Male and female rats differ in brain cannabinoid CB1 receptor density and function and in behavioural traits predisposing to drug addiction: Effect of ovarian hormones

Current Pharmaceutical Design

Volumn 20, Issue 13, 2014, Pages 2100-2113

  Castelli, Maria Paola ^a   Fadda, Paola ^a   Casu, Angelo ^a   Spano, Maria Sabrina ^b   Casti, Alberto ^a   Fratta, Walter ^a   Fattore, Liana ^a,b  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b CNR   (Italy)

Author keywords

Anxiety; Locomotor activity; Oestrogen; Ovariectomy; Prepulse inhibition; Sex difference; Social interaction

Indexed keywords

CANNABINOID; CANNABINOID 1 RECEPTOR; ESTROGEN;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTORADIOGRAPHY; BEHAVIOR DISORDER; CANNABIS ADDICTION; CONTROLLED STUDY; ESTRUS CYCLE; FEMALE; HIPPOCAMPUS; LOCOMOTION; MALE; MOTOR ACTIVITY; NONHUMAN; NUCLEUS ACCUMBENS; OVARIECTOMY; PREFRONTAL CORTEX; PREPULSE INHIBITION; PRIORITY JOURNAL; RAT; SENSORY GATING; SEX DIFFERENCE; SOCIAL BEHAVIOR; SOCIAL INTERACTION; STARTLE REFLEX; ANIMAL; BRAIN; DRUG EFFECTS; PHYSIOLOGY; SEXUAL DEVELOPMENT; SOCIAL ADAPTATION; SUBSTANCE-RELATED DISORDERS;

ANIMALS; BRAIN; ESTROGENS; FEMALE; MALE; MOTOR ACTIVITY; OVARIECTOMY; RATS; RECEPTOR, CANNABINOID, CB1; REFLEX, STARTLE; SEX CHARACTERISTICS; SOCIAL SKILLS; SUBSTANCE-RELATED DISORDERS;

EID: 84903692628     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/13816128113199990430     Document Type: Article

References (140)

1. Eriksson K. Genetic selection for voluntary alcohol consumption in albino rats. Science 1968; 159: 739-40.
2. Eriksson K, Pikkarainen PH. Differences between the sexes in voluntary alcohol consumption and liver ADH-activity in inbred strains of mice. Metabolism 1968; 17: 1037-42.
3. Heppner CC, Kemble ED, Cox MD. Effects of food deprivation on caffeine consumption in male and female rats. Pharmacol Biochem Behav 1986; 24: 1555-9.
4. Matthews KM, Robbins TW, Everitt BJ, Caine SB. Repeated maternal separation alters intravenous cocaine self-administration in rats. Psychopharmacology 1999; 141: 123-4.
5. Morse AC, Erwin VG, Jones. Strain and housing affect cocaine self-selection and open-field locomotor activity in mice. Pharmacol Biochem Behav 1993; 4: 905-12.
6. Carroll ME, Campbell UC, Heideman P. Ketoconazole inhibits food-restriction induced increases in i.v. heroin self-administration in rats: sex differences. Exp Clin Psychopharm 2001; 9: 307-16.
7. Alexander BK, Coambs RB, Hadaway PF. The effect of housing and gender on morphine self-administration in rats. Psychopharmacology 1978; 58: 175-9.
8. Hill SY, Powell BJ. Cocaine and morphine self-administration: effects of differential nose poke. Pharmacol Biochem Behav 1976; 5: 701-4.
9. Klein LC, Popke JE, Grunberg NE. Sex differences in effects of predictable and unpredictable footshock on fentanyl selfadministrationinrats. Exp Clin Psychopharmacol 1997; 5: 99-106.
10. Silverman JL, Koenig JI. Evidence for the involvement of ERbeta and RGS9-2 in 17-beta estradiol enhancement of amphetamineinduced place preference behavior. Horm Behav 2007; 52: 146-55.
