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Organizational effects of testosterone, estradiol, and dihydrotestosterone on vasopressin mRNA expression in the bed nucleus of the stria terminalis

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Neuroendocrine regulation and behavior Hypothalamic control of reproductive hormones Sexual Differentiation and Disorders

Abstract

In adulthood, male rats express higher levels of arginine vasopressin (AVP) mRNA in the bed nucleus of the stria terminalis (BST) than do female rats. We tested whether this sex difference is primarily due to differences in neonatal levels of testosterone. Male and female rats were gonadectomized on the day of birth and treated with testosterone propionate (TP) or vehicle on postnatal days 1, 3, and 5 (P1, P3, and P5). Three months later, all rats were implanted with testosterone-filled capsules. Two weeks later, brains were processed for in situ hybridization to detect AVP mRNA. We found that neonatal TP treatment significantly increased the number of vasopressinergic cells in the BST over control injections. We then sought to determine the effects of testosterone metabolites, estradiol and dihydrotestosterone, given alone or in combination, on AVP expression in the BST. Rat pups were treated as described above, except that instead of testosterone, estradiol benzoate (EB), dihydrotestosterone propionate (DHTP), a combination of EB and DHTP (EB+DHTP), or vehicle was injected neonatally. Neonatal treatment with either EB or EB+DHTP increased the number of vasopressinergic cells in the BST over that of DHTP or oil treatment. However, treatment with DHTP also significantly increased the number of vasopressinergic cells over that of oil treatment. Hence, in addition to bolstering evidence that estradiol is the more potent metabolite of testosterone in causing sexual differentiation of the brain, these data provide the first example of a masculinizing effect of a nonaromatizable androgen on a sexually dimorphic neuropeptide system.

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References

1983The origin of the vasopressinergic and oxytocinergic innervation of the rat brain with special reference to the lateral septum 1988Septal vasopressin modulates social memory in male rats 1985Vasopressin cells in the bed nucleus of the stria terminalis of the rat: sex differences and the influence of androgens 1994Sex differences in the effects of testosterone and its metabolites on vasopressin messenger RNA levels in the bed nucleus of the stria terminalis of rats 1990Androgen-dependent vasopressinergic neurons are involved in social recognition in rats 1993Differential lateral septal vasopressin innervation in aggressive and nonaggressive male mice 1981Sex-dependent effects of amygdaloid lesions on the social play of prepubertal rats 1989Sex differences in vasopressin neurons in the bed nucleus of the stria terminalis by in situ hybridization

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2006Oxytocin and Vasopressin: Genetics and Behavioral Implications 2005Estrogen receptor‐α distribution in male rodents is associated with social organization 2005Sexual dimorphism in the vasopressin system: Lack of an altered behavioral phenotype in female V1a receptor knockout mice 2012Sexually dimorphic effects of a prenatal immune challenge on social play and vasopressin expression in juvenile rats

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