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mise à jour du
27 mars 2003
Journal of Comparative and Physiological Psychology 1982;96(5):823-833
lexique
 Sexual behavior in adult gonadectomized female pseudohermaphrodite, female, and male Rhesus Macaques treated with estradiol benzoate and testosterone propionate
Charles H. Phoenix and Kathleen C. Chambers
Department of Primate Behavior Oregon Regional Primate Research Center, Beaverton, Oregon

Chat-logomini

Data supporting the original "organization hypothesis" were based on our research involving guinea pigs. In those experiments, genetic female guinea pigs treated prenatally with testosterone propionate (TP) displayed mating behavior as adults similar to that of castrated males when both were treated with TP. In addition, responsiveness to female hormones was suppressed. The "organization hypothesis" led us to predict that genetic males deprived of testosterone before the period of sexual differentiation was complete would have a diminished capacity to display mating behavior and an enhanced capacity to display femelle receptive behavior when appropriately treated in adulthood. Support for the hypothesis came from a series of experiments in which male rats castrated before they were 5 days old displayed less male mating behavior when treated with testosterone and more female mating behavior when treated with estradiol in adulthood than males castrated after Day 5 of life and similarly treated.

An important aspect of the organization concept was the hypothesis that "the masculinity or femininity of an animal's behavior beyond that which is purely sexual ... developed in response to certain hormonal substances within the embryo and fetus". It was largely this component of our hypothesis that led us to turn to the rhesus macaque as a model; we thought it was better suited than the guinea pig or rat.

In a series of studies on young genetic rhesus females between 3 and 48 mo of age that had been treated prenatally with TP, we found that they displayed more social threats, initiated play more frequently, and engaged in rough-and-tumble play more often than did control females. Mounting behavior also was displayed at an early age, with a frequency like that of same-age males rather than that of females. In all of those studies, the female pseudohermaphrodites (hermaphrodites) were tested without hormone treatment and with ovaries intact. Most of the tests were carried out before the animals reached the age of menarche, which was delayed.

After ovariectomy, when the hermaphrodites were between 5 and 7 yr of age, they were paired with ovariectomized, estrogentreated females in a series of 30 weekly tests. In pretreatment tests, the hermaphrodites (n = 7) displayed significantly higher levels of aggression than did control females (n = 7). The two groups were then treated with testosterone, and again aggressive behavior was displayed at a significantly higher level by the hermaphrodites than by similarly treated control females. The mounting rate did not differ between hermaphrodites and control females before or after treatment with TP. One hermaphrodite (Monkey 1640) achieved intromission and ejaculateu in two separate tests of sexual behavior. Two other hermaphrodites (Monkeys 1616 and 1239) masturbated to ejaculation in their home cages but did not achieve intromission or ejaculation during tests of sexual behavior. Thus, although evidence for the masculinizing action of testosterone on the tissues that mediate nonsexual behavior in adolescent and young adult rhesus macaques is quite clear, evidence for the same action on tissues that mediate adult mating behavior rests largely on the performance of a single animal (Monkey 1640).

These hermaphrodites were used in two additional behavioral studies when they were approximately 9-11 yr old and again when they were between 13 and 14 yr of age. Other studies that did not concern behavior but that indicated masculinization of their anatomy and physiology also were carried out. In one study, it was demonstrated that the canine dental complexes of the hermaphrodites had been masculinized. In another study, hermaphrodites and males were less sensitive to the long-term estradiol inhibition of luteinizing hormone secretion than were similarly treated females.

We undertook the experiments reported here to determine how, at the more mature age of 15-17 yr, the behavior of these hermaphrodites would differ from that of ovariectomized females; and castrated males in the absence of exogenous hormones and when treated with TP. In addition, we wished to compare the effects, if any, of estradiol on the sexual performance of hermaphrodites, control females, and castrated males in pair tests with receptive females. To our knowledge, the effects of exogenous estradiol on the sexual behavior of gonadectomized rhesus males and hermaphrodites have not been investigated. [...]

 
Discussion : It is well established that in rodents, patterns of mating behavior are readily masculinized by testosterone treatment during psychosexual differentiation. In rodents, dogs, rhesus macaques, and perhaps even human beings, behaviors other than those that are purely sexual are likewise readily masculinized by appropriate testosterone treatment during the period of differentiation. What is not well established and needs further delineation is the extent to which prenatal testosterone masculinizes the tissues mediating the mating behavior of adult primates.

In this study, the sexual behavior of gonadectomized adult females treated prenatally with testosterone did not differ substantially frora that of untreated fernales. The hermaphrodites differed only in grimace rate from females in the untreated condition. Although there was a significant overall group difference in the aggression rate, hermaphrodites did not differ from females as determined by the Newman-Keuls test. However, the proportion of hermaphrodites displaying aggression was significantly greater than the proportions of untreated males and females. When differences in behavior occurred between females and males, the hermaphrodites resembled females rather than males. Because these comparisons involved untreated animals, similarities and differences reflected something other than changes in sensitivity to hormonal stimulation in adulthood. Rather, they indicated the extent to which prenatal testosterone treatment of females modified hormonally independent behavior in adulthood.

