Restoration of sexual performance in old rhesus macaques paired with a preferred female partner

Experiments were undertaken to determine whether the decline in the ejaculation frequency of old male rhesus macaques is due to a decrease in physical capacity. In the first experiment, the capacity of old males to ejaculate in a series of biweekly tests was investigated. Six old (18–23 years) and six young (8– 12 years) male rhesus macaques were given 10-min tests of sexual behavior with nine different females chosen at random. The old males were also given 10-min tests with a preferred female, 1339. When the old males were tested with nine different females, their sexual performance (e.g., frequency of ejaculation) was significantly less than that of the young males, but their performance was comparable to that of young males in nine tests with female 1339. In a second experiment, the capacity of old males to show repeated ejaculations over a 3-hr period was tested. The same old and young males were given a 3-hr test with female 1339. The sexual performances (number of ejaculatory series completed and behavior displayed within each ejaculatory series) of the old males did not differ significantly from those of the young. Also, no significant differences in behavior were observed between young and old males during the first 10 min of the 3-hr tests. Our data show that the decline in the sexual performance of old rhesus males is not due to a decreased capacity to perform sexually or to physical debilitation.     

Diurnal patterns of testosterone, dihydrotestosterone, estradiol, and cortisol in serum of rhesus males: Relationship to sexual behavior in aging males

This study was carried out to determine differences between old and young rhesus males in levels and diurnal patterns of testosterone, dihydrotestosterone, cortisol, and estradiol, and to determine correlations between these hormones and sexual behavior of the old males. Blood was drawn from old (n = 9) and young (n = 9) rhesus males over 5 consecutive days at 0900, 1300, and 2100 hr. The two groups of males did not differ in mean serum levels of testosterone, dihydrotestosterone, or estradiol at any time. Although the old and young did not differ in cortisol levels at 0900 and 1300 hr, the cortisol levels at 2100 hr were lower in the old males. Diurnal variations in testosterone, dihydrotestosterone, and cortisol were comparable in old and young males. Mean serum levels of estradiol were significantly higher at 0900 hr than at 1300 hr in the old males, whereas in the young males estradiol levels did not differ with time of day. There was a significant positive correlation between testosterone and yawning rate, and cortisol levels were correlated positively with rate of contacting, rate of mounting, and percentage of tests with erections. The decline in sexual performance of old rhesus males cannot be attributed to changes in the levels or diurnal patterns of testosterone, dihydrotestosterone, or estradiol, but lower cortisol levels in old males may contribute to the decline in sexual behavior.     

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.     

Sexual behavior in aging male rhesus macaques: Effects of test duration on sexual performance

The sexual behavior displayed by nine old (20-year and older) rhesus (Macaca mulatta) males in 10-min tests was compared to that displayed in 1-hr tests. The tests were part of a long-term study on the decline in male sexual activity that accompanies old age. The males were paired with 10 ovariectomized, estrogentreated females in two blocks of 10 tests; each male was tested once with each female in each test block. The percentages of males that achieved intromissions and ejaculated in the two test blocks were the same (P < 0.05). Although the percentage of tests in which males displayed these behaviors was higher in the longer-test block (P > 0.05), there was a significant positive correlation of performance in 10-min tests with performance in 1-hr tests. Assuming a random distribution of contacting, mounting, intromission, and ejaculation throughout the hour, we would have predicted a significantly lower number of these behaviors in the first 10 min of the 1-hr tests than we actually observed. The mean percentages of 1-hr tests with contacting, mounting, intromission, and ejaculation was significantly lower than that of 10-min tests conducted with the same males 11 years earlier. Thus, the decline in sexual performance was not an artifact of the limited (10-min) test duration.     

Threshold for behavioral response to testosterone in old castrated male rhesus macaques

The sexual behaviors of old, intact (N = 5) and old, castrated (N = 6) rhesus macaque males were compared in six series of pair tests with receptive females. The castrated monkeys were tested when untreated and when given five doses of testosterone propionate (TP; 0.004, 0.016, 0.064, 0.256, and 1.024 mg/kg of body weight) in consecutive months. The serum testosterone (T) level was determined for each male before and after each series of tests. When untreated, none of the castrated males ejaculated, and yawning was significantly less in these monkeys than in intact males-no other behavioral measures differed significantly. Within 2 weeks of daily injections of 0.004 mg of TP/kg, two males ejaculated, and all differences in measures of ejaculation were eliminated. A third male ejaculated after 1 week of treatment with 0.016 mg of TP/kg. Yawning values did not differ during and after treatment with 0.064 mg of TP/kg. Although final mean serum T levels were six times higher in castrated (24.3 ng/ml) than in intact males (4.2 ng/ml), sexual performance levels did not exceed those of intact males.     

