Fetal testosterone surge: specific modulations induced in male rats by maternal stress and/or alcohol consumption

Plasma testosterone (T) was measured in control male and female rats on gestational days 16, 17, 18, 19, and 20 and on days 17-20 in males from dams who were fed ethanol and/or were stressed during pregnancy. Circulating T in control males showed an earlier rise, yielding a longer period of prenatal T elevation, than was reported previously (Endocrinology 106 (1980)306). Compared to control males, exposure to alcohol-alone augmented T on days 18 and 19, stress-alone attenuated prenatal T, and the combination of stress and alcohol completely blocked the normal rise in T between days 17 and 18. When these prenatal alterations in T are viewed along with effects these same treatments have on the postparturient T surge (Horm. Behav. 41 (2002) 229), a possible explanatory mechanism emerges for the uniquely different behavioral patterns of sexual behavior differentiation induced in males by prenatal exposure to alcohol, stress, or both factors. Whereas the potential for feminine behavior is retained to the extent that either the prenatal or the neonatal T surge is attenuated, the male potential is more sensitive to reductions in the fetal surge and is maximally disrupted if both the prenatal and the postparturitional T surges are suppressed.     

Androgen threshold to activate copulation differs in male rats prenatally exposed to alcohol, stress, or both factors.

Few male rats prenatally exposed to a combination of alcohol and stress copulate spontaneously. This study determined adult sensitivity to testosterone (T) in males prenatally exposed to alcohol, to stress, or to both factors. Sexually naive males were tested with receptive females following castration and implantation of 20-, 30-, or 45-mm Silastic T-filled capsules. Serum T levels provided by these implants were measured. The behavior shown by males exposed only to prenatal alcohol did not differ from untreated control animals at any T dosage. Prenatal stress alone diminished the copulatory potential below control levels only when the intermediate T dosage was provided. Few males exposed to both alcohol and stress copulated under the lowest or the intermediate dose of adult T replacement, but most ejaculated normally when the largest capsule was implanted. The threshold to the sexual behavior-activating-properties of adult T exposure was moderately raised by prenatal stress but was severely affected when prenatal stress was combined with alcohol. We conclude that a diminished sensitivity to androgen in adulthood underlies some copulatory deficits resulting from treatments that alter fetal T levels. Such deficits may be concealed when behavior is evaluated in gonadally intact animals.     

Importance of intense male sexual behavior for inducing the preovulatory LH surge and ovulation in seasonally anovulatory female goats

The present study was carried out to determine whether the presence of photostimulated sedated male goats could stimulate the LH preovulatory surge and ovulation in seasonal anestrous goats. Sexually experienced male goats were treated with artificial long days (16 hours light per day) from 1 November to 15 January to stimulate their sexual activity in March and April, corresponding to the natural sexual rest. A female group of goats (n = 20) was exposed to non-sedated males who displayed an intense sexual behavior and provided strong odor (non-sedated group). Another female group of goats (n = 20) was exposed to the photo-stimulated male goats, but these males were sedated with Xylazine 2% to prevent the expression of sexual behavior (sedated group). The sedated males also provided a strong odor. Females of both groups had full physical and visual contact with non-sedated or sedated males. In both groups, the males remained with females during 4 days. The LH preovulatory surge of 10 female goats per group was measured by determination of LH plasma concentrations in samples taken every 3 hours. In addition, in all goats, (n = 20 by group), ovulation was determined by measuring plasma concentrations of progesterone. The proportion of female goats showing a preovulatory LH surge was higher in goats exposed to non-sedated (10/10) than in those exposed to sedated bucks (0/10; P < 0.0001). Similarly, most of does in contact with non-sedated males ovulated (19/20), but none of those in contact with sedated males did so (0/20; P < 0.0001). We conclude that the expression of an intense sexual behavior by male goats is necessary to induce LH preovulatory surge and ovulation in seasonally anovulatory goats.     

