Distinct neuroendocrine mechanisms control neural activity underlying sex differences in sexual motivation and performance (original) (raw)
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Hormones and Behavior, 1996
appear to be of an activational nature and cannot there-Early workers interested in the mechanisms mediating fore explain sex differences in behavior that are still sex differences in morphology and behavior assumed present in gonadectomized steroid-treated adults. This that differences in behavior that are commonly observed research has also revealed many aspects of brain morbetween males and females result from the sex specificphology and chemistry that are markedly affected by steity of androgens and estrogens. Androgens were thought roids in adulthood and are thought to mediate the activato facilitate male-typical traits, and estrogens were tion of behavior at the central level. It has been explicitly, thought to facilitate female-typical traits. By the midor in some cases, implicitly assumed that the sexual dif-20th century, however, it was apparent that administerferentiation of brain and behavior driven by early expoing androgens to females or estrogens to males was not sure to steroids concerns primarily those neuroanatomialways effective in sex-reversing behavior and that in cal/neurochemical characteristics that are altered by some cases a ''female'' hormone such as an estrogen steroids in adulthood and presumably mediate the acticould produce male-typical behavior and an androgen vation of behavior. Extensive efforts to identify these could induce female-typical behavior. These conceptual sexually differentiated brain characteristics over the past difficulties were resolved to a large extent by the seminal 20 years has only met with limited success, however. As paper of C. H. Phoenix, R. W. Goy, A. A. Gerall, and W. C. regards reproductive behavior, in all model species that Young in (1959, Endocrinology 65, 369-382) that illushave been studied it is still impossible to identify satistrated that several aspects of sexual behavior are differfactorily brain characteristics that differentiate under ent between males and females because the sexes have early steroid action and explain the sex differences in been exposed during their perinatal life to a different behavioral activating effects of steroids. This problem endocrine milieu that has irreversibly modified their reis illustrated by research conducted on Japanese quail sponse to steroids in adulthood. Phoenix et al. (1959) (Coturnix japonica), an avian model system that displays therefore formalized a clear dichotomy between the orprominent sex differences in the sexual behavioral reganizational and activational effects of sex steroid horsponse to testosterone, and in which the endocrine mones. Since this paper, a substantial amount of remechanisms that control sexual differentiation of behavsearch has been carried out in an attempt to identify ior have been clearly identified so that subjects with a the aspects of brain morphology or neurochemistry that fully sex-reversed behavioral phenotype can be easily differentiate under the embryonic/neonatal effects of produced. In this species, studies of sex differences in steroids and are responsible for the different behavioral the neural substrate mediating the action of steroids in response of males and females to the activation by stethe brain, including the activity of the enzymes that meroids in adulthood. During the past 25 years, research in tabolize steroids such as aromatase and the distribution behavioral neuroendocrinology has identified many sex of steroid hormone receptors as well as related neurodifferences in brain morphology or neurochemistry; transmitter systems, did not result in a satisfactory exhowever many of these sex differences disappear when planation of sex differences in the behavioral effectivemale and female subjects are placed in similar endocrine ness of testosterone. Possible explanations for the relaconditions (e.g., are gonadectomized and treated with tive failure to identify the organized brain characteristics responsible for behavioral sex differences in the respon-the same amount of steroids) so that these differences 627
Brain Research Bulletin, 2000
We investigated the expression of Fos, the protein product of the immediate early gene c-fos in the brain of male Japanese quail after they engaged in either appetitive or consummatory sexual behavior (i.e., copulation). For 1 h, castrated males treated with testosterone were either allowed to copulate with a female or to exhibit a learned social proximity response indicative of appetitive sexual behavior. Control birds were either left in their home cage or placed in the experimental chamber but did not exhibit the appetitive sexual behavior because they had never learned it. Fos expression was studied with an immunocytochemical procedure in two sets of adjacent sections through the entire forebrain. These sections were immunolabelled with 2 different antibodies raised against a synthetic fragment corresponding to the 21 carboxy-terminal residues of the chicken Fos sequence. Contrary to the results of a previous study in which gonadally intact birds