Expression of male-typical behavior in adult female pseudohermaphroditic rhesus: Comparisons with normal males and neonatally gonadectomized males and females

Two types of pseudohermaphroditic female rhesus produced by exposure to either testosterone propionate (TP) or dihydrotestosterone propionate (DHTP) prior to birth were ovariectomized postpuberally and evaluated for the display of male-typical sexual behavior in response to exogenous TP in adulthood (2 mg/kg/day for 12 weeks). Their performance in standardized tests with estrogenized female partners was compared to that of neonatally gonadectomized males and females identically tested and treated with exogenous TP as adults. In addition intact adult males not given exogenous TP were tested with the same estrogenized female partners. There were no reliable differences between the two types of pseudohermaphrodites on any measure of behavior shown during the tests. Accordingly results were combined. Reliable behavioral changes induced by the TP given in adulthood were limited to increases in purse-lip responses, the induced increases were similar in pseudohermaphrodites and castrated males, and increases were reliably greater in these two groups of subjects than in females. Pseudohermaphrodites and castrated males did not differ reliably from intact males in performance of purse-lip gestures during TP treatment. In the performance of mounting, however, pseudohermaphrodites and castrated males remained consistently below the standard of the intact males. The estrogenized female partners displayed proceptive responses most frequently to the intact males and least frequently to the females. Their proceptive responses with castrated males resembled their performance with intact males, but with pseudohermaphrodites their proceptive responses more closely resembled their performance with females. Receptive behavior of the female partners was displayed most frequently to intact males, at intermediate levels to castrated males, and least often to pseudohermaphrodites. Results are completely consistent with the notion that androgens in high concentrations before birth alter mechanisms related to the later display of masculine behavior. These alterations in behavioral mechanisms are of such a nature that the display of male-typical behavior induced by androgens in adulthood is more pronounced and more frequent than it would have been otherwise. The alterations in masculine behavior observed in pseudohermaphroditic rhesus are not different in kind or scope than those reported extensively for lower mammals.(ABSTRACT TRUNCATED AT 400 WORDS)     

Sexual behavior and serum hormone levels in aging rhesus males: effects of environmental change

Old (N = 9) and middle-aged (N = 9) rhesus males (Macaca mulatta) that were housed in the same type of home cage and the same room for several years were moved to a new location in an adjacent building. Their sexual behavior and hormone levels in the weeks preceding the move were compared to those after the move. The hypothesis that the nonspecific sensory stimulation provided by the move would increase levels of sexual behavior was not supported by the data. To the contrary, the percentages of tests with contacts, mounts, and penile erections, and the rate of contacting the female, decreased significantly for both old and middle-aged males. The intromission rate of middle-aged, but not of old, males also decreased. In consonance with previous findings, middle-aged males displayed significantly higher levels of sexual activity than did old males. The differences were observed both before and after the move. Serum testosterone levels did not differ between middle-aged and old males, and the move did not produce significant changes in testosterone levels. Serum cortisol levels were significantly higher immediately after the move (1 hr) but returned to premove levels the following day.     

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.     

Social interactions among female rhesus macaques (Macaca mulatta) during the nonbreeding season: Responses to the introduction of males

When rhesus monkeys are observed in social groups during the breeding season, increases in interfemale aggression coincide with midcycle increases in sexual activity between males and females. However, some investigators have suggested that both aggressive and affiliative interactions between females are influenced by the presence or absence of males, irrespective of menstrual cycle stage. In the present study, social interactions among members of a captive group of rhesus females were measured during the non-breeding season in response to the introduction of rhesus males. Ovariectomized rhesus females (estrogen-treated or untreated) served as stimulus controls. Tests with males were characterized by significantly decreased interfemale proximity and grooming and significantly increased aggression from that seen in tests with stimulus females or in the absence of stimulus animals. Only interfemale proximity declined significantly during stimulus female tests, but results suggest that this may merely reflect a decline in this behavior that occurs across the course of the day. Estrogen treatment did not alter either the aggressive or affiliative behavior of stimulus females or group female response to stimulus females. The possibility is discussed that changes in interfemale interactions during tests with males reflect female interest in interacting with the male, particularly under social conditions that may limit such interactions.     

