A brain on cannabinoids: The role of dopamine release in reward seeking

Cold Spring Harbor Perspectives in Medicine

Volumn 2, Issue 8, 2012, Pages

  Oleson, Erik B ^a   Cheer, Joseph F ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 ARACHIDONOYLGLYCEROL; 2, 3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL) PYRROLO [1, 2, 3 DE] [1, 4] BENZOXAZINE; 4 AMINOBUTYRIC ACID RECEPTOR; ALCOHOL; AMPHETAMINE; ANANDAMIDE; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABIS; COCAINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; ENDOCANNABINOID; LIPOPROTEIN LIPASE; MORPHINE; N (4 HYDROXY 2 METHYLPHENYL) ARACHIDONAMIDE; RIMONABANT; TETRAHYDROCANNABINOL; UNCLASSIFIED DRUG; CANNABINOID RECEPTOR AGONIST; DOPAMINE;

ARTICLE; BRAIN DEPTH STIMULATION; CYCLIC POTENTIOMETRY; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DOPAMINERGIC TRANSMISSION; DRUG ABUSE; GABAERGIC SYSTEM; HUMAN; MESOLIMBIC DOPAMINERGIC SYSTEM; MICRODIALYSIS; MOTIVATION; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; NUCLEUS ACCUMBENS; REWARD; STIMULATION; THERAPEUTIC MISCONCEPTION; VENTRAL TEGMENTUM; WITHDRAWAL SYNDROME; ANIMAL; BRAIN; CANNABIS ADDICTION; DRUG EFFECT; METABOLISM; MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGICAL ASPECT; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ANIMALIA; CANNABIS;

ANIMALS; BRAIN; CANNABINOID RECEPTOR AGONISTS; DOPAMINE; ENDOCANNABINOIDS; HUMANS; MARIJUANA ABUSE; MICE; REWARD; SIGNAL TRANSDUCTION; SUBSTANCE WITHDRAWAL SYNDROME; SYNAPTIC TRANSMISSION; TETRAHYDROCANNABINOL;

EID: 84886668510     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a012229     Document Type: Article

References (84)