11. Segarra AC, Agosto-Rivera JL, Febo M, et al. Estradiol: A key biological substrate mediating the response to cocaine in female rats. Horm Behav 2010; 58: 33-43.
12. United Nation Office on Drugs and Crime (UNODC). World Drug Report 2011 2011; 933: 175-93.
13. Levin KH, Copersino ML, Heishman SJ, et al. Cannabis withdrawal symptoms in non-treatment-seeking adult cannabis smokers. Drug Alcohol Depend 2010; 111: 120-7.
14. Filbey FM, Schacht JP, Myers US, Chavez RS, Hutchison KE. Marijuana craving in the brain. Proc Natl Acad Sci USA 2009; 106: 13016-21.
15. EMCDDA, European Monitoring Centre for Drugs and Drug Addiction. Differences in patterns of drug use between women and men 2005; 2-4.
16. Mello NK, Mendelson JH. Operant acquisition of marihuana by women. J Pharmacol Exp Ther 1985; 235: 162-71.
17. Filbey FM, Schacht JP, Myers US, Chavez RS, Hutchison KE. Individual and additive effects of the CNR1 and FAAH genes on brain response to marijuana cues. Neuropsychopharmacology 2010; 35: 967-75.
18. Gruber SA, Rogowska J, Yurgelun-Todd DA. Altered affective response in marijuana smokers: an FMRI study. Drug Alcohol Depend 2009; 105: 139-53.
19. Fattore L, Fadda P, Fratta W. Sex differences in the selfadministration of cannabinoids and other drugs of abuse. Psychoneuroendocrinology 2009; 1: S227-36.
20. Fattore L, Fratta W. How important are sex differences in cannabinoid action? Br J Pharmacol 2010; 160: 544-8.
21. López HH. Cannabinoid-hormone interactions in the regulation of motivational processes. Horm Behav 2010; 58: 100-10.
22. Burston JJ, Wiley JL, Craig AA, Selley DE, Sim-Selley LJ. Regional enhancement of cannabinoid CB1 receptor desensitization in female adolescent rats following repeated Deltatetrahydrocannabinol exposure. Br J Pharmacol 2010; 161: 103-12.
23. Rubino T, Vigano' D, Realini N, et al. Chronic delta 9-tetrahydrocannabinol during adolescence provokes sex-dependent changes in the emotional profile in adult rats: behavioral and biochemical correlates. Neuropsychopharmacology 2008; 33: 2760-71.
24. Fattore L, Viganò D, Fadda P, Rubino T, Fratta W, Parolaro D. Bidirectional regulation of mu-opioid and CB1-cannabinoid receptor in rats self-administering heroin or WIN 55,212-2. Eur J Neurosci 2007; 25: 2191-200.
25. Fattore L, Spano MS, 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.
26. Fattore L, Spano MS, Altea S, Fadda P, Fratta W. Drug-and cueinduced reinstatement of cannabinoid-seeking behaviour in male and female rats: influence of ovarian hormones. Br J Pharmacol 2010; 160: 724-35.
27. Koethe D, Llenos IC, Dulay JR, et al. Expression of CB1 cannabinoid receptor in the anterior cingulate cortex in schizophrenia, bipolar disorder, and major depression. J Neural Transm 2007; 114: 1055-63.
28. Vinod KY, Arango V, Xie S, et al. Elevated levels of endocannabinoids and CB1 receptor-mediated G-protein signaling in the prefrontal cortex of alcoholic suicide victims. Biol Psychiatry 2005; 57: 480-6.
29. Hungund BL, Vinod KY, Kassir SA, et al. Upregulation of CB1 receptors and agonist-stimulated [35S]GTPgammaS binding in the prefrontal cortex of depressed suicide victims. Mol Psychiatry 2004; 9: 184-90.
30. Castelli MP, Paola Piras A, D'Agostino A, et al. Dysregulation of the endogenous cannabinoid system in adult rats prenatally treated with the cannabinoid agonist WIN 55,212-2. Eur J Pharmacol 2007; 573: 11-9.
