Low-threshold calcium currents contribute to locomotor-like activity in neonatal mice

Journal of Neurophysiology

Volumn 107, Issue 1, 2012, Pages 107-113

  Anderson, Tatiana M ^a   Abbinanti, Matthew D ^b   Peck, Jack H ^a   Gilmour, Megan ^c   Brownstone, Robert M ^c   Masino, Mark A ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Hb9 interneuron; Locomotion; Rhythm generation; Spinal cord

Indexed keywords

CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; ENHANCED GREEN FLUORESCENT PROTEIN; HOMEOBOX HB9 PROTEIN; HOMEODOMAIN PROTEIN; N METHYL DEXTRO ASPARTIC ACID; UNCLASSIFIED DRUG; CALCIUM CHANNEL T TYPE;

ANIMAL EXPERIMENT; ARTICLE; CALCIUM CURRENT; CONTROLLED STUDY; HYPOTHESIS; INTERNEURON; LOCOMOTION; MOUSE; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROTRANSMISSION; NEWBORN; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD; SYNAPSE; ACTION POTENTIAL; ANIMAL; BIOLOGICAL RHYTHM; CALCIUM SIGNALING; CELL LINE; DIFFERENTIAL THRESHOLD; METABOLISM; NERVE CELL NETWORK; PHYSIOLOGY; TRANSGENIC MOUSE;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL CLOCKS; CALCIUM; CALCIUM CHANNELS, T-TYPE; CALCIUM SIGNALING; CELL LINE; DIFFERENTIAL THRESHOLD; INTERNEURONS; LOCOMOTION; MICE; MICE, TRANSGENIC; NERVE NET; SPINAL CORD;

EID: 84255182645     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00583.2011     Document Type: Article

References (82)

