Segmental oscillators in axial motor circuits of the salamander: Distribution and bursting mechanisms

Journal of Neurophysiology

Volumn 104, Issue 5, 2010, Pages 2677-2692

  Ryczko, Dimitri ^a,c   Charrier, Vanessa ^a   Ijspeert, Auke ^b   Cabelguen, Jean Marie ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b EPFL   (Switzerland)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

APAMIN; N METHYL DEXTRO ASPARTIC ACID; POTASSIUM CHANNEL; RILUZOLE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MOTOR ACTIVITY; MOTOR SYSTEM; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NONHUMAN; OSCILLATOR; PRIORITY JOURNAL; SALAMANDER; SODIUM CURRENT; SPINAL CORD; VENTRAL ROOT;

ACTION POTENTIALS; ANIMALS; ELECTROPHYSIOLOGY; EXCITATORY AMINO ACID ANTAGONISTS; LOCOMOTION; N-METHYLASPARTATE; NERVE NET; NEURONS; PERIODICITY; PLEURODELES; RILUZOLE; SPINAL CORD;

EID: 78049506300     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00479.2010     Document Type: Article

References (120)

1. Alford S, Grillner S. CNQX and DNQX block non-NMDA synaptic transmission but not NMDA-evoked locomotion in lamprey spinal cord. Brain Res 506: 297-302, 1990.
2. Alford S, Williams TL. Endogenous activation of glycine and NMDA receptors in lamprey spinal cord during fictive locomotion. J Neurosci 9: 2792-2800, 1989.
3. Angstadt JD, Calabrese RL. A hyperpolarization-activated inward current in heart interneurons of the medicinal leech. J Neurosci 9: 2846-2857, 1989.
4. Aoki F, Wannier T, Grillner S. Slow dorsal-ventral rhythm generator in the lamprey spinal cord. J Neurophysiol 85: 211-218, 2001.
5. Ayali A, Fuchs E, Ben-Jacob E, Cohen A. The function of intersegmental connections in determining temporal characteristics of the spinal cord rhythmic output. Neuroscience 147: 236-246, 2007.
6. Berg RW, Hounsgaard J. Signaling in large-scale neural networks. Cogn Process Suppl 1: S9-15, 2009.
7. Blatz AL, Magleby KL. Single apamin-blocked Ca-activated K channels of small conductance in cultured rat skeletal muscle. Nature 323: 718-720, 1986.
8. Bonnot A, Morin D. Hemisegmental localisation of rhythmic networks in the lumbosacral spinal cord of neonate mouse. Brain Res 793: 136-148, 1998. (Pubitemid 28294082)
9. Bracci E, Ballerini L, Nistri A. Localization of rhythmogenic networks responsible for spontaneous bursts induced by strychnine and bicuculline in the rat isolated spinal cord. J Neurosci 16: 7063-7076, 1996.
10. Brodie ED Jr, Gibson LS. Defensive behavior and skin glands of the Northwestern Salamander, Ambystoma gracile. Herpetologica 25: 187-194, 1969.
11. Brodin L, Grillner S, Rovainen CM. N-Methyl-D-aspartate (NMDA), kainate and quisqualate receptors and the generation of fictive locomotion in the lamprey spinal cord. Brain Res 325: 302-306, 1985. (Pubitemid 15134894)
12. Buchanan JT. Identification of interneurons with contralateral, caudal axons in the lamprey spinal cord: synaptic interactions and morphology. J Neurophysiol 47: 961-975, 1982.
13. Butt SJ, Lebret JM, Kiehn O. Organization of left-right coordination in the mammalian locomotor network. Brain Res Rev 40: 107-117, 2002.
14. Cabelguen JM, Ijspeert AJ, Lamarque S, Ryczko D. Axial dynamics during locomotion in vertebrates: lesson from the salamander. Prog Brain Res In press.
15. Cangiano L, Wallén P, Grillner S. Role of apamin-sensitive KCa channels for reticulospinal synaptic transmission to motoneuron and for the afterhyperpolarization. J Neurophysiol 88: 289-299, 2002.
