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See detailClick-Evoked Otoacoustic Emissions in Children and Adolescents with Gender Identity Disorder.
Burke, Sarah M.; Menks, Willeke M.; Cohen-Kettenis, Peggy T. et al

in Archives of sexual behavior (2014)

Click-evoked otoacoustic emissions (CEOAEs) are echo-like sounds that are produced by the inner ear in response to click-stimuli. CEOAEs generally have a higher amplitude in women compared to men and ... [more ▼]

Click-evoked otoacoustic emissions (CEOAEs) are echo-like sounds that are produced by the inner ear in response to click-stimuli. CEOAEs generally have a higher amplitude in women compared to men and neonates already show a similar sex difference in CEOAEs. Weaker responses in males are proposed to originate from elevated levels of testosterone during perinatal sexual differentiation. Therefore, CEOAEs may be used as a retrospective indicator of someone's perinatal androgen environment. Individuals diagnosed with Gender Identity Disorder (GID), according to DSM-IV-TR, are characterized by a strong identification with the other gender and discomfort about their natal sex. Although the etiology of GID is far from established, it is hypothesized that atypical levels of sex steroids during a critical period of sexual differentiation of the brain might play a role. In the present study, we compared CEOAEs in treatment-naive children and adolescents with early-onset GID (24 natal boys, 23 natal girls) and control subjects (65 boys, 62 girls). We replicated the sex difference in CEOAE response amplitude in the control group. This sex difference, however, was not present in the GID groups. Boys with GID showed stronger, more female-typical CEOAEs whereas girls with GID did not differ in emission strength compared to control girls. Based on the assumption that CEOAE amplitude can be seen as an index of relative androgen exposure, our results provide some evidence for the idea that boys with GID may have been exposed to lower amounts of androgen during early development in comparison to control boys. [less ▲]

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See detailHypothalamic response to the chemo-signal androstadienone in gender dysphoric children and adolescents.
Burke, Sarah M.; Cohen-Kettenis, Peggy T.; Veltman, Dick J. et al

in Frontiers in endocrinology (2014), 5

The odorous steroid androstadienone, a putative male chemo-signal, was previously reported to evoke sex differences in hypothalamic activation in adult heterosexual men and women. In order to investigate ... [more ▼]

The odorous steroid androstadienone, a putative male chemo-signal, was previously reported to evoke sex differences in hypothalamic activation in adult heterosexual men and women. In order to investigate whether puberty modulated this sex difference in response to androstadienone, we measured the hypothalamic responsiveness to this chemo-signal in 39 pre-pubertal and 41 adolescent boys and girls by means of functional magnetic resonance imaging. We then investigated whether 36 pre-pubertal children and 38 adolescents diagnosed with gender dysphoria (GD; DSM-5) exhibited sex-atypical (in accordance with their experienced gender), rather than sex-typical (in accordance with their natal sex) hypothalamic activations during olfactory stimulation with androstadienone. We found that the sex difference in responsiveness to androstadienone was already present in pre-pubertal control children and thus likely developed during early perinatal development instead of during sexual maturation. Adolescent girls and boys with GD both responded remarkably like their experienced gender, thus sex-atypical. In contrast, pre-pubertal girls with GD showed neither a typically male nor female hypothalamic activation pattern and pre-pubertal boys with GD had hypothalamic activations in response to androstadienone that were similar to control boys, thus sex-typical. We present here a unique data set of boys and girls diagnosed with GD at two different developmental stages, showing that these children possess certain sex-atypical functional brain characteristics and may have undergone atypical sexual differentiation of the brain. [less ▲]

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See detailAssessment of urinary pheromone discrimination, partner preference, and mating behaviors in female mice.
Brock, Olivier; Bakker, Julie ULg; Baum, Michael J.

in Methods in molecular biology (Clifton, N.J.) (2013), 1068

Behavioral testing methods are described for determining whether female mice can discriminate between volatile urinary pheromones of conspecifics of the same vs. opposite sex and/or in different endocrine ... [more ▼]

