Cannabinoid-hormone interactions in the regulation of motivational processes

Hormones and Behavior

Volumn 58, Issue 1, 2010, Pages 100-110

  López, Hassan H ^a  

^a SKIDMORE COLLEGE   (United States)

Author keywords

Cannabinoids; Copulation; CP 55,940; Estrogen; Estrous; HPG axis; Reward; Sex difference; Sexual motivation; THC

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N MORPHOLINO 1H PYRAZOLE 3 CARBOXAMIDE; 2 ARACHIDONOYLGLYCEROL; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 4 (1,1 DIMETHYLHEPTYL) 1',2',3',4',5',6' HEXAHYDRO 2,3' DIHYDROXY 6' (3 HYDROXYPROPYL)BIPHENYL; 4 [6 METHOXY 2 (4 METHOXYPHENYL) 3 BENZOFURANYLCARBONYL]BENZONITRILE; ANANDAMIDE; CANNABINOID; COCAINE; DEXANABINOL; DRONABINOL; ENDOCANNABINOID; ESTRADIOL; RIMONABANT; SEX HORMONE; CANNABINOID RECEPTOR AFFECTING AGENT; CENTRAL NERVOUS SYSTEM AGENTS; HORMONE;

ARTICLE; COPULATION; DRUG ABUSE; DRUG DEPENDENCE; DRUG MECHANISM; ESTRUS; HORMONAL REGULATION; HUMAN; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; MOTIVATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REINFORCEMENT; REWARD; SEX DIFFERENCE; SEXUAL BEHAVIOR; ANIMAL; DRUG EFFECTS; METABOLISM; PHYSIOLOGY;

ANIMALS; CANNABINOIDS; CENTRAL NERVOUS SYSTEM AGENTS; ENDOCANNABINOIDS; HORMONES; HUMANS; MOTIVATION; CANNABINOID RECEPTOR MODULATORS;

EID: 77953479184     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2009.10.005     Document Type: Article

References (142)

1. Agmo A., Turi A.L., Ellingsen E., Kaspersen H. Preclinical models of sexual desire: conceptual and behavioral analyses. Pharmacol. Biochem. Behav. 2004, 78:379-404.
2. Ayalon D., Nir I., Cordova T., Bauminger S., Puder M., Naor Z., Kashi R., Zor U., Harell A., Lindner H.R. Acute effect of delta1-tetrahydrocannabinol on the hypothalamo-pituitary-ovarian axis in the rat. Neuroendocrinology 1977, 23:31-42.
3. Becker J.B. Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol. Biochem. Behav. 1999, 64:803-812.
4. Becker J.B., Rudick C.N., Jenkins W.J. The role of dopamine in the nucleus accumbens and striatum during sexual behavior in the female rat. J. Neurosci. 2001, 21:3236-3241.
5. Besch N.F., Smith C.G., Besch P.K., Kaufman R.H. The effect of marihuana (delta-9-tetrahydrocannabinol) on the secretion of luteinizing hormone in the ovariectomized rhesus monkey. Am. J. Obstet. Gynecol. 1977, 128:635-642.
6. Bloch E., Thysen B., Morrill G.A., Gardner E., Fujimoto G. Effects of cannabinoids on reproduction and development. Vitam. Horm. 1978, 36:203-258.
7. Bonnin A., Fernandez-Ruiz J.J., Martin M., Rodriguez de Fonseca F., Hernandez M.L., Ramos J.A. delta 9-Tetrahydrocannabinol affects mesolimbic dopaminergic activity in the female rat brain: interactions with estrogens. J. Neural Transm. Gen. Sect. 1993, 92:81-95.
8. Bonnin A., Ramos J.A., Rodriguez de Fonseca F., Cebeira M., Fernandez-Ruiz J.J. Acute effects of delta 9-tetrahydrocannabinol on tuberoinfundibular dopamine activity, anterior pituitary sensitivity to dopamine and prolactin release vary as a function of estrous cycle. Neuroendocrinology 1993, 58:280-286.
9. Bradshaw H.B., Rimmerman N., Krey J.F., Walker J.M. Sex and hormonal cycle differences in rat brain levels of pain-related cannabimimetic lipid mediators. Am. J. Physiol., Regul. Integr. Comp. Physiol. 2006, 291:R349-358.
