Carbachol induces burst firing of dopamine cells in the ventral tegmental area by promoting calcium entry through L-type channels in the rat

Journal of Physiology

Volumn 568, Issue 2, 2005, Pages 469-481

  Zhang, Lei ^a   Liu, Yudan ^a   Chen, Xihua ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIHYDRO 2,6 DIMETHYL 5 NITRO 4 [2 (TRIFLUOROMETHYL)PHENYL] 3 PYRIDINECARBOXYLIC ACID METHYL ESTER; 2 AMINO 5 PHOSPHONOVALERIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; ANATOXIN; APAMIN; ATROPINE; CADMIUM; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; CALCIUM ION; CARBACHOL; CHOLINERGIC RECEPTOR; CHOLINERGIC RECEPTOR STIMULATING AGENT; CYCLOPIAZONIC ACID; GLUTAMATE RECEPTOR; MECAMYLAMINE; MUSCARINIC RECEPTOR; NICKEL; NICOTINIC RECEPTOR; NIFEDIPINE; NYSTATIN; PICROTOXIN; SODIUM CHANNEL BLOCKING AGENT; TETRODOTOXIN; GLUTAMIC ACID; IONOTROPIC RECEPTOR;

ANIMAL CELL; ARTICLE; BRAIN SLICE; CALCIUM TRANSPORT; CELL KINETICS; CHOLINERGIC SYSTEM; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; DRUG RESPONSE; FEMALE; FREQUENCY ANALYSIS; MALE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL STIMULATION; NEUROMODULATION; NEWBORN; NONHUMAN; OSCILLATION; PATCH CLAMP; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; RECORDING; SYNAPSE; VENTRAL TEGMENTUM; ACTION POTENTIAL; ANIMAL TISSUE; CALCIUM ENTRY; CHOLINERGIC ACTIVITY; EXCITATION; KINETICS; MEMBRANE POTENTIAL; PATCH CLAMP TECHNIQUE; SYNAPTIC TRANSMISSION;

3-PYRIDINECARBOXYLIC ACID, 1,4-DIHYDRO-2,6-DIMETHYL-5-NITRO-4-(2-(TRIFLUOROMETHYL)PHENYL)-, METHYL ESTER; ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; CADMIUM; CALCIUM; CALCIUM CHANNEL AGONISTS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CARBACHOL; CHOLINERGIC AGONISTS; DOPAMINE; FEMALE; MALE; NEURONS; NIFEDIPINE; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTIC TRANSMISSION; TIME FACTORS; VENTRAL TEGMENTAL AREA;

EID: 27644520813     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2005.094722     Document Type: Article

References (58)