Behavioral testing methods are described for determining whether female mice can discriminate between volatile urinary pheromones of conspecifics of the same vs. opposite sex and/or in different endocrine conditions, for determining sexual partner preference, for quantifying receptive (lordosis) behavior, and for monitoring the expression of male-typical mounting behavior in female mice. [less ▲]

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See detailRoles of sex and gonadal steroids in mammalian pheromonal communication.
Baum, Michael J.; Bakker, Julie ULg

in Frontiers in neuroendocrinology (2013), 34(4), 268-84

A brain circuit (the accessory olfactory system) that originates in the vomeronasal organ (VNO) and includes the accessory olfactory bulb (AOB) plus additional forebrain regions mediates many of the ... [more ▼]

A brain circuit (the accessory olfactory system) that originates in the vomeronasal organ (VNO) and includes the accessory olfactory bulb (AOB) plus additional forebrain regions mediates many of the effects of pheromones, typically comprised of a variety of non-volatile and volatile compounds, on aspects of social behavior. A second, parallel circuit (the main olfactory system) that originates in the main olfactory epithelium (MOE) and includes the main olfactory bulb (MOB) has also been shown to detect volatile pheromones from conspecifics. Studies are reviewed that point to specific roles of several different steroids and their water-soluble metabolites as putative pheromones. Other studies are reviewed that establish an adult, 'activational' role of circulating sex hormones along with sex differences in the detection and/or processing of non-steroidal pheromones by these two olfactory circuits. Persisting questions about the role of sex steroids in pheromonal processing are posed for future investigation. [less ▲]

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See detailThe two kisspeptin neuronal populations are differentially organized and activated by estradiol in mice.
Brock, Olivier; Bakker, Julie ULg

in Endocrinology (2013)

In rodents, kisspeptin expressing neurons are localized in two hypothalamic brain nuclei [anteroventral periventricular nucleus/periventricular nucleus continuum (AVPv/PeN) and arcuate nucleus (ARC)] and ... [more ▼]

In rodents, kisspeptin expressing neurons are localized in two hypothalamic brain nuclei [anteroventral periventricular nucleus/periventricular nucleus continuum (AVPv/PeN) and arcuate nucleus (ARC)] and modulated by sex steroids. By using wild-type (WT) and aromatase knockout mice (ArKO, which cannot convert testosterone into estradiol) and immunohistochemistry, we observed that WT females showed a continuous increase in kisspeptin peptide expression in the ARC across postnatal ages (P5 to P25), whereas WT males did not show any expression before P25. Kisspeptin peptide expression was also present in ArKO females but did not increase over this early postnatal period, suggesting that kisspeptin peptide expression in the ARC is organized by estradiol-dependent and -independent mechanisms. We also compared kisspeptin peptide expression between groups of adult male and female mice which were left gonadally intact or gonadectomized and treated or not with estradiol (E2) or dihydrotestosterone (DHT). In the ARC, kisspeptin peptide expression decreased after gonadectomy but was completely rescued by either E2 or DHT treatment in each sex/genotype. However, kisspeptin peptide expression was lower in ArKO compared to WT subjects. In the AVPv/PeN, ArKO females showed a male-typical kisspeptin peptide expression, and adult E2 treatment partially restored kisspeptin peptide expression. Finally, we showed that, after E2 treatment of WT and ArKO mice between either P5 and P15 or P15 and P25, AVPv/PeN kisspeptin peptide expression could be still masculinized at P5, but was feminized from P15 onwards. In conclusion, the two kisspeptin neuronal populations (AVPv/PeN versus ARC) seem to be differentially organized and activated by E2. [less ▲]

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See detailSex differences in the neurokinin B system in the human infundibular nucleus.
Taziaux, Mélanie ULg; Swaab, Dick F.; Bakker, Julie ULg

in Journal of Clinical Endocrinology and Metabolism (2012), 97(12), 2210-20

CONTEXT: The recent report that loss-of-function mutations in either the gene encoding neurokinin B (NKB) or its receptor (NK3R) produce gonadotropin deficiencies in humans strongly points to NKB as a key ... [more ▼]