Effects of testosterone on ontogeny of urinary behavior in male and female dogs

Development of urinary behavior from birth to adulthood was observed in six groups of beagles including normal males (NM), normal females (NF), males castrated soon after birth (CM), males castrated soon after birth and treated with testosterone (T) for the next 90 days (CMT), females exposed to T in utero (FTU), and females exposed to T in utero and during infancy, i.e., the first 30-40 days postpartum (FTUI). Prenatal treatment with T had masculinizing effects on juvenile urinary behavior in FTU and FTUI. On the other hand normal development of fully adult masculine urinary patterns in males and females necessitated both prenatal and postnatal androgenic stimulation. It was not necessary that T be present at the time the overt behavior developed. For example, adult male behavior appeared in FTUI at the same time as in NM, i.e., 6-10 months, although the supply of exogenous androgen in FTUI had been exhausted within 30-40 days after birth. CMT showed precocious development of all components of the adult male pattern. Development of adult responses was markedly retarded in most CM, and their performance did not equal that of NM at 23 months. They were then injected with TP which promptly evoked completely normal male urinary behavior. It is tentatively concluded that T acting before birth and during the juvenile period "prepares" critical CNS mechanisms so that when general maturation reaches the appropriate point adult male behavior develops. Although the preparatory role of T is essential, the behavior is not dependent on T after it has developed.     

Influence of environmental events immediately after birth on postnatal testosterone secretion and adult sexual behavior in the male rat

A rise in plasma testosterone (T) levels occurs in male rats during the first 2 hr after birth which is of importance for the process of sexual differentiation. To study the influence of environmental factors on the postnatal T surge and sexual development, newborn male rats were subjected to various treatments immediately after cesarean delivery including cooling, ether anesthesia, and mother-infant separation. In adulthood, the animals were observed for masculine and feminine sexual behavior. Males anesthetized at 0 hr showed elevated levels of feminine sexual behavior and impaired masculine sexual behavior. Pups subjected to cooling or mother-infant separation showed slightly prolonged intromission latencies, but otherwise normal levels of feminine sexual behavior. Significantly elevated plasma T levels were found in intact pups 2 hr after birth but not in pups subjected to cooling or ether anesthesia. Significantly higher levels of T were observed in pups subjected to cooling 4 hr after birth, suggesting a delay of the T surge. The most pronounced impairing effects were seen in the defeminization process, but the masculinization process also is affected by ether anesthesia. It was concluded that ether anesthesia immediately after birth may permanently interfere with the sexual development by suppressing the neonatal T surge.     

Endocrine and energetic mediation of play behavior in free-living Belding's ground squirrels.

Many juvenile mammals play, and rates and patterns of play behavior often differ between young males and females. The sexual dimorphisms typical of mammalian play suggest that it might be influenced by gonadal hormones. Moreover, because play competes with growth, physical development, and acquisition of fat reserves for available energy, play behavior should theoretically be influenced by energetic variables. We examined patterns of social play behavior and endocrine and energetic mediation of social play in free-living juvenile Belding's ground squirrels (Spermophilus beldingi). Bouts of social play in young S. beldingi resembled adult copulation and fighting, and young males initiated sexual play but not play fighting at much higher rates than did young females. To elucidate the proximal causes of play, we altered early androgen exposure by treating females with testosterone (T) at birth and used females treated with oil vehicle as controls. We concurrently manipulated energy availability by provisioning with extra food and used unprovisioned squirrels as controls. Hourly rates of play behavior were highest near the time of weaning and declined thereafter among both experimental and control groups of juveniles. Thus, we observed no influence of either T treatment or food provisioning on the temporal patterning of play behavior. Perinatal T treatment had no effect on play fighting, but caused rates of sexual play behavior initiated by young females to increase to near those observed for young males, suggesting that T organizes a masculine tendency to initiate sexual play behavior but not play fighting. Food provisioning increased rates of play among males and females from both T-treated and control litters, suggesting that energy availability limits play behavior.     