16. Cangiano L, Grillner S. Fast and slow locomotor burst generation in the hemispinal cord of the lamprey. J Neurophysiol 89: 2931-2942, 2003.
17. Cangiano L, Grillner S. Mechanisms of rhythm generation in a spinal locomotor network deprived of crossed connections: the lamprey hemicord. J Neurosci 25: 923-935, 2005.
18. Cheng J, Jovanovic K, Aoyagi Y, Bennett DJ, Han Y, Stein RB. Differential distribution of interneurons in the neural networks that control walking in the mudpuppy (Necturus maculatus) spinal cord. Exp Brain Res 145: 190-198, 2002.
19. Cheng J, Stein RB, Jovanovic K, Yoshida K, Bennett DJ, Han Y. Identi- fication, localization, and modulation of neural networks for walking in the mudpuppy (Necturus maculatus) spinal cord. J Neurosci 18: 4295-4304, 1998.
20. Chevallier S, Landry M, Nagy F, Cabelguen JM. Recovery of bimodal locomotion in the spinal-transected salamander, Pleurodeles waltlii. Eur J Neurosci 20: 1995-2007, 2004.
21. Chevallier S, Nagy F, Cabelguen JM. Cholinergic control of excitability of spinal motoneurons in the salamander. J Physiol 570: 525-540, 2006.
22. Chevallier S, Ijspeert AJ, Ryczko D, Nagy F, Cabelguen JM. Organisation of the spinal central pattern generators for locomotion in the salamander: biology and modelling. Brain Res Rev 57: 147-161, 2008.
23. Cohen AH. Effects of oscillator frequency on phase-locking in the lamprey central pattern generator. J Neurosci Methods 21: 113-125, 1987.
24. Cohen AH, Harris-Warrick RM. Strychnine eliminates alternating motor output during fictive locomotion in the lamprey. Brain Res 293: 164-167, 1984.
25. Cowley KC, Schmidt BJ. Regional distribution of the locomotor patterngenerating network in the neonatal rat spinal cord. J Neurophysiol 77: 247-259, 1997.
26. Davis BM, Duffy MT, Simpson SB, Jr. Bulbospinal and intraspinal connections in normal and regenerated salamander spinal cord. Exp Neurol 103: 41-51, 1989.
27. De Sèze M, Falgairolle M, Viel S, Assaiante C, Cazalets JR. Sequential activation of axial muscles during different forms of rhythmic behavior in man. Exp Brain Res 185: 237-247, 2008.
28. Delvolvé I, Bem T, Cabelguen JM. Epaxial and limb muscle activity during swimming and terrestrial stepping in the adult newt, Pleurodeles waltl. J Neurophysiol 78: 638-650, 1997.
29. Delvolvé I, Branchereau P, Dubuc R, Cabelguen JM. Fictive rhythmic motor patterns induced by NMDA in an in vitro brain stem-spinal cord preparation from an adult urodele. J Neurophysiol 82: 1074-1077, 1999.
30. El Manira A, Tegnér J, Grillner S. Calcium-dependent potassium channels play a critical role for burst termination in the locomotor network in lamprey. J Neurophysiol 72: 1852-1861, 1994.
31. Faber ES, Delaney AJ, Sah P. SK channels regulate excitatory synaptic transmission and plasticity in the lateral amygdala. Nat Neurosci 8: 635-641, 2005.
32. Fagerstedt P, Zelenin PV, Deliagina TG, Orlovsky GN, Grillner S. Crossed reciprocal inhibition evoked by electrical stimulation of the lamprey spinal cord. Exp Brain Res 134: 147-154, 2000.
33. Falgairolle M, Cazalets JR. Metachronal coupling between spinal neuronal networks during locomotor activity in newborn rat. J Physiol 580: 87-102, 2007.
34. Falgairolle M, de Sèze M, Juvin L, Morin D, Cazalets JR. Coordinated network functioning in the spinal cord: an evolutionary perspective. J Physiol 100: 304-316, 2006.
35. Francis ETB. The Anatomy of the Salamander. Oxford, UK: Clarendon, 1934.
36. Friesen WO, Cang J. Sensory and central mechanisms control intersegmental coordination. Curr Opin Neurobiol 11: 678-683, 2001.