Sex and context: hormones and primate sexual motivation

Gonadal hormones regulate the ability to copulate in most mammalian species, but not in primates because copulatory ability has been emancipated from hormonal control. Instead, gonadal hormones primarily influence sexual motivation. This separation of mating ability from hormonally modulated mating interest allows social experience and context to powerfully influence the expression of sexual behavior in nonhuman primates, both developmentally and in adulthood. For example, male rhesus monkeys mount males and females equally as juveniles, but mount females almost exclusively as adults. Having ejaculated with a female better predicted this transition to female mounting partners than did increased pubertal testosterone (T). It is proposed that increased pubertal T stimulates male sexual motivation, increasing the male's probability of sexual experience with females, ultimately producing a sexual preference for females. Eliminating T in adulthood reduces male sexual motivation in both humans and rhesus monkeys, but does not eliminate the capacity to engage in sex. In male rhesus monkeys the effects of reduced androgens on sexual behavior vary with social status and sexual experience. Human sexual behavior also varies with hormonal state, social context, and cultural conventions. Ovarian hormones influence female sexual desire, but the specific sexual behaviors engaged in are affected by perceived pregnancy risk, suggesting that cognition plays an important role in human sexual behavior. How the physical capacity to mate became emancipated from hormonal regulation in primates is not understood. This emancipation, however, increases the importance of motivational systems and results in primate sexual behavior being strongly influenced by social context.     

Effect of estradiol-treated females on all-female groups of rhesus monkeys during the transition between the nonbreeding and breeding seasons

Behavior, sex steroid levels and sex skin color were monitored in 2 out-door-housed all-female groups of rhesus monkeys during the nonbreeding season and into the breeding period. Each group contained gonadally intact and ovariectomized (OVX) females. In one group, 2 OVX females were implanted with estradiol benzoate pellets. Female-to-female sexual behavior, sex skin redness and endocrine indices of ovulation (in intact females) all increased as the breeding season approached. The two groups did not differ with regard to these measures. This lack of difference suggests that the presence of males may be required to mediate socially facilitated out-of-season breeding by females. No strong relationships were detected between steroid levels of intact females and sex skin color or female-to-female sexual behavior in all-female groups.     

Sexual behavior of laboratory- and wild-born male Rhesus monkeys.

Rearing method has an important influence on the sexual performance of adult male rhesus monkeys. Testosterone levels and sexual behavior of laboratory-born and -reared adult males were compared with those of males born in the wild and brought to the laboratory as adults. The mean sexual performance level of colony-reared animals was significantly below that of males born in the wild but testosterone levels in the two groups did not differ significantly. Not all laboratory-reared males were sexually inadequate but less than 30% ejaculated in tests of sexual behavior. The sexual behavior and testosterone levels of adult males treated prenatally with testosterone propionate were found not to differ from those of untreated males reared in the same way. Conclusions about sexual adequacy based on 10-mm tests of sexual behavior differed very little from those based on 1-hr tests.     

Changes in androgen receptor, estrogen receptor alpha, and sexual behavior with aging and testosterone in male rats

Reproductive aging in males is characterized by a diminution in sexual behavior beginning in middle age. We investigated the relationships among testosterone, androgen receptor (AR) and estrogen receptor alpha (ERα) cell numbers in the hypothalamus, and their relationship to sexual performance in male rats. Young (3 months) and middle-aged (12 months) rats were given sexual behavior tests, then castrated and implanted with vehicle or testosterone capsules. Rats were tested again for sexual behavior. Numbers of AR and ERα immunoreactive cells were counted in the anteroventral periventricular nucleus and the medial preoptic nucleus, and serum hormones were measured. Middle-aged intact rats had significant impairments of all sexual behavior measures compared to young males. After castration and testosterone implantation, sexual behaviors in middle-aged males were largely comparable to those in the young males. In the hypothalamus, AR cell density was significantly (5-fold) higher, and ERα cell density significantly (6-fold) lower, in testosterone- than vehicle-treated males, with no age differences. Thus, restoration of serum testosterone to comparable levels in young and middle-aged rats resulted in similar preoptic AR and ERα cell density concomitant with a reinstatement of most behaviors. These data suggest that age-related differences in sexual behavior cannot be due to absolute levels of testosterone, and further, the middle-aged brain retains the capacity to respond to exogenous testosterone with changes in hypothalamic AR and ERα expression. Our finding that testosterone replacement in aging males has profound effects on hypothalamic receptors and behavior has potential medical implications for the treatment of age-related hypogonadism in men.     