孕期低氧应激对子代雄性大鼠性行为的影响

目的:研究孕期低氧应激对子代雄性大鼠的繁殖行为及相关激素分泌的影响。方法:实验将配对获得的怀孕第14天的母鼠随机分为3组:对照组(Control)、3300m模拟高原低氧应激组和5000m模拟高原低氧应激组,实验组母鼠放入低氧舱中进行持续7天的模拟低氧应激处理,对照组在实验条件下常规饲养。结果:孕期经低氧应激子代雄性性成熟个体具有与雌性个体交配的能力,但是行为能力有不同程度的下降。同时,应激组个体肛阴距变短,血浆睾酮水平下降而皮质酮水平显著升高,而3组动物睾酮、附睾以及肾上腺指数间无显著差异。结论:出生前受到低氧应激对子代雄性个体的性行为能力产生持久的抑制影响。     

Early androgen treatment and male and female sexual behavior in mice

To investigate the role of neonatal androgen stimulation in the development of the potential for masculine and feminine sexual behavior in the mouse, different groups of mice were hormonally manipulated early in life. One group of female mice was administered testosterone propionate (TP) within 24 hr of birth; a second group of females was given a control injection of oil on the day of birth; a third group of females received an injection of TP on the 10th day after birth. A group of males received a control injection of oil on the day of birth. All mice were gonadectomized at about 30 days of age. At 60 days of age, mice were injected with estrogen and progesterone and tested for sexual receptivity; several weeks later all mice were injected with TP and tested for male sexual behavior. Female behavior: Females given oil at birth and females given TP on the 10th day after birth showed high levels of sexual receptivity as adults following estrogen-progesterone treatment. Females given TP on the day of birth, and male mice, rarely exhibited lordosis following estrogen-progesterone treatment. Male behavior: Most mice, regardless of genetic sex or neonatal treatment, mounted in adulthood following administration of exogenous androgen. There was little difference in mounting frequency between groups, suggesting that exogenous or endogenous androgen stimulation of the neonatal mouse does not facilitate adult mounting behavior. These data for the mouse are in essential agreement with existing data for the rat, and indicate that sexual behavioral differentiation induced by androgen stimulation in infancy is best characterized as an inhibition of the potential to display feminine sexual behavior in adulthood.     

Changes in masculine sexual behavior, corticosterone and testosterone in response to acute and chronic stress in male rats

Chronic exposure to stressors increases HPA axis activity and concomitantly reduces HPG axis activity. This antagonistic relationship between both these axes has been proposed to underlie the inhibition of reproductive function due to stress. Sexual behavior in males may be the most vulnerable aspect of male reproduction to acute and chronic stress and it has been suggested that alterations in sexual behavior during stress are due to the antagonistic relationship between testosterone and corticosteroids. However, only in a few studies has a correlation between the levels of testosterone and corticosterone, and sexual behavior been made. In this study, we evaluated the effects of different stressors, applied both acute and chronically, on masculine sexual behavior and whether or not these effects on sexual behavior are accompanied by changes in plasma levels of corticosterone and testosterone. Additionally, we evaluated the effect of testosterone treatment on the effects of stress on sexual behavior. Sexually experienced male rats were exposed to one of the following stressors: immobilization (IMB), electric foot shocks (EFS) or immersion in cold water (ICW). Sexual behavior and plasma levels of testosterone and corticosterone were assessed on days 1, 5, 10, 15, and 20 of stress. In a second experiment, males were castrated, treated with 3 different doses of testosterone propionate (TP) and exposed to ICW for 20 consecutive days. Sexual behavior was assessed on days 1, 5, 10, 15, and 20 and steroids were evaluated on day 20. Parameters of masculine sexual behavior were modified depending on the characteristics of each stressor. Mount, intromission and ejaculation latencies increased significantly, the number of mounts increased, and ejaculations decreased significantly in males exposed to EFS and to ICW but not in males exposed to IMB. Associated with these effects, testosterone decreased in the EFS and ICW groups on days 1, 15, and 20. However, corticosterone increased only in males exposed to ICW. In castrated males, TP treatment failed to block the effects of stress by ICW on sexual behavior and corticosterone. These results indicate that the effects of stress on sexual behavior depend on the characteristics of each stressor, and these effects, as well as the decrease in testosterone are not necessarily associated with the increase in corticosterone. The fact that testosterone treatment did not prevent the effects of stress on sexual behavior suggests that other mediators could be involved in the alterations of sexual behavior caused by stress.     

