Involvement of the endogenous cannabinoid system in the effects of alcohol in the mesolimbic reward circuit: Electrophysiological evidence in vivo

Psychopharmacology

Volumn 183, Issue 3, 2005, Pages 368-377

  Perra, Simona ^a   Pillolla, Giuliano ^a   Melis, Miriam ^a   Muntoni, Anna Lisa ^a   Gessa, Gian Luigi ^a   Pistis, Marco ^a  

^a UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Alcohol; Basolateral amygdala; Cannabinoids; Dopamine neurons; Electrophysiology; Endocannabinoids; Mesolimbic system; Nucleus accumbens

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; ALCOHOL; ANANDAMIDE; CANNABINOID; ENDOCANNABINOID; FATTY ACID AMIDASE; RIMONABANT;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; ELECTROPHYSIOLOGY; IN VIVO STUDY; LIMBIC SYSTEM; MALE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RAT; REWARD; SYNAPSE; SYNAPTIC TRANSMISSION; VENTRAL TEGMENTUM;

ANIMALS; BENZAMIDES; CARBAMATES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCANNABINOIDS; ETHANOL; MALE; NUCLEUS ACCUMBENS; PIPERIDINES; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; REWARD; VENTRAL TEGMENTAL AREA;

EID: 27844583905     PISSN: 00333158     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00213-005-0195-0     Document Type: Article

References (78)

