Nicotinic Cholinergic Synaptic Mechanisms in the Ventral Tegmental Area Contribute to Nicotine Addiction

Learning and Memory

Volumn 11, Issue 1, 2004, Pages 60-69

  Pidoplichko, Volodymyr I ^a   Noguchi, Jun ^a   Areola, Oluwasanmi O ^a   Liang, Yong ^a   Peterson, Jayms ^a   Zhang, Tianxiang ^a   Dani, John A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; DOPAMINE RECEPTOR; GLUTAMATE RECEPTOR; NICOTINE; NICOTINIC RECEPTOR;

ARTICLE; BEHAVIOR; CHOLINERGIC SYNAPSE; CONCENTRATION (PARAMETERS); DOPAMINERGIC NERVE CELL; HUMAN; LEARNING; LONG TERM POTENTIATION; MEMORY; MESENCEPHALON; MESOLIMBIC DOPAMINERGIC SYSTEM; MORTALITY; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; REINFORCEMENT; TOBACCO DEPENDENCE; VENTRAL TEGMENTUM;

ACETYLCHOLINE; AFFERENT PATHWAYS; ANIMALS; CHOLINERGIC FIBERS; DOPAMINE; ELECTROPHYSIOLOGY; EXTRACELLULAR SPACE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; MICRODIALYSIS; NEURONAL PLASTICITY; NICOTINE; NUCLEUS ACCUMBENS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NICOTINIC; SUBSTANCE-RELATED DISORDERS; SYNAPTIC TRANSMISSION; TIME FACTORS; VENTRAL TEGMENTAL AREA;

EID: 0842282615     PISSN: 10720502     EISSN: None     Source Type: Journal    
DOI: 10.1101/lm.70004     Document Type: Article

References (95)

1. Albuquerque, E.X., Alkondon, M., Pereira, E.F., Castro, N.G., Schrattenholz, A., Barbosa, C.T., Bonfante-Cabarcas, R., Aracava, Y., Eisenberg, H.M., and Maelicke, A. 1997. Properties of neuronal nicotinic acetylcholine receptors: Pharmacological characterization and modulation of synaptic function. J. Pharmacol. Exp. Ther. 280: 1117-1136.
2. Alkondon, M. and Albuquerque, E.X. 1991. Initial characterization of the nicotinic acetylcholine receptors in rat hippocampal neurons. J. Recept. Res. 11: 1001-1021.
3. Alkondon, M., Pereira, E.F., Wonnacott, S., and Albuquerque, E.X. 1992. Blockade of nicotinic currents in hippocampal neurons defines methyllycaconitine as a potent and specific receptor antagonist. Mol. Pharmacol. 41: 802-808.
4. Alkondon, M., Pereira, E.F., Barbosa, C.T., and Albuquerque, E.X. 1997. Neuronal nicotinic acetylcholine receptor activation modulates γ-aminobutyric acid release from CA1 neurons of rat hippocampal slices. J. Pharmacol. Exp. Ther. 283: 1396-1411.
5. Alkondon, M., Pereira, E.F., and Albuquerque, E.X. 1998. α-Bungarotoxin- and methyllycaconitine-sensitive nicotinic receptors mediate fast synaptic transmission in interneurons of rat hippocampal slices. Brain Res. 810: 257-263.
6. Alkondon, M., Pereira, E.F., Almeida, L.E., Randall, W.R., and Albuquerque, E.X. 2000. Nicotine at concentrations found in cigarette smokers activates and desensitizes nicotinic acetylcholine receptors in CA1 interneurons of rat hippocampus. Neuropharmacology 39: 2726-2739.
7. Arroyo-Jimenez, M.M., Bourgeois, J.P., Marubio, L.M., Le Sourd, A.M., Ottersen, O.P., Rinvik, E., Fairen, A., and Changeux, J.P. 1999. Ultrastructural localization of the α4-subunit of the neuronal acetylcholine nicotinic receptor in the rat substantia nigra. J. Neurosci. 19: 6475-6487.
8. Azam, L., Winzer-Serhan, U.H., Chen, Y., and Leslie, F.M. 2002. Expression of neuronal nicotinic acetylcholine receptor subunit mRNAs within midbrain dopamine neurons. J. Comp. Neurol. 444: 260-274.