1. Alvina K, Ellis-Davies G, Khodakhah K. T-type calcium channels mediate rebound firing in intact deep cerebellar neurons. Neuroscience 158: 635-641, 2009.
2. Angstadt JD, Grassmann JL, Theriault KM, Levasseur SM. Mechanisms of postinhibitory rebound and its modulation by serotonin in excitatory swim motor neurons of the medicinal leech. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191: 715-732, 2005.
3. Arshavsky YI, Deliagina TG, Orlovsky GN. Pattern generation. Curr Opin Neurobiol 7: 781-789, 1997.
4. Bertrand S, Cazalets JR. Postinhibitory rebound during locomotor-like activity in neonatal rat motoneruons in vitro. J Neurophysiol 79: 342-351, 1998.
5. Brown TG. The intrinsic factors in the act of progression in the mammal. Proc R Soc Lond B 84: 308-319, 1911.
6. Brownstone RM, Wilson JM. Strategies for delineating spinal locomotor rhythm-generating networks and the possible role of Hb9 interneurones in rhythmogenesis. Brain Res Rev 57: 64-76, 2008.
7. Calabrese RL, Feldman JL. Intrinsic membrane properties and synaptic mechanisms in motor rhythm generators. In: Neurons, Networks, and Motor Behavior, edited by Stein PSG, Grillner S, Selverston AI, and Stuart DG. Cambridge, MA: MIT, 1997, p. 119-130.
8. Clarac F, Pearlstein E, Pflieger JF, Vinay L. The in vitro neonatal rat spinal cord preparation: a new insight into mammalian locomotor mechansims. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190: 343-357, 2004.
9. Delcomyn F. Motor activity during searching and walking movements of cockroach legs. J Exp Biol 133: 111-120, 1987.
10. Destexhe A, Sejnowski TJ. The initiation of bursts in thalamic neurons and the cortical control of thalamic sensitivity. Philos Trans R Soc Lond B Biol Sci 357: 1649-1657, 2002.
11. Dougherty KJ, Kiehn O. Firing and cellular properties of V2a interneurons in the rodent spinal cord. J Neurosci 30: 24-37, 2010.
12. Eisen JS, Marder E. A mechanism for production of phase shifts in a pattern generator. J Neurophysiol 51: 1375-1393, 1984.
13. Fan YP, Horn EM, Waldrop TG. Biophysical characterization of rat caudal hypothalamic neurons: calcium channel contribution to excitability. J Neu-rophysiol 84: 2896-2903, 2000.
14. Fedirchuk B, Nielsen J, Petersen N, Hultborn H. Pharmacologically evoked fictive motor patterns in the acutely spinalized marmoset monkey (Callithrix jacchus). Exp Brain Res 122: 351-361, 1998.
15. Gabriel JP, Mahmood R, Kyriakatos A, Soll I, Hauptmann G, Calabrese RL, El Manira A. Serotonergic modulation of locomotion in zebrafish: endogenous release and synaptic mechanisms. J Neurosci 29: 10387-10395, 2009.
16. 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.
17. Gavazzo P, Guida P, Zanardi I, Marchetti C. Molecular determinants of multiple effects of nickel on NMDA receptor channels. Neurotox Res 15: 38-48, 2009.
18. Getting PA. Emerging principles governing the operation of neural networks. Annu Rev Neurosci 12: 185-204, 1989.
19. Gordon IT, Whelan PJ. Monoaminergic control of cauda-equina-evoked locomotion in the neonatal mouse spinal cord. J Neurophysiol 96: 3122-3129, 2006.
20. Grillner S. Neurobiological bases of rhythmic motor acts in vertebrates. Science 228: 143-149, 1985.
21. Grillner S, McClellan A, Sigvardt K, Wallen P, Wilen M. Activation of NMDA-receptors elicits "fictive locomotion" in lamprey spinal cord in vitro. Acta Physiol Scand 113: 549-551, 1981.
22. 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.
23. Harris-Warrick RM. Voltage-sensitive ion channels in rhythmic motor systems. Curr Opin Neurobiol 12: 646-651, 2002.
24. Harris-Warrick RM, Coniglio LM, Barazangi N, Guckenheimer J, Gueron S. Dopamine modulation of transient potassium current evokes phase shifts in a central pattern generator network. J Neurosci 15: 342-358, 1995.
25. Harris-Warrick RM, Sparks DL. Neural control. Curr Opin Neurobiol 5: 721-726, 1995.
26. Hayes JA, Mendenhall JL, Brush BR, Del Negro CA. 4-Aminopyridine-sensitive outward currents in preBotzinger complex neurons influence respiratory rhythm generation in neonatal mice. J Physiol 586: 1921-1936, 2008.
27. Hess D, El Manira A. Characterization of a high-voltage-activated IA current with a role in spike timing and locomotor pattern generation. Proc Natl Acad Sci USA 98: 5276-5281, 2001.
28. Hille B. Ionic Channels of Excitable Membranes. Sunderland, MA: Sinauer, 1992.
29. Hinckley C, Seebach B, Ziskind-Conhaim L. Distinct roles of glycinergic and GABAergic inhibition in coordinating locomotor-like rhythms in the neonatal mouse spinal cord. Neuroscience 131: 745-758, 2005.
