Individual differences in the effects of cannabinoids on motor activity, dopaminergic activity and DARPP-32 phosphorylation in distinct regions of the brain

International Journal of Neuropsychopharmacology

Volumn 13, Issue 9, 2010, Pages 1175-1191

  Polissidis, Alexia ^a,b   Chouliara, Olga ^a   Galanopoulos, Andreas ^b   Rentesi, Georgia ^a   Dosi, Maria ^a   Hyphantis, Thomas ^a   Marselos, Marios ^a   Papadopoulou Daifoti, Zeta ^b   Nomikos, George G ^c   Spyraki, Christina ^b   Tzavara, Eleni T ^d   Antoniou, Katerina ^a  

^a UNIVERSITY OF IOANNINA   (Greece)

^b UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^c TAKEDA PHARMACEUTICALS   (United States)

^d INSERM   (France)

Author keywords

9 tetrahydrocannabinol; DARPP 32; dopamine; individual differences; motor activity; WIN55,212 2

Indexed keywords

11 HYDROXYDRONABINOL; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; DOPAMINE; PHOSPHOPROTEIN DARPP 32;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE METABOLISM; DOPAMINERGIC ACTIVITY; HABITUATION; MALE; MOTOR ACTIVITY; NONHUMAN; NUCLEUS ACCUMBENS; PHENOTYPE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; TURNOVER TIME;

ANALGESICS; ANIMALS; BEHAVIOR, ANIMAL; BENZOXAZINES; BRAIN; CANNABINOIDS; CORPUS STRIATUM; DOPAMINE; DOPAMINE AND CAMP-REGULATED PHOSPHOPROTEIN 32; DOSE-RESPONSE RELATIONSHIP, DRUG; MALE; MORPHOLINES; MOTOR ACTIVITY; NAPHTHALENES; NUCLEUS ACCUMBENS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; TETRAHYDROCANNABINOL;

EID: 77957236773     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145709991003     Document Type: Article

References (65)

