Psychoneuroendocrinology
Volume 35, Issue 2 , Pages 197-208 , February 2010

Methamphetamine facilitates female sexual behavior and enhances neuronal activation in the medial amygdala and ventromedial nucleus of the hypothalamus

  • Mary K. Holder

      Affiliations

    • Program in Neuroscience, University of Maryland, Baltimore, School of Medicine Baltimore, MD 21201, United States
    • Corresponding Author InformationCorresponding author at: 655 West Baltimore Street, BRB 4-002, Baltimore, MD 21201, United States. Tel.: +1 410 706 5581; fax: +1 410 706 0032.
  • ,
  • Maria M. Hadjimarkou

      Affiliations

    • Department of Pharmacology and Experimental Therapeutics, University of Maryland, Baltimore, School of Medicine Baltimore, MD 21201, United States
    • Current address: Department of Psychology, University of Cyprus, Nicosia, Cyprus.
  • ,
  • Susan L. Zup

      Affiliations

    • Department of Physiology, University of Maryland, Baltimore, School of Medicine Baltimore, MD 21201, United States
    • Current address: Department of Psychology, University of Massachusetts, Boston, Boston, MA, United States.
  • ,
  • Tamara Blutstein

      Affiliations

    • Program in Neuroscience, University of Maryland, Baltimore, School of Medicine Baltimore, MD 21201, United States
  • ,
  • Rebecca S. Benham

      Affiliations

    • Department of Pharmacology and Experimental Therapeutics, University of Maryland, Baltimore, School of Medicine Baltimore, MD 21201, United States
    • Current address: Program in Biomedical Neurosciences, Boston University, School of Medicine, Boston, MA, United States.
  • ,
  • Margaret M. McCarthy

      Affiliations

    • Program in Neuroscience, University of Maryland, Baltimore, School of Medicine Baltimore, MD 21201, United States
    • Department of Physiology, University of Maryland, Baltimore, School of Medicine Baltimore, MD 21201, United States
  • ,
  • Jessica A. Mong

      Affiliations

    • Program in Neuroscience, University of Maryland, Baltimore, School of Medicine Baltimore, MD 21201, United States
    • Department of Pharmacology and Experimental Therapeutics, University of Maryland, Baltimore, School of Medicine Baltimore, MD 21201, United States

Received 12 March 2009 ,Revised 29 May 2009 ,Accepted 8 June 2009.