CONTEXT: The recent report that loss-of-function mutations in either the gene encoding neurokinin B (NKB) or its receptor (NK3R) produce gonadotropin deficiencies in humans strongly points to NKB as a key regulator of GnRH release. OBJECTIVES: We used NKB immunohistochemistry on postmortem human brain tissue to determine: 1) whether the human NKB system in the infundibular nucleus (INF) is sexually dimorphic; 2) at what stage in development the infundibular NKB system would diverge between men and women; 3) whether this putative structural difference is reversed in male-to-female (MtF) transsexual people; and 4) whether menopause is accompanied by changes in infundibular NKB immunoreactivity. METHODS: NKB immunohistochemical staining was performed on postmortem hypothalamus material of both sexes from the infant/pubertal period into the elderly period and from MtF transsexuals. RESULTS: Quantitative analysis demonstrated that the human NKB system exhibits a robust female-dominant sexual dimorphism in the INF. During the first years after birth, both sexes displayed a moderate and equivalent level of NKB immunoreactivity in the INF. The adult features emerged progressively around puberty until adulthood, where the female-dominant sex difference appeared and continued into old age. In MtF transsexuals, a female-typical NKB immunoreactivity was observed. Finally, in postmenopausal women, there was a significant increase in NKB immunoreactivity compared to premenopausal women. CONCLUSION: Our results indicate that certain sex differences do not emerge until adulthood when activated by sex steroid hormones and the likely involvement of the human infundibular NKB system in the negative and positive feedback of estrogen on GnRH secretion. [less ▲]

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See detailHeterosexual men and women both show a hypothalamic response to the chemo-signal androstadienone.
Burke, Sarah M.; Veltman, Dick J.; Gerber, Johannes et al

in PLoS ONE (2012), 7(7), 40993

The odorous steroid compound 4,16-androstadien-3-one (androstadienone), found in axillary sweat, was previously reported to evoke hypothalamic activation in heterosexual women, but not in heterosexual men ... [more ▼]

The odorous steroid compound 4,16-androstadien-3-one (androstadienone), found in axillary sweat, was previously reported to evoke hypothalamic activation in heterosexual women, but not in heterosexual men. However, subjects were exposed to the pure crystalline form of androstadienone, which raised the question whether the observed hypothalamic response is physiologically relevant. Therefore, in the present study, we asked whether sexually dimorphic hypothalamic responses could be measured when subjects were exposed to lower, more physiologically relevant concentrations of androstadienone. A total of 21 women and 16 men, all heterosexual, participated in our functional magnetic resonance imaging study (fMRI). Three different concentrations of androstadienone diluted in propylene glycol (10 mM "high," 0.1 mM "medium" and 0.001 mM "low") were delivered to the subjects' nostrils using a computer-controlled stimulator. When exposed to the "high" androstadienone concentration, women showed stronger hypothalamic activation than men. By contrast, men showed more hypothalamic activation when exposed to the "medium" androstadienone concentrations in comparison to women. Thus, we replicated that smelling the chemo-signal androstadienone elicits a hypothalamic activation. However, this effect does not seem to be gender-specific, because androstadienone activated the hypothalamus in both men and women, suggesting that androstadienone exerts specific effects in heterosexual individuals of both sexes. [less ▲]

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See detailFemale mice deficient in alpha-fetoprotein show female-typical neural responses to conspecific-derived pheromones.
Brock, Olivier; Keller, Matthieu; Douhard, Quentin et al

in PLoS ONE (2012), 7(6), 39204

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 ... [more ▼]

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. [less ▲]

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See detailAromatase knockout mice show normal steroid-induced activation of gonadotrophin-releasing hormone neurones and luteinising hormone surges with a reduced population of kisspeptin neurones in the rostral hypothalamus.
Szymanski, L.; Bakker, Julie ULg

in Journal of Neuroendocrinology (2012), 24(9), 1222-33

We recently reported that female aromatase knockout (ArKO) mice show deficits in sexual behaviour and a decreased population of kisspeptin-immunoreactive neurones in the rostral periventricular area of ... [more ▼]

