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Steroid sensitive sites in the avian brain: does the distribution of the estrogen receptor alpha and beta types provide insight into their function?

Studies in avian species have often been useful in elucidating basic concepts relevant to the regulation of reproductive behaviors by sex steroid hormones. Once a link between a steroid hormone and a behavioral response has been established, one can use the localization of steroid hormone receptors in the brain to facilitate the identification of neural circuits that control behavior. The recent identification of a second type of estrogen receptor called estrogen receptor beta or ERbeta has raised new issues about the action of steroid hormones in the brain. A hypothesis has been proposed by Kuiper et al. [1998] based on studies in mammalian species suggesting that ERalpha (the name given to the ER that was previously described) is important for reproduction while ERbeta is more important for non-reproductive functions. In this paper we apply this hypothesis more generally by examining possible functions of ERbeta in avian species. We have initiated studies of the ERbeta in the brain of two avian species, the Japanese quail (Coturnix japonica) and the European starling (Sturnus vulgaris). ERbeta was cloned in both species and the mRNA for this receptor type was localized in the brain employing in situ hybridization histochemistry methods. In both species ERbeta was found to be diffusely present in telencephalic areas consistent with a role for this receptor subtype in cognitive functions. However, ERbeta mRNA was also found in many brain areas that are traditionally thought to be important in the regulation of reproductive functions such as the preoptic region, the bed nucleus of the stria terminalis and the nucleus taeniae. Of the two receptor types, only mRNA for ERalpha was observed in the telencephalic vocal control nucleus HVc of male starlings. Steroid receptors in this nucleus are thought to be an example of an evolutionary specialization that has evolved to coordinate the production of courtship vocalizations with other aspects of reproduction. The lack of ERbeta mRNA expression in HVc is consistent with the hypothesis that ERalpha is preferentially involved in reproductive behaviors while ERbeta is involved in the steroid regulation of other neural functions. However, the widespread occurrence of ERbeta in other nuclei involved in reproductive function suggests that one must be cautious about the general applicability of the above hypothesis until more is known about ERbeta function in these other nuclei.

Animals↗

Observations of mating, birthing and parental behaviour in three subspecies of slender loris (Loris tardigradus and Loris lydekkerianus ) in India and Sri Lanka.

Studies of the life history parameters of slender lorises in captivity have led to conflicting results regarding gestation length, birth seasonality, interspecies variation in litter size and the degree of parental care given to offspring. During the course of field studies of Loris lydekkerianus lydekkerianus, L. l. nordicus and L. tardigradus tardigradus, data were collected on these life history variables, as well as on behaviours relating to mating. All 3 taxa displayed courtship behaviour involving the pursuit of a female by multiple males. Mating corresponded closely with captive observations, with a period of prolonged single intromissions lasting 3-11 min. One gestation period of 163 days was calculated for L. l. lydekkerianus. Births for all 3 taxa were distributed throughout the year, and males were seen mating throughout the year. All 3 taxa gave birth to singletons and twins; no subspecific pattern in litter size was evident. Females carried infants for the first 4 weeks of life and were regularly attended by males, which groomed both the mother and her offspring. After infants had been parked, female L. l. lydekkerianus and L. l. nordicus rarely returned before dawn, though males visited and played with infants. Female L. t. tardigradus maintained proximity with their infants, whilst males were not observed in proximity to infants during the night. All 3 taxa slept in social groups. High-energy milk, in combination with male care, may aid in the potentially high reproductive output of 4 infants per year.

Animals↗

Immunoreactive gonadotropin-releasing hormone (GnRHir) is associated with vestibular structures in the green anole (Anolis carolinensis).

