Transient reversal of olfactory preference following castration in male rats: Implication for estrogen receptor involvement

Xiao, Kai; Chiba, Atsuhiko; Sakuma, Yasuo; Kondo, Yasuhiko

doi:10.1016/j.physbeh.2015.09.016

Cited by 5 publications

(9 citation statements)

References 31 publications

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“…When given a choice between two castrated opposite-sex rats, males and females of all treatment groups showed the expected preference for hormone- over a non-hormone-treated stimulus animal (Moy et al, 2004, Xiao et al, 2015). The most interesting data were for nose touching, which was sexually dimorphic, with males nose-touching significantly more than females.…”

Section: Discussionmentioning

confidence: 96%

Social and neuromolecular phenotypes are programmed by prenatal exposures to endocrine-disrupting chemicals

Topper

Reilly

Wagner

et al. 2019

Molecular and Cellular Endocrinology

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Exposures to endocrine-disrupting chemicals (EDCs) affect the development of hormone-sensitive neural circuits, the proper organization of which are necessary for the manifestation of appropriate adult social and sexual behaviors. We examined whether prenatal exposure to polychlorinated biphenyls (PCBs), a family of ubiquitous industrial contaminants detectable in virtually all humans and wildlife, caused changes in sexually-dimorphic social interactions and communications, and profiled the underlying neuromolecular phenotype. Rats were treated with a PCB commercial mixture, Aroclor 1221 (A1221), estradiol benzoate (EB) as a positive control for estrogenic effects of A1221, or the vehicle (4% DMSO), on embryonic day (E) 16 and 18. In adult F1 offspring, we first conducted tests of ultrasonic vocalization (USV) calls in a sociosexual context as a measure of motivated communications. Numbers of certain USV call types were significantly increased by prenatal treatment with A1221 in males, and decreased by EB in females. In a test of sociosexual preference for a hormone- vs. a non-hormone-primed opposite sex conspecific, male (but not female) nose-touching with opposite-sex rats was significantly diminished by EDCs. Gene expression profiling was conducted in two brain regions that are part of the social decision-making network in the brain: the medial preoptic nucleus (MPN) and the ventromedial nucleus (VMN). In both regions, many more genes were affected by A1221 or EB in females than males. In female MPN, A1221 changed expression of steroid hormone receptor and neuropeptides (e.g., Ar, Esr1, Esr2, and Kiss1). In male MPN, only Per2 was affected by A1221. The VMN had a number of genes affected by EB (females: Kiss1, Kiss1r, Pgr; males: Crh) but not A1221. These differences between EB and A1221 indicate that the mechanism of action of A1221 goes beyond estrogenic pathways. These data show sex-specific effects of prenatal PCBs on adult behaviors and the neuromolecular phenotype.

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Section: Discussionmentioning

confidence: 96%

Social and neuromolecular phenotypes are programmed by prenatal exposures to endocrine-disrupting chemicals

Topper

Reilly

Wagner

et al. 2019

Molecular and Cellular Endocrinology

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“…The MePD itself makes reciprocal projections with areas involved in reproductive behavior, including the POA and BnST (Morrell et al, 1984, Pardo-Bellver et al, 2012). Either castration or lesions of the MePD resulted in decreased preference for female odors by males (Maras and Petrulis, 2006, Xiao et al, 2015). Interestingly, oxytocin receptor binding densities in the medial amygdala correlated positively with social interest in males, but negatively in females, and males also showed higher overall levels of oxytocin receptor binding than females (Dumais et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

Aging and estradiol effects on gene expression in the medial preoptic area, bed nucleus of the stria terminalis, and posterodorsal medial amygdala of male rats

