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mise à jour du 16 janvier 2003
Biology of reproduction 1986;35:918-926
Threshold for Behavioral Response to Testosterone in Old Castrated Male Rhesus Macaques
Charles H Phoenix, Kathleen C
ChambersDivision of Reproductive Biology and Bebavior Oregon Regional.Primate Research Center Beaverton, Oregon 97006


Introduction : The level of sexual behavior displayed by rhesus macaque males declines significantly with old age (Phoenix, 1977; Phoenix and Chambers, 1982a; Robinson et al., 1975), but serum testosterone (T) levels, bound and free, do not decline (Chambers et al., 1981). Nor do serum levels of dihydrotestosterone (DHT) or luteinizing hormone (LH) decline, and diurnal patterns of these hormones do not differ in young and old rhesus males (Chambers and Phoenix, 1981; Chambers et al., 1982). if levels of sexual behavior decline but T levels do not, T must be less effective in activating sexual behavior in aging males. Eventually, the level of sexual behavior displayed by old males should not differ from that shown by old, castrated males as T becomes increasingly ineffective in supporting high levels of sexual activity.

Fully adult (about 10-yr-old), sexually vigorous rhesus males show a rapid depletion of serum T levels after castration (Resko and Phoenix, 1972) and a much slower but significant decline in sexual behavior (Michael, 1972; Wilson et al., 1972; Phoenix, 1973b). One can restore sexual behavior to mean precastration levels in at least 90% of such males by treating them with testosterone propionate (TP; Phoenix et al., 1973). However, TP does not increase the levels of sexual behavior displayed by older intact males (about 15-yr-old) whose sexual behavior has declined (Phoenix, 1977), and TP (10 mg/day) increases the sexual behavior displayed by old castrated males (18-22 years) only to the level displayed by intact males of the same age (Chambers and Phoenix, 1983). Increasing the daily dose of TP from 10 to 50 mg does not produce a further increase in sexual performance.

Not all males show the same rate or extent of loss of sexual behavior in old age any more than all young adult males show the same rate or extent of decline in sexual behavior after castration (Resko and Phoenix, 1972; Phoenix, 1973b; Phoenix et al., 1973). Baseline levels of sexual behavior displayed after castration vary widely among individuals, and serum T levels required to reinstitute the full pattern of sexual behavior may also be expected to vary widely (Michael and Wilson, 1974). in this study, we proposed to determine threshold amounts of TP that would increase individual components of sexual behavior in old, castrated males to levels displayed by equally old, intact males. We compared levels of serum T and DHT in intact and castrated males before and after each series of behavioral tests that corresponded to each graded dose level of TP, and related behavioral changes to changes in serum hormone levels. [...]

Discussion : Testosterone failed to induce mounting in two castrated males, and three of the castrated monkeys (50%) did not achieve intromission or ejaculation in 21 weeks of TP treatment. In behavioral tests 14 years earlier, the males had responded to T by displaying the complete copulatory pattern; but 3 years ago, only two of the three males ejaculated when injected with TP (10 mg/day), and one male displayed only mounting behavior. This male did not mount in the pair test reported here but did masturbate to ejaculation during two tests. Ejaculatory plugs were frequently observed in the drop pans below the home cage of this and the other males; however, systematic records of ejaculatory plugs were not kept during this study (but see Phoenix and Jensen, 1973). Under very different circumstances, adult rhesus males that sustained lesions to the medial preoptic-anterior hypothalamic area no longer copulated with females but continued to masturbate to ejaculation (Slimp et aL, 1978). The behavioral deficits could not be attributed to a T deficiency. Long-term castration and old age (or old age alone) could lead to changes in comparable areas of the central nervous system with similar behavioral consequences. Whatever the explanation for the loss of responsiveness to T, the absence of copulatory behavior by these males was not a function of low serum levels of T. During the last series of tests, the mean serum T level for castrated males that did not intromit was 23.9 ng/ml; for those that did, the mean was 24.5 ng/mI. The mean T level for intact males in this test series was 4.2 ng/ml. In previous studies the mean levels of serum T at 0900 h in old males were 3.9 and 6.2 ng/ml, and at 2 100 h the means were 11.71 and 16.9 ng/ml (Chambers and Phoenix, 1981; Chambers et al., 1982). We have also shown that sexual performance levels are no higher when males are tested at 2 100 h when T levels are high than when tested at 0900 h when levels are low (Chambers et al., 1982). The fallure to mount and intromit in the present study likewise cannot be ascribed to a deficiency in serum DHT levels.

