Learning mechanisms in addiction: Synaptic plasticity in the ventral tegmental area as a result of exposure to drugs of abuse

Annual Review of Physiology

Volumn 66, Issue , 2004, Pages 447-475

  Kauer, Julie A ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Dopamine; LTD; LTP; Psychostimulant; Sensitization; VTA

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; ALCOHOL; AMPA RECEPTOR; AMPHETAMINE; CARBAMAZEPINE; COCAINE; DIAMORPHINE; FLUOXETINE; GLUCOCORTICOID RECEPTOR; GLUTAMATE RECEPTOR; MORPHINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NALTREXONE; NICOTINE; OPIATE; PHENCYCLIDINE; PSYCHOSTIMULANT AGENT; STREET DRUG;

ADDICTION; CELL FUNCTION; CENTRAL NERVOUS SYSTEM; DOPAMINE RELEASE; DRUG ABUSE; DRUG EXPOSURE; GABAERGIC TRANSMISSION; HIPPOCAMPUS; HUMAN; LEARNING; MESOLIMBIC DOPAMINERGIC SYSTEM; NERVE CELL PLASTICITY; NEUROBIOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SENSITIZATION; STRESS; VENTRAL TEGMENTUM; ANIMAL; DRUG EFFECT; PATHOPHYSIOLOGY; PSYCHOLOGICAL ASPECT; SYNAPSE;

ANIMALS; HUMANS; LEARNING; NEURONAL PLASTICITY; STREET DRUGS; SUBSTANCE-RELATED DISORDERS; SYNAPSES; VENTRAL TEGMENTAL AREA;

EID: 2342539137     PISSN: 00664278     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.physiol.66.032102.112534     Document Type: Review

References (160)

1. Hyman SE, Malenka RC. 2001. Addiction and the brain: the neurobiology of compulsion and its persistence. Nat. Rev. Neurosci. 2:695-703
2. Nestler EJ. 2001. Molecular basis of long-term plasticity underlying addiction. Nat. Rev. Neurosci. 2:119-28
3. Gerdeman GL, Partridge JG, Lupica CR, Lovinger DM. 2003. It could be habit forming: drugs of abuse and striatal synaptic plasticity. Trends Neurosci. 26:184-92
4. Di Chiara G, Imperato A. 1988. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc. Natl. Acad. Sci. USA 85:5274-78
5. Koob GF. 1992. Drugs of abuse: anatomy, pharmacology, and function of reward pathways. Trends Pharmacol. Sci. 13:177-84
6. Nestler EJ. 1992. Molecular mechanisms of drug addiction. J. Neurosci. 12:2439-50
7. Schultz W. 1998. Predictive reward signal of dopamine neurons. J. Neurophysiol. 80:1-27
8. Wise RA. 1996. Neurobiology of addiction. Curr. Opin. Neurobiol. 6:243-51
9. Wise RA, Bozarth MA. 1987. A psychomotor stimulant theory of addiction. Psychol. Rev. 94:469-92
10. Schultz W. 1997. Dopamine neurons and their role in reward mechanisms. Curr. Opin. Neurobiol. 7:191-97
11. Grace AA, Onn S-P. 1989. Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J. Neurosci. 9:3463-81
12. 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. 9:1233-41
13. Johnson SW, North RA. 1992. Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J. Physiol. 450:455-68
14. Johnson SW, North RA. 1992. Opioids excite dopamine neurons by hyperpolarization of local interneurons. J. Neurosci. 12:483-88
15. Beart PM, McDonald D, Gundlach AL. 1979. Mesolimbic dopaminergic neurones and somatodendritic, mechanisms. Neurosci. Lett. 15:165-70
16. Kalivas PW, Duffy P, Barrow J. 1989. Regulation of the mesocorticolimbic dopamine system by glutamic acid receptor subtypes. J. Pharmacol. Exp. Ther. 251:378-87
17. Aghajanian GK, Bunney BS. 1977. Dopamine "autoreceptors:" pharmacological characterization by microiontophoretic single unit recording studies. Naunyn Schmiedebergs Arch. Pharmacol. 297:1-7
18. 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(10):6084-93
19. Gonon F. 1997. Prolonged and extrasynaptic excitatory action of dopamine mediated by D1 receptors in the rat striatum in vivo. J. Neurosci. 17:5972-78
20. Kalivas PW, Duffy P. 1995. D1 receptors modulate glutamate transmission in the ventral tegmental area. J. Neurosci. 15:5379-88