were used, Fos induction was observed neither in the medial preoptic nucleus nor in the nucleus intercollicularis in birds that had interacted for 1 h with a female. This may be related to a lower frequency of copulation in the testosterone-implanted birds than in intact birds, or to differences in the time the brains were collected after the birds engaged in sexual behavior between the two studies (60 min in this study, 120 min in the previous study). The performance of copulation and/or appetitive sexual behavior increased the number of Fos-immunoreactive cells in the ventral hyperstriatum, medial archistriatum, and nucleus striae terminalis. These increases were observed using both antibodies, although each antibody produced minor differences in the number of Fosimmunoreactive cells observed. Using one of the antibodies, but not the other, increases in Fos immunoreactivity were also observed in the nucleus accumbens and hyperstriatum after either copulation or appetitive sexual behavior. These differences illustrate how minor technical variations in the Fos immunocytochemical procedure influence the results obtained. These differences also show that Fos induction in a number of brain regions is observed after performance of consummatory (copulation) as well as appetitive (looking at the female) sexual behavior. This induction is, therefore, not related solely to the control of copulatory acts but, presumably, also to the process-ing in a variety of telencephalic association areas of stimuli originating from the female. The observation that increased Fos immunoreactivity is present in birds that had learned the response indicative of appetitive sexual behavior, and not in those that had not learned the behavior, further indicates that it is not simply the sight of the female that results in this Fos induction, but the analysis of the relevant stimuli in a sexually explicit context. Conditioned neural activity resulting from a learned association between the stimulus female and the performance of copulatory behavior may also explain some aspects of the brain activation observed in birds viewing, but not allowed to interact with, the female.
Frontiers in Neuroendocrinology, 1996
About 10 years ago, a sexually differentiated nucleus was identified in the preoptic area (POA) of the Japanese quail in the course of studies analyzing the dimorphic mechanisms involved in the activation of sexual behavior. In this species, males exposed to testosterone copulate while females never show this masculine behavior. The present paper reviews anatomical, neurochemical, and functional data that have been collected since that time about the quail dimorphic nucleus. The medial preoptic nucleus (POM) is significantly larger in adult male than in adult female quail. Its volume is also steroidsensitive in adulthood: it decreases when circulating levels of testosterone are low (castration, exposure to short-days) and it increases when testosterone levels are high (treatment with testosterone, exposure to long-days). The POM is a necessary and sufficient site of steroid action for the activation of male copulatory behavior. The volumetric difference of the POM results from a difference in the adult hormonal milieu of males and females (activational effect) and is not affected by embryonic treatments that permanently modify sexual behavior (no organizational effects on POM). In contrast, the size of neurons in the dorsolateral part of POM appears to be irreversibly affected by embryonic steroids and this feature is therefore a better correlate of the behavioral sex difference. The POM is characterized by the presence of a wide variety of neurotransmitters, neuropeptides, and receptors. It can, in addition, be specifically distinguished from the surrounding POA by the presence of aromatase-immunoreactive cells, by a high density of a 2 -adrenergic receptors, and by a dense vasotocinergic innervation. Some of these neurochemical markers of the dimorphic nucleus are themselves modulated by steroids. In particular, the aromatase-immunoreactive cells of the lateral POM appear to be a key target for steroids in the activation of male copulatory behavior. The POM is bidirectionally connected to many brain areas. It receives inputs from a variety of sensory areas and from a number of regulatory areas (e.g., catecholaminergic cell groups). This nucleus also sends outputs to ''neurovegetative'' centers and to brain regions directly connected to the motor pathways. These connections fully support the role of the POM as an integrative center for the control of male sexual behavior. The available data indicate that there is a high degree of steroid-induced neuronal plasticity in the POM, including changes in neuronal function, in protein synthesis, and in specific inputs. These phenomena can easily be studied in the POM because they are of a large magnitude, they are localized in a specific brain site, and they develop rapidly after exposure to steroids. They are also directly related to a clear functional output, the activation of male sexual behavior. The quail POM therefore constitutes an exceptional model for the analysis of steroid-induced brain plasticity in a functionally relevant context.
