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Effects of opiate antagonists on hormones and behavior of male and female rhesus monkeys

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Abstract

Opiate antagonists, naloxone (100 µg/kg) and naltrexone (1 mg/kg) were given to singly housed adult male or female rhesus prior to a 20-minute behavioral test with an oppositely sexed stimulus monkey. Four of the intact adult males were socially and sexually experienced. The remaining two intact males and two castrated males had been reared in socially restricted conditions and were psychosexually deficient. Adult females were ovariectomized, and the effects of opiate antagonists were examined with or without concurrent estradiol treatment. Both antagonists inhibited sexual behavior of the socially reared, sexually active, intact males. No stimulatory effects on sexual behavior were observed for sexually deficient males, whether intact or castrated. Females showed little change in sexual behavior following opiate antagonist treatment, regardless of endocrine status. The proportion of approaches of the female to the male was increased when naloxone, but not naltrexone, was given. Specific endocrine effects of the opiate antagonists were only found in intact males. Naltrexone significantly increased LH concentrations in the two males tested, while the increase in LH in the four males receiving naloxone was not significant. In all intact males, increases in LH were accompanied by statistically significant increases in circulating concentrations of testosterone following naloxone and naltrexone. The gonadotropic stimulating effect of the opiate antagonists was specific to LH, and no changes were observed in circulating concentrations of FSH in either sex.

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References

  • Aceto, M. D., Flora, R. E., and Harris, L. S. (1977). The effects of naloxone and nalorphine during the development of morphine dependence in rhesus monkeys.Pharmacology 15: 1.

    PubMed  Google Scholar 

  • Bertolini, A., and Gessa, G. L. (1981). Behavioral effects of ACTH and MSH peptides.J. Endocrinol. Invest. 4: 241.

    PubMed  Google Scholar 

  • Bielert, C. (1978). Androgen treatments of young male rhesus monkeys. In Chivers, D. J., and Herbert, J. (eds.),Recent Advances in Primatology (Vol. 1), Academic Press, London, p. 485.

    Google Scholar 

  • Bielert, C., and Goy, R. W. (1973). Sexual behavior of male rhesus: Effects of repeated ejaculation and partner's cycle stage.Horm. Behav. 4: 109.

    Google Scholar 

  • Bloom, F., Rossier, J., Battenburg, E., Banyon, A., French, E., Hendrickson, S., Siggins, G., Segal, D., Browne, R., Ling, N., and Guilleman, R. (1978).β-Endorphin: Cellular localization, electrophysiological and behavioral effects. In Costa, E., and Trabucchi, M. (eds.),Advances in Biochemical Psychopharmacology (Vol. 18), Raven Press, New York, p. 89.

    Google Scholar 

  • Boorman, G. A., Niswender, G. D., Gay, V. L., Reichert, L. E., Jr., and Midgeley, A. R., Jr. (1973). Radioimmunoassay for follicle-stimulating hormone in the rhesus monkey using an anti-human FSH serum and rat FSH131I.Endocrinology 92: 618.

    PubMed  Google Scholar 

  • Bradbury, A. F., Smyth, D. G., Snell, C. R., Birdsall, N J. M., and Hulme, E. C. (1976). C-fragment of lipotropin has a high affinity for brain opiate receptors.Nature (London) 260: 793.

    Google Scholar 

  • Brady, J. P., and Bianco, C. F. (1980). Endorphins: Naloxone failure to increase sexual arousal in sexually unresponsive women: A preliminary report.Biol. Psychiat. 15: 627.

    PubMed  Google Scholar 

  • Braude, M. C., and Morrison, J. M. (1976). Preclinical toxicity studies of naltrexone.Nat. Inst. Drug Abuse Monogr. Ser. 9: 16.

    Google Scholar 

  • Cicero, T. J., Meyer, E. R., Bell, R. D., and Koch, G. (1976). Effects of morphine and methadone on testosterone, luteinizing hormone and the secondary sex organs of the male rat.Endocrinology 98: 367.

    PubMed  Google Scholar 

  • Cicero, T. J., Bell, R. D., Wiest, W. G., Allison, J. H., Polakoski, K., and Robins, E. (1979a). Functions of the male sex organs in heroin and methadone users.New Engl. J. Med. 24: 882.

    Google Scholar 

  • Cicero, T. J., Schainker, B. A., and Meyers, E. R. (1979b). Endogenous opioids participate in the regulation of the hypothalamic-pituitary-luteinizing hormone axis and testosterone's negative feedback control of luteinizing hormone.Endocrinology 104: 1286.

