Stress-induced inhibition of sexual behavior: Corticosterone inhibits courtship behaviors of a male amphibian (Taricha granulosa)

When male rough-skinned newts (Taricha granulosa) are exposed to presumptive stressors, the incidence of courtship decreases and plasma corticosterone concentration increases. When sexually active males are injected intraperitoneally with corticosterone (1, 5, 10, 15, 20, or 25 μg), the incidence of courtship decreases rapidly and in proportion to the dose of corticosterone. Intracerebroventricular infusion of synthetic corticotropin-releasing factor (CRF) elevates plasma corticosterone levels and suppresses courtship. When male newts receive an injection of metyrapone, a drug that interferes with corticosterone synthesis, the inhibitory effects of stress or CRF infusion on courtship are reduced. These results support the hypothesis that, in this amphibian, elevated levels of corticosterone associated with exposure to stressful stimuli inhibit sexual behaviors.     

Temporary inhibition by progesterone of sexual behavior in intact male mice

Administration of 0.50 mg or 1.00 mg progesterone (P) daily resulted in suppression of portions of the male sexual repertoire. Mice treated with 0.25 mg P daily behaved like control subjects. Sexual behavior of mice treated with the higher P doses resembled that of controls three weeks after cessation of P treatment. No lasting effects of P on total body weight or on weights of testes or seminal vesicles were detected.     

Variation in male sexual behavior

Relaxation of natural selection on sexual performance traits in male ruminants has increased phenotypic variation in these heritable traits. Thus, males with sub-standard sexual performance continue to reproduce. This has created a "dud" phenomenon that is costly to animal agriculture. Identification and culling of these lesser performers at an early age and identification of high performing males are critical management goals that must be addressed, and for which greater research priority is needed.     

Patterns of sexual behavior in male macaques

One large social group of each of three species of macaques (Macaca mulatta, M. fascicularis, M. radiata), housed in half-acre field cages at the California Primate Research Center, were observed for a total of 150 h. Data on sexual behavior and dominance interactions were recorded by pairs of experienced observers using a focal animal technique. Single or multiple mount-to-ejaculation sequences, number of thrusts per mount, number of mounts per sequence, duration of mounts per sequence, duration of sequences, social rank and frequency of sexual activity were recorded for each adult male. M. mulatta used a multiple mount-to-ejaculation (MME) pattern in 91% of their copulations. M. radiata used a single mount-to-ejaculation (SME) pattern in 91% of their copulations. M. fascicularis used both patterns—53% MME and 47% SME. A positive correlation was found between rank and sexual activity in fascicularis and mulatta males. A negative correlation between rank and sexual activity was found in radiata males and also a positive correlation between rank and age indicating that the youngest and most subordinate radiata males were the most sexually active males. In reviewing the literature, a relationship between degree of intermale competition, intermale tolerance and type of mounting pattern was revealed. Macaque species that primarily use an SME pattern also show sa high degree of intermale tolerance and little interrnale competition. Macaque species that primarily use an MME pattern typically show a high degree of intermale competition and a low degree of intermale tolerance. Possible events leading to such relationships are discussed.     

Genetic basis of male sexual behavior

Male sexual behavior is increasingly the focus of genetic study in a variety of animals. Genetic analysis in the soil roundworm Caenorhabditis elegans and the fruit fly Drosophila melanogaster has lead to identification of genes and circuits that govern behaviors ranging from motivation and mate-searching to courtship and copulation. Some worm and fly genes have counterparts with related functions in higher animals and many more such correspondences can be expected. Analysis of mutations in mammals can potentially lead to insights into such issues as monogamous versus promiscuous sexual behavior and sexual orientation. Genetic analysis of sexual behavior has implications for understanding how the nervous system generates and controls a complex behavior. It can also help us to gain an appreciation of how behavior is encoded by genes and their regulatory sequences.     

X-chromosome dosage affects male sexual behavior

Sex differences in the brain and behavior are primarily attributed to dichotomous androgen exposure between males and females during neonatal development, as well as adult responses to gonadal hormones. Here we tested an alternative hypothesis and asked if sex chromosome complement influences male copulatory behavior, a standard behavior for studies of sexual differentiation. We used two mouse models with non-canonical associations between chromosomal and gonadal sex. In both models, we found evidence for sex chromosome complement as an important factor regulating sex differences in the expression of masculine sexual behavior. Counter intuitively, males with two X-chromosomes were faster to ejaculate and display more ejaculations than males with a single X. Moreover, mice of both sexes with two X-chromosomes displayed increased frequencies of mounts and thrusts. We speculate that expression levels of a yet to be discovered gene(s) on the X-chromosome may affect sexual behavior in mice and perhaps in other mammals.     

