Effects of nicotine on dopaminergic nigrostriatal axons requires stimulation of presynaptic glutamatergic receptors

Journal of Pharmacology and Experimental Therapeutics

Volumn 277, Issue 3, 1996, Pages 1685-1693

  Garcia Munoz, M ^a,b   Patino, P ^a   Young, S J ^a   Groves, P M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 7 PHOSPHONOHEPTANOIC ACID; 6,7 DINITRO 2,3 QUINOXALINEDIONE; AUTORECEPTOR; CHLORISONDAMINE; DOPAMINE; GLUTAMATE RECEPTOR; GLUTAMIC ACID; MECAMYLAMINE; METIROSINE; N METHYL DEXTRO ASPARTIC ACID; NICOTINE; NICOTINIC RECEPTOR;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDROMIC STIMULATION; ARTICLE; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DOSE RESPONSE; DRUG ANTAGONISM; DRUG COMPETITION; DRUG RECEPTOR BINDING; ELECTROPHYSIOLOGY; MALE; NERVE EXCITABILITY; NEUROTRANSMISSION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING;

ANIMALS; AXONS; CORPUS STRIATUM; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUTAMIC ACID; MALE; NICOTINE; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 12644272785     PISSN: 00223565     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (77)

1. AMADOR, M. AND DANI, J. A.: MK-801 inhibition of nicotine acetylcholine receptor channels. Synapse 7: 207-215, 1991.
2. BALFOUR, D. J. K.: The effects of nicotine on brain neurotransmitter systems. Pharmacol. Ther. 16: 169-282, 1982.
3. 3H]Mecamylamine binding to rat brain membranes: Studies with mecamylamine and nicotine analogues. Biochem. Pharmacol. 40: 2105-2120, 1990.
4. BARBEITO, L., CHERAMY, A., GODEHEU, G., DESCE, J., M. AND GLOWINSKI, J.: Glutamate receptors of a quisqualate-kainate subtype are involved in the presynaptic regulation of dopamine release in cat caudate nucleus in vivo. Eur. J. Neurosci. 2: 304-311, 1989.
5. 3H]-D-aspartate and endogenous GABA in freely moving guinea pigs. Br. J. Pharmacol. 104: 15-20, 1991.
6. BEN-ELIYAHU, S., MAREK, P., VACCARINO, A. L., MOGIL, J. S., STERNBERG, W. F. AND LIEBESKIND, J. C.: The NMDA receptor antagonist MK801 prevents long-lasting non-associative morphine tolerance in the rat. Brain Res. 575: 304-308, 1992.
7. BIZIERE, K. AND COYLE, J. T.: Influence of cortico-striatal afferents on striatal kainic acid neurotoxicity. Neurosci. Lett. 8: 303-310, 1978.
8. CHAVEZ-NORIEGA, L., PATINO, P. AND GARCIA-MUNOZ, M.: Excitability changes induced in the striatal dopamine-containing terminals following frontal cortex stimulation. Brain Res. 379: 300-306, 1986.
9. CHESSELET, M. F.: Presynaptic regulation of dopamine release. Implications for the functional organization of the basal ganglia. In Presynaptic Receptors and the Question of Autoregulation of Neurotransmitter Release, ed. by S. Kalsner and T. C. Westfall, pp. 17-22, Annals of the New York Academy of Science, New York, 1990.
10. CLARKE, P. B. S., CHAUDIEU, I., EL-BIZRI, H., BOKSA, P., QUIK, M., EPSLIN, B. A. AND CAPEK, R.: The pharmacology of the nicotinic antagonist, chlorisondamine, investigated in rat brain and autonomic ganglion. Br. J. Pharmacol. 111: 397-405, 1994.
11. 125I-alphabungarotoxin labeled nicotinic receptors inter-peduncular nucleus of rats. II. Effects of habenular deafferentation. J. Comp. Neurol. 251: 407-413, 1986.
12. CLARKE, P. B. S. AND PERT, A.: Autoradiographic evidence for nicotinic receptors on nigrostriatal and mesolimbic dopaminergic neurons. Brain Res. 348: 355-358, 1985.