30. Ho S, O'Donovan MJ. Regionalization and intersegmental coordination of rhythm-generating networks in the spinal cord of the chick embryo. J Neurosci 13: 1354-1371, 1993.
31. Huang L, Keyser BM, Tagmose TM, Hansen JB, Taylor JT, Zhuang H, Zhang M, Ragsdale DS, Li M. NNC 55-0396 [(1S,2S)-2-(2-(N-[(3-benzimidazol-2-yl)propyl]-N-methylamino)ethyl)-6-fluo ro-1,2,3,4-tetrahydro-1-isopropyl-2-naphtyl cyclopropanecarboxylate dihydrochlo- ride]: a new selective inhibitor of T-type calcium channels. J Pharmacol Exp Ther 309: 193-199, 2004.
32. Huguenard JR. Low-threshold calcium currents in central nervous system neurons. Annu Rev Physiol 58: 329-348, 1996.
33. Jiang Z, Carlin KP, Brownstone RM. An in vitro functionally mature mouse spinal cord preparation for the study of spinal motor networks. Brain Res 816: 493-499, 1999.
34. Juvin L, Simmers J, Morin D. Propriospinal circuitry underlying interlimb coordination in mammalian quadrupedal locomotion. J Neurosci 25: 6025-6035, 2005.
35. Kaku T, Lee TS, Arita M, Hadama T, Ono K. The gating and conductance properties of Cav3.2 low-voltage-activated T-type calcium channels. Jpn J Physiol 53: 165-172, 2003.
36. Kang HW, Moon HJ, Joo SH, Lee JH. Histidine residues in the IS3-IS4 loop are critical for nickel-sensitive inhibition of the Cav2.3 calcium channel. FEBS Lett 581: 5774-5780, 2007.
37. Kang HW, Park JY, Jeong SW, Kim JA, Moon HJ, Perez-Reyes E, Lee JH. A molecular determinant of nickel inhibition in Cav3.2 T-type calcium channels. J Biol Chem 281: 4823-4830, 2006.
38. Kiehn O. Locomotor circuits in the mammalian spinal cord. Annu Rev Neurosci 29: 279-306, 2006.
39. Kiehn O, Harris-Warrick RM. 5-HT modulation of hyperpolarization-activated inward current and calcium-dependent outward current in a crustacean motor neuron. J Neurophysiol 68: 496-508, 1992.
40. Kiehn O, Kjaerulff O. Distribution of central pattern generators for rhythmic motor outputs in the spinal cord of limbed vertebrates. Ann NY Acad Sci 16: 110-129, 1998.
41. Kim D, Song I, Keum S, Lee T, Jeong MJ, Kim SS, McEnery MW, Shin HS. Lack of the burst firing of thalamocortical relay neurons and resistance to absence seizures in mice lacking alpha(1G) T-type Ca(2+) channels. Neuron 31: 35-45, 2001.
42. Kjaerulff O, Kiehn O. Distribution of networks generating and coordinating locomotor activity in the neonatal rat spinal cord in vitro: a lesion study. J Neurosci 16: 5777-5794, 1996.
43. Kwan AC, Dietz SB, Webb WW, Harris-Warrick RM. Activity of Hb9 interneurons during fictive locomotion in mouse spinal cord. J Neurosci 29: 11601-11613, 2009.
44. Li M, Hansen JB, Huang L, Keyser BM, Taylor JT. Towards selective antagonists of T-type calcium channels: design, characterization and potential applications of NNC 55-0396. Cardiovasc Drug Rev 23: 173-196, 2005.
45. Li WC, Roberts A, Soffe SR. Specific brainstem neurons switch each other into pacemaker mode to drive movement by activating NMDA receptors. J Neurosci 30: 16609-16620, 2010.
46. Llinas RR, Steriade M. Bursting of thalamic neurons and states of vigilance. J Neurophysiol 95: 3297-3308, 2006.
47. Lundberg A. Half-centres revisited. In: Regulatory Functions of the CNS. Motion and Organization Principles. Advances in Physiological Sciences, edited by Szentagothai J, Palkovits M, and Hamori J. Budapest: Pergamon Akadem Kiado, 1981, vol. 1, p. 155-167.
48. Marder E, Bucher D. Central pattern generators and the control of rhythmic movements. Curr Biol 11: R986-R996, 2001.
49. 2+ currents, postinhibitory rebound, and postspike afterhyperpolarization in lamprey neurons. J Neurophysiol 70: 2606-2619, 1993.
50. McDearmid JR, Drapeau P. Rhythmic motor activity evoked by NMDA in the spinal zebrafish larva. J Neurophysiol 95: 401-417, 2006.
51. McKay BE, McRory JE, Molineux ML, Hamid J, Snutch TP, Zamponi GW, Turner RW. Ca(V)3 T-type calcium channel isoforms differentially distribute to somatic and dendritic compartments in rat central neurons. Eur J Neurosci 24: 2581-2594, 2006.
52. Molineux ML, McRory JE, McKay BE, Hamid J, Mehaffey WH, Rehak R, Snutch TP, Zamponi GW, Turner RW. Specific T-type calcium channel isoforms are associated with distinct burst phenotypes in deep cerebellar nuclear neurons. Proc Natl Acad Sci USA 103: 5555-5560, 2006.
53. Mulloney B, Perkel DH, Budelli RW. Motor-pattern production: interaction of chemical and electrical synapses. Brain Res 229: 25-33, 1981.
54. + current by mGluR1. J Neurophysiol 103: 441-445, 2010.
