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Distribution of Fos immunoreactivity following mating versus anogenital investigation in the male rat brain.

In the present study a detailed quantitative analysis was made using Fos as a marker for neural activation to define which subregions in the neural circuitry underlying male sexual behavior are involved in display of anogenital investigation versus copulation. Neural activity was differentially distributed following anogenital investigation versus mating and was restricted to specific subdivisions that form a heavily interconnected network. Chemosensory investigation increased neural activity in the posteromedial subdivision of the bed nucleus of the stria terminalis and the posterodorsal subdivision of the medial amygdala, brain regions that receive chemosensory signals processed through the olfactory bulbs, presumably reflecting the acquisition of chemosensory signals or the display of anogenital investigation. However, other sensory signals or sexual experience may also have contributed to the induction of neural activation in these brain areas. Moreover, consummatory behavior increased neural activity in the subparafascicular nucleus, a brain region that receives genital sensory inputs. In turn, this brain region projects to the medial preoptic nucleus and posterior nucleus of the amygdala, where neural activity was also abundant only following copulation. In addition, clusters of neurons were activated in the posteromedial subdivision of the bed nucleus of the stria terminalis and posterodorsal subdivision of the medial amygdala following consummatory behavior. The present study provides an anatomically detailed picture about the distribution of neural activation following sexual behavior in the rat, specifically in relation to differences following anogenital investigation versus mating.

Amygdala↗

Sexual behavior reduces hypothalamic androgen receptor immunoreactivity.

Male sexual behavior is regulated by limbic areas like the medial preoptic nucleus (MPN), the bed nucleus of the stria terminalis (BST), the nucleus accumbens (nAcc) and the ventromedial hypothalamic nucleus (VMN). Neurons in these brain areas are rich in androgen receptors (AR) and express FOS-immunoreactivity in response to mating. In many species sexual satiation, a state of sexual behavior inhibition, is attained after multiple ejaculations. The mechanisms underlying sexual satiation are largely unknown. In this study we show that sexual activity reduces androgen receptor immunoreactivity (AR-ir) in some of the brain areas associated with the control of male sexual behavior, but not in others. Thus, one ejaculation reduced the AR-ir in the MPN and nAcc, but not in the BST and VMN. Copulation to satiation, on the other hand, reduced AR-ir in the MPN, nAcc and VMN, and not in the BST. The AR-ir reduction observed in the MPN of sexually satiated rats was drastic when compared to that of animals ejaculating once. Serum androgen levels did not vary after one ejaculation or copulation to exhaustion. These data reveal that sexual activity reduces AR in specific brain areas and suggest the possibility that such a reduction underlies the sexual inhibition that characterizes sexual satiety.

Analysis of Variance↗

Love: an emergent property of the mammalian autonomic nervous system.

The evolution of the autonomic nervous system provides an organizing principle to interpret the adaptive significance of mammalian affective processes including courting, sexual arousal, copulation, and the establishment of enduring social bonds. According to the Polyvagal Theory (Porges, 1995, 1996, 1997), the well-documented phylogenetic shift in the neural regulation of the autonomic nervous system passes through three stages, each with an associated behavioral strategy. The first stage is characterized by a primitive unmyelinated visceral vagus that fosters digestion and responds to threat by depressing metabolic activity. Behaviorally, the first stage is associated with immobilization behaviors. The second stage is characterized by the sympathetic nervous system that is capable of increasing metabolic output and inhibiting the visceral vagus to foster mobilization behaviors necessary for 'fight or flight'. The third stage, unique to mammals, is characterized by a myelinated vagus that can rapidly regulate cardiac output to foster engagement and disengagement with the environment. The mammalian vagus is neuroanatomically linked to the cranial nerves that regulate social engagement via facial expression and vocalization. The Polyvagal Theory provides neurobiological explanations for two dimensions of intimacy: courting and the establishment of enduring pair-bonds. Courting is dependent upon the social engagement strategies associated with the mammalian vagus. The establishment of enduring pair-bonds is dependent upon a co-opting of the visceral vagus from an immobilization system associated with fear and avoidance to an immobilization system associated with safety and trust. The theory proposes that the phylogenetic development of the mammalian vagus is paralleled by a specialized communication, via oxytocin and vasopressin, between the hypothalamus and the medullary source nuclei of the viscera vagus, which facilitates sexual arousal, copulation, and the development of enduring pair-bonds.

Animals↗

Effects of hydroxyflutamide in the medial preoptic area or lateral septum on reproductive behaviors in male rats.