13. CUELLO, C. A.: Nonclassical neuronal communications. Fed. Proc. 42: 2912-2922, 1966.
14. EARLE, M. L. AND DAVIES, J. A.: The effect of methamphetamine on the release of glutamate from striatal slices. J. Neural Transm. 86: 217-222, 1991.
15. ELVERFORS, A. AND NISSBRANDT, H.: Effects of d-amphetamine on dopaminergic neurotransmission; a comparison between substantia nigra and the striaturn. Neuropharmacology 31: 661-670, 1992.
16. FAGG, G. E., FOSTER, A. C., MENA, E. E. AND COTMAN, C. W.: Chloride and calcium ions separate L-glutamate receptor populations in synaptic membranes. Eur. J. Pharmacol. 88: 105-110, 1983.
17. FREUND, T. F., POWELL, J. F. AND SMITH, A. D.: Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience 13: 1189-1215, 1984.
18. FUNG, Y. K. AND LAU, Y.-S.: Effect of nicotine pretreatment on striatal dopaminergic system in rats. Pharmacol. Biochem. Behav. 32: 221-226, 1989.
19. FUNG, Y. K. AND LAU, Y.-S.: Chronic effects of nicotine on mesolimbic dopaminergic system in rats. Pharmacol. Biochem. Behav. 41: 57-63, 1991.
20. FUXE, K. AND AGNATI, L. F.: Volume Transmission in the Brain: Novel Mechanisms for Neural Transmission, Raven Press, New York, 1991.
21. GARCIA-MUNOZ, M., YOUNG, S. J. AND GROVES, P. M.: Terminal excitability of the corticostriatal pathway. I. Regulation by dopamine receptor stimulation. Brain Res. 551: 195-206, 1991a.
22. GARCIA-MUNOZ, M., YOUNG, S. J. AND GROVES, P. M.: Terminal excitability of the corticostriatal pathway. II. Regulation by glutamate receptor stimulation. Brain Res. 551: 207-215, 1991b.
23. GIORGUIEFF-CHESSELET, M. F., KEMEL, M. F., WANDSCHEER, D. AND GLOWINSKI, J.: Regulation of dopamine release by presynaptic nicotinic receptors in rat striatal slices: Effect of nicotine in low concentration. Life Sci. 25: 1257-1262, 1979.
24. GRACE, A. A.: The regulation of dopamine neuron activity as determined by in vivo and in vitro intracellular recordings. In Neurophysiology of Dopaminergic Systems. Current Status and Clinical Perspectives., ed. by L. A. Chiodo and A. S. Freeman, pp. 1-66, Lakeshore Publishing Co., Grosse Pointe, MI 1987.
25. GREENAMYRE, J. T. AND YOUNG, A. B.: Synaptic localization of striatal NMDA, quisqualate and kainate receptors. Neurosci. Lett. 101: 133-137, 1989.
26. GROVES, P. M., FENSTER, G. A., TEPPER, J. M., NAKAMURA, S. AND YOUNG, S. J.: Changes in dopaminergic terminal excitability induced by amphetamine and haloperidol. Brain Res. 221: 425-431, 1981.
27. GROVES, P. M., LINDER, J. C. AND YOUNG, S. J.: 5-Hydroxydopamine-labeled dopaminergic axons: Three dimensional reconstructions of axons, synapses, and postsynaptic targets in rat neostriatum. Neuroscience 58: 593-604, 1994.
28. HALLIWELL, R. F., PETERS, A. J. AND LAMBERT, J. J.: The mechanism of action and pharmacological specificity of the anticonvulsant NMDA antagonist MK-801: A voltage clamp study of neuronal cells in culture. Br. J. Pharmacol. 96: 480-484, 1989.
29. HALPAIN, S., GIRAULT, J. A. AND GREENGARD, P.: Activation of NMDA receptors induces dephosphorylation of DARPP-32 in rat striatal slices. Nature 343: 369-372, 1990.
30. + depolarization or to N-methyl-D-aspartate increases the transcription of genes encoding the α1-and α5 GABAA receptor subunits. Mol. Brain Res. 28: 338-342, 1995.