1998
Central testosterone aromatization is required for the activation of both appetitive (ASB) and consummatory (CSB) male sexual behavior in Japanese quail. There are two major clusters of aromatase immunoreactive (ARO-ir) cells in the rostral forebrain; these outline the nucleus preopticus medialis (POM) and the nucleus striae terminalis (BST). We investigated the role of these nuclei in the regulation of ASB and CSB. Appetitive male sexual behavior was measured with the use of a learned social proximity procedure that quantified the time spent by a male in front of a window with a view of a female who was subsequently released into the cage, providing an opportunity for CSB. Males first acquired the response and then received bilateral electrolytic lesions aimed at the POM or BST, followed by retesting for ASB and CSB. Brain sections were stained for ARO-ir, and lesions to the two ARO-ir cell groups were quantitatively char-acterized. Lesions damaging the POM completely abolished CSB and also significantly decreased ASB. Lesions of the rostral BST had no effect on ASB, but moderately decreased CSB. Detailed anatomical analysis revealed that lesions of a subdivision of the POM just rostral to the anterior commissure specifically impair CSB, whereas lesions that are more rostral to this subdivision induce a severe deficit in ASB. These data indicate that different subregions of the POM regulate ASB and CSB in a somewhat independent manner, whereas the BST is only important in the regulation of CSB.
Hormones and behavior, 2016
Although aromatase is expressed in both male and female brains, its functional significance in females remains poorly understood. In female quail, sexual receptivity is activated by estrogens. However it is not known whether sexual motivation is similarly estrogen-dependent and whether estrogens locally produced in the brain contribute to these behavioral responses. Four main experiments were designed to address these questions. In Experiment 1 chronic treatment of females with the anti-estrogen tamoxifen decreased their receptivity, confirming that this response is under the control of estrogens. In Experiment 2 chronic treatment with tamoxifen significantly decreased sexual motivation as treated females no longer approached a sexual partner. In Experiment 3 (a) ovariectomy (OVX) induced a significant decrease of time spent near the male and a significantly decreased receptivity compared to gonadally intact females, (b) treatment with testosterone (OVX+T) partially restored these r...
Hypothalamic inhibition of socio-sexual behaviour by increasing neuroestrogen synthesis
Nature Communications, 2014
Gonadotropin-inhibitory hormone (GnIH) is a hypothalamic neuropeptide that inhibits gonadotropin secretion and socio-sexual behaviours. Oestrogen (neuroestrogen) synthesized in the brain from androgen by aromatase regulates male socio-sexual behaviours. Here we show that GnIH directly activates aromatase and increases neuroestrogen synthesis in the preoptic area (POA) and inhibits socio-sexual behaviours of male quail. Aromatase activity and neuroestrogen concentration in the POA are low in the morning when the birds are active, but neuroestrogen synthesis gradually increases until the evening when the birds become inactive. Centrally administered GnIH in the morning increases neuroestrogen synthesis in the POA and decreases socio-sexual behaviours. Centrally administered 17b-oestradiol at higher doses also inhibits socio-sexual behaviours in the morning. These results suggest that GnIH inhibits male socio-sexual behaviours by increasing neuroestrogen synthesis beyond its optimum concentration for the expression of socio-sexual behaviours. This is the first demonstration of any hypothalamic neuropeptide that directly regulates neuroestrogen synthesis.