37. Gabbay H, Delvolvé I, Lev-Tov A. Pattern generation in caudal-lumbar and sacrococcygeal segments of the neonatal rat spinal cord. J Neurophysiol 88: 732-739, 2002.
38. Gabriel JP, Mahmood R, Walter AM, Kyriakatos A, Hauptmann G, Calabrese RL, El Manira A. Locomotor pattern in the adult zebrafish spinal cord in vitro. J Neurophysiol 99: 37-48, 2008.
39. Green CS, Soffe SR. Roles of ascending inhibition during two rhythmic motor patterns in Xenopus tadpoles. J Neurophysiol 79: 2316-2328, 1998.
40. Grillner S. Control of locomotion in bipeds, tetrapods, and fish. In: Handbook of Physiolog., The Nervous System. Motor Control, edited by Brooks VB. Bethesda, MD: Am. Physiol. Soc, 1981, sect. I, vol. 2, p. 1179-1236.
41. Grillner S. Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52: 751-766, 2006.
42. Hagevik A, McClellan AD. Coupling of spinal locomotor networks in larval lamprey revealed by receptor blockers for inhibitory amino acids: Neurophysiology and computer modeling. J Neurophysiol 72: 1810-1829, 1994.
43. Hägglund M, Borgius L, Dougherty KJ, Kiehn O. Activation of groups of excitatory neurons in the mammalian spinal cord or hindbrain evokes locomotion. Nat Neurosci 13: 246-252, 2010.
44. Harris-Warrick RM. Voltage-sensitive ion channels in rhythmic motor systems. Curr Opin Neurobiol 12: 646-651, 2002.
45. Heaulme M, Chambon JP, Leyris R, Molimard JC, Wermuth CG, Biziere K. Biochemical characterization of the interaction of three pyridazinyl-GABA derivatives with the GABAA receptor site. Brain Res 384: 224-231, 1986.
46. Heiss E, Natchev N, Rabanser A, Weisgram J, Hilgers H. Three types of cutaneous glands in the skin of the salamandrid Pleurodeles waltl. A histological and ultrastructural study. J Morphol 270: 892-902, 2009.
47. + currents in larval lamprey spinal cord neurons. J Neurophysiol 97: 3484-3493, 2007.
48. Hill AA, Lu J, Masino MA, Olsen OH, Calabrese RL. A model of a segmental oscillator in the leech heartbeat neuronal network. J Comput Neurosci 10: 281-302, 2001.
49. Hill RH, Matsushima T, Shotland J, Grillner S. Apamin blocks the slow AHP in lamprey and delays termination of locomotor bursts. Neuroreport 3: 943-945, 1992.
50. Hinckley CA, Ziskind-Conhaim L. Electrical coupling between locomotorrelated excitatory interneurons in the mammalian spinal cord. J Neurosci 26: 8477-8483, 2006.
51. Hocker CG, Yu X, Friesen WO. Functionally heterogeneous segmental oscillators generate swimming in the medical leech. J Comp Physiol [A] 186: 871-883, 2000.
52. Hoffman N, Parker D. Lesioning alters functional properties in isolated spinal cord hemisegmental networks, Neuroscience 168: 732-743, 2010.
53. Hu GY, Biró Z, Hill RH, Grillner S. Intracellular QX-314 causes depression of membrane potential oscillations in lamprey spinal neurons during fictive locomotion. J Neurophysiol 87: 2676-2683, 2002.
54. Huss M, Lansner A, Wallén P, El Manira A, Grillner S, Kotaleski JH. Roles of ionic currents in lamprey CPG neurons: a modeling study. J Neurophysiol 97: 2696-2711, 2007.
55. Ijspeert AJ. Central pattern generators for locomotion control in animals and robots: a review. Neural Netw 21: 642-653, 2008.
56. Ijspeert AJ, Crespi A, Ryczko D, Cabelguen JM. From swimming to walking with a salamander robot driven by a spinal cord model. Science 315: 1416-1420, 2007.
57. Jackson AW, Horinek DF, Boyd MR, McClellan AD. Disruption of left-right reciprocal coupling in the spinal cord of larval lamprey abolishes brain-initiated locomotor activity. J Neurophysiol 94: 2031-2044, 2005.
