Roles of subthreshold calcium current and sodium current in spontaneous firing of mouse midbrain dopamine neurons

Journal of Neuroscience

Volumn 27, Issue 3, 2007, Pages 645-656

  Puopolo, Michelino ^a   Raviola, Elio ^a   Bean, Bruce P ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Calcium current; I h; Nimodipine; Pacemaker currents; Sodium current; Substantia nigra; Tyrosine hydroxylase

Indexed keywords

ALKALINE PHOSPHATASE PLACENTA ISOENZYME; CALCIUM CHANNEL BLOCKING AGENT; COBALT; NIMODIPINE; OMEGA CONOTOXIN GVIA; TETRODOTOXIN; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CELL MEMBRANE; CELL MEMBRANE POTENTIAL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; HYPERPOLARIZATION; MESENCEPHALON; MOUSE; NONHUMAN; PACEMAKER; PRIORITY JOURNAL; SODIUM CURRENT; SPIKE WAVE; SUBSTANTIA NIGRA; VOLTAGE CLAMP;

ACTION POTENTIALS; ANIMALS; CALCIUM CHANNELS; DOPAMINE; HUMANS; MESENCEPHALON; MICE; MICE, TRANSGENIC; NEURONS; SODIUM CHANNELS;

EID: 33846453291     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4341-06.2007     Document Type: Article

References (68)

