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Estrous cycle and sex affect cocaine-induced behavioural changes in CD1 mice

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An Erratum to this article was published on 03 February 2015

Abstract

Rationale

Several findings on sex differences in cocaine response suggest a role for hormonal milieu in modulating the subjective effects of cocaine. Nitric oxide (NO) has been involved in the neurochemical, hormonal, and behavioral changes related to stress and anxiety. Within the brain, the anteroventral subdivision of the medial amygdala (MeAV) is an important area involved in processing emotional responses such as anxiety and a high density of NO-producing neurons is observed in this area.

Objectives

In this study, we hypothesize the possibility of sex/hormonal differences in response to cocaine and that these differences may reflect a change in the MeAV nitrergic system. We have examined cocaine’s acute effects on nicotinamide adenine dinucleotide phosphate diaphorase (nadph-d) expression, as well as its effect on motor activity and anxiety in male and estrus and diestrus females.

Results

Our results show that acute cocaine administration produces an increase in both anxiety behaviors and nadph-d expression in the MeAV. Male and diestrus female mice were more susceptible to these effects of cocaine than estrus female mice in which no differences were detected. In addition, we examined individual differences in male and female mice responding to intravenous cocaine reinforcement in a self-administration paradigm. Female mice acquired cocaine self-administration at a faster rate than males and showed a higher motivation to self-administer cocaine under a progressive ratio schedule of reinforcement.

Conclusions

Our data suggest a complex interaction between hormonal milieu and the behavioral and reinforcing effects of cocaine.

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References

  • Adamec RE, Morgan HD (1994) The effect of kindling of different nuclei in the left and right amygdala on anxiety in the rat. Physiol Behav 55:1–12

    Article  CAS  PubMed  Google Scholar 

  • Anker JJ, Carroll ME (2010) The role of progestins in the behavioral effects of cocaine and other drugs of abuse: human and animal research. Neurosci Biobehav Rev 35:315–333

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Anker JJ, Carroll ME (2011) Females are more vulnerable to drug abuse than males: evidence from preclinical studies and the role of ovarian hormones. Curr Top Behav Neurosci 8:73–96

    Article  CAS  PubMed  Google Scholar 

  • Anker JJ, Zlebnik NE, Navin SF, Carroll ME (2011) Responding during signaled availability and nonavailability of iv cocaine and food in rats: age and sex differences. Psychopharmacology (Berl) 215:785–799

    Article  CAS  Google Scholar 

  • Becker JB (1999) Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol Biochem Behav 64:803–812

    Article  CAS  PubMed  Google Scholar 

  • Becker JB, Hu M (2008) Sex differences in drug abuse. Front Neuroendocrinol 29:36–47

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Becker JB, Molenda H, Hummer DL (2001) Gender differences in the behavioral responses to cocaine and amphetamine. Implications for mechanisms mediating gender differences in drug abuse. Ann N Y Acad Sci 937:172–187

    Article  CAS  PubMed  Google Scholar 

  • Bhargava HN, Kumar S (1997) Sensitization to the locomotor stimulant activity of cocaine is associated with increases in nitric oxide synthase activity in brain regions and spinal cord of mice. Pharmacology 55:292–298

    Article  CAS  PubMed  Google Scholar 

  • Bowman BP, Kuhn CM (1996) Age-related differences in the chronic and acute response to cocaine in the rat. Dev Psychobiol 29:597–611

    Article  CAS  PubMed  Google Scholar 

  • Bredt DS, Snyder SH (1990) Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci U S A 87:682–685

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Byers SL, Wiles MV, Dunn SL, Taft RA (2012) Mouse estrous cycle identification tool and images. PLoS One 7:e35538

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Caine SB, Bowen CA, Yu G, Zuzga D, Negus SS, Mello NK (2004) Effect of gonadectomy and gonadal hormone replacement on cocaine self-administration in female and male rats. Neuropsychopharmacology 29:929–942

    Article  CAS  PubMed  Google Scholar 

  • Canteras NS, Simerly RB, Swanson LW (1995) Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 360:213–245