We examined whether androgen receptors in the medial preoptic area (MPOA) and lateral septum (LS) are required for the expression of copulation and sexual motivation. Castrated males received testosterone-filled silastic capsules to restore behavior, and were implanted with the antiandrogen hydroxyflutamide (OHF) or blank cannulae. One group was implanted in either the anteroventral MPOA or LS (ANT group). Another group was implanted in the posterodorsal MPOA or LS (POST group). Copulation was tested on days 2, 6, 10, and 14 of OHF exposure; partner preference, a measure of sexual motivation, was tested on day 15. The results showed that sexual behavior was significantly suppressed by OHF in the MPOA of the ANT group, but not the POST group. However, sexual motivation was significantly reduced by OHF in the MPOA of the POST group, but not the ANT group. In the LS, OHF had no effect on sexual behavior and partner preference regardless of implant site. The data suggest site specificity within the MPOA for androgen receptor activation of male reproductive behaviors.

Androgen Antagonists↗

Effects of nickel chloride on reproduction of the rat and possible antagonistic role of selenium.

Nickel (10-100 ppm added as NiCl2) was studied to determine its effects on reproduction of Wistar rats. In nine experimental groups, females, males or both were exposed to nickel in drinking water. In one female group and one male group, the drinking water was also supplemented with 0.3 ppm selenium (added as Na2SeO3). Breeding success and the growth and viability of pups were recorded. Nickel, copper and zinc concentrations in kidneys, liver and skin (with fur) of the females, males and pups were determined with an atomic absorption spectrophotometer. In addition, histology of the male testes (from control and nickel-exposed groups) was studied. The female exposures started 14, 28 or 100 days before copulation and continued during pregnancy and lactation. When the males were exposed (for 28 or 42 days before copulation), NiCl2 reduced both the number of pregnancies and the number of pups born. In the testes, NiCl2 induced shrinkage of the seminiferous tubules, which seemed to close some of the tubules. In the tubules, NiCl2 decreased the number of basal spermatogonia. When the females or both parents were exposed to NiCl2, pup mortality during lactation was high. However, when the females were drinking NiCl2 supplemented with selenium, all the pups survived and development of the total mass of the litters was even better than in the control group. In the same way, in males, selenium supplementation of the drinking water protected those pups that were born; but fertility was lower than with the control treatment. In the tissues studied, nickel accumulated most in the kidneys and then in the liver and skin. In each type of organ, there was a clear dose response relationship. In the pups, in particular, selenium (given to the females) increased the amount of nickel in tissues compared with corresponding administration of nickel without selenium. In summary, selenium seemed to counteract the deleterious effects of NiCl2 on the reproduction of rats.

Animals↗

Reproductive effects of prenatal exposure to 5-bromo-2'-deoxyuridine on male rats.

5-Bromo-2'-deoxyuridine (BrdU) was administered intraperitoneally to Sprague-Dawley rats at doses of 12.5, 25, 50, or 100 mg/kg/d on days 9 through 15 of gestation, and at 50 or 100 mg/kg/d on days 16 through 20 of gestation. Dams were allowed to deliver naturally and the numbers of live and dead pups were recorded. Male offspring were allowed to mature and then cohabited with untreated female rats for assessment of reproductive performance. Dam body weight gain during pregnancy and lactation periods was not reduced by the treatment with BrdU. Dams treated with 50 and 100 mg BrdU/kg on days 9 through 15 of gestation had litters with decreased survival rates. The male offspring from dams treated with 25, 50, and 100 mg BrdU/kg on days 9 through 15 of gestation had reduced body weights over the course of the entire study. A dose-related decrease in copulation and fertility rates was found in the male offspring of dams treated on days 9 through 15 of gestation, while no significant decrease in those rates were found in the male offspring of dams treated on days 16 through 20 of gestation. Neither histopathologic examination of testes nor sperm examination indicated the cause of the impaired fertility in the male offspring from dams treated with BrdU on days 9 through 15 of gestation. All of the male offspring of dams treated with 100 mg BrdU/kg on days 9 through 15 of gestation failed to copulate, and some of the male offspring of dams treated with 50 mg BrdU/kg on days 9 through 15 of gestation did not form copulatory plugs or formed very small plugs. Dilatation of the lateral ventricles and cysts in the pars distalis of the pituitary were observed in all of the male offspring of dams treated with 100 mg BrdU/kg on days 9 through 15 of gestation. The impaired fertility of the male offspring of dams treated prenatally with BrdU may have resulted from BrdU exposure effects on central nervous system action such as loss of libido and from failure to form proper copulatory plugs, rather than the direct effects of BrdU on the male reproductive organs.

