Mechanism of spontaneous firing in dorsomedial suprachiasmatic nucleus neurons

Journal of Neuroscience

Volumn 24, Issue 37, 2004, Pages 7985-7998

  Jackson, Alexander C ^a   Yao, Gui Lan ^a   Bean, Bruce P ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Calcium current; Pacemaker; Pacemaking; Persistent sodium current; Sodium current; Spike

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; NIMODIPINE; TETRODOTOXIN;

ANIMAL CELL; ARTICLE; CALCIUM CURRENT; CELL ACTIVITY; CONTROLLED STUDY; DEPOLARIZATION; ION CONDUCTANCE; ION CURRENT; MEMBRANE STEADY POTENTIAL; NERVE CELL; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; RAT; SODIUM CURRENT; SUPRACHIASMATIC NUCLEUS; VOLTAGE CLAMP;

ACTION POTENTIALS; ANIMALS; ARGININE VASOPRESSIN; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; CIRCADIAN RHYTHM; ION TRANSPORT; NEURONS; NIMODIPINE; PATCH-CLAMP TECHNIQUES; POTASSIUM; RATS; RATS, LONG-EVANS; SODIUM; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; SUPRACHIASMATIC NUCLEUS; TETRODOTOXIN;

EID: 4644293035     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2146-04.2004     Document Type: Article

References (55)