The extent to which behavior was modified by EB or TP in adulthood also indicated that the hermaphrodites as adults resembled females rather than males. Yawning was the only behavior to show a significant rate increase after TP treatment for females and for hermaphrodites. The effect, of TP on the yawning rate in males and fernales has been well documented. The percentage of tests in which hermaphrodites showed penile erections increased significantly under TP treatment, but for all treatment conditions the percentage was significantly lower than in males. Some investigators have suggested that the malelike behavior displayed by hermaphrodites as youngsters was the result of genital development comparable to that of males. It was argued that as a consequence of each possessing a penis and scrotum, the hermaphrodites were treated as males by their mothers and were perceived to be males by their siblings; therefore, they acted as males. Yet, as adults with penile erections, and having presumably received differential treatment as infants and juveniles, they failed to display male behavior. Explaining their early masculine behavior as the result of alterations in the central nervous system rather than as changes in genital structure does not eliminate the need to account for the absence of male behavior in adulthood.

In their rates of contacting, a specifically sexual behavior (interpreted as an invitation to copulate), females and hermaphrodites did not differ, but in this behavior both groups differed from males under all treatment conditions. Mounting was rarely displayed by fernales and hermaphrodites. In the 12 tests without hormone treatment, one hemaphrodite, Monkey 1616, mounted once; when treated with EB, the same animal mounted five times in 12 tests. In the 12 tests when given TP, none of the hermaphrodites mounted. The one hermaphrodite that mounted in this study had received 750 mg of TP prenatally, but two other hermaphrodites that had received the same prenatal treatment failed to mount. Both fernale and male groups had been given more tests than the hermaphrodites over the past decade, although in all other respects they were treated alike. The TP treatment did not result in an increase in mounting by females, although they had as much experience in the test situation as males. Both fernales and hermaphrodites differed significantly from the males; neither group displayed a significant increased mounting rate as a result of TP treatment. This finding is the same as in a previous study when the amount of testing experience of the hermaphrodites was approximately the same as in the comparison group.

When the six hermaphrodites tested in this study were 1, 2, 3, and 4 yr of age, their mean mounting rates per test were .10, .15, .18, and .15, respectively. Those testing conditions were not comparable with the ones reported here, and we mention them only to aid in the interpretation of results. The hermaphrodites at that time were tested with ovaries in situ, and they were tested in mixed-sex groups of four or five peers. Their mean mounting rates were based on all mounts, including those without a foot-clasp. The mounting rate of the hermaphrodites was intermediate between those of males and females of the same age given comparable tests.

When the hermaprodites were between 5 and 7 yr of age, ovariectomized and paired with receptive females, as in the experiments reported here, the mean mounting frequency per test in the absence of hormonal stimulation was .43, and in the presence of TP treatment it was .91. The mounting frequency did not differ significantly from that of control fernales before or after treatment, and it did not increase significantly with TP treatment. Two intervening unpublished studies of the hermaphrodites as adults gave no indication of masculinization of sexual behavior. In the study reported here, none of the hermaphrodites achieved intromission or ejaculated; one hermaphrodite (Monkey 1640) had done so in the 1973 study.

In sharp contrast to the few mounts displayed by the hermaphrodites was the mounting rate of males that had been castrated 11 yr earlier. One male failed to mount when given no hormone treatment but did mount under EB and under TP influence. Two of the nine castrated males failed to ejaculate with TP treatment, but they had ejaculated 10 yr earlier when similarly treated; this difference may have been due to their advanced age in the later study (21 yr or older), but such an explanation is unlikely in the case of the hermaphrodite, Monkey 1640, which was 15 yr old at the tîme of testing. Differences in the ditration of treatment and the total dose of TP are more probable explanations for this particular difference. In the 1973 study, the hermaphrodites were given a total of 1,470 mg of TP over 30 wk, whereas in the present study they received 510 mg over 7 wk; hence the difference in performance may be primarily one of threshold.