10. Breivogel C.S., Sim L.J., Childers S.R. Regional differences in cannabinoid receptor/G-protein coupling in rat brain. J. Pharmacol. Exp. Ther. 1997, 282:1632-1642.
11. Brown T.T., Dobs A.S. Endocrine effects of marijuana. J. Clin. Pharmacol. 2002, 42:90S-96S.
12. Caprioli D., Celentano M., Paolone G., Badiani A. Modeling the role of environment in addiction. Prog. Neuropsychopharmacol. Biol. Psychiatry 2007, 31:1639-1653.
13. Carroll M.E., Lynch W.J., Roth M.E., Morgan A.D., Cosgrove K.P. Sex and estrogen influence drug abuse. Trends Pharmacol. Sci. 2004, 25:273-279.
14. Castelli M.P., Piras A.P., Melis T., Succu S., Sanna F., Melis M.R., Collu S., Grazia Ennas M., Diaz G., Mackie K., Argiolas A. Cannabinoid CB1 receptors in the paraventricular nucleus and central control of penile erection: immunocytochemistry, autoradiography and behavioral studies. Neuroscience 2007, 147:197-206.
15. Chakravarty I., Sheth A.R., Ghosh J.J. Effect of acute delta9-tetrahydrocannabinol treatment on serum luteinizing hormone and prolactin levels in adult female rats. Fertil. Steril. 1975, 26:947-948.
16. Chakravarty I., Sheth P.R., Sheth A.R., Ghosh J.J. Delta-9-tetrahydrocannabinol: its effect on hypothalamo-pituitary system in male rats. Arch. Androl. 1982, 8:25-27.
17. Chaperon F., Thiebot M.H. Behavioral effects of cannabinoid agents in animals. Crit. Rev. Neurobiol. 1999, 13:243-281.
18. Cota D. The role of the endocannabinoid system in the regulation of hypothalamic-pituitary-adrenal axis activity. J. Neuroendocrinol. 2008, 20(Suppl 1):35-38.
19. Cota D., Marsicano G., Lutz B., Vicennati V., Stalla G.K., Pasquali R., Pagotto U. Endogenous cannabinoid system as a modulator of food intake. Int. J. Obes. Relat. Metab. Disord. 2003, 27:289-301.
20. Craft R.M. Sex differences in behavioral effects of cannabinoids. Life Sci. 2005, 77:2471-2478.
21. Craft R.M., Leitl M.D. Gonadal hormone modulation of the behavioral effects of Delta9-tetrahydrocannabinol in male and female rats. Eur. J. Pharmacol. 2008, 578:37-42.
22. Dalterio S.L., Mayfield D.L., Bartke A. Effects of delta 9-THC on plasma hormone levels in female mice. Subst. Alcohol Actions/Misuse 1983, 4:339-345.
23. Daniel J.M., Winsauer P.J., Brauner I.N., Moerschbaecher J.M. Estrogen improves response accuracy and attenuates the disruptive effects of delta9-THC in ovariectomized rats responding under a multiple schedule of repeated acquisition and performance. Behavioral Neuroscience 2002, 116:989-998.
24. de Miguel R., Romero J., Munoz R.M., Garcia-Gil L., Gonzalez S., Villanua M.A., Makriyannis A., Ramos J.A., Fernandez-Ruiz J.J. Effects of cannabinoids on prolactin and gonadotrophin secretion: involvement of changes in hypothalamic gamma-aminobutyric acid (GABA) inputs. Biochem. Pharmacol. 1998, 56:1331-1338.
25. Devane W.A., Dysarz F.A., Johnson M.R., Melvin L.S., Howlett A.C. Determination and characterization of a cannabinoid receptor in rat brain. Mol. Pharmacol. 1988, 34:605-613.
26. Devane W.A., Hanus L., Breuer A., Pertwee R.G., Stevenson L.A., Griffin G., Gibson D., Mandelbaum A., Etinger A., Mechoulam R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 1992, 258:1946-1949.
27. Di Chiara G., Acquas E., Tanda G., Cadoni C. Drugs of abuse: biochemical surrogates of specific aspects of natural reward?. Biochem. Soc. Symp. 1993, 59:65-81.