The distribution of immunoreactive gonadotropin-releasing hormone (GnRHir) in relation to endocrine and behavioral pathways is not well established for lizards. To more completely understand the GnRHir distribution and its possible function in a lizard, we investigated the brain of Anolis carolinensis, a species whose visual courtship displays, mating postures and gonadal cycles are well known. Using antisera that recognize multiple GnRH forms, we observed no GnRHir cells or fibers in the forebrain. In the midbrain, however, GnRHir cells occurred along the medial border of the medial longitudinal fasciculus. These cells appeared to project GnRHir fibers to nuclei of cranial nerve III and IV. In the hindbrain, positive fibers were observed in the area of the vestibular nuclei and dorsal funiculus. These hindbrain fibers were followed to their terminals in the cerebellum. The GnRHir midbrain distribution suggests an association of GnRH with eye movements, whereas the hindbrain distribution suggests a GnRH-vestibular association. The lack of GnRHir in the forebrain of Anolis could reflect the minimal role of the vomeronasal system in mediating reproduction in this species. Thus, our study cannot verify hypothalamic GnRH control of the pituitary in A. carolinensis, but it does indicate GnRH control of oculomotor and vestibular nuclei, which might play a role in Anolis reproductive behaviors.

Animals↗

Sex differences in neuropeptide staining of song-control nuclei in zebra finch brains.

This study examined the distribution of the neuropeptides somatostatin (SS) and calcitonin gene-related peptide (CGRP) in forebrain and midbrain song-control nuclei of male versus female brains in adult zebra finches (Poephila guttata) using immunohistochemical techniques. Vocal learning in songbirds is controlled by an interconnected, highly-localized system of brain nuclei. Male zebra finches produce learned vocalizations, and females do not. This behavioral sexual dimorphism is reflected in a substantial difference in the size of these song-control nuclei: males have larger nuclei containing a greater number of neurons than do females. Interestingly, previous studies describing neurochemical aspects of the song-control system in other songbird species have not reported any obvious sex differences. However, the results of this study showed that the level of neuropeptide staining was substantially greater in telencephalic song-control nuclei of male brains compared to female brains in zebra finches. In some brain regions females lacked any apparent staining, whereas male brains were intensely labeled. In other cases the number of neurons and/or intensity of labeling were diminished in females relative to males. The telencephalic pattern of somatostatin labeling revealed a large number of SS-labeled somata in the magnocellular nucleus of the anterior neostriatum species that occupy habitats with different hydrodynamic conditions. (MAN), the high vocal center (HVC) and the robust nucleus of the archistriatum (RA) of males, whereas female song-control nuclei contained many fewer or no labeled cells in these regions. Area X of the striatum appeared to contain a slightly higher level of somatostatin immunoreactivity than surrounding striatum in males, but the region corresponding to Area X in females could not be distinguished from the rest of striatum. The telencephalic pattern of CGRP staining was less extensive than that seen for SS. In male brains the magnocellular core region of lateral MAN contained many darkly labeled neurons, and RA was stained by a dense field of anterograde terminal label. Well labeled somata were also seen in medial MAN of males, but HVC was devoid of immunoreactivity. Area X in male brains contained a light field of terminal immunoreactivity. The pattern of labeling seen in males indicates that CGRP acts selectively as a neuromodulator along the efferent projection from lateral MAN to RA and Area X but not in the HVC-to-RA pathway. No telencephalic song-control nuclei in female brains contained CGRP staining. Although some diencephalic and midbrain nuclei contained well-labeled somata or fibers with either or both neuropeptides, there was little or no evidence of a sex difference in neuropeptide expression in these regions. This latter finding suggests that the greater anatomical specialization seen in cortical regions of songbirds compared to those regions in non-oscine species is accompanied by a greater neurochemical differentiation, whereas thalamic and midbrain regions may be more conserved across sex as well as species. These findings indicate that male neurons produce high levels of somatostatin and calcitonin gene-related peptide in major telencephalic vocal-control regions in zebra finches, whereas female neurons produce less or none at all. These dramatic neurochemical sex differences may be directly related to production of learned vocalizations in males, as well as to other aspects of song behavior and courtship.

Animals↗

Chemical ecology of the red-sided garter snake, Thamnophis sirtalis parietalis.