31. Mateos B, Borcel E, Loriga R, et al. Adolescent exposure to nicotine and/or the cannabinoid agonist CP 55,940 induces genderdependent long-lasting memory impairments and changes in brain nicotinic and CB(1) cannabinoid receptors. J Psychopharmacol 2011; 25: 1676-90.
32. Wiley JL, Kendler SH, Burston JJ, Howard DR, Selley DE, Sim-Selley LJ. Antipsychotic-induced alterations in CB1 receptormediated G-protein signaling and in vivo pharmacology in rats. Neuropharmacology 2008; 55: 1183-90.
33. Van Laere K, Goffin K, Casteels C, et al. Gender-dependent increases with healthy aging of the human cerebral cannabinoid-type 1 receptor binding using [(18)F]MK-9470 PET. Neuroimage 2008; 39: 1533-41.
34. Rodríguez de Fonseca F, Cebeira M, Ramos JA, Martín M, Fernández-Ruiz JJ. Cannabinoid receptors in rat brain areas: sexual differences, fluctuations during estrous cycle and changes after gonadectomy and sex steroid replacement. Life Sci 1994; 54: 159-70.
35. González S, Bisogno T, Wenger T, et al. Sex steroid influence on cannabinoid CB(1) receptor mRNA and endocannabinoid levels in the anterior pituitary gland. Biochem Biophys Res Commun 2000; 270: 260-6.
36. Riebe CJ, Hill MN, Lee TT, Hillard CJ, Gorzalka BB. Estrogenic regulation of limbic cannabinoid receptor binding. Psychoneuroendocrinology 2010; 35: 1265-9.
37. Fattore L, Cossu G, Martellotta CM, Fratta W. Intravenous selfadministration of the cannabinoid CB1 receptor agonist WIN 55,212-2 in rats. Psychopharmacology 2001; 156: 410-6.
38. Deiana S, Fattore L, Spano MS, et al. Strain and scheduledependent differences in the acquisition, maintenance and extinction of intravenous cannabinoid self-administration in rats. Neuropharmacology 2007; 52: 646-54.
39. Spano MS, Fattore L, Cossu G, Deiana S, Fadda P, Fratta W. CB1 receptor agonist and heroin, but not cocaine, reinstate cannabinoidseeking behaviour in the rat. Br J Pharmacol 2004; 143: 343-50.
40. Winsauer PJ, Daniel JM, Filipeanu CM, et al. Long-term behavioral and pharmacodynamic effects of delta-9-tetrahydrocannabinol in female rats depend on ovarian hormone status. Addict Biol 2011; 16: 64-81.
41. Piazza PV, Deminiere JM, Le Moal M, Simon H. Factors that predict individual vulnerability to amphetamine self-administration. Science 1989; 245: 1511-3.
42. Piazza PV, Deminiere JM, Le Moal M, Simon H. Stress-and pharmacologically-induced behavioural sensitization increases vulnerabilità to acquisition of amphetamine self-administration. Brain Res 1990; 514: 22-6.
43. Koob GF, Le Moal M. Neurobiological mechanisms for opponent motivational processes in addiction. Philos Trans R Soc Lond B Biol Sci 2008; 363: 3113-23.
44. Kushner MG, Maurer E, Menary K, Thuras P. Vulnerability to the rapid (telescoped) development of alcohol dependence in individuals with anxiety disorder. J Stud Alcohol Drugs 2011; 72: 1019-27.
45. Evans SM, Foltin RW. Does the response to cocaine differ as a function of sex or hormonal status in human and non-human primates? Horm Behav 2010; 58: 13-21.