9. Balfour, D.J., Wright, A.E., Benwell, M.E., and Birrell, C.E. 2000. The putative role of extra-synaptic mesolimbic dopamine in the neurobiology of nicotine dependence. Behav. Brain Res. 113: 73-83.
10. Benowitz, N.L., Porchet, H., and Jacob III, P. 1989. Nicotine dependence and tolerance in man: Pharmacokinetic and pharmacodynamic investigations. Prog. Brain Res. 79: 279-287.
11. Bertrand, D., Devillers-Thiery, A., Revah, F., Galzi, J.L., Hussy, N., Mulle, C., Bertrand, S., Ballivet, M., and Changeux, J.P. 1992. Unconventional pharmacology of a neuronal nicotinic receptor mutated in the channel domain. Proc. Natl. Acad. Sci. 89: 1261-1265.
12. Bonci, A. and Malenka, R.C. 1999. Properties and plasticity of excitatory synapses on dopaminergic and GABAergic cells in the ventral tegmental area. J. Neurosci. 19: 3723-3730.
13. Calabresi, P., Lacey, M.G., and North, R.A. 1989. Nicotinic excitation of rat ventral tegmental neurones in vitro studied by intracellular recording. Br. J. Pharmacol. 98: 135-140.
14. Castro, N.G. and Albuquerque, E.X. 1995. α-Bungarotoxin-sensitive hippocampal nicotinic receptor channel has a high calcium permeability. Biophys. J. 68: 516-524.
15. CDC. 2002. Annual smoking-attributable mortality, years of potential life lost, and economic costs; United States, 1995-1999. Morbidity and Mortality Weekly Report, 51: 300-303. CDC.
16. Champtiaux, N., Han, Z.Y., Bessis, A., Rossi, F.M., Zoli, M., Marubio, L., McIntosh, J.M., and Changeux, J.P. 2002. Distribution and pharmacology of α 6-containing nicotinic acetylcholine receptors analyzed with mutant mice. J. Neurosci. 22: 1208-1217.
17. Charpantier, E., Barneoud, P., Moser, P., Besnard, F., and Sgard, F. 1998. Nicotinic acetylcholine subunit mRNA expression in dopaminergic neurons of the rat substantia nigra and ventral tegmental area. Neuroreport 9: 3097-3101.
18. Clarke, P.B. 1990. Dopaminergic mechanisms in the locomotor stimulant effects of nicotine. Biochem. Pharmacol. 40: 1427-1432.
19. -. 1991. The mesolimbic dopamine system as a target for nicotine. In Effects of nicotine on biological systems (eds. F. Adlkofer and K. Thurau), pp. 285-294. Birkhäuser Verlag, Basel.
20. 125I]-α-bungarotoxin. J. Neurosci. 5: 1307-1315.
21. Corrigall, W.A. 1999. Nicotine self-administration in animals as a dependence model. Nicotine Tob. Res. 1: 11-20.
22. Corrigall, W.A. and Coen, K.M. 1989. Nicotine maintains robust self-administration in rats on a limited-access schedule. Psychopharmacology 99: 473-478.
23. Corrigall, W.A., Franklin, K.B., Coen, K.M., and Clarke, P.B. 1992. The mesolimbic dopaminergic system is implicated in the reinforcing effects of nicotine. Psychopharmacology 107: 285-289.
24. Corrigall, W.A., Coen, K.M., and Adamson, K.L. 1994. Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area. Brain Res. 653: 278-284.
25. Dani, J.A. and De Biasi, M. 2001. Cellular mechanisms of nicotine addiction. Pharmacol. Biochem. Behav. 70: 439-446.
26. Dani, J.A. and Heinemann, S. 1996. Molecular and cellular aspects of nicotine abuse. Neuron 16: 905-908.
27. Dani, J.A., Radcliffe, K.A., and Pidoplichko, V.I. 2000. Variations in desensitization of nicotinic acetylcholine receptors from hippocampus and midbrain dopamine areas. Eur. J. Pharmacol. 393: 31-38.
28. Dani, J.A., Ji, D., and Zhou, F.M. 2001. Synaptic plasticity and nicotine addiction. Neuron 31: 349-352.
29. Di Chiara, G. 1999. Drug addiction as dopamine-dependent associative learning disorder. Eur. J. Pharmacol. 375: 13-30.
30. -. 2000. Role of dopamine in the behavioural actions of nicotine related to addiction. Eur. J. Pharmacol. 393: 295-314.
