Neurochemical evidence that stimulation of CB1 cannabinoid receptors on GABAergic nerve terminals activates the dopaminergic reward system by increasing dopamine release in the rat nucleus accumbens

Neurochemistry International

Volumn 54, Issue 7, 2009, Pages 452-457

  Sperlágh, Beáta ^a,b   Windisch, Katalin ^a   Andó, Rómeó D ^a   Sylvester Vizi, E ^a,b  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Cannabinoid; CB1 receptor; Dopamine; GABA; Nucleus accumbens; Release

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 4 AMINOBUTYRIC ACID RECEPTOR; BICUCULLINE; CANNABINOID 1 RECEPTOR; N (4 HYDROXY 2 METHYLPHENYL)ARACHIDONAMIDE; N METHYL DEXTRO ASPARTIC ACID; VANOXERINE;

ARTICLE; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC SYSTEM; ELECTRIC FIELD; ELECTROSTIMULATION; NERVE ENDING; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; VENTRAL TEGMENTUM;

ANIMALS; BENZOXAZINES; BICUCULLINE; DOPAMINE; ELECTRIC STIMULATION; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; MALE; MORPHOLINES; NAPHTHALENES; NERVE ENDINGS; NUCLEUS ACCUMBENS; PIPERIDINES; PYRAZOLES; RATS; RATS, WISTAR; RECEPTOR, CANNABINOID, CB1; RECEPTORS, GABA-A; REWARD;

RATTUS;

EID: 63149154839     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2009.01.017     Document Type: Article

References (56)