    Article  CAS  PubMed  Google Scholar 

  • Carrillo B, Pinos H, Guillamon A, Panzica G, Collado P (2007) Morphometrical and neurochemical changes in the anteroventral subdivision of the rat medial amygdala during estrous cycle. Brain Res 1150:83–93

    Article  CAS  PubMed  Google Scholar 

  • Carroll ME, Morgan AD, Lynch WJ, Campbell UC, Dess NK (2002) Intravenous cocaine and heroin self-administration in rats selectively bred for differential saccharin intake: phenotype and sex differences. Psychopharmacology (Berl) 161:304–313

    Article  CAS  Google Scholar 

  • Creese I, Iversen SD (1975) The pharmacological and anatomical substrates of the amphetamine response in the rat. Brain Res 83:419–436

    Article  CAS  PubMed  Google Scholar 

  • Crespo C, Arevalo R, Brinon JG, Porteros A, Bravo IG, Aijon J, Alonso JR (1995) Colocalization of NADPH-diaphorase and acetylcholinesterase in the rat olfactory bulb. J Chem Neuroanat 9:207–216

    Article  CAS  PubMed  Google Scholar 

  • Fattore L, Altea S, Fratta W (2008) Sex differences in drug addiction: a review of animal and human studies. Womens Health (Lond Engl) 4:51–65

    Article  CAS  Google Scholar 

  • Festa ED, Quinones-Jenab V (2004) Gonadal hormones provide the biological basis for sex differences in behavioral responses to cocaine. Horm Behav 46:509–519

    Article  CAS  PubMed  Google Scholar 

  • Forestiero D, Manfrim CM, Guimaraes FS, de Oliveira RM (2006) Anxiolytic-like effects induced by nitric oxide synthase inhibitors microinjected into the medial amygdala of rats. Psychopharmacology (Berl) 184:166–172

    Article  CAS  Google Scholar 

  • Franklin KBJ, Paxinos G (1997) The mouse brain in stereotaxic coordinates. Academic, New York

    Google Scholar 

  • Gonzalez-Flores O, Etgen AM (2004) The nitric oxide pathway participates in estrous behavior induced by progesterone and some of its ring A-reduced metabolites. Horm Behav 45:50–57

    Article  CAS  PubMed  Google Scholar 

  • Gotti S, Chiavegatto S, Sica M, Viglietti-Panzica C, Nelson RJ, Panzica G (2004) Alteration of NO-producing system in the basal forebrain and hypothalamus of Ts65Dn mice: an immunohistochemical and histochemical study of a murine model for Down syndrome. Neurobiol Dis 16:563–571

    Article  CAS  PubMed  Google Scholar 

  • Griffin WC 3rd, Middaugh LD (2006) The influence of sex on extracellular dopamine and locomotor activity in C57BL/6J mice before and after acute cocaine challenge. Synapse 59:74–81

    Article  CAS  PubMed  Google Scholar 

  • Griffin WC 3rd, Randall PK, Middaugh LD (2007) Intravenous cocaine self-administration: individual differences in male and female C57BL/6J mice. Pharmacol Biochem Behav 87:267–279

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guimaraes FS, Beijamini V, Moreira FA, Aguiar DC, de Lucca AC (2005) Role of nitric oxide in brain regions related to defensive reactions. Neurosci Biobehav Rev 29:1313–1322

    Article  CAS  PubMed  Google Scholar 

  • Haney M, Maccari S, Le Moal M, Simon H, Piazza PV (1995) Social stress increases the acquisition of cocaine self-administration in male and female rats. Brain Res 698:46–52

    Article  CAS  PubMed  Google Scholar 

  • Haracz JL, MacDonall JS, Sircar R (1997) Effects of nitric oxide synthase inhibitors on cocaine sensitization. Brain Res 746:183–189

    Article  CAS  PubMed  Google Scholar 

  • He M, Shippenberg TS (2000) Strain differences in basal and cocaine-evoked dopamine dynamics in mouse striatum. J Pharmacol Exp Ther 293:121–127