The red-sided garter snake, Thamnophis sirtalis parietalis is an ideal model for the study of chemical or pheromonal communication in vertebrates. Results of long-term field and laboratory investigations of the chemical ecology of these unusual animals is summarized. These studies include a description of the characterization of the female attractiveness pheromone that serves to induce male courtship behavior. The male sex recognition pheromone system that identifies males as inappropriate individuals to court is also described. She-males, individual males that are courted as if they were females, seem to possess semiochemical components intermediate to both males and females. Finally, investigations of the species-specific nature of these pheromones indicate that chemical differences exist in the methyl ketones of all species examined to date.

Animal Communication↗

Sexual behavior and 2-deoxyglucose uptake in male red-sided garter snakes (Thamnophis sirtalis parietalis).

The [14C]2-deoxyglucose (2-DG) technique was used to study patterns of neural activity associated with the species-typical courtship behavior of male red-sided garter snakes (Thamnophis sirtalis parietalis). Males in this species court females intensely during the first month following spring emergence from their prolonged winter hibernation. Autoradiographic methods were used to measure the accumulation of radioactive label in various regions through the brains of male garter snakes that courted females, males that failed to court females, and males not exposed to females. Male garter snakes that actively courted females showed a pronounced increase in 2-DG accumulation, and therefore presumably neural activity, in the region of the anterior hypothalamus/preoptic area, relative to males that did not actively court females. Males exposed to females (regardless of whether they courted or not) showed widespread, non-specific increases in 2-DG uptake relative to males not exposed to females. The results indicate the utility of the 2-DG technique for studying complex, species-typical behaviors in vertebrates.

Animals↗

Striatal afferents in the newt Triturus cristatus.

In order to investigate the neuronal populations projecting to the corpus striatum in the brain of a urodele, Triturus cristatus, horseradish peroxidase (HRP) retrograde labeling was used in parallel with anterograde degeneration, glyoxylic acid histofluorescence and behavioral testing. Striatal injections of HRP revealed that the main striatal afferent systems originate within the diencephalon, specifically in the dorsal thalamus and paraventricular organ of the hypothalamus. Several small groups of neurons in other diencephalic areas also participate in striatal innervation: proeminentia ventralis, amygdala, contralateral corpus striatum, preoptic area, posterior tuberal nucleus, locus coeruleus and raphe nuclei. Degeneration experiments after mechanical lesion of the paraventricular organ established the existence of a hypothalamostriatal projection. Degenerating axonal profiles were also found in many of the structures already identified as projecting to the striatum, suggesting that the paraventricular organ might influence the striatum not only directly but also indirectly through these other afferent systems. In the paraventricular organ, glyoxylic acid fluorescence histochemistry showed numerous monoamine neurons that corresponded in distribution and morphology to the retrogradely HRP-labeled neurons. Paraventricular-organ-lesioned males displayed a severe impairment of courtship behavior in the form of decreased tail beating and head stepping by the females. This suggests that the regulation of stereotyped hypermotricity might involve the monoamine component of the hypothalamo-striatal projection.

Afferent Pathways↗

Luteinizing hormone-releasing factor (LRF) and reproductive behavior in male doves exposed to long and short photoperiods.

In order to determine whether the variable degree of nest-building behavior displayed by male doves exposed to different photoregimes is related to differences in luteinizing hormone-releasing factor (LRF) levels, androgen-treated castrates held on long (16L:8D) or short (8L:16D) daylengths were treated with 20 microgram LRF or saline daily. Birds in both groups exhibited higher levels of initial courtship and nest-building when held on long days. LRF treatment had no effect on any of the behavior patterns examined. The results suggest that photoperiod does not affect reproductive behavior in male doves through changes in endogenous levels of LRF.

Animals↗

Nuclear uptake of estrogens in the male dove hypothalamus: relationship to aromatase activity and behavioral effects.

