Androgenic and oestrogenic influences on tyrosine hydroxylase-immunoreactive cells of the prairie vole medial amygdala and bed nucleus of the stria terminalis

Abstract

The posterodorsal medial amygdala (MeApd) and principal nucleus of the bed nucleus of the stria terminalis (pBST) are densely interconnected sites integrating steroid hormone and olfactory information necessary for sociosexual behaviours in many rodents. Our laboratory recently reported sexually dimorphic populations of cells containing tyrosine hydroxylase (TH) located in the MeApd and pBST of prairie voles (Microtus ochrogaster), with males having many more TH-immunoreactive (-ir) cells in these sites than do females. Gonadal hormones circulating during adulthood were showm to regulate this sex difference because it was eliminated by castrating adult males or implanting females with testosterone-filled capsules. In the present study, we demonstrate that many (25-65%) TH-ir cells in the MeApd and pBST of adult virgin male and female prairie voles also contain immunoreactivity for either the androgen receptor or oestrogen receptor alpha. Subcutaneous implants of oestradiol benzoate mimicked the effects of testosterone and maintained high numbers of TH-ir cells in these sites in castrated males. However, implants of dihydrotestosterone (DHT) did not, and these males had low numbers of TH-ir cells similar to castrated males given empty capsules. A similar effect was found in females, where testosterone or oestradiol benzoate greatly increased the number of TH-ir cells in these sites compared to intact or ovariectomised controls, but DHT did not. DHT implants did, however, maintain high seminal vesicle weights in males. Thus, many of the TH-ir cells in the prairie vole MeApd and pBST are potentially sensitive to androgens and oestrogens, although maintaining immunocytochemically detectable levels of TH in these cells may depend more on an oestrogen-mediated mechanism in both sexes. These data have implications for understanding how gonadal hormone release across the reproductive cycle modulates these species-specific groups of catecholaminergic cells and socially monogamous behaviours in prairie voles.

Figure 1

Photomicrograph of the pBST of a male prairie vole showing representative cells immunoreactive for TH alone (small black arrows, blue cytoplasmic label), immunoreactive for AR alone (medium gray arrows, brown nuclear label), and immunoreactive for both TH and AR (large black arrows, blue cytoplasmic plus brown nuclear labels). LV = lateral ventricle.

Figure 2

Photomicrograph of cells in the pBST of a male prairie vole showing representative cells immunoreactive for TH alone (small black arrows, blue cytoplasmic label), immunoreactive for ERα alone (medium gray arrows, brown nuclear label), and immunoreactive for both TH and ERα (large black arrows, blue cytoplasmic plus brown nuclear labels). LV = lateral ventricle.

Figure 3

Number (Mean ± SEM) of TH-ir cells in the MeApd (left) and pBST (right) of male prairie voles that were gonadally intact (Sham; n = 10), castrated and implanted with an empty capsule (GDX; n = 10), or castrated and implanted with a capsule containing T (n = 8), DHT (n = 9), or EB (n = 9). Significant differences among groups indicated by different letters above bars, p < 0.05.

Figure 4

Photomicrographs of TH-ir cells in the pBST of representative male (top) and female (bottom) prairie voles that were gonadally intact (Sham) or gonadectomized (GDX) and implanted with an empty capsule or one filled with T, DHT, or EB. LV = lateral ventricle.

Figure 5

Number (Mean ± SEM) of TH-ir cells in the MeApd (left) and pBST (right) of female prairie voles that were gonadally intact (Sham; n = 10), ovariectomized and implanted with an empty capsule (GDX; n = 9), or ovariectomized and implanted with a capsule containing T (n = 9), DHT (n = 11), or EB (n = 11). Significant differences among groups indicated by different letters above bars, p < 0.05.