Hormonal responses to different sexually related conditions in male rats

Plasma levels of corticosterone (C) and testosterone (T) increase after sexual activity in males of several species. However, the physiological significance of these increases has not been elucidated. In the present study, hormonal response to different conditions linked to sexual activity was assessed. In the first experiment, plasma levels of C and T were assessed both in sexually experienced and naive male rats after the following conditions: (A) control group, without sexual stimulation; (B) males exposed to ovariectomized females; (C) males exposed to intact, non-receptive females; (D) males exposed to receptive females with the vagina obstructed, to avoid intromission; (E) males exposed to receptive females: but separated by a grid that prevents physical contact; (F) males exposed to receptive females during 30 min. In a second experiment, experienced male rats were allowed to repeatedly copulate until reaching the criteria for sexual exhaustion, and 24 h later, they were allowed to copulate. Once sexually related conditions ended, males were killed and their blood was obtained. C and T plasma levels were assessed by HPLC with ultraviolet (UV) detection. Results indicate that T did not increase significantly in naive male in any sexual condition, while in the experienced males, significant increases were observed with the mere presence of a receptive female and also after ejaculation. These increases were significantly larger in experienced males. On the other hand, C also increased in all sexual conditions, both in experienced and naive rats; however, the increase observed was larger in experienced males. Regarding sexual satiety, both C and T increased after copulating ad libitum to satiety. T increased almost three-fold compared to control, while C increased two-fold. No significant changes were observed in either one of the steroids 24 h after sexual exhaustion, even though males remained with a receptive female during an hour. These results show that sexual experience has an important influence on the hormonal response to sexual activity. C rises could be directly related to sexual arousal involved in the different sexual conditions, while T rises seem to have a direct relationship with both the motivation and execution aspects of masculine sexual behavior.     

Investigation of the role of postnatal testosterone in the expression of sex differences in behavior in infant rhesus macaques (Macaca mulatta)

In several primate species, males have been shown to exhibit a surge in circulating testosterone during the early postnatal period. This surge has been postulated to play a role in the development of sex differences in behavior. In this study, the role of postnatal testosterone in infant behavioral development was investigated in socially living rhesus macaques. Seven male infants were treated with a GnRH agonist, avorelin, from the first week of life onwards. Ten female infants were exposed to testosterone by implantation of capsules containing testosterone. The behavioral development of these and control infants was recorded from birth to 6 months of age. The sexually dimorphic patterns of play and mounting were not affected by manipulation of postnatal testosterone in either male or female infants. Similarly, most mother-infant interactions were not affected by the hormonal manipulation of infants. Mothers of testosterone-treated females were found to take more responsibility for moving into and out of arm's reach of their infants than mothers of some other groups of infants; however, this measure did not normally differ between mothers of male and female infants. Manipulation of the postnatal testosterone surge does significantly affect penile growth and development, but does not affect the expression of infant sex differences in behavior nor greatly affect the development of the mother-infant relationship in rhesus macaques.     

Neonatal hormonal influences on the development of proceptive and receptive feminine sexual behavior in rats

The objective of this study was to examine the influence of androgen and of the inhibiting of aromatization of androgen to estrogen during the early neonatal period on the development of receptive (lordosis and acceptance of stimulus male mounting attempts) and proceptive (affiliation with and solicitation of stimulus males) feminine sexual behavior. Within 8 hr of birth, male rats were castrated or received subcutaneous implants of the aromatase inhibitor androst-1,4,6-triene-3, 17-dione (ATD) while females received injections of testosterone propionate (TP). At 90 days of age all treated animals and controls were tested for receptive and proceptive feminine sexual behavior. It was found that androgen present neonatally blocked proceptive as well as receptive behavior patterns in adult rats. The proceptive and receptive feminine sexual behavior patterns displayed by adult males deprived of the effects of androgen neonatally either by castration or by treatment with ATD were comparable to those of normal females.     

Effects of perinatal alcohol on sexual differentiation and open-field behavior in rats

Prenatal alcohol treatment prolonged the gestation period by 1 day in 5 out of 11 mothers and decreased the anogenital distance of pups of both sexes measured at birth. There were no effects on body weights of the pups at birth, total number of pups per litter, or sex ratio. The postnatally alcohol-treated males (pups nursed by alcohol-drinking mothers) had a significantly earlier preputial separation than animals treated with alcohol prenatally only or controls. There were no differences among the groups on the parameters of adult masculine sexual behavior, plasma testosterone, weights of sex accessory glands, or open-field behavior. Animals treated perinatally with alcohol showed a significant inhibition of penile reflexes. Repeated testing, however, abolished this effect.     