1. Arnone M, Maruani J, Chaperon F, Thiebot MH, Poncelet M, Soubrie P, Le Fur G (1997) Selective inhibition of sucrose and ethanol intake by SR 141716, an antagonist of central cannabinoid (CB1) receptors. Psychopharmacology (Berl) 132:104-106
2. Basavarajappa BS, Hungund BL (1999a) Chronic ethanol increases the cannabinoid receptor agonist anandamide and its precursor N- arachidonoylphosphatidylethanolamine in SK-N-SH cells. J Neurochem 72:522-528
3. Basavarajappa BS, Hungund BL (1999b) Down-regulation of cannabinoid receptor agonist-stimulated [35S]GTP gamma S binding in synaptic plasma membrane from chronic ethanol exposed mouse. Brain Res 815:89-97
4. Basavarajappa BS, Cooper TB, Hungund BL (1998) Chronic ethanol administration down-regulates cannabinoid receptors in mouse brain synaptic plasma membrane. Brain Res 793:212-218
5. Basavarajappa BS, Saito M, Cooper TB, Hungund BL (2000) Stimulation of cannabinoid receptor agonist 2-arachidonylglycerol by chronic ethanol and its modulation by specific neuromodulators in cerebellar granule neurons. Biochim Biophys Acta 1535:78-86
6. Bisogno T, Berrendero F, Ambrosino G, Cebeira M, Ramos JA, Fernandez-Ruiz JJ, Di Marzo V (1999) Brain regional distribution of endocannabinoids: implications for their biosynthesis and biological function. Biochem Biophys Res Commun 256:377-380
7. Brodie MS, 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
8. Brodie MS, Pesold C, Appel SB (1999) Ethanol directly excites dopaminergic ventral tegmental area reward neurons. Alcohol Clin Exp Res 23:1848-1852
9. Colombo G, Agabio R, Fa M, Guano L, Lobina C, Loche A, Reali R, Gessa GL (1998) Reduction of voluntary ethanol intake in ethanol-preferring sP rats by the cannabinoid antagonist SR-141716. Alcohol Alcohol 33:126-130
10. Colombo G, Serra S, Brunetti G, Gomez R, Melis S, Vacca G, Carai MM, Gessa L (2002) Stimulation of voluntary ethanol intake by cannabinoid receptor agonists in ethanol-preferring sP rats. Psychopharmacology (Berl) 159:181-187
11. Colombo G, Vacca G, Serra S, Carai MA, Gessa GL (2004) Suppressing effect of the cannabinoid CB1 receptor antagonist, SR 141716, on alcohol's motivational properties in alcohol-preferring rats. Eur J Pharmacol 498:119-123
12. Colombo G, Serra S, Vacca G, Carai MA, Gessa GL (2005) Endocannabinoid system and alcohol addiction: pharmacological studies. Pharmacol Biochem Behav 81:369-380
13. Criado JR, Lee RS, Berg GI, Henriksen SJ (1997) Ethanol inhibits single-unit responses in the nucleus accumbens evoked by stimulation of the basolateral nucleus of the amygdala. Alcohol Clin Exp Res 21:368-374
14. da Silva GE, Morato GS, Takahashi RN (2001) Rapid tolerance to Delta(9)-tetrahydrocannabinol and cross-tolerance between ethanol and Delta(9)-tetrahydrocannabinol in mice. Eur J Pharmacol 431:201-207
15. 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 U S A 85:5274-5278
16. Di Chiara G, Bassareo V, Fenu S, De Luca MA, Spina L, Cadoni C, Acquas E, Carboni E, Valentini V, Lecca D (2004) Dopamine and drug addiction: the nucleus accumbens shell connection. Neuropharmacology 47 (Suppl 1):227-241
17. Di Marzo V, Berrendero F, Bisogno T, Gonzalez S, Cavaliere P, Romero J, Cebeira M, Ramos JA, Fernandez-Ruiz JJ (2000) Enhancement of anandamide formation in the limbic forebrain and reduction of endocannabinoid contents in the striatum of delta9-tetrahydrocannabinol-tolerant rats. J Neurochem 74:1627-1635
18. Floresco SB, Blaha CD, Yang CR, Phillips AG (2001) Modulation of hippocampal and amygdalar-evoked activity of nucleus accumbens neurons by dopamine: cellular mechanisms of input selection. J Neurosci 21:2851-2860
19. Foddai M, Dosia G, Spiga S, Diana M (2004) Acetaldehyde increases dopaminergic neuronal activity in the VTA. Neuropsychopharmacology 29:530-536
20. French ED, Dillon K, Wu X (1997) Cannabinoids excite dopamine neurons in the ventral tegmentum and substantia nigra. Neuroreport 8:649-652
21. Freund TF, Katona I, Piomelli D (2003) Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83:1017-1066
22. Gallate JE, McGregor IS (1999) The motivation for beer in rats: effects of ritanserin, naloxone and SR 141716. Psychopharmacology (Berl) 142:302-308
23. Gallate JE, Saharov T, Mallet PE, McGregor IS (1999) Increased motivation for beer in rats following administration of a cannabinoid CB1 receptor agonist. Eur J Pharmacol 370:233-240
24. Gallate JE, Mallet PE, McGregor IS (2004) Combined low dose treatment with opioid and cannabinoid receptor antagonists synergistically reduces the motivation to consume alcohol in rats. Psychopharmacology (Berl) 173:210-216
