Neural substrates of drug craving and relapse in drug addiction

Annals of Medicine

Volumn 30, Issue 4, 1998, Pages 379-389

  Self, David W ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Addiction; Cocaine; Craving; Dopamine; Nucleus accumbens; Reinstatement

Indexed keywords

CYCLIC AMP; DOPAMINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR;

ABSTINENCE; ADAPTATION; AMYGDALOID NUCLEUS; ASSOCIATION; DRUG DEPENDENCE; DRUG USE; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MESOLIMBIC DOPAMINERGIC SYSTEM; MOTIVATION; NERVE CELL; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RELAPSE; REVIEW; REWARD; SATIETY; SECOND MESSENGER; STRESS; WITHDRAWAL SYNDROME;

EID: 0031720297     PISSN: 07853890     EISSN: None     Source Type: Journal    
DOI: 10.3109/07853899809029938     Document Type: Review

References (93)

1. DSM-IV: Diagnostic and Statistical Manual of Mental Disorders, 3rd edn rev. Washington, DC: American Psychiatric Association; 1994.
2. Wise RA. The brain and reward. In: Liebman JM, Cooper SJ, eds. The Neuropharmacological Basis of Reward. New York: Oxford University Press; 1989: 377-424.
3. Koob GF, Le Moal M. Drug abuse: hedonic homeostatic dysregulation. Science 1997; 278: 52-8.
4. Di Chiara G, North RA. Neurobiology of opiate abuse. Trends Pharmacol Sci 1992; 13: 185-92.
5. Self DW, Nestler EJ. Molecular mechanisms of drug reinforcement and addiction. Annu Rev Neurosci 1995; 18: 463-95.
6. Robinson TE, Berridge KC. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 1993; 18: 247-91.
7. Stewart J, De Wit H, Eikelboom R. Role of unconditioned and conditioned drug effects in the self-administration of opiates and stimulants. Psychol Rev 1984; 91: 251-68.
8. Wise RA, Bozarth MA. A psychomotor stimulant theory of addiction. Psychol Rev 1987; 94: 469-92.
9. Solomon R, Corbitt J. An opponent process theory of motivation. Psychol Rev 1974; 81: 119-45.
10. Nestler EJ, Aghajanian GK. Molecular and cellular basis of addiction. Science 1997; 278: 58-63.
11. Wise RA. The role of reward pathways in the development of drug dependence. In: Balfour DJK, ed. Psychotropic Drugs of Abuse. Oxford: Pergamon Press; 1990: 23-57.
12. Kuhar MJ, Ritz MC, Boja JW. The dopamine hypothesis of the reinforcing properties of cocaine. Trends Neurosci 1991; 14: 299-302.
13. Koob GF. Drugs of abuse: anatomy, pharmacology and function of reward pathways. Trends Pharmacol Sci 1992; 13: 177-84.
14. Fibiger HC, Phillips AG, Brown EE. The neurobiology of cocaine-induced reinforcement. Ciba Found Symp 1992; 166: 96-124.
15. Dworkin SI, Goeders NE, Smith JE. The reinforcing and rate effects of intracranial dopamine administration. In: Harris LS, ed. NIDA Research Monogr Vol 67. Bethesda, MD: National Institute on Drug Abuse; 1986: 242-8.
16. Hoebel BG, Monaco AP, Hernandez L, Aulisi EF, Stanley BG, Lenard L. Self-injection of amphetamine directly into the brain. Psychopharmacology 1983; 81: 158-63.
17. Carlezon WAJ, Devine DP, Wise RA. Habit-forming actions of nomifensine in nucleus accumbens. Psychopharmacology 1995; 122: 194-7.
18. Bozarth MA, Wise RA. Intracranial self-administration of morphine into the ventral tegmental area. Life Sci 1981; 28: 551-5.
19. Johnson SW, North RA. Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 1992; 12: 483-8.
20. Leone P, Pocock D, Wise RA. Morphine-dopamine interaction: ventral tegmental morphine increases nucleus accumbens dopamine release. Pharmacol Biochem Behav 1991; 39: 469-72.
21. Imperato A, Di Chiara G. Preferential stimulation of dopamine release in the nucleus accumbens of freely moving rats by ethanol. J Pharmacol Exp Ther 1986; 239: 219-28.
22. 9-tetrahydrocannabinal produces naloxone blockable enhancement of presynaptic dopamine eflux in nucleus accumbens of conscious, freely-moving rats as measured by intracerebral microdialysis. Psychopharmacology 1990; 102: 156-62.