Hormonal differentiation of sexual behavior in Japanese quail

The effect of hormones on the development of Japanese quail during the postembryonic period was examined. First, subcutaneous implants of estradiol monobenzoate (EB) and testosterone propionate (TP) were implanted 6–12 hr after hatching. EB and TP had no effect on the differentiation of sexual behavior in genetic males or females. However, EB had marked feminizing effects on plumage in genetic males. Second, the role of gonadal hormones during development was examined by gonadectomizing males and females 6–12 hr after hatching and treating them intramuscularly with EB or TP as adults. EB-treated adult females displayed sexual behavior typical of the genetic female and developed female plumage. A significant proportion of TP-treated females (57%) displayed male sexual behavior patterns. Cloacal gland development and male-type vocalizations were induced. EB-treated males displayed either male or female sexual patterns depending on the stimulus conditions. Third, to test whether bisexuality in gonadectomized males and females is maintained despite steroid treatment and expression of sexual behavior in adulthood, gonadectomized quail which were originally treated with EB received TP and vice versa. The results indicate that in the absence of gonadal hormones after hatching female quail remain bisexual until exposed to estrogen, whereas gonadectomized male quail retain behavioral bisexuality irrespective of prior estrogen or androgen exposure.     

Lack of sexual experience does not reduce the responses of LH, estrus or fertility in anestrous goats exposed to sexually active males

We investigated whether LH secretion, estrous behavior and fertility would differ between sexually inexperienced and experienced anestrous goats exposed to the males. Male goats were rendered sexually active during the reproductive rest season by exposure to 2.5 months of artificial long days. Two groups of anovulatory sexually inexperienced and sexually experienced does were exposed to males during 15 days (n = 20 per group). LH pulsatility was determined every 15 min from 4 h before to 8 h after introducing males (Day 0). Estrous behavior was recorded twice daily. Pregnancy rates were determined on Day 50. Fertility was determined at parturition. Male sexual behavior was registered on days 1 and 2 during 1 h. Before introducing the males, the number of LH pulses did not differ between groups. After introduction of the males, all females increased their LH pulsatility, but the number of pulses did not differ between sexually inexperienced and experienced goats. The proportion of females displaying estrous behavior with a high pregnancy rate and fertility did not differ between inexperienced and experienced goats. The sexual behavior of the males did not differ significantly between those interacting with sexually inexperienced or experienced goats. We conclude that goats can show substantial endocrine and reproductive responses to males, even in the absence of previous sexual experience, when sexually active bucks are used.     

The effects of infant births on the sociosexual behavior and hormonal patterns of a cooperatively breeding primate (Cebuella pygmaea)

This study examined changes in the behavioral and hormonal patterns of cooperatively breeding pairs in a primate species with the passing of time and with specific reproductive events. We (1) compared patterns of sexual, agonistic, and affiliative behavior of newly paired pygmy marmosets with the same behavioral patterns immediately after the birth of their first set of infants; (2) determined if postpartum behavioral differences existed between pairs whose infants lived and those whose infants died; and (3) examined whether behavioral patterns changed over the course of ovarian cycles in parous pygmy marmosets as had been documented in nulliparous pairs. The behavior of pairs was recorded during daily half-hour focal samples for 60 days after pairing, and 30 or 60 days after the birth of infants for pairs whose litters died or lived, respectively. Daily urine samples from females during the study were analyzed for luteinizing hormone and pregnanediol glucuronide concentrations to determine dates of ovulation. The results indicated that males consistently altered their sexual behavior and olfactory monitoring of mates during periovulatory periods in the females' cycles both postpairing and postpartum, while similar rates of social and sexual behavior were maintained between the conditions. Sexual behavior occurred throughout the females' ovarian cycles. Peaks in sexual behavior during the periovulatory period in nulliparous pairs disappeared after the birth of infants. Pairs whose infants died showed higher rates of sexual behavior than pairs with surviving infants. Social and sexual behavior may function to maintain the relationship both during and outside of ovulation, especially with the loss of infants. © 1996 Wiley-Liss, Inc.     