We recently reported that female aromatase knockout (ArKO) mice show deficits in sexual behaviour and a decreased population of kisspeptin-immunoreactive neurones in the rostral periventricular area of the third ventricle (RP3V), resurrecting the question of whether oestradiol actively contributes to female-typical sexual differentiation. To further address this question, we assessed the capacity of ArKO mice to generate a steroid-induced luteinising hormone (LH) surge. Adult, gonadectomised wild-type (WT) and ArKO mice were given silastic oestradiol implants s.c. and, 1 week later, received s.c. injections of either oestradiol benzoate (EB) followed by progesterone, EB alone, or no additional steroids to activate gonadotrophin-releasing hormone (GnRH) neurones and generate an LH surge. Treatment with EB and progesterone induced significant Fos/GnRH double-labelling and, consequently, an LH surge in female WT and in ArKO mice of both sexes but not in male WT mice. ArKO mice of both sexes had fewer cells expressing Kiss-1 mRNA in the RP3V compared to female WT mice but had more Kiss-1 mRNA-expressing cells compared to WT males, reflecting an incomplete sexual differentiation of this system. To determine the number of cells expressing kisspeptin, the same experimental design was repeated in Experiment 2 with the addition of groups of WT and ArKO mice that were given EB + progesterone and sacrificed 2 h before the expected LH surge. No differences were observed in the number of kisspeptin-immunoreactive cells 2 h before and at the time of the LH surge. The finding that ArKO mice of both sexes have a competent LH surge system suggests that oestradiol has predominantly defeminising actions on the GnRH/LH surge system in males and that the steroid-induced LH surge can occur in females even with a greatly reduced population of kisspeptin neurones in the RP3V. [less ▲]

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See detailRapid activation of phosphorylated mitogen-activated protein kinase after sexual stimulation in male mice.
Taziaux, Mélanie ULg; Keller, Matthieu; Balthazart, Jacques ULg et al

in Neuroreport (2011), 22(6), 294-8

We mapped cells immunoreactive for the phosphorylated form (p44/p42) of the mitogen-activated protein kinase (pMAPK--also known as ERK1/2) in the brain of male mice after exposure to female olfactory cues ... [more ▼]

We mapped cells immunoreactive for the phosphorylated form (p44/p42) of the mitogen-activated protein kinase (pMAPK--also known as ERK1/2) in the brain of male mice after exposure to female olfactory cues or after the display of male copulatory behaviors. Exposure to soiled bedding from estrous females or the display of coital behaviors rapidly (within 10 min) induced MAPK phosphorylation in most of the brain regions known to be involved in the processing of olfactory cues (main and accessory olfactory bulbs, amygdala, and medial preoptic area) and in the control of copulatory behavior (amygdala and medial preoptic area). MAPK phosphorylation thus seems to be a useful marker to study short-term neural activation associated with the expression of specific behaviors. [less ▲]

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See detailThe main and accessory olfactory systems of female mice are activated differentially by dominant versus subordinate male urinary odors.
Veyrac, Alexandra; Wang, Guan; Baum, Michael J et al

in Brain Research (2011), 1402

Previous studies have shown that female preferences for male pheromones depend on the female's reproductive condition and the dominance status of the male. However, it is unknown which olfactory system ... [more ▼]