1. Astman N, Gutnick MJ, Fleidervish IA (2006) Persistent sodium current in layer 5 neocortical neurons is primarily generated in the proximal axon. J Neurosci 26:3465-3473.
2. Atherton JF, Bevan MD (2005) Ionic mechanisms underlying autonomous action potential generation in the somata and dendrites of GABAergic substantia nigra pars reticulata neurons in vitro. J Neurosci 25:8272-8281.
3. Banerjee SA, Hoppe P, Brilliant M, Chikaraishi DM (1992) 5′ flanking sequences of the rat tyrosine hydroxylase gene target accurate tissuespecific, developmental, and transsynaptic expression in transgenic mice. J Neurosci 12:4460-4467.
4. Bennett BD, Callaway JC, Wilson CJ (2000) Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J Neurosci 20:8493-8503.
5. Beurrier C, Bioulac B, Hammond C (2000) Slowly inactivating sodium current (I(NaP)) underlies single-spike activity in rat subthalamic neurons. J Neurophysiol 83:1951-1957.
6. Bevan MD, Wilson CJ (1999) Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons. J Neurosci 19:7617-7628.
7. 2+ current in the action potentials of nociceptive sensory neurons. J Neurosci 22:10277-10290.
8. Cardozo DL, Bean BP (1995) Voltage-dependent calcium channels in rat midbrain dopamine neurons: modulation by dopamine and GABAB receptors. J Neurophysiol 74:1137-1148.
9. Cloues RK, Sather WA (2003) Afterhyperpolarization regulates firing rate in neurons of the suprachiasmatic nucleus. J Neurosci 23:1593-1604.
10. Dauer W, Przedborski S (2003) Parkinson's disease: mechanisms and models. Neuron 39:889-909.
11. De Groote G, De Waele P, Van de Voorde A, De Broe M, Fiers W (1983) Use of monoclonal antibodies to detect human placental alkaline phosphatase. Clin Chem 29:115-119.
12. Do MT, Bean BP (2003) Subthreshold sodium currents and pacemaking of subthalamic neurons: modulation by slow inactivation. Neuron 39:109-120.
13. 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.
14. 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.
15. Feigenspan A, Gustincich S, Bean BP, Raviola E (1998) Spontaneous activity of solitary dopaminergic cells of the retina. J Neurosci 18:6776-6789.
16. Fujimura K, Matsuda Y (1989) Autogenous oscillatory potentials in neurons of the guinea pig substantia nigra pars compacta in vitro. Neurosci Lett 10453-57.
17. Grace AA, Bunney BS (1984) The control of firing pattern in nigral dopamine neurons: single spike firing. J Neurosci 4:2866-2876.
18. Grace AA, Onn SP (1989) Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J Neurosci 9:3463-3481.
19. Gustincich S, Feigenspan A, Wu DK, Koopman LJ, Raviola E (1997) Control of dopamine release in the retina: a transgenic approach to neural networks. Neuron 18:723-736.
20. Hainsworth AH, Roper J, Kapoor R, Ashcroft FM (1991) Identification and electrophysiology of isolated pars compacta neurons from guinea-pig substantia nigra. Neuroscience 43:81-93.
21. Hallworth NE, Wilson CJ, Bevan MD (2004) Apamin-sensitive small conductance calcium-activated potassium channels, through their selective coupling to voltage-gated calcium channels, are critical determinants of the precision, pace, and pattern of action potential generation in rat subthalamic nucleus neurons in vitro. J Neurosci 23:7525-7542.
22. Harris NC, Webb C, Greenfield SA (1989) A possible pacemaker mechanism in pars compacta neurons of the guinea-pig substantia nigra revealed by various ion channel blocking agents. Neuroscience 31:355-362.
23. Häusser M, Stuart G, Racca C, Sakmann B (1995) Axonal initiation and active dendritic propagation of action potentials in substantia nigra neurons. Neuron 15:637-647.
24. Jackson AC, Yao GL, Bean BP (2004) Mechanism of spontaneous firing in dorsomedial suprachiasmatic nucleus neurons. J Neurosci 24:7985-7998.
25. Kang Y, Kitai ST (1993a) A whole cell patch-clamp study on the pacemaker potential in dopaminergic neurons of rat substantia nigra compacta. Neurosci Res 18:209-221.
26. Kang Y, Kitai ST (1993b) Calcium spike underlying rhythmic firing in dopaminergic neurons of the rat substantia nigra. Neurosci Res 18:195-207.
27. Kole MH, Hallermann S, Stuart GJ (2006) Single Ih channels in pyramidal neuron dendrites: properties, distribution, and impact on action potential output. J Neurosci 26:1677-1687.
28. Koob GF, Sanna PP, Bloom FE (1998) Neuroscience of addiction. Neuron 21:467-476.
29. 2+ channels activating at negative voltages. J Biol Chem 276:22100-22106.
30. Kuznetsov AS, Kopell NJ, Wilson CJ (2006) Transient high-frequency firing in a coupled-oscillator model of the mesencephalic dopaminergic neuron. J Neurophysiol 95:932-947.
31. Lewis DA, Lieberman JA (2000) Catching up on schizophrenia: natural history and neurobiology. Neuron 28:325-334.
32. Llinás R, Alonso A (1992) Electrophysiology of the mammillary complex in vitro. I. Tuberomammillary and lateral mammillary neurons. J Neurophysiol 68:1307-1320.
33. 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.