European Journal of Neuroscience, 2007
We investigated the effects of presenting a sexual conditioned stimulus on the expression of c-fos in male Japanese quail. Eight brain sites were selected for analysis based on previous reports of c-fos expression in these areas correlated with sexual behaviour or learning. Males received either paired or explicitly unpaired presentations of an arbitrary stimulus and visual access to a female. Nine conditioning trials were conducted, one per day, for each subject. On the day following the ninth trial, subjects were exposed to the conditional stimulus (CS) for 5 min. Conditioning was confirmed by analysis of rhythmic cloacal sphincter movements (RCSM), an appetitive sexual behaviour, made in response to the CS presentation. Subjects in the paired condition performed significantly more RCSM than subjects in the unpaired group. Brains were collected 90 min following the stimulus exposure and stained by immunohistochemistry for the FOS protein. Significant group differences in the number of FOS-immunoreactive (FOS-ir) cells were found in two brain regions, the nucleus taeniae of the amygdala (TnA) and the hippocampus (Hp). Subjects in the paired condition had fewer FOS-ir cells in both areas than subjects in the unpaired condition. These data provide additional support to the hypothesis that TnA is implicated in the expression of appetitive sexual behaviours in male quail and corroborate numerous previous reports of the involvement of the hippocampus in conditioning. Further, these data suggest that conditioned and unconditioned sexual stimuli activate different brain regions but have similar behavioural consequences.
European Journal of Neuroscience, 2013
Environmental stimulation results in an increased expression of transcription factors called immediate early genes (IEG) in specific neuronal populations. In male Japanese quail, copulation with a female increases the expression of the IEGs zenk and c-fos in the medial preoptic nucleus (POM), a key nucleus controlling male sexual behavior. The functional significance of this increased IEG expression that follows performance of copulatory behavior is unknown. We addressed this question by repeatedly quantifying the performance of appetitive (learned social proximity response) and consummatory (actual copulation) sexual behavior in castrated, testosterone-treated males that received daily intracerebroventricular injection of an antisense oligodeoxynucleotide targeting c-fos or control vehicle. Daily antisense injections significantly inhibited expression of copulatory behavior as well as acquisition of the learned social proximity response. A strong reduction of the proximity response was still observed in antisense-treated birds that copulated with a female, ruling out the indirect effect of the absence of interactions with females on the learning process. After a two-day interruption of behavioral testing but not of antisense injections, birds were submitted to a final copulatory test that confirmed the behavioral inhibition in antisense-injected birds. Brains were collected 90 min after the behavioral testing for quantification of c-fos immunoreactive cells. A significant reduction of the number of c-fospositive cells in POM but not in other brain regions was observed following antisense injection. Together, data suggest that c-fos expression in POM modulates copulatory behavior and sexual learning in male quail.
Hormones and Behavior, 1996
In a seminal experiment, Phoenix, Goy, Gerall, and treated daily with estradiol benzoate (EB), females con- showed that prenatal administration of sistently prefer to approach and interact sexually with testosterone propionate (TP) to pregnant guinea pigs a stud male whereas male subjects, on average, prefer significantly reduced the later capacity of female offan estrous female. In the present experiment this sexuspring to display lordosis behavior after ovariectomy ally allomorphic pattern of partner preference was and treatment with estradiol benzoate (EB) and progeschanged in males given lesions of the medial preoptic terone. Subsequent studies (reviewed in Baum, 1979; area/anterior hypothalamus (mPOA/AH). Electrolytic Goy and McEwen, 1980) carried out on a variety of lesions, which caused extensive bilateral damage to rodent species established that perinatal exposure of the mPOA/AH, including the sexually dimorphic male the male brain to testosterone (T) secreted by the testes, nucleus (MN) of the POA/AH, led males to shift their mean preference away from the estrous female to the or to estradiol (E) formed in the developing brain from stud male. Their postoperative profile of partner prefercirculating T, causes a permanent reduction in receptive ence more closely resembled that of sham-operated responsiveness to ovarian steroids. In addition to actifemales than that of sham-operated males or of males vating receptive sexual behavior, ovarian hormones which sustained either partial or minimal bilateral dampromote the expression of proceptive aspects of femiage to the mPOA/AH so as to spare the MN-POA/AH nine sexual behavior (Beach, 1976). These proceptive in one or both hemispheres. Males with extensive bilatbehaviors include approach to the male and the display eral mPOA/AH lesions, like sham-operated females,