31. HAYES, W. L.: Statistics, Harcourt Brace, New York, 1991.
32. KALSNER, S. AND WESTFALL, T. C. (EDS.): Presynaptic receptors and the question of autoregulation of neurotransmitter release. Ann. NY Acad. Sci. 604: 652-655, 1990.
33. KARLER, R., CALDER, L. D., CHAUDHRY, I. A. AND TURKANIS, S. A.: Blockade of 'reverse tolerance' to cocaine and amphetamine by MK-801. Life Sci. 45: 599-606, 1989.
34. KARLER, R., CHAUDHRY, I. A., CALDER, L. D. AND TURKANIS, S. A.: Amphetamine behavioral sensitization and the excitatory amino acids. Brain Res. 537: 76-82, 1990.
35. KEMEL, M.-L., DESBAN, M., GLOWINSKI, J. AND GAUCHY, C.: Distinct presynaptic control of dopamine release in striosomal and matrix areas of the cat caudate nucleus. Proc. Natl. Acad. Sci. U.S.A. 86: 9006-9010, 1989.
36. KREBS, M. O., DESCE, J. M., KEMEL, M. L., GAUCHY, C., GODEHEU, G., CHERAMY, A. AND GLOWINSKY, J.: Glutamatergic control of dopamine release in the rat striatum: evidence for presynaptic N-methyl-D-aspartate receptors on dopaminergic nerve terminals. J. Neurochem. 56: 81-85, 1991.
37. KURIBARA, H., ASAMI, T., IDA, I., IIJIMA, Y. AND TADOKORA, S.: Effects of repeated MK-801 on ambulation in mice and in sensitization following methamphetamine. Psychopharmacology 108: 271-275, 1992.
38. LEVEY, A. I., HERSCH, S. M., RYE, D. B., SUNAHARA, R. K., NIZNIK, H. B., KITT, C. A., PRICE, D. L., MAGGIOU, R., BRANN, M. R. AND CILIAX, B. J.: Localization of D1 and D2 dopamine receptors in brain with subtype-specific antibodies. Proc. Natl. Acad. Sci. U.S.A. 90: 8861-8865, 1993.
39. LIPPIELLO, P. K., FERNANDES, K. G., LANGONE, J. L. AND BJERCKE, R. J.: Characterization of nicotinic receptors on cultured cortical neurons using antiidiotypic antibodies and ligand binding. J. Pharmacol. Exp. Ther. 257: 1216-1224, 1991.
40. MANLEY, L. D., YOUNG, S. J., MANLEY, M. S. AND GROVES, P. M.: Serotoninergic modulation of nigrostriatal terminal excitability. In Soc. Neurosci. Abstr., vol. 18, pt. 1, p. 695, 1992.
41. MARTIN, B. R., ONAIVI, E. S. AND MARTIN, T. J.: What is the nature of mecamylamine's antagonism of the central effects of nicotine? Biochem. Pharmacol. 38: 3391-3397, 1989.
42. MASUO, Y., PELAPRAT, D., MONTAGNE, M. N., SCHERMAN, D. AND ROSTENE, W.: Regulation of neurotensin-containing neurons in the rat striatum and substantia nigra. Effects of unilateral nigral lesion with 6-hydroxydopamine on neurotensin content and its binding site density. Brain Res. 510: 203-210, 1990.
43. MAURA, G., GIARDI, A. AND RAITERI, M.: Release regulating D-2 dopamine receptors are located on striatal glutamatergic nerve terminals. J. Pharmacol. Exp. Ther. 247: 680-684, 1988.
44. MCGEHEE, D. A., HEATH, M. J. S., GELBER, S., DEVAY, P. AND ROLE, L. W.: Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269: 1692-1696, 1995.
45. MEREU, G., WESTFALL, T. C. AND WANG, R. Y.: Modulation of terminal excitability of mesolimbic dopaminergic neurons by d-amphetamine and haloperidol. Brain Res. 359: 88-96, 1985.