1. Beckstead MJ, Grandy DK, Wickman K & Williams JT (2004). Vesicular dopamine release elicits an inhibitory postsynaptic current in midbrain dopamine neurons. Neuron 42, 939-946.
2. Berridge MJ, Lipp P & Bootman MD (2000). The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1, 11-21.
3. Bonci A, Grillner P, Mercuri NB & Bernardi G (1998). L-type calcium channels mediate a slow excitatory synaptic transmission in rat midbrain dopaminergic neurons. J Neurosci 18, 6693-6703.
4. 2+ dependence and time course of somatodendritic dopamine release: substantia nigra versus striatum. J Neurosci 21, 7841-7847.
5. Chergui K, Suaud-Chagny MF & Gonon F (1994). Nonlinear relationship between impulse flow, dopamine release and dopamine elimination in the rat brain in vivo. Neuroscience 62, 641-645.
6. Choong K & Shen R (2004). Prenatal ethanol exposure alters the postnatal development of the spontaneous electrical actiyity of dopamine neurons in the ventral tegmental area. Neuroscience 126, 1083-1091.
7. Cooper DC (2002). The significance of action potential bursting in the brain reward circuit. Neurochem Int 41, 333-340.
8. Corrigall WA, Coen KM & Adamson KL (1994). Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area. Brain Res 653, 278-284.
9. 2+ channels contributes to the irregular firing of dopamine neurons in neonatal rats. J Neurosci 24, 11079-11087.
10. 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.
11. Dzhura I, Wu Y, Colbran RJ, Balser JR & Anderson ME (2000). Calmodulin kinase determines calcium-dependent facilitation of L-type calcium channels. Nat Cell Biol 2, 173-177.
12. Fiorillo CD & Williams JT (2000). Selective inhibition by adenosine of mGluR IPSPs in dopamine neurons after cocaine treatment. J Neurophysiol 83, 1307-1314.
13. Floresco SB, West AR, Ash B, Moore H & Grace AA (2003). Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat Neurosci 6, 968-973.
14. Garris PA, Ciolkowski EL, Pastore P & Wightman RM (1994). Efflux of dopamine from the synaptic cleft in the nucleus accumbens of the rat brain. J Neurosci 14, 6084-6093.
15. Gonon FG (1988). Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry. Neuroscience 24, 19-28.
16. Grace AA (2000). The tonic/phasic model of dopamine system regulation and its implications for understanding alcohol and psychostimulant craving. Addiction 95 (Suppl. 2), S119-S128.
17. Grace AA & Bunney BS (1984). The control of firing pattern in nigral dopamine neurons: Burst firing. J Neurosci 4, 2877-2890.
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. Grillner P, Berretta N, Bernardi G, Svensson TH & Mercuri NB (2000). Muscarinic receptors depress GABAergic synaptic transmission in rat midbrain dopamine neurons. Neuroscience 96, 299-307.
20. 3) receptors reduce excitatory transmission in dopamine neurons of the rat mesencephalon. Neuroscience 91, 557-565.
21. Grillner P & Mercuri NB (2002). Intrinsic membrane properties and synaptic inputs regulating the firing activity of the dopamine neurons. Behav Brain Res 130, 149-169.
22. Gronier B & Rasmussen K (1998). Activation of midbrain presumed dopaminergic neurones by muscarinic cholinergic receptors: An in vivo electrophysiological study in the rat. Br J Pharmacol 124, 455-464.
23. Ikemoto S & Wise RA (2002). Rewarding effects of the cholinergic agents carbachol and neostigmine in the posterior ventral tegmental area. J Neurosci 22, 9895-9904.
24. Johnson SW & North RA (1992). Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J Physiol 450, 455-468.
25. Johnson SW, Seutin V & North RA (1992). Burst firing in dopamine neurons induced by N-methyl-D-aspartate: role of electrogenic sodium pump. Science 258, 665-667.
26. Johnson SW & Wu YN (2004). Multiple mechanisms underlie burst firing in rat midbrain dopamine neurons in vitro. Brain Res 1019, 293-296.
27. Kang Y & Kitai ST (1993). Calcium spike underlying rhythmic firing in dopaminergic neurons of the rat substantia nigra. Neurosci Res 18, 195-207.
28. Kitai ST, Shepard PD, Callaway JC & Scroggs R (1999). Afferent modulation of dopamine neuron firing patterns. Curr Opin Neurobiol 9, 690-697.
29. Kiyatkin EA (1995). Functional significance of mesolimbic dopamine. Neurosci Biobehav Rev 19, 573-598.