55. Newcomb R, Szoke B, Palma A, Wang G, Chen X, Hopkins W, Cong R, Miller J, Urge L, Tarczy-Hornoch K, Loo JA, Dooley DJ, Nadasdi L, Tsien RW, Lemos J, Miljanich G. Selective peptide antagonist of the class E calcium channel from the venom of the tarantula. Hysterocrates gigas. Biochemistry 37: 15353-15362, 1998.
56. 2+ channels in cardiac pace-making. J Pharmacol Sci 99: 197-204, 2005.
57. Pearson KG, Rossignol S. Fictive motor patterns in chronic spinal cats. J Neurophysiol 66: 1874-1887, 1991.
58. Pena F, Parkis MA, Tryba AK, Ramirez JM. Differential contribution of pacemaker properties to the generation of respiratory rhythms during nor-moxia and hypoxia. Neuron 43: 105-117, 2004.
59. Perkel DH, Mulloney B. Motor pattern production in reciprocally inhibitory neurons exhibiting postinhibitory rebound. Science 185: 181-183, 1974.
60. Roberts A, Li WC, Soffe SR. Roles for inhibition: studies on networks controlling swimming in young frog tadpoles. J Comp Physiol ANeuroethol Sens Neural Behav Physiol 194: 185-193, 2008.
61. 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.
62. Roberts A, Tunstall MJ, Wolf E. Properties of networks controlling locomotion and significance of voltage dependency of NMDA channels: stimulation study of rhythm generation sustained by positive feedback. J Neurophysiol 73: 485-495, 1995.
63. Satterlie RA. Reciprocal and postinhibitory rebound produce reverberations in a locomotor pattern generator. Science 26: 402-404, 1985.
64. 2+ channel alpha 1 subunit. Receptors Channels 2: 255-270, 1994.
65. Serrano GE, Martinez-Rubio C, Miller MW. Endogenous motor neuron properties contribute to a program-specific phase of activity in the multifunctional feeding central pattern generator of Aplysia. J Neurophysiol 98: 29-42, 2007.
66. Swensen AM, Bean BP. Ionic mechanisms of burst firing in dissociated Purkinje neurons. J Neurosci 23: 9650-9663, 2003.
67. 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.
68. Tegnér J, Hellgren-Kotaleski J, Lansner A, Grillner S. Low-voltage-activated calcium channels in the lamprey locomotor network: simulation and experiment. J Neurophysiol 77: 1795-1812, 1997.
69. Tobin AE, Calabrese RL. Myomodulin increases Ih and inhibits the Na/K pump to modulate bursting in leech heart interneurons. J Neurophysiol 94: 3938-3950, 2005.
70. 2+ current in adult rat sensory neurons: effects of anticonvulsant and anesthetic agents. J Neurophysiol 79: 240-252, 1998.
71. Tsien RW, Lipscombe D, Madison DV, Bley KR, Fox AP. Multiple types of neuronal calcium channels and their selective modulation. Trends Neurosci 11: 431-438, 1988.
72. Wang D, Grillner S, Wallen P. Effects of flufenamic acid on fictive locomotion, plateau potentials, calcium channels and NMDA receptors in the lamprey spinal cord. Neuropharmacology 51: 1038-1046, 2006.
73. Wang D, Grillner S, Wallen P. 5-HT and dompamine modulates CaV1.3 calcium channels involved in postinhibitory rebound in the spinal network for locomotion in lamprey. J Neurophysiol 105: 1212-1224, 2011.
74. Wang G, Dayanithi G, Newcomb R, Lemos JR. An R-type Ca(2+) current in neurohypophysial terminals preferentially regulates oxytocin secretion. J Neurosci 19: 9235-9241, 1999.
75. 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.
76. Wilson JM, Blagovechtchenski E, Brownstone RM. Genetically defined inhibitory interneurons in the mouse spinal cord dorsal horn: a possible source of rhythmic inhibition of motoneurons during fictive locomotion. J Neurosci 30: 1137-1148, 2010.
77. Wilson JM, Cowan AI, Brownstone RM. Heterogeneous electrotonic coupling and synchronization of rhythmic bursting activity in mouse Hb9 interneurons. J Neurophysiol 98: 2370-2381, 2007.
78. Wilson JM, Hartley R, Maxwell DJ, Todd AJ, Lieberam I, Kaltschmidt JA, Yoshida Y, Jessell TM, Brownstone RM. Conditional rhythmicity of ventral spinal interneurons defined by expression of the Hb9 homeodomain protein. J Neurosci 25: 5710-5719, 2005.
79. Zamponi GW, Bourinet E, Snutch TP. Nickel block of a family of neuronal calcium channels: subtype- and subunit-dependent action at multiple sites. J Membr Biol 151: 77-90, 1996.
80. Zhong G, Droho S, Crone SA, Dietz S, Kwan AC, Webb WW, Sharma K, Harris-Warrick RM. Electrophysiological characterization of V2a interneurons and their locomotor-related activity in the neonatal mouse spinal cord. J Neurosci 30: 170-182, 2010.
81. 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.
82. 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.