46. Quinones-Jenab V. Why are women from Venus and men from Mars when they abuse cocaine? Brain Res 2006; 1126: 200-3.
47. Milesi-Hallé A, McMillan DE, Laurenzana EM, Byrnes-Blake KA, Owens SM. Sex differences in (+)-amphetamine-and (+)-methamphetamine-induced behavioral response in male and female Sprague-Dawley rats. Pharmacol Biochem Behav 2007; 86: 140-9.
48. Davis BA, Clinton SM, Akil H, Becker JB. The effects of noveltyseeking phenotypes and sex differences on acquisition of cocaine self-administration in selectively bred High-Responder and Low-Responder rats. Pharmacol Biochem Behav 2008; 90: 331-8.
49. Buckner JD, Schmidt NB. Social anxiety disorder and marijuana use problems: the mediating role of marijuana effect expectancies. Depress Anxiety 2009; 26: 864-70.
50. Buckner JD, Mallott MA, Schmidt NB, Taylor J. Peer influence and gender differences in problematic cannabis use among individuals with social anxiety. J Anxiety Disord 2006; 20: 1087-102.
51. La Greca AM, Lopez N. Social anxiety among adolescents: linkages with peer relations and friendships. J Abnorm Child Psychol 1998; 26: 83-94.
52. Hutchison KE, Rohsenow D, Monti P, Palfai T, Swift R. Prepulse inhibition of the startle reflex: preliminary study of the effects of a low dose of alcohol in humans. Alcohol Clin Exp Res 1997; 21: 1312-9.
53. Grillon C, Sinha R, Ameli R, O'Malley SS. Effects of alcohol on baseline startle and prepulse inhibition in young men at risk for alcoholism and/or anxiety disorders. J Stud Alcohol 2000; 61: 46-54.
54. Kumari V, Gray JA. Smoking withdrawal, nicotine dependence and prepulse inhibition of the acoustic startle reflex. Psychopharmacology 1999; 141: 11-5.
55. Swerdlow NR, Eastvold A, Gerbranda T, et al. Effects of caffeine on sensorimotor gating of the startle reflex in normal control subjects: impact of caffeine intake and withdrawal. Psychopharmacology 2000; 151: 368-78.
56. Adams JU, Efferen TR, Duncan EJ, Rotrosen J. Prepulse inhibition of the acoustic startle response in cocaine-withdrawn rats. Pharmacol Biochem Behav 2001; 68: 753-9.
57. Martin RS, Secchi RL, Sung E, et al. Effects of cannabinoid receptor ligands on psychosis-relevant behavior models in the rat. Psychopharmacology 2003; 165: 128-35.
58. Ballmaier M, Bortolato M, Rizzetti C, Zoli M, Gessa G, Heinz A, Spano P. Cannabinoid receptor antagonists counteract sensorimotor gating deficits in the phencyclidine model of psychosis. Neuropsychopharmacology 2007; 32: 2098-107.
59. Graham FK. The more or less startling effects of weak prestimulation. Psychophysiology 1975; 12: 238-48.
60. Rabinowitz J, Bromet EJ, Lavelle J, Carlson G, Kovasznay B, Schwartz JE. Prevalence and severity of substance use disorders and onset of psychosis in first-admission psychotic patients. Psychol Med 1998; 28: 1411-9.
61. Dubertret C, Bidard I, Adès J, Gorwood P. Lifetime positive symptoms in patients with schizophrenia and cannabis abuse are partially explained by co-morbid addiction. Schizophr Res 2006; 86: 284-90.
62. Koskinen J, Löhönen J, Koponen H, Isohanni M, Miettunen J. Rate of cannabis use disorders in clinical samples of patients with schizophrenia: a meta-analysis. Schizophr Bull 2010; 36: 1115-30.
63. Køster A, Lajer M, Lindhardt A, Rosenbaum B. Gender differences in first episode psychosis. Soc Psychiatry Psychiatr Epidemiol 2008; 43: 940-6.
64. Llorente-Berzal A, Fuentes S, Gagliano H, et al. Sex-dependent effects of maternal deprivation and adolescent cannabinoid treatment on adult rat behaviour. Addict Biol 2011; 16: 624-37.