The natural estrogen, estradiol-17 beta, and a synthetic agonist, diethyl stilbestrol (DES), accumulated selectively in cell nuclei of the male dove preoptic area and posterior hypothalamus following intramuscular injection of the corresponding 3H-labelled tracers. Nuclear incorporation of radioactivity was saturable and specific, as shown by the effect of competition doses of unlabelled estrogens. The non-aromatizable androgen, 5 alpha-dihydrotestosterone (DHT), did not compete with estrogens for nuclear binding sites, indicating that cross-reaction with androgen receptors is unlikely. Estradiol uptake was higher in the preoptic area than in the posterior hypothalamus, whereas DES uptake did not differ significantly between these areas. Although both brain areas are likely to contain specific estrogen receptors, only the preoptic area is known to be directly involved in the control of male precopulatory courtship behavior in the dove. Aromatase activity responsible for the local conversion of testosterone to biologically active estradiol-17 beta, measured in vitro, was also much higher in the preoptic and posterior hypothalamic areas than in adjacent areas of the basal forebrain and hypothalamus. The similarity in localization of aromatase activity and intranuclear uptake of estradiol indicates that the formation of estrogen may occur only within discrete brain areas containing specific estrogen receptors. Intranuclear uptake of DES in the preoptic area, which is half that of estradiol, is correlated with lower effectiveness both in inducing aromatase activity in the preoptic area and in eliciting an estrogen-dependent behavior in castrated males. The effectiveness of estrogens on behavior in the male dove is likely to depend upon characteristics of estrogen receptors in the preoptic area.

Animals↗

Neuroanatomical localization of sex steroid-concentrating cells in the Japanese quail (Coturnix japonica): autoradiography with [3H]-testosterone, [3H]-estradiol, and [3H]-dihydrotestosterone.

Steroid autoradiography was undertaken to determine the neuroanatomical loci which might be involved in the activation of steroid-sensitive behaviors in the Japanese quail (Coturnix japonica). Male and female quail were either surgically gonadectomized or photically regressed and implanted with androgen or estrogen to restore normal sexual and courtship behavior. After gonadectomy or implant removal, each quail was injected with 250 microCi of [3H]-testosterone (3H-T), [3H]-estradiol (3H-E2), or [3H]-dihydrotestosterone (3H-DHT), sacrificed, processed for autoradiography, and the telencephalon, diencephalon, mesencephalon, and rhombencephalon were examined for labelled cells. Following 3H-T or 3H-E2 injection and autoradiography, labelled cells were found in nucleus septalis lateralis (SL), nucleus preopticus medialis (POM), nucleus paraventricularis (PVN), regio lateralis hypothalami (LHy), nucleus inferior hypothalami (IH), nucleus infundibuli (IN), nucleus intercollicularis (ICo), substantia grisea centralis (GCt), nucleus taeniae (Tn), and in the reticular formation near nucleus motorius nervi trigemini (MV). In addition, following 3H-E2 autoradiography, labelled cells were found around nucleus accumbens (Ac). Following 3H-DHT autoradiography, labelled cells were found only in SL, PVN, Tn, LHy, ICo, and CGt. No labelled cells were found in Ac, POM, IH, IN, or MV even after long exposure times. These results suggest that the nuclei labelled following 3H-E2 but not 3H-DHT administration bind exclusively the aromatized metabolites of T. Since quail show a sex difference in male-typical copulatory behavior in response to E2, labelled cells were counted in POM, LHy, IH, and Tn of male and female quail following 3H-E2 injection and autoradiography. No sex differences in the number of labelled cells were found in POM, LHy, or IH. Males were found to have more labelled cells than females in Tn. These results show that sex differences in male-typical copulatory behavior are not due to sex differences in the number of cells binding estrogens in POM. The results reported here constitute the most neuroanatomically extensive report of steroid binding cells to date for a galliform brain, the first comparison in a galliform bird of the distributions of cells labelled following injection of 3H-T, 3H-E2, and 3H-DHT and the first analysis of sex differences in numbers of estrogen-binding cells in four nuclei in the avian brain.

Animals↗

A comparison of nonpatient and bipolar patient-well spouse couples.