Steroids and sexual behavior in castrated male rheusus monkeys.

Sexual behavior of long-term castrated rhesus males was not increased by administration of the hydroxylated metabolite of testosterone (T), 17 beta, 19-dihydroxy-5 alpha-androstan-3-one diacetate (19-OH-DHTA) at a dose of 1 mg/kg/day. Simultaneous administration of 19-OH-DHTA and estradiol benzoate (EB) also failed to increase the level of sexual performance, but daily injection (1 mg/kg/day) of testosterone propionate (TP) was very effective in effective in activating sexual behavior.     

Sexual deprivation and its influence on testosterone levels and sexual behavior of old and middle-aged rhesus males

After approximately 6 mo without access to a receptive female, eight old (19 to 25 yr) and eight middle-aged (9 to 15 yr) males were given nine daily 10-min tests of sexual behavior with receptive females. Three ovariectomized, estrogen-primed females served as partners. Blood samples were taken from the males at 0900 and 2100 h on 2 consecutive days before and after the series of nine behavioral tests. Serum levels of testosterone (T) were measured by means of radioimmunoassay. There were no significant differences between serum T levels after 6 mo of sexual deprivation and after the nine tests of sexual behavior, nor did serum T levels differ between middle-aged and old males. Serum T levels were significantly higher in the 2100-h samples than in the 0900-h samples for both groups. The nocturnal increases in serum T, both absolute amounts and percentages of increase, did not differ between middle-aged and old males. Repeated daily testing had little effect on the major components of male sexual behavior. Middle-aged males outperformed old males; middle-aged males had higher rates of contracting the female, mounting and intromitting. They ejaculated earlier and had a greater percentage of tests with ejaculations than did old males.     

Effects of ovarian hormones on the behavior of captive Macaca fascicularis

To examine the effects of ovarian hormones on the behavior of female Macaca fascicularis and their male partners, daily 1-hr behavior tests were conducted while ovariectomized females were (1) untreated, (2) given estradiol benzoate (EB) (5 μg subcutaneously [s.c.]/day), (3) given estradiol benzoate together with increasing doses of progesterone (P) (5 mg, 10 mg, and 20 mg. s.c./day), and (4) given testosterone propionate (TP) (0.25 mg s.c./day) (six pairs, 540 tests). Weekly blood samples were analyzed by radioimmunoassay for plasma hormone levels (81 samples). Estrogen treatment produced plasma estradiol levels similar to those of intact females during the late follicular phase of the menstrual cycle. Additional progesterone at the lowest dose produced plasma progesterone levels similar to or somewhat higher than those during the midluteal phase, while higher doses produced supraphysiological levels. Androgen treatment resulted in plasma levels well above the physiological range. Hormone treatments produced highly significant effects on the sexual, social, and aggressive interactions of the pairs. As in rhesus monkeys, estrogen increased male and female sexual activity, and increasing doses of additional progesterone reversed these effects. Unlike in rhesus monkeys, testosterone propionate increased both female sexual motivation (invitations) and also male sexual activity and ejaculatory performance. The direction of the hormone-dependent changes in grooming and aggressive interactions confirmed earlier results with intact females and indicated that aggressive interactions and male grooming times were highest, and female grooming times were lowest, when copulatory activity was at its height.     

Unhealthy lifestyles during the life course: association with physical decline in late life

This study aimed to examine the association between unhealthy lifestyle in young age, midlife and/or old age and physical decline in old age, and to examine the association between chronic exposure to an unhealthy lifestyle throughout life and physical decline in old age. The study sample included 1297 respondents of the Longitudinal Aging Study Amsterdam (LASA). Lifestyle in old age (55-85 y) was assessed at baseline, while lifestyle in young age (around 25 y) and midlife (around 40 y) were assessed retrospectively. Lifestyle factors included physical activity, body mass index (BMI), number of alcohol drinks per week and smoking. Physical decline was calculated as change in physical performance score between baseline and six-year follow-up. Of the lifestyle factors present in old age, a BMI of 25-29 vs. BMI <25 kg/m2 (odds ratio (OR) 1.6; 95% confidence interval (CI) 1.1-2.2) and a BMI of > or =30 vs. BMI <25 kg/m2 (OR 1.8; 95% CI 1.2-2.7) were associated with physical decline in old age. Being physically inactive in old age was not significantly associated with an increased risk of physical decline, however, being physically inactive both in midlife and in old age increased the odds of physical decline in old age to 1.6 (95% CI 1.1-2.4) as compared to respondents who were physically inactive in midlife and physically active in old age. Being overweight in both age periods was associated with an OR of 1.5 (95% CI 1.1-2.2). These data suggest that overweight in old age, and chronic exposure to physical inactivity or overweight throughout life increases the risk of physical decline in old age. Therefore, physical activity and prevention of overweight at all ages should be stimulated to prevent physical decline in old age.     