1. Andersson M, Usiello A, Borgkvist A, Pozzi L, et al. (2005). Cannabinoid action depends on phosphorylation of dopamine- and cAMP-regulated phosphoprotein of 32 kDa at the protein kinase a site in striatal projection neurons. Journal of Neuroscience 25, 8432-8438. (Pubitemid 41324729)
2. Antoniou K, Papathanasiou G, Panagis G, Nomikos GG, et al. (2004). Individual responses to novelty predict qualitative differences in d-amphetamine-induced open field but not reward-related behaviors in rats. Neuroscience 123, 613-623. (Pubitemid 38045400)
3. Antoniou K, Papathanasiou G, Papalexi E, Hyphantis T, et al. (2008). Individual responses to novelty are associated with differences in behavioral and neurochemical profiles. Behavioural Brain Research 187, 462-472.
4. Borgkvist A, Fisone G (2007). Psychoactive drugs and regulation of the cAMP/PKA/DARPP-32 cascade in striatal medium spiny neurons. Neuroscience and Biobehavioral Reviews 31, 79-88. (Pubitemid 44880073)
5. Borgkvist A, Marcellino D, Fuxe K, Greengard P, et al. (2008). Regulation of DARPP-32 phosphorylation by delta9-tetrahydrocannabinol. Neuropharmacology 54, 31-35.
6. Carey RJ (1986). Relationship of limbic dopamine levels to amphetamine- and anticholinergic-induced hyperactivity in the rat. Biological Psychiatry 21, 317-321.
7. Castaneda E, Moss DE, Oddie SD, Whishaw IQ (1991). THC does not affect striatal dopamine release: microdialysis in freely moving rats. Pharmacology Biochemistry and Behavior 40, 587-591.
8. Cerbone A, Sadile AG (1994). Behavioral habituation to spatial novelty: interference and noninterference studies. Neuroscience and Biobehavioral Reviews 18, 497-518.
9. Cheer JF, Wassum KM, Heien ML, Phillips PE, et al. (2004). Cannabinoids enhance subsecond dopamine release in the nucleus accumbens of awake rats. Journal of Neuroscience 24, 4393-4400.
10. Chen J, Paredes W, Lowinson JH, Gardner EL (1990a). Delta 9-tetrahydrocannabinol enhances presynaptic dopamine efflux in medial prefrontal cortex. European Journal of Pharmacology 190, 259-262. (Pubitemid 20372332)
11. Chen JP, Paredes W, Li J, Smith D, et al. (1990b). 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 (Berlin) 102, 156-162. (Pubitemid 20264653)
12. Chen JP, Paredes W, Lowinson JH, Gardner EL (1991). Strain-specific facilitation of dopamine efflux by delta 9-tetrahydrocannabinol in the nucleus accumbens of rat: an in vivo microdialysis study. Neuroscience Letters 129, 136-180.
13. Commissiong JW (1985). Monoamine metabolites: their relationship and lack of relationship to monoaminergic neuronal activity. Biochemical Pharmacology 34, 1127-1131. (Pubitemid 15009224)
14. Cools AR, Ellenbroek BA, Gingras MA, Engbersen A, et al. (1997). Differences in vulnerability and susceptibility to dexamphetamine in Nijmegen high and low responders to novelty: a dose-effect analysis of spatio-temporal programming of behaviour. Psychopharmacology (Berlin) 132, 181-187. (Pubitemid 27338993)
15. Darmani NA (2001). The cannabinoid CB1 receptor antagonist SR 141716A reverses the antiemetic and motor depressant actions of WIN 55,212-2. European Journal of Pharmacology 430, 49-58.
16. Davis WM, Borgen LA (1974). Effects of cannabidiol and delta-9-tetrahydrocannabinol on operant behavior. Research Communications in Chemical Pathology and Pharmacology 9, 453-462.
17. Degroot A, Nomikos GG (2007). In vivo neurochemical effects induced by changes in endocannabinoid neurotransmission. Current Opinion in Pharmacology 7, 62-68. (Pubitemid 46238039)
18. Di Chiara G, Bassareo V, Fenu S, De Luca MA, et al. (2004). Dopamine and drug addiction: the nucleus accumbens shell connection. Neuropharmacology 47 (Suppl.), 227-241. (Pubitemid 39298267)
19. Drews E, Schneider M, Koch M (2005). Effects of the cannabinoid receptor agonist WIN 55,212-2 on operant behavior and locomotor activity in rats. Pharmacology Biochemistry and Behavior 80, 145-150. (Pubitemid 40126212)
20. Ferre S (1997). Adenosine-dopamine interactions in the ventral striatum. Implications for the treatment of schizophrenia. Psychopharmacology (Berlin), 133, 107-120. (Pubitemid 27404740)
21. Gardner EL (2005). Endocannabinoid signaling system and brain reward: emphasis on dopamine. Pharmacology Biochemistry and Behavior 81, 263-284.
22. Giuliani D, Ferrari F, Ottani A (2000). The cannabinoid agonist HU 210 modifies rat behavioural responses to novelty and stress. Pharmacological Research 41, 47-53. (Pubitemid 30008936)