    CAS  PubMed  Google Scholar 

  • Hu M, Crombag HS, Robinson TE, Becker JB (2004) Biological basis of sex differences in the propensity to self-administer cocaine. Neuropsychopharmacology 29:81–85

    Article  CAS  PubMed  Google Scholar 

  • Itzhak Y (1997) Modulation of cocaine- and methamphetamine-induced behavioral sensitization by inhibition of brain nitric oxide synthase. J Pharmacol Exp Ther 282:521–527

    CAS  PubMed  Google Scholar 

  • Itzhak Y, Ali SF, Martin JL, Black MD, Huang PL (1998) Resistance of neuronal nitric oxide synthase-deficient mice to cocaine-induced locomotor sensitization. Psychopharmacology (Berl) 140:378–386

    Article  CAS  Google Scholar 

  • Jackson LR, Robinson TE, Becker JB (2006) Sex differences and hormonal influences on acquisition of cocaine self-administration in rats. Neuropsychopharmacology 31:129–138

    CAS  PubMed  Google Scholar 

  • Jori A, Colturani F, Dolfini E, Rutczynski M (1976) Modifications of the striatal dopamine metabolism during the estrus cycle in mice. Neuroendocrinology 21:262–266

    Article  CAS  PubMed  Google Scholar 

  • Justice AJ, de Wit H (1999) Acute effects of d-amphetamine during the follicular and luteal phases of the menstrual cycle in women. Psychopharmacology (Berl) 145:67–75

    Article  CAS  Google Scholar 

  • Kelly PH, Iversen SD (1976) Selective 6OHDA-induced destruction of mesolimbic dopamine neurons: abolition of psychostimulant-induced locomotor activity in rats. Eur J Pharmacol 40:45–56

    Article  CAS  PubMed  Google Scholar 

  • Kim HS, Park WK (1995) Nitric oxide mediation of cocaine-induced dopaminergic behaviors: ambulation-accelerating activity, reverse tolerance and conditioned place preference in mice. J Pharmacol Exp Ther 275:551–557

    CAS  PubMed  Google Scholar 

  • Knowles RG, Palacios M, Palmer RM, Moncada S (1989) Formation of nitric oxide from L-arginine in the central nervous system: a transduction mechanism for stimulation of the soluble guanylate cyclase. Proc Natl Acad Sci U S A 86:5159–5162

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Krukoff TL, Khalili P (1997) Stress-induced activation of nitric oxide-producing neurons in the rat brain. J Comp Neurol 377:509–519

    Article  CAS  PubMed  Google Scholar 

  • Kuhn CM, Walker QD, Kaplan KA, Li ST (2001) Sex, steroids, and stimulant sensitivity. Ann N Y Acad Sci 937:188–201

    Article  CAS  PubMed  Google Scholar 

  • Lukas SE, Sholar M, Lundahl LH, Lamas X, Kouri E, Wines JD, Kragie L, Mendelson JH (1996) Sex differences in plasma cocaine levels and subjective effects after acute cocaine administration in human volunteers. Psychopharmacology (Berl) 125:346–354

    Article  CAS  Google Scholar 

  • Lund TD, Rovis T, Chung WC, Handa RJ (2005) Novel actions of estrogen receptor-beta on anxiety-related behaviors. Endocrinology 146:797–807

    Article  CAS  PubMed  Google Scholar 

  • Lynch WJ, Carroll ME (1999) Sex differences in the acquisition of intravenously self-administered cocaine and heroin in rats. Psychopharmacology (Berl) 144:77–82

    Article  CAS  Google Scholar 

  • Lynch WJ, Roth ME, Carroll ME (2002) Biological basis of sex differences in drug abuse: preclinical and clinical studies. Psychopharmacology (Berl) 164:121–137

    Article  CAS  Google Scholar 

  • Lynch WJ, Kiraly DD, Caldarone BJ, Picciotto MR, Taylor JR (2007) Effect of cocaine self-administration on striatal PKA-regulated signaling in male and female rats. Psychopharmacology (Berl) 191:263–271

