Cannabinoid modulation of opiate reinforcement through the ventral striatopallidal pathway

Neuropsychopharmacology

Volumn 31, Issue 4, 2006, Pages 804-813

  Caillé, Stéphanie ^a   Parsons, Loren H ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

CB1; GABA microdialysis; Heroin self administration; Morphine; Rat; Receptors; SR 141716A

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 4 AMINOBUTYRIC ACID; CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR AGONIST; CANNABINOID RECEPTOR ANTAGONIST; DIAMORPHINE; DOPAMINE; MORPHINE; NALOXONE; OPIATE; RIMONABANT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE BRAIN LEVEL; DOSE RESPONSE; DRUG EFFECT; DRUG MECHANISM; DRUG SELF ADMINISTRATION; GLOBUS PALLIDUS; INFUSION; MALE; NEUROCHEMISTRY; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RAT; REINFORCEMENT;

ANALGESICS, OPIOID; ANIMALS; AREA UNDER CURVE; BEHAVIOR, ANIMAL; CANNABINOIDS; COCAINE; CONDITIONING, OPERANT; CORPUS STRIATUM; DOPAMINE; DRUG ADMINISTRATION ROUTES; DRUG INTERACTIONS; GAMMA-AMINOBUTYRIC ACID; MALE; MICRODIALYSIS; MORPHINE; NEURAL PATHWAYS; PIPERIDINES; PYRAZOLES; RATS; RATS, WISTAR; REINFORCEMENT (PSYCHOLOGY); SELF ADMINISTRATION; TIME FACTORS;

EID: 33645034385     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1300848     Document Type: Article

References (72)