23. Hashimotodani Y, Ohno-Shosaku T, Kano M (2007). Endocannabinoids and synaptic function in the CNS. Neuroscientist 13, 127-137. (Pubitemid 46524316)
24. Hernandez-Tristan R, Arevalo C, Canals S, Leret ML (2000). The effects of acute treatment with delta9-THC on exploratory behaviour and memory in the rat. Journal of Physiology and Biochemistry 56, 17-24. (Pubitemid 30263740)
25. Hitzemann R, Curell J, Hom D, Loh H (1982). Effects of naloxone on d-amphetamine- and apomorphine-induced behavior. Neuropharmacology 21, 1005-1011. (Pubitemid 12001296)
26. Iversen L (2003). Cannabis and the brain. Brain 126, 1252-1270. (Pubitemid 36644373)
27. Jarbe TU, Andrzejewski ME, DiPatrizio NV (2002). Interactions between the CB1 receptor agonist delta 9-THC and the CB1 receptor antagonist SR-141716 in rats: openfield revisited. Pharmacology Biochemistry and Behavior 73, 911-919.
28. Kabbaj M, Norton CS, Kollack-Walker S, Watson SJ, et al. (2001). Social defeat alters the acquisition of cocaine self-administration in rats: role of individual differences in cocaine-taking behavior. Psychopharmacology (Berlin) 158, 382-387. (Pubitemid 33141314)
29. Lecca D, Cacciapaglia F, Valentini V, Di Chiara G (2006). Monitoring extracellular dopamine in the rat nucleus accumbens shell and core during acquisition and maintenance of intravenous WIN 55,212-2 self-administration. Psychopharmacology (Berlin) 188, 63-74. (Pubitemid 44268242)
30. Lichtman AH, Fisher J, Martin BR (2001). Precipitated cannabinoid withdrawal is reversed by delta(9)- tetrahydrocannabinol or clonidine. Pharmacology Biochemistry and Behavior 69, 181-188. (Pubitemid 32566261)
31. Lindskog M, Svenningsson P, Pozzi L, Kim Y, et al. (2002). Involvement of DARPP-32 phosphorylation in the stimulant action of caffeine. Nature 418, 774-778.
32. Lundberg DJ, Daniel AR, Thayer SA (2005). Delta(9)- tetrahydrocannabinol- induced desensitization of cannabinoid-mediated inhibition of synaptic transmission between hippocampal neurons in culture. Neuropharmacology 49, 1170-1177.
33. Malone DT, Taylor DA (1999). Modulation by fluoxetine of striatal dopamine release following delta9- tetrahydrocannabinol: a microdialysis study in conscious rats. British Journal of Pharmacology 128, 21-26.
34. Miura H, Qiao H, Ohta T (2002). Influence of aging and social isolation on changes in brain monoamine turnover and biosynthesis of rats elicited by novelty stress. Synapse 46, 116-124.
35. Navarro M, Fernandez-Ruiz JJ, de Miguel R, Hernandez ML, et al. (1993a). An acute dose of delta 9-tetrahydrocannabinol affects behavioral and neurochemical indices of mesolimbic dopaminergic activity. Behavioral Brain Research 57, 37-46. (Pubitemid 23339725)
36. Navarro M, Fernandez-Ruiz JJ, De Miguel R, Hernandez ML, et al. (1993b). Motor disturbances induced by an acute dose of delta 9-tetrahydrocannabinol: possible involvement of nigrostriatal dopaminergic alterations. Pharmacology Biochemistry and Behavior 45, 291-298. (Pubitemid 23165218)
37. Ng Cheong Ton JM, Gerhardt GA, Friedemann M, Etgen AM, et al. (1988). The effects of delta 9-tetrahydrocannabinol on potassium-evoked release of dopamine in the rat caudate nucleus: an in vivo electrochemical and in vivo microdialysis study. Brain Research 451, 59-68.
38. ONeill C, Evers-Donnelly A, Nicholson D, OBoyle KM, et al. (2009). D2 receptor-mediated inhibition of dopamine release in the rat striatum in vitro is modulated by CB1 receptors: studies using fast cyclic voltammetry. Journal of Neurochemistry 108, 545-551.
39. Panagis G, Vlachou S, Nomikos GG (2008). Behavioral pharmacology of cannabinoids with a focus on preclinical models for studying reinforcing and dependenceproducing properties. Current Drug Abuse Reviews 1, 350-374.
40. Pandolfo P, Pamplona FA, Prediger RD, Takahashi RN (2007). Increased sensitivity of adolescent spontaneously hypertensive rats, an animal model of attention deficit hyperactivity disorder, to the locomotor stimulation induced by the cannabinoid receptor agonist WIN 55,212-2. European Journal of Pharmacology 563, 141-148. (Pubitemid 46602239)
41. Pertwee RG (2005). Pharmacological actions of cannabinoids. Handbook of Experimental Pharmacology 168, 1-51.
42. Piazza PV, Deminiere JM, Le Moal M, Simon H (1989). Factors that predict individual vulnerability to amphetamine self-administration. Science 245, 1511-1513. (Pubitemid 19243245)
