Attenuation of cue-induced heroin-seeking behavior by cannabinoid CB 1 antagonist infusions into the nucleus accumbens core and prefrontal cortex, but not basolateral amygdala

Neuropsychopharmacology

Volumn 33, Issue 10, 2008, Pages 2483-2493

  Alvarez Jaimes, Lily ^a   Polis, Ilham ^a   Parsons, Loren H ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Addiction; Basolateral amygdala; CB1; Nucleus accumbens; Prefrontal cortex; Relapse

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 4 (1,1 DIMETHYLHEPTYL) 1',2',3',4',5',6' HEXAHYDRO 2,3' DIHYDROXY 6' (3 HYDROXYPROPYL)BIPHENYL; CANNABINOID 1 RECEPTOR; CANNABINOID 1 RECEPTOR ANTAGONIST; COCAINE; DEXANABINOL; DIAMORPHINE; NICOTINE; RIMONABANT;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; ATTENUATION; DOSE RESPONSE; DRUG EFFECT; HEROIN DEPENDENCE; INSTRUMENTAL CONDITIONING; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; REINFORCEMENT; RELAPSE;

AMYGDALA; ANIMALS; CONDITIONING, OPERANT; CUES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EXTINCTION, PSYCHOLOGICAL; HEROIN; HEROIN DEPENDENCE; MALE; MOTIVATION; NARCOTICS; NUCLEUS ACCUMBENS; PIPERIDINES; PREFRONTAL CORTEX; PYRAZOLES; RATS; RATS, WISTAR; RECEPTOR, CANNABINOID, CB1; REINFORCEMENT (PSYCHOLOGY); REWARD;

EID: 49549112724     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1301630     Document Type: Article

References (80)