65. Harte-Hargrove LC, Dow-Edwards DL. Withdrawal from THC during adolescence: Sex differences in locomotor activity and anxiety. Behav Brain Res 2012; 231: 48-59.
66. Walf AA, Frye CA. Antianxiety and antidepressive behavior produced by physiological estradiol regimen may be modulated by hypothalamic- pituitary-adrenal axis activity. Neuropsychopharmacology 2005; 30: 1288-301.
67. Hill MN, Karacabeyli ES, Gorzalka BB. Estrogen recruits the endocannabinoid system to modulate emotionality. Psychoneuroendocrinology 2007; 32: 350-7.
68. Kellert BA, Nguyen MC, Nguyen C, Nguyen QH, Wagner EJ. Estrogen rapidly attenuates cannabinoid-induced changes in energy homeostasis. Eur J Pharmacol 2009; 622: 15-24.
69. López HH, Webb SA, Nash S. Cannabinoid receptor antagonism increases female sexual motivation. Pharmacol Biochem Behav 2009; 92: 17-24.
70. Peris J, Decambre CH, Coleman-Hardee ML, Simpkins JW. Estradiol enhances behavioral sensitization to cocaine and amphetamine-stimulated striatal [3H] dopamine release. Brain Res 1991; 566: 255-64.
71. Paxinos G, Watson C. The rat brain in Stereotaxic Coordinates. 3rd Ed., 1997; San Diego: Academic Press.
72. Castelli MP, Piras AP, Melis T, et al. Cannabinoid CB1 receptors in the paraventricular nucleus and central control of penile erection: immunocytochemistry, autoradiography and behavioral studies. Neuroscience 2007; 147: 197-206.
73. Spano MS, Fadda P, Frau R, Fattore L, Fratta W. Cannabinoid selfadministration attenuates PCP-induced schizophrenia-like symptoms in adult rats. Eur Neuropsychopharmacol 2010; 20: 25-36.
74. Swerdlow NR, Geyer MA. Using an animal model of deficient sensorimotor gating to study the pathophysiology and new treatments of schizophrenia. Schizophr Bull 1998; 24: 285-301.
75. Becker JB. Sexual differentiation of motivation: A novel mechanism? Hormones and Behavior 2009; 55: 646-54.
76. Van Etten ML, Anthony JC. Male-female differences in transitions from first drug opportunity to first use: Searching for subgroup variation by age, race, region, and urban status. J Women's Health Gen Bas Med 2001; 10: 797-804.
77. Redolat R, Pérez-Martínez A, Carrasco MC, Mesa P. Individual differences in novelty-seeking and behavioral responses to nicotine: a review of animal studies. Curr Drug Abuse Rev 2009; 2: 230-42.
78. Batel P. Addiction and schizophrenia. Eur Psychiatry 2000; 15: 115-22.
79. Chambers RA, Krystal JH, Self DW. A neurobiological basis for substance abuse comorbidity in schizophrenia. Biol Psychiatry 2001; 5: 71-83.
80. Reich CG, Taylor ME, McCarthy MM. Differential effects of chronic unpredictable stress on hippocampal CB1 receptors in male and female rats. Behav Brain Res 2009; 203: 264-9.
81. Perry JL, Joseph JE, Jiang Y, et al. Prefrontal cortex and drug abuse vulnerability: translation to prevention and treatment interventions. Brain Res Rev 2011; 65: 124-49.
82. Gruber SA, Yurgelun-Todd DA. Neuroimaging of marijuana smokers during inhibitory processing: a pilot investigation. Brain Res Cogn Brain Res 2005; 23: 107-18.
83. Krebs-Kraft DL, Hill MN, Hillard CJ, McCarthy MM. Sex difference in cell proliferation in developing rat amygdala mediated by endocannabinoids has implications for social behavior. Proc Natl Acad Sci USA 2010; 107: 20535-40.
