Apamin-sensitive calcium-activated potassium currents (SK) are activated by persistent calcium currents in rat motoneurons

Journal of Neurophysiology

Volumn 97, Issue 5, 2007, Pages 3314-3330

  Li, X ^a   Bennett, D J ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

APAMIN; CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL N TYPE; CALCIUM CHANNEL P TYPE; NIMODIPINE; OMEGA CONOTOXIN; BARIUM; CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; LOCAL ANESTHETIC AGENT; TETRODOTOXIN;

AFTERHYPERPOLARIZATION; ANIMAL CELL; ARTICLE; CALCIUM CURRENT; COMPARATIVE STUDY; CONTROLLED STUDY; DENDRITE; ELECTRIC POTENTIAL; HYPERPOLARIZATION; HYSTERESIS; IN VITRO STUDY; INTRACELLULAR SPACE; MOTONEURON; NERVE STIMULATION; NONHUMAN; OSCILLATION; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; SACRAL SPINAL CORD; SODIUM CURRENT; SPIKE WAVE; SPINAL CORD; SPINE INJURY; VENTRAL ROOT; ANIMAL; CELL MEMBRANE POTENTIAL; CYTOLOGY; DRUG EFFECT; DRUG INTERACTION; ELECTRIC CONDUCTIVITY; ELECTROSTIMULATION; FEMALE; METABOLISM; METHODOLOGY; PHYSIOLOGY; RADIATION RESPONSE; SPRAGUE DAWLEY RAT;

ANESTHETICS, LOCAL; ANIMALS; APAMIN; BARIUM; CALCIUM; CALCIUM CHANNEL BLOCKERS; DOSE-RESPONSE RELATIONSHIP, RADIATION; DRUG INTERACTIONS; ELECTRIC CONDUCTIVITY; ELECTRIC STIMULATION; FEMALE; MEMBRANE POTENTIALS; MOTOR NEURONS; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; TETRODOTOXIN;

EID: 34447341746     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01068.2006     Document Type: Article

References (69)