31. Di Chiara, G. and Imperato, A. 1988. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc. Natl. Acad. Sci. 85: 5274-5278.
32. Fenster, C.P., Rains, M.F., Noerager, B., Quick, M.W., and Lester, R.A. 1997. Influence of subunit composition on desensitization of neuronal acetylcholine receptors at low concentrations of nicotine. J. Neurosci. 17: 5747-5759.
33. Fenster, C.P., Whitworth, T.L., Sheffield, E.B., Quick, M.W., and Lester, R.A. 1999. Upregulation of surface α4β2 nicotinic receptors is initiated by receptor desensitization after chronic exposure to nicotine. J. Neurosci. 19: 4804-4814.
34. Frazier, C.J., Buhler, A.V., Weiner, J.L., and Dunwiddie, T.V. 1998. Synaptic potentials mediated via α-bungarotoxin-sensitive nicotinic acetylcholine receptors in rat hippocampal interneurons. J. Neurosci. 18: 8228-8235.
35. Garzon, M., Vaughan, R.A., Uhl, G.R., Kuhar, M.J., and Pickel, V.M. 1999. Cholinergic axon terminals in the ventral tegmental area target a subpopulation of neurons expressing low levels of the dopamine transporter. J. Comp. Neurol. 410: 197-210.
36. Goldner, F.M., Dineley, K.T., and Patrick, J.W. 1997. Immunohistochemical localization of the nicotinic acetylcholine receptor subunit α6 to dopaminergic neurons in the substantia nigra and ventral tegmental area. Neuroreport 8: 2739-2742.
37. Gourlay, S.G. and Benowitz, N.L. 1997. Arteriovenous differences in plasma concentration of nicotine and catecholamines and related cardiovascular effects after smoking, nicotine nasal spray, and intravenous nicotine. Clin. Pharmacol. Ther. 62: 453-463.
38. Gray, R., Rajan, A.S., Radcliffe, K.A., Yakehiro, M., and Dani, J.A. 1996. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383: 713-716.
39. Grenhoff, J. and Johnson, S.W. 1996. Sulfonylureas enhance GABAA synaptic potentials in rat midbrain dopamine neurones. Acta Physiol. Scand. 156: 147-148.
40. Guo, J.Z., Tredway, T.L., and Chiappinelli, V.A. 1998. Glutamate and GABA release are enhanced by different subtypes of presynaptic nicotinic receptors in the lateral geniculate nucleus. J. Neurosci. 18: 1963-1969.
41. Hefft, S., Hulo, S., Bertrand, D., and Muller, D. 1999. Synaptic transmission at nicotinic acetylcholine receptors in rat hippocampal organotypic cultures and slices. J. Physiol. 515: 769-776.
42. Henningfield, J.E., Stapleton, J.M., Benowitz, N.L., Grayson, R.F., and London, E.D. 1993. Higher levels of nicotine in arterial than in venous blood after cigarette smoking. Drug Alcohol Depend. 33: 23-29.
43. Imperato, A., Mulas, A., and Di Chiara, G. 1986. Nicotine preferentially stimulates dopamine release in the limbic system of freely moving rats. Eur. J. Pharmacol. 132: 337-338.
44. Ji, D. and Dani, J.A. 2000. Inhibition and disinhibition of pyramidal neurons by activation of nicotinic receptors on hippocampal interneurons. J. Neurophysiol. 83: 2682-2690.
45. Ji, D., Lape, R., and Dani, J.A. 2001. Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron 31: 131-141.
46. Jones, S., Sudweeks, S., and Yakel, J.L. 1999. Nicotinic receptors in the brain: Correlating physiology with function. Trends. Neurosci. 22: 555-561.
47. Jones, I.W., Bolam, J.P., and Wonnacott, S. 2001. Presynaptic localization of the nicotinic acetylcholine receptor β2 subunit immunoreactivity in rat nigrostriatal dopaminergic neurones. J. Comp. Neurol. 439: 235-247.
48. Kalivas, P.W., Churchill, L., and Klitenick, M.A. 1993. GABA and enkephalin projection from the nucleus accumbens and ventral pallidum to the ventral tegmental area. Neuroscience 57: 1047-1060.
49. Karan, L.D., Dani, J.A., and Benowitz, N.L. 2003. The pharmacology of nicotine dependence. In Principles of addiction medicine, 3rd ed. (eds. A. Graham et al.), pp. 225-248. American Society of Addiction Medicine, Inc.