In contrast to the three castrated monkeys whose performance we just described, the other three males mounted and achieved intromission without T treatment. Their relatively high levels of performance account for the absence of statistically significant differences between castrated and intact males for these behaviors during the the first test series. After 1 week of treatment with TP (0.004 mg/kg, or about 0.036 mg/male), one of the castrated monkeys ejaculated; after 2 weeks of treatment, a second male ejaculated. Their mean serum T level at the end of the series was 0.39 ng/ml. The third castrated male to ejaculate did so after the first week of treatment with 0.016 mg of TP/kg (or about 0.14 mg/male). His serum T level at the end of the series was 1.91 ng/ml. Michael et al. (1984) reported an increase in ejaculation in recently castrated adult rhesus males each given 0.05-0.10 mg of TP and whose plasma T levels were between 1.20 and 2.05 ng/ml. In spite of the many differences in procedures and behavioral measures, the threshold values for ejaculation that we found in old long-term-castrated monkeys were very similar. However, supraphysiologic levels of T did not increase performance rates in responding males and did not induce nonresponders to mourit, intromit, and ejaculate.

Ejaculation was the only component of sexual behavior to differentiate untreated, castrated males from intact males. The percentage of tests with ejaculations and the proportion of males that ejaculated differed during the first test series when vehicle alone was injected. Treatment of the castrated males with 0.004 mg of TP/kg during the second series of behavioral tests eliminated all statistically significant group differences in sexual performance. During the fifth series of tests, however, there was a statistically significant difference between the groups in the proportion of males that ejaculated. In that series, two of the six castrated males ejaculated, the saine proportion that ejaculated in the second and sixth series of tests. But in the fifth series, all five of the intact males ejaculated, and so there was a statistically significant difference in proportion.

Yawning behavior is sexually dimorphic and T-dependent (Phoenix et al., 1967; Phoenix and Chambers, 1982c), but its role in the total pattern of mating behavior is a matter of conjecture. The proportion of intact males that yawned during series 1 and 2 was greater than that of castrated males, and the rate of yawning was also higher in intact males during Series 1 and 3. Not until mean serum levels of T reached 5.66 ng/ml during the fourth series of tests were all differences in yawning between the groups eliminated.

There were no differences in any measure of sexual behavior across the six treatment conditions for the intact males (p>0.05); but among the castrated males, contact, mount, and yawn rates differed significantly overall. When they received 0.064 mg/kg of TP, they contacted females at a higher rate than when they received 0.004 and 0.016 mg of TP/kg, but the rate was no greater than that shown when they were not treated. Nor did the contact rate differ from the rate in tests involving higher doses of T. It is difficult to attach much meaning to this difference or to that found in mounting rate across treatments since the Newman-Keuls test did not identify significar- differences in mounting rate between any specific test series despite a significant F value.

However, the yawning rate was significantly higher in series 5 and 6 than in series 1-4. The same was true for differences in serum T levels among castrated males. The orderly increase in yawning rate with increases in serum T levels suggests a causal relationship between the two. It is ironic that T, "the male sex hormone," is more closely associated with the yawning rate than with the mounting or intromitting rates.

The importance of female partners to the outcome of pair tests of sexual behavior in nonhuman primates is well known (Herbert, 1968; Phoenix, 1973a; Goy, 1979; Michael et al., 1984), and the partner is especially important in tests involving old males. We have shown that the performance levels of old males paired with females chosen at random was significantly lower than that of young and middle-aged males tested with the same females; but, when old males were paired with selected preferred females, their performance level equalled that of young males (Chambers and Phoenix, 1984). In the study reported here, the percentage of tests in which intact males ejaculated increased significantly when these males were tested with our most highly receptive and proceptive females. The increase for castrated males, however, was not significant. The three males that did not intromit or ejaculate in earlier tests did not do so with the highly proceptive females.

We considered the possibility that a dichotomy existed in the population of old, castrated males. There were old, castrated males whose sexual behavior, especially ejaculation, increased with T treatment and old males whose level of sexual behavior could not be enhanced by T. This dichotomy is in fact what we found in the sample of animals from this study. A more parsimonious explanation of our findings, however, is that with age all males eventually become unresponsive to T. The process is gradual, and signs of decline are evident in the reduced levels of sexual behavior observed in intact males whose serum levels of T have not declined. Some old, intact males stop intromitting and ejaculating altogether. Eventually, the level of sexual behavior of very old, intact males should not differ from that of old, castrated males. The hypothesis is testable, but not easily so, because most males die before reaching that age.

« 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
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