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1 mai 2010
Hormones and Behavior
1977;8:175-187
Dihydrotestosterone Propionate Effects on Dominance and Sexual Behaviors in Gonadectomized Male and Female Rhesus Monkeys
 
Cochran CA, Perachio AA 
 
Laboratory of Neurophysiology Yerkes Regional Primate Research Center, Emory University, Atlanta, Georgia
 

Chat-logomini

 
One triad of male and two triads of female gonadectomized rhesus monkeys were observed as social groups assembled for repeated hour-long sessions. Social relationships were measured in terms of aggressive behavior between the members of each group in order to determine the dominance hierarchical order. Sexual performance was assessed for each male, before and alter castration, in tests with an estrogen-stimulated ovariectoinized female. Siniilar measures were made when the same female was periodically introduced to the all-male triad. When dihydrotestosterone propionate (DHTP) was administered for a period of 6 weeks to the middle-ranking member of each group, social status changes occurred in two groups, one male and one female, resulting in the elevation of the treated monkeys to the highest rank in the dominance hierarchy. In the other female group, aggressive behavior was increased with DHTP treatment of the middle-ranking female. Somatic effects, particularly again in body weight, occurred in all treated animals. Yawning behavior also increased significantly in those animals receiving DHTP. The latter two effects returned toward pretreatment levels following the cessation of hormone injection; however, changes in dominance hierarchy persisted to the end of the experiment, 6 weeks following the last DHTP treatment.
  
The role of gonadal hormones in the regulation of social behavior has been evaluated in nonhuman primates through measures of aggressive interactions and sexual behavior. Treatment with testosterone can increase aggression and alter dominance status in infant female rhesus monkeys (Joslyn, 1973) and adult female chimpanzees (Birch and Clark, 1946). In social groups of talapoins, castrated males treated with testosterone became more aggressive toward lower ranking male members of a heterosexual group, while not producing any change in social hierarchy (Dixson and Herbert, 1974). Alternatively, it has been reported that testosterone has no marked effect on the aggressive behavior or social standing of adolescent female or male rhesus monkeys (Mirsky, 1955) and adult male or female squirrel monkeys (Green, Whalen, Rutley, and Battie, 1972). With respect to sexual behavior, testosterone propionate (TP) treatment can restore the performance of castrated male rhesus
monkeys to more or less preoperative levels (Phoenix, 1973; Michael and Wilson, 1974). Testosterone treatment of ovariectomized estrogenprimed female rhesus monkeys has elevated sexual behavior (Trimble and Herbert, 1968; Goy and Resko, 1972). Similarly, androstenedione and testosterone have restored sexual receptivity in adrenalectomized, ovariectomized, estrogen-treated female rhesus monkeys (Everitt, Herbert, and Hamer, 1972; Everitt and Herbert, 1975).
 
A metabolite of testosterone, dihydrotestosterone (5a-androstan- 17/3ol-3-one; DHT), has been implicated as a possible factor in the behavioral-endocrine mechanisms underlying sexual behavior in male rhesus monkeys (Phoenix, 1974). When administered to long-term castrated males, DHT, in the propionate form (DHTP), was found to restore sexual performance as effectively as TP. These findings stand in contrast to earlier work with other species which demonstrated that DHT failed to promote or maintain sexual behavior in castrated male rats (McDonald, Beyer, Newton, Brien, Baker, Tan, Sampson, Kitching, Greenhill, and Pritchard, 1970; Whalen and Luttge, 1971) and that it was less effective than TP in initiating sexual behavior in prepuberally castrated rabbits (Beyer and Rivaud, 1973). Since DHT, unlike testosterone, is not aromatized to estrogenic compounds, the influence of this hormone on castrated male rhesus sexual behavior implies an androgen-related mechanism. In females, a similar mechanism may be important for sexual behavior. Although DHT has not been investigated in rhesus females, the androgenic effects of testosterone and its metabolites may account for the restoration of sexual receptivity in adrenalectomized females following treatment with hypothalamic implants of TP (Everitt and Herbert, 1975).
 
If an androgenic hormone effect is a necessary component of sexual and aggressive behavior, a nonaromatizable androgen compound such as DHT would be a useful investigative tool. Given the apparent sensitivity of the species to this hormone and the equivocal results obtained with testosterone treatment in producing changes in dominance and aggression, a set of experiments was designed to investigate the effects of DHT on social dominance in gonadectomized male and female rhesus monkeys as reflected in measures of sexual and agonistic behaviors.
 
