Hokfelt T., Cullheim S., and Meister B. Cellular localization of three vesicular glutamate transporter mRNAs and proteins in rat spinal cord and dorsal root ganglia. Synapse 50 (2003) 117-129
68. Ozaki S., Yamada T., Iizuka M., Nishimaru H., and Kudo N. Development of locomotor activity induced by NMDA receptor activation in the lumbar spinal cord of the rat fetus studied in vitro. Brain. Res. Dev. Brain Res. 97 (1996) 118-125
69. Peng C.Y., Yajima H., Burns C.E., Zon L.I., Sisodia S.S., Pfaff S.L., and Sharma K. Notch and MAML signaling drives Scl-dependent interneuron diversity in the spinal cord. Neuron 53 (2007) 813-827
70. Perreault M.C. Motoneurons have different membrane resistance during fictive scratching and weight support. J. Neurosci. 22 (2002) 8259-8265
71. Perret C. Centrally generated pattern of motoneuron activity during locomotion in the cat. Symp. Soc. Exp. Biol. 37 (1983) 405-422
72. Perret C., and Cabelguen J.M. Central and reflex participation in the timing of locomotor activations of a bifunctional muscle, the semi-tendinosus, in the cat. Brain Res. 106 (1976) 390-395
73. Perrins R., and Roberts A. Cholinergic and electrical motoneuron-to-motoneuron synapses contribute to on-cycle excitation during swimming in Xenopus embryos. J. Neurophysiol. 73 (1995) 1005-1012
74. Perrins R., and Roberts A. Cholinergic and electrical synapses between synergistic spinal motoneurones in the Xenopus laevis embryo. J. Physiol. 485 Pt. 1 (1995) 135-144
75. Pierani A., Brenner-Morton S., Chiang C., and Jessell T.M. A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell 97 (1999) 903-915
76. Pierani A., Moran-Rivard L., Sunshine M.J., Littman D.R., Goulding M., and Jessell T.M. Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29 (2001) 367-384
77. Quinlan K., and Kiehn O. Segmental, synaptic actions of commissural interneurons in the mouse spinal cord. J. Neurosci. 27 (2007) 6521-6530
78. Raastad M., Johnson B.R., and Kiehn O. Analysis of EPSCs and IPSCs carrying rhythmic, locomotor-related information in the isolated spinal cord of the neonatal rat. J. Neurophysiol. 78 (1997) 1851-1859
79. Restrepo C.E., Lundfald L., Glover J., and Kiehn O. Neurotransmitter phenotype of commissural interneurons in neonatal rodents. Society for Neuroscience (2005)
80. Roberts A., Soffe S.R., Wolf E.S., Yoshida M., and Zhao F.Y. Central circuits controlling locomotion in young frog tadpoles. Ann. N.Y. Acad. Sci. 860 (1998) 19-34
81. Russell D.F., and Wallen P. On the control of myotomal motoneurones during "fictive swimming" in the lamprey spinal cord in vitro. Acta. Physiol. Scand. 117 (1983) 161-170
82. 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
83. Shefchyk S., McCrea D., Kriellaars D., Fortier P., and Jordan L. Activity of interneurons within the L4 spinal segment of the cat during brainstem-evoked fictive locomotion. Exp. Brain Res. 80 (1990) 290-295
84. Stein P.S. Neuronal control of turtle hindlimb motor rhythms. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 191 (2005) 213-229
85. Talpalar A., Borgius L., Lundfald L., Pierani A., and Kiehn O. Ablation of Dbx1-generated commissural interneurons leads to hopping gait. Society for Neuroscience Abstract (2007)
86. Wallen-Mackenzie A., Gezelius H., Thoby-Brisson M., Nygard A., Enjin A., Fujiyama F., Fortin G., and Kullander K. Vesicular glutamate transporter 2 is required for central respiratory rhythm generation but not for locomotor central pattern generation. J. Neurosci. 26 (2006) 12294-12307
87. 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
88. 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
89. Yokoyama N., Romero M.I., Cowan C.A., Galvan P., Helmbacher F., Charnay P., Parada L.F., and Henkemeyer M. Forward signaling mediated by ephrin-B3 prevents contralateral corticospinal axons from recrossing the spinal cord midline. Neuron 29 (2001) 85-97
90. Zhong G., Masino M.A., and Harris-Warrick R.M. Persistent sodium currents participate in fictive locomotion generation in neonatal mouse spinal cord. J. Neurosci. 27 (2007) 4507-4518