Effects of the social environment during adolescence on the development of social behaviour, hormones and morphology in male zebra finches (Taeniopygia guttata)

Abstract Background Individual differences in behaviour are widespread in the animal kingdom and often influenced by the size or composition of the social group during early development. In many vertebrates the effects of social interactions early in life on adult behaviour are mediated by changes in maturation and physiology. Specifically, increases in androgens and glucocorticoids in response to social stimulation seem to play a prominent role in shaping behaviour during development. In addition to the prenatal and early postnatal phase, adolescence has more recently been identified as an important period during which adult behaviour and physiology are shaped by the social environment, which so far has been studied mostly in mammals. We raised zebra finches ( Taeniopygia guttata ) under three environmental conditions differing in social complexity during adolescence\ua0-\ua0juvenile pairs, juvenile groups, and mixed-age groups - and studied males\u2019 behavioural, endocrine, and morphological maturation, and later their adult behaviour. Results As expected, group-housed males exhibited higher frequencies of social interactions. Group housing also enhanced song during adolescence, plumage development, and the frequency and intensity of adult courtship and aggression. Some traits, however, were affected more in juvenile groups and others in mixed-age groups. Furthermore, a testosterone peak during late adolescence was suppressed in groups with adults. In contrast, corticosterone concentrations did not differ between rearing environments. Unexpectedly, adult courtship in a test situation was lowest in pair-reared males and aggression depended upon the treatment of the opponent with highest rates shown by group-reared males towards pair-reared males. This contrasts with previous findings, possibly due to differences in photoperiod and the acoustic environment. Conclusion Our results support the idea that effects of the adolescent social environment on adult behaviour in vertebrates are mediated by changes in social interactions affecting behavioural and morphological maturation. We found no evidence that long-lasting differences in behaviour reflect testosterone or corticosterone levels during adolescence, although differences between juvenile and mixed-age groups suggest that testosterone and song behaviour during late adolescence may be associated

Mammal-Like Organization of the Avian Midbrain Central Gray and a Reappraisal of the Intercollicular Nucleus

In mammals, rostrocaudal columns of the midbrain periaqueductal gray (PAG) regulate diverse behavioral and physiological functions, including sexual and fight-or-flight behavior, but homologous columns have not been identified in non-mammalian species. In contrast to mammals, in which the PAG lies ventral to the superior colliculus and surrounds the cerebral aqueduct, birds exhibit a hypertrophied tectum that is displaced laterally, and thus the midbrain central gray (CG) extends mediolaterally rather than dorsoventrally as in mammals. We therefore hypothesized that the avian CG is organized much like a folded open PAG. To address this hypothesis, we conducted immunohistochemical comparisons of the midbrains of mice and finches, as well as Fos studies of aggressive dominance, subordinance, non-social defense and sexual behavior in territorial and gregarious finch species. We obtained excellent support for our predictions based on the folded open model of the PAG and further showed that birds possess functional and anatomical zones that form longitudinal columns similar to those in mammals. However, distinguishing characteristics of the dorsal/dorsolateral PAG, such as a dense peptidergic innervation, a longitudinal column of neuronal nitric oxide synthase neurons, and aggression-induced Fos responses, do not lie within the classical avian CG, but in the laterally adjacent intercollicular nucleus (ICo), suggesting that much of the ICo is homologous to the dorsal PAG

Specific Activation of Estrogen Receptor Alpha and Beta Enhances Male Sexual Behavior and Neuroplasticity in Male Japanese Quail

Two subtypes of estrogen receptors (ER), ERα and ERβ, have been identified in humans and numerous vertebrates, including the Japanese quail. We investigated in this species the specific role(s) of each receptor in the activation of male sexual behavior and the underlying estrogen-dependent neural plasticity. Castrated male Japanese quail received empty (CX) or testosterone-filled (T) implants or were daily injected with the ER general agonist diethylstilbestrol (DES), the ERα-specific agonist PPT, the ERβ-specific agonist DPN or the vehicle, propylene glycol. Three days after receiving the first treatment, subjects were alternatively tested for appetitive (rhythmic cloacal sphincter movements, RCSM) and consummatory aspects (copulatory behavior) of male sexual behavior. 24 hours after the last behavioral testing, brains were collected and analyzed for aromatase expression and vasotocinergic innervation in the medial preoptic nucleus. The expression of RCSM was activated by T and to a lesser extent by DES and PPT but not by the ERβagonist DPN. In parallel, T fully restored the complete sequence of copulation, DES was partially active and the specific activation of ERα or ERβ only resulted in a very low frequency of mount attempts in few subjects. T increased the volume of the medial preoptic nucleus as measured by the dense cluster of aromatase-immunoreactive cells and the density of the vasotocinergic innervation within this nucleus. DES had only a weak action on vasotocinergic fibers and the two specific ER agonists did not affect these neural responses. Simultaneous activation of both receptors or treatments with higher doses may be required to fully activate sexual behavior and the associated neurochemical events