30. Klink R, de Kerchove d'Exaerde A, Zoli M & Changeux JP (2001). Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J Neurosci 21, 1452-1463.
31. Knable MB & Weinberger DR (1997). Dopamine, the prefrontal cortex and schizophrenia. J Psychopharmacol 11, 123-131.
32. Koob GF (2000). Neurobiology of addiction. Toward the development of new therapies. Ann N Y Acad Sci 909, 170-185.
33. Korotkova TM, Sergeeva OA, Eriksson KS, Haas HL & Brown RE (2003). Excitation of ventral tegmental area dopaminergic and nondopaminergic neurons by orexins/hypocretins. J Neurosci 23, 7-11.
34. 1-like receptors. J Pharmacol Exp Ther 253, 395-400.
35. Lacey MG, Mercuri NB & North RA (1989). Two cell types in rat substantia nigra zona compacta distinguished by membrane properties and the actions of dopamine and opioids. J Neurosci 9, 1233-1241.
36. Lipscombe D, Helton TD & Xu W (2004). L-type calcium channels: the low down. J Neurophysiol 92, 2633-2641.
37. Mansvelder HD, Keath JR & McGehee DS (2002). Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 33, 905-919.
38. Mansvelder HD & McGehee DS (2000). Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron 27, 349-357.
39. 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.
40. 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.
41. Mereu G, Lilliu V, Casula A, Vargiu PF, Diana M, Musa A & Gessa GL (1997). Spontaneous bursting activity of dopaminergic neurons in midbrain slices from immature rats: role of N-methyl-D-aspartate receptors. Neuroscience 77, 1029-1036.
42. 2+ conductances in guinea-pig substantia nigra pars compacta neurones. J Physiol 466, 727-747.
43. 2+ channel activation of ryanodine receptors. Neuron 40, 53-63.
44. Pidoplichko VI, DeBiasi M, Williams JT & Dani JA (1997). Nicotine activates and desensitizes midbrain dopamine neurons. Nature 390, 401-404.
45. Pidoplichko VI, Noguchi J, Areola OO, Liang Y, Peterson J, Zhang T & Dani JA (2004). Nicotinic cholinergic synaptic mechanisms in the ventral tegmental area contribute to nicotine addiction. Learn Mem 11, 60-69.
46. + channels regulate pacemaker activity in nigral dopamine neurons. Neuroreport 7, 809-814.
47. Power JM & Sah P (2005). Intracellular calcium store filling by an L-type calcium current in the basolateral amygdala at subthreshold membrane potentials. J Physiol 562, 439-453.
48. Santi CM, Cayabyab FS, Sutton KG, McRory JE, Mezeyova J, Hamming KS, Parker D, Stea A & Snutch TP (2002). Differential inhibition of T-type calcium channels by neuroleptics. J Neurosci 22, 396-403.
49. Schultz W (2002). Getting formal with dopamine and reward. Neuron 36, 241-263.
50. Seutin V, Johnson SW & North RA (1993). Apamin increases NMDA-induced burst-firing of rat mesencephalic dopamine neurons. Brain Res 630, 341-344.
51. Shepard PD & Stump D (1999). Nifedipine blocks apamin-induced bursting activity in nigral dopamine-containing neurons. Brain Res 817, 104-109.
52. Shulman A, Jagoda J, Laycock G & Kelly H (1998). Calcium channel blocking drugs in the management of drug dependence, withdrawal and craving. A clinical pilot study with nifedipine and verapamil. Aust Fam Physician 27 (Suppl. 1), S19-S24.
53. Suaud-Chagny MF, Chergui K, Chouvet G & Gonon F (1992). Relationship between dopamine release in the rat nucleus accumbens and the discharge activity of dopaminergic neurons during local in vivo application of amino acids in the ventral tegmental area. Neuroscience 49, 63-72.
54. Wolfart J & Roeper J (2002). Selective coupling of T-type calcium channels to SK potassium channels prevents intrinsic bursting in dopaminergic midbrain neurons. J Neurosci 22, 3404-3413.
55. 1.2 phosphorylation by protein kinase C isoforms. J Biol Chem 280, 207-214.
56. Yin R & French ED (2000). A comparison of the effects of nicotine on dopamine and non-dopamine neurons in the rat ventral tegmental area: an in vitro electrophysiological study. Brain Res Bull 51, 507-514.
57. 2+ potentials via differential protein kinase A and C activation in rat prefrontal cortical neurons. J Neurosci 24, 8-23.
58. Zheng F & Johnson SW (2003). Metabotropic glutamate and muscarinic cholinergic receptor-mediated preferential inhibition of N-methyl-D-aspartate component of transmissions in rat ventral tegmental area. Neuroscience 116, 1013-1020.