1. Caillé S, Parsons LH (2006). Cannabinoid modulation of opiate reinforcement through the ventral striatopallidal pathway. Neuropsychopharmacology 31: 804-813.
2. Carelli RM (2000). Activation of accumbens cell firing by stimuli associated with cocaine delivery during self-administration. Synapse 35: 238-242.
3. Carter BL, Tiffany ST (1999). Meta-analysis of cue-reactivity in addiction research. Addiction 94: 327-340.
4. Childress AR, Mozley PD, McElgin W, Fitzgerald J, Reivich M, O'Brien CP (1999). Limbic activation during cue-induced cocaine craving. Am J Psychiatry 156: 11-18.
5. Ciccocioppo R, Angeletti S, Weiss F (2001a). Long-lasting resistance to extinction of response reinstatement induced by ethanol-related stimuli: role of genetic ethanol preference. Alcohol Clin Exp Res 25: 1414-1419.
6. Ciccocioppo R, Sanna PP, Weiss F (2001b). Cocaine-predictive stimulus induces drug-seeking behavior and neural activation in limbic brain regions after multiple months of abstinence: reversal by D(1) antagonists. Proc Natl Acad Sci USA 98: 1976-1981.
7. Collins DR, Pare D (1999). Reciprocal changes in the firing probability of lateral and central medial amygdala neurons. J Neurosci 19: 836-844.
8. Cornish JL, Kalivas PW (2000). Glutamate transmission in the nucleus accumbens mediates relapse in cocaine addiction. J Neurosci 20: RC89.
9. Daglish MR, Weinstein A, Malizia AL, Wilson S, Melichar JK, Britten S et al (2001). Changes in regional cerebral blood flow elicited by craving memories in abstinent opiate-dependent subjects. Am J Psychiatry 158: 1680-1686.
10. DeJong W (1994). Relapse prevention: an emerging technology for promoting long-term drug abstinence. Int J Addict 29: 681-705.
11. De Vries TJ, de Vries W, Janssen MCW, Schoffelmeer ANM (2005). Suppression of conditioned nicotine and sucrose seeking by the cannabinoid-1 receptor antagonist SR141716A. Behav Brain Res 161: 164-168.
12. De Vries TJ, Homberg JR, Binnekade R, Raaso H, Schoffelmeer AN (2003). Cannabinoid modulation of the reinforcing and motivational properties of heroin and heroin-associated cues in rats. Psychopharmacology (Berl) 168: 164-169.
13. De Vries TJ, Shaham Y, Homberg JR, Crombag H, Schuurman K, Dieben J et al (2001). A cannabinoid mechanism in relapse to cocaine seeking. Nat Medicine 7: 1151-1154.
14. Di Ciano P, Cardinal RN, Cowell RA, Little SJ, Everitt BJ (2001). Differential involvement of NMDA, AMPA/kainate, and dopamine receptors in the nucleus accumbens core in the acquisition and performance of pavlovian approach behavior. J Neurosci 21: 9471-9477.
15. Di Ciano P, Everitt BJ (2001). Dissociable effects of antagonism of NMDA and AMPA/KA receptors in the nucleus accumbens core and shell on cocaine seeking behavior. Neuropsychopharmacology 25: 341-360.
16. Di Ciano P, Everitt BJ (2004). Direct interactions between the basolateral amygdala and nucleus accumbens core underlie cocaine-seeking behavior by rats. J Neurosci 24: 7167-7173.
17. Egertová M, Elphick MR (2000). Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB. J Comp Neurol 422: 159-171.
18. Epstein DH, Preston KL, Stewart J, Shaham Y (2006). Toward a model of drug relapse: an assessment of the validity of the reinstatement procedure. Psychopharmacology (Berl) 189: 1-16.
19. Fattore L, Spano MS, Cossu G, Deiana S, Fratta W (2003). Cannabinoid mechanism in reinstatement of heroin-seeking after a long period of abstinence in rats. Eur J Neurosci 17: 1723-1726.
20. Fattore L, Vigano D, Fadda P, Rubino T, Fratta W, Parolaro D (2007). Bidirectional regulation of mu-opioid and CB1-cannabinoid receptor in rats self-administering heroin or WIN 55,212-2. Eur J Neurosci 25: 2191-2200.
21. Franklin TR, Druhan JP (2000). Involvement of the nucleus accumbens and medial prefrontal cortex in the expression of conditioned hyperactivity to a cocaine-associated environment in rats. Neuropsychopharmacology 23: 633-644.
22. Fuchs RA, Evans KA, Ledford CC, Parker MP, Case JM, Mehta RH, See RE (2005). The role of the dorsomedial prefrontal cortex, basolateral amygdala, and dorsal hippocampus in contextual reinstatement of cocaine seeking in rats. Neuropsychopharmacology 30: 296-309.
23. Fuchs RA, See RE (2002). Basolateral amygdala inactivation abolishes conditioned stimulus- and heroin-induced reinstatement of extinguished heroin-seeking behavior in rats. Psychopharmacology (Berl) 160: 425-433.
24. Ghitza UE, Fabbricatore AT, Prokopenko V, Pawlak AP, West MO (2003). Persistent cue-evoked activity of accumbens neurons after prolonged abstinence from self-administered cocaine. J Neurosci 23: 7239-7245.
25. Gioanni Y, Thierry AM, Glowinski J, Tassin JP (1998). Alpha1-adrenergic, D1, and D2 receptors interactions in the prefrontal cortex: implications for the modality of action of different types of neuroleptics. Synapse 30: 362-370.
26. Gracy KN, Dankiewicz LA, Weiss F, Koob GF (2000). Heroin-specific stimuli reinstate operant heroin-seeking behavior in rats after prolonged extinction. Pharm Biochem Behav 65: 489-494.