1. Bardo MT (1998). Neuropharmacological mechanisms of drug reward: beyond dopamine in the nucleus accumbens. Crit Rev Neurobiol 12: 37-67.
2. Bourdelais A, Kalivas PW (1990). Amphetamine lowers extracellular GABA concentration in the ventral pallidum. Brain Res 516: 132-136.
3. Bourdelais A, Kalivas PW (1992). Apomorphine decreases extracellular GABA in the ventral pallidum of rats with 6-OHDA lesions in the nucleus accumbens. Brain Res 577: 306-311.
4. Caillé S, Parsons LH (2003). SR141716A reduces the reinforcing properties of heroin but not heroin-induced increases in the nucleus accumbens in rats. Eur J Neurosci 18: 3145-3149.
5. Caillé S, Parsons LH (2004). Intravenous heroin self-administration decreases GABA efflux in the ventral pallidum: an in vivo microdialysis study in rats. Eur J Neurosci 20: 593-596.
6. Caine SB, Lintz R, Koob GF (1993). Intravenous drug self-administration techniques in animals. In: Sahgal, A (ed). Behavioural Neuroscience: A Practical Approach. Oxford University Press, New York. pp 117-143.
7. Chang HT, Kitai ST (1985). Projection neurons of the nucleus accumbens: an intracellular labeling study. Brain Res 347: 112-116.
8. Childers SR, Fleming L, Konkoy C, Marckel D, Pacheco M, Sexton T et al (1992). Opioid and cannabinoid receptor inhibition of adenylyl cyclase in brain. Ann N Y Acad Sci 654: 33-51.
9. Corchero J, Manzanares J, Fuentes JA (2004). Cannabinoid/opioid crosstalk in the central nervous system. Crit Rev Neurobiol 16: 159-172.
10. Cossu G, Ledent C, Fattore L, Imperato A, Bohme GA, Parmentier M et al (2001). Cannabinoid CB1 receptor knockout mice fail to self-administer morphine but not other drugs of abuse. Behav Brain Res 118: 61-65.
11. David V, Durkin TP, Cazala P (2002). Differential effects of the dopamine D2/D3 receptor antagonist sulpiride on self-administration of morphine into the ventral tegmental area or the nucleus accumbens. Psychopharmacology (Berlin) 160: 307-317.
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 (Berlin) 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 Med 7: 1151-1154.
14. Fattore L, Cossu G, Spano MS, Delana S, Fadda P, Scherma M et al (2004). Cannabinoids and reward: interactions with the opioid system. Crit Rev Neurobiol 16: 147-158.
15. Fattore L, Martellotta MC, Cossu G, Mascia MS, Fratta W (1999). CB1 cannabinoid receptor agonist WIN 55,212-2 decreases intravenous cocaine self-administration in rats. Behav Brain Res 104: 141-146.
16. 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.
17. Frantz KJ, Hansson KJ, Stouffer DG, Parsons LH (2002). 5-HT(6) receptor antagonism potentiates the behavioral and neurochemical effects of amphetamine but not cocaine. Neuropharmacology 42: 170-180.
18. French ED, Dillon K, Wu X (1997). Cannabinoids excite dopamine neurons in the ventral tegmentum and substantia nigra. Neuroreport 8: 649-652.
19. Gerrits MA, Van Ree JM (1996). Effect of nucleus accumbens dopamine depletion on motivational aspects involved in initiation of cocaine and heroin self-administration in rats. Brain Res 713: 114-124.
20. Gessa GL, Casu MA, Carta G, Mascia MS (1998b). Cannabinoids decrease acetylcholine release in the medial-prefrontal cortex and hippocampus, reversal by SR 141716A. Eur J Pharmacol 355: 119-124.
21. Gessa GL, Melis M, Muntoni AL, Diana M (1998a). Cannabinoids activate mesolimbic dopamine neurons by an action on cannabinoid CB1 receptors. Eur J Pharmacol 341: 39-44.
22. Gong W, Neill D, Justice Jr JB (1996). Conditioned place preference and locomotor activation produced by injection of psychostimulants into ventral pallidum. Brain Res 707: 64-74.
23. Groenewegen HJ, Russchen FT (1984). Organization of the efferent projections of the nucleus accumbens to pallidal, hypothalamic, and mesencephalic structures: a tracing and immunohistochemical study in the cat. J Comp Neurol 223: 347-367.
24. Groenewegen HJ, Wright CI, Beijer AV, Voor P (1999). Convergence and segregation of ventral striatal inputs and outputs. Ann NY Acad Sci. 877: 49-63.