21. Beckstead RM. 1979. An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal-projection (prefrontal) cortex in the rat. J. Comp. Neurol. 184:43-62
22. Christie MJ, Bridge S, James LB, Beart PM. 1985. Excitotoxic lesions suggest an aspartatergic projection from rat medial prefrontal cortex to ventral tegmental area. Brain Res. 333:169-72
23. Thierry AM, Chevalier G, Ferron A, Glowinski J. 1983. Diencephalic and mesencephalic efferents of the medial prefrontal cortex in the rat: electrophysiological evidence for the existence of branched axons. Exp. Brain Res. 50:273-82
24. Sesack SR, Pickel VM. 1992. Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J. Comp. Neurol. 320:145-60
25. Semba K, Fibiger HC. 1992. Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro- and antero-grade transport and immunohistochemical study. J. Comp. Neurol. 323:387-410
26. Garzon M, Vaughan RA, Uhl GR, Kuhar MJ, Pickel VM. 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
27. Georges F, Aston-Jones G. 2001. Potent regulation of midbrain dopamine neurons by the bed nucleus of the stria terminalis. J. Neurosci. 21:RC160
28. Carr DB, Sesack SR. 2000. Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J. Neurosci. 20:3864-73
29. Seutin V, Verbanck P, Massotte L, Dresse A. 1990. Evidence for the presence of NMDA receptors in the ventral tegmental area of the rat: an electrophysiological in vitro study. Brain Res. 514:147-50
30. Mercuri NB, Stratta F, Calabresi P, Bernardi G. 1992. A voltage-clamp analysis of NMDA-induced responses on dopaminergic neurons of the rat substantia nigra zona compacta and ventral tegmental area. Brain Res. 593:51-56
31. Mercuri NB, Stratta F, Calabresi P, Bonci A, Bernardi G. 1993. Activation of metabotropic glutamate receptors induces an inward current in rat dopamine mesencephalic neurons. Neuroscience 56:399-407
32. Wang T, French ED. 1993. L-glutamate excitation of A10 dopamine neurons is preferentially mediated by activation of NMDA receptors: extra- and intracellular electrophysiological studies in brain slices. Brain Res. 627:299-306
33. Wang T, French ED. 1993. Electrophysiological evidence for the existence of NMDA and non-NMDA receptors on rat ventral tegmental dopamine neurons. Synapse 13:270-77
34. Overton PG, Clark D. 1997. Burst firing in midbrain dopaminergic neurons. Brain Res. Rev. 25:312-34
35. Mercuri NB, Grillner P, Bernardi G. 1996. N-methyl-D-aspartate receptors mediate a slow excitatory postsynaptic potential in the rat midbrain dopaminergic neurons. Neuroscience 14:785-91
36. Bonci A, Malenka RC. 1999. Properties and plasticity of excitatory synapses on dopaminergic and GABAergic cells in the ventral tegmental area. J. Neurosci. 19:3723-30
37. Jones S, Kauer JA. 1999. Amphetamine depresses excitatory synaptic transmission in the ventral tegmental area via serotonin receptors. J. Neurosci. 19:9780-87
38. White FJ. 1996. Synaptic regulation of mesocorticolimbic dopamine neurons. Annu. Rev. Neurosci. 16:405-36
39. White FJ, Kalivas PW. 1998. Neuroadaptations involved in amphetamine and cocaine addiction. Drug Alcohol Depend. 51:141-53
40. Kalivas PW, Stewart J. 1991. Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity. Brain Res. Rev. 16:223-44
41. Robinson TE, Berridge KC. 1993. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res. Rev. 18:247-91
42. Robinson TE, Berridge KC. 2000. The psychology and neurobiology of addiction: an incentive-sensitization view. Addiction 95(Suppl.)2:S91-117
43. Robinson TE, Berridge KC. 2001. Incentive-sensitization and addiction Addiction 96:103-14