23. Tanda G, Pontieri FE, Di Chiara G. Cannabinoid and heroin activation of mesolimbic dopamine transmission by a common mu1 opioid receptor mechanism. Science 1997; 276: 2048-50.
24. Bozarth MA, Wise RA. Involvement of the ventral tegmental dopamine system in opioid and psychomotor stimulant reinforcement. In: Harris LS, ed. NIDA Research Monogr Vol 67. Bethesda, MD: National Institute on Drug Abuse; 1986: 190-6.
25. Di Chiara G, Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci U S A 1988; 85: 5274-8.
26. Bardo MT. Neuropharmacological mechanisms of drug reward: beyond dopamine in the nucleus accumbens. Crit Rev Neurobiol 1998; 12: 37-67.
27. Ettenberg A, Pettit HO, Bloom FE, Koob GF. Heroin and cocaine intravenous self-administration in rats: mediation by separate neural systems. Psychopharmacology 1982; 78: 204-9.
28. Dworkin SI, Guerin GF, Co C, Goeders NE, Smith JE. Lack of an effect of 6-hydroxydopamine lesions of the nucleus accumbens on intravenous morphine self-administration. Pharmacol Biochem Behav 1988; 30: 1051-7.
29. Pettit HO, Ettenberg A, Bloom FE, Koob GF. Destruction of dopamine in the nucleus accumbens selectively attenuates cocaine but not heroin self-administration in rats. Psychopharmacology 1984; 84: 167-73.
30. Goeders NE, Lane JD, Smith JE. Self-administration of methionine enkephalin into the nucleus accumbens. Pharmacol Biochem Behav 1984; 20: 451-5.
31. Olds ME. Reinforcing effects of morphine in the nucleus accumbens. Brain Res 1982; 237: 429-40.
32. Zito KA, Vickers G, Roberts DCS. Disruption of cocaine and heroin self-administration following kainic acid lesions of the nucleus accumbens. Pharmacol Biochem Behav 1985; 23: 1029-36.
33. Self DW, Nestler EJ. Relapse to drug seeking: neural and molecular mechanisms. Drug Alcohol Depend (in press).
34. Tiffany ST, Singleton E, Haertzen CA, Henningfiled JE. The development of a cocaine craving questionnaire. Drug Alcohol Depend 1993; 34: 19-28.
35. De Wit H, Stewart J. Reinstatement of cocaine-reinforced responding in the rat. Psychopharmacology 1981; 75: 134-43.
36. Slikker WJ, Brocco MJ, Killam KFJ. Reinstatement of responding maintained by cocaine or thiamylal. J Pharmacol Exp Ther 1984; 228: 43-52.
37. De Wit H, Stewart J. Drug reinstatement of heroin-reinforced responding in the rat. Psychopharmacology 1983; 79: 29-31.
38. Stewart J, Vezina P. A comparison of the effects of intra-accumbens injections of amphetamine and morphine on reinstatement of heroin intravenous self-administration behavior. Brain Res 1988; 457: 287-94.
39. Wise RA, Murray A, Bozarth MA. Bromocriptine self-administration and bromocriptine-reinstatement of cocaine-trained and heroin-trained lever pressing in rats. Psychopharmacology 1990; 100: 355-60.
40. 2-like dopamine receptor agonists. Science 1996; 271: 1586-9.
41. Ettenberg A. Haloperidol prevents the reinstatement of amphetamine-rewarded runway responding inrats. Pharmacol Biochem Behav 1990; 36: 635-8.
42. Shaham Y, Stewart J. Effects of opioid and dopamine receptor antagonists on relapse induced by stress and reexposure to heroin in rats. Psychopharmacology 1996; 125: 385-91.
43. Weissenborn R, Deroche V, Koob G, Weiss F. Effects of dopamine agonists and antagonists on cocaine-induced operant responding for a cocaine-associated stimulus. Psychopharmacology 1996; 126: 311-22.
44. Ehrman RN, Robbins SJ, Childress AR, O'Brien CP. Conditioned responses to cocaine-related stimuli in cocaine abuse patients. Psychopharmacology 1992; 107: 523-9.
45. O'Brien C, Childress A, McLellan A, Ehrman R. A learning model of addiction. In: O'Brien CP, Jaffe JH, eds. Addictive States. New York: Raven Press; 1992: 157-77.
46. Wise RA. Cocaine reward and cocaine craving: the role of dopamine in perspective. In: Harris LS, ed. NIDA Research Monogr Vol 145. Bethesda, MD: National Institute on Drug Abuse; 1994: 191-206.