1. Akasu T, Shoji S, Hasuo H (1993) Inward rectifier and low-threshold calcium currents contribute to the spontaneous firing mechanism in neurons of the rat suprachiasmatic nucleus. Pflügers Arch 425:109-116.
2. Avery RB, Johnston D (1996) Multiple channel types contribute to the low-voltage-activated calcium current in hippocampal CA3 pyramidal neurons. J Neurosci 16:5567-5582.
3. Bennett BD, Callaway JC, Wilson CJ (2000) Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J Neurosci 20:8493-88503.
4. Bogdanov KY, Vinogradova TM, Lakatta EG (2001) Sinoatrial nodal cell ryanodine receptor and Na(+)-Ca(2+) exchanger: molecular partners in pacemaker regulation. Circ Res 88:1254-1258.
5. Bouskila Y, Dudek FE (1995) A rapidly activating type of outward rectifier K+ current and A-current in rat suprachiasmatic nucleus neurones. J Physiol (Lond) 488:339-350.
6. Brumberg JC, Nowak LG, McCormick DA (2000) Ionic mechanisms underlying repetitive high-frequency burst firing in supragranular cortical neurons. J Neurosci 20:4829-4843.
7. Buijs RM, Swaab DF, Dogterom J, van Leeuwen FW (1978) Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat. Cell Tissue Res 186:423-433.
8. Cloues RK, Sather WA (2003) Afterhyperpolarization regulates firing rate in neurons of the suprachiasmatic nucleus. J Neurosci 23:1593-1604.
9. Grill WE (1996) Persistent sodium current in mammalian central neurons. Annu Rev Physiol 58:349-362.
10. de Haas V, Vogel W (1989) Sodium and potassium currents recorded during an action potential. Eur Biophys J 17:49-51.
11. de Jeu MTG, Pennartz CMA (1997) Functional characterization of the H-current in SCN neurons in subjective day and night: a whole-cell patch-clamp study in acutely prepared brain slices. Brain Res 767:72-80.
12. de Jeu MTG, Hermes M, Pennartz CMA (1998) Circadian modulation of membrane properties in slices of rat suprachiasmatic nucleus. NeuroReport 9:3725-3729.
13. Derambure PS, Boulant JA (1994) Circadian thermosensitive characteristics of suprachiasmatic neurons in vitro. Am J Physiol Regul Integr Comp Physiol 266:R1876-R1884.
14. Do MT, Bean BP (2003) Subthreshold sodium currents and pacemaking of subthalamic neurons. Modulation by slow inactivation. Neuron 39:109-120.
15. Durante P, Cardenas CG, Whittaker JA, Kitai ST, Scroggs RS (2004) Low-threshold L-type calcium channels in rat dopamine neurons. J Neurophysiol 91:1450-1454.
16. Eggermann E, Bayer L, Serafin M, Saint-Mleux B, Bernheim L, Machard D, Jones BE, Muhlethaler M (2003) The wake-promoting hypocretinorexin neurons are in an intrinsic state of membrane depolarization. J Neurosci 23:1557-1562.
17. Gillette MU, Tischkau (1999) Suprachiasmatic nucleus: the brain's circadian clock Recent Prog Horm Res 54:35-58.
18. Green DJ, Gillette R (1982) Circadian rhythm of firing rate recorded from single cells in the rat suprachiasmatic brain slice. Brain Res 245:198-200.
19. Hamada T, LeSauter J, Venuti JM, Silver R (2001) Expression of period genes: rhythmic and nonrhythmic compartments of the suprachiasmatic nucleus pacemaker. J Neurosci 21:7742-7750.
20. Huang RC (1993) Sodium and calcium currents in acutely dissociated neurons from rat suprachiasmatic nucleus. J Neurophysiol 70:1692-1703.
21. Huang RC, Peng YW, Yau KW (1993) Zinc modulation of a transient potassium current and histochemical localization of the metal in neurons of the suprachiasmatic nucleus. Proc Natl Acad Sci USA 90:11806-11810.
22. Inouye ST, Kawamura H (1979) Persistence of circadian rhythmicity in a mammalian hypothalamic "island" containing the suprachiasmatic nucleus. Proc Natl Acad Sci USA 76:5962-5966.
23. Jac M, Sumova A, Illnerova H (2000) c-Fos rhythm in subdivisions of the rat suprachiasmatic nucleus under artificial and natural photoperiods. Am J Physiol Regul Integr Comp Physiol 279:R2270-R2276.
24. Jones HC, Keep RF (1988) Brain fluid calcium concentration and response to acute hypercalcemia during development in rat. J Physiol (Lond) 402:579-593.
25. King DP, Takahashi JS (2000) Molecular genetics of circadian rhythms in mammals. Ann Rev Neurosci 23:713-742.
26. Kononenko NI, Dudek FE (2004) Mechanism of irregular firing of suprachiasmatic nucleus neurons in rat hypothalamic slices. J Neurophysiol 91:267-273.
27. Kononenko NI, Shao LR, Dudek FE (2004) Riluzole-sensitive slowly inactivating sodium current in rat suprachiasmatic nucleus neurons. J Neurophysiol 91:710-718.
28. 2+ channels activating at negative voltages. J Biol Chem 276:22100-22106.
29. Kurata Y, Hisatome I, Imanishi S, Shibamoto T (2002) Dynamical description of sinoatrial node pacemaking: improved mathematical model for primary pacemaker cell. Am J Physiol Heart Circ Physiol 283:H2074-H2101.
30. Leak RK, Moore RY (2001) Topographic organization of suprachiasmatic nucleus projection neurons. J Comp Neurol 433:312-334.
31. Llinás R, Sugimori M, Simon SM (1982) Transmission by presynaptic spike-like depolarization in the squid giant synapse. Proc Natl Acad Sci USA 79:2415-2419.
32. Magistretti J, Mantegazza M, Guatteo E, Wanke E (1996) Action potentials with patch-clamp amplifiers: are they genuine? Trends Neurosci 12:530-534.
33. Manthei RC, Wricht DC, Kenny AD (1973) Altered CSF constituents and retrograde amnesia in rats: a biochemical approach. Physiol Behav 10:517-521.
34. Moga MM, Moore RY (1997) Organization of neural inputs to the suprachiasmatic nucleus in the rat. J Comp Neurol 389:508-534.
35. Moore RY (1983) Organization and function of a central nervous system circadian oscillator: the suprachiasmatic hypothalamic nucleus. Fed Proc 42:2783-2789.
36. Moore RY (1996) Entrainment pathways and the functional organization of the circadian system. Prog Brain Res 111:103-119.
37. Moore RY, Speh JC, Leak RK (2002) Suprachiasmatic nucleus organization. Cell Tissue Res 309:89-98.
38. Neher E (1992) Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol 207:123-131.
39. Panda S, Hogenesch JB, Kay SA (2002) Circadian rhythms from flies to human. Nature 417:329-335.
40. Pennartz CM, Bos NP, Jeu MT, Geurtsen AM, Mirmiran M, Sluiter AA, Buijs RM (1998a) Membrane properties and morphology of vasopressin neurons in slices of rat suprachiasmatic nucleus. J Neurophysiol 80:2710-2717.
41. Pennartz CMA, Bierlaagh MA, Geurtsen AMS (1997) Cellular mechanisms underlying spontaneous firing in rat suprachiasmatic nucleus: Involvement of a slowly inactivating component of sodium current. J Neurophysiol 78:1811-1825.
42. Pennartz CMA, de Jeu MTG, Geurtsen AMS, Sluiter AA, Hermes MLHJ (1998b) Electrophysiological and morphological heterogeneity of neurons in slices of rat suprachiasmatic nucleus. J Physiol (Lond) 506:775-793.
43. Pennartz CMA, de Jeu MTG, Bos NPA, Schaap J, Geurtsen AMS (2002) Diurnal modulation of pacemaker potentials and calcium current in the mammalian circadian clock. Nature 416:286-290.
44. Raman IM, Gustafson AE, Padgett D (2000) Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J Neurosci 20:9004-9016.
45. Reppert SM, Weaver DR (2001) Molecular analysis of mammalian circadian rhythms. Annu Rev Physiol 63:647-676.
46. Schaap J, Bos NPA, de Jeu MTG, Geurtsen AMS, Meijer JH, Pennartz CMA (1999) Neurons of the suprachiasmatic nucleus show a circadian rhythm in membrane properties that is lost during prolonged whole-cell recording. Brain Res 815:154-166.
47. Shibata S, Oomura Y, Liou SY, Ueki S (1984) Electrophysiological studies of the development of suprachiasmatic neuronal activity in hypothalamic slice preparations. Brain Res 315:29-35.
48. Taddese A, Bean BP (2002) Subthreshold sodium current from rapidly inactivating sodium channels drives spontaneous firing of tuberomammillary neurons. Neuron 33:587-600.
49. Teshima K, Kim SH, Allen CN (2003) Characterization of an apamin-sensitive potassium current in suprachiasmatic nucleus neurons. Neuroscience 120:65-73.
50. van den Pol AN (1980) The hypothalamic suprachiasmatic nucleus of rat: intrinsic anatomy. J Comp Neurol 191:661-702.
51. van den Pol AN, Tsujimoto KL (1985) Neurotransmitters of the hypothalamic suprachiasmatic nucleus: immunocytochemical analysis of 25 neuronal antigens. Neuroscience 15:1049-1086.
52. Walsh IB, van den Berg RJ, Rietveld WJ (1995) Ionic currents in cultured rat suprachiasmatic nucleus. Neuroscience 69:915-929.
53. Welsh DK, Logothetis DE, Meister M, Reppert SM (1995) Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14:697-706.
54. Xu W, Lipscombe D (2001) Neuronal Ca(V)1.3α(1) L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J Neurosci 21:5944-5951.
55. Zaza A, Micheletti M, Brioschi A, Rocchetti M (1997) Ionic currents during sustained pacemaker activity in rabbit sino-atrial myocytes. J Physiol (Lond) 505:677-688.