Previous studies have shown that female preferences for male pheromones depend on the female's reproductive condition and the dominance status of the male. However, it is unknown which olfactory system detects the odors that result in a preference for a dominant male. Therefore, in the present study, we asked whether dominant versus subordinate male urinary odors differentially activate the main and accessory olfactory systems in female (C57Bl/6j) mice by monitoring the induction of the immediate early gene, c-fos. A more robust induction of Fos was observed in female mice which had direct nasal contact with dominant male urinary odors in four specific segments of the accessory olfactory system, i.e., the posteroventral part of the medial amygdala, the bed nucleus of the stria terminalis, the medial part of the preoptic nucleus and the ventrolateral part of the ventromedial hypothalamus, compared to females that were exposed to subordinate male urine. This greater activation of the accessory olfactory pathway by dominant male urine suggests that there are differences in the nonvolatile components of dominant versus subordinate male urine that are detected by the vomeronasal organ. By contrast, subordinate male urinary odors induced a greater activation in the piriform cortex which is part of the main olfactory system, suggesting that female mice discriminate between dominant and subordinate male urine using their main olfactory system as well. [less ▲]

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See detailPostnatal and adult exposure to estradiol differentially influences adult neurogenesis in the main and accessory olfactory bulb of female mice.
Veyrac, Alexandra; Bakker, Julie ULg

in FASEB Journal (2011), 25(3), 1048-57

Neurons incorporated into the adult main olfactory bulb (MOB) and accessory olfactory bulb (AOB) derive from the subventricular zone (SVZ). Despite some recent studies on the role of olfactory ... [more ▼]

Neurons incorporated into the adult main olfactory bulb (MOB) and accessory olfactory bulb (AOB) derive from the subventricular zone (SVZ). Despite some recent studies on the role of olfactory neurogenesis in sociosexual behaviors mediated by hormones, data on the implication of estrogens are still lacking. Taking advantage of female aromatase-knockout (ArKO) mice, which are unable to produce estradiol across their life span, we investigated the role of estradiol exposure during early postnatal and adult periods on adult neurogenesis in the MOB and AOB. We found that proliferation of progenitor cells in the adult female SVZ was not influenced by estradiol. However, whereas adult exposure to estradiol influences the turnover of MOB newborn neurons, the survival of those in the AOB depends on exposure to estradiol during the early postnatal period. Finally, based on their expression of Zif268, we showed that newborn neurons in the MOB responded to sociosexual odors, albeit to a lesser extent in ArKO females, suggesting a contribution of estradiol during the early postnatal period to this response. Together, these results suggest that the survival and functional integration of newborn neurons in the adult female MOB and AOB are differentially influenced by estrogens from the early postnatal period to adulthood. [less ▲]

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See detailSex differences in adolescent depression: do sex hormones determine vulnerability?
Naninck, E. F. G.; Lucassen, P. J.; Bakker, Julie ULg

in Journal of Neuroendocrinology (2011), 23(5), 383-92

Depression is one of the most common, costly and severe psychopathologies worldwide. Its incidence, however, differs significantly between the sexes, and depression rates in women are twice those of men ... [more ▼]

Depression is one of the most common, costly and severe psychopathologies worldwide. Its incidence, however, differs significantly between the sexes, and depression rates in women are twice those of men. Interestingly, this sex difference emerges during adolescence. Although the adolescent period is characterised by major physical and behavioural transformations, it is unclear why the incidence of depression increases so dramatically in girls during this otherwise generally healthy developmental period. Although psychological and environmental factors are also involved, we discuss the neuroendocrinological factors determining adolescent vulnerability to depression. In particular, we address the role of sex steroids in mood regulation, hypothalamic-pituitary-adrenal axis maturation and sexual differentiation of the brain, with a focus on hippocampal plasticity. [less ▲]

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See detailThe development of female sexual behavior requires prepubertal estradiol.
Brock, Olivier; Baum, Michael J; Bakker, Julie ULg

in Journal of Neuroscience (2011), 31(15), 5574-8

The classic view of brain and behavioral sexual differentiation holds that the neural mechanisms controlling sexual behavior in female rodents develop in the absence of ovarian sex hormone actions ... [more ▼]