1. Andersen P.H. The dopamine inhibitor GBR 12909: selectivity and molecular mechanism of action. Eur. J. Pharmacol. 166 (1989) 493-504
2. Cadogan A.K., Alexander S.P., Boyd E.A., and Kendall D.A. Influence of cannabinoids on electrically evoked dopamine release and cyclic AMP generation in the rat striatum. J. Neurochem. 69 (1997) 1131-1137
3. Cheer J.F., Wassum K.M., Heien M.L., Phillips P.E., and Wightman R.M. Cannabinoids enhance subsecond dopamine release in the nucleus accumbens of awake rats. J. Neurosci. 24 (2004) 4393-4400
4. Chen J.P., Paredes W., Li J., Smith D., Lowinson J., and Gardner E.L. Delta 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 102 (1990) 156-162
5. B receptor interactions in rat hippocampal membranes. Neurochem. Int. 52 (2008) 1402-1409
6. Crespo J.A., Sturm K., Saria A., and Zernig G. Activation of muscarinic and nicotinic acetylcholine receptors in the nucleus accumbens core is necessary for the acquisition of drug reinforcement. J. Neurosci. 26 (2006) 6004-6010
7. de Lago E., de Miguel R., Lastres-Becker I., Ramos J.A., and Fernandez-Ruiz J. Involvement of vanilloid-like receptors in the effects of anandamide on motor behavior and nigrostriatal dopaminergic activity: in vivo and in vitro evidence. Brain Res. 1007 (2004) 152-159
8. Fadda P., Scherma M., Spano M.S., Salis P., Melis V., Fattore L., and Fratta W. Cannabinoid self-administration increases dopamine release in the nucleus accumbens. Neuroreport 17 (2006) 1629-1632
9. A receptors. Nat. Rev. 6 (2005) 215-229
10. Fattore L., Fadda P., Spano M.S., Pistis M., and Fratta W. Neurobiological mechanisms of cannabinoid addiction. Mol. Cell. Endocrinol. 286 (2008) S97-S107
11. Ferraro L., Tanganelli S., O'Connor W.T., Antonelli T., Rambert F., and Fuxe K. The vigilance promoting drug modafinil increases dopamine release in the rat nucleus accumbens via the involvement of a local GABAergic mechanism. Eur. J. Pharmacol. 306 (1996) 33-39
12. French E.D., Dillon K., and Wu X. Cannabinoids excite dopamine neurons in the ventral tegmentum and substantia nigra. Neuroreport 8 (1997) 649-652
13. Freund T.F., Katona I., and Piomelli D. Role of endogenous cannabinoids in synaptic signaling. Physiol. Rev. 83 (2003) 1017-1066
14. 1 receptors. Eur. J. Pharmacol. 341 (1998) 39-44
15. Glykys J., Mann E.O., and Mody I. Which GABA(A) receptor subunits are necessary for tonic inhibition in the hippocampus?. J. Neurosci. 28 (2008) 1421-1426
16. 1 receptors colocalize with tyrosine hydroxylase in cultured fetal mesencephalic neurons and their activation increases the levels of this enzyme. Brain Res. 857 (2000) 56-65
17. Katona I., Sperlagh B., Sik A., Kafalvi A., Vizi E.S., Mackie K., and Freund T.F. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J. Neurosci. 19 (1999) 4544-4558
18. Katona I., and Freund T.F. Endocannabinoid signaling as a synaptic circuit breaker in neurological diseases. Nat. Med. 14 (2008) 923-930
19. 2+ levels and transmitter release in the hippocampus. Br. J. Pharmacol. 151 (2007) 551-563
20. Kofalvi A., Rodrigues R.J., Ledent C., Mackie K., Vizi E.S., Cunha R.A., and Sperlagh B. Involvement of cannabinoid receptors in the regulation of neurotransmitter release in the rodent striatum: a combined immunochemical and pharmacological analysis. J. Neurosci. 25 (2005) 2874-2884
21. 3H]glutamate from rodent hippocampal synaptosomes via a novel CB1 receptor-independent action. Eur. J. Neurosci. 18 (2003) 1973-1978
22. Lau T., and Schloss P. The cannabinoid CB1 receptor is expressed on serotonergic and dopaminergic neurons. Eur. J. Pharmacol. 578 (2008) 137-141
23. Lecca D., Cacciapaglia F., Valentini V., and Di Chiara G. Monitoring extracellular dopamine in the rat nucleus accumbens shell and core during acquisition and maintenance of intravenous WIN 55,212-2 self-administration. Psychopharmacology 188 (2006) 63-74
24. Liao C., Zheng J., David L.S., and Nicholson R.A. Inhibition of voltage-sensitive sodium channels by the cannabinoid 1 receptor antagonist AM 251 in mammalian brain. Basic Clin. Pharmacol. Toxicol. 94 (2004) 73-78
25. Lopez-Moreno J.A., Gonzalez-Cuevas G., Moreno G., and Navarro M. The pharmacology of the endocannabinoid system: functional and structural interactions with other neurotransmitter systems and their repercussions in behavioral addiction. Addict. Biol. 13 (2008) 160-187
26. Maldonado R., Valverde O., and Berrendero F. Involvement of the endocannabinoid system in drug addiction. Trends Neurosci. 29 (2006) 225-232
27. Manzoni O.J., and Bockaert J. Cannabinoids inhibit GABAergic synaptic transmission in mice nucleus accumbens. Eur. J. Pharmacol. 412 (2001) R3-R5
28. Matsuda L.A., Bonner T.I., and Lolait S.J. Localization of cannabinoid receptor mRNA in rat brain. J. Comp. Neurol. 327 (1993) 535-550