25. Gardner EL (2005) Endocannabinoid signaling system and brain reward: emphasis on dopamine. Pharmacol Biochem Behav 81:263-284
26. Gessa GL, Muntoni F, Collu M, Vargiu L, Mereu G (1985) Low doses of ethanol activate dopaminergic neurons in the ventral tegmental area. Brain Res 348:201-203
27. 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
28. Gonzalez S, Fernandez-Ruiz J, Di Marzo V, Hernandez M, Arevalo C, Nicanor C, Cascio MG, Ambrosio E, Ramos JA (2004) Behavioral and molecular changes elicited by acute administration of SR141716 to Delta9-tetrahydrocannabinol- tolerant rats: an experimental model of cannabinoid abstinence. Drug Alcohol Depend 74:159-170
29. Grace AA, Bunney BS (1983) Intracellular and extracellular electrophysiology of nigral dopaminergic neurons - 1. Identification and characterization. Neuroscience 10:301-315
30. Grace AA, Bunney BS (1984) The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 4:2877-2890
31. Guyenet PG, Aghajanian GK (1978) Antidromic identification of dopaminergic and other output neurons of the rat substantia nigra. Brain Res 150:69-84
32. Hakan RL, Eyl C (1995) Neuropharmacology of the nucleus accumbens: iontophoretic applications of morphine and nicotine have contrasting effects on single-unit responses evoked by ventral pallidal and fimbria stimulation. Synapse 20:175-184
33. Hakan RL, Hart C, Eyl C (1993) Specific neurophysiological effects of systemic nicotine on neurons in the nucleus accumbens. Synapse 15:191-197
34. Hanlon EC, Baldo BA, Sadeghian K, Kelley AE (2004) Increases in food intake or food-seeking behavior induced by GABAergic, opioid, or dopaminergic stimulation of the nucleus accumbens: is it hunger? Psychopharmacology (Berl) 172:241-247
35. 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
36. Hill MN, Patel S, Carrier EJ, Rademacher DJ, Ormerod BK, Hillard CJ, Gorzalka BB (2005) Downregulation of endocannabinoid signaling in the hippocampus following chronic unpredictable stress. Neuropsychopharmacology 30:508-515
37. 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
38. Hoffman PL, Rabe CS, Moses F, Tabakoff B (1989) N-methyl-D-aspartate receptors and ethanol: inhibition of calcium flux and cyclic GMP production. J Neurochem 52:1937-1940
39. Houchi H, Babovic D, Pierrefiche O, Ledent C, Daoust M, Naassila M (2005) CB1 receptor knockout mice display reduced ethanol-induced conditioned place preference and increased striatal dopamine D2 receptors. Neuropsychopharmacology 30:339-349
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. Imperato A, Di Chiara G (1986) Preferential stimulation of dopamine release in the nucleus accumbens of freely moving rats by ethanol. J Pharmacol Exp Ther 239:219-228
42. Kathuria S, Gaetani S, Fegley D, Valino F, Duranti A, Tontini A, Mor M, Tarzia G, La Rana G, Calignano A, Giustino A, Tattoli M, Palmery M, Cuomo V, Piomelli D (2003) Modulation of anxiety through blockade of anandamide hydrolysis. Nat Med 9:76-81
43. Lipski J (1981) Antidromic activation of neurones as an analytic tool in the study of the central nervous system. J Neurosci Methods 4:1-32
44. Lovinger DM, White G, Weight FF (1989) Ethanol inhibits NMDA-activated ion current in hippocampal neurons. Science 243:1721-1724
45. 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
46. Mato S, Chevaleyre V, Robbe D, Pazos A, Castillo PE, Manzoni OJ (2004) A single in-vivo exposure to delta 9THC blocks endocannabinoid-mediated synaptic plasticity. Nat Neurosci 7:585-586
47. Melis M, Perra S, Muntoni AL, Pillolla G, Lutz B, Marsicano G, Di Marzo V, Gessa GL, Pistis M (2004a) Prefrontal cortex stimulation induces 2-arachidonoyl-glycerol-mediated suppression of excitation in dopamine neurons. J Neurosci 24:10707-10715
48. Melis M, Pistis M, Perra S, Muntoni AL, Pillolla G, Gessa GL (2004b) Endocannabinoids mediate presynaptic inhibition of glutamatergic transmission in rat ventral tegmental area dopamine neurons through activation of CB1 receptors. J Neurosci 24:53-62
49. Mulder AB, Hodenpijl MG, Lopes da Silva FH (1998) Electrophysiology of the hippocampal and amygdaloid projections to the nucleus accumbens of the rat: convergence, segregation, and interaction of inputs. J Neurosci 18:5095-5102
50. Naassila M, Pierrefiche O, Ledent C, Daoust M (2004) Decreased alcohol self-administration and increased alcohol sensitivity and withdrawal in CB1 receptor knockout mice. Neuropharmacology 46:243-253
51. Newman LM, Lutz MP, Gould MH, Domino EF (1972) 9-Tetrahydrocannabinol and ethyl alcohol: evidence for cross-tolerance in the rat. Science 175:1022-1023