References 

  1. Apostolakis EM, Garai J, Clark JH, O’Malley BW. In vivo regulation of central nervous system progesterone receptors: cocaine induces steroid-dependent behavior through dopamine transporter modulation of D5 receptor in rats. Mol. Endocrinol. 1996;10:1595–1604
  2. Auger AP. Ligand-independent activation of progestin receptors: relevance for female sexual behavior. Reproduction. 2001;122:847–855
  3. Auger AP. Steroid receptor control of reproductive behavior. Horm. Behav. 2004;45:168–172
  4. Auger AP, Moffatt CA, Blaustein JD. Progesterone-independent activation of rat brain progestin receptors by reproductive stimuli. Endocrinology. 1997;138:511–514
  5. Bai W, Rowan BG, Allgood VE, O’Malley BW, Weigel NL. Differential phosphorylation of chicken progesterone receptor in hormone-dependent and ligand-independent activation. J. Biol. Chem. 1997;272:10457–10463
  6. Bao SLX. Regulation of estrogen and phytoestrogen on the dopaminergic systems of amygdala in rats. Acta Physiol. Sin. 2003;55:589–593
  7. Beach FA. Importance of progesterone to induction of sexual receptivity in spayed female rats. Proc. Soc. Exp. Biol. Med. 1942;51:369–371
  8. Beach FA. Sexual attractivity, proceptivity and receptivity in female mammals. Horm. Behav. 1976;7:105–138
  9. Becker JB, Rudrick CN. Rapid effects of estrogen or progesterone on the amphetamine-induced increase in striatal dopamine are enhanced by estrogen priming: a microdialysis study. Pharmacol. Biochem. Behav. 1999;64:53–57
  10. Becker JB, Rudrick CN, Jenkins WJ. The role of dopamine in the nucleus accumbens and striatum during sexual behavior in the female rat. J. Neurosci. 2001;21:3236–3241
  11. Berridge KC. The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology (Berlin). 2007;191:391–431
  12. Blaustein JD. Neuroendocrine regulation of feminine sexual behavior: lessons from rodent models and thoughts about humans. Annu. Rev. Psychol. 2008;59:93–118
  13. Denner LA, Weigel NL, Maxwell BL, Schader WT, O’Malley BW. Regulation of progesterone receptor-mediated transcription by phosphorylation. Science. 1990;250:1740–1743
  14. Edgar DM, Seidel WF. Modafinil induces wakefulness without intensifying motor activity of subsequent rebound hypersomnolence in the rat. J. Pharmacol. Exp. Ther. 1997;283:757–769
  15. Ellingsen E, Ågmo A. Sexual-incentive motivation and paced sexual behavior in female rats after treatment with drugs modifying dopaminergic neurotransmission. Pharmacol. Biochem. Behav. 2004;77:431–445
  16. Ellinwood EH, Balster RL. Rating the behavioral effects of amphetamine. Eur. J. Pharmacol. 1974;28:35–41
  17. Erskine MS. Solicitation behavior in the estrous female rat: a review. Horm. Behav. 1989;23:473–502
  18. Erskine MS. Mating-induced increases in FOS protein in preoptic area and medial amygdala of cycling female rats. Brain Res. Bull. 1993;32:447–451
  19. Fleckenstein AE, Gibb JW, Hanson GR. Differential effects of stimulants on monoaminergic transporters: pharmacological consequences and implication for neurotoxicy. Eur. J. Pharmacol. 2000;406:1–13
  20. Fukui R, Svenningsson P, Matsuishi T, Higashi H, Nairn AC, Greengard P, et al. Effect of methylphenidate on dopamine/DARPP signalling in adult, but not young, mice. J. Neurochem. 2003;87:1391–1401
  21. Gray TS. Functional and anatomical relationships among the amygdala, basal forebrain, ventral striatum, and cortex. An integrative discussion. Ann. N. Y. Acad. Sci. 1999;877:439–444
  22. Guarraci FA, Benson A. “Coffee, tea and me”: moderate doses of caffeine affect sexual behavior in female rats. Pharmacol. Biochem. Behav. 2005;82:522–530
  23. Guarraci FA, Clark AS. Amphetamine modulation of paced mating behavior.. Pharmacol. Biochem. Behav. 2003;76:505–515
  24. Guarraci FA, Megroz AB, Clark AS. Paced mating behavior in the female rat following lesions of three regions responsive to vaginocervical stimulation. Brain Res. 2004;999:40–52
  25. Hadjimarkou MM, Benham R, Schwarz JM, Holder MK, Mong JA. Estradiol suppresses rapid eye movement sleep and activation of sleep-active neurons in the ventrolateral preoptic area. Eur. J. Neurosci. 2008;27:1780–1792
  26. Hardy DF, Debold JF. Effects of mounts without intromission upon the behavior of female rats during the onset of estrogen-induced heat. Physiol. Behav. 1971;7:643–645
  27. Hosokawa N, Chiba A. Effects of sexual experience on conspecific odor preference and male odor-induced activation of the vomeronasal projection pathway and the nucleus accumbens in female rats. Brain Res. 2007;1175:66–75
  28. Ikemoto S, Panksepp J. The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res. Brain Res. Rev. 1999;31:6–41
  29. Jenkins WJ, Becker JB. Dynamic increases in dopamine during paced copulatioin in the female rat. Eur. J. Neurosci. 2003;18:1997–2001
  30. Käll K, Nilsonne Å. Preference for sex on amphetamine: a marker for HIV risk behavior among male intravenous amphetamine users in Stockholm. AIDS Care. 1995;7:171–188
  31. Lehmann ML, Erskine MS. Glutaminergic stimulation of the medial amygdala induces steriod dependent c-fos expression within forebrain nuclei responsive to mating stimulation. Neuroscience. 2005;136:55–64
