Skip to main content
Log in

Mating alters topography and content of oxytocin immunoreactivity in male mouse brain

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Sexual stimulation of males has been reported to affect hypothalamic oxytocinergic systems. In the present study we used radioimmunoassays of micro-dissected forebrain regions and immunocytochemical analysis of Vibratome sections to study the oxytocin systems of naive males, males killed after one mating, and males mated daily with different receptive females for 3 weeks. In males that had mated once, less oxytocin-immunoreactive neurons were observed in the paraventricular (PVN), supraoptic (SON) and periventricular (NPE) nuclei than in naive males. However, after repeated matings, the number of immunoreactive neurons and their staining intensity was increased in these regions. Furthermore, additional oxytocinergic neurons could be found in the lateral subcommissural nucleus, the zona incerta and the ansa lenticularis of repeatedly mated males. Oxytocin-immunoreactive neurons were only occasionally seen in these areas in unmated males or in animals that had been killed after initial mating. Radio-immunoassays of microdissected PVN, SON, NPE and the lateral hypothalamus confirmed the reduction in oxytocin-immunoreactive levels after a first mating by a male and the increase after repeated matings. It is likely that oxytocin secretion into peripheral and portal circulation is stimulated by the endocrine conditions associated with initial mating. These immediate effects may be followed by the activation of synthesis in oxytocin neurons in several sites of the basal forebrain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Agmo A, Anderson R, Johanson C (1978) Effect of oxytocin on sperm numbers in spontanous rat ejaculates. Biol Rep 18:346–349

    Google Scholar 

  • Antoni FA, Kovacs KJ, Dohanits J, Makara GB, Holmes MC, Mazurek MF (1988) Hypophyseotrophic function of vascopressin and oxytocin. Brain Res Bull 20:729–736

    Google Scholar 

  • Argiolas A, Gessa GL (1987) Oxytocin: a powerful stimulant of penile erection and yawning in male rats. In: Nerozzi M, Goodwin H, Costa RA (eds) Hypothalamic dysfunction in neuropsychiatric disorders. Raven Press, New York, pp 42–65

    Google Scholar 

  • Buijs RM, Van Heerikhuizen JJ (1982) Vasopresin and oxytocin release in the brain—a synaptic event. Brain Res 252:71–76

    Google Scholar 

  • Buijs RM, Swaab DF, Dorgertom J, Van Leeuwen FW (1978) Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat. Cell Tissue Res 186:423–433

    Google Scholar 

  • Caldwell JD, Greer ER, Johnson MF, Prange AJ Jr, Pedersen CA (1987) Oxytocin and vasopressin immunoreactivity in hypothalamic and extrahypothalamic sites in late pregnancy and post-partum rats. Neuroendocrinology 14:39–47

    Google Scholar 

  • Caldwell JD, Jirikowski GF, Greer ER, Stumpf WE, Pedersen CA (1988) Ovarian steroids and sexual interaction alter oxytocinergic content and distribution in the basal forebrain. Brain Res 446:236–244

    Google Scholar 

  • Caldwell JD, Brooks PJ, Jirikowski GF, Barakat A, Lund PK, Pedersen CA (1989) Estrogen alters oxytocin production in the preoptic area. J Neuroendocrinology 1:273–278

    Google Scholar 

  • Christensen LW, Clemens LG (1974) Intrahypothalamic implants of testosterone or estradiol and resumption of masculine sexual behavior in long-term castrated male rats. Encodrinology 95:984–990

    Google Scholar 

  • Davidson JM (1966) Activation of the male rat's sexual behaviour by intracerebral implantation of androgen. Endocrinology 79:783–794

    Google Scholar 

  • De Vries GJ, Buijs RM (1983) The origin of the vasopressinergic and oxytocinergic innervation of the rat brain with special reference to the lateral septum. Brain Res 273:307–314

    Google Scholar 

  • Dewsbury DA (1973) II. Copulatory behavior of deer mice. J Comp Physiol Psych 93:1778–1888

    Google Scholar 

  • Everitt BJ, Lightman SL, Hughes ASM (1985) Oxytocin and sexual behavior in the male rat and rabbit. In: Everitt BJ, Lightman SL, Hughes AM (eds) Proc Brit Neuroendocrine Group No 57. Oxford University Press Oxford, p 126

    Google Scholar 

  • Fuchs AR (1972) Uterine activation during and after mating in the rabbit. Fert Ster 23:915–923

    Google Scholar 

  • Fuchs AR, Cubile L, Dawood MY (1981) Effects of mating on levels of oxytocin and prolactin in the plasma of male and female rabbits. J Endocrinology 90:245–253