52. Newman LM, Lutz MP, Domino EF (1974) Delta9-tetrahydrocannabinol and some CNS depressants: evidence for cross-tolerance in the rat. Arch Int Pharmacodyn Ther 207:254-259
53. Ortiz S, Oliva JM, Perez-Rial S, Palomo T, Manzanares J (2004) Differences in basal cannabinoid CB1 receptor function in selective brain areas and vulnerability to voluntary alcohol consumption in Fawn Hooded and Wistar rats. Alcohol Alcohol 39:297-302
54. Patel S, Roelke CT, Rademacher DJ, Hillard CJ (2005) Inhibition of restraint stress-induced neural and behavioural activation by endogenous cannabinoid signalling. Eur J Neurosci 21:1057-1069
55. Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates, 3rd edn. Academic, San Diego
56. Pistis M, Ferraro L, Pira L, Flore G, Tanganelli S, Gessa GL, Devoto P (2002a) Delta(9)-tetrahydrocannabinol decreases extracellular GABA and increases extracellular glutamate and dopamine levels in the rat prefrontal cortex: an in vivo microdialysis study. Brain Res 948:155-158
57. Pistis M, Muntoni AL, Pillolla G, Gessa GL (2002b) Cannabinoids inhibit excitatory inputs to neurons in the shell of the nucleus accumbens: an in vivo electrophysiological study. Eur J Neurosci 15:1795-1802
58. Pistis M, Perra S, Pillolla G, Melis M, Gessa GL, Muntoni AL (2004) Cannabinoids modulate neuronal firing in the rat basolateral amygdala: evidence for CB1- and non-CB1-mediated actions. Neuropharmacology 46:115-125
59. Pistis M, Muntoni AL, Pillolla G, Perra S, Cignarella G, Melis M, Gessa GL (2005) Gamma-hydroxybutyric acid (GHB) and the mesoaccumbens reward circuit: evidence for GABA(B) receptor-mediated effects. Neuroscience 131:465-474
60. Poncelet M, Maruani J, Calassi R, Soubrie P (2003) Overeating, alcohol and sucrose consumption decrease in CB1 receptor deleted mice. Neurosci Lett 343:216-218
61. Riegel AC, Lupica CR (2004) Independent presynaptic and postsynaptic mechanisms regulate endocannabinoid signaling at multiple synapses in the ventral tegmental area. J Neurosci 24:11070-11078
62. 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
63. Serra S, Brunetti G, Pani M, Vacca G, Carai MA, Gessa GL, Colombo G (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. Sprague GL, Craigmill AL (1976) Ethanol and delta-9-tetrahydrocannabinol: mechanism for cross-tolerance in mice. Pharmacol Biochem Behav 5:409-415
65. Sugiura T, Kondo S, Sukagawa A, Nakane S, Shinoda A, Itoh K, Yamashita A, Waku K (1995) 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun 215:89-97
66. Sugiura T, Kodaka T, Nakane S, Miyashita T, Kondo S, Suhara Y, Takayama H, Waku K, Seki C, Baba N, Ishima Y (1999) Evidence that the cannabinoid CB1 receptor is a 2-arachidonoylglycerol receptor. Structure-activity relationship of 2-arachidonoylglycerol, ether-linked analogues, and related compounds. J Biol Chem 274:2794-2801
67. Suzdak PD, Schwartz RD, Skolnick P, Paul SM (1986) Ethanol stimulates gamma-aminobutyric acid receptor-mediated chloride transport in rat brain synaptoneurosomes. Proc Natl Acad Sci U S A 83:4071-4075
68. 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
69. Ungless MA, Magill PJ, Bolam JP (2004) Uniform inhibition of dopamine neurons in the ventral tegmental area by aversive stimuli. Science 303:2040-2042
70. Weiss F, Lorang MT, Bloom FE, Koob GF (1993) Oral alcohol self-administration stimulates dopamine release in the rat nucleus accumbens: genetic and motivational determinants. J Pharmacol Exp Ther 267:250-258
71. Wenger T, Moldrich G, Furst S (2003) Neuromorphological background of cannabis addiction. Brain Res Bull 61:125-128
72. Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483-494
73. Wise RA, Bozarth MA (1987) A psychomotor stimulant theory of addiction. Psychol Rev 94:469-492
74. Wise R, Gardner E (2002) Functional anatomy of substance-related disorders. In: D'haenen H, den Boer J, Willner P (eds) Biological psychiatry. Wiley, New York, pp 509-522
75. Wright A, Terry P (2002) Modulation of the effects of alcohol on driving-related psychomotor skills by chronic exposure to cannabis. Psychopharmacology (Berl) 160:213-219
76. Yoshimoto K, McBride WJ, Lumeng L, Li TK (1992) Alcohol stimulates the release of dopamine and serotonin in the nucleus accumbens. Alcohol 9:17-22
77. Zahm DS (2000) An integrative neuroanatomical perspective on some subcortical substrates of adaptive responding with emphasis on the nucleus accumbens. Neurosci Biobehav Rev 24:85-105
78. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di Marzo V, Julius D, Hogestatt ED (1999) Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400:452-457