28. Erskine M.S. Solicitation behavior in the estrous female rat: a review. Horm. Behav. 1989, 23:473-502.
29. Ettenberg A. The runway model of drug self-administration. Pharmacol. Biochem. Behav. 2009, 91:271-277.
30. Fattore L., Spano M.S., Altea S., Angius F., Fadda P., Fratta W. Cannabinoid self-administration in rats: sex differences and the influence of ovarian function. Br. J. Pharmacol. 2007, 152:795-804.
31. Fattore L., Spano M.S., Deiana S., Melis V., Cossu G., Fadda P., Fratta W. An endocannabinoid mechanism in relapse to drug seeking: a review of animal studies and clinical perspectives. Brain Res. Rev. 2007, 53:1-16.
32. Fattore L., Altea S., Fratta W. Sex differences in drug addiction: a review of animal and human studies. Womens Health (Lond. Engl) 2008, 4:51-65.
33. Fattore L., Fadda P., Spano M.S., Pistis M., Fratta W. Neurobiological mechanisms of cannabinoid addiction. Mol. Cell. Endocrinol. 2008, 286:S97-S107.
34. Feltenstein M.W., See R.E. Plasma progesterone levels and cocaine-seeking in freely cycling female rats across the estrous cycle. Drug Alcohol Depend 2007, 89:183-189.
35. Fernández-Ruiz J.J., Munoz R.M., Romero J., Villanua M.A., Makriyannis A., Ramos J.A. Time course of the effects of different cannabimimetics on prolactin and gonadotrophin secretion: evidence for the presence of CB1 receptors in hypothalamic structures and their involvement in the effects of cannabimimetics. Biochem. Pharmacol. 1997, 53:1919-1927.
36. Fernández-Ruiz J.J., Berrendero F., Hernandez M.L., Romero J., Ramos J.A. Role of endocannabinoids in brain development. Life Sci. 1999, 65:725-736.
37. Fernández-Solari J., Scorticati C., Mohn C., De Laurentiis A., Billi S., Franchi A., McCann S.M., Rettori V. Alcohol inhibits luteinizing hormone-releasing hormone release by activating the endocannabinoid system. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:3264-3268.
38. Ferrari F., Ottani A., Giuliani D. Inhibitory effects of the cannabinoid agonist HU 210 on rat sexual behaviour. Physiol. Behav. 2000, 69:547-554.
39. Freund T.F., Katona I., Piomelli D. Role of endogenous cannabinoids in synaptic signaling. Physiol. Rev. 2003, 83:1017-1066.
40. Gammon C.M., Freeman G.M., Xie W., Petersen S.L., Wetsel W.C. Regulation of gonadotropin-releasing hormone secretion by cannabinoids. Endocrinology 2005, 146:4491-4499.
41. Ganoni Y., Mechoulam R. Isolation, structure, and partial synthesis of an active constituent of hashish. J. Am. Chem. Soc. 1964, 86:1646-1647.
42. Gardner E.L. Endocannabinoid signaling system and brain reward: emphasis on dopamine. Pharmacol. Biochem. Behav. 2005, 81:263-284.
43. Genn R.F., Tucci S., Marco E.M., Viveros M.P., File S.E. Unconditioned and conditioned anxiogenic effects of the cannabinoid receptor agonist CP 55,940 in the social interaction test. Pharmacol. Biochem. Behav. 2004, 77:567-573.
44. Glass M., Dragunow M., Faull R.L. Cannabinoid receptors in the human brain: a detailed anatomical and quantitative autoradiographic study in the fetal, neonatal and adult human brain. Neuroscience 1997, 77:299-318.
45. Gong J.P., Onaivi E.S., Ishiguro H., Liu Q.R., Tagliaferro P.A., Brusco A., Uhl G.R. Cannabinoid CB2 receptors: immunohistochemical localization in rat brain. Brain Res. 2006, 1071:10-23.
46. González S., Manzanares J., Berrendero F., Wenger T., Corchero J., Bisogno T., Romero J., Fuentes J.A., Di Marzo V., Ramos J.A., Fernández-Ruiz J. Identification of endocannabinoids and cannabinoid CB(1) receptor mRNA in the pituitary gland. Neuroendocrinology 1999, 70:137-145.
47. González S., Bisogno T., Wenger T., Manzanares J., Milone A., Berrendero F., Di Marzo V., Ramos J.A., Fernández-Ruiz J.J. Sex steroid influence on cannabinoid CB(1) receptor mRNA and endocannabinoid levels in the anterior pituitary gland. Biochem. Biophys. Res. Commun. 2000, 270:260-266.