In evaluating the effects of prenatal hormones on the patterns of mating behavior displayed in adulthood, we did not overlook the importance of rearing conditions. Goy pointed out that the display of social behaviors in early life is entirely unrelated to copulatory success in young adulthood. Although the patterns of social behavior (especially play) we noted in hermaphroditic monkeys were indeed masculinized in early life (years 1-4), such behavior was not correlated with the copulatory ability at that age, and we now know it was not predictive of the display of male patterns of mounting behavior in adulthood. Evidence for the masculinization of behavior in primates by prenatal treatment with androgens rests largely on the display of malelike social behavior during infancy and the juvenile period of development. Evidence for the masculinization of sexual behavior in adult primates is based on the performance of one animal. The behavior of this single animal should not be dismissed; the intromissions and ejaculations by Monkey 1640 at 6 yr of age have been well documented, but additional adult hermaphrodites reared under optimal conditions need to be studied as adults.

injected with 19-hydroxytestosterone (the hydroxylated metabolite of testosterone), a hormone that is readily converted to estradiol. Blood levels of estradiol increased significantly after treatment and LH levels decreased, but the only behavior that changed signif icantly was the frequency with which males sat close to their female partners. There was no change in mean latency to the first mount. Those males with blood levels of estradiol above the group mean failed to achieve intromission or to ejaculate. On the basis of that study, we would not have predicted the increase in mounting with estradiol treatment that we observed. It bas been reported that the majority of castrated, sexually experienced rats treated daily with 100jug of EB for an extended period show the complete pattern of sexual behavior (Sôdersten, 1973). Our males had been castrated 11 yr earlier and received only 20 Mg of EB a day. Although dose comparisons across species are not necessarily appropriate, comparable dose in terms of body weight would have involved injecting each monkey with no' less than 2,000 jug of EB per day. The entire question requires additional study, but old long-terrn-castrated monkeys are not appropriate subjects for such an investigation. We can conclude that, at least in the dose used, sexual behavior was not suppressed by EB and that EE may have had a facilitating, albeit limited, effect.

Few significant differences in behavior were differentially displayed by partner females toward the three groups of experimental animals; one difference of note was that the greatest PAD, threat-away, and prox rates occurred when they were paired with males. Within each group the greatest PAD rate occurred when the experimental monkeys were untreated. It was under this condition that the experimental animals, especially the males, displayed the lowest level of sexual behavior. This fact may accourit in part for the greater rates of presenting by the partner females during the no-treatment tests. The level of aggression was highest when partner females were paired with hermaphrodites, and in turn the hermaphrodites displayed more aggression toward their partners than did males or experimental fernales. When partner fernales were paired with hermaphrodites, their behavior resembled that displayed in pairings with females rather than males.

Repeated observations of the hermaphrodites implanted with testosterone from adolescence to adulthood and housed in groups with other males and females would be needed to provide conditions (hormonal and enviromnental) that simulate more closely those of normal males in nature.

Although treatment with EB did not produce any significant changes in the behavior of females or hermaphrodites, males displayed a higher percentage of tests with mounts, and their mount latency was shorter with EB treatment than without hormone treatment. The findings are not readily understandable since no other behavioral measures changed, and in a previous study, mounting rate was negatively correlated with estradiol levels in the blood. In that study, castrated rhesus males were injected with 19-hydroxytestosterone (the hydroxylated metabolite of testosterone), a hormone that is readily converted to estradiol. Blood levels of estradiol increased significantly after treatment and LH levels decreased, but the only behavior that changed signif icantly was the frequency with which males sat close to their female partners. There was no change in mean latency to the first mount. Those males with blood levels of estradiol above the group mean failed to achieve intromission or to ejaculate. On the basis of that study, we would not have predicted the increase in mounting with estradiol treatment that we observed. It bas been reported that the majority of castrated, sexually experienced rats treated daily with 100 µg of EB for an extended period show the complete pattern of sexual behavior. Our males had been castrated 11 yr earlier and received only 20 µg of EB a day. Although dose comparisons across species are not necessarily appropriate, comparable dose in terms of body weight would have involved injecting each monkey with no' less than 2,000 µg of EB per day. The entire question requires additional study, but old long-terrn-castrated monkeys are not appropriate subjects for such an investigation. We can conclude that, at least in the dose used, sexual behavior was not suppressed by EB and that EE may have had a facilitating, albeit limited, effect.

Few significant differences in behavior were differentially displayed by partner females toward the three groups of experimental animals; one difference of note was that the greatest PAD, threat-away, and prox rates occurred when they were paired with males. Within each group the greatest PAD rate occurred when the experimental monkeys were untreated. It was under this condition that the experimental animals, especially the males, displayed the lowest level of sexual behavior. This fact may accourit in part for the greater rates of presenting by the partner females during the no-treatment tests. The level of aggression was highest when partner females were paired with hermaphrodites, and in turn the hermaphrodites displayed more aggression toward their partners than did males or experimental fernales. When partner females were paired with hermaphrodites, their be havior resembled that displayed in pairings with females rather than males.


« It is ironic that testosterone "the male sex hormone," is more closely associated with the yawning rate than with the mounting or intromitting rates » Charles Phoenix
 
 
Sexual steroids exert several effects on both central dopaminergic and oxytocinergic systems by acting either at the genomic or membrane level  
yawns-canines
credit photo : "Asif A. Ghazanfar and Aristides Arrenberg"
Max Planck Institute for Biological Cybernetics
Tuebingen; Germany.
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