47. Brown EE, Fibiger HC. Cocaine-induced conditioned locomotion: absence of associated increases in dopamine release. Neuroscience 1992; 48: 621-9.
48. Fontana DJ, Post RM, Pert A. Conditioned increases in mesolimbic dopamine overflow by stimuli associated with cocaine. Brain Res 1993; 629: 31-9.
49. Di Ciano P, Blaha CD, Phillips AG. Conditioned increases in motor activity and dopamine concentrations in the nucleus accumbens of the rat following repeated administration of cocaine or d-amphetamine. Soc Neurosci Abstr 1995; 21: 2103.
50. Schultz W, Apicella P, Ljungberg T. Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J Neurosci 1993; 13: 900-13.
51. Mirenowicz J, Schultz W. Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 1996; 379: 449-51.
52. Meil WM, See RE. Lesions of the basolateral amygdala abolish the ability of drug associated cues to reinstate responding during withdrawal from self-administered cocaine. Behav Brain Res 1997; 87: 139-48.
53. Maeda H, Mogenson GJ. Electrophysiological responses of neurons in the ventral tegmental area to electrical stimulation of amygdala and lateral septum. Neuroscience 1981; 6: 367-76.
54. Gonzales C, Chesselet MF. Amydalonigral pathway: an anterograde study in the rat with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 1990; 297: 182-200.
55. Wallace DM, Magnuson DJ, Gray TS. Organization of amygdaloid projections to brainstem dopaminergic, noradrenergic, and adrenergic cell groups in the rat. Brain Res Bull 1992; 28: 447-54.
56. McDonald AJ. Organisation of amygdaloid projections to prefrontal cortex and associated striatum in the rat. Neuroscience 1991; 44: 1-14.
57. Shaham Y, Stewart J. Stress reinstates heroin-seeking in drug-free animals: an effect mimicking heroin, not withdrawal. Psychopharmacology 1995; 119: 334-41.
58. Erb S, Shaham Y, Stewart J. Stress reinstates cocaine-seeking behavior after prolonged extinction and a drug-free period. Psychopharmacology 1996; 128: 408-12.
59. Ahmed SH, Koob GF. Cocaine- but not food-seeking behavior is reinstated by stress after prolonged extinction. Psychopharmacology 1997; 132: 289-95.
60. Shaham Y, Rajabi H, Stewart J. Relapse to heroin-seeking in rats under opioid maintenance: the effects of stress, heroin priming, and withdrawal. J Neurosci 1996; 16: 1957-63.
61. Moghaddam B. Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia. J Neurochem 1993; 60: 1650-7.
62. Taber MT, Das S, Fibiger HC. Cortical regulation of subcortical dopamine release: mediation via the ventral tegmental area. J Neurochem 1995; 65: 1407-10.
63. Karreman M, Moghaddam B. The prefrontal cortex regulates the basal release of dopamine in the limbic striatum: an effect mediated by ventral tegmental area. J Neurochem 1996; 66: 589-98.
64. Shaham Y, Funk D, Erb S, Brown TJ, Walker C-D, Stewart J. Corticotropin-releasing factor in stress-induced relapse to heroin-seeking in rats. J Neurosci 1997; 17: 2605-14.
65. Overton PG, Tong ZY, Brain PF, Clark D. Preferential occupation of mineralcorticoid receptors by corticosterone enhances glutamate-induced burst firing in rat midbrain dopaminergic neurons. Brain Res 1996; 737: 146-54.
66. Piazza PV, Rouge-Pont F, Deroche V, Maccari S, Simon H, Le Moal M. Glucocorticoids have state-dependent stimulant effects on the mesencephalic dopamine transmission. Proc Natl Acad Sci U S A 1996; 93: 8716-20.
67. Deroche V, Marinelli M, Le Moal M, Piazza PV. Glucocorticoids and behavioral effects of psychostimulants. II: Cocaine intravenous self-administration and reinstatement depend on glucocorticoid levels. J Pharmacol Exp Ther 1997; 281: 1401-07.
68. Stewart J, Wise RA. Reinstatement of heroin self-administration habits: morphine prompts and naltrexone discourages renewed responding after extinction. Psychopharmacology 1992; 108: 79-84.