    PubMed  Google Scholar 

  • Creese, I., and Snyder, S. H. (1975). Receptor binding and pharmacological activity of opiates in the guinea-pig intestine.J. Pharm. Exp. Ther. 194: 205.

    Google Scholar 

  • Cushman, P. (1972). Sexual behavior in heroin addiction and methadone maintenance.New York State J. Med. 72: 1261.

    Google Scholar 

  • Czaja, J. A., and Bielert, C. (1975). Female rhesus sexual behavior and distance to a male partner: Relation to stage of the menstrual cycle.Arch. Sex. Behav. 4: 583.

    PubMed  Google Scholar 

  • DeLeon, G., and Wexler, H. (1973). Heroin addiction: Its relation to sexual behavior and sexual experience.J. Abnorm. Psychol. 81: 36.

    PubMed  Google Scholar 

  • DeWied, D., Toivola, P. T. K., Goldfoot, D. A., and Goy, R. W. (1982). Behavioral effects of intracranial administration of ACTH (1-24) in the rhesus monkey. Personal communication.

  • Downs, D. A., and Woods, J. H. (1976). Naloxone as a negative reinforcer in rhesus monkeys: Effects of dose, schedule and narcotic regimen.Pharmacol. Rev. 27: 397.

    Google Scholar 

  • Eipper, B. A., and Mains, R. E. (1980). Structure and biosynthesis of proadrenocorticotropin/endorphin and related peptides.Endocrine Rev. 1: 1.

    Google Scholar 

  • Epstein, A. N., and Teitelbaum, P. (1962). Regulation of food intake in the absence of taste, smell and other oropharyngeal sensations.J. Comp. Physiol. Psychol. 55: 753.

    Google Scholar 

  • Fabre-Nys, C., Meller, R. E., and Keverne, E. B. (1982). Opiate antagonists stimulate affiliative behaviour in monkeys.Pharmacol. Biochem. Behav.

  • Ferrari, W. (1958). Behavioural changes in animals after intracisternal injection with adrenocorticotrophic hormone and melanocyte-stimulating hormone.Nature (London) 181: 925.

    Google Scholar 

  • Gessa, G. L., Vargiu, L., and Ferrari, W. (1966). Stretchings and yawnings induced by adrenocorticotrophic hormone.Nature (London) 211: 426.

    Google Scholar 

  • Gessa, G. L., Pisano, M., Vargiu, L., Crabai, F., and Ferrari, W. (1967). Stretching and yawning movements after intracerebral injection of ACTH.Rev. Can. Biol. 26: 229.

    PubMed  Google Scholar 

  • Gessa, G. L., Paglietti, E., and Pellegrini-Quarantotti, B. (1979). Induction of copulatory behavior in sexually inactive rats by naloxone.Science 204: 203.

    PubMed  Google Scholar 

  • Gispen, W. H., Buitelaar, J., Weigant, V. M., Terenius, L., and DeWied, D. (1976). Interaction between ACTH fragments, brain opiate receptors and morphine-induced analgesia.Europe. J. Pharmacol. 39: 393.

    Google Scholar 

  • Glick, B. B., Baughman, W. L., Jensen, J. N., and Phoenix, C. H. (1982). Endogenous opiate systems and primate reproduction: Inability of naloxone to induce sexual activity in rhesus males.Arch. Sex. Behav. 11: 267.

    PubMed  Google Scholar 

  • Gold, M. S., Redmond, D. E., Jr., and Donabedian, R. K. (1979). The effects of opiate agonist and antagonist on serum prolactin in primates: Possible role for endorphins in prolactin regulation.Endocrinology 105: 284.

    PubMed  Google Scholar 

  • Goldfoot, D. A. (1977). Sociosexual behaviors of non-human primates during development and maturity: Social and hormonal relationships. In Schrier, A. M. (ed.),Behavioural Primatology Advances in Research and Theory (Vol. 1), Erlbaum, Hillsdale, New Jersey, p. 139.

    Google Scholar 

  • Goldfoot, D. A. (1980). Psychophysiology of arousal and orgasm in female subhuman primates. Paper presented at the International Academy of Sex Research in Tucson, Arizona.

  • Goldstein, A., and Cox, B. M. (1978). Opiate receptors and their endogenous ligands (endorphins). In Hahn, F. E. (ed.),Progress in Molecular and Subcellular Biology (Vol. 6), Springer-Verlag, New York, p. 113.

    Google Scholar 

  • Goy, R. W., and Goldfoot, D. A. (1974). Experimental and hormonal factors influencing development of sexual behavior in the male rhesus monkey. In Schmitt, F. O., and Wordon, F. G. (eds.),The Neurosciences, Third Study Program MIT Press, Cambridge, Massachusetts, p. 571.