29. Matyas F., Yanovsky Y., Mackie K., Kelsch W., Misgeld U., and Freund T.F. Subcellular localization of type 1 cannabinoid receptors in the rat basal ganglia. Neuroscience 137 (2006) 337-361
30. 2 upon chronic rotenone treatment. Free Radic. Biol. Med. 39 (2005) 133-142
31. A receptors in the crosshairs of hormones and ethanol. Neurochem. Int. 52 (2008) 60-64
32. A receptors. Trends Neurosci. 27 (2004) 569-575
33. Onaivi E.S., Ishiguro H., Gong J.P., Patel S., Perchuk A., Meozzi P.A., Myers L., Mora Z., Tagliaferro P., Gardner E., Brusco A., Akinshola B.E., Liu Q.R., Hope B., Iwasaki S., Arinami T., Teasenfitz L., and Uhl G.R. Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain. Ann. N. Y. Acad. Sci. 1074 (2006) 514-536
34. Parolaro D., Vigano D., and Rubino T. Endocannabinoids and drug dependence. Curr. Drug Targets 4 (2005) 643-655
35. Pickel V.M., Chan J., Kash T.L., Rodriguez J.J., and MacKie K. Compartment-specific localization of cannabinoid 1 (CB1) and mu-opioid receptors in rat nucleus accumbens. Neuroscience 127 (2004) 101-112
36. Pickel V.M., Chan J., Kearn C.S., and Mackie K. Targeting dopamine D2 and cannabinoid-1 (CB1) receptors in rat nucleus accumbens. J. Comp. Neurol. 495 (2006) 299-313
37. Robbe D., Alonso G., Duchamp F., Bockaert J., and Manzoni O.J. Localization and mechanisms of action of cannabinoid receptors at the glutamatergic synapses of the mouse nucleus accumbens. J. Neurosci. 21 (2001) 109-116
38. Robbe D., Alonso G., and Manzoni O.J. Exogenous and endogenous cannabinoids control synaptic transmission in mice nucleus accumbens. Ann. N. Y. Acad. Sci. 1003 (2003) 212-225
39. Robbe D., Kopf M., Remaury A., Bockaert J., and Manzoni O.J. Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 8384-8388
40. Schlicker E., and Kathmann M. Modulation of transmitter release via presynaptic cannabinoid receptors. Trends Pharmacol. Sci. 22 (2001) 565-572
41. Schoffelmeer A.N., Hogenboom F., Wardeh G., and De Vries T.J. Interactions between CB1 cannabinoid and mu opioid receptors mediating inhibition of neurotransmitter release in rat nucleus accumbens core. Neuropharmacology 51 (2006) 773-781
42. A receptor subunits in the basal ganglia and associated limbic brain areas of the adult rat. J. Comp. Neurol. 433 (2001) 526-549
43. ATP channels. Neurochem. Int. 52 (2008) 80-88
44. Smolders I., De Klippel N., Sarre S., Ebinger G., and Michotte Y. Tonic GABA-ergic modulation of striatal dopamine release studied by in vivo microdialysis in the freely moving rat. Eur. J. Pharmacol. 284 (1995) 83-91
45. Spanagel R., and Weiss F. The dopamine hypothesis of reward:past and current status. Trends Neurosci. 22 (1999) 521-527
46. Szabo B., Muller T., and Koch H. Effects of cannabinoids on dopamine release in the corpus striatum and the nucleus accumbens in vitro. J. Neurochem. 73 (1999) 1084-1089
47. Szabo B., Siemes S., and Wallmichrath I. Inhibition of GABAergic neurotransmission in the ventral tegmental area by cannabinoids. Eur. J. Neurosci. 15 (2002) 2057-2061
48. Tanda G., Pontieri F.E., and Di Chiara G. Cannabinoid and heroin activation of mesolimbic dopamine transmission by a common mu1 opioid receptor mechanism. Science 276 (1997) 2048-2050
49. Tsou K., Brown S., Sanudo-Pena M.C., Mackie K., and Walker J.M. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83 (1998) 393-411
50. van der Stelt M., and Di Marzo V. The endocannabinoid system in the basal ganglia and in the mesolimbic reward system: implications for neurological and psychiatric disorders. Eur. J. Pharmacol. 480 (2003) 133-150
51. Vizi E.S. Role of high-affinity receptors and membrane transporters in nonsynaptic communication and drug action in the central nervous system. Pharmacol. Rev. 52 (2000) 63-89
52. Vizi E.S., Palkovits M., Lendvai B., Baranyi M., Kovacs K.J., and Zelles T. Distinct temperature-dependent dopamine-releasing effect of drugs of abuse in the olfactory bulb. Neurochem. Int. 45 (2004) 63-71
53. Vizi E.S., Rozsa B., Mayer A., Kiss J.P., Zelles T., and Lendvai B. Further evidence for the functional role of nonsynaptic nicotinic acetylcholine receptors. Eur. J. Pharmacol. 500 (2004) 499-508
54. Whitehead K.J., Rose S., and Jenner P. Involvement of intrinsic cholinergic and GABAergic innervation in the effect of NMDA on striatal dopamine efflux and metabolism as assessed by microdialysis studies in freely moving rats. Eur. J. Neurosci. 14 (2001) 851-860
55. Yan Q. Focal bicuculline increases extracellular dopamine concentration in the nucleus accumbens of freely moving rats as measured by in vivo microdialysis. Eur. J. Pharmacol. 385 (1999) 7-13
56. Yanovsky Y., Mades S., and Misgeld U. Retrograde signaling changes the venue of postsynaptic inhibition in rat substantia nigra. Neuroscience 122 (2003) 317-328