1. Bennett DJ, Gorassini M, Fouad K, Sanelli L, Han Y, Cheng J. Spasticity in rats with sacral spinal cord injury. J Neurotrauma 16: 69-84, 1999a.
2. Bennett DJ, Gorassini MA, Siu M. In vitro preparation to study spasticity in chronic spinal rats. Soc Neurosci Abstr 25: 1394, 1999b.
3. Bennett DJ, Hultborn H, Fedirchuk B, Gorassini M. Synaptic activation of plateaus in hindlimb motoneurons of decerebrate cats. J Neurophysiol 80: 2023-2037, 1998.
4. Bennett DJ, Li Y, Siu M. Plateau potentials in sacrocaudal motoneurons of chronic spinal rats, recorded in vitro. J Neurophysiol 86: 1955-1971, 2001.
5. Bennett DJ, Sanelli L, Cooke C, Harvey PJ, Gorassini MA. Spastic long-lasting reflexes in the awake rat after sacral spinal cord injury. J Neurophysiol 91: 2247-2258, 2004.
6. Buschges A. The physiology of sensory cells in the ventral scoloparium of the stick insect femoral chordotonal organ. J Exp Biol 189: 285-292, 1994.
7. Cai X, Liang CW, Muralidharan S, Kao JP, Tang CM, Thompson SM. Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 44: 351-364, 2004.
8. Carlin KP, Jiang Z, Brownstone RM. Characterization of calcium currents in functionally mature mouse spinal motoneurons. Eur J Neurosci 12: 1624-1634, 2000a.
9. Carlin KP, Jones KE, Jiang Z, Jordan LM, Brownstone RM. Dendritic L-type calcium currents in mouse spinal motoneurons: implications for bistability. Eur J Neurosci 12: 1635-1646, 2000b.
10. Cens T, Rousset M, Leyris JP, Fesquet P, Charnet P. Voltage- and calcium-dependent inactivation in high voltage-gated Ca(2+) channels. Prog Biophys Mol Biol 90: 104-117, 2005.
11. Elbasiouny SM, Bennett DJ, Mushahwar VK. Simulation of dendritic CaV1.3 channels in cat lumbar motoneurons: spatial distribution. J Neurophysiol 94: 3961-3974, 2005.
12. + channel in normal and cancerous mammary cells in culture. J Membr Biol 119: 133-139, 1991.
13. Gorassini M, Bennett DJ, Kiehn O, Eken T, Hultborn H. Activation patterns of hindlimb motor units in the awake rat and their relation to motoneuron intrinsic properties. J Neurophysiol 82: 709-717, 1999.
14. Gorassini M, Yang JF, Siu M, Bennett DJ. Intrinsic activation of human motoneurons: possible contribution to motor unit excitation. J Neurophysiol 87: 1850-1858, 2002.
15. Gorassini MA, Bennett DJ, Yang JF. Self-sustained firing of human motor units. Neurosci Lett 247: 13-16, 1998.
16. Gorassini MA, Knash M, Harvey PJ, Bennett DJ, Yang JF. Role of motoneuron plateau potentials in the generation of involuntary muscle activity after spinal cord injury. Brain 127: 2247-2258, 2004.
17. Harvey PJ, Li X, Li Y, Bennett DJ. Endogenous monoamines are essential for persistent sodium currents and repetitive firing in rat spinal motoneurons. J Neurophysiol 96: 1171-1186, 2005a.
18. Harvey PJ, Li Y, Li X, Bennett DJ. Persistent sodium currents and repetitive firing in motoneurons of the sacrocaudal spinal cord of adults. J Neurophysiol 96: 1141-1157, 2005b.
19. 2 receptor activation facilitates a persistent sodium current and repetitive firing in spinal motoneurons of rats with and without chronic spinal injury. J Neurophysiol 96: 1158-1170, 2007c.
20. Heckman CJ, Lee RH. The role of voltage-sensitive dendritic conductances in generating bistable firing patterns in motoneurons. J Physiol Paris 93: 97-100, 1999.
21. Hille B. Ion Channels of Excitable Membranes (3rd ed.) Sunderland, MA: Sinauer, 2001.
22. Hounsgaard J, Hultborn H, Jespersen B, Kiehn O. Bistability of alpha-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan. J Physiol 405: 345-367, 1988a.
23. Hounsgaard J, Kiehn O. Ca++ dependent bistability induced by serotonin in spinal motoneurons. Exp Brain Res 57: 422-425, 1985.
24. Hounsgaard J, Kiehn O. Calcium spikes and calcium plateaux evoked by differential polarization in dendrites of turtle motoneurones in vitro. J Physiol 468: 245-259, 1993.
25. Hounsgaard J, Kiehn O. Serotonin-induced bistability of turtle motoneurones caused by a nifedipine-sensitive calcium plateau potential. J Physiol 414: 265-282, 1989.
26. Hounsgaard J, Kiehn O, Mintz I. Response properties of motoneurones in a slice preparation of the turtle spinal cord. J Physiol 398: 575-589, 1988b.
27. Hounsgaard J, Mintz I. Calcium conductance and firing properties of spinal motoneurones in the turtle. J Physiol 398: 591-603, 1988.
28. Hultborn H. Plateau potentials and their role in regulating motoneuronal firing. Adv Exp Med Biol 508: 213-218, 2002.
29. Hultborn H. Plateau potentials and their role in regulating motoneuronal firing. Prog Brain Res 123: 39-48, 1999.
30. Kernell D. The limits of firing frequency in cat lumbosacral motoneurones possessing different time course of afterhyperpolarization. Acta Physiol Scand 65: 87-100, 1965.
31. Kiehn O, Eken T. Prolonged firing in motor units: evidence of plateau potentials in human motoneurons? J Neurophysiol 78: 3061-3068, 1997.
32. Lancaster B, Nicoll RA, Perkel DJ. Calcium activates two types of potassium channels in rat hippocampal neurons in culture. J Neurosci 11: 23-30, 1991.
33. Lape R, Nistri A. Current and voltage clamp studies of the spike medium afterhyperpolarization of hypoglossal motoneurons in a rat brain stem slice preparation. J Neurophysiol 83: 2987-2995, 2000.