27. Grimm JW, See RE (2000). Dissociation of primary and secondary reward-relevant limbic nuclei in an animal model of relapse. Neuropsychopharmacology 22: 473-479.
28. Hayes RJ, Vorel SR, Spector J, Liu X, Gardner EL (2003). Electrical and chemical stimulation of the basolateral complex of the amygdala reinstates cocaine-seeking behavior in the rat. Psychopharmacology (Berl) 168: 75-83.
29. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC (1991). Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11: 563-583.
30. Hoffman AF, Lupica CR (2001). Direct actions of cannabinoids on synaptic transmission in the nucleus accumbens: a comparison with opioids. J Neurophysiol 85: 72-83.
31. Hollander JA, Carelli RM (2007). Cocaine-associated stimuli increase cocaine seeking and activate accumbens core neurons after abstinence. J Neurosci 27: 3535-3539.
32. Hutcheson DM, Parkinson JA, Robbins TW, Everitt BJ (2001). The effects of nucleus accumbens core and shell lesions on intravenous heroin self administration and the acquisition of drug-seeking behaviour under a second-order schedule of heroin reinforcement. Psychopharmacology (Berl) 153: 464-472.
33. Jaffe JH, Cascella NG, Kumor KM, Sherer MA (1989). Cocaine-induced cocaine craving. Psychopharmacology (Berl) 97: 59-64.
34. Kalivas PW, Volkow ND (2005). The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry 162: 1403-1413.
35. Katona I, Rancz EA, Acsády L, Ledent C, Mackie K, Hájos N et al (2001). Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci 21: 9506-9518.
36. Katona I, Sperlágh B, Sík A, Käfalvi A, Vizi ES, Mackie K et al (1999). Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19: 4544-4558.
37. Kilts CD, Schweitzer JB, Quinn CK, Gross RE, Faber TL, Muhammad F et al (2001). Neural activity related to drug craving in cocaine addiction. Arch Gen Psychiatry 58: 334-341.
38. Kodas E, Cohen C, Louis C, Griebel G (2007). Cortico-limbic circuitry for conditioned nicotine-seeking behavior in rats involves endocannabinoid signaling. Psychopharmacology (Berl) 194: 161-171.
39. Koya E, Spijker S, Voorn P, Binnekade R, Schmidt ED, Schoffelmeer ANM et al (2006). Enhanced cortical and accumbal molecular reactivity associated with conditioned heroin, but not sucrose-seeking behaviour. J Neurochem 98: 905-915.
40. Kreek MJ, Koob GF (1998). Drug dependence: stress and dysregulation of brain reward pathways. Drug Alcohol Depend 51: 23-47.
41. Laviolette SR, Grace AA (2006). Cannabinoids potentiate emotional learning plasticity in neurons of the medial prefrontal cortex through basolateral amygdala inputs. J Neurosci 26: 6458-6468.
42. Laviolette SR, Lipski WJ, Grace AA (2005). A subpopulation of neurons in the medial prefrontal cortex encodes emotional learning with burst and frequency codes through a dopamine D4 receptor-dependent basolateral amygdala input. J Neurosci 25: 6066-6075.
43. Ledford CC, Fuchs RA, See RE (2003). Potentiated reinstatement of cocaine-seeking behavior following D-amphetamine infusion into the basolateral amygdala. Neuropsychopharmacology 28: 1721-1729.
44. Lee JL, Everitt BJ, Thomas KL (2004). Independent cellular processes for hippocampal memory consolidation and reconsolidation. Science 304: 839-843.
45. Leshner AI (1997). Addiction is a brain disease, and it matters. Science 278: 5335-5345.
46. Mailleux P, Vanderhaeghen JJ (1992). Localization of cannabinoid receptor in the human developing and adult basal ganglia. Higher levels in the striatonigral neurons. Neurosci Lett 148: 173-176.
47. Manzoni OJ, Bockaert J (2001). Cannabinoids inhibit GABAergic synaptic transmission in mice nucleus accumbens. Eur J Pharmacol 412: R3-R5.
48. Matsuda LA, Bonner TI, Lolait SJ (1993). Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 327: 535-550.
49. McDonald AJ, Mascagni F (2001). Localization of the CB1 type cannabinoid receptor in the rat basolateral amygdala: high concentrations in a subpopulation of cholecystokinin-containing interneurons. Neuroscience 107: 641-652.
50. McFarland K, Davidge SB, Lapish CC, Kalivas P (2004). Limbic and motor circuitry underlying footshock-induced reinstatement of cocaine-seeking behavior. J Neurosci 24: 1551-1560.
51. McFarland K, Lapish CC, Kalivas P (2003). Prefrontal glutamate release into the core of the nucleus accumbens mediates cocaine-induced reinstatement of drug-seeking behavior. J Neurosci 23: 3531-3537.
52. McLaughlin J, See RE (2003). Selective inactivation of the dorsomedial prefrontal cortex and the basolateral amygdala attenuates conditioned-cued reinstatement of extinguished cocaine-seeking behavior in rats. Psychopharmacology 168: 57-65.
53. McLellan AT, Lewis DC, O'Brien CP, Kleber HD (2000). Drug dependence, a chronic medical illness: implications for treatment, insurance, and outcomes evaluation. JAMA 284: 1689-1695.
54. Meil WM, See RE (1997). Lesions of the basolateral amygdala abolish the ability of drug associated cues to reinstate responding during withdrawal from self-administered cocaine. Behav Brain Res 87: 139-148.