44. Paulson PE, Robinson TE. 1991. Sensitization to systemic amphetamine produces an enhanced locomotor response to a subsequent intra-accumbens amphetamine challenge in rats. Psychopharmacology 104:140-41
45. Valadez A, Schenk S. 1994. Persistence of the ability of amphetamine preexposure to facilitate acquisition of cocaine self-administration. Pharmacol. Biochem. Behav. 47:203-5
46. Self DW, Nestler EJ. 1998. Relapse to drug-seeking: neural and molecular mechanisms. Drug Alcohol Depend. 51:49-60
47. Badiani A, Anagnostaras SG, Robinson TE. 1995. The development of sensitization to the psychomotor stimulant effects of amphetamine is enhanced in a novel environment. Psychopharmacology 117:443-52
48. Badiani A, Oates MM, Day HEW, Watson SJ, Akil H, Robinson TE. 1998. Amphetamine-induced behavior, dopamine release, and c-fos mRNA expression: modulation by environmental novelty. J. Neurosci. 18:10579-93
49. Robinson TE, Browman KE, Crombag HS, Badiani A. 1998. Modulation of the induction or expression of psychostimulant sensitization by the circumstances surrounding drug administration. Neurosci. Biobehav. Rev. 22:347-54
50. Crombag HS, Badiani A, Robinson TE. 1996. Signalled versus unsignalled intravenous amphetamine: large differences in the acute psychomotor response and sensitization. Brain Res. 722:227-31
51. Kuzcenski R. 1983. Biochemical actions of amphetamine and other stimulants. In Stimulants, Neurochemical, Behavioral, and Clinical Perspectives, ed. I Creese, pp. 31-61. New York: Raven
52. Reith MEA, Meisler BE, Sershen H, Lajtha A. 1986. Structural requirements for cocaine congeners to interact with dopamine and serotonin uptake sites in mouse brain and to induce stereotyped behavior. Biochem. Pharmacol. 35:1123-29
53. Koob GF, Stinus L, LeMoal M. 1981. Hyperactivity and hypoactivity produced by lesions to the mesolimbic dopamine system. Behav. Brain Res. 3:341-59
54. Clarke PBS, Jakubovic A, Fibiger HC. 1988. Anatomical analysis of the involvement of mesolimbocortical dopamine in the locomotor stimulant actions of D-amphetamine and apomorphine. Psychopharmacology 96:511-20
55. Kelley AE, Throne LC. 1992. NMDA receptors mediate the behavioral effects of amphetamine infused into the nucleus accumbens. Brain Res. Bull. 29:247-54
56. Dougherty GG, Ellinwood EH. 1981. Chronic D-amphetamine in nucleus accumbens: lack of tolerance or reverse tolerance of locomotor activity. Life Sci. 28:2295-98
57. Kalivas PW, Weber B. 1988. Amphetamine injection into the ventral mesencephalon sensitizes rats to peripheral amphetamine and cocaine. J. Pharmacol. Exp. Ther. 245:1095-101
58. Vezina P. 1993. Amphetamine injected into the ventral tegmental area sensitizes the nucleus accumbens dopaminergic response to systemic amphetamine: an in vivo microdialysis study in the rat. Brain Res. 605:332-37
59. Perugini M, Vezina P. 1994. Amphetamine administered to the ventral tegmental area sensitizes rats to the locomotor effects of nucleus accumbens amphetamine. J. Pharmacol. Exp. Ther. 270:690-96
60. Vezina P, Stewart J. 1990. Amphetamine administration to the ventral tegmental area but not to the nucleus accumbens sensitizes rats to systemic morphine: lack of conditioned effects. Brain Res. 516:99-106
61. Deleted in proof
62. Vezina P, Kalivas PW, Stewart J. 1987. Sensitization occurs to the locomotor effects of morphine and the specific mu opioid receptor agonist, DAGO, administered repeatedly to the VTA but not to the nucleus accumbens. Brain Res. 417:51-58
63. Kalivas PW, Duffy P. 1987. Sensitization to repeated morphine injection in the rat: possible involvement of A10 dopamine neurons. J. Pharmacol. Exp. Ther. 241:204-12
64. Lett BT. 1989. Repeated exposures intensify rather than diminish the rewarding effects of amphetamine, morphine, and cocaine. Psychopharmacology 98:357-62