50. Klink, R., de Kerchove d'Exaerde, A., Zoli, M., and Changeux, J.P. 2001. Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J. Neurosci. 21: 1452-1463.
51. Lena, C., Changeux, J.P., and Mulle, C. 1993. Evidence for "preterminal" nicotinic receptors on GABAergic axons in the rat interpeduncular nucleus. J. Neurosci. 13: 2680-2688.
52. Le Novère, N., Zoli, M., and Changeux, J.P. 1996. Neuronal nicotinic receptor α 6 subunit mRNA is selectively concentrated in catecholaminergic nuclei of the rat brain. Eur. J. Neurosci. 8: 2428-2439.
53. Li, X., Rainnie, D.G., McCarley, R.W., and Greene, R.W. 1998. Presynaptic nicotinic receptors facilitate monoaminergic transmission. J. Neurosci. 18: 1904-1912.
54. 3|nicotine binding to putative high affinity receptor sites in rat brain. Mol. Pharmacol. 31: 392-400.
55. Mansvelder, H.D. and McGehee, D.S. 2000. Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron 27: 349-357.
56. -. 2002. Cellular and synaptic mechanisms of nicotine addiction. J. Neurobiol. 53: 606-617.
57. Mansvelder, H.D., Keath, J.R., and McGehee, D.S. 2002. Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 33: 905-919.
58. Martin, S.J., Grimwood, P.D., and Morris, R.G. 2000. Synaptic plasticity and memory: An evaluation of the hypothesis. Annu. Rev. Neurosci. 23: 649-711.
59. McGehee, D.S. and Role, L.W. 1995. Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu. Rev. Physiol. 57: 521-546.
60. McGehee, D.S., Heath, M.J., Gelber, S., Devay, P., and Role, L.W. 1995. Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269: 1692-1696.
61. McMahon, L.L., Yoon, K.W., and Chiappinelli, V.A. 1994. Nicotinic receptor activation facilitates GABAergic neurotransmission in the avian lateral spiriform nucleus. Neuroscience 59: 689-698.
62. McQuiston, A.R. and Madison, D.V. 1999. Nicotinic receptor activation excites distinct subtypes of interneurons in the rat hippocampus. J. Neurosci. 19: 2887-2896.
63. Nestler, E.J. 1992. Molecular mechanisms of drug addiction. J. Neurosci. 12: 2439-2450.
64. -. 1993. Cellular responses to chronic treatment with drugs of abuse. Crit. Rev. Neurobiol. 7: 23-39.
65. Nisell, M., Nomikos, G.G., and Svensson, T.H. 1994. Systemic nicotine-induced dopamine release in the rat nucleus accumbens is regulated by nicotinic receptors in the ventral tegmental area. Synapse 16: 36-44.
66. -. 1995. Nicotine dependence, midbrain dopamine systems and psychiatric disorders. Pharmacol. Toxicol. 76: 157-162.
67. Papke, R.L., Meyer, E., Nutter, T., and Uteshev, V.V. 2000. α7 receptor-selective agonists and modes of α7 receptor activation. Eur. J. Pharmacol. 393: 179-195.
68. Peng, X., Gerzanich, V., Anand, R., Whiting, P.J., and Lindstrom, J. 1994. Nicotine-induced increase in neuronal nicotinic receptors results from a decrease in the rate of receptor turnover. Mol. Pharmacol. 46: 523-530.
69. Peto, R., Lopez, A.D., Boreham, J., Thun, M., and Heath Jr., C. 1992. Mortality from tobacco in developed countries: Indirect estimation from national vital statistics. Lancet 339: 1268-1278.
70. Peto, R., Lopez, A.D., Boreham, J., Thun, M., Heath Jr., C., and Doll, R. 1996. Mortality from smoking worldwide. Br. Med. Bull. 52: 12-21.
71. Picciotto, M.R., Zoli, M., Rimondini, R., Lena, C., Marubio, L.M., Pich, E.M., Fuxe, K., and Changeux, J.P. 1998. Acetylcholine receptors containing the β2 subunit are involved in the reinforcing properties of nicotine. Nature 391: 173-177.
72. Pidoplichko, V.I., De Biasi, M., Williams, J.T., and Dani, J.A. 1997. Nicotine activates and desensitizes midbrain dopamine neurons. Nature 390: 401-404.