    Article  CAS  Google Scholar 

  • Mani SK, Allen JM, Rettori V, McCann SM, O’Malley BW, Clark JH (1994) Nitric oxide mediates sexual behavior in female rats. Proc Natl Acad Sci U S A 91:6468–6472

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Martini M, Valverde O (2012) A single episode of maternal deprivation impairs the motivation for cocaine in adolescent mice. Psychopharmacology (Berl) 219:149–158

    Article  CAS  Google Scholar 

  • Morse AC, Erwin VG, Jones BC (1993) Strain and housing affect cocaine self-selection and open-field locomotor activity in mice. Pharmacol Biochem Behav 45:905–912

    Article  CAS  PubMed  Google Scholar 

  • Orsini C, Izzo E, Koob GF, Pulvirenti L (2002) Blockade of nitric oxide synthesis reduces responding for cocaine self-administration during extinction and reinstatement. Brain Res 925:133–140

    Article  CAS  PubMed  Google Scholar 

  • Osterlund MK, Witt MR, Gustafsson JA (2005) Estrogen action in mood and neurodegenerative disorders: estrogenic compounds with selective properties—the next generation of therapeutics. Endocrine 28:235–242

    Article  PubMed  Google Scholar 

  • Panzica GC, Viglietti-Panzica C, Sica M, Gotti S, Martini M, Pinos H, Carrillo B, Collado P (2006) Effects of gonadal hormones on central nitric oxide producing systems. Neuroscience 138:987–995

    Article  CAS  PubMed  Google Scholar 

  • Parylak SL, Caster JM, Walker QD, Kuhn CM (2008) Gonadal steroids mediate the opposite changes in cocaine-induced locomotion across adolescence in male and female rats. Pharmacol Biochem Behav 89:314–323

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Perrotti LI, Russo SJ, Fletcher H, Chin J, Webb T, Jenab S, Quinones-Jenab V (2001) Ovarian hormones modulate cocaine-induced locomotor and stereotypic activity. Ann N Y Acad Sci 937:202–216

    Article  CAS  PubMed  Google Scholar 

  • Quinones-Jenab V, Ho A, Schlussman SD, Franck J, Kreek MJ (1999) Estrous cycle differences in cocaine-induced stereotypic and locomotor behaviors in Fischer rats. Behav Brain Res 101:15–20

    Article  CAS  PubMed  Google Scholar 

  • Ramoa CP, Doyle SE, Naim DW, Lynch WJ (2013) Estradiol as a mechanism for sex differences in the development of an addicted phenotype following extended access cocaine self-administration. Neuropsychopharmacology 38:1698–1705

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rasia-Filho AA, Londero RG, Achaval M (2000) Functional activities of the amygdala: an overview. J Psychiatry Neurosci 25:14–23

    CAS  PubMed Central  PubMed  Google Scholar 

  • Reith ME, Wiener HL, Fischette CT (1991) Sertraline and cocaine-induced locomotion in mice. I. Acute studies. Psychopharmacology (Berl) 103:297–305

    Article  CAS  Google Scholar 

  • Richardson NR, Roberts DC (1996) Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy. J Neurosci Methods 66:1–11

    Article  CAS  PubMed  Google Scholar 

  • Roth ME, Cosgrove KP, Carroll ME (2004) Sex differences in the vulnerability to drug abuse: a review of preclinical studies. Neurosci Biobehav Rev 28:533–546

    Article  CAS  PubMed  Google Scholar 

  • Russo SJ, Jenab S, Fabian SJ, Festa ED, Kemen LM, Quinones-Jenab V (2003) Sex differences in the conditioned rewarding effects of cocaine. Brain Res 970:214–220

    Article  CAS  PubMed  Google Scholar 

  • Scalia F, Winans SS (1975) The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J Comp Neurol 161:31–55