A role for ATP-sensitive potassium channels in male sexual behavior

ATP-sensitive potassium (K⁺_ATP) channels regulate cell excitability and are expressed in steroid-responsive brain regions involved in sexual behavior, such as the preoptic area (POA) and medial basal hypothalamus (MBH). We hypothesized that K⁺_ATP channels serve as a mechanism by which testosterone can control the electrical activity of neurons and consequently elicit male sexual responsiveness. RT-PCR analysis indicated that castration induces, while testosterone inhibits, mRNA expression of the K⁺_ATP channel subunit Kir6.2 in both the POA and MBH of adult male rats. Intracerebral infusion of the pharmacological K⁺_ATP channel inhibitor tolbutamide increased the proportion of long-term castrates displaying sexual behavior and restored mount frequency, intromission frequency, and copulatory efficacy to values observed in testes-intact animals. Infusions of tolbutamide, but not vehicle, also decreased latencies to mount and intromit in castrated males. Unilateral tolbutamide infusion directly into the POA significantly reduced mount latency of castrates; however, it did not affect other copulatory measures, suggesting that blockade of K⁺_ATP channels in additional brain regions may be necessary to recover the full range of sexual behavior. These data indicate that blockade of K⁺_ATP channels is sufficient to elicit the male sexual response in the absence of testosterone. Our observations are consistent with the hypothesis that testosterone modulates male sexual behavior by regulating K⁺_ATP channels in the brain. Decreased channel expression or channel blockade may increase the excitability of androgen-target neurons, rendering them more sensitive to the hormonal, chemical, and somatosensory inputs they receive, and potentially increase secretion of neurotransmitters that facilitate sexual behavior.     

Role of neurotransmitters in coordination of male sexual behavior

The review considers the published data and the results obtained by the author on the role of monoamines (serotonin, dopamine, and noradrenaline) in the control of male sexual behavior. In the above respect, the central mechanisms of action of the neurotransmitters are discussed.     

Photoperiodic influences on sexual behavior in male Syrian hamsters

The effect of photoperiodic conditions on sexual behavior was investigated in male Syrian hamsters that were either gonadally intact, or castrated and treated with low doses of testosterone throughout the experiment. Hamsters were exposed to long (LD 16:8) or short (LD 8:16) days for 7 weeks; for the next 8 weeks, either they were exposed to an intermediate daylength (LD 12:12), or daylength conditions remained unchanged. Sexual behavior was affected by photoperiod conditions in both gonadally intact animals and testosterone-treated castrates, but to different degrees. Intact males exposed to short days for 15 weeks exhibited gonadal regression, and their copulatory performance was impaired. The percentage of animals that intromitted or ejaculated was significantly reduced. Additional measures of sexual performance among the copulating males were also affected. In contrast, among the castrates with testosterone clamped at low but stable levels, the proportion of males that mounted, intromitted, or ejaculated was not affected by photoperiod. However, among the males that continued to copulate, sexual performance changes were present in the short-day castrates that resembled those displayed by the intact males. We infer that these behavioral effects in both hormonal conditions reflect primarily a difficulty in the attainment of intromission. Gonadal regression alone cannot easily account for the behavioral deficits of the intact males, because circulating testosterone levels at the end of the experiment were not significantly different between the gonadally intact hamsters and the castrated, testosterone-treated hamsters exposed continuously to short days. Males transferred from either long or short days to the intermediate-daylength condition responded behaviorally to this photoperiod as if it were a short day, that is, their ejaculatory frequency declined. We conclude that male hamsters exposed to photoinhibitory daylengths exhibit deficits in their sexual behavior, not only because endogenous levels of testosterone decrease, but also because the substrates on which this hormone acts become less responsive. We hypothesize that under physiological conditions, the episodic secretion of testosterone imposes constraints on the maintenance or restoration of copulation, and that the potent behavioral effects achieved by constant-release implants of testosterone may mask the presence of photoperiodically induced alterations in the hamster's sensitivity to this gonadal hormone.     

Plasma corticosterone levels during sexual behavior in male rats

The activity of the pituitary-adrenal (p-a) system, as reflected in plasma levels of corticosterone, was determined in 14 male Long Evans rats during copulation, exposure to an open field and in control conditions. Plasma corticosterone concentration during copulation was higher than in control conditions (13.3 ± 1.2 vs 9.4 ± 1.2 μm%, p < .01), but well below mean levels obtained in the open field (21.2 ± 0.8 μm%). Individual data indicated that some males gave no evidence of p-a activation during sexual activity. Furthermore, animals which showed increased steroid levels during copulation tended to have longer latencies to reinitiate copulation after ejaculation and were behaviorally less active in a subsequent open field test. It was suggested that neither sexual arousal nor copulatory performance necessarily activates the p-a system. Males showing p-a activation may be slow to habituate to a novel stimulus and thus the elevated steroid levels may reflect an insufficient number of habituation trials with the receptive female.     

