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Previous studies have demonstrated that oxytocin receptors in specific nuclei of rat forebrain are regulated by gonadal steroids. The current study used in vitro receptor autoradiography to investigate the distribution and regulation of oxytocin receptors in the forebrain of the female prairie vole (Microtus ochrogaster). In contrast to rats, in female prairie voles gonadal steroid secretion and oestrus behaviour result from male chemosignal stimulation and ovulation is induced by mating. Thus, the prairie vole brain provides an opportunity for investigating links between environmental stimuli, gonadal steroids and oxytocin receptors. Using a selective oxytocin receptor ligand [I-125]d(CH2)5[Tyr(Me)2,Tyr-NH2(9)]ornithine vasotocin I-125]OTA), specific binding was found in several regions including the anterior olfactory nucleus, the ventromedial nucleus of the hypothalamus, the bed nucleus of the stria terminalis, the amygdala and several cortical areas. Following ovariectomy, oestradiol benzoate (10-mu-g) administration increased oxytocin receptor binding 100% in the anterior olfactory nucleus, but did not affect receptors in other regions. Gonadally-intact females, exposed to male chemosignals, had significant increases in both endogenous oestradiol levels and anterior olfactory nucleus oxytocin receptor binding relative to gonadally-intact females unexposed to male chemosignals. Following prolonged exposure to males with ad libitum mating, [I-125]OTA receptor binding decreased to the levels found in unstimulated females. These results demonstrate that increases in oestrogen levels, of either exogenous or endogenous origin, can modulate oxytocin receptors in the brains of female prairie voles. In contrast to rats, oestrogen in female prairie voles appears to affect receptors in the anterior olfactory nucleus rather than the hypothalamus. We suggest that the species differences in oxytocin receptor distribution and gonadal steroid responsiveness reflect variations in reproductive physiology and possibly behaviour