34. Lorincz A, Notomi T, Tamas G, Shigemoto R, Nusser Z (2002) Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci 5:1185-1193.
35. Magee JC (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18:7613-7624.
36. Magistretti J, Mantegazza M, Guatteo E, Wanke E (1996) Action potentials recorded with patch-clamp amplifiers: are they genuine? Trends Neurosci 19:530-534.
37. Magistretti J, Mantegazza M, de Curtis M, Wanke E (1998) Modalities of distortion of physiological voltage signals by patch-clamp amplifiers: a modeling study. Biophys J 74:831-842.
38. Medvedev GS, Wilson CJ, Callaway JC, Kopell N (2003) Dendritic synchrony and transient dynamics in a coupled oscillator model of the dopaminergic neuron. J Comput Neurosci 15:53-69.
39. Mercuri NB, Bonci A, Calabresi P, Stratta F, Stefani A, Bernardi G (1994) Effects of dihydropyridine calcium antagonists on rat midbrain dopaminergic neurones. Br J Pharmacol 113:831-838.
40. Mercuri NB, Bonci A, Calabresi P, Stefani A, Bernardi G (1995) Properties of the hyperpolarization-activated cation current Ih in rat midbrain dopaminergic neurons. Eur J Neurosci 7:462-469.
41. Mintz IM, Adams ME, Bean BP (1992) P-type calcium channels in central and peripheral neurons. Neuron 9:1-20.
42. Nedergaard S, Greenfield SA (1992) Sub-populations of pars compacta neurons in the substantia nigra: the significance of qualitatively and quantitatively distinct conductances. Neuroscience 48:423-437.
43. 2+ conductances in guinea-pig substantia nigra pars compacta neurones. J Physiol (Lond) 466:727-747.
44. Neher E (1992) Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol 207:123-131.
45. Neuhoff H, Neu A, Liss B, Roeper J (2002) I(h) channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J Neurosci 22:1290-1302.
46. Nieoullon A (2002) Dopamine and the regulation of cognition and attention. Prog Neurobiol 67:53-83.
47. Pennartz CM, Bierlaagh MA, Geurtsen AM (1997) Cellular mechanisms underlying spontaneous firing in rat suprachiasmatic nucleus: involvement of a slowly inactivating component of sodium current. J Neurophysiol 78:1811-1825.
48. Pignatelli A, Kobayashi K, Okano H, Belluzzi O (2005) Functional properties of dopaminergic neurones in the mouse olfactory bulb. J Physiol (Lond) 564:501-514.
49. + channels regulate pacemaker activity in nigral dopamine neurons. NeuroReport 7:809-814.
50. Puopolo M, Bean BP, Raviola E (2005) Spontaneous activity of isolated dopaminergic periglomerular cells of the main olfactory bulb. J Neurophysiol 94:3618-3627.
51. Raman IM, Bean BP (1999) Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J Neurosci 19:1663-1674.
52. Raman IM, Gustafson AE, Padgett D (2000) Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J Neurosci 20:9004-9016.
53. 2+ exchange for the pacemaking mechanism in guinea-pig sino-atrial node. J Physiol (Lond) 571:639-649.
54. Scholze A, Plant TD, Dolphin AC, Nurnberg B (2001) Functional expression and characterization of a voltage-gated CaV1.3 (alpha1D) calcium channel subunit from an insulin-secreting cell line. Mol Endocrinol 15:1211-1221.
55. Schultz W (2002) Getting formal with dopamine and reward. Neuron 36:241-263.
56. Seutin V, Massotte L, Renette MF, Dresse A (2001) Evidence for a modulatory role of Ih on the firing of a subgroup of midbrain dopamine neurons. NeuroReport 12:255-258.
57. Steffen MA, Seay CA, Amini B, Cai Y, Feigenspan A, Baxter DA, Marshak DW (2003) Spontaneous activity of dopaminergic retinal neurons. Biophys J 85:2158-2169.
58. Taddese A, Bean BP (2002) Subthreshold sodium current from rapidly inactivating sodium channels drives spontaneous firing of tuberomammillary neurons. Neuron 33:587-600.
59. Takada M, Kang Y, Imanishi M (2001) Immunohistochemical localization of voltage-gated calcium channels in substantia nigra dopamine neurons. Eur J Neurosci 13:757-762.
60. Takakusaki K, Kitai ST (1997) Ionic mechanisms involved in the spontaneous firing of tegmental pedunculopontine nucleus neurons of the rat. Neuroscience 78:771-794.
61. Walter JT, Alvina K, Womack MD, Chevez C, Khodakhah K (2006) Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia. Nat Neurosci 9:389-397.
62. Williams SR, Stuart GJ (2000) Site independence of EPSP time course is mediated by dendritic Ih in neocortical pyramidal neurons. J Neurophysiol 83:3177-3182.
63. Wilson CJ, Callaway JC (2000) Coupled oscillator model of the dopaminergic neuron of the substantia nigra. J Neurophysiol 83:3084-3100.
64. Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483-494.
65. Wolfart J, Neuhoff H, Franz O, Roeper J (2001) Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons. J Neurosci 21:3443-3456.
66. α1 L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J Neurosci 21:5944-5951.
67. Yung WH, Hausser MA, Jack JJ (1991) Electrophysiology of dopaminergic and non-dopaminergic neurones of the guinea-pig substantia nigra pars compacta in vitro. J Physiol (Lond) 436:643-667.
68. 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.