Hormonal Control of Female Sexual Behavior in the Japanese Quail

Four experiments were carried out to study the hormonal control of female receptivity and proceptivity in Japanese quail. Both aspects of reproductive behavior can be activated in a dose-dependent manner by injections of estradiol benzoate (EB). Progesterone (P) given in addition to suboptimal doses of EB has little additional stimulatory effect. Other aspects of the reproductive physiology such as enlargement of the cloacal diameter and growth of the oviduct also seem to be controlled primarily by estrogens with little or no additive effect of P. These conclusions were confirmed by injecting egg-laying females with an antiestrogen, tamoxifen, or an antiprogestin, RU38486. Only the former had marked effects on sexual receptivity, cloacal diameter, and oviduct weight. The inhibiting effects of tamoxifen could easily be reversed by injecting females with large doses of estrogen, which demonstrates that tamoxifen acts on an estrogen-dependent mechanism and not through nonspecific effects

Diurnal variations of sexual receptivity in the female Japanese quail (Coturnix coturnix japonica).

A series of experiments was performed to study the changes during the day of female receptivity in Japanese quail. In each experiment, the frequency of squatting and the percentage of male approaches which were followed by squatting increased at the end of the day, approximately 11 to 13 hr after lights on (in a photoperiod of 16L:8D). In some cases this increased receptivity was associated with a significant decrease of the long-avoid frequency. Analyses are presented which demonstrate that the increased receptivity at the end of the day is not directly caused by the oviposition and does not result directly from changes in the behavior of the male stimuli. This is strongly supported by the observation that the increase in receptivity was observed at the same time after lights on (but different clock times) in two groups of females which were raised in two different photoperiods shifted by 6 hr and tested with the same group of males raised in one of the two photoperiods. The increase in receptivity coincides with an increase in plasma estradiol and progesterone. Considering that this behavior is suppressed by ovariectomy, it is argued that the daily changes in receptivity could be controlled by the hormonal changes associated with the ovulatory cycle

Hormonal correlates of gonadal regression and spontaneous recovery in Japanese quail exposed to short day-lengths.

Adult male Japanese quail were transferred from long to short days. Plasma testosterone and dihydrotestosterone quickly decreased and this endocrine response was followed by a regression of the cloacal gland, an androgen-target organ. After about a month, a spontaneous recovery of gonadal activity was observed in some but not all birds. It was not associated with obvious shifts in the circadian system. The physiological bases of this spontaneous recovery are discussed as well as the detailed relationships between plasma testosterone and cloacal gland size

Central and Peripheral Metabolism of 5 Alpha-Dihydrotestosterone in the Male Japanese Quail: Biochemical Characterization and Relationship with Reproductive Behavior

An in vitro radioenzymatic assay and purification procedure by thin-layer chromatography were used to study the metabolism of dihydrotestosterone (DHT) into 3 alpha- and 3 beta-androstanediols by the brain and cloacal gland of Japanese quail. Kinetic studies showed that these 2 metabolites are produced in a linear fashion with respect to time of incubation for up to 15 min but that they continue to accumulate for up to 4 h. The maximum velocity of these reactions is high (nmol/mg protein/15 min), but the affinities of the enzymes for DHT are low (in the microM range). The enzymatic activities are not evenly distributed in the brain: they are high in the tuberal hypothalamus and lobus parolfactorius but low in the preoptic area and anterior hypothalamus. Enzyme activities are not markedly affected by treatment of the birds with either testosterone or DHT. The activity of these enzymes is lower in the preoptic area and tuberal hypothalamus of DHT-treated birds which display female-directed sexual behavior than in the same brain areas of birds which are sexually inactive. We discuss the relationships between this reductive metabolism of DHT and the activational effects of the steroid on sexual behavior

Testosterone metabolism and testosterone-dependent characteristics in Japanese quail.

In 2 independent experiments, we measured and correlated in maturing male Japanese quail the individual variations in sexual and aggressive behavior, cloacal gland size, testes weight, plasma testosterone concentrations and intracellular testosterone metabolism by hypothalamus and cloacal gland. Cloacal gland area was only weakly related to plasma testosterone levels but was positively correlated with the production of active androgenic metabolites and negatively related to the production of 5 beta-reduced androgens (inactive) in the glandular tissue. Several measures of behavior were correlated with aspects of the testosterone metabolism in the anterior hypothalamus. In both experiments, the behavior of the birds was also strongly correlated with their testes weight and their cloacal gland area but weakly or not at all with their plasma testosterone levels. These studies suggest that testosterone metabolism is involved in the control of hormone action in maturing animals