65. Stewart J. 1983. Conditioned and unconditioned drug effects in relapse to opiate and stimulant drug self-administration. Prog. Neuropsychopharmacol. Biol. Psychiatry 1:591-97
66. Vorel SR, Liu X, Hayes RJ, Spector JA, Gardner EL. 2001. Relapse to cocaine-seeking after hippocampal theta burst stimulation. Science 292:1175-78
67. De Vries TJ, Schoffelmeer AN, Binnekade R, Mulder AH, Vanderschuren LJ. 1998. Drug-induced reinstatement of heroin- and cocaine-seeking behaviour following long-term extinction is associated with expression of behavioural sensitization. Eur. J. Neurosci. 10:3565-71
68. Nestler EJ. 2001. Molecular basis of long-term plasticity underlying addiction. Nat. Rev. Neurosci. 2:119-28
69. Nestler EJ. 2002. Common molecular and cellular substrates of addiction and memory. Neurobiol. Learn. Mem. 78:637-47
70. Wolf ME. 1998. The role of excitatory amino acids in behavioral sensitization to psychomotor stimulants. Prog. Neurobiol. 54:1-42
71. Karler R, Calder LD, Chaudhry IA, Turkanis SA. 1989. Blockade of "reverse tolerance" to cocaine and amphetamine by MK-801. Life Sci. 45:599-606
72. Stewart J, Druhan JP. 1993. Development of both conditioning and sensitization to the behavioral activating effects of amphetamine is blocked by the non-competitive NMDA receptor antagonist, MK-801. Psychopharmacology. 110:125-32
73. Wolf ME, Jeziorski M. 1993. Coadministration of MK-801 with amphetamine, cocaine or morphine prevents rather than transiently masks the development of behavioral sensitization. Brain Res. 613:291-94
74. Jeziorski M, White FJ, Wolf ME. 1994. MK-801 prevents the development of behavioral sensitization during repeated morphine administration. Synapse 16:137-47
75. Ohmori T, Abekawa T, Muraki A, Koyama T. 1994. Competitive and non-competitive NMDA antagonists block sensitization to methamphetamine. Pharmacol. Biochem. Behav. 48:587-91
76. Li Y, Wolf ME. 1999. Can the "state-dependency" hypothesis explain prevention of amphetamine sensitization in rats by NMDA receptor antagonists? Psychopharmacology 141:351-61
77. Kalivas PW, Alesdatter JE. 1993. Involvement of NMDA receptor stimulation in the ventral tegmental area and amygdala in behavioral sensitization to cocaine. J. Pharmacol. Exp. Ther. 267:486-95
78. Wolf ME, Dahlin SL, Hu X-T, Xue C-J, White K. 1995. Effects of lesions of prefrontal cortex, amygdala, or fornix on behavioral sensitization to amphetamine: comparison with NMDA antagonists. Neuroscience 69:417-39
79. Wolf ME, Xue CJ. 2000. Amphetamine increases glutamate efflux in the rat ventral tegmental area by a mechanism involving glutamate transporters and reactive oxygen species. J. Neurochem. 75:1634-44
80. Schenk S, Snow S. 1994. Sensitization to cocaine's motor activating properties produced by electrical kindling of the medial prefrontal cortex but not of the hippocampus. Brain Res. 659:17-22
81. Karler R, Calder LD, Turkanis SA. 1991. DNQX blockade of amphetamine behavioral sensitization. Brain Res. 552:295-300
82. Tong Z-Y, Overton PG, Clark D. 1995. Chronic administration of (+)-amphetamine alters the reactivity of midbrain dopaminergic neurons to prefrontal cortex stimulation in the rat. Brain Res. 674:63-74
83. Collingridge GL, Kehl SJ, McLennan H. 1983. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J. Physiol. 334:33-46
84. Artola A, Singer W. 1987. Long-term potentiation and NMDA receptors in rat visual cortex. Nature 330:649-52
85. Dudek SM, Bear MF. 1992. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc. Natl. Acad. Sci. USA 89:4363-67
86. Mulkey RM, Malenka RC. 1992. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9:967-75