1. Aceto MD, Scates SM, Lowe JA, Martin BR. 1995. Cannabinoid precipitated withdrawal by the selective cannabinoid receptor antagonist, SR 141716A. Eur J Pharmacol 282: R1-R2.
2. 9-tetrahydrocannabinol: Studies on precipitated and abrupt withdrawal. J Pharmacol Exp Ther 278: 1290-1295.
3. Aceto MD, Scates SM, Martin BB. 2001. Spontaneous and precipitated withdrawal with a synthetic cannabinoid, WIN 55212-2. Eur J Pharmacol 416: 75-81.
4. Alger BE, Kim J. 2011. Supply and demand for endocannabinoids. Trends Neurosci 34: 304-315.
5. Aragona BJ, Cleaveland NA, Stuber GD, Day JJ, Carelli RM, Wightman RM. 2008. Preferential enhancement of dopamine transmission within the nucleus accumbens shell by cocaine is attributable to a direct increase in phasic dopamine release events. J Neurosci 28: 8821-8831.
6. Budney AJ, Hughes JR. 2006. The cannabis withdrawal syndrome. Curr Opin Psychiatry 19: 233-238.
7. Budney AJ, Novy PL, Hughes JR. 1999. Marijuana withdrawal among adults seeking treatment for marijuana dependence. Addiction 94: 1311-1322.
8. Castaneda E, Moss DE, Oddie SD, Whishaw IQ. 1991. THC does not affect striatal dopamine release: Microdialysis in freely moving rats. Pharmacol Biochem Behav 40: 587-591.
9. Cheer JF, Marsden CA, Kendall DA, Mason R. 2000. Lack of response suppression follows repeated ventral tegmental cannabinoid administration: An in vitro electrophysiological study. Neuroscience 99: 661-667.
10. Cheer JF, Wassum KM, Heien ML, Phillips PE, Wightman RM. 2004. Cannabinoids enhance subsecond dopamine release in the nucleus accumbens of awake rats. J Neurosci 24: 4393-4400.
11. Cheer JF, Wassum KM, Sombers LA, Heien ML, Ariansen JL, Aragona BJ, PhillipsPE, Wightman RM. 2007. Phasic dopamine release evoked by abused substances requires cannabinoid receptor activation. J Neurosci 27: 791-795.
12. 9-Tetrahydrocannabinol produces naloxone-blockable enhancement of presynaptic basal dopamine efflux in nucleus accumbens of conscious, freely-moving rats as measured by intracerebral microdialysis. Psychopharmacology (Berl) 102: 156-162.
13. 9-tetrahydrocannabinol in the nucleus accumbens of rat: An in vivo microdialysis study. Neurosci Lett 129: 136-180.
14. 9-tetrahydrocannabinol enhances ventral tegmental somatodendritic dopamine levels but not forebrain dopamine levels: Evidence for local neural action by marijuana's psychoactive ingredient. Brain Res 621: 65-70.
15. Childress AR, McLellan AT, Ehrman R, O'Brien CP. 1988. Classically conditioned responses in opioid and cocaine dependence: A role in relapse. NIDA Res Monogr 84: 25-43.
16. Childress AR, Hole AV, Ehrman RN, Robbins SJ, McLellan AT, O'Brien CP. 1993. Cue reactivity and cue reactivity interventions in drug dependence. NIDA Res Monogr 137: 73-95.
17. Devane WA, Dysarz FA, Johnson MR, Melvin LS, Howlett AC. 1988. Determination and characterization of a cannabinoid receptor in rat brain. Mol Pharmacol 34: 605-613.
18. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, Gibson D, Mandelbaum A, Etinger A, Mechoulam R. 1992. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258: 1946-1949.
19. Diana M, Muntoni AL, Pistis M, Melis M, Gessa GL. 1999. Lasting reduction in mesolimbic dopamine neuronal activity after morphine withdrawal. Eur J Neurosci 11: 1037-1041.
20. 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 85: 5274-5278.
21. Dreyer JK, Herrik KF, Berg RW, Hounsgaard JD. 2010. Influence of phasic and tonic dopamine release on receptor activation. J Neurosci 30: 14273-14283.
22. Einhorn LC, Johansen PA, White FJ. 1988. Electrophysiological effects of cocaine in the mesoaccumbens dopamine system: Studies in the ventral tegmental area. J Neurosci 8: 100-112.
23. 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.
24. Forget B, Coen KM, Le Foll B. 2009. Inhibition of fatty acid amide hydrolase reduces reinstatement of nicotine seeking but not break point for nicotine self-administration comparison with CB 1 receptor blockade. Psychopharmacology 205: 613-624.
25. French ED. 1997. Δ9-Tetrahydrocannabinol excites rat VTA dopamine neurons through activation of cannabinoid CB1 but not opioid receptors. Neurosci Lett 226: 159-162.
26. French ED, Dillon K, Wu X. 1997. Cannabinoids excite dopamine neurons in the ventral tegmentum and substantia nigra. Neuroreport 8: 649-652.
27. Freund TF, Katona I, Piomelli D. 2003. Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83: 1017-1066.
28. Gamaleddin I, Guranda M, Goldberg SR, Le Foll B. 2011. The selective anandamide transport inhibitor VDM11 attenuates reinstatement of nicotine seeking induced by nicotine associated cues and nicotine priming, but does not affect nicotine-intake. Br J Pharmacol 164: 1652-1660.