    Google Scholar 

  • Gray GD, Smith ER, Davidson JM (1980) Hormonal regulation of penile erection in castrated male rabbits. Physiol Behav 24:463–468

    Google Scholar 

  • Greer ER, Caldwell JD, Johnson MF, Prange AJ Jr, Pedersen CA (1986) Variations in concentration of oxytocin and vasopressin in the paraventricular nucleus of the hypothalamus during the estrous cycle in the rat. Life Sci 38:2311–2318

    Google Scholar 

  • Häussler HU, Jirikowski GF, Caldwell JD, Pilgrim C (1990) Sex differences among oxytocin immunoreactive neuronal systems in the mouse hypothalamus. J Chem Neuroanat 3:271–276

    Google Scholar 

  • Heimer L, Larsson LI (1966) Impairment of mating behaviour in male rats following lesions in the preoptic anterior hypothalamic continuum. Brain Res 3:248–263

    Google Scholar 

  • Hughes AM, Everitt BJ, Lightman SL, Todd K (1987) Oxytocin in the central nervous system and sexual behaviour in male rats. Brain Res 414:133–137

    Google Scholar 

  • Jirikowski GF, Caldwell JD, Pedersen CA, Stumpf WE (1988) Estradiol influences oxytocin immunoreactive brain systems. Neuroscience 25:237–248

    Google Scholar 

  • Jirikowski GF, Caldwell JD, Pilgrim C, Stumpf WE, Pedersen CA (1989) Changes in immunostaining for oxytocin in the forebrain of the female rat during late pregnancy, parturition and early lactation. Cell Tissue Res 256:411–417

    Google Scholar 

  • Johnston Ca, Negro-Villar A (1988) Role of oxytocin on prolactin secretion during proestrus and in different physiological or pharmacological paradigms. Endocrinology 122:341–350

    Google Scholar 

  • Miller FD, Ozimek G, Milner RJ, Bloom FE (1988) Regulation of neuronal oxytocin mRNA by ovarian steroids in the mature and developing hypothalamus. Proc Natl Acad Sci USA 86:2468–2472

    Google Scholar 

  • Niemi M, Kormano M (1965) Contractility of the semiferous tubule of the postnatal rat testis and its response to oxytocin. Ann Med Exp Fenn 43:40–42

    Google Scholar 

  • Ogawa S, Kudo S, Kitsunai Y, Fukuchi S (1980) Increase in oytocin secretion at ejaculation in male. Clin Endocrinol 13:95–97

    Google Scholar 

  • Palkovits M (1973) Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res 59:449–450

    Google Scholar 

  • Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic Press, Sydney New York London

    Google Scholar 

  • Rhodes CH, Morell JJ, Pfaff DW (1981) Changes in oxytocin content in the magnocellular neurons following water deprivation or estrogen treatment. Cell Tissue Res 216:47–55

    Google Scholar 

  • Robinson ICAF (1980) The development and evaluation of a sensitive and specific RIA for oxytocin in unextracted plasma. J Immunoassay 1:323–347

    Google Scholar 

  • Roselli E, Ellinwood WE, Resko JA (1984) Regulation of brain aromatase activity in male rats. Endocrinology 114:192–200

    Google Scholar 

  • Sachs BD, Barfield RJ (1970) Temporal patterning of sexual behavior in the male rat. J Comp Physiol Psych 73:359–364

    Google Scholar 

  • Sharma OP, Hays RL (1976) A possible role of oxytocin in sperm transport in the male rabbit. J Endocrinol 68:43–47

    Google Scholar 

  • Schumacher M, Balthazart J (1986) Testosterone-induced brain aromatase in sexually dimorphic. Brain Res 370:285–293

    Google Scholar 

  • Sofroniew MV (1985) Vasopressin, oxytocin and their related neurophysins. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy, vol 4, part 1. Elsevier, Amsterdam, pp 93–165

    Google Scholar 

  • Stoneham MD, Everitt BJ, Lightman SL, Todd R, hansen S (1983) The role of oxytocin in male reproduction. J Anat 139:17–21

    Google Scholar 

  • Stoneham MD, Everitt BJ, Hansen S, Lightman SL, Todd R (1985) Oxytocin and sexual behaviour in the male rat and rabbit. J Endocrinol 107:97–106

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jirikowski, G.F., Caldwell, J.D., Häussler, H.U. et al. Mating alters topography and content of oxytocin immunoreactivity in male mouse brain. Cell Tissue Res 266, 399–403 (1991). https://doi.org/10.1007/BF00318196

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00318196

Key words

Navigation