Animals↗

Effects of prenatal exposure to 5-bromo-2'-deoxyuridine on the developing brain and reproductive function in male mouse offspring.

The effect of prenatal exposure to 5-bromo-2'-deoxyuridine (BrdU) on the brain and reproduction in mice was studied. ICR mice were treated intraperitoneally (i.p.) with BrdU at 200 mg/kg on Day 10, 13, or 15 of gestation, or with BrdU at various doses (100 to 800 mg/kg) on Day 10 of gestation. In both experiments, dams were allowed to deliver, and male offspring were aged for 10 weeks and then cohabited with untreated females. In the phase-specificity study, the copulation rate was significantly decreased in the group treated on Day 10 of gestation, while the rate in the groups treated on Day 13 or 15 was comparable to the control level. In the dose-dependency study, copulation rates in the groups treated with BrdU at 200, 400, and 800 mg/kg were significantly lower than the control level, while the rate in the group treated with BrdU at 100 mg/kg was comparable to the control level. Masculine sexual behavior in the group treated with BrdU at 800 mg/kg was markedly impaired. Neither histopathologic changes of testis and sex-accessory glands nor alterations of sperm motility and concentration were observed in the offspring of the highest dose group. Dilatation of the third ventricles was observed in the highest dose group, whereas the relative brain weight in this group was comparable to that in the control group. In the subsequent study, ICR mice were treated i.p. with BrdU at various doses (25 to 800 mg/kg) on Day 10 of gestation, and the embryos were obtained 24 h after treatment. Histopathologic evaluation was performed in the ventricular zone of the telencephalon as well as ependymal and mantle layers of diencephalon (hypothalamus). The incidence of pyknotic cells in these areas was increased linearly with increasing BrdU dose and the incidence in the ependymal and mantle layers of the diencephalon was higher than that in the ventricular zone of the telencephalon. From these results, we conclude that damage to the central nervous system resulting from excessive cell death in the developing brain, particularly in the ependymal and mantle layers of the diencephalon (hypothalamus) may lead to reproductive dysfunction in postpubertal male offspring.

Animals↗

An additional type of male sterility and inherited urinary obstruction in mice with the t-haplotype th7.

The t-complex on mouse chromosome 17 results in transmission ratio distortion in males heterozygous for complete haplotypes, and sterility in those homozygous for semi-lethal or doubly heterozygous for complementing lethal haplotypes. This sterility is due to inability of spermatozoa to fertilize. The haplotype th7 is an unusual laboratory-derived haplotype, postulated to carry a small duplication of t chromatin. Males heterozygous for th7 show a new form of sterility, apparently due to failure to form copulation plugs during mating. This is accompanied by a strong propensity to acute urinary obstruction. It is suggested that both the failure to form copulation plugs and the urinary obstruction are due to some abnormality in function of the accessory sex glands, and are the result of incorrect dosage of a gene in the postulated duplication. The symbol Msu for male sterility and urinary obstruction is suggested for the locus concerned. Previously a recessive form of abnormal behaviour had also been attributed to this duplication.

Acute Disease↗

The genetics of mating recognition between Drosophila simulans and D. sechellia.

During courtship, visual and chemical signals are often exchanged between the sexes. The proper exchange of such signals ensures intraspecific recognition. We have examined the genetic basis of interspecific differences in male mating behaviour and pheromone concentration between Drosophila simulans and D. sechellia by using Drosophila simulans/D. sechellia introgression lines. Our results show a majority of quantitative trait loci (QTLs) explaining variation in both male mating behaviour and pheromone concentration to be located on the third chromosome. One QTL found on the third chromosome explains variation in time needed to start courtship and copulation as well as time spent courting. The position of such QTL (approximately 84A-88B) with effects on courtship and copulation aspects of mating includes the candidate sex determination gene doublesex (84E5-6) and Voila (86E1-2), a gene that affects male courtship in D. melanogaster. One additional third chromosome QTL explained variation in 7-tricosene pheromone concentrations among males. The interval mapping position of this QTL (approximately 68E-76E) did not overlap with the position detected for differences in mating behaviour and the intervals did not include candidate genes previously identified as having an effect on D. melanogaster cuticular hydrocarbon production. We did not detect any directionality of the effect of Drosophila sechellia allele introgressions in male mating recognition.

Alkenes↗

Sexual behavior and diel activity of citrus fruit borer Ecdytolopha aurantiana.