    Article  CAS  PubMed  Google Scholar 

  • Sell SL, Dillon AM, Cunningham KA, Thomas ML (2005) Estrous cycle influence on individual differences in the response to novelty and cocaine in female rats. Behav Brain Res 161:69–74

    Article  CAS  PubMed  Google Scholar 

  • Sershen H, Hashim A, Lajtha A (1998) Gender differences in kappa-opioid modulation of cocaine-induced behavior and NMDA-evoked dopamine release. Brain Res 801:67–71

    Article  CAS  PubMed  Google Scholar 

  • Sica M, Martini M, Viglietti-Panzica C, Panzica G (2009) Estrous cycle influences the expression of neuronal nitric oxide synthase in the hypothalamus and limbic system of female mice. BMC Neurosci 10:78, 2202-10-78

    Article  PubMed Central  PubMed  Google Scholar 

  • Simonin F, Valverde O, Smadja C, Slowe S, Kitchen I, Dierich A, Le Meur M, Roques BP, Maldonado R, Kieffer BL (1998) Disruption of the kappa-opioid receptor gene in mice enhances sensitivity to chemical visceral pain, impairs pharmacological actions of the selective kappa-agonist U-50,488H and attenuates morphine withdrawal. EMBO J 17:886–897

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Simpson J, Kelly JP (2012) An investigation of whether there are sex differences in certain behavioural and neurochemical parameters in the rat. Behav Brain Res 229:289–300

    Article  CAS  PubMed  Google Scholar 

  • Sofuoglu M, Dudish-Poulsen S, Nelson D, Pentel PR, Hatsukami DK (1999) Sex and menstrual cycle differences in the subjective effects from smoked cocaine in humans. Exp Clin Psychopharmacol 7:274–283

    Article  CAS  PubMed  Google Scholar 

  • Soria G, Mendizabal V, Tourino C, Robledo P, Ledent C, Parmentier M, Maldonado R, Valverde O (2005) Lack of CB1 cannabinoid receptor impairs cocaine self-administration. Neuropsychopharmacology 30:1670–1680

    Article  CAS  PubMed  Google Scholar 

  • Soria G, Castane A, Ledent C, Parmentier M, Maldonado R, Valverde O (2006) The lack of A2A adenosine receptors diminishes the reinforcing efficacy of cocaine. Neuropsychopharmacology 31:978–987

    Article  CAS  PubMed  Google Scholar 

  • Soria G, Barbano MF, Maldonado R, Valverde O (2008) A reliable method to study cue-, priming-, and stress-induced reinstatement of cocaine self-administration in mice. Psychopharmacology (Berl) 199:593–603

    Article  CAS  Google Scholar 

  • Spiteri T, Musatov S, Ogawa S, Ribeiro A, Pfaff DW, Agmo A (2010) The role of the estrogen receptor alpha in the medial amygdala and ventromedial nucleus of the hypothalamus in social recognition, anxiety and aggression. Behav Brain Res 210:211–220

    Article  CAS  PubMed  Google Scholar 

  • Thomsen M, Caine SB (2011) Psychomotor stimulant effects of cocaine in rats and 15 mouse strains. Exp Clin Psychopharmacol 19:321–341

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tomihara K, Soga T, Nomura M, Korach KS, Gustafsson JA, Pfaff DW, Ogawa S (2009) Effect of ER-beta gene disruption on estrogenic regulation of anxiety in female mice. Physiol Behav 96:300–306

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tourino C, Valjent E, Ruiz-Medina J, Herve D, Ledent C, Valverde O (2012) The orphan receptor GPR3 modulates the early phases of cocaine reinforcement. Br J Pharmacol 167:892–904

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Valverde O, Torrens M (2012) CB1 receptor-deficient mice as a model for depression. Neuroscience 204:193–206

    Article  CAS  PubMed  Google Scholar 

  • Van Swearingen AE, Sanchez CL, Frisbee SM, Williams A, Walker QD, Korach KS, Kuhn CM (2013a) Estradiol replacement enhances cocaine-stimulated locomotion in female C57BL/6 mice through estrogen receptor alpha. Neuropharmacology 72:236–249