48. Gordon J.H., Bromley B.L., Gorski R.A., Zimmermann E. Delta9-Tetrahydrocannabinol enhancement of lordosis behavior in estrogen treated female rats. Pharmacol. Biochem. Behav. 1978, 8:603-608.
49. Gorzalka B.B., Hill M.N. Cannabinoids, reproduction, and sexual behavior. Annu. Rev. Sex Res. 2006, 17:132-161.
50. Gorzalka B.B., Hill M.N., Hillard C.J. Regulation of endocannabinoid signaling by stress: implications for stress-related affective disorders. Neurosci. Biobehav. Rev. 2008, 32:1152-1160.
51. Gorzalka B.B., Morrish A.C., Hill M.N. Endocannabinoid modulation of male rat sexual behavior. Psychopharmacology. (Berl) 2008, 198:479-486.
52. Harkany T., Keimpema E., Barabas K., Mulder J. Endocannabinoid functions controlling neuronal specification during brain development. Mol. Cell. Endocrinol. 2008, 286:S84-90.
53. Herkenham M., Lynn A.B., Johnson M.R., Melvin L.S., de Costa B.R., Rice K.C. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci. 1991, 11:563-583.
54. Hill M.N., Karacabeyli E.S., Gorzalka B.B. Estrogen recruits the endocannabinoid system to modulate emotionality. Psychoneuroendocrinology 2007, 32:350-357.
55. Hull E.M., Muschamp J.W., Sato S. Dopamine and serotonin: influences on male sexual behavior. Physiol. Behav. 2004, 83:291-307.
56. Jenkins W.J., Becker J.B. Dynamic increases in dopamine during paced copulation in the female rat. Eur. J. Neurosci. 2003, 18:1997-2001.
57. Kalbasi Anaraki D., Sianati S., Sadeghi M., Ghasemi M., Javadi P., Ejtemaei Mehr S., Dehpour A.R. Modulation by female sex hormones of the cannabinoid-induced catalepsy and analgesia in ovariectomized mice. Eur. J. Pharmacol. 2008, 586:189-196.
58. Klinger F.G., Battista N., De Felici M., Maccarrone M. Stage-variations of anandamide hydrolase activity in the mouse uterus during the natural oestrus cycle. J. Exp. Clin. Assist. Reprod. 2006, 3:3.
59. Koob G.F. Neuroadaptive mechanisms of addiction: studies on the extended amygdala. Eur. Neuropsychopharmacol. 2003, 13:442-452.
60. Koob G., Kreek M.J. Stress, dysregulation of drug reward pathways, and the transition to drug dependence. Am. J. Psychiatry 2007, 164:1149-1159.
61. Lazzarin N., Valensise H., Bari M., Ubaldi F., Battista N., Finazzi-Agro A., Maccarrone M. Fluctuations of fatty acid amide hydrolase and anandamide levels during the human ovulatory cycle. Gynecol. Endocrinol. 2004, 18:212-218.
62. Le Foll B., Forget B., Aubin H.J., Goldberg S.R. Blocking cannabinoid CB1 receptors for the treatment of nicotine dependence: insights from pre-clinical and clinical studies. Addict. Biol. 2008, 13:239-252.
63. Le Foll B., Goldberg S.R. Cannabinoid CB1 receptor antagonists as promising new medications for drug dependence. J. Pharmacol. Exp. Ther. 2005, 312:875-883.
64. López H.H., Olster D.H., Ettenberg A. Sexual motivation in the male rat: the role of primary incentives and copulatory experience. Horm. Behav. 1999, 36:176-185.
65. López H.H., Wurzel G., Ragen B. The effect of acute bupropion on sexual motivation and behavior in the female rat. Pharmacol. Biochem. Behav. 2007, 87:369-379.
66. López, H.H., Cushman, C.L., Chadwick, B., 2008. The effect of acute and chronic cannabinoid administration on female sexual motivation. Program No. 97.16. 2008 Neuroscience Meeting Planner. Washington, DC: Society for Neuroscience. Online.
67. López H.H., Webb S.A., Nash S. Cannabinoid receptor antagonism increases female sexual motivation. Pharmacol. Biochem. Behav. 2009, 92:17-24.