The authors compared responses of 16 couples, in which one partner had a diagnosis of remitted bipolar illness, to a lengthy self-report questionnaire (KDS-15) designed to assess many aspects of marital adjustment with those of 16 matched nonpatient couples. The bipolar patient-well spouse couples had marital adjustments closely resembling those of the nonpatient couples; three of four global ratings of satisfaction failed to discriminate between the two groups. Perceptions of the courtship, first year of marriage, and the degree to which the marriage had met expectations were also similar for both groups.

Adjustment Disorders↗

Life histories of rural Mexican American adolescents experiencing abuse.

Histories of family violence are predictors of adolescent acceptance of interpersonal violence within intimate relationships. This study focused on the progression of abusive relationships from childhood to courtship and intimacy among 40 rural Mexican American adolescents in the southwestern United States. Emphasis was on interactions that were extensions of cultural expectations for intimacy, family, and sex roles. Within these life histories, transgenerational patterns of violence were found in patterns of learning, loving and belonging through past and present relationships. Sex-role identification with abusive behavior occurred across generations, emulating roles from the past and perpetuating expectations for abuse as part of intimacy. Previous abusive experiences were described as motivation for behavioral change, yet, within the patterns of learning, loving, and belonging in relationships, patterns of abuse and behaviors similar to the family of origin were found. An understanding of the influential role attitudes and expectations of abused individuals and their families has on behavior is relevant for interventions preventing existent and future abuse.

Adolescent↗

Male adolescent sexual offenders: the offender and the offense.

A group of male adolescent sexual offenders were divided into three groups: Courtship Disorders (Exhibitionism, Toucherism and Obscene Phone Calls), Sexual Assaults, and Pedophilic Offenses. Group I offenders tended to come from a less disorganized family background, were better adjusted to school and in the community and were seen by clinicians as less seriously disturbed than the adolescents in the other two groups. In addition, these adolescents did not experience the offense as a sexual act. Group II offenders (Sexual Assaulters) came from a more disturbed family background characterized by a high rate of long-term parent-child separations, committed more violent offenses and had a higher frequency of intellectual functioning in the Borderline Range of Intelligence. Group III offenders (Pedophilic Offenses) were Canadian born, had witnessed physical violence between their parents, were described as having been infants who did not enjoy being cuddled and had siblings who were truant. This study suggests that classifying adolescent sexual offenders along the line suggested in adult literature seems to be justified.

Adolescent↗

Photoperiodic control of reproduction and molt in the kestrel, Falco tinnunculus.

An adaptive decline in average clutch size with progressive date of laying is characteristic of most bird species with a single clutch of variable size per year. The effect of photoperiod on timing of laying, clutch size, and subsequent molt was investigated in kestrel pairs breeding and raising their young in captivity. In natural daylight (nLD), clutch size, under ad libitum feeding, showed the same decline with date as in nature. Birds breeding later also started molt later and molted faster (more feathers simultaneously), so that all birds completed molt more or less at the same time. Constant long days (LD 17.5:6.5 and LD 13:11) from December 1 onward advanced both reproduction and molt. The LD 17.5:6.5 group developed the reproductive system faster, had a shorter courtship period, and laid eggs earlier than the LD 13:11 group. In both photoperiods there was a decrease in clutch size with progressive laying date, similar to that in nLD. Molt started in both groups at about the end of the laying period and slowed down in the longer photoperiod, especially in males. Plasma luteinizing hormone (LH) changes in the two photoperiods were different for males and females. Males showed the expected slower LH response in the shorter photoperiod, but the initial LH response by females was the same in both photoperiods. Data on LH, reproductive behavior, and body mass suggest that females have a wider annual reproductive window than males. Data on time of laying and number of eggs suggest that clutch size in the kestrel is determined by laying date itself, following an endogenous rhythm that is phase-locked to the reproductive cycle.

Androgens↗

Genetic analysis of male reproductive success in relation to density in the zebrafish, Danio rerio.

