Age dependent nicotinic influences over dopamine neuron synaptic plasticity

Biochemical Pharmacology

Volumn 78, Issue 7, 2009, Pages 686-692

  Placzek, Andon N ^a   Zhang, Tao A ^a   Dani, John A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Development; Long term potentiation; Mesolimbic; Nicotine addiction; Nicotinic acetylcholine receptors; Ventral tegmental area

Indexed keywords

AMPA RECEPTOR; IONOTROPIC RECEPTOR; METHYLPHENIDATE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NICOTINE; NICOTINIC RECEPTOR;

ADAPTATION; ADOLESCENCE; AGE; ATTENTION DEFICIT DISORDER; BRAIN ELECTROPHYSIOLOGY; CIGARETTE SMOKING; DOPAMINERGIC NERVE CELL; HEALTH PROMOTION; HIGH RISK POPULATION; HUMAN; LONG TERM POTENTIATION; MESENCEPHALON; MESOLIMBIC DOPAMINERGIC SYSTEM; NERVE CELL PLASTICITY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; REVIEW; SMOKING CESSATION; SOCIAL PSYCHOLOGY; SYNAPTIC TRANSMISSION; TOBACCO DEPENDENCE;

ADOLESCENT; ADOLESCENT BEHAVIOR; AGE FACTORS; ANIMALS; DOPAMINE; HUMANS; MESENCEPHALON; NEURONAL PLASTICITY; NEURONS; NICOTINE; RECEPTORS, NICOTINIC; SYNAPSES; TOBACCO USE DISORDER;

EID: 68349148356     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2009.05.014     Document Type: Review

References (109)