68. Lynch W.J. Sex differences in vulnerability to drug self-administration. Exp. Clin. Psychopharmacol. 2006, 14:34-41.
69. MacCarrone M., De Felici M., Bari M., Klinger F., Siracusa G., Finazzi-Agro A. Down-regulation of anandamide hydrolase in mouse uterus by sex hormones. Eur. J. Biochem. 2000, 267:2991-2997.
70. Mailleux P., Vanderhaeghen J.J. Distribution of neuronal cannabinoid receptor in the adult rat brain: a comparative receptor binding radioautography and in situ hybridization histochemistry. Neuroscience 1992, 48:655-668.
71. Maldonado R., Valverde O., Berrendero F. Involvement of the endocannabinoid system in drug addiction. Trends Neurosci. 2006, 29:225-232.
72. Mani S.K., Mitchell A., O'Malley B.W. Progesterone receptor and dopamine receptors are required in Delta 9-tetrahydrocannabinol modulation of sexual receptivity in female rats. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:1249-1254.
73. Martinez-Gonzalez D., Bonilla-Jaime H., Morales-Otal A., Henriksen S.J., Velazquez-Moctezuma J., Prospero-Garcia O. Oleamide and anandamide effects on food intake and sexual behavior of rats. Neurosci. Lett. 2004, 364:1-6.
74. Matsuda L.A., Lolait S.J., Brownstein M.J., Young A.C., Bonner T.I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990, 346:561-564.
75. McGregor I.S., Arnold J.C. Cannabis reward: biased towards the fairer sex?. Br. J. Pharmacol. 2007, 152:562-564.
76. Mechoulam R., Ben-Shabat S., Hanus L., Ligumsky M., Kaminski N.E., Schatz A.R., Gopher A., Almog S., Martin B.R., Compton D.R., et al. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem. Pharmacol. 1995, 50:83-90.
77. Melis M., Perra S., Muntoni A.L., Pillolla G., Lutz B., Marsicano G., Di Marzo V., Gessa G.L., Pistis M. Prefrontal cortex stimulation induces 2-arachidonoyl-glycerol-mediated suppression of excitation in dopamine neurons. J. Neurosci. 2004, 24:10707-10715.
78. Melis M.R., Succu S., Mascia M.S., Argiolas A. Antagonism of cannabinoid CB1 receptors in the paraventricular nucleus of male rats induces penile erection. Neurosci. Lett. 2004, 359:17-20.
79. Melis M.R., Succu S., Mascia M.S., Sanna F., Melis T., Castelli M.P., Argiolas A. The cannabinoid receptor antagonist SR-141716A induces penile erection in male rats: involvement of paraventricular glutamic acid and nitric oxide. Neuropharmacology 2006, 50:219-228.
80. Moldrich G., Wenger T. Localization of the CB1 cannabinoid receptor in the rat brain. An immunohistochemical study. Peptides 2000, 21:1735-1742.
81. Munro S., Thomas K.L., Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993, 365:61-65.
82. Murphy L.L., Steger R.W., Smith M.S., Bartke A. Effects of delta-9-tetrahydrocannabinol, cannabinol and cannabidiol, alone and in combinations, on luteinizing hormone and prolactin release and on hypothalamic neurotransmitters in the male rat. Neuroendocrinology 1990, 52:316-321.
83. Murphy L.L., Newton S.C., Dhali J., Chavez D. Evidence for a direct anterior pituitary site of delta-9-tetrahydrocannabinol action. Pharmacol. Biochem. Behav. 1991, 40:603-607.
84. Murphy L.L., Rodriguez de Fonseca F., Steger R.W. delta 9-Tetrahydrocannabinol antagonism of the anterior pituitary response to estradiol in immature female rats. Steroids 1991, 56:97-102.
85. Murphy L.L., Chandrashekar V., Bartke A. Delta-9-tetrahydrocannabinol inhibits pulsatile luteinizing hormone secretion in the male rat: effect of intracerebroventricular norepinephrine infusion. Neuroendocrinol. Lett. 1994, 16:1-7.
86. Murphy L.L., Gher J., Steger R.W., Bartke A. Effects of [Delta]9-tetrahydrocannabinol on copulatory behavior and neuroendocrine responses of male rats to female conspecifics. Pharmacol. Biochem. Behav. 1994, 48:1011-1017.