58. Johnson JW, Ascher P. Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325: 529-531, 1987.
59. Jones SR, Mulloney B, Kaper TJ, Kopell N. Coordination of cellular pattern-generating circuits that control limb movements: the sources of stable differences in intersegmental phases. J Neurosci 23: 3457-3468, 2003.
60. Jovanovic K, Petrov T, Stein RB. Effects of inhibitory neurotransmitters on the mudpuppy (Necturus maculatus) locomotor pattern in vitro. Exp Brain Res 129: 172-184, 1999.
61. Kahn JA, Roberts A. Experiments on the central pattern generator for swimming in amphibian embryos. Philos Trans R Soc Lond B Biol Sci 296: 229-243, 1982.
62. Kalinina NI, Kurchavyi GG, Amakhin DV, Veselkin NP. Differences in the activation of inhibitory motoneuron receptors in the frog Rana ridibunda by GABA and glycine and their interaction. Neurosci Behav Physiol 39: 775-783, 2009.
63. Kiehn O. Contributions of intrinsic motor neuron properties to the production of rhythmic motor output in the mammalian spinal cord. Brain Res Bull 53: 649-659, 2000.
64. Kiehn O. Locomotor circuits in the mammalian spinal cord. Annu Rev Neurosci 29: 279-306, 2006.
65. Kiehn O, Butt SJ. Physiological, anatomical and genetic identification of CPG neurons in the developing mammalian spinal cord. Prog Neurobiol 70: 347-361, 2003.
66. Kiehn O, Quinlan KA, Restrepo CE, Lundfald L, Borgius L, Talpalar AE, Endo T. Excitatory components of the mammalian locomotor CPG. Brain Res Rev 57: 56-63, 2008.
67. Kleckner NW, Dingledine R. Requirement for glycine in activation of NMDA-receptors expressed in Xenopus oocytes. Science 241: 835-837, 1988.
68. Kremer E, Lev-Tov A. Localization of the spinal network associated with generation of hindlimb locomotion in the neonatal rat and organization of its transverse coupling system. J Neurophysiol 77: 1155-1170, 1997.
69. Kudo N, 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: 43-48, 1987.
70. Lavrov I, Cheng J. Activation of NMDA receptors is required for the initiation and maintenance of walking-like activity in the mudpuppy (Necturus maculatus). Can J Physiol Pharmacol 82: 637-644, 2004.
71. Lavrov I, Cheng J. Methodological optimization of applying neuroactive agents for the study of locomotor-like activity in the mudpuppies (Necturus maculatus). J Neurosci Methods 174: 97-102, 2008.
72. Li WC, Roberts A, Soffe SR. Locomotor rhythm maintenance: electrical coupling among premotor excitatory interneurons in the brainstem and spinal cord of young Xenopus tadpoles. J Physiol 587: 1677-1693, 2009.
73. Li WC, Sautois B, Roberts A, Soffe SR. Reconfiguration of a vertebrate motor network: specific neuron recruitment and context-dependent synaptic plasticity. J Neurosci 27: 12267-12276, 2007.
74. Lu J, Gramoll S, Schmidt J, Calabrese RL. Motor pattern switching in the heartbeat pattern generator of the medicinal leech: membrane properties and lack of synaptic interaction in switch interneurons. J Comp Physiol [A] 3: 311-324, 1999.
75. Madriaga MA, McPhee LC, Chersa T, Christie KJ, Whelan PJ. Modulation of locomotor activity by multiple 5-HT and dopaminergic receptor subtypes in the neonatal mouse spinal cord. J Neurophysiol 92: 1566-1576, 2004.
76. McClellan AD. Functional regeneration and restoration of locomotor activity following spinal cord transection in the lamprey. Prog Brain Res 103: 203-217, 1994.
77. McCrea DA, Rybak IA. Organization of mammalian locomotor rhythm and pattern generation. Brain Res Rev 57: 134-146, 2008.
78. Meer DP, Buchanan JT. Apamin reduces the late afterhyperpolarization of lamprey spinal neurons, with little effect on fictive swimming. Neurosci Lett 143: 1-4, 1992.