55. Nicola SM, Yun IA, Wakabayashi KT, Fields HL (2004). Cue-evoked firing of nucleus accumbens neurons encodes motivational significance during a discriminative stimulus task. J Neurophysiol 91: 1840-1865.
56. O'Brien CP, Childress AR, McLellan AT, Ehrman R (1992). Classical conditioning in drug-dependent humans. Ann NY Acad Sci 654: 400-415.
57. Parkinson JA, Olmstead MC, Burns LH, Robbins TW, Everitt BJ (1999). Dissociation in effects of lesions of the nucleus accumbens core and shell on appetitive pavlovian approach behavior and the potentiation of conditioned reinforcement and locomotor activity by D-amphetamine. J Neurosci 19: 2401-2411.
58. Paxinos G, Watson C (1998). The Rat Brain in Stereotaxic Coordinates. Academic Press: San Diego.
59. Pirot S, Godbout R, Mantz J, Tassin JP, Glowinski J, Thierry AM (1992). Inhibitory effects of ventral tegmental area stimulation on the activity of prefrontal cortical neurons: evidence for the involvement of both dopaminergic and GABAergic components. Neuroscience 49: 857-865.
60. Pistis M, Porcu G, Melis M, Diana M, Gessa GL (2001). Effects of cannabinoids on prefrontal neuronal responses to ventral tegmental area stimulation. Eur J Neurosci 14: 96-102.
61. See RE (2005). Neural substrates of cocaine-cue associations that trigger relapse. Eur J Pharmacol 526: 140-146.
62. See RE, Kruzich PJ, Grimm JW (2001). Dopamine, but not glutamate, receptor blockade in the basolateral amygdala attenuates conditioned reward in a rat model of relapse to cocaine-seeking behavior. Psychopharmacology (Berl) 154: 301-310.
63. Serra S, Brunetti G, Pani M, Vacca G, Carai MAM, Gessa GL et al (2002). Blockade by the cannabinoid CB(1) receptor antagonist, SR 141716, of alcohol deprivation effect in alcohol-preferring rats. Eur J Pharmacol 443: 95-97.
64. Sesack SR, Bressler CN, Lewis DA (1995a). Ultrastructural associations between dopamine terminals and local circuit neurons in the monkey prefrontal cortex: a study of calretinin-immunoreactive cells. Neurosci Lett 200: 9-12.
65. Sesack SR, Bunney BS (1989). Pharmacological characterization of the receptor mediating electrophysiological responses to dopamine in the rat medial prefrontal cortex: a microiontophoretic study. J Pharmacol Exp Ther 248: 1323-1333.
66. Sesack SR, Snyder CL, Lewis DA (1995b). Axon terminals immunolabeled for dopamine or tyrosine hydroxylase synapse on GABA-immunoreactive dendrites in rat and monkey cortex. J Comp Neurol 363: 264-280.
67. 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.
68. Shalev U, Grimm JW, Shaham Y (2002). Neurobiology of relapse to heroin and cocaine seeking: a review. Pharmacol Rev 54: 1-42.
69. Sinha R, Catapano D, O'Malley S (1999). Stress-induced craving and stress response in cocaine dependent individuals. Psychopharmacology 142: 343-351.
70. Stewart J (2000). Pathways to relapse: the neurobiology of drug-and stress-induced relapse to drug taking. J Psychiatry Neurosci 25: 125-136.
71. Tims FM, Leukefeld CG (1986). Relapse and recovery in drug abuse. NIDA Research Monograph 72: 1-195.
72. Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM (1998). Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83: 393-411.
73. Tzavara ET, Davis RJ, Perry KW, Li X, Salhoff C, Bymaster FP et al (2003). The CB1 receptor antagonist SR141716A selectively increases monoaminergic neurotransmission in the medial prefrontal cortex: implications for therapeutic actions. Br J Pharmacol 138: 544-553.
74. Weiss F (2005). Neurobiology of craving, conditioned reward and relapse. Curr Opin Pharmacol 5: 9-19.
75. Weiss F, Maldonado-Vlaar CS, Parsons LH, Kerr TM, Smith DL, Ben-Shahar O (2000). Control of cocaine-seeking behavior by drug-associated stimuli in rats: effects on recovery of extinguished operant-responding and extracellular dopamine levels in amygdala and nucleus accumbens. Proc Natl Acad Sci USA 97: 4321-4326.
76. Xi ZX, Gilbert JG, Peng XQ, Pak AC, Li X, Gardner EL (2006). Cannabinoid CB1 receptor antagonist AM251 inhibits cocaine-primed relapse in rats: role of glutamate in the nucleus accumbens. J Neurosci 26: 8531-8536.
77. Yao L, McFarland K, Fan P, Jiang Z, Inoue Y, Diamond I (2005). Activator of G protein signaling 3 regulates opiate activation of protein kinase A signaling and relapse of heroin-seeking behavior. Proc Natl Acad Sci USA 102: 8746-8751.
78. Yun IA, Fields HL (2003). Basolateral amygdala lesions impair both cue- and cocaine-induced reinstatement in animals trained on a discriminative stimulus task. Neuroscience 121: 747-757.
79. Yun IA, Nicola SM, Fields HL (2004). Contrasting effects of dopamine and glutamate receptor antagonist injection in the nucleus accumbens suggest a neural mechanism underlying cue-evoked goal-directed behavior. Eur J Neurosci 20: 249-263.
80. Zavala AR, Biswas S, Harlan RE, Neisewander JL (2007). Fos and glutamate AMPA receptor subunit co-expression associated with cue-elicited cocaine-seeking behavior in abstinent rats. Neuroscience 145: 438-452.