Males and virgin females of the citrus fruit borer Ecdytolopha aurantiana Lima, displayed two flight peaks during a 24-hr period, one at dawn and the other at dusk in an orange grove near Gavião Peixoto, São Paulo, Brazil. During the day, when temperatures were highest and relative humidity lowest, most individuals rested on leaves in the lower and middle crown. Moths rapidly moved higher in the crown after sunset, and many were observed flying above the tree canopy. This behavior was mainly associated with mating. Males and virgin females marked with fluorescent powder of different colors were observed in the dark with the aid of a black light. Mating was observed only in the upper crown of citrus trees from 6:00 to 9:00 PM, with a peak (64%) between 7:00 and 8:00 PM. Males of E. aurantiana were captured in traps baited either with virgin females or female extracts, suggesting the use of a long-range sex pheromone. At close distance (1-2 cm), males and females displayed a short-range communication behavior, with males exposing hairpencils and vibrating their wings. Females were frequently stimulated to contact the body of a male before copulation. The mean duration of copulation was 1 hr 40 min.

Animal Communication↗

Mutations in raised Drosophila melanogaster affect experience-dependent aspects of sexual behavior in both sexes.

Many aspects of the reproductive behavior of Drosophila melanogaster are modified dramatically by experience and age. Males' courtship of immature males and fertilized females decreases over time. Females' receptivity to copulation, and the behaviors that females perform and elicit, are affected by their age and sexual experience. We show that mutations in a raised stock affect all of these age- and experience-dependent aspects of male and female sexual behavior. Experience has no effect on raised males' courtship of immature males and has opposite effects on raised and wild-type males' courtship of fertilized females. In comparison to controls, raised females become sexually mature at an earlier age, and sexually mature raised virgin females copulate more quickly. Following mating, raised females elicit more courtship and remate faster and more frequently than control females.

Animals↗

Is human ovulation concealed? Evidence from conception beliefs in a hunter-gatherer society.

Several researchers have suggested that ovulation may not be concealed in humans living under natural conditions with minimal hygiene. Because measuring coital frequency in such a population is problematic, I tested this proposition indirectly by asking Hadza hunter-gatherers of Tanzania when a woman can get pregnant. If people (1) know that pregnancy is caused by sex, and people (2) say that women conceive in the middle of the menstrual cycle, we might infer that people think women conceive in the middle of the cycle because most copulations occur then. If copulation peaks strongly around ovulation, it is not concealed. The Hadza know that pregnancy is caused by sex but most say conception occurs right after menstruation ends. Hadza conception beliefs therefore do not suggest that ovulation is more detectable in humans under more natural conditions.

Adult↗

Microlesions of the ventromedial nucleus of the hypothalamus: effects on sociosexual behaviors in male rats.

Electrolytic microlesions aimed at the dorsomedial portion of the ventromedial nucleus (VMN) of the hypothalamus were generated, and effects on copulation, 50-kHz vocalizations, scent marking, and sexual motivation were measured. Male rats were tested before and after lesions, after castration, and after testosterone replacement. Three control groups were used: One received sham surgery, another received no surgery or testosterone replacement, and a 3rd received lesions primarily outside the VMN. VMN lesions produced impairments in testosterone's ability to restore ultrasonic vocalizations and scent marking, assessed with 2 different test methods. Copulation, sexual motivation, and weight gain were largely unaffected, although some differences were observed in copulatory efficiency. The authors conclude that the integrity of the VMN is important for full expression of sociosexual behaviors in male rats.

Analysis of Variance↗

Hypothetical spinal pacemaker regulating penile reflexes in rats: evidence from transection of spinal cord and dorsal penile nerves.

Male rats were given three weekly tests for penile reflexes, which were evoked from supine animals by extending, and then maintaining, the glans penis outside its sheath. Six days prior to Tests 2 and 3, five groups (n = 5--7) of males were subjected to spinal cord (SC) transection (at the ninth thoracic vertebra), dorsal penile nerve (DPN) transection, both operations (one after Test 1, the other after Test 2), or no surgery. Penile reflex potential was drastically depressed in males receiving DPN surgery after Test 1 and much enhanced in males in which the SC was cut. The depression in reflexes following DPN transection was reversed by subsequent SC transection. Conversely, SC transection prevented most of the depressive effects of subsequent DPN transection. It is inferred that (a) during the reflex latency of intact males, DPN-mediated tonic stimulation acts to reduce the suprasegmental inhibition of penile reflexes and (b) following the reduction in suprasegmental inhibition, whether functionally by DPN-mediated stimulation or surgically by spinal transection, a spinal pacemaker regulates the rate at which clusters of penile reflexes occur, irrespective of further DPN-mediated afference. The reflex pacemaker may also contribute to the pacing of the male's attempts to copulate, but the pacemaker must have considerable latitude for entrainment during copulation by stimuli extrinsic and intrinsic to the male.