79. Miller WL, Sigvardt KA. Extent and role of multisegmental coupling in the lamprey spinal locomotor pattern generator. J Neurophysiol 83: 465-476, 2000.
80. Mortin LI, Stein PS. Spinal cord segments containing key elements of the central pattern generators for three forms of scratch reflex in the turtle. J Neurosci 9: 2285-2296, 1989.
81. Mulloney B. A test of the excitability-gradient hypothesis in the swimmeret system of crayfish. J Neurosci 17: 1860-1868, 1997.
82. Muñoz A, Muñoz M, González A, ten Donkelaar HJ. Spinal ascending pathways in amphibians: cells of origin and main targets. J Comp Neurol 78: 205-228, 1997.
83. Nakayama K, Nishimaru H, Kudo N. Basis of changes in left-right coordination of rhythmic motor activity during development in the rat spinal cord. J Neurosci 22: 10388-10398, 2002.
84. Nishimaru H, Kakizaki M. The role of inhibitory neurotransmission in locomotor circuits of the developing mammalian spinal cord. Acta Physiol 197: 83-97, 2009.
85. Nowak RT, Brodie ED Jr. Rib penetration and associated antipredator adaptations in the salamander Pleurodeles waltl (Salamandridae). Copeia 1978: 424-429, 1978.
86. Ohta Y, Dubuc R, Grillner S. A new population of neurons with crossed axons in the lamprey spinal cord. Brain Res 564: 143-148, 1991.
87. Olsen OH, Calabrese RL. Activation of intrinsic and synaptic currents in leech heart interneurons by realistic waveforms. J Neurosci 16: 4958-4970, 1996.
88. Opdyke CA, Calabrese RL. A persistent sodium current contributes to oscillatory activity in heart interneurons of the medicinal leech. J Comp Physiol [A] 175: 781-789, 1994.
89. Pape HC. Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Annu Rev Physiol 58: 299-327, 1996.
90. Parker D, Bevan S. Modulation of cellular and synaptic variability in the lamprey spinal cord. J Neurophysiol 97: 44-56, 2007.
91. Paul DH, Mulloney B. Intersegmental coordination of swimmeret rhythms in isolated nerve cords of crayfish. J Comp Physiol 158: 215-224, 1986.
92. Perrins R, Roberts A. Cholinergic and electrical synapses between synergistic spinal motoneurons in the Xenopus laevis embryo. J Physiol 485: 135-144, 1995.
93. Rioult-Pedotti MS. Intrinsic NMDA-induced oscillations in motoneurons of an adult vertebrate spinal cord are masked by inhibition. J Neurophysiol 77: 717-730, 1997.
94. Roberts A, Alford ST. Descending projections and excitation during fictive swimming in Xenopus embryos: neuroanatomy and lesion experiments. J Comp Neurol 250: 253-261, 1986.
95. Roberts A, Li WC, Soffe SR. Roles for inhibition: studies on networks controlling swimming in young frog tadpoles. J Comp Physiol [A] 194: 185-193, 2008.
96. Roberts A, Tunstall MJ. Mutual re-excitation with post-inhibitory rebound: a simulation study on the mechanisms for locomotor rhythm generation in the spinal cord of Xenopus embryos. Eur J Neurosci 2: 11-23, 1990.
97. Rozental R, Srinivas M, Spray DC. How to close a gap junction channel. Efficacies and potencies of uncoupling agents. Methods Mol Biol 154: 447-476, 2001.
98. Ryczko D, Ijspeert AJ, Nagy F, Cabelguen JM. Rhythmic motor bursting in the spinal cord segments of the salamander. Soc Neurosci Abstr 188.6, 2007.
99. Samara RF, Currie SN. Crossed commissural pathways in the spinal hindlimb enlargement are not necessary for right left hindlimb alternation during turtle swimming. J Neurophysiol 98: 2223-2231, 2007.
100. Shin KS, Rothberg BS, Yellen G. Blocker state dependence and trapping in hyperpolarization-activated cation channels: evidence for an intracellular activation gate. J Gen Physiol 117: 91-101, 2001.