25. Hakan RL, Henriksen SJ (1989). Opiate influences on nucleus accumbens neuronal electrophysiology: dopamine and non-dopamine mechanisms. J Neurosci 9: 3538-3546.
26. Hajos N, Katona I, Naiem SS, MacKie K, Ledent C, Mody I et al (2000). Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci 12: 3239-3249.
27. Hemby SE, Martin TJ, Co C, Dworkin SI, Smith JE (1995). The effects of intravenous heroin administration on extracellular nucleus accumbens dopamine concentrations as determined by in vivo microdialysis. J Pharmacol Exp Ther 273: 591-598.
28. 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.
29. 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.
30. Johnson PI, Stellar JR (1994). Comparison of delta opiate receptor agonist induced reward and motor effects between the ventral pallidum and dorsal striatum. Neuropharmacology 33: 1171-1182.
31. Johnson PI, Stellar JR, Paul DA (1993). Regional reward differences within the ventral pallidum are revealed by microinjections of a mu opiate receptor agonist. Neuropharmacology 32: 1305-1314.
32. Johnson SW, North RA (1992). Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12: 483-488.
33. Ledent C, Valverde O, Cossu G, Petitet F, Aubert JF, Beslot F et al (1999). Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 283: 401-404.
34. Lee RS, Criado JR, Koob GF, Henriksen SJ (1999). Cellular responses of nucleus accumbens neurons to opiate-seeking behavior: I. Sustained responding during heroin self-administration. Synapse 33: 49-58.
35. Manzoni OJ, Bockaert J (2001). Cannabinoids inhibit GABAergic synaptic transmission in mice nucleus accumbens. Eur J Pharmacol 412: R3-R5.
36. Martin M, Ledent C, Parmentier M, Maldonado R, Valverde O (2000). Cocaine, but not morphine, induces conditioned place preference and sensitization to locomotor responses in CB1 knockout mice. Eur J Neurosci 12: 4038-4046.
37. Mas-Nieto M, Pommier B, Tzavara ET, Caneparo A, Da Nascimento S, Le Fur G et al (2001). Reduction of opioid dependence by the CB1 antagonist SR141716A in mice: evaluation of the interest in pharmacotherapy of opioid addiction. Br J Pharmacol 132: 1809-1816.
38. Mason Jr DJ, Lowe J, Welch SP (1999). Cannabinoid modulation of dynorphin A: correlation to cannabinoid-induced antinociception. Eur J Pharmacol 378: 237-248.
39. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI (1990). Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346: 561-564.
40. Napier TC, Mitrovic I (1999). Opioid modulation of ventral pallidal inputs. Ann NY Acad Sci 877: 176-201.
41. Navarro M, Carrera MR, Fratta W, Valverde O, Cossu G, Fattore L et al (2001). Functional interaction between opioid and cannabinoid receptors in drug self-administration. J Neurosci 21: 5344-5350.
42. Olds ME (1982). Reinforcing effects of morphine in the nucleus accumbens. Brain Res 237: 429-440.
43. Panagis G, Miliaressis E, Anagnostakis Y, Spyraki C (1995). Ventral pallidum self-stimulation: a moveable electrode mapping study. Behav Brain Res 68: 165-172.
44. Paxinos G, Watson C (1998). The Rat Brain in Stereotaxic Coordinates. Academic: San Diego.
45. Pettit HO, Ettenberg A, Bloom FE, Koob GF (1984). Destruction of dopamine in the nucleus accumbens selectively attenuates cocaine but not heroin self-administration in rats. Psychopharmacology (Berlin) 84: 167-173.
46. Pickel VM, Chan J, Kash TL, Rodriguez JJ, MacKie K (2004). Compartment-specific localization of cannabinoid 1 (CB1) and micro-opioid receptors in rat nucleus accumbens. Neuroscience 127: 101-112.
47. Pistis M, Muntoni AL, Pillolla G, Gessa GL (2002). Cannabinoids inhibit excitatory inputs to neurons in the shell of the nucleus accumbens: an in vivo electrophysiological study. Eur J Neurosci 15: 1795-1802.
48. Platt DM, Rowlett JK, Spealman RD (2001). Discriminative stimulus effects of intravenous heroin and its metabolites in rhesus monkeys: opioid and dopaminergic mechanisms. J Pharmacol Exp Ther 299: 760-767.
49. Pontieri FE, Tanda G, Di Chiara G (1995). Intravenous cocaine, morphine, and amphetamine preferentially increase extracellular dopamine in the 'shell' as compared with the 'core' of the rat nucleus accumbens. Proc Natl Acad Sci USA 92: 12304-12308.