29. Gaoni Y, Mechoulam R. 1964. Isolation, structure, and partial synthesis of an active constituent of hashish. J Am Chem Soc 86: 1646-1647.
30. Gardner EL. 2002. Addictive potential of cannabinoids: The underlying neurobiology. Chem Phys Lipids 121: 267-290.
31. Gardner EL. 2005. Endocannabinoid signaling system and brain reward: Emphasis on dopamine. Pharmacol Biochem Behav 81: 263-284.
32. Gardner EL, Lowinson JH. 1991. Marijuana's interaction with brain reward systems: Update 1991. Pharmacol Biochem Behav 40: 571-580.
33. Gessa GL, Melis M, Muntoni AL, Diana M. 1998. Cannabinoids activate mesolimbic dopamine neurons by an action on cannabinoid CB1 receptors. Eur J Pharmacol 341: 39-44.
34. Gonon F. 1988. Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry. Neuroscience 24: 19-28.
35. Grace AA. 1991. Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: A hypothesis for the etiology of schizophrenia. Neuroscience 41: 1-24.
36. Haney M, Ward AS, Comer SD, Foltin RW, Fischman MW. 1999. Abstinence symptoms following smoked marijuana in humans. Psychopharmacology 141: 395-404.
37. Herkenham M, Lynn AB, de Costa BR, Richfield EK. 1991. Neuronal localization of cannabinoid receptors in the basal ganglia of the rat. Brain Res 547: 267-274.
38. 1-tetrahydrocannabinol and psychoactive drugs: Effects on uptake of biogenic amines and on behavior. Eur J Pharmacol 59: 267-276.
39. Howlett AC, Mukhopadhyay S. 2000. Cellular signal transduction by anandamide and 2-arachidonoylglycerol. Chem Phys Lipids 108: 53-70.
40. Hungund BL, Szakall I, Adam A, Basavarajappa BS, Vadasz C. 2003. Cannabinoid CB1 receptor knockout mice exhibit markedly reduced voluntary alcohol consumption and lack alcohol induced dopamine release in the nucleus accumbens. J Neurochem 84: 698-704.
41. Jones RT, Benowitz N, Bachman J. 1976. Clinical studies of cannabis tolerance and dependence. Ann NY Acad Sci 282: 221-239.
42. Julian MD, Martin AB, Cuellar B, Rodriguez De Fonseca F, Navarro M, MoratallaR, Garcia-Segura LM. 2003. Neuroanatomical relationship between type 1 cannabinoid receptors and dopaminergic systems in the rat basal ganglia. Neuroscience 119: 309-318.
43. Justinova Z, Munzar P, Panlilio L, Yasar S, Redhi G, Tanda G, Goldberg S. 2008. Blockade of THC-seeking behavior and relapse in monkeys by the cannabinoid CB1-receptor antagonist rimonabant. Neuropsychopharmacology 33: 2870-2877.
44. Justinova Z, Panlilio LV, Goldberg SR. 2009. Drug addiction. Curr Top Behav Neurosci 1: 309-346.
45. Koob GF. 2009. Neurobiological substrates for the dark side of compulsivity in addiction. Neuropharmacology 56: 18-31.
46. Koob GF, Sanna PP, Bloom FE. 1998. Neuroscience of addiction. Review. Neuron 21: 461-476.
47. Le Foll B, Goldberg S. 2004. Rimonabant, a CB1 antagonist, blocks nicotine-conditioned place preferences. Neuroreport 15: 2139-2143.
48. Lichtman AH, Martin BR. 2002. Marijuana withdrawal syndrome in the animal model. J Clin Pharmacol 42: 20S-27S.
49. Lupica CR, Riegel AC. 2005. Endocannabinoid release from midbrain dopamine neurons: A potential substrate for cannabinoid receptor antagonist treatment of addiction. Neuropharmacology 48: 1105-1116.
50. 9-tetrahydrocannabinol: A microdialysis study in conscious rats. Br J Pharmacol 128: 21-26.
51. 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.
52. Mechoulam R, Ben-Shabat S, Hanus L, Ligumsky M, Kaminski NE, Schatz AR, Gopher A, Almog S, Martin BR, Compton DR. 1995. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 50: 83-90.
53. Melis M, Pistis M, Perra S, Muntoni AL, Pillolla G, Gessa GL. 2004. Endocannabinoids mediate presynaptic inhibition of glutamatergic transmission in rat ventral tegmental area dopamine neurons through activation of CB1 receptors. J Neurosci 24: 53-62.
54. 9-tetrahydrocannabinol on potassium-evoked release of dopamine in the rat caudate nucleus: An in vivo electrochemical and in vivo microdialysis study. Brain Res 451: 59-68.
55. Oleson EB, Beckert MV, Morra JT, Lansink CS, Cachope R, Abdullah RA, LoriauxAL, Schetters D, Pattij T, Roitman MF, et al. 2012. Endocannabinoids shape accumbal encoding of cue-motivated behavior via CB1 receptor activation in the ventral tegmentum. Neuron 73: 360-373.
56. Owesson-White CA, Ariansen J, Stuber GD, Cleaveland NA, Cheer JF, WightmanRM, Carelli RM. 2009. Neural encoding of cocaine-seeking behavior is coincident with phasic dopamine release in the accumbens core and shell. Eur J Neurosci 30: 1117-1127.