1. Dani J.A., and Heinemann S. Molecular and cellular aspects of nicotine abuse. Neuron 16 (1996) 905-908
2. Di Chiara G. Role of dopamine in the behavioural actions of nicotine related to addiction. Eur J Pharmacol 393 (2000) 295-314
3. Karan L., Dani J.A., and Benowitz N. The Pharmacology of Nicotine and Tobacco. In: Graham A.W., Schultz T.K., Mayo-Smith M.F., Ries R.K., and Wilford B.B. (Eds). Principles of Addiction Medicine (2003), American Society of Addiction Medicine, Chevy Chase MD 225-248
4. Balfour D.J. The neurobiology of tobacco dependence: a preclinical perspective on the role of the dopamine projections to the nucleus. Nicotine Tob Res 6 (2004) 899-912
5. Di Chiara G., Bassareo V., Fenu S., De Luca M.A., Spina L., Cadoni C., et al. Dopamine and drug addiction: the nucleus accumbens shell connection. Neuropharmacology 47 Suppl 1 (2004) 227-241
6. Dani J.A., and Harris R.A. Nicotine addiction and comorbidity with alcohol abuse and mental illness. Nat Neurosci 8 (2005) 1465-1470
7. Dani J.A., Ji D., and Zhou F.M. Synaptic plasticity and nicotine addiction. Neuron 31 (2001) 349-352
8. Hyman S.E., Malenka R.C., and Nestler E.J. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29 (2006) 565-598
9. Gray R., Rajan A.S., Radcliffe K.A., Yakehiro M., and Dani J.A. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383 (1996) 713-716
10. Pidoplichko V.I., DeBiasi M., Williams J.T., and Dani J.A. Nicotine activates and desensitizes midbrain dopamine neurons. Nature 390 (1997) 401-404
11. Mansvelder H.D., and McGehee D.S. Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron 27 (2000) 349-357
12. Mansvelder H.D., Keath J.R., and McGehee D.S. Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 33 (2002) 905-919
13. Saal D., Dong Y., Bonci A., and Malenka R.C. Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37 (2003) 577-582
14. Pidoplichko V.I., Noguchi J., Areola O.O., Liang Y., Peterson J., Zhang T., et al. Nicotinic cholinergic synaptic mechanisms in the ventral tegmental area contribute to nicotine addiction. Learn Mem 11 (2004) 60-69
15. Ungless M.A., Whistler J.L., Malenka R.C., and Bonci A. Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411 (2001) 583-587
16. Malinow R., and Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25 (2002) 103-126
17. Borgland S.L., Malenka R.C., and Bonci A. Acute and chronic cocaine-induced potentiation of synaptic strength in the ventral tegmental area: electrophysiological and behavioral correlates in individual rats. J Neurosci 24 (2004) 7482-7490
18. Chen B.T., Bowers M.S., Martin M., Hopf F.W., Guillory A.M., Carelli R.M., et al. Cocaine but not natural reward self-administration nor passive cocaine infusion produces persistent LTP in the VTA. Neuron 59 (2008) 288-297
19. WHO. Tobacco or health, a global status report. World Health Organization 1997:495.
20. Chen J., and Millar W.J. Age of smoking initiation: implications for quitting. Health Rep 9 (1998) 39-46(Eng); 39-48(Fre)
21. Benowitz N.L. Nicotine addiction. Prim Care 26 (1999) 611-631
22. Taioli E., and Wynder E.L. Effect of the age at which smoking begins on frequency of smoking in adulthood. N Engl J Med 325 (1991) 968-969
23. Breslau N., and Peterson E.L. Smoking cessation in young adults: age at initiation of cigarette smoking and other suspected influences. Am J Public Health 86 (1996) 214-220
24. Kandel D.B., and Chen K. Extent of smoking and nicotine dependence in the United States: 1991-1993. Nicotine Tob Res 2 (2000) 263-274
25. Henningfield J.E., Moolchan E.T., and Zeller M. Regulatory strategies to reduce tobacco addiction in youth. Tob Control 12 Suppl 1 (2003) i14-i24
26. Berke J.D., and Hyman S.E. Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25 (2000) 515-532
27. Schultz W., Dayan P., and Montague P.R. A neural substrate of prediction and reward. Science 275 (1997) 1593-1599
28. Balfour D.J., Wright A.E., Benwell M.E., and Birrell C.E. The putative role of extra-synaptic mesolimbic dopamine in the neurobiology of nicotine dependence. Behav Brain Res 113 (2000) 73-83
29. Corrigall W.A., Franklin K.B., Coen K.M., and Clarke P.B. The mesolimbic dopaminergic system is implicated in the reinforcing effects of nicotine. Psychopharmacology (Berl) 107 (1992) 285-289
30. Dani J.A., and De Biasi M. Cellular mechanisms of nicotine addiction. Pharmacol Biochem Behav 70 (2001) 439-446
31. Dani J.A., and Montague P.R. Disrupting addiction through the loss of drug-associated internal states. Nat Neurosci 10 (2007) 403-404