Nutsch

Bell

Will

et al. 2017

Molecular and Cellular Endocrinology

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Studies on the role of hormones in male reproductive aging have traditionally focused on testosterone, but estradiol also plays important roles in the control of masculine physiology and behavior. Our goal was to examine the effects of E2 on the expression of genes selected for E2-sensitivity, involvement in behavioral neuroendocrine functions, and impairments with aging. Mature adult (MAT, 5 mo.) and aged (AG, 18 mo.) Sprague-Dawley male rats were castrated, implanted with either vehicle or estradiol (E2) subcutaneous capsules, and euthanized one month later. Bilateral punches were taken from the bed nucleus of the stria terminalis (BnST), posterodorsal medial amygdala (MePD) and the preoptic area (POA). RNA was extracted, and expression of 48 genes analyzed by qPCR using Taqman low-density arrays. Results showed that effects of age and E2 were age- and region-specific. In the POA, 5 genes were increased with E2 compared to vehicle, and there were no age effects. By contrast the BnST showed primarily age-related changes, with 6 genes decreasing with age. The MePD had 5 genes that were higher in aged than mature males, and 17 genes with significant interactions between age and E2. Gene families identified in the MePD included nuclear hormone receptors, neurotransmitters and neuropeptides and their receptors. Ten serum hormones were assayed in these same males, with results revealing both age- and E2-effects, in several cases quite profound. These results support the idea that the male brain continues to be highly sensitive to estradiol even with aging, but the nature of the response can be substantially different in mature and aging animals.

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“…Male rats attracted to the odor of castrated males must be primed with estrogen or aromatizable androgens because males treated with aromatase inhibitors or castrated males treated with nonaromatizable dihydrotestosterone (DHT) did not prefer castrated males [ 57 ], indicating that the odor of castrated males must be explicitly different from the estrous odors attracting castrated males treated with not only estrogen but DHT. In real ecological environments, however, there is no opportunity for castrated male odor to attract sexually active males.…”

Section: Sexual Stimuli Attributesmentioning

confidence: 99%

“…As shown in Figure 1 B, preferences for conspecific odors are distinctly sexually dimorphic; sexually mature active males prefer the odor of receptive females to that of males or ovariectomized anestrous females, while receptive females prefer the odors of sexually active males to that of females or castrated sexually inactive males [ 6 ]. These sex-specific preferences are due to sex differences in the brain resulting from the organizational effects of perinatal sex steroids, as administration of opposite-sex hormones after gonadectomy in adult animals could not reproduce a heterosexual preference pattern [ 57 , 60 , 61 ].…”

Section: Sexually Dimorphic Preference and Organizational Effects Of Sex Steroidsmentioning

confidence: 99%

“…Similar to endocrine controls of sexual behavior, adult male rat castration eliminates masculine preference, which can be restored by T replacement therapy [ 6 , 62 , 64 ]. On the other hand, chronic treatment, but not a single injection [ 64 , 86 ], of either estrogen or DHT can induce masculine preference in castrated male rats [ 57 ]. Interestingly, male rat castration induces transient feminine preference, preferring male odors over estrous odor for one to two weeks followed by disappearing preference [ 6 , 57 ], while removal of the sex hormone source in female rats does eliminate sexual preference ( Figure 2 ).…”

Section: Hormonal Control For Opposite-sex Preferencementioning

confidence: 99%

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Neural and Hormonal Basis of Opposite-Sex Preference by Chemosensory Signals

Kondo

Hayashi

2021

IJMS

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In mammalian reproduction, sexually active males seek female conspecifics, while estrous females try to approach males. This sex-specific response tendency is called sexual preference. In small rodents, sexual preference cues are mainly chemosensory signals, including pheromones. In this article, we review the physiological mechanisms involved in sexual preference for opposite-sex chemosensory signals in well-studied laboratory rodents, mice, rats, and hamsters of both sexes, especially an overview of peripheral sensory receptors, and hormonal and central regulation. In the hormonal regulation section, we discuss potential rodent brain bisexuality, as it includes neural substrates controlling both masculine and feminine sexual preferences, i.e., masculine preference for female odors and the opposite. In the central regulation section, we show the substantial circuit regulating sexual preference and also the influence of sexual experience that innate attractants activate in the brain reward system to establish the learned attractant. Finally, we review the regulation of sexual preference by neuropeptides, oxytocin, vasopressin, and kisspeptin. Through this review, we clarified the contradictions and deficiencies in our current knowledge on the neuroendocrine regulation of sexual preference and sought to present problems requiring further study.

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Transient reversal of olfactory preference following castration in male rats: Implication for estrogen receptor involvement

Cited by 5 publications

References 31 publications

Social and neuromolecular phenotypes are programmed by prenatal exposures to endocrine-disrupting chemicals

Social and neuromolecular phenotypes are programmed by prenatal exposures to endocrine-disrupting chemicals

Aging and estradiol effects on gene expression in the medial preoptic area, bed nucleus of the stria terminalis, and posterodorsal medial amygdala of male rats

Neural and Hormonal Basis of Opposite-Sex Preference by Chemosensory Signals

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