84. Van Laere K, Goffin K, Bormans G, et al. Relationship of type 1 cannabinoid receptor availability in the human brain to noveltyseeking temperament. Arch Gen Psychiatry 2009; 66: 196-204.
85. Kelly TH, Robbins G, Martin CA, et al. Individual differences in drug abuse vulnerability: d-amphetamine and sensation-seeking status. Psychopharmacology 2006; 189: 17-25.
86. Bardo MT, Donohew RL, Harrington NG. Psychobiology of novelty seeking and drug seeking behavior. Behav Brain Res 1996; 77: 23-43.
87. Hale RL, Whiteman S, Muehl K, Faynberg E. Tridimensional personality traits of college student marijuana users. Psychol Rep 2003; 92: 661-6.
88. Wills TA, Vaccaro D, McNamara G. Novelty seeking, risk taking, and related constructs as predictors of adolescent substance use: an application of Cloninger's theory. J Subst Abuse 1994; 6: 1-20.
89. Chen JP, Paredes W, Lowinson JH, Gardner EL. Strain-specific facilitation of dopamine efflux by delta 9-tetrahydrocannabinol in the nucleus accumbens of rat: an in vivo microdialysis study. Neurosci Lett 1991; 129: 136-80.
90. Mize AL, Alper RH. Acute and long-term effects of 17betaestradiol on G(i/o) coupled neurotransmitter receptor function in the female rat brain as assessed by agonist-stimulated [35S]GTPgammaS binding. Brain Res 2000; 859: 326-33.
91. Giordano M, Mejía-Viggiano MC. Gender differences in spontaneous and MK-801-induced activity after striatal lesions. Brain Res Bull 2001; 56: 553-61.
92. Bethancourt JA, Vásquez CE, Britton GB. Sex-dependent effects of long-term oral methylphenidate treatment on spontaneous and learned fear behaviors. Neurosci Lett 2011; 496: 30-4.
93. Takase K, Kimura F, Yagami T, Mitsushima D. Sex-specific 24-h acetylcholine release profile in the medial prefrontal cortex: simultaneous measurement of spontaneous locomotor activity in behaving rats. Neuroscience 2009; 159: 7-15.
94. Cailhol S, Mormède P. Strain and sex differences in the locomotor response and behavioral sensitization to cocaine in hyperactive rats. Brain Res 1999; 842: 200-5.
95. Belin D, Berson N, Balado E, Piazza PV, Deroche-Gamonet V. High-novelty-preference rats are predisposed to compulsive cocaine self-administration. Neuropsychopharmacology 2011; 36: 569-79.
96. Becker JB, Hu M. Sex differences in drug abuse. Front Neuroendocrinol 2008; 29: 36-47.
97. Lynch WJ. Sex differences in vulnerability to drug selfadministration. Exp Clin Psychopharmacol 2006; 14: 34-41.
98. Roth ME, Cosgrove KP, Carroll ME. Sex differences in the vulnerability to drug abuse: a review of preclinical studies. Neurosci Biobehav Rev 2004; 28: 533-46.
99. Becker JB. Estrogen rapidly potentiates amphetamine-induced striatal dopamine release and rotational behavior during microdialysis. Neurosci Lett 118; 1990: 169-71.
100. McDermott JL. Effects of estrogen upon dopamine release from the corpus striatum of young and aged female rats, Brain Res 1993; 606: 118-25.
101. Thompson TL, Moss RL. Estrogen regulation of dopamine release in the nucleus accumbens: genomic and nongenomic-mediated effects. J Neurochem 1994; 62: 1750-6.
102. Di Paolo T, Rouillard C, Berndard P. 17Beta-estradiol at a physiological dose acutely increases dopamine turnover in rat brain. Eur J Pharmacol 1985; 117: 197-203.
103. Renard GM, Suárez MM, Levin GM, Rivarola MA. Sex differences in rats: effects of chronic stress on sympathetic system and anxiety. Physiol Behav 2005; 85: 363-9.