32. Nestler E.J. Cellular responses to chronic treatment with drugs of abuse. Crit Rev Neurobiol 7 (1993) 23-39
33. Nisell M., Nomikos G.G., and Svensson T.H. Infusion of nicotine in the ventral tegmental area or the nucleus accumbens of the rat differentially affects accumbal dopamine release. Pharmacol Toxicol 75 (1994) 348-352
34. Pontieri F.E., Tanda G., Orzi F., and Di Chiara G. Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs. Nature 382 (1996) 255-257
35. Spanagel R., and Weiss F. The dopamine hypothesis of reward: past and current status. Trends Neurosci 22 (1999) 521-527
36. Wonnacott S. The paradox of nicotinic acetylcholine receptor upregulation by nicotine. Trends Pharmacol Sci 11 (1990) 216-219
37. Calabresi P., Lacey M.G., and North R.A. Nicotinic excitation of rat ventral tegmental neurones in vitro studied by intracellular recording. Br J Pharmacol 98 (1989) 135-140
38. Grenhoff J., and Johnson S.W. Sulfonylureas enhance GABAA synaptic potentials in rat midbrain dopamine neurones. Acta Physiol Scand 156 (1996) 147-148
39. Mansvelder H.D., and McGehee D.S. Cellular and synaptic mechanisms of nicotine addiction. J Neurobiol 53 (2002) 606-617
40. Picciotto M.R., Zoli M., Rimondini R., Lena C., Marubio L.M., Pich E.M., et al. Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine. Nature 391 (1998) 173-177
41. Wooltorton J.R., Pidoplichko V.I., Broide R.S., and Dani J.A. Differential desensitization and distribution of nicotinic acetylcholine receptor subtypes in midbrain dopamine areas. J Neurosci 23 (2003) 3176-3185
42. Zhang T., Zhang L., Liang Y., Siapas A.G., Zhou F.M., and Dani J.A. Dopamine signaling differences in the nucleus accumbens and dorsal striatum exploited by nicotine. J Neurosci 29 (2009) 4035-4043
43. Clarke P.B. Nicotinic receptor blockade therapy and smoking cessation. Br J Addict 86 (1991) 501-505
44. Corrigall W.A. Nicotine self-administration in animals as a dependence model. Nicotine Tob Res 1 (1999) 11-20
45. Corrigall W.A., and Coen K.M. Nicotine maintains robust self-administration in rats on a limited-access schedule. Psychopharmacology (Berl) 99 (1989) 473-478
46. Corrigall W.A., Coen K.M., and Adamson K.L. Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area. Brain Res 653 (1994) 278-284
47. Jones I.W., Bolam J.P., and Wonnacott S. Presynaptic localisation of the nicotinic acetylcholine receptor beta2 subunit immunoreactivity in rat nigrostriatal dopaminergic neurones. J Comp Neurol 439 (2001) 235-247
48. Wonnacott S., Kaiser S., Mogg A., Soliakov L., and Jones I.W. Presynaptic nicotinic receptors modulating dopamine release in the rat striatum. Eur J Pharmacol 393 (2000) 51-58
49. Zhou F.M., Liang Y., and Dani J.A. Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum. Nat Neurosci 4 (2001) 1224-1229
50. Watkins S.S., Koob G.F., and Markou A. Neural mechanisms underlying nicotine addiction: acute positive reinforcement and withdrawal. Nicotine Tob Res 2 (2000) 19-37
51. Buisson B., and Bertrand D. Chronic exposure to nicotine upregulates the human (alpha)4((beta)2 nicotinic acetylcholine receptor function. J Neurosci 21 (2001) 1819-1829
52. Clarke P.B., Schwartz R.D., Paul S.M., and Pert C.B. Pert A. Nicotinic binding in rat brain: autoradiographic comparison of [3H]acetylcholine, [3H]nicotine, and [125I]-alpha-bungarotoxin. J Neurosci 5 (1985) 1307-1315
53. Benowitz N.L., Porchet H., and Jacob III P. Nicotine dependence and tolerance in man: pharmacokinetic and pharmacodynamic investigations. Prog Brain Res 79 (1989) 279-287
54. Benowitz N.L., and Gourlay S.G. Cardiovascular toxicity of nicotine: implications for nicotine replacement therapy. J Am Coll Cardiol 29 (1997) 1422-1431
55. Henningfield J.E., Stapleton J.M., Benowitz N.L., Grayson R.F., and London E.D. Higher levels of nicotine in arterial than in venous blood after cigarette smoking. Drug Alcohol Depend 33 (1993) 23-29
56. Dani J.A., and Bertrand D. Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu Rev Pharmacol Toxicol 47 (2007) 699-729
57. Jones S., Sudweeks S., and Yakel J.L. Nicotinic receptors in the brain: correlating physiology with function. Trends Neurosci 22 (1999) 555-561
58. McGehee D.S., and Role L.W. Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu Rev Physiol 57 (1995) 521-546
59. Role L.W., and Berg D.K. Nicotinic receptors in the development and modulation of CNS synapses. Neuron 16 (1996) 1077-1085