34. 2+]i changes in guinea pig vagal motoneurons: relationship to the slow afterhyperpolarization. J Neurophysiol 78: 825-834, 1997.
35. Lee RH, Heckman CJ. Bistability in spinal motoneurons in vivo: systematic variations in persistent inward currents. J Neurophysiol 80: 583-593, 1998a.
36. Lee RH, Heckman CJ. Bistability in spinal motoneurons in vivo: systematic variations in rhythmic firing patterns. J Neurophysiol 80: 572-582, 1998b.
37. Lee RH, Heckman CJ. Enhancement of bistability in spinal motoneurons in vivo by the noradrenergic alpha1 agonist methoxamine. J Neurophysiol 81: 2164-2174, 1999a.
38. Lee RH, Heckman CJ. Paradoxical effect of QX-314 on persistent inward currents and bistable behavior in spinal motoneurons in vivo. J Neurophysiol 82: 2518-2527, 1999b.
39. 2+]i and Ca(2+)-activated currents in neurons. Cell Calcium 19: 431-438, 1996.
40. Li Y, Bennett DJ. Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J Neurophysiol 90: 857-869, 2003.
41. Li Y, Gorassini MA, Bennett DJ. Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J Neurophysiol 91: 767-783, 2004a.
42. Li Y, Harvey PJ, Li X, Bennett DJ. Spastic long-lasting reflexes in the chronic spinal rat, studied in vitro. J Neurophysiol 91: 2236-2246, 2004b.
43. 2+ channels in hippocampal neurons. Nature 395: 900-905, 1998.
44. Matthews PB. Relationship of firing intervals of human motor units to the trajectory of post-spike after-hyperpolarization and synaptic noise. J Physiol 492: 597-628, 1996.
45. Maxwell L, Maxwell DJ, Neilson M, Kerr R. A confocal microscopic survey of serotoninergic axons in the lumbar spinal cord of the rat: co-localization with glutamate decarboxylase and neuropeptides. Neuroscience 75: 471-480, 1996.
46. McCarthy RT, TanPiengco PE. Multiple types of high-threshold calcium channels in rabbit sensory neurons: high-affinity block of neuronal L-type by nimodipine. J Neurosci 12: 2225-2234, 1992.
47. McLarnon JG. Potassium currents in motoneurones. Prog Neurobiol 47: 513-531, 1995.
48. Oomura Y, Maeno T. Does the neurone soma actually generate action potentials? Nature 197: 358-359, 1963.
49. Patel R, Kerr R, Maxwell DJ. Absence of co-localized glutamic acid decarboxylase and neuropeptides in noradrenergic axons of the rat spinal cord. Brain Res 749: 164-169, 1997.
50. 2+ channels. Brain Res Brain Res Rev 40: 223-229, 2002.
51. Perrier JF, Hounsgaard J. Ca(2+)-activated nonselective cationic current (I(CAN)) in turtle motoneurons. J Neurophysiol 82: 730-735, 1999.
52. Perrier JF, Hounsgaard J. 5-HT2 receptors promote plateau potentials in turtle spinal motoneurons by facilitating an L-type calcium current. J Neurophysiol 89: 954-959, 2003.
53. 2+-dependent AHPs and firing behavior in neocortical pyramidal neurons. J Neurophysiol 79: 2522-2534, 1998.
54. Powers RK, Binder MD. Persistent sodium and calcium currents in rat hypoglossal motoneurons. J Neurophysiol 89: 615-624, 2003.
55. Purvis LK, Butera RJ. Ionic current model of a hypoglossal motoneuron. J Neurophysiol 93: 723-733, 2005.
56. Safronov BV, Wolff M, Vogel W. Excitability of the soma in central nervous system neurons. Biophys J 78: 2998-3010, 2000.
57. Schwindt PC, Crill WE. Properties of a persistent inward current in normal and TEA-injected motoneurons. J Neurophysiol 43: 1700-1724, 1980.
58. Schwindt PC, Crill WE. Factors influencing motoneuron rhythmic firing: results from a voltage-clamp study. J Neurophysiol 48: 875-890, 1982.
59. Schwindt PC, Spain WJ, Foehring RC, Stafstrom CE, Chubb MC, Crill WE. Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro. J Neurophysiol 59: 424-449, 1988.
60. 2+ channels responsible for plateau potentials in motoneurons from the lumbar spinal cord of the turtle. Eur J Neurosci 18: 258-266, 2003.
61. Svirskis G, Hounsgaard J. Depolarization-induced facilitation of a plateau-generating current in ventral horn neurons in the turtle spinal cord. J Neurophysiol 78: 1740-1742, 1997.
62. Svirskis G, Hounsgaard J. Transmitter regulation of plateau properties in turtle motoneurons. J Neurophysiol 79: 45-50, 1998.
63. 2+ channels in hypoglossal motoneurons. J Neurosci 14: 5652-5660, 1994.
64. Viana F, Bayliss DA, Berger AJ. Multiple potassium conductances and their role in action potential repolarization and repetitive firing behavior of neonatal rat hypoglossal motoneurons. J Neurophysiol 69: 2150-2163, 1993.
65. Williams S, Serafin M, Muhlethaler M, Bernheim L. Distinct contributions of high- and low-voltage-activated calcium currents to afterhyperpolarizations in cholinergic nucleus basalis neurons of the guinea pig. J Neurosci 17: 7307-7315, 1997.
66. 2+-activated non-selective cation current in rabbit ventricular myocytes. J Physiol 522: 51-57, 2000.
67. Xu W, Lipscombe D. Neuronal Ca(V)1.3alpha(1) L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J Neurosci 21: 5944-5951, 2001.
68. Zador A, Koch C. Linearized models of calcium dynamics: formal equivalence to the cable equation. J Neurosci 14: 4705-4715, 1994.
69. Zong S, Zhou J, Tanabe T. Molecular determinants of calcium-dependent inactivation in cardiac L-type calcium channels. Biochem Biophys Res Commun 201: 1117-1123, 1994.