  32. Mani SK. Ligand-independent activation of progestin receptors in sexual receptivity. Horm. Behav. 2001;40:183–190
  33. Mani SK, Allen JMC, Clark JH, Blaustein JD, O’Malley BW. Convergent pathways for steroid hormone- and neurotransmitter-induced rat sexual behavior. Science. 1994;265:1246–1249
  34. Mani SK, Allen JM, Lydon JP, Mulac-Jericevic B, Blaustein JD, DeMayo FJ, et al. Dopamine requires the unoccupied progesterone receptor to induce sexual behavior in mice. Mol. Endocrinol. 1996;10:1728–1737
  35. Mani SK, Fienberg AA, O’Callaghan JP, Snyder GL, Allen PB, Dash PK, et al. Requirement for DARPP-32 in progesterone-facilitate sexual receptivity in female rats and mice. Science. 2000;287:1053–1056
  36. Mansergh G, Purcell DM, Stall R, McFarlane M, Semann S, Valentine J, et al. CDC consultation on methamphetamine use and sexual risk behavior for HIV/STD infection: summary and suggestions. Public Health Rep. 2006;121:127–132
  37. Masco DH, Carrer HF. Pathways conducting amygdaloid influence on feminine sexual behavior in the rat. Behav. Brain Res. 1984;11:205–212
  38. Melega WP, Cho AK, Harvey D, Lacan G. Methamphetamine blood concentrations in human abusers: application to pharmacokinetic modeling. Synapse. 2007;61:216–220
  39. Meredith JM, Moffatt CA, Auger AP, Snyder GL, Greengard P, Blaustein JD. Mating-related stimulation induces phosphorylation of dopamine- and cyclic AMP-regulated phosphoprotein-32 in progestin receptor-containing areas in the female brain. J. Neurosci. 1998;18:10189–10195
  40. Mermelstein PG, Becker JB. Increased extracellular dopamine in the nucleus accumbens and striatum of the female rat during paced copulatory behavior. Behav. Neurosci. 1995;109:354–365
  41. Michanek A. Potention of d- and l-amphetamine effects on copulatory behavior in female rats by treatment with a-adrenoreceptor blocking drugs. Arch. Int. Pharmacodyn. Ther. 1979;239:241–256
  42. Michanek A, Meyerson BJ. A comparative study of different amphetamines of copulatory behavior and stereotype activity in the female rat. Psychopharmacology (Berlin). 1977;53:175–183
  43. Michanek A, Meyerson BJ. The effects of different amphetamines on copulatory behaviour and stereotype activity in the female rat, after treatment with monoamine depletors and synthesis inhibitors. Arch. Int. Pharmacodyn. Ther. 1977;229:301–312
  44. Milesi-Halle 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;86:140–149
  45. Newman SW. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann. N. Y. Acad. Sci. 1999;877:242–257
  46. Pfaff DW, Ågmo A. Reproductive motivation. In:  Phashler H,  Gallistel R editor. Steven's Handbook of Experimental Psychology. Learning, Motivation, and Emotion. New York: Wiley; 2002;p. 709–736
  47. Pfaus JG, Damsma G, Wenkstern D, Fibiger HC. Sexual activity increase dopamine transmisstion in the nucleus accumbens and striatum of female rats. Brain Res. 1995;693:21–30
  48. Pfaus JG, Kippin TE, Coria-Avila G. What can animal models tell us about human sexual response?. Annu. Rev. Sex Res. 2003;14:1–63
  49. Pitkänen A. Connectivity of the rat amygdaloid complex. In:  Aggleton JP editors. The Amygdala. New York: Oxford University Press; 2000;p. 31–115
  50. Polston EK, Erskine MS. Patterns of induction of the immediate-early genes c-fos and egr-1 in the female rat brain following differential amounts of mating stimulation. Neuroendocrinology. 1995;62:371–384
  51. Polston EK, Heitz M, Barnes K, Erskine MS. NMDA-mediated activation of the medial amygdala initiates a downstream neuroendocrine memory responsible for pseudopregnancy in the female rat. J. Neurosci. 2001;21:4104–4110
  52. Power RF, Mani SK, Codina J, Conneely OM, O’Malley BW. Dopaminergic and ligand-independent activation of steroid hormone receptors. Science. 1991;254:1636–1639
  53. Rawson RA, Washton A, Domier CP, Reiber C. Drugs and sexual effects: role of drug type and gender. J. Subst. Abuse Treat. 2002;22:103–108
  54. Riviere GJ, Byrnes KA, Gentry WB, Owens SM. Spontaneous locomotor activity and pharmacokinetics of Intrvenous methamphetamine and its metabolite amphetamine in the rat. J. Pharmacol. Exp. Ther. 1999;291:1220–1226
  55. Salamone JD, Correa M, Farrar A, Mingote SM. Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology (Berlin). 2007;191:461–482
  56. Segal DS, Kuczenski R. Repeated binge exposures to amphetamine and methamphetamine: behavioral and neurochemical characterization. J. Pharmacol. Exp. Ther. 1997;282:561–573
  57. Semple SJ, Grant I, Patterson TL. Female methamphetamine users: social characteristics and sexual risk behavior. Women Health. 2004;40:35–50
  58. Semple SJ, Patterson TL, Grant I. The context of sexual risk behavior among heterosexual methamphetamine users. Addict. Behav. 2004;29:807–810
  59. Whalen RE. Estrogen-progesterone induction of mating behavior in female rats. Horm. Behav. 1974;5:157–162

PII: S0306-4530(09)00195-4

doi: 10.1016/j.psyneuen.2009.06.005

Psychoneuroendocrinology
Volume 35, Issue 2 , Pages 197-208 , February 2010