Animals↗

Sperm competition between Drosophila males involves both displacement and incapacitation.

Females in almost all animal groups copulate with multiple males. This behaviour allows different males to compete for fertilization and gives females the opportunity to mediate this competition. In many animals and most insects, the second male to copulate with a female typically sires most of her offspring. In Drosophila melanogaster, this second-male sperm precedence has long been studied but, as in most species, its mechanism has remained unknown. Here we show, using labelled sperm in doubly mated females, that males can both physically displace and incapacitate stored sperm from earlier-mating males. Displacement occurs only if the second male transfers sperm to the female, and in only one of her three sperm-storage organs. Incapacitation can be caused by either fertile or spermless second males, but requires extended intervals between matings. Sperm from different males are not 'stratified' in the storage organs but mix freely. Many animal species may have multiple mechanisms of sperm competition like those observed here, and revealing these mechanisms is necessary to understand the genetic and evolutionary basis of second-male sperm precedence in animals.

Animals↗

DNA fingerprinting in birds.

Several regions of the human genome are highly variable in populations because the number of repeats in these regions of a short 'minisatellite' sequence varies at high frequency. Different minisatellites have a core sequence in common, however, and probes made up of tandem repeats of this core sequence detect many highly variable DNA fragments in several species including humans, cats, dogs and mice. The hypervariable sequences detected in this way are dispersed in the genome and their variability means that they can be used as a DNA 'fingerprint', providing a novel method for the identification of individuals, confirmation of biological relationships and human genetic analysis. We show here that human minisatellite-derived probes also detect highly variable regions in bird DNAs. Segregation analysis in a house sparrow family confirms that these regions comprise many mostly heterozygous dispersed loci and we conclude that house sparrow DNA fingerprints are analogous to those of humans. Fingerprint analysis identified one nestling, with fingerprint bands not present in the parent pair's fingerprints, which we conclude resulted from an extrapair copulation. Extrabond copulations have been described in many wild bird species, but their success and hence adaptive significance have rarely been quantifiable. DNA fingerprinting will be of great significance to studies of the sociobiology, demography and ecology of wild birds.

Animals↗

Mate guarding as paternity insurance in Idaho ground squirrels.

Following a copulation, males in many species of vertebrates (particularly birds) and invertebrates remain near the inseminated female and repel other suitors with displays or force. Guarding males must delay resumption of competitive mate searching, but they may insure their paternity by reducing possibilities for secondary matings and sperm competition. Among mammals, post-copulatory mate guarding has been reported in rodents, mongooses, ungulates and primates, including humans, but the effects of such behaviour on male reproductive success have not been determined genetically. I report here that mate guarding by male Idaho ground squirrels (Spermophilus brunneus) enhances a male's probability of paternity. Furthermore, an analysis based on game theory shows that mate guarding is an evolutionarily stable strategy for male S. brunneus, but not male Belding's ground squirrels (S. beldingi), which resume searching once copulation is completed.

Animals↗

Sexual behavior and sex-associated environmental cues activate the mesolimbic system in male rats.

The mesolimbic system plays an important role in the regulation of both pathological behaviors such as drug addiction and normal motivated behaviors such as sexual behavior. The present study investigated the mechanism by which this system is endogenously activated during sexual behavior. Specifically, the effects of sexual experience and sex-related environmental cues on the activation of several components of the mesolimbic system were studied. The mesolimbic system consists of a dopaminergic projection from the ventral tegmental area (VTA) to the nucleus accumbens (NAc). Previous studies suggest that these neurons are under tonic inhibition by local GABA interneurons, which are in turn modulated by mu opioid receptor (MOR) ligands. To test the hypothesis that opioids are acting in the VTA during sexual behavior, visualization of MOR internalization in VTA was used as a marker for ligand-induced activation of the receptor. Significant increases in MOR internalization were observed following copulation or exposure to sex-related environmental cues. The next goal was to determine if sexual behavior activates dopamine neurons in the VTA, using tyrosine hydroxylase as a marker for dopaminergic neurons and Fos-immunoreactivity as a marker for neuronal activation. Significant increases in the percentage of activated dopaminergic neurons were observed following copulation or exposure to sex-related environmental cues. In addition, mating and sex-related cues activated a large population of nondopaminergic neurons in VTA as well as neurons in both the NAc Core and Shell. Taken together, our results provide functional neuroanatomical evidence that the mesolimbic system is activated by both sexual behavior and exposure to sex-related environmental cues.

Animals↗