87. Crair MC, Malenka RC. 1995. A critical period for long-term potentiation at thalamocortical synapses. Nature 375:325-28
88. Bliss TVP, Lomo T. 1973. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232:331-56
89. 2+ of NMDA responses in spinal cord neurones. Nature 309:261-63
90. Nowak L, Bregestovski P, Ascher P, Herbert A, Prochiantz A. 1984. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307:462-65
91. Overton PG, Richards CD, Berry MS, Berry DC. 1999. Long-term potentiation at excitatory amino acid synapses on midbrain dopamine neurons. Neuro-Report 10:221-26
92. Mansvelder HD, McGehee DS. 2000. Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron 27:349-57
93. Karler R, Chaudhry IA, Calder LD, Turkanis SA. 1990. Amphetamine behavioral sensitization and the excitatory amino acids. Brain Res. 537:76-82
94. Kauer JA, Malenka RC, Nicoll RA. 1988. A persistent postsynaptic modification mediates long-term potentiation in the hippocampus. Neuron 1:911-17
95. Isaac JTR, Nicoll RA, Malenka RC. 1995. Evidence for silent synapses: implications for the expression of LTP. Neuron 15:427-34
96. Liao D, Hessler NA, Malinow R. 1995. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375:400-4
97. Oliet SHR, Malenka RC, Nicoll RA. 1996. Bidirectional control of quantal size by synaptic activity in the hippocampus. Science 271:1294-97
98. Zamanillo D, Sprengel R, Hvalby O, Jensen V, Burnashev N, et al. 1999. Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284:1805-11
99. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, et al. 1999. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284:1811-16
100. Malinow R, Malenka RC. 2002. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25:103-26
101. Carlezon WA Jr, Boundy VA, Haile CN, Lane SB, Kalb RG, et al. 1997. Sensitization to morphine induced by viral-mediated gene transfer. Science 277:812-14
102. White FJ, Hu X-T, Zhang X-F, Wolf ME. 1995. Repeated administration of cocaine or amphetamine alters neuronal responses to glutamate in the mesoaccumbens dopamine system. J. Pharmacol. Exp. Ther. 273:445-54
103. Zhang X-F, Hu X-T, White FJ, Wolf ME. 1997. Increased responsiveness of ventral tegmental area dopamine neurons to glutamate after repeated administration of cocaine or amphetamine is transient and selectively involves AMPA receptors. J. Pharmacol. Exp. Ther. 281:699-706
104. Churchill L, Swanson CJ, Urbina M,Kalivas PW. 1999. Repeated cocaine alters glutamate receptor subunit levels in the nucleus accumbens and ventral tegmental area of rats that develop behavioral sensitization. J. Neurochem. 72:2397-403
105. Fitzgerald LW, Ortiz J, Hamedani AG, Nestler EJ. 1996. Drugs of abuse and stress increase the expression of GluR1 and NMDAR1 glutamate receptor subunits in the rat ventral tegmental area: common adaptations among cross-sensitizing agents. J. Neurosci. 16:274-82
106. Wells DG, Dong X, Quinlan EM, Huang YS, Bear MF, et al. 2001. A role for the cytoplasmic polyadenylation element in NMDA receptor-regulated mRNA translation in neurons. J. Neurosci. 21:9541-48
107. Ungless MA, Whistler JL, Malenka RC, Bonci A. 2001. Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411:583-87
108. Cameron DL, Williams JT. 1993. Dopamine D1 receptors facilitate transmitter release. Nature 366:344-47
109. Saal D, Dong Y, Bonci A, Malenka RC. 2003. Drugs of abuse trigger a common synaptic adaptation in dopamine neurons. Neuron 37:577-82
110. Faleiro L, Kauer JA. 2003. An increase in AMPAR/NMDAR ratios in the ventral tegmental area (VTA) is detectable within two hours of amphetamine injection. Ann. NY Acad. Sci. In press