60. Wonnacott S. Presynaptic nicotinic ACh receptors. Trends Neurosci 20 (1997) 92-98
61. Alkondon M., Pereira E.F., Wonnacott S., and Albuquerque E.X. Blockade of nicotinic currents in hippocampal neurons defines methyllycaconitine as a potent and specific receptor antagonist. Mol Pharmacol 41 (1992) 802-808
62. Castro N.G., and Albuquerque E.X. alpha-Bungarotoxin-sensitive hippocampal nicotinic receptor channel has a high calcium permeability. Biophys J 68 (1995) 516-524
63. Quick M.W., and Lester R.A. Desensitization of neuronal nicotinic receptors. J Neurobiol 53 (2002) 457-478
64. Klink R., de Kerchove d'Exaerde A., Zoli M., and Changeux J.P. Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J Neurosci 21 (2001) 1452-1463
65. Charpantier E., Barneoud P., Moser P., Besnard F., and Sgard F. Nicotinic acetylcholine subunit mRNA expression in dopaminergic neurons of the rat substantia nigra and ventral tegmental area. Neuroreport 9 (1998) 3097-3101
66. Goldner F.M., Dineley K.T., and Patrick J.W. Immunohistochemical localization of the nicotinic acetylcholine receptor subunit alpha6 to dopaminergic neurons in the substantia nigra and ventral tegmental area. Neuroreport 8 (1997) 2739-2742
67. Le Novere N., Zoli M., and Changeux J.P. Neuronal nicotinic receptor alpha 6 subunit mRNA is selectively concentrated in catecholaminergic nuclei of the rat brain. Eur J Neurosci 8 (1996) 2428-2439
68. Wada E., McKinnon D., Heinemann S., Patrick J., and Swanson L.W. The distribution of mRNA encoded by a new member of the neuronal nicotinic acetylcholine receptor gene family (alpha 5) in the rat central nervous system. Brain Res 526 (1990) 45-53
69. Wada E., Wada K., Boulter J., Deneris E., Heinemann S., Patrick J., et al. Distribution of alpha 2, alpha 3, alpha 4, and beta 2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybridization histochemical study in the rat. J Comp Neurol 284 (1989) 314-335
70. Mansvelder H.D., Lodder J.C., Sons M.S., and Kits K.S. Dopamine modulates exocytosis independent of Ca(2+) entry in melanotropic cells. J Neurophysiol 87 (2002) 793-801
71. Ji D., Lape R., and Dani J.A. Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron 31 (2001) 131-141
72. Albuquerque E.X., Pereira E.F., Alkondon M., Schrattenholz A., and Maelicke A. Nicotinic acetylcholine receptors on hippocampal neurons: distribution on the neuronal surface and modulation of receptor activity. J Recept Signal Transduct Res 17 (1997) 243-266
73. Ge S., and Dani J.A. Nicotinic acetylcholine receptors at glutamate synapses facilitate long-term depression or potentiation. J Neurosci 25 (2005) 6084-6091
74. Guo J.Z., Tredway T.L., and Chiappinelli V.A. Glutamate and GABA release are enhanced by different subtypes of presynaptic nicotinic receptors in the lateral geniculate nucleus. J Neurosci 18 (1998) 1963-1969
75. Li X., Rainnie D.G., McCarley R.W., and Greene R.W. Presynaptic nicotinic receptors facilitate monoaminergic transmission. J Neurosci 18 (1998) 1904-1912
76. McGehee D.S., Heath M.J., Gelber S., Devay P., and Role L.W. Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269 (1995) 1692-1696
77. Radcliffe K.A., and Dani J.A. Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J Neurosci 18 (1998) 7075-7083
78. Radcliffe K.A., Fisher J.L., Gray R., and Dani J.A. Nicotinic modulation of glutamate and GABA synaptic transmission of hippocampal neurons. Ann N Y Acad Sci 868 (1999) 591-610
79. Martin S.J., Grimwood P.D., and Morris R.G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23 (2000) 649-711
80. Di Chiara G. Drug addiction as dopamine-dependent associative learning disorder. Eur J Pharmacol 375 (1999) 13-30
81. Di Chiara G., and Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci USA 85 (1988) 5274-5278
82. Imperato A., Mulas A., and Di Chiara G. Nicotine preferentially stimulates dopamine release in the limbic system of freely moving rats. Eur J Pharmacol 132 (1986) 337-338
83. Rathouz M.M., Vijayaraghavan S., and Berg D.K. Elevation of intracellular calcium levels in neurons by nicotinic acetylcholine receptors. Mol Neurobiol 12 (1996) 117-131
84. Seguela P., Wadiche J., Dineley-Miller K., Dani J.A., and Patrick J.W. Molecular cloning, functional properties, and distribution of rat brain alpha 7: a nicotinic cation channel highly permeable to calcium. J Neurosci 13 (1993) 596-604
85. DiFranza J.R., Rigotti N.A., McNeill A.D., Ockene J.K., Savageau J.A., St Cyr D., et al. Initial symptoms of nicotine dependence in adolescents. Tob Control 9 (2000) 313-319