69. Shippenberg TS, Herz A. Place preference reveals the involvement of D-1 dopamine receptors in the motivational properties of μ- and κ-opioid agonists. Brain Res 1987; 436: 169-72.
70. Childress AR, McLellan AT, O'Brien CP. Extinguishing conditioned responses in drug dependent persons. In: Ray B, ed. Learning Factors and Drug Dependence: NIDA Research Monogr Vol 81. Bethesda, MD: National Institute on Drug Abuse; 1988: 137-44.
71. Robbins SJ, Ehrman RN, Childress AR, O'Brien CP. Relationships among physiological and self-report responses produced by cocaine-related cues. Addict Behav 1997; 22: 157-67.
72. Sibley DR, Monsma FJ Jr, Shen Y. Molecular neurobiology of dopaminergic receptors. Int Rev Neurobiol 1993; 35: 391-415.
73. Meador-Woodruff JH, Mansour A, Healy DJ, et al. Comparison of the distribution of D1 and D2 dopamine receptor mRNAs in rat brain. Neuropsychopharmacology 1991; 5: 231-42.
74. Curran EJ, Watson SJ. Dopamine receptor mRNA expression patterns by opioid peptide cells in the nucleus accumbens of the rat: a double in situ hybridization study. J Comp Neurol 1995; 361: 57-76.
75. 1 agonists SKF 82958 and SKF 77434 are self-administered by rats. Brain Res 1992; 582: 349-52.
76. Caine SB, Koob GF. Modulation of cocaine self-administration in the rat through D-3 dopamine receptors. Science 1993; 260: 1814-6.
77. 2 mediation of the discriminative stimulus properties of d-amphetamine and cocaine. Psychopharmacology 1991; 103: 50-5.
78. Spealman RD, Bergman J, Madras BK, Melia KF. Discriminitive stimulus effects of cocaine in squirrel monkeys: involvement of dopamine receptor subtypes. J Pharmacol Exp Ther 1991; 258: 945-53.
79. Witkin JM, Nichols DE, Terry P, Katz J. Behavioral effects of selective dopaminergic compounds in rats discriminating cocaine injections. J Pharmacol Exp Ther 1991; 257: 706-13.
80. Leshner AI. Molecular mechanisms of cocaine addiction. N Engl Med 1996; 355: 128-9.
81. Johanson C-E, Schuster CR. Cocaine. In: Bloom FE, Kupfer DJ, eds. Psychopharmacology: The Fourth Generation of Progress. New York: Raven Press; 1995: 1675-97.
82. Jaffe JH, Cascella NG, Kumor KM, Sherer MA. Cocaine-induced cocaine craving. Psychopharmacology 1989; 97: 59-64.
83. Preston KL, Sullivan JT, Strain EC, Bigelow GE. Effects of cocaine alone and in combination with bromocriptine in human cocaine abusers. J Pharmacol Exp Ther 1992; 262: 279-91.
84. Gavin FH. Cocaine addiction: psychology and neurophysiology. Science 1991; 251: 1580-6.
85. Belmaker RH, Wald D. Haloperidol in normals. Br J Psychiatry 1977; 131: 222-3.
86. Worley CM, Valadez A, Schenk S. Reinstatement of extinguished cocaine-taking behavior by cocaine and caffeine. Pharmacol Biochem Behav 1994; 48: 217-21.
87. Ferre S, Fuxe K, Von Euler G, Johansson B, Fredholm BB. Adenosine-dopamine interactions in the brain. Neuroscience 1992; 51: 501-12. V
88. Ferre S, Fredholm BB, Morelli M, Popoli P, Fuxe K. Adenosine-dopamine receptor-receptor interactions as an integrative mechanism in the basal ganglia. Trends Neurosci 1997; 20: 482-7.
89. Nestler EJ, Greengard P. Protein phosphorylation and the regulation of neuronal function. In: Siegel GJ, Agranoff BW, Albers RW, eds. Basic Neurochemistry: Molecular, Cellular and Medical Aspects, 5th edn. New York: Raven Press; 1994: 449-74.
90. Self DW, Genova LM, Hope BT, Barnhart WJ, Spencer JJ, Nestler EJ. Involvement of cAMP-dependent protein kinase in the nucleus accumbens in cocaine self-administration and relapse of cocaine-seeking behavior. J Neurosci 1998; 18: 1848-59.
91. o proteins in nucleus accumbens reduces both cocaine and heroin reinforcement. J Neurosci 1994; 14: 6239-47.
92. Sibley DR, Ventura AL, Jiang D, Mak C. Regulation of the D1 dopamine receptor through cAMP-mediated pathways. Adv Pharmacol 1998; 42: 447-50.
93. 2 dopamine receptor-mediated inhibition of forskolin-stimulated adenylate cyclase activity in rat. Neurosci Lett 1985; 59: 177-82.