111. Brown SA, Vik PW, Patterson TL, Grant I, Schuckit MA. 1995. Stress, vulnerability and adult alcohol relapse. J. Stud. Alcohol 56:538-45
112. McFall ME, Mackay PW, Donovan DM. 1992. Combat-related posttraumatic stress disorder and severity of substance abuse in Vietnam veterans. J. Stud. Alcohol 53:357-63
113. Marinelli M, Piazza PV 2002. Interaction between glucocorticoid hormones, stress and psychostimulant drugs. Eur. J. Neurosci. 16:387-94
114. Kalivas PW, Duffy P. 1990. Effect of acute and daily cocaine treatment on extracellular dopamine in the nucleus accumbens. Synapse 5:48-58
115. Curzon G, Hutson PH, Knott PJ. 1979. Voltammetry in vivo: effect of stressful manipulation and drugs on the caudate nucleus of the rat. Br. J. Pharmacol. 66:127P-28
116. Shaham Y, Erb S, Stewart J. 2000. Stress-induced relapse to heroin and cocaine seeking in rats: a review. Brain Res. Rev. 33:13-33
117. Rivet JM, Stinus L, LeMoal M, Mormede P. 1989. Behavioral sensitization to amphetamine is dependent on corticosteroid receptor activation. Brain Res. 498:149-53
118. Piazza PV, Le Moal M. 1998. The role of stress in drug self-administration. Trends Pharmacol. Sci. 19:67-74
119. Chen YZ, Qiu J. 1999. Pleiotropic signaling pathways in rapid, nongenomic action of glucocorticoid. Mol. Cell Biol. Res. Commun. 2:145-49
120. 2+ elevation in cultured rat hippocampal neurons. J. Neurochem. 83:1441-51
121. Mercuri NB, Calabresi P, Bernardi G. 1989. The mechanism of amphetamine-induced inhibition of rat substantia nigra compacta neurones investigated with intracellular recording in vitro. Br. J. Pharmacol. 98:127-34
122. Brodie MS, Dunwiddie TV. 1990. Cocaine effects in the ventral tegmental area: evidence for an indirect dopaminergic mechanism of action. Naunyn Schmiedebergs Arch. Pharmacol. 342:660-65
123. Lacey MG, Mercuri NB, North RA. 1990. Actions of cocaine on rat dopaminergic neurones in vitro. Br. J. Pharmacol. 99:731-35
124. Seutin V, Verbanck P, Massotte L, Dresse A. 1991. Acute amphetamine-induced subsensitivity of A10 dopamine autoreceptors in vitro. Brain Res. 558:141-44
125. Xue C-J, Ng JP, Li Y, Wolf ME. 1996. Acute and repeated systemic amphetamine administration: effects on extracellular glutamate, aspartate, and serine levels in rat ventral tegmental area and nucleus accumbens. J. Neurochem. 67:352-63
126. Wolf ME, Xue C-J. 1998. Amphetamine and D1 dopamine receptor agonists produce biphasic effects on glutamate efflux in rat ventral tegmental area: modification by repeated amphetamine administration. J. Neurochem. 70:198-209
127. Deleted in proof
128. Flores C, Rodaros D, Stewart J. 1998. Long-lasting induction of astrocytic basic fibroblast growth factor by repeated injections of amphetamine: blockade by concurrent treatment with a glutamate antagonist. J. Neurosci. 18:9547-55
129. Flores C, Samaha AN, Stewart J. 2000. Requirement of endogenous basic fibroblast growth factor for sensitization to amphetamine. J. Neurosci. 20:RC55
130. Chadi G, Cao Y, Pettersson RF, Fuxe K. 1994. Temporal and spatial increase of astroglial basic fibroblast growth factor synthesis after 6-hydroxydopamine-induced degeneration of the nigrostriatal dopamine neurons. Neuroscience 61:891-910
131. Kawamata T, Dietrich W, Schallen T, Gotts J, Cocke R, et al. 1997. Intra cisternal basic fibroblast growth factor enhances functional recovery and up-regulates the expression of a molecular marker of neuronal sprouting following focal cerebral infarction. Proc. Natl. Acad. Sci. USA 94:8179-84
132. Malenka RC, Nicoll RA. 1993. NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci. 16:521-27
133. Heynen AJ, Abraham WC, Bear MF. 1996. Bidirectional modification of CA1 synapses in the adult hippocampus in vivo. Nature 381:163-66