The classic view of brain and behavioral sexual differentiation holds that the neural mechanisms controlling sexual behavior in female rodents develop in the absence of ovarian sex hormone actions. However, in a previous study, female aromatase knock-out (ArKO) mice, which cannot convert testosterone to estradiol, showed deficient male-oriented partner preference and lordosis behaviors in response to adult ovarian hormones, raising the possibility that estradiol may contribute to the development of these female sexual behaviors. In the present experiments, administering estradiol prepubertally [between postnatal day 15 (P15) and P25] significantly enhanced the ability of ArKO female mice to display lordosis behavior in response to ovarian hormones administered later in adulthood, whereas treatment with estradiol over an earlier postnatal period (P5-P15) had no such effect. Treatment of ArKO females with estradiol between P15 and P25 also rescued their later preference to approach distal cues from an intact male over an estrous female. ArKO females also displayed significantly less female-directed (male-typical) mounting behavior than wild-type control females when treated with testosterone in adulthood. Prepubertal estradiol treatment failed to reverse this deficit in ArKO females, whereas earlier postnatal estradiol augmented later mounting in both genotypes. Our results provide new evidence for an organizing role of prepubertal estradiol in the development of neural mechanisms that control female-typical sexual behavior. [less ▲]

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See detailPotential contribution of prenatal estrogens to the sexual differentiation of mate preferences in mice.
Brock, Olivier; Bakker, Julie ULg

in Hormones and Behavior (2011), 59(1), 83-9

The neural mechanisms controlling sexual behavior are sexually differentiated by perinatal actions of gonadal hormones. We recently observed using female mice deficient in alpha-fetoprotein (AFP-KO) and ... [more ▼]

The neural mechanisms controlling sexual behavior are sexually differentiated by perinatal actions of gonadal hormones. We recently observed using female mice deficient in alpha-fetoprotein (AFP-KO) and which lack the protective actions of AFP against maternal estrogens, that exposure to prenatal estrogens completely defeminized their potential to show lordosis behavior in adulthood. Therefore, we determined here whether mate preferences were also affected in female AFP-KO mice. We observed a robust preference for an estrous female over an intact male in female AFP-KO mice, which were ovariectomized in adulthood and subsequently treated with estradiol and progesterone, whereas similarly treated WT females preferred the intact male over the estrous female. Gonadally intact WT males preferred the estrous female over the male, but only when visual cues were blocked by placing stimulus animals behind opaque partitions. Furthermore, when given the choice between an intact male and a castrated male, WT females preferred the intact male, whereas AFP-KO females showed no preference. Finally when given the choice between an estrous female and an ovariectomized female, WT males preferred the estrous female whereas AFP-KO females preferred the ovariectomized female or showed no preference depending on whether they could see the stimulus animals or not. Taken together, when AFP-KO females are tested under estrous conditions, they do not show any male-directed preferences, indicating a reduced sexual motivation to seek out the male in these females. However, they do not completely resemble males in their mate preferences suggesting that the male-typical pattern of mate preferences is not solely organized by prenatal estrogens. [less ▲]

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See detailThe alpha-fetoprotein knock-out mouse model suggests that parental behavior is sexually differentiated under the influence of prenatal estradiol.
Keller, Matthieu; Pawluski, Jodi ULg; Brock, Olivier ULg et al

in Hormones & Behavior (2010)

In rodent species, sexual differentiation of the brain for many reproductive processes depends largely on estradiol. This was recently confirmed again by using the α-fetoprotein knockout (AFP-KO) mouse ... [more ▼]

In rodent species, sexual differentiation of the brain for many reproductive processes depends largely on estradiol. This was recently confirmed again by using the α-fetoprotein knockout (AFP-KO) mouse model, which lacks the protective actions of α-fetoprotein against maternal estradiol and as a result represents a good model to determine the contribution of prenatal estradiol to the sexual differentiation of the brain and behavior. In the present study, we determined whether parental responses are differentiated prenatally under the influence of estradiol. It was found that AFP-KO females showed longer latencies to retrieve pups to the nest and also exhibited lower levels of crouching over the pups in the nest in comparison to WT females. Thus our results suggest that prenatal estradiol defeminizes the parental brain in mice. [less ▲]

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