104. Sullivan RM, Duchesne A, Hussain D, Waldron J, Laplante F. Effects of unilateral amygdala dopamine depletion on behaviour in the elevated plus maze: role of sex, hemisphere and retesting. Behav Brain Res 2009; 205: 115-22.
105. Verma P, Hellemans KG, Choi FY, Yu W, Weinberg J. Circadian phase and sex effects on depressive/anxiety-like behaviors and HPA axis responses to acute stress. Physiol Behav 2010; 99: 276-85.
106. File SE. Behavioural detection of anxiolytic action. In: Elliott JM, Heal DJ, Marsden CA, Eds. Experimental approaches to anxiety and depression. London, John Wiley, 1992; 25-44.
107. Koss WA, Gehlert DR, Shekhar A. Different effects of subchronic doses of 17-beta estradiol in two ethologically based models of anxiety utilizing female rats. Horm Behav 2004; 46: 158-64.
108. Diaz-Veliz G, Butron S, Benavides MS, Dussaubat N, Mora N. Gender, estrous cycle, ovariectomy, and ovarian hormones influence the effects of diazepam on avoidance conditioning in rats. Pharmacol Biochem Behav 2000; 66: 887-92.
109. Martínez-Mota L, Estrada-Camarena E, López-Rubalcava C, Contreras CM, Fernández-Guasti A. Interaction of desipramine with steroid hormones on experimental anxiety. Psychoneuroendocrinology 2000; 25: 109-20.
110. Nomikos GG, Spyraki C. Influence of oestrogen on spontaneous and diazepam-induced exploration of rats in an elevated plus maze. Neuropharmacology 1988; 27: 691-6.
111. McCarthy MM. Estrogen modulation of oxytocin and its relation to behavior. Adv Exp Med Biol. 1995; 395: 235-45.
112. Rodriguez-Sierra JF, Howard JL, Pollard GT, Hendricks SE. Effect of ovarian hormones on conflict behavior. Psychoneuroendocrinology 1984; 9: 293-300.
113. Morgan MA, Pfaff DW. Estrogen's effects on activity, anxiety, and fear in two mouse strains. Behav Brain Res 2002; 132: 85-93.
114. Boutros NN, Korzyukov O, Jansen B, Feingold A, Bell M. Sensory gating deficits during the mid-latency phase of information processing in medicated schizophrenia patients. Psychiatry Res 2004; 126: 203-15.
115. Plappert CF, Rodenbucher AM, Pilz PK. Effects of sex and estrous cycle on modulation of the acoustic startle response in mice. Physiol Behav 2005; 84: 585-94.
116. Kinkead B, Yan F, Owens MJ, Nemeroff CB. Endogenous neurotensin is involved in estrous cycle related alterations in prepulse inhibition of the acoustic startle reflex in female rats. Psychoneuroendocrinology 2008; 33: 178-87.
117. Koch M. Sensorimotor gating changes across the estrous cycle in female rats. Physiol Behav 1998; 64: 625-8.
118. D'Souza DC, Sewell RA, Ranganathan M. Cannabis and psychosis/ schizophrenia: human studies. Eur Arch Psychiatry Clin Neurosci 2009; 259: 413-31.
119. Pelayo-Terán JM, Pérez-Iglesias R, Mata I, et al. Catechol-OMethyltransferase (COMT) Val158Met variations and cannabis use in first-episode non-affective psychosis: clinical-onset implications. Psychiatry Res 2010; 179: 291-6.
120. Bhattacharyya S, Atakan Z, Martin-Santos R, et al. Preliminary report of biological basis of sensitivity to the effects of cannabis on psychosis: AKT1 and DAT1 genotype modulates the effects of δ-9-tetrahydrocannabinol on midbrain and striatal function. Mol Psychiatry 2012; 17: 1152-5.