    Google Scholar 

  • Goy, R. W., and Resko, J. A. (1972). Gonadal hormones and behavior of normal and pseudohermaphroditic nonhuman female primates.Rec. Prog. Horm. Res. 28: 707.

    PubMed  Google Scholar 

  • Guerra, F. (1974). Sex and drugs in the 16th century.Brit. J. Addict. 69: 269.

    Google Scholar 

  • Guillemin, R., Vargo, T., Rossier, J., Minick, S., Ling, N., Rivier, C., Vale, W., and Bloom, F. (1977).β-endorphin and adrenocorticotrophin are secreted concomitantly by the pituitary gland.Science 197: 1367.

    PubMed  Google Scholar 

  • Hayward, S. (1957). Modification of sexual behavior of the male albino rat.J. Comp. Physiol. Psychol. 50: 70.

    PubMed  Google Scholar 

  • Helwig, J. T., and Council, K. A. (1979).The SAS User's Guide, 1979 Edition. SAS Institute Inc., Cary, North Carolina.

    Google Scholar 

  • Hetta, J. (1977). Effects of morphine and naltrexone on sexual behavior of the male rat.Acta Pharmacol. Toxicol. 41 (Suppl. 4): 53.

    Google Scholar 

  • Heybach, J. P., and Vernikos, J. (1981). Naloxone inhibits and morphine potentiates the adrenal steroidogenic response to ACTH.Europe. J. Pharmacol. 15: 1.

    Google Scholar 

  • Hinde, R. A., and Atkinson, S. (1970). Assessing the roles of social partners in maintaining mutual proximity, as exemplified by mother-infant relations in rhesus monkeys.Anim. Behav. 18: 169.

    Google Scholar 

  • Hodgen, G. D., Wilks, J. W., Vaitukaitis, J. L., Chen, H. C., Pakoff, H., and Ross, F. T. (1976). A new radioimmunoassay for follicle-stimulating hormone in macaques: Ovulatory menstrual cycles.Endocrinology 99: 137.

    PubMed  Google Scholar 

  • Hollister, L. E. (1975). The mystique of social drugs and sex. In Sandler, M., and Gessa, G. L. (eds.),Sexual Behavior: Pharmacology and Biochemistry Raven Press, New York, p. 85.

    Google Scholar 

  • Hughes, J., Smith, T. W., Kosterlitz, H. W., Fothergill, L. A., Morgan, B. A., and Morris, H. R. (1975). Identification of two related pentapeptides from the brain with potent opiate agonist activity.Nature (Londont) 258: 577.

    Google Scholar 

  • Jacquet, Y. F. (1979).β-endorphin and ACTH-opiate peptides with coordinated roles in the regulation of behaviour?Trends in Neuroscience 2: 140–145.

    Google Scholar 

  • Jensen, D. (1980).The Principles of Physiology. Appleton-Century-Crofts, New York.

    Google Scholar 

  • Korányi, L., Endroczi, E., and Tárnok, F. (1965). Sexual behavior in the course of avoidance conditioning in male rabbits.Neuroendocrinology 1: 144.

    Google Scholar 

  • Krieger, D. T., Liotta, A., and Brownstein, M. J. (1977a). Presence of corticotropin in brain of normal and hypophysectomised rats.Proc. Nat. Acad. Sci. U.S.A. 74: 648.

    Google Scholar 

  • Krieger, D. T., Liotta, A., and Brownstein, M. J. (1977b). Presence of corticotropin in limbic system of normal and hypophysectomised rats.Brain Res. 128: 575.

    PubMed  Google Scholar 

  • Krieger, D. T., Liotta, A. S., Brownstein, M. J., and Zimmermann, E. A. (1980). ACTH,β-lipotropin and related peptides in brain, pituitary and blood.Rec. Prog. Horm. Res. 36: 277.

    PubMed  Google Scholar 

  • Lymangrover, J. R., Dokas, L. A., Kong, A., Martin, R., and Saffran, M. (1981). Naloxone has a direct effect on the adrenal cortex.Endocrinology 109: 1132.

    PubMed  Google Scholar 

  • Machella, T. E., and Griffith, J. Q. (1942). The digestive system. In Griffith, J. Q., and Farris, E. J. (eds.),The Rat in Laboratory Investigation J. B. Lippincott, Philadelphia, p. 164.

    Google Scholar 

  • Mains, R. E., Eipper, B. A., and Ling, N. (1977). Common precursor to corticotropins and endorphins.Proc. Nat. Acad. Sci. U. S. A. 74: 3014.