50. Reisine T, Law SF, Blake A, Tallent M (1996). Molecular mechanisms of opiate receptor coupling to G proteins and effector systems. Ann NY Acad Sci 780: 168-175.
51. Rice OV, Gordon N, Gifford AN (2002). Conditioned place preference to morphine in cannabinoid CB1 receptor knockout mice. Brain Res 945: 135-138.
52. Robbe D, Alonso G, Duchamp F, Bockaert J, Manzoni OJ (2001). Localization and mechanisms of action of cannabinoid receptors at the glutamatergic synapses of the mouse nucleus accumbens. J Neurosci 21: 109-116.
53. Robbe D, Alonso G, Manzoni OJ (2003). Exogenous and endogenous cannabinoids control synaptic transmission in mice nucleus accumbens. Ann NY Acad Sci 1003: 212-225.
54. Robbe D, Kopf M, Remaury A, Bockaert J, Manzoni OJ (2002). Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc Natl Acad Sci USA 99: 8384-8388.
55. Roberto M, Schweitzer P, Madamba SG, Stouffer DG, Parsons LH, Siggins GR (2004). Acute and chronic ethanol alter glutamatergic transmission in rat central amygdala: an in vitro and in vivo analysis. J Neurosci 24: 1594-1603.
56. Robledo P, Koob GF (1993). Two discrete nucleus accumbens projection areas differentially mediate cocaine self-administration in the rat. Behav Brain Res 55: 159-166.
57. Sesack SR, Pickel VM (1990). In the rat medial nucleus accumbens, hippocampal and catecholaminergic terminals converge on spiny neurons and are in apposition to each other. Brain Res 527: 266-279.
58. Shippenberg TS, Elmer GI (1998). The neurobiology of opiate reinforcement. Crit Rev Neurobiol 12: 267-303.
59. Smith AD, Bolam JP (1990). The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurones. Trends Neurosci 13: 259-265.
60. Solinas M, Panlilio LV, Antoniou K, Pappas LA, Goldberg SR (2003). The cannabinoid CB1 antagonist SR-141716A, differentially alters the reinforcing effects of heroin under continuous-reinforcement, fixed-ratio and progressive-ratio schedules of drug self-administration in rats. J Pharmacol Exp Ther 306: 93-102.
61. Tanda G, Pontieri FE, Di Chiara G (1997). Cannabinoid and heroin activation of mesolimbic dopamine transmission by a common mu1 opioid receptor mechanism. Science 276: 2048-2050.
62. Tzavara ET, Wade M, Nomikos GG (2003). Biphasic effects of cannabinoids on acetylcholine release in the hippocampus: site and mechanism of action. J Neurosci 23: 9374-9384.
63. Vaccarino FJ, Bloom FE, Koob GF (1985). Blockade of nucleus accumbens opiate receptors attenuates intravenous heroin reward in the rat. Psychopharmacology (Berlin) 86: 37-42.
64. Valverde O, Noble F, Beslot F, Dauge V, Fournie-Zaluski MC, Roques BP (2001). Delta9-tetrahydrocannabinol releases and facilitates the effects of endogenous enkephalins: reduction in morphine withdrawal syndrome without change in rewarding effect. Eur J Neurosci 13: 1816-1824.
65. Van Der Kooy D, Mucha RF, O'Shaughnessy M, Bucenieks P (1982). Reinforcing effects of brain microinjections of morphine revealed by conditioned place preference. Brain Res 243: 107-117.
66. Vlachou S, Nomikos GG, Panagis G (2003). WIN 55,212-2 decreases the reinforcing actions of cocaine through CB1 cannabinoid receptor stimulation. Behav Brain Res 141: 215-222.
67. Welch SP, Eads M (1999). Synergistic interactions of endogenous opioids and cannabinoid systems. Brain Res 848: 183-190.
68. Wise RA, Leone P, Rivest R, Leeb K (1995). Elevations of nucleus accumbens dopamine and DOPAC levels during intravenous heroin self-administration. Synapse 21: 140-148.
69. Xi ZX, Stein EA (1999). Baclofen inhibits heroin self-administration behavior and mesolimbic dopamine release. J Pharmacol Exp Ther 290: 1369-1374.
70. Xi ZX, Stein EA (2000). Increased mesolimbic GABA concentration blocks heroin self-administration in the rat. J Pharmacol Exp Ther 294: 613-619.
71. Xi ZX, Stein EA (2002). GABAergic mechanisms of opiate reinforcement. Alcohol Alcohol 37: 485-494.
72. Yang CR, Mogenson GJ (1989). Ventral pallidal neuronal responses to dopamine receptor stimulation in the nucleus accumbens. Brain Res 489: 237-246.