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Unexpected Effects of Perinatal Gonadal Hormone Manipulations on Sexual Differentiation of the Extrahypothalamic Arginine-Vasopressin System in Prairie Voles

Program in Neuroscience and Department of Psychology (J.S.L.), Michigan State University, East Lansing, Michigan 48823; and Center for Neuroendocrine Studies (B.D.R., G.J.D.), University of Massachusetts, Amherst, Massachusetts 01003

Address all correspondence and requests for reprints to: Program in Neuroscience, Department of Psychology, Giltner Hall, Michigan State University, East Lansing, Michigan 48823. E-mail: lonstein{at}msu.edu.

The sexually dimorphic extrahypothalamic arginine-vasopressin (AVP) projections from the bed nucleus of the stria terminalis to the lateral septum (LS) and lateral habenula (LHb) are denser in males than females and, in rats, require males’ perinatal exposure to gonadal hormones but the absence of such exposure in females. We examined perinatal hormone effects on development of this sex difference in prairie voles (Microtus ochrogaster), which show atypical effects of hormones on sexual differentiation of some reproductive behaviors. Neonatal castration reduced the number of AVP mRNA-expressing cells in the bed nucleus of the stria terminalis and AVP immunoreactivity (ir) in the LS and LHb. Surprisingly, daily injections of 1000 µg of testosterone propionate (TP) during the first postnatal week did not maintain high levels of AVP-ir in neonatally castrated males. Furthermore, perinatal treatments with TP (75, 500, or 1000 µg), testosterone (100 µg), or dihydrotestosterone (200 µg) did not masculinize AVP-ir in the female LS or LHb. In fact, 1000 µg TP reduced it in some cases. However, 1000 µg TP lengthened anogenital distance, indicating that TP was biologically active. Neonatal estrogen receptor antagonism with tamoxifen reduced AVP-ir in the male LS, whereas treating neonatal females with the synthetic estrogen diethylstilbestrol increased septal AVP-ir. Tamoxifen and diethylstilbestrol had no effects in the LHb. Similar to rats, therefore, postnatal estrogen influences some components of the extrahypothalamic AVP system in prairie voles, but this developing system appears to be insensitive to exogenous androgens, including aromatizable androgens. Such insensitivity is atypical for a sexually dimorphic neural system in a rodent and may reflect the unusual effects of hormones on sexual differentiation of some behaviors in prairie voles.