43. Piazza PV, Deminiere JM, Maccari S, Mormede P, et al. (1990). Individual reactivity to novelty predicts probability of amphetamine self-administration. Behavioural Pharmacology 1, 339-345.
44. Pierce RC, Kumaresan V (2006). The mesolimbic dopamine system: the final common pathway for the reinforcing effect of drugs of abuse? Neuroscience and Biobehavioral Reviews 30, 215-238. (Pubitemid 41821810)
45. Pistis M, Ferraro L, Pira L, Flore G, et al. (2002). Delta(9)- tetrahydrocannabinol decreases extracellular GABA and increases extracellular glutamate and dopamine levels in the rat prefrontal cortex: an in vivo microdialysis study. Brain Research 948, 155-158. (Pubitemid 35283774)
46. 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. Proceedings of the National Academy of Sciences USA 92 12304-12308. (Pubitemid 26014059)
47. Pontieri FE, Tanda G, Orzi F, Di Chiara G (1996). Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs. Nature 382, 255-257. (Pubitemid 26251360)
48. Przegalinski E, Gothert M, Frankowska M, Filip M (2005). WIN 55,212-2-induced reduction of cocaine hyperlocomotion: possible inhibition of 5-HT(3) receptor function. European Journal of Pharmacology 517, 68-73. (Pubitemid 40910255)
49. Rodriguez De Fonseca F, Fernandez-Ruiz JJ, Murphy LL, Cebeira M, et al. (1992). Acute effects of delta-9- tetrahydrocannabinol on dopaminergic activity in several rat brain areas. Pharmacology Biochemistry and Behavior 42, 269-275.
50. Rodvelt KR, Bumgarner DM, Putnam WC, Miller DK (2007). WIN-55,212-2 and SR-141716A alter nicotine-induced changes in locomotor activity, but do not alter nicotine-evoked [3H]dopamine release. Life Sciences 80, 337-344.
51. Sanudo-Pena MC, Romero J, Seale GE, Fernandez-Ruiz JJ, et al. (2000). Activational role of cannabinoids on movement. European Journal of Pharmacology 391, 269-274. (Pubitemid 30154094)
52. Schramm-Sapyta NL, Cha YM, Chaudhry S, Wilson WA, et al. (2007). Differential anxiogenic, aversive, and locomotor effects of thc in adolescent and adult rats. Psychopharmacology (Berlin) 191, 867-877. (Pubitemid 46399144)
53. Solinas M, Goldberg SR, Piomelli D (2008). The endocannabinoid system in brain reward processes. British Journal of Pharmacology 154, 369-383. (Pubitemid 351670594)
54. Steffens M, Engler C, Zentner J, Feuerstein TJ (2004). Cannabinoid CB1 receptor-mediated modulation of evoked dopamine release and of adenylyl cyclase activity in the human neocortex. British Journal of Pharmacology 141, 1193-1203. (Pubitemid 38582257)
55. Steffens M, Feuerstein TJ (2004). Receptor-independent depression of DA and 5-HT uptake by cannabinoids in rat neocortex-involvement of Na(+)/K(+)-ATPase. Neurochemistry International 44, 529-538. (Pubitemid 38183303)
56. Sulcova E, Mechoulam R, Fride E (1998). Biphasic effects of anandamide. Pharmacology Biochemistry and Behavior 59, 347-352. (Pubitemid 28072727)
57. Svenningsson P, Tzavara ET, Carruthers R, Rachleff I, et al. (2003). Diverse psychotomimetics act through a common signaling pathway. Science 302, 1412-1415. (Pubitemid 37452186)
58. Svenningsson P, Tzavara ET, Witkin JM, Fienberg AA, et al. (2002). Involvement of striatal and extrastriatal DARPP-32 in biochemical and behavioral effects of fluoxetine (Prozac). Proceedings of the National Academy of Sciences USA 99, 3182-3187. (Pubitemid 34240606)
59. Tanda G, Goldberg SR (2003). Cannabinoids: reward, dependence and underlying neurochemical mechanisms - a review of recent preclinical data. Psychopharmacology (Berlin) 169, 115-134. (Pubitemid 37129963)
60. Tanda G, Loddo P, Di Chiara G (1999). Dependence of mesolimbic dopamine transmission on delta9- tetrahydrocannabinol. European Journal of Pharmacology 376, 23-26. (Pubitemid 29320166)
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. (Pubitemid 27443611)
62. Tavares JV, Drevets WC, Sahakian BJ (2003). Cognition in mania and depression. Psychological Medicine 33, 959-967.
63. Thiel CM, Muller CP, Huston JP, Schwarting RK (1999). High versus low reactivity to a novel environment: behavioural, pharmacological and neurochemical assessments. Neuroscience 93, 243-251.
64. Tzavara ET, Wade M, Nomikos GG (2003). Biphasic effects of cannabinoids on acetylcholine release in the hippocampus: site and mechanism of action. Journal of Neuroscience 23, 9374-9384. (Pubitemid 37323037)
65. Wise RA (1996). Neurobiology of addiction. Current Opinion in Neurobiology 6, 243-251.