101. Sillar KT, Simmers AJ, Wedderburn JF. The post-embryonic development of cell properties and synaptic drive underlying locomotor rhythm generation in Xenopus larvae. Proc Biol Sci 249: 65-70, 1992.
102. Skinner FK, Mulloney B. Intersegmental coordination in invertebrates and vertebrates. Curr Opin Neurobiol 8: 725-732, 1998.
103. Soffe SR. Roles of glycinergic inhibition and N-methyl-D-aspartate receptor mediated excitation in the locomotor rhythmicity of one half of the Xenopus embryo central nervous system. Eur J Neurosci 1: 561-571, 1989.
104. Soffe SR, Zhao FY, Roberts A. Functional projection distances of spinal interneurons mediating reciprocal inhibition during swimming in Xenopus tadpoles. Eur J Neurosci 13: 617-627, 2001.
105. Sorensen M, DeWeerth S, Cymbalyuk G, Calabrese RL. Using a hybrid neural system to reveal regulation of neuronal network activity by an intrinsic current. J Neurosci 24: 5427-5438, 2004.
106. Sun Q, Dale N. Developmental changes in expression of ion currents accompany maturation of locomotor pattern in frog tadpoles. J Physiol 507: 257-264, 1998.
107. Székely G, Czéh G. Organisation of Locomotion. Berlin: Springer Verlag, 1976.
108. Tazerart S, Viemari JC, Darbon P, Vinay L, Brocard F. Contribution of persistent sodium current to locomotor pattern generation in neonatal rats. J Neurophysiol 98: 613-628, 2007.
109. Tazerart S, Vinay L, Brocard F. The persistent sodium current generates pacemaker activities in the central pattern generator for locomotion and regulates the locomotor rhythm. J Neurosci 28: 8577-8589, 2008.
110. Tresch MC, Kiehn O. Motor coordination without action potentials in the mammalian spinal cord. Nat Neurosci 3 593-599, 2000.
111. Tresch MC, Kiehn O. Synchronization of motor neurons during locomotion in the neonatal rat: predictors and mechanisms. J Neurosci 22: 9997-10008, 2002.
112. Tsvyetlynska NA, Hill RH, Grillner S. Role of AMPA receptor desensitization and the side effects of a DMSO vehicle on reticulospinal EPSPs and locomotor activity. J Neurophysiol 94: 3951-3960, 2005.
113. Tunstall MJ, Roberts A. A longitudinal gradient of synaptic drive in the spinal cord of Xenopus embryos and its role in coordination of swimming. J Physiol 474: 393-405, 1994. (Pubitemid 24060773)
114. Tunstall MJ, Roberts A, Soffe SR. Modelling inter-segmental coordination of neuronal oscillators: synaptic mechanisms for uni-directional coupling during swimming in Xenopus tadpoles. J Comput Neurosci 13: 143-158, 2002.
115. + current that plays a role in termination of swimming in Xenopus embryos. J Physiol 487: 557-572, 1995.
116. Wallén P, Robertson B, Cangiano L, Löw P, Bhattacharjee A, Kaczmarek LK, Grillner S. Sodium-dependent potassium channels of a Slack-like subtype contribute to the slow afterhyperpolarization in lamprey spinal neurons. J Physiol 585: 75-90, 2007.
117. Whelan P, Bonnot A, O'Donovan MJ. Properties of rhythmic activity generated by the isolated spinal cord of the neonatal mouse. J Neurophysiol 84: 2821-2833, 2000.
118. Zhang HY, Li WC, Heitler WJ, Sillar KT. Electrical coupling synchronises spinal motoneuron activity during swimming in hatchling Xenopus tadpoles. J Physiol 587: 4455-4466, 2009.
119. Zhong G, Masino MA, Harris-Warrick RM. Persistent sodium currents participate in fictive locomotion generation in neonatal mouse spinal cord. J Neurosci 27: 4507-4518, 2007.
120. Ziskind-Conhaim L, Wu L, Wiesner EP. Persistent sodium current contributes to induced voltage oscillations in locomotor-related hb9 interneurons in the mouse spinal cord. J Neurophysiol 100: 2254-2264, 2008.