86. O'Loughlin J., Gervais A., Dugas E., and Meshefedjian G. Milestones in the process of cessation among novice adolescent smokers. Am J Public Health 99 (2009) 499-504
87. Laviolette S.R., and van der Kooy D. The motivational valence of nicotine in the rat ventral tegmental area is switched from rewarding to aversive following blockade of the alpha7-subunit-containing nicotinic acetylcholine receptor. Psychopharmacology (Berl) 166 (2003) 306-313
88. Laviolette S.R., and van der Kooy D. The neurobiology of nicotine addiction: bridging the gap from molecules to behaviour. Nat Rev 5 (2004) 55-65
89. Wonnacott S., Sidhpura N., and Balfour D.J. Nicotine: from molecular mechanisms to behaviour. Curr Opin Pharmacol 5 (2005) 53-59
90. Slotkin T.A. Nicotine and the adolescent brain: insights from an animal model. Neurotoxicol Teratol 24 (2002) 369-384
91. Jones S., and Bonci A. Synaptic plasticity and drug addiction. Curr Opin Pharmacol 5 (2005) 20-25
92. Levin E.D., Rezvani A.H., Montoya D., Rose J.E., and Swartzwelder H.S. Adolescent-onset nicotine self-administration modeled in female rats. Psychopharmacology (Berl) 169 (2003) 141-149
93. Adriani W., Spijker S., Deroche-Gamonet V., Laviola G., Le Moal M., Smit A.B., et al. Evidence for enhanced neurobehavioral vulnerability to nicotine during periadolescence in rats. J Neurosci 23 (2003) 4712-4716
94. Schochet T.L., Kelley A.E., and Landry C.F. Differential expression of arc mRNA and other plasticity-related genes induced by nicotine in adolescent rat forebrain. Neuroscience 135 (2005) 285-297
95. Shram M.J., Funk D., Li Z., and Le A.D. Acute nicotine enhances c-fos mRNA expression differentially in reward-related substrates of adolescent and adult rat brain. Neurosci Lett 418 (2007) 286-291
96. Dwyer J.B., McQuown S.C., and Leslie F.M. The dynamic effects of nicotine on the developing brain. Pharmacol Ther (2009)
97. Spear L.P. Adolescent brain development and animal models. Ann N Y Acad Sci 1021 (2004) 23-26
98. Azam L., Chen Y., and Leslie F.M. Developmental regulation of nicotinic acetylcholine receptors within midbrain dopamine neurons. Neuroscience 144 (2007) 1347-1360
99. Kauer J.A., and Malenka R.C. Synaptic plasticity and addiction. Nat Rev 8 (2007) 844-858
100. Petersen D.R., Norris K.J., and Thompson J.A. A comparative study of the disposition of nicotine and its metabolites in three inbred strains of mice. Drug Metab Dispos 12 (1984) 725-731
101. Matta S.G., Balfour D.J., Benowitz N.L., Boyd R.T., Buccafusco J.J., Caggiula A.R., et al. Guidelines on nicotine dose selection for in vivo research. Psychopharmacology (Berl) 190 (2007) 269-319
102. Fiedler E.P., Marks M.J., and Collins A.C. Postnatal development of two nicotinic cholinergic receptors in seven mouse brain regions. Int J Dev Neurosci 8 (1990) 533-540
103. Zhang X., Liu C., Miao H., Gong Z.H., and Nordberg A. Postnatal changes of nicotinic acetylcholine receptor alpha 2, alpha 3, alpha 4, alpha 7 and beta 2 subunits genes expression in rat brain. Int J Dev Neurosci 16 (1998) 507-518
104. Doura M.B., Gold A.B., Keller A.B., and Perry D.C. Adult and periadolescent rats differ in expression of nicotinic cholinergic receptor subtypes and in the response of these subtypes to chronic nicotine exposure. Brain Res 1215 (2008) 40-52
105. Drenan R.M., Grady S.R., Whiteaker P., McClure-Begley T., McKinney S., Miwa J.M., et al. In vivo activation of midbrain dopamine neurons via sensitized, high-affinity alpha 6 nicotinic acetylcholine receptors. Neuron 60 (2008) 123-136
106. Pons S., Fattore L., Cossu G., Tolu S., Porcu E., McIntosh J.M., et al. Crucial role of alpha4 and alpha6 nicotinic acetylcholine receptor subunits from ventral tegmental area in systemic nicotine self-administration. J Neurosci 28 (2008) 12318-12327
107. Connor D.F. Preschool attention deficit hyperactivity disorder: a review of prevalence, diagnosis, neurobiology, and stimulant treatment. J Dev Behav Pediatr 23 (2002) S1-9
108. Killen J.D., Robinson T.N., Ammerman S., Hayward C., Rogers J., Stone C., et al. Randomized clinical trial of the efficacy of bupropion combined with nicotine patch in the treatment of adolescent smokers. J Consult Clin Psychol 72 (2004) 729-735
109. Niederhofer H., and Huber M. Bupropion may support psychosocial treatment of nicotine-dependent adolescents: preliminary results. Pharmacotherapy 24 (2004) 1524-1528