46. MORRISETT, R. A., REZVANI, A. H., OVERSTREET, D., JANOWSKY, D. S., WILSON, W. A. AND SWARTZWELDER, H. S.: MK-801 potently inhibits alcohol withdrawal seizures in rats. Eur. J. Pharmacol. 176: 103-105, 1990.
47. NAKAMURA, S., TEPPER, J. M., YOUNG, S. J. AND GROVES, P. M.: Neurophysiological consequences of presynaptic receptor activation in noradrenergic terminal excitability. Brain Res. 226: 155-170, 1981.
48. OVERTON, P. AND CLARK, D.: N-methyl-D-aspartate increases the excitability of nigrostriatal dopamine terminals. Eur. J. Pharmacol. 201: 117-120, 1991.
49. PAPKE, R. L.: The kinetic properties of neuronal nicotinic receptors: genetic basis of functional diversity. Prog. Neurobiol. 41: 509-531, 1993.
50. PEREZ DE LA MORA, M., MENDEZ-FRANCO, J., SALCEDA, R., AGUIRRE, A. AND FUXE, K.: Neurochemical effects of nicotine on glutamate and GABA mechanisms in the rat brain. Acta Physiol. Scand. 141: 241-250, 1991.
51. RAMOA, A. S., ALKONDON, M., ARACAVA, Y., IRONS, J., LUNT, G. G., DESPANDE, S. S., WONNACOTT, S., ARONSTAM, R. S. AND ALBUQUERQUE, E. X.: The anticonvulsant MK-801 interacts with peripheral and central nicotinic acetylcholine receptor ion channels. J. Pharmacol. Exp. Ther. 254: 71-82, 1990.
52. ROMO, R. AND SCHULTZ, W.: Prolonged changes in dopaminergic terminal excitability and short changes in dopaminergic neuron discharge rate after short peripheral stimulation in monkey. Neurosci. Lett. 62: 335-340, 1985.
53. ROWLANDS, G. J. AND ROBERTS, P. J.: Activation of dopamine receptors inhibits calcium-dependent glutamate release from cortico-striatal terminals in vitro. Eur. J. Pharmacol. 62: 241-242, 1980.
54. SACAAN, A. I., BYMASTER, F. P. AND SCHOEPP, D. D.: Metabotropic glutamate receptor activation produces extrapyramidal motor system activation that is mediated by striatal dopamine. J. Neurochem. 59: 245-251, 1992.
55. SAHIN, M., BOWEN, W. D. AND DONOGHUE, J. P.: Location of nicotinic and muscarinic cholinergic and mu-opiate receptors in rat cerebral neocortex: evidence from thalamic and cortical lesions. Brain Res. 579: 135-147, 1992.
56. SAWYER, S. F., TEPPER, J. M., YOUNG, S. J. AND GROVES, P. M.: Antidromic activation of dorsal raphe neurons from neostriatum: Physiological characterization and effects of terminal autoreceptor activation. Brain Res. 332: 15-28, 1985.
57. SCHENK, S., VALADEZ, A., MCNAMARA, C., HOSE, D. T., HIGLEY, D., BANKSON, M. G., GIBBS, S. AND HORGER, B. A.: Development and expression of sensitization to cocaine's reinforcing properties: Role of NMDA receptors. Psychopharmacology 111: 332-338, 1993.
58. 3H]acetylcholine on catecholamine and serotonin axons in brain. J. Neurochem. 42: 1495-1498, 1984.
59. SHOAIB, M., BENWELL, M. E. M., AKBAR, M. T., STOLERMAN, I. P. AND BALFOUR, D. J. K.: Behavioural and neurochemical adaptations to nicotine in rats: Influence of NMDA antagonists. Br. J. Pharmacol. 111: 1073-1080, 1994.
60. STASHEFF, S. F., HINES, M. AND WILSON, W. A.: Axon terminal hyperexcitability associated with epileptogenesis in vitro. I. Origin of ectopic spikes. J. Neurophysiol. 70: 961-975, 1993.
61. SWANSON, L. W., SIMMONS, D. M., WHITING, P. J. AND LINDSTROM, J.: Immunohistochemical localization of neuronal nicotinic receptors in the rodent central nervous system. J. Neurosci. 7: 3334-3342, 1987.