Effects of castration and hormone replacement on male sexual behavior and pattern of expression in the brain of sex-steroid receptors in BALB/c AnN mice

Little is known about the hormonal regulation of sexual behavior and about the pattern of expression in the brain of sex-steroid receptors in the BALB/c AnN strain of mice (Mus musculus). In this study, 8-week old male BALB/c AnN mice were castrated and the temporal course of decline of sexual behavior was studied, as well as the effects of daily treatment with either testosterone propionate (TP), estradiol benzoate (EB), or dihydrotestosterone propionate (PDHT). Castration resulted in rapid decline of sexual behavior, in both control or vehicle-treated mice. TP maintained full sexual behavior of castrated mice, while PDHT or EB did not have this effect. The expression of ER-alpha dropped nearly 50% after castration, and this pattern remained in TP or PDHT-treated mice, while EB increased the ER-alpha mRNA levels to almost the same values as in intact control mice. The same pattern was found when ER-beta mRNA levels were analyzed. The expression of the PR-A/B gene in the different brain regions in intact mice and after castration, or among the differently treated mice, showed significant differences between normal and castrated mice at all times in all brain regions studied, with the exception of the frontal cortex. Castration reduced the expression of AR by 10-fold, as compared to intact control mice, while TP or PDHT treatment returned its expression to the same levels as in intact control mice, in all brain areas studied. The changes are more prominent in POA-HIP than in HYP and CF. These results demonstrated a rapid decline of sexual behavior in this strain of mice after castration, and show that only TP was able to maintain male sexual behavior, with no correlation with the pattern of expression of sex hormone receptors in specific areas of the mouse brain.     

Effects of testosterone on the behavior of male cynomolgus monkeys (Macaca fascicularis)

To determine the threshold doses of testosterone propionate (TP) that cause clear-cut behavioral changes in the sexual behavior of castrated male cynomolgus monkeys, observations were made on three males during successive 5-week treatment periods while they received daily subcutaneous doses of 100 μg TP increasing in octaves to 25.6 mg TP. Males were tested with each of the same two ovariectomized, estrogen-treated females (6 pairs, 330 1-hr behavior tests). To mimic the diurnal plasma testosterone rhythm, TP injections were given at 1600 hr and blood samples were obtained at 0800 hr (141 samples). Male ejaculatory activity increased at the threshold dose of 200 μg TP per day giving plasma testosterone levels of 830 ng/100 ml, which is in the physiological range of 600–1600 ng/100 ml for intact males. This threshold dose was eight times higher than in rhesus monkeys on a dose per kilogram body weight basis. There was a further marked increase in ejaculatory performance at higher doses (6.4 to 25.6 mg) giving supraphysiological plasma levels of 4000–9000 ng/100 ml. There were individual differences in the behavioral changes occurring with TP treatment, and the female partner modulated the effects. These findings were generally similar to those obtained with male rhesus monkeys, but certain species differences were noted.     

Changing costs of reproduction: age-based differences in reproductive allocation and escape performance in a livebearing fish

The reproductive value hypothesis predicts that if residual reproductive value declines as a female ages, then young females should allocate less of available energy to current fecundity and more to future reproduction; whereas, older females should allocate more of available energy to current fecundity and less to future reproduction (i.e. survival). We test the prediction that older female Gambusia affinis exhibit higher levels of allocation to reproduction (i.e. fecundity) and consequently experience greater decline in escape performance (survival cost) during pregnancy compared to young females. Old females had relatively larger clutch wet masses and clutch wet mass increased more during pregnancy compared to young females. Correspondingly, old females exhibit a significant decline in escape velocity over the course of pregnancy; whereas young females show no change in escape velocity throughout pregnancy. Old females have higher escape velocities early in pregnancy and their performance only declines to about the level of performance of young females by the end of pregnancy. Thus, although old females exhibit a greater decline in performance they are better able to ameliorate the cost of decreased performance.