134. Nicoll R, Oliet S, Malenka R. 1998. NMDA receptor-dependent and metabotropic glutamate receptor-dependent forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neurobiol. Learn. Mem. 70:62-67
135. Jones S, Kornblum JL, Kauer JA. 2000. Amphetamine blocks long-term synaptic depression in the ventral tegmental area. J. Neurosci. 20:5575-80
136. Thomas MT, Malenka RC, Bonci A. 2000. Modulation of long-term depression by dopamine in the mesolimbic system. J. Neurosci. 20:5581-86
137. Gutlerner JL, Chapin-Penick E, Snyder EM, Kauer JA. 2002. Novel protein kinase A-dependent long-term depression of excitatory synapses. Neuron 36:921-31
138. Deleted in proof
139. Thomas MT, Malenka RC, Bonci A. 2000. Modulation of long-term depression by dopamine in the mesolimbic system. J. Neurosci. 20:5581-86
140. Koob GF. 1992. Drugs of abuse: anatomy, pharmacology, and function of reward pathways. Trends Pharmacol. Sci. 13:177-84
141. Calabresi P, Lacey MG, North RA. 1989. Nicotinic excitation of rat ventral tegmental neurones in vitro studied by intracellular recording. Br. J. Pharmacol. 98:135-40
142. Pidoplichko VI, DeBiasi M, Williams JT, Dani JA. 1997. Nicotine activates and desensitizes midbrain dopamine neurons. Nature 390:401-4
143. Picciotto MR, Zoli M, Rimondini R, Lena C, Marubio LM, et al. 1998. Acetylcholine receptors containing the β2 subunit are involved in the reinforcing properties of nicotine. Nature 391:173-77
144. Mansvelder HD, McGehee DS. 2002. Cellular and synaptic mechanisms of nicotine addiction. J. Neurobiol. 53:606-17
145. Johnson SW, North RA. 1992. Opioids excite dopamine neurons by hyperpolarization of local interneurons. J. Neurosci. 12:483-88
146. Deleted in proof
147. Bonci A, Williams JT. 1996. A common mechanism mediates long-term changes in synaptic transmission after chronic cocaine and morphine. Neuron 16:631-39
148. Koob GF, Roberts AJ, Schulteis G, Parsons LH, Heyser CJ, et al. 1998. Neurocircuitry targets in ethanol reward and dependence. Alcohol Clin. Exp. Res. 22:3-9
149. McBride WJ, Murphy JM, Ikemoto S. 1999. Localization of brain reinforcement mechanism: intracranial self-administration and intracranial place-conditioning studies. Behav. Brain Res. 101:129-52
150. Bailey CP, Manley SJ, Watson WP, Wonnacott S, Molleman A, Little HJ. 1998. Chronic ethanol administration alters activity in ventral tegmental area neurons after cessation of withdrawal hyperexcitability. Brain Res. 803:144-52
151. Brodie MA, Shefner SA, Dunwiddie TV. 1990. Ethanol increases the firing rate of dopamine neurons of the rat ventral tegmental area in vitro. Brain Res. 508:65-69
152. Brodie MS, Pesold C, Appel SB. 1999. Ethanol directly excites dopaminergic ventral tegmental area reward neurons. Alcohol Clin. Exp. Res. 23:1848-52
153. Melis M, Camarini R, Ungless MA, Bonci A. 2002. Long-lasting potentiation of GABAergic synapses in dopamine neurons after a single in vivo ethanol exposure. J. Neurosci. 22:2074-82
154. Carlezon WA Jr, Nestler EJ. 2002. Elevated levels of GluR1 in the midbrain: a trigger for sensitization to drugs of abuse? Trends Neurosci. 25:610-15
155. Deleted in proof
156. Schultz W, Apicella P, Ljungberg T. 1993. Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J. Neurosci. 13:900-13
157. 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
158. Cooper DC. 2002. The significance of action potential bursting in the brain reward circuit. Neurochem. Int. 41:333-40
159. Deleted in proof
160. Kolta MG, Scalzo FM, Ali SF, Holson RR. 1990. Ontogeny of the enhanced behavioral response to amphetamine in amphetamine-pretreated rats. Psychopharmacology 100:377-82