57. Perra S, Pillolla G, Melis M, Muntoni AL, Gessa GL, Pistis M. 2005. Involvement of the endogenous cannabinoid system in the effects of alcohol in the mesolimbic reward circuit: Electrophysiological evidence in vivo. Psychopharmacology (Berl) 183: 368-377.
58. Phillips PE, Stuber GD, Heien ML, Wightman RM, Carelli RM. 2003. Subsecond dopamine release promotes cocaine seeking. Nature 422: 614-618.
59. Pierce RC, Kumaresan V. 2006. The mesolimbic dopamine system: The final common pathway for the reinforcing effect of drugs of abuse? Neurosci Biobehav Rev 30: 215-238.
60. Poddar MK, Dewey WL. 1980. Effects of cannabinoids on catecholamine uptake and release in hypothalamic and striatal synaptosomes. J Pharmacol Exp Ther 214: 63-67.
61. Ritz MC, Lamb RJ, Goldberg SR, Kuhar MJ. 1987. Cocaine receptors on dopamine transporters are related to self-administration of cocaine. Science 237: 1219-1223.
62. Roberts DC, Corcoran ME, Fibiger HC. 1977. On the role of ascending catecholaminergic systems in intravenous self-administration of cocaine. Pharmacol Biochem Behav 6: 615-620.
63. Rossetti ZL, Hmaidan Y, Gessa GL. 1992. Marked inhibition of mesolimbic dopamine release: A common feature of ethanol, morphine, cocaine and amphetamine abstinence in rats. Eur J Pharmacol 221: 227-234.
64. Scherma M, Medalie J, Fratta W, Vadivel SK, Makriyannis A, Piomelli D, MikicsE, Haller J, Yasar S, Tanda G. 2008. The endogenous cannabinoid anandamide has effects on motivation and anxiety that are revealed by fatty acid amide hydrolase (FAAH) inhibition. Neuropharmacology 54: 129-140.
65. Solinas M, Goldberg SR, Piomelli D. 2008. The endocannabinoid system in brain reward processes. Br J Pharmacol 154: 369-383.
66. Sombers LA, Beyene M, Carelli RM, Wightman RM. 2009. Synaptic overflow of dopamine in the nucleus accumbens arises from neuronal activity in the ventral tegmental area. J Neurosci 29: 1735-1742.
67. Spanagel R, Weiss F. 1999. The dopamine hypothesis of reward: Past and current status. Trends Neurosci 22: 521-527.
68. Szabo B, Siemes S, Wallmichrath I. 2002. Inhibition of GABAergic neurotransmission in the ventral tegmental area by cannabinoids. Eur J Neurosci 15: 2057-2061.
69. Tanda G, Pontieri FE, Di Chiara G. 1997. Cannabinoid and heroin activation of mesolimbic dopamine transmission by a common μ1 opioid receptor mechanism. Science 276: 2048-2050.
70. 9-tetrahydrocannabinol. Eur J Pharmacol 376: 23-26.
71. Tanimura A, Yamazaki M, Hashimotodani Y, Uchigashima M, Kawata S, Abe M, Kita Y, Hashimoto K, Shimizu T, Watanabe M, et al. 2010. The endocannabinoid 2-arachidonoylglycerol produced by diacylglycerol lipase α mediates retrograde suppression of synaptic transmission. Neuron 65: 320-327.
72. Todd A. 1946. Hashish. Experientia 2: 55-60.
73. 9-tetrahydrocannabinol precipitated by a cannabinoid receptor antagonist. Eur J Pharmacol 280: R13-R15.
74. Van Der Stelt M, Mazzola C, Esposito G, Matias I, Petrosino S, Filippis DD, Micale V, Steardo L, Drago F, Iuvone T. 2006. Endocannabinoids and β-amyloid-induced neurotoxicity in vivo: Effect of pharmacological elevation of endocannabinoid levels. Cell Mol Life Sci 63: 1410-1424.
75. Vries T, Schoffelmeer A. 2005. Cannabinoid CB1 receptors control conditioned drug seeking. Trends Pharmacol Sci 26: 420-426.
76. Weiss F, Markou A, Lorang MT, Koob GF. 1992. Basal extracellular dopamine levels in the nucleus accumbens are decreased during cocaine withdrawal after unlimited-access self-administration. Brain Res 593: 314-318.
77. Weiss F, Parsons LH, Schulteis G, Hyyti P, Lorang MT, Bloom FE, Koob GF. 1996. Ethanol self-administration restores withdrawal-associated deficiencies in accumbal dopamine and 5-hydroxytryptamine release in dependent rats. J Neurosci 16: 3474-3485.
78. Weiss F, Ciccocioppo R, Parsons LH, Katner S, Liu X, Zorrilla EP, Valdez GR, Ben-Shahar O, Angeletti S, Richter RR. 2001. Compulsive drug-seeking behavior and relapse. Neuroadaptation, stress, and conditioning factors. Ann NY Acad Sci 937: 1-26.
79. Wheeler RA, Carelli RM. 2009. Dissecting motivational circuitry to understand substance abuse. Neuropharmacology 56: 149-159.
80. Wickelgren I. 1997. Marijuana: Harder than thought? Science 276: 1967-1968.
81. Wilson RI, Nicoll RA. 2001. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410: 588-592.
82. Wilson RI, Nicoll RA. 2002. Endocannabinoid signaling in the brain. Science 296: 678-682.
83. Wise RA, Bozarth MA. 1985. Brain mechanisms of drug reward and euphoria. Psychiatr Med 3: 445-460.
84. 9-tetrahydrocannabinol on rat midbrain dopamine neurons: An electrophysiological assessment. Neuropharmacology 39: 391-398.