    Google Scholar 

  • Martensz, N. D., and Herbert, J. (1982). Personal communication.

  • McConnell, S. K., Baum, M. J., and Badger, T. M. (1981). Lack of correlation between naloxone-induced changes in sexual behavior and serum LH in male rats.Horm. Behav. 15: 16–35.

    PubMed  Google Scholar 

  • McIntosh, T. K., Vallano, M. L., and Barfield, R. J. (1980). Effects of morphine,β-endorphin and naloxone on catecholamine levels and sexual behavior in the male rat.Pharmacol. Biochem. Behav. 13: 435.

    PubMed  Google Scholar 

  • Meites, J., Bruni, J. F., and Van Vugt, D. A. (1979a). Effects of endogenous opiate peptides on release of anterior pituitary hormones. In Collu, R., Barbeau, A., Rochefort, J., and Ducharme, J. R. (eds.),Central Nervous System Effects of Hypothalamic Hormones and Other Peptides Raven Press, New York, p. 261.

    Google Scholar 

  • Meites, J., Bruni, J. F., Van Vugt, D. A., and Smith, A. F. (1979b). Relation of endogenous opioid peptides and morphine to neuroendocrine functions.Life Sci. 24: 1325.

    PubMed  Google Scholar 

  • Meller, R. E., Keverne, E. B., and Herbert, J. (1980). Behavioural and endocrine effects of naltrexone in male talapoin monkeys.Pharmacol. Biochem. Behav. 13: 663.

    PubMed  Google Scholar 

  • Mendelson, J. H., Meyer, R. E., Ellingboe, J., Mirin, S. M., and McDougle, M. (1975). Effects of heroin and methadone on plasma cortisol and testosterone.J. Pharmacol. Exp. Ther. 195: 296.

    PubMed  Google Scholar 

  • Mendelson, J. H., Ellingboe, J., Keuhnle, J. L., and Mello, N. K. (1979). Effects of naltrexone on mood and neuroendocrine function in normal adult males.Psychoneuroendocrinology 3: 231.

    Google Scholar 

  • Meyerson, B. J., and Terenius, L. (1977).β-endorphin and male sexual behavior.Europe. J. Pharmacol. 42: 191.

    Google Scholar 

  • Michael, R. P., and Zumpe, D. (1970). Sexual initiating behaviour by female rhesus monkeys (Macaca mulatta) under laboratory conditions.Behaviour 36: 168.

    Google Scholar 

  • Monferini, E., Strada, D., and Manara, L. (1981). Evidence for opiate receptor binding in rat small intestine.Life Sci. 29: 595.

    PubMed  Google Scholar 

  • Murphy, M. R. (1981). Methadone reduces sexual performance and sexual inactivation in the male Syrian golden hamster.Pharmacol. Biochem. Behav. 14: 561.

    PubMed  Google Scholar 

  • Myers, B. M., and Baum, M. J. (1979). Facilitation by opiate antagonists of sexual performance in the male rat.Pharmacol. Biochem. Behav. 10: 615.

    PubMed  Google Scholar 

  • Naggar, A. N., Toner, J. P., and Adler, N. T. (1980). Induction of the “stretching response” by vagino-cervical stimulation in the rat.Physiol. Behav. 24: 1041.

    PubMed  Google Scholar 

  • Nakanishi, S., Inoue, A., Kita, T., Nakamura, M., Chang, A. C. Y., Cohen, S. N., and Numa, S. (1979). Nucleotide sequence of cloned cDNA for bovine corticotropin-β-lipotropin precursor.Nature (London) 278: 423.

    Google Scholar 

  • Niswender, G. D., Monroe, S. E., Peckham, W. D., Midgeley, A. R., Jr., Knobil, E., and Reichert, L. E., Jr. (1971). Radioimmunoassay for rhesus monkey luteinizing hormone (LH) with anti-ovine LH serum and ovine LH-131 I.Endocrinology 88: 1327.

    PubMed  Google Scholar 

  • Parr, D. (1977). Sexual aspects of drug abuse in narcotic addicts.Br. J. Addict. 71: 261–268.

    Google Scholar 

  • Phoenix, C. H., Slob, A. K., and Goy, R. W. (1973). Effects of castration and replacement therapy on sexual behavior of adult male rhesus monkeys.J. Comp. Physiol. Psychol. 84: 472.

    PubMed  Google Scholar 

  • Renshaw, D. C. (1978). Sex and drugs.South African Med. J. 54: 322.

    Google Scholar 

  • Robinson, J. A., and Bridson, W. E. (1978). Neonatal hormone patterns in the macaque. I. Steroids.Biol. Reprod. 19: 773.