BACKGROUND: We used behavioural and genetic data to investigate the effects of density on male reproductive success in the zebrafish, Danio rerio. Based on previous measurements of aggression and courtship behaviour by territorial males, we predicted that they would sire more offspring than non-territorial males. RESULTS: Microsatellite analysis of paternity showed that at low densities territorial males had higher reproductive success than non-territorial males. However, at high density territorial males were no more successful than non-territorials and the sex difference in the opportunity for sexual selection, based on the parameter Imates, was low. CONCLUSION: Male zebrafish exhibit two distinct mating tactics; territoriality and active pursuit of females. Male reproductive success is density dependent and the opportunity for sexual selection appears to be weak in this species.

Journal Article↗

Song function and the evolution of female preferences: why birds sing, why brains matter.

Analyzing the function of song and its evolution as a communication signal provides an essential backdrop for understanding the physiological and neural mechanisms responsible for song learning, perception, and production. The reverse also is true-understanding the mechanisms underlying song learning provides insight into how song has evolved as a communication signal. Song has two primary functions: to repel other males from a defended space and to attract females and stimulate their courtship. The developmental stress hypothesis we present here builds on studies of the development of the song system to suggest how learned features of song, including complexity and local dialect structure, can serve as indicators of male quality useful to females in mate choice. The link between song and male quality depends on the fact that brain structures underlying song learning largely develop during the first few months post-hatching and that during this same period, songbirds are likely to be subject to nutritional and other developmental stresses. Individuals faring well in the face of stress are able to invest more resources to brain development and are expected to be correspondingly better at song learning. Learned features of song thus become reliable indicators of male quality, with reliability maintained by the developmental costs of song. Data from both field and laboratory studies are now beginning to provide broad support for the developmental stress hypothesis, illustrating the utility of connecting mechanistic and evolutionary analyses of song learning.

Animal Communication↗

Endocannabinoids mediate the effects of acute stress and corticosterone on sex behavior.

For animals in the wild, survival depends on being able to detect and respond rapidly to danger by switching from risky (e.g. conspicuous courtship) to survival-oriented behaviors. Very little is known about the hormonal or neuroendocrine mechanisms that control the rapid switch in behavioral state that occurs when an animal detects threats or other stressors. Prior studies with rough-skinned newts (Taricha granulosa), an amphibian model, found that stress-induced suppression of male sexual behaviors (amplectic clasping) involves corticosterone (CORT) and that this steroid hormone uses a novel membrane receptor and modulates the responsiveness of medullary neurons in clasp-controlling neural circuits. We provide evidence that this rapid suppression of male sex behaviors, when induced by either acute stress or CORT administration, involves activation of endocannabinoids signaling in the hindbrain. In a series of behavioral studies, administration of a cannabinoid antagonist, AM281, blocked the suppressive effects of exposure to acute stress or an injection of CORT on the performance of clasping behaviors in sexually active males. Similarly, in electrophysiological studies, prior treatment with AM281 blocked CORT-induced suppression of spontaneous neuronal activity and sensory responsiveness of hindbrain neurons in clasp-controlling neural circuits. These data suggest that, in response to acute stress, elevated CORT concentration increases endocannabinoid signaling in the hindbrain and alters sexual behaviors by modulating the excitability of medullary circuits.

Acute Disease↗

Male-like behavioral patterns and physiological alterations induced by androgenic gland implantation in female crayfish.

The androgenic gland (AG) has been shown to regulate male sexual differentiation and secondary male characteristics in Crustacea. This study presents for the first time in crustaceans evidence for masculinization effects of the AG on reproductive behavior, in addition to morpho-anatomical and physiological effects. AG implantation into immature female red claw crayfish Cherax quadricarinatus inhibited secondary vitellogenesis and development of the ovaries, as well as morphological traits that facilitate maternal egg brooding; it also caused the appearance of secondary male characteristics. However, primary male characteristics and a masculine reproductive system were not developed. In pair encounters, aggression was substantially lower in interactions between AG-implanted and intact females than in interactions within AG-implanted or intact pairs. Moreover, elements of mating behavior, i.e. male courtship displays and false copulations, were exhibited by AG-implanted females in several encounters with intact females. In addition to known morpho-anatomical and physiological effects of the AG in crustaceans, the present study suggests that the AG has novel effects on the neural network that generates social behavior.

Aggression↗