87. Murphy L.L., Munoz R.M., Adrian B.A., Villanua M.A. Function of cannabinoid receptors in the neuroendocrine regulation of hormone secretion. Neurobiol. Dis. 1998, 5:432-446.
88. Murphy L.L., Adrian B.A., Kohli M. Inhibition of luteinizing hormone secretion by delta9-tetrahydrocannabinol in the ovariectomized rat: effect of pretreatment with neurotransmitter or neuropeptide receptor antagonists. Steroids 1999, 64:664-671.
89. Narimatsu S., Watanabe K., Yamamoto I., Yoshimura H. Sex difference in the oxidative metabolism of delta 9-tetrahydrocannabinol in the rat. Biochem. Pharmacol. 1991, 41:1187-1194.
90. Navarro M., Fernandez-Ruiz J.J., de Miguel R., Hernandez M.L., Cebeira M., Ramos J.A. An acute dose of delta 9-tetrahydrocannabinol affects behavioral and neurochemical indices of mesolimbic dopaminergic activity. Behav. Brain Res. 1993, 57:37-46.
91. Nguyen Q.H., Wagner E.J. Estrogen differentially modulates the cannabinoid- induced presynaptic inhibition of amino acid neurotransmission in proopiomelanocortin neurons of the arcuate nucleus. Neuroendocrinology 2006, 84:123-137.
92. Nir I., Ayalon D., Tsafriri A., Cordova T., Lindner H.R. Letter: Suppression of the cyclic surge of luteinizing hormone secretion and of ovulation in the rat by delta 1-tetrahydrocannabinol. Nature 1973, 243:470-471.
93. Ohno-Shosaku T., Tsubokawa H., Mizushima I., Yoneda N., Zimmer A., Kano M. Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses. J. Neurosci. 2002, 22:3864-3872.
94. Ojeda S.R., Roth C., Mungenast A., Heger S., Mastronardi C., Parent A.S., Lomniczi A., Jung H. Neuroendocrine mechanisms controlling female puberty: new approaches, new concepts. Int. J. Androl. 2006, 29:256-263. discussion 286-90.
95. Onaivi E.S., Chaudhuri G., Abaci A.S., Parker M., Manier D.H., Martin P.R., Hubbard J.R. Expression of cannabinoid receptors and their gene transcripts in human blood cells. Prog. Neuropsychopharmacol. Biol. Psychiatry 1999, 23:1063-1077.
96. 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., Uhl G.R. Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain. Ann. N.Y. Acad. Sci. 2006, 1074:514-536.
97. Ong W.Y., Mackie K. A light and electron microscopic study of the CB1 cannabinoid receptor in primate brain. Neuroscience 1999, 92:1177-1191.
98. Pagotto U., Marsicano G., Fezza F., Theodoropoulou M., Grubler Y., Stalla J., Arzberger T., Milone A., Losa M., Di Marzo V., Lutz B., Stalla G.K. Normal human pituitary gland and pituitary adenomas express cannabinoid receptor type 1 and synthesize endogenous cannabinoids: first evidence for a direct role of cannabinoids on hormone modulation at the human pituitary level. J. Clin. Endocrinol. Metab. 2001, 86:2687-2696.
99. Pagotto U., Marsicano G., Cota D., Lutz B., Pasquali R. The emerging role of the endocannabinoid system in endocrine regulation and energy balance. Endocr. Rev. 2006, 27:73-100.
100. Paredes R.G., Vazquez B. What do female rats like about sex? Paced mating. Behav. Brain. Res. 1999, 105:117-127.
101. Paredes R.G., Agmo A. Has dopamine a physiological role in the control of sexual behavior? A critical review of the evidence. Prog. Neurobiol. 2004, 73:179-226.
102. Park B., McPartland J.M., Glass M. Cannabis, cannabinoids and reproduction. Prostaglandins Leukot. Essent. Fat. Acids 2004, 70:189-197.
103. Patel S., Hillard C.J. Pharmacological evaluation of cannabinoid receptor ligands in a mouse model of anxiety: further evidence for an anxiolytic role for endogenous cannabinoid signaling. J. Pharmacol. Exp. Ther. 2006, 318:304-311.
104. Pertwee R.G. Pharmacology of cannabinoid CB1 and CB2 receptors. Pharmacol. Ther. 1997, 74:129-180.
105. Pertwee R.G. The pharmacology of cannabinoid receptors and their ligands: an overview. Int. J. Obes. (Lond) 2006, 30(Suppl 1):S13-18.