73. Pontieri, F.E., Tanda, G., Orzi, F., and Di Chiara, G. 1996. Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs. Nature 382: 255-257.
74. Quick, M.W. and Lester, R.A. 2002. Desensitization of neuronal nicotinic receptors. J. Neurobiol. 53: 457-478.
75. Radcliffe, K.A. and Dani, J.A. 1998. Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J. Neurosci. 18: 7075-7083.
76. Radcliffe, K.A., Fisher, J.L., Gray, R., and Dani, J.A. 1999. Nicotinic modulation of glutamate and GABA synaptic transmission of hippocampal neurons. Ann. NY Acad. Sci. 868: 591-610.
77. Rathouz, M.M., Vijayaraghavan, S., and Berg, D.K. 1996. Elevation of intracellular calcium levels in neurons by nicotinic acetylcholine receptors. Mol. Neurobiol. 12: 117-131.
78. Role, L.W. and Berg, D.K. 1996. Nicotinic receptors in the development and modulation of CN5 synapses. Neuron 16: 1077-1085.
79. 3H]dopamine from rat striatal synaptosomes. Neurosci. Lett. 189: 171-175.
80. Russell, M.A. 1987. Estimation of smoke dosage and mortality of non-smokers from environmental tobacco smoke. Toxicol. Lett. 35: 9-18.
81. Séguéla, P., Wadiche, J., Dineley-Miller, K., Dani, J.A., and Patrick, J.W. 1993. Molecular cloning, functional properties, and distribution of rat brain α 7: A nicotinic cation channel highly permeable to calcium. J. Neurosci. 13: 596-604.
82. Spanagel, R. and Weiss, F. 1999. The dopamine hypothesis of reward: Past and current status. Trends Neurosci. 22: 521-527.
83. Steffensen, S.C., Svingos, A.L., Pickel, V.M., and Henriksen, S.J. 1998. Electrophysiological characterization of GABAergic neurons in the ventral tegmental area. J. Neurosci. 18: 8003-8015.
84. Stolerman, I.P. and Jarvis, M.J. 1995. The scientific case that nicotine is addictive. Psychopharmacology (Berl) 117: 2-20.
85. Stolerman, I.P. and Shoaib, M. 1991. The neurobiology of tobacco addiction. Trends Pharmacol. Sci. 12: 467-473.
86. Wada, E., Wada, K., Boulter, J., Deneris, E., Heinemann, S., Patrick, J., and Swanson, L.W. 1989. Distribution of α 2, α 3, α 4, and β 2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: A hybridization histochemical study in the rat. J. Comp. Neurol. 284: 314-335.
87. Wada, E., McKinnon, D., Heinemann, S., Patrick, J., and Swanson, L.W. 1990. The distribution of mRNA encoded by a new member of the neuronal nicotinic acetylcholine receptor gene family (α 5) in the rat central nervous system. Brain Res. 526: 45-53.
88. WHO. 1997. Tobacco or health, a global status report, p. 495. World Health Organization Publications, Geneva.
89. Wonnacott, S. 1987. Brain nicotine binding sites. Hum. Toxicol. 6: 343-353.
90. -. 1997. Presynaptic nicotinic ACh receptors. Trends Neurosci. 20: 92-98.
91. Wonnacott, S., Drasdo, A., Sanderson, E., and Rowell, P. 1990. Presynaptic nicotinic receptors and the modulation of transmitter release. Ciba Found. Symp. 152: 87-101.
92. Wonnacott, S., Kaiser, S., Mogg, A., Soliakov, L., and Jones, I.W. 2000. Presynaptic nicotinic receptors modulating dopamine release in the rat striatum. Eur. J. Pharmacol. 393: 51-58.
93. Wooltorton, J.R., Pidoplichko, V.I., Broide, R.S., and Dani, J.A. 2003. Differential desensitization and distribution of nicotinic acetylcholine receptor subtypes in midbrain dopamine areas. J. Neurosci. 23: 3176-3185.
94. Yu, C.R. and Role, L.W. 1998. Functional contribution of the α7 subunit to multiple subtypes of nicotinic receptors in embryonic chick sympathetic neurones. J. Physiol. 509: 651-665.
95. Zhou, F.M., Liang, Y., and Dani, J.A. 2001. Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum. Nat. Neurosci. 4: 1224-1229.