    PubMed  Google Scholar 

  • Robinson, J. A., Scheffler, G., Eisele, S. G., and Goy, R. W. (1975). Effects of age and season on sexual behavior and plasma testosterone and dihydrotestosterone concentrations of laboratory-housed male rhesus monkeys (Macaca mulatta).Biol. Reprod. 13: 203.

    PubMed  Google Scholar 

  • Rossier, J., French, E., Rivier, C., Ling, N., Guillemin, R., and Bloom, F. E. (1977). Footshock induced stress increasesβ-endorphin levels in blood but not brain.Nature (London) 270: 618.

    Google Scholar 

  • Sholl, S. A., Robinson, J. A., and Wolf, R. C. (1979). Estrone, 17β-estradiol and cortisol in serum of peripartum rhesus monkeys.Endocrinology 104: 1274.

    PubMed  Google Scholar 

  • Siegel, S. (1956).Nonparametric Statistics for the Behavioral Sciences. McGraw-Hill, New York.

    Google Scholar 

  • Tallarida, R. J., Harakal, C., Maslow, J., Geller, E. B., and Adler, M. W. (1978). The relationship between pharmokinetics and pharmocodynamics action as applied toin vivo pA2: Applications to the analgesic effect of morphine.J. Pharmacol. Exp. Ther. 206: 38.

    PubMed  Google Scholar 

  • Terenius, L. (1975a). Comparison between narcotic “receptors” in the guinea-pig ileum and the rat brain.Acta Pharmacol. Toxicol. 37: 211.

    Google Scholar 

  • Terenius, L. (1975b). Effect of peptides and amino acids on dihydro-morphine binding to the opiate receptor.J. Pharma. Pharmacol. 27: 450.

    Google Scholar 

  • Terenius, L. (1978). Endogenous peptides and analgesia.Ann. Rev. Pharmacol. Toxicol. 18: 189.

    Google Scholar 

  • Toivola, P. T. K., Bridson, W. E., and Robinson, J. A. (1977). Effect of luteinizing hormone-releasing hormone on the secretion of luteinizing hormone, follicle-stimulating hormone, and testosterone in adult male rhesus monkeys.Endocrinology 102: 1815.

    Google Scholar 

  • Volavka, J., Cho, D., Mallya, A., and Bauman, J. (1979). Naloxone increases ACTH and cortisol levels in man.New Engl. J. Med. 300: 1056.

    Google Scholar 

  • Wallen, K., Goldfoot, D. A., and Goy, R. W. (1981). Peer and maternal influences on the expression of foot-clasp mounting by juvenile male rhesus monkeys.Dev. Psychobiol. 14: 299.

    PubMed  Google Scholar 

  • Wang, C., Chan, V., and Yeung, R. T. T. (1978). The effect of heroin addiction on pituitary-testicular function.Clin. Endocrinol. 9: 455.

    Google Scholar 

  • Watson, S. J., Akil, H., Richard, C. W., III, and Barchas, J. D. (1978). Evidence for two separate opiate peptide neuronal systems.Nature (London) 275: 226.

    Google Scholar 

  • Wiegant, V. M., Gispen, W. H., Terenius, L., and DeWied, D. (1977). ACTH-like peptides and morphine: Interaction at the level of the CNS.Psychoneuroendocrinology 2: 63.

    PubMed  Google Scholar 

  • Woods, J. H., Downs, D. A., and Carney, J. (1975). Behavioral functions of narcotic antagonists: Response-drug contingencies.Fed. Proc. 34: 1777.

    PubMed  Google Scholar 

  • Zimbardo, P. G. (1958). The effects of early avoidance training and rearing conditions upon the sexual behavior of the male rat.J. Comp. Physiol. Pyschol. 51: 764.

    Google Scholar 

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  1. David H. Abbott Ph.D.

    Present address: Department of Anatomy, University of Cambridge, Downing Street, CB2 3DY, Cambridge, England, U.K.

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  1. Wisconsin Regional Primate Research Center, 1223 Capitol Court, 53706, Madison, Wisconsin, USA

    David H. Abbott Ph.D., Stephen D. Holman, Michael Berman, Deborah A. Neff & Robert W. Goy Ph.D.

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Publication Number 22-030 of the Wisconsin Regional Primate Research Center. This work was presented in part at the Eastern Conference on Reproductive Behavior, June 22–25, 1980. The Rockefeller University, New York, New York.

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Abbott, D.H., Holman, S.D., Berman, M. et al. Effects of opiate antagonists on hormones and behavior of male and female rhesus monkeys. Arch Sex Behav 13, 1–25 (1984). https://doi.org/10.1007/BF01542974

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