106. Pertwee R.G., Ross R.A. Cannabinoid receptors and their ligands. Prostaglandins Leukot. Essent. Fat. Acids 2002, 66:101-121.
107. Piomelli D., Tarzia G., Duranti A., Tontini A., Mor M., Compton T.R., Dasse O., Monaghan E.P., Parrott J.A., Putman D. Pharmacological profile of the selective FAAH inhibitor KDS-4103 (URB597). CNS Drug Rev. 2006, 12:21-38.
108. Plant T.M., Barker-Gibb M.L. Neurobiological mechanisms of puberty in higher primates. Hum. Reprod. Updat. 2004, 10:67-77.
109. Puder M., Nir I., Siegel R.A., Weidenfeld J., Ayalon D. The effect of delta 1tetrahydrocannabinol on luteinizing hormone release in castrated and hypothalamic deafferented male rats. Exp. Brain Res. 1985, 59:213-216.
110. Robinson T.E., Berridge K.C. Review. The incentive sensitization theory of addiction: some current issues. Philos. Trans. R. Soc. Lond., B Biol. Sci. 2008, 363:3137-3146.
111. Rodríguez de Fonseca F., Fernández-Ruiz J.J., Murphy L.L., Cebeira M., Steger R.W., Bartke A., Ramos J.A. Acute effects of delta-9-tetrahydrocannabinol on dopaminergic activity in several rat brain areas. Pharmacol. Biochem. Behav. 1992, 42:269-275.
112. Rodríguez de Fonseca F., Cebeira M., Ramos J.A., Martin M., Fernández-Ruiz J.J. Cannabinoid receptors in rat brain areas: sexual differences, fluctuations during estrous cycle and changes after gonadectomy and sex steroid replacement. Life Sci. 1994, 54:159-170.
113. Rodríguez de Fonseca F., Wenger T., Navarro M., Murphy L.L. Effects of delta9-THC on VIP-induced prolactin secretion in anterior pituitary cultures: evidence for the presence of functional cannabinoid CB1 receptors in pituitary cells. Brain Res. 1999, 841:114-122.
114. Roth M.E., Cosgrove K.P., Carroll M.E. Sex differences in the vulnerability to drug abuse: a review of preclinical studies. Neurosci. Biobehav. Rev. 2004, 28:533-546.
115. Ruiu S., Pinna G.A., Marchese G., Mussinu J.M., Saba P., Tambaro S., Casti P., Vargiu R., Pani L. Synthesis and characterization of NESS 0327: a novel putative antagonist of the CB1 cannabinoid receptor. J. Pharmacol. Exp. Ther. 2003, 306:363-370.
116. Samat A., Tomlinson B., Taheri S., Thomas G.N. Rimonabant for the treatment of obesity. Recent. Pat. Cardiovasc. Drug Discov. 2008, 3:187-193.
117. Sanford A.E., Castillo E., Gannon R.L. Cannabinoids and hamster circadian activity rhythms. Brain Res. 2008, 1222:141-148.
118. Scorticati C., Mohn C., De Laurentiis A., Vissio P., Fernandez Solari J., Seilicovich A., McCann S.M., Rettori V. The effect of anandamide on prolactin secretion is modulated by estrogen. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:2134-2139.
119. Scorticati C., Fernandez-Solari J., De Laurentiis A., Mohn C., Prestifilippo J.P., Lasaga M., Seilicovich A., Billi S., Franchi A., McCann S.M., Rettori V. The inhibitory effect of anandamide on luteinizing hormone-releasing hormone secretion is reversed by estrogen. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:11891-11896.
120. Shrenker P., Bartke A. Suppression of male copulatory behavior by delta 9-THC is not dependent on changes in plasma testosterone or hypothalamic dopamine or serotonin content. Pharmacol. Biochem. Behav. 1985, 22:415-420.
121. Smith C.G., Besch N.F., Smith R.G., Besch P.K. Effect of tetrahydrocannabinol on the hypothalamic-pituitary axis in the ovariectomized rhesus monkey. Fertil. Steril. 1979, 31:335-339.
122. Solinas M., Goldberg S.R., Piomelli D. The endocannabinoid system in brain reward processes. Br. J. Pharmacol. 2008, 154:369-383.