    Article  PubMed Central  PubMed  Google Scholar 

  • Van Swearingen AE, Walker QD, Kuhn CM (2013b) Sex differences in novelty- and psychostimulant-induced behaviors of C57BL/6 mice. Psychopharmacology (Berl) 225:707–718

    Article  Google Scholar 

  • Vincent SR, Kimura H (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46:755–784

    Article  CAS  PubMed  Google Scholar 

  • Volke V, Wegener G, Bourin M, Vasar E (2003a) Antidepressant- and anxiolytic-like effects of selective neuronal NOS inhibitor 1-(2-trifluoromethylphenyl)-imidazole in mice. Behav Brain Res 140:141–147

    Article  CAS  PubMed  Google Scholar 

  • Volke V, Wegener G, Vasar E (2003b) Augmentation of the NO-cGMP cascade induces anxiogenic-like effect in mice. J Physiol Pharmacol 54:653–660

    CAS  PubMed  Google Scholar 

  • Walker QD, Francis R, Cabassa J, Kuhn CM (2001) Effect of ovarian hormones and estrous cycle on stimulation of the hypothalamo-pituitary-adrenal axis by cocaine. J Pharmacol Exp Ther 297:291–298

    CAS  PubMed  Google Scholar 

  • Walker QD, Schramm-Sapyta NL, Caster JM, Waller ST, Brooks MP, Kuhn CM (2009) Novelty-induced locomotion is positively associated with cocaine ingestion in adolescent rats; anxiety is correlated in adults. Pharmacol Biochem Behav 91:398–408

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Watson RE Jr, Wiegand SJ, Clough RW, Hoffman GE (1986) Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 7:155–159

    Article  CAS  PubMed  Google Scholar 

  • Xiao L, Becker JB (1994) Quantitative microdialysis determination of extracellular striatal dopamine concentration in male and female rats: effects of estrous cycle and gonadectomy. Neurosci Lett 180:155–158

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Schlussman SD, Ho A, Kreek MJ (2001) Effect of acute binge cocaine on levels of extracellular dopamine in the caudate putamen and nucleus accumbens in male C57BL/6J and 129/J mice. Brain Res 923:172–177

    Article  CAS  PubMed  Google Scholar 

  • Zhou L, Zhu DY (2009) Neuronal nitric oxide synthase: structure, subcellular localization, regulation, and clinical implications. Nitric Oxide 20:223–230

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank Dr. Laura Szymanski (Georgia State University) for critical reading of the manuscript and for the English revision of the final text. This study was supported by grant from Spanish Ministry of Science and Innovation (SAF2010-15793), the Spanish Ministry of Health (PNSD 2010) and Red Temática de Investigación Cooperativa en Salud (ISCIII) (RETIC-Trastornos adictivos RTA 001/06/1001-FEDER and RTA 12/0028/0024-FEDER), and Generalitat de Catalunya (2009SGR684).

Conflict of interest

The authors report no biomedical financial interest or potential conflicts of interest.

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  1. Mariangela Martini

    Present address: Equipe “Neuropsychopharmacologie de l’Addiction”, Institut de Neurosciences Cognitives et Intégratives d’Aquitaine, UMR CNRS 5287, 33076, Bordeaux, France

Authors and Affiliations

  1. Neurobiology of Behaviour Research Group (GReNeC), Department of Health and Experimental Sciences, Universitat Pompeu Fabra, Barcelona Biomedical Research Park C/Dr. Aiguader 88, 08003, Barcelona, Spain

    Mariangela Martini, Ana Xavier Pinto & Olga Valverde

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  1. Mariangela Martini
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Correspondence to Olga Valverde.

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Martini, M., Pinto, A.X. & Valverde, O. Estrous cycle and sex affect cocaine-induced behavioural changes in CD1 mice. Psychopharmacology 231, 2647–2659 (2014). https://doi.org/10.1007/s00213-014-3433-5

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