Resumption of seasonal breeding patterns in male and female rhesus monkeys transferred from an indoor to an outdoor environment

Seasonal aspects of social behavior and sex steroid levels were observed in two groups of rhesus monkeys from March through December. One group (3 males, 7 females) had lived outdoors for several years. The other group (6 males, 5 females), transferred outdoors in late February, had lived indoors for several years. In March-April, the long-term outdoor residents displayed the expected seasonal pattern of sexual behavior, characterized by absence of complete sequences of copulatory behavior. At this time the indoor-adapted group displayed high levels of copulatory behavior. Thereafter, frequencies of sexual behavior of the two groups were similar. Testosterone in the males was positively correlated with frequency of sexual behavior in each group. Females in the indoor-adapted group displaced menstrual cycles in March and April and 3 of 5 became pregnant at this time. The two remaining indoor-adapted females continued to display ovulatory cycles, but little sexual behavior, throughout the summer. Interestingly, two females in the outdoor-adapted group also displayed summer ovulatory cycles; without concomitant sexual activity. These data show that the disruption of seasonal breeding patterns produced by lengthy indoor housing remains briefly apparent following transfer outdoors, but is substantially overcome within a few months.     

Hormonal regulation of male reproductive behavior in the lizard Anolis sagrei: a test of the aromatization hypothesis

This study examined the hypothesis that aromatization of testosterone (T) to estradiol (E) is required to activate reproductive behavior in castrated male lizards (Anolis sagrei). Adult, reproductively active males were assigned to an intact control group or to one of four treatment groups. Treatment males were castrated and 1 week later three of the four castrated groups were implanted with subcutaneous pellets containing either 0.05 mg of E, 0.5 mg of T, or 0.5 mg of dihydrotestosterone (DHT). Two weeks after pellet implantation, males were tested with stimulus males, and 2 days later were tested with stimulus females. Behavioral tests were of 15-min duration and were videotaped. Significantly fewer E-treated castrates erected a crest in tests with stimulus males than did intact males. In tests with stimulus females, significantly fewer E-treated castrates displayed, neck-gripped, and intromitted than did intact males. Estradiol-treated castrates also showed significantly less display behavior than did intact males. However, aggressive and sexual behavior of DHT-treated castrates was not significantly different from that of intact males. The same was true for T-treated castrates with the exception that display behavior in tests with stimulus females was reduced compared to that of intact males. The results suggest that aromatization of T to E is not required for induction of androgen-dependent reproductive behavior in this lizard.     

Effect of maternal adrenocorticotropin injections on the differentiation of sexual behavior of the offspring

Male and female rats were prenatally exposed to high levels of corticosteroids, by treatment of their mothers with ACTH, during the last third of pregnancy. In the females, treatment increased the ano-genital distance at birth, but no effect on sexual differentiation could be detected in the adult animals: They had normal cyclic reproductive function and female lordotic sexual behavior. The prenatal treatment demasculinized the males, who showed decreased ability for complete male copulatory behavior. The demasculinizing effect of prenatal corticosteroids was, however, particularly pronounced in certain litters, while not affecting others at all.     

Aromatase inhibition during adolescence reduces adult sexual and paternal behavior in the biparental dwarf hamster Phodopus campbelli

Previous studies have failed to identify an activational role for estradiol in the paternal behavior of Phodopus campbelli fathers. However, none of these studies addressed a developmental role that estradiol might play in establishing paternal behavior in this species. Males were orally administered the aromatase inhibitor letrozole (1 mg/kg/day) for three days at 18, 34, or 90 days of age. As adults, males were tested for paternal and sexual behavior. Letrozole treatment at 18 days resulted in males that spent less time huddling over pups during the birth, and had higher pup losses and male-biased pup survival for the first litter. Letrozole treatment at 34 days resulted in males that had altered sexual behavior; males had a longer interval between mounts and between intromissions, and took longer to achieve ejaculations over the first three ejaculatory series. Furthermore, these males sired smaller first litters and produced second litters with a male-biased sex ratio. Males treated with letrozole as adults showed a modest increase in paternal care during the birth, but pup development and survival were not altered. There was no effect of treatment on attack or retrieval behavior either as sexually naive adults or as new fathers. Thus, the results of the present study suggest that estradiol acts during adolescence to establish the normal expression of midwifery behavior and sexual behavior during adulthood.