121. Di Forti M, Iyegbe C, Sallis H, et al. Confirmation that the AKT1 (rs2494732) Genotype Influences the Risk of Psychosis in Cannabis Users. Biol Psychiatry 2012; 72: 811-6.
122. Caspi A, Moffitt TE, Cannon M, et al. Moderation of the effect of adolescent-onset cannabis use on adult psychosis by a functional polymorphism in the catechol-O-methyltransferase gene: longitudinal evidence of a gene X environment interaction. Biol Psychiatry 2005; 57: 1117-27.
123. Zammit S, Spurlock G, Williams H, et al. Genotype effects of CHRNA7, CNR1 and COMT in schizophrenia: interactions with tobacco and cannabis use. Br J Psychiatry 2007; 191: 402-7.
124. van Winkel R. Genetic Risk and Outcome of Psychosis (GROUP) Investigators. Family-based analysis of genetic variation underlying psychosis-inducing effects of cannabis: sibling analysis and proband follow-up. Arch Gen Psychiatry 2011; 68: 148-57.
125. Fattore L. Considering gender in cannabinoid research: A step towards personalized treatment of marijuana addicts. Drug Test Anal 2012 Aug 11. doi: 10.1002/dta.1401.
126. Häring M, Guggenhuber S, Lutz B. Neuronal populations mediating the effects of endocannabinoids on stress and emotionality. Neuroscience 2012; 204: 145-58.
127. McLaughlin RJ, Gobbi G. Cannabinoids and emotionality: a neuroanatomical perspective. Neuroscience 2012; 204: 134-44.
128. Davis M, Rainnie D, Cassell M. Neurotransmission in the rat amygdala related to fear and anxiety. Trends Neurosci 1994; 17: 208-14.
129. Graeff FG, Guimarães FS, De Andrade TG, Deakin JF. Role of 5-HT in stress, anxiety, and depression. Pharmacol Biochem Behav 1996; 54: 129-41.
130. Cahill L, McGaugh JL. Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci 1998; 21: 294-9.
131. Fattore L, Cossu G, Spano MS, et al. Cannabinoids and reward: interactions with the opioid system. Crit Rev Neurobiol 2004; 16: 147-58.
132. Chaouloff F, Dubreucq S, Bellocchio L, Marsicano G. Endocannabinoids and motor behavior: CB1 receptors also control running activity. Physiology 2011; 26: 76-7.
133. Romero EM, Fernández B, Sagredo O, et al. Antinociceptive, behavioural and neuroendocrine effects of CP 55,940 in young rats. Brain Res Dev Brain Res 2002; 136: 85-92.
134. Wiley JL. Sex-dependent effects of Delta(9)-tetrahydrocannabinol on locomotor activity in mice. Neurosci Lett 2003; 352: 77-80.
135. Craft RM, Leitl MD. Gonadal hormone modulation of the behavioral effects of Delta9-tetrahydrocannabinol in male and female rats. Eur J Pharmacol 2008; 578: 37-42.
136. 9-tetrahydrocannabinol in female vs. male rats. Behav Brain Res 2011; 216: 200-6.
137. Dreher JC, Schmidt PJ, Kohn P, Furman D, Rubinow D, Berman KF. Menstrual cycle phase modulates reward-related neural function in women. Proc Natl Acad Sci USA 2007; 104: 2465-70.
138. Elman I, Karlsgodt KH, Gastfriend DR. Gender differences in cocaine craving among non-treatment-seeking individuals with cocaine dependence. Am J Drug Alcohol Abuse 2001; 27: 193-202.
139. Moura PJ, Petersen SL. Estradiol acts through nuclear-and membrane-initiated mechanisms to maintain a balance between GABAergic and glutamatergic signaling in the brain: implications for hormone replacement therapy. Rev Neurosci 2010; 21: 363-80.
140. Bodo C, Rissman EF. New roles for estrogen receptor beta in behavior and neuroendocrinology. Front Neuroendocrinol 2006; 27: 217-32.