62. TAKEUCHI, H., YOUNG, S. J. AND GROVES, P. M.: Dopaminergic terminal excitability following arrival of the nerve impulse: The influence of amphetamine and haloperidol. Brain Res. 245: 47-56, 1982.
63. TALLAKSEN-GREENE, S. J., WILEY, R. G. AND ALBIN, R. L.: Localization of striatal excitatory amino acid binding site subtypes to striatonigral projection neurons. Brain Res. 594: 165-170, 1992.
64. TEPPER, J. M., GROVES, P. M. AND YOUNG, S. J.: The neuropharmacology of the autoinhibition of monoamine release. Trends Pharmacol. Sci. 6: 251-256, 1985.
65. TEPPER, J. M., YOUNG, S. J. AND GROVES, P. M.: Autoreceptor-mediated changes in dopaminergic terminal excitability: effects of increases in impulse flow. Brain Res. 309: 309-316, 1984.
66. TOTH, E., SERHEN, H., HASHIM, A., VIZI, E. S. AND LAJTHA, A.: Effect of nicotine on extracellular levels of neurotransmitters assessed by microdialysis in various brain regions: Role of glutamic acid. Neurochem. Res. 17: 265-271, 1992.
67. TOTH, E., Vizi, E. S. AND LAJTHA, A.: Effect of nicotine on levels of extracellular amino acids in regions of the rat brain in vivo. Neuropharmacology 32: 827-832, 1993.
68. TRUJILLO, K. A. AND AKIL, H.: Inhibition of morphine tolerance and dependence by the NMDA receptor antagonist MK-801. Science 251: 85-87, 1991.
69. URETSKY, N. J., SNODGRASS, S. R. AND LORENZO, A. V.: Studies on the mechanism of depletion of striatal dopamine by alpha-methyl-m-tyrosine. J. Pharmacol. Exp. Ther. 195: 465-479, 1975.
70. WANG, J. K. T.: Presynaptic glutamate receptors modulate dopamine release from striatal synaptosomes. J. Neurochem. 57: 819-822, 1991.
71. WESTFALL, T. C., GRANT, H. AND PERRY, J.: Release of dopamine and 5-hydroxytryptamine from rat striatal slices following activation of nicotinic-cholinergic receptors. Gen. Pharmacol. 14: 321-325, 1983.
72. WOLF, M., WHITE, F. J. AND XIU-TI, H.: MK-801 prevents alterations in the mesoaccumbens dopamine system associated with behavioral sensitization to amphetamine. J. Neurosci. 14: 1735-1745, 1994.
73. WOLF, M. E. AND KHANSA, M. R.: Repeated administration of MK-801 produces sensitization to its own locomotor stimulant effects but blocks sensitization to amphetamine. Brain Res. 562: 164-168, 1991.
74. WONNACOTT, S., DRASDO, A., SANDERSON, E. AND ROWELL, P.: Presynaptic nicotinic receptors and the modulation of transmitter release. In The Biology of Nicotine Dependence, Ciba Foundation Symposium 152, ed. by G. Bock and J. Marsh, pp. 87-101. John Wiley & Sons, New York, 1990.
75. WONNACOTT, S., IRONS, J., RAPIER, C., THORNE, B. AND LUNT, G. G.: Presynaptic modulation of transmitter release by nicotinic receptors. In Nicotine Receptors in the CNS: Their Role in Synaptic Transmission., ed. by A. Nordberg, K. Fuxe, B. Holmstedt and A. Sundwall, Progr. Brain Res., pp. 157-163, Elsevier, Amsterdam, 1989.
76. YANG, C. R. AND MOGENSON, G. J.: Dopamine enhances terminal excitability of hippocampal aceumbens neurons via D2 receptor: Role of dopamine in presynaptic inhibition. J. Neurosci. 6: 2470-2478, 1986.
77. YU, Z. J. AND WECKER, L.: Chronic nicotine administration differentially affects neurotransmitter release from rat striatal slices. J. Neurochem. 63: 186-194, 1994.