Subthalamic lesions eliminate sexual behavior in the male rat

Electrical stimulation of parts of the subthalamus and mesencephalon produces coordinated stepping movements, and for this reason these areas are sometimes referred to as the subthalamic and mesencephalic "locomotor" regions. In this study we contrast the sexual behavioral effect of electrolytic destruction of these two regions in the male rat. Lesions of the mesencephalic locomotor region had no significant effect on male sexual behavior. In contrast, subthalamic lesions centered on the caudal zona incerta just dorsal to the subthalamic nucleus eliminated sexual behavior in 6 of 15 males. The sexual behavior of the remaining males was affected to a lesser degree, for the most part in accord with the extent of destruction to this "critical zone." Subthalamic lesions produced no obvious impairment in locomotion, posture, limb use, muscle tone or sensorimotor orientation. Even so, the fact that electrical stimulation of the subthalamus elicits coordinated stepping suggests that the region is linked with systems directly concerned with movement and locomotion. These links could be particularly important in the process by which sexual motivation is translated into sexual behavior.     

Evidence for the involvement of the Arabidopsis SEC24A in male transmission

Eukaryotic cells use COPII-coated carriers for endoplasmic reticulum (ER)-to-Golgi protein transport. Selective cargo capture into ER-derived carriers is largely driven by the SEC24 component of the COPII coat. The Arabidopsis genome encodes three AtSEC24 genes with overlapping expression profiles but it is yet to be established whether the AtSEC24 proteins have overlapping roles in plant growth and development. Taking advantage of Arabidopsis thaliana as a model plant system for studying gene function in vivo, through reciprocal crosses, pollen characterization, and complementation tests, evidence is provided for a role for AtSEC24A in the male gametophyte. It is established that an AtSEC24A loss-of-function mutation is tolerated in the female gametophyte but that it causes defects in pollen leading to failure of male transmission of the AtSEC24A mutation. These data provide a characterization of plant SEC24 family in planta showing incompletely overlapping functions of the AtSEC24 isoforms. The results also attribute a novel role to SEC24 proteins in a multicellular model system, specifically in male fertility.     

Evidence that sex chromosome genes affect sexual differentiation of female sexual behavior

Female receptivity including the immobile hormone-dependent lordosis posture is essential for successful reproduction in rodents. It is well documented that lordosis is organized during the perinatal period when the actions of androgens decrease the males' ability to display this behavior in adulthood. Conversely the absence of androgens, and the presence of low levels of prepubertal estrogens, preserve circuitry that regulates this behavior in females. The current study set out to determine whether sex chromosomal genes are involved in the differentiation of this behavior. An agonadal mouse model was used to test this hypothesis. The SF-1 gene (Nr5a1) is required for development of gonads and adrenal glands, and knockout mice are consequently not exposed to endogenous gonadal steroids. Thus contributions of sex chromosome genes can be disassociated from the actions of estrogens. Use of this model reveals a direct genetic contribution from sex chromosomes in the display of lordosis and other female-typical sexual behavior patterns. It is likely that the concentrations of gonadal steroids present during normal male development modify the actions of sex chromosome genes on the potential to display female sexual behavior.     

Study of pharmacological activation of the male sexual behavior

The model of sexual exhaustion of male rats was used in the study. The specific aim was to compare the effects of cocaine on the mount latency, number of mounts, intromissions and ejaculations during the entire copulatory cycle with the same indices during the first 30 min of observation (the latter is most frequently used in laboratory settings). Experiments consisted of four 3-day test periods. On days 1 and 2, male rats were allowed to interact with receptive females until the satiation criterion was reached (30 min without mounts). On day 3, male rats were injected with cocaine (5, 10, or 30 mg/kg, i.p.) or its vehicle 15 min prior to testing. Cocaine administration in a dose-dependent way increased the total number of mounts and ejaculations during the entire observation session but not during the initial 30-min period. The mount latency was unaffected by cocaine treatment. The results suggest that the expression of the stimulating effects of cocaine on sexual behavior depends on the duration of the observation period.     

Restoration of male sexual behavior by adult exogenous estrogens in male aromatase knockout mice

We previously found that male aromatase knockout (ArKO) mice that carry a targeted mutation in exons 1 and 2 of the CYP19 gene and as a result cannot aromatize androgen to estrogen show impaired sexual behavior in adulthood. To determine whether this impairment was due to a lack of activation of sexual behavior by estradiol, we studied here male coital behavior as well as olfactory investigation of sexually relevant odors in male ArKO mice following adult treatment with estradiol benzoate (EB) or dihydrotestosterone propionate (DHTP). Again, we found that gonadally intact ArKO males show pronounced behavioral deficits affecting their male coital behavior as well as their olfactory investigation of volatile body odors but not that of soiled bedding. Deficits in male coital behavior were largely corrected following adult treatment with EB and the androgen DHTP, suggesting that estradiol has prominent activational effects on this behavior. By contrast, adult treatment with EB to either castrated or gonadally intact ArKO males did not stimulate olfactory investigation of volatile body odors, suggesting that this impairment may result from a lack of proper organization of this behavior during ontogeny due to the chronic lack of estrogens. In conclusion, the present studies suggest that the behavioral deficits in sexual behavior in male ArKO mice result predominantly from a lack of activation of the behavior by estrogens. This is in contrast with earlier pharmacological studies performed on rats and ferrets that have suggested strong organizational effects of estradiol on male sexual behavior.