123. Steger R.W., Silverman A.Y., Siler-Khodr T.M., Asch R.H. The effects of delta 9-tetrahydrocannabinol on the positive and negative feedback control of luteinizing hormone release. Life Sci. 1980, 27:1911-1916.
124. Steger R.W., DePaolo L., Asch R.H., Silverman A.Y. Interactions of delta 9-tetrahydrocannabinol (THC) with hypothalamic neurotransmitters controlling luteinizing hormone and prolactin release. Neuroendocrinology 1983, 37:361-370.
125. Succu S., Mascia M.S., Sanna F., Melis T., Argiolas A., Melis M.R. The cannabinoid CB1 receptor antagonist SR 141716A induces penile erection by increasing extra-cellular glutamic acid in the paraventricular nucleus of male rats. Behav. Brain Res. 2006, 169:274-281.
126. Sugiura T., Kondo S., Sukagawa A., Nakane S., Shinoda A., Itoh K., Yamashita A., Waku K. 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem. Biophys. Res. Commun. 1995, 215:89-97.
127. Szabo B., Schlicker E. Effects of cannabinoids on neurotransmission. Handb. Exp. Pharmacol. 2005, 327-365.
128. Thomasson H.R. Gender differences in alcohol metabolism. Physiological responses to ethanol. Recent Dev. Alcohol. 1995, 12:163-179.
129. Tseng A.H., Craft R.M. Sex differences in antinociceptive and motoric effects of cannabinoids. Eur. J. Pharmacol. 2001, 430:41-47.
130. Tseng A.H., Craft R.M. CB(1) receptor mediation of cannabinoid behavioral effects in male and female rats. Psychopharmacology. (Berl) 2004, 172:25-30.
131. Turley W.A., Floody O.R. Delta-9-tetrahydrocannabinol stimulates receptive and proceptive sexual behaviors in female hamsters. Pharmacol. Biochem. Behav. 1981, 14:745-747.
132. Viveros M.P., Llorente R., Moreno E., Marco E.M. Behavioural and neuroendocrine effects of cannabinoids in critical developmental periods. Behav. Pharmacol. 2005, 16:353-362.
133. Viveros M.P., Marco E.M., File S.E. Endocannabinoid system and stress and anxiety responses. Pharmacol. Biochem. Behav. 2005, 81:331-342.
134. Waleh N.S., Cravatt B.F., Apte-Deshpande A., Terao A., Kilduff T.S. Transcriptional regulation of the mouse fatty acid amide hydrolase gene. Gene 2002, 291:203-210.
135. Wenger T., Rettori V., Snyder G.D., Dalterio S., McCann S.M. Effects of delta-9-tetrahydrocannabinol on the hypothalamic-pituitary control of luteinizing hormone and follicle-stimulating hormone secretion in adult male rats. Neuroendocrinology 1987, 46:488-493.
136. Wenger T., Fernandez-Ruiz J.J., Ramos J.A. Immunocytochemical demonstration of CB1 cannabinoid receptors in the anterior lobe of the pituitary gland. J. Neuroendocrinol. 1999, 11:873-878.
137. Wenger T., Jamali K.A., Juaneda C., Bacsy E., Tramu G. The endogenous cannabinoid, anandamide regulates anterior pituitary secretion in vitro. Addict. Biol. 2000, 5:59-64.
138. Wenger T., Gerendai I., Fezza F., Gonzalez S., Bisogno T., Fernandez-Ruiz J., Di Marzo V. The hypothalamic levels of the endocannabinoid, anandamide, peak immediately before the onset of puberty in female rats. Life Sci. 2002, 70:1407-1414.
139. Wiley J.L., Barrett R.L., Lowe J., Balster R.L., Martin B.R. Discriminative stimulus effects of CP 55,940 and structurally dissimilar cannabinoids in rats. Neuropharmacology 1995, 34:669-676.
140. Wise R.A. Drug-activation of brain reward pathways. Drug Alcohol Depend 1998, 51:13-22.
141. Xiao L., Becker J.B. Hormonal activation of the striatum and the nucleus accumbens modulates paced mating behavior in the female rat. Horm. Behav. 1997, 32:114-124.
142. Zangen A., Solinas M., Ikemoto S., Goldberg S.R., Wise R.A. Two brain sites for cannabinoid reward. J. Neurosci. 2006, 26:4901-4907.