Abstract
The neural mechanisms controlling sexual behavior are sexually differentiated by the perinatal actions of sex steroid hormones. We recently observed using female mice deficient in alpha-fetoprotein (AFP-KO) and which lack the protective actions of AFP against maternal estradiol, that exposure to prenatal estradiol completely defeminized the potential to show lordosis behavior in adulthood. Furthermore, AFP-KO females failed to show any male-directed mate preferences following treatment with estradiol and progesterone, indicating a reduced sexual motivation to seek out the male. In the present study, we asked whether neural responses to male- and female-derived odors are also affected in AFP-KO female mice. Therefore, we compared patterns of Fos, the protein product of the immediate early gene, c-fos, commonly used as a marker of neuronal activation, between wild-type (WT) and AFP-KO female mice following exposure to male or estrous female urine. We also tested WT males to confirm the previously observed sex differences in neural responses to male urinary odors. Interestingly, AFP-KO females showed normal, female-like Fos responses, i.e. exposure to urinary odors from male but not estrous female mice induced equivalent levels of Fos protein in the accessory olfactory pathways (e.g. the medial part of the preoptic nucleus, the bed nucleus of the stria terminalis, the amygdala, and the lateral part of the ventromedial hypothalamic nucleus) as well as in the main olfactory pathways (e.g. the piriform cortex and the anterior cortical amygdaloid nucleus), as WT females. By contrast, WT males did not show any significant induction of Fos protein in these brain areas upon exposure to either male or estrous female urinary odors. These results thus suggest that prenatal estradiol is not involved in the sexual differentiation of neural Fos responses to male-derived odors.
Highlights
In mice, body odors provide essential information about the sex, social, and reproductive status of conspecifics [1] and may play a key role in mate recognition and mate preferences
Accessory olfactory pathway Overall, in WT females as well as in AFP-KO females, exposure to male urine, but not to estrous female urine, induced a significant expression of Fos in several brain regions receiving inputs from the accessory olfactory bulbs, including parts of the amygdala (MeA, MePV, MePD), the MPOA, the BnST and the VMH-vl (Fig. 1). These neural Fos responses to intact male urine were sexually dimorphic for all analyzed regions of the accessory olfactory pathways with only females (WT and AFP-KO), but not males, showing significant Fos activation
ANOVA on the number of Fos-ir cells showed a significant interaction between sex, genotype and odor exposure in the MeA (F(4,63) = 13.38, P,0.001), MePD (F(4,63) = 9.64, P,0.001), MePV (F(4,63) = 6.16, P,0.001), MPOA (F(4,63) = 12.75, P,0.001), BnST (F(4,63) = 14.98, P,0.001) and the VMH-vl (F(4,63) = 16.88, P,0.001). In all of these brain regions, post hoc analysis indicated that females (WT and AFP-KO) showed significantly more Fos-ir cells when exposed to intact male urine, but not to estrous female urine, compared to females (WT and AFP-KO) exposed to deionized water
Summary
Body odors provide essential information about the sex, social, and reproductive status of conspecifics [1] and may play a key role in mate recognition and mate preferences These socially relevant odors are detected by either the main or the accessory olfactory system or both. Sex differences in immediate early gene (c-Fos) responses were observed along the entire accessory olfactory projection pathway when mice were exposed to bedding soiled by gonadally intact males [7]. These sex differences may reflect the perinatal action of estradiol in the male brain as male rats treated neonatally with an aromatase inhibitor
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