DISCUSSION
 
The results of this experiment indicate that DHT can influence social interactions in gonadectomized adult male and female rhesus monkeys, leading to a disruption of the social structure of small groups and producing a long-term alteration in the dominance hierarchy. The present investigation also provides support for previous findings (Phoenix, 1974) that DHTP can restore sexual performance in long-term castrated male rhesus monkeys. In addition to physiological variables, aspects of the experimental design, including group size, gender of members of the group, acuteness of social contact, and size of the observation cage, may have contributed to this set of findings. The DHTP effects on behavior may also have been species-dependent. Peripheral tissue responses during hormone treatment, as reflected by weight gain and reddening of sex skin in the treated monkeys, resembled those reported for nonprimate species; however, the effects of DHT on some behavioral measures in this experiment, e.g., restoration of the castrated male's sexual behavior, differed from those reported for some nonprimates (McDonald et al., 1970; Whalen and Luttge, 1971; Beyer and Rivaud, 1973).
 
Previous investigations failed to detect changes in primate dominance hierarchies with androgen treatment (Mirsky, 1955; Green et al., 1972). In part, this may have been due to the use of testosterone as the treatment hormone. However, other factors distinguish those studies from the present experiment. On one hand, the social rank of the treated animal may mask the social consequences of behavior affected by the hormone. In one study (Green et al., 1972), testosterone was administered only to the two highest ranking members of two groups, each composed of six squirrel monkeys; thus, any possible change in social status was limited. However, in another experiment (Mirsky, 1955), TP was given first to the lowest and then to the second-ranking members of two groups of five rhesus monkeys; no dominance alteration was noted. Alternatively, the social conditions in those tests may have been a crucial variable. In both studies (Mirsky, 1955; Green et al., 1972), the monkeys were housed and tested together throughout the experiment; in the present investigation, the animals were housed individually between test sessions. Acute social contact may exacerbate hormonal effects on behavior. This notion is reinforced by the incidental observation that, in most groups in our experiment, more intense aggression was exhibited in the early portion of each test. Further evidence that duration of social contact is important is
 
DISCUSSION
 
The results of this experiment indicate that DHT can influence social interactions in gonadectomized adult male and female rhesus monkeys, leading to a disruption of the social structure of small groups and producing a long-term alteration in the dominance hierarchy. The present investigation also provides support for previous findings (Phoenix, 1974) that DHTP can restore sexual performance in long-term castrated male rhesus monkeys. In addition to physiological variables, aspects of the experimental design, including group size, gender of members of the group, acuteness of social contact, and size of the observation cage, may have contributed to this set of findings. The DHTP effects on behavior may also have been species-dependent. Peripheral tissue responses during hormone treatment, as reflected by weight gain and reddening of sex skin in the treated monkeys, resembled those reported for nonprimate species; however, the effects of DHT on some behavioral measures in this experiment, e.g., restoration of the castrated male's sexual behavior, differed from those reported for some nonprimates (McDonald et al., 1970; Whalen and Luttge, 1971; Beyer and Rivaud, 1973).
 
Previous investigations failed to detect changes in primate dominance hierarchies with androgen treatment (Mirsky, 1955; Green et al., 1972). In part, this may have been due to the use of testosterone as the treatment hormone. However, other factors distinguish those studies from the present experiment. On one hand, the social rank of the treated animal may mask the social consequences of behavior affected by the hormone. In one study (Green et al., 1972), testosterone was administered only to the two highest ranking members of two groups, each composed of six squirrel monkeys; thus, any possible change in social status was limited. However, in another experiment (Mirsky, 1955), TP was given first to the lowest and then to the second-ranking members of two groups of five rhesus monkeys; no dominance alteration was noted. Alternatively, the social conditions in those tests may have been a crucial variable. In both studies (Mirsky, 1955; Green et al., 1972), the monkeys were housed and tested together throughout the experiment; in the present investigation, the animals were housed individually between test sessions. Acute social contact may exacerbate hormonal effects on behavior. This notion is reinforced by the incidental observation that, in most groups in our experiment, more intense aggression was exhibited in the early portion of each test. Further evidence that duration of social contact is important is the fact that Female Group I, in which a dominance reversal did not take place, had been established for a longer period than had the other groups. The amount of time the animals spent together seems to have affected the stability of the group.
 
Not all effects observed can be readily ascribed to a physiological mechanism affected by the hormone treatments. The increases in limb shaking displays may have been a type of indirect effect of DHTP treatment. This behavior, also referred to as cage or branch shaking, is typical of dominant rhesus monkeys and is rarely seen in a subordinate animal (Altmann, 1962). During DHTP treatment, limb shaking behavior was displayed more often by the dominant animals in all groups. Since this included the untreated dominant female in the group that did not alter its dominance hierarchy, the change in behavior was not related to a physiological effect of DHTP.
 
In contrast, yawning displays, typical of adult male rhesus monkeys in stressful situations, appeared to be more directly related to the hormone treatment. It has previously been found that TP increases the frequency of yawning in adult rhesus females in a social group context (Goy and Resko, 1972; Phoenix, 1973). Similarly, an increase in yawning was observed with DHTP treatment of castrated male rhesus monkeys (Phoenix, 1974). Yawning in the DHTP-treated animals occurred independently of changes in their dominance rank; however, it seemed to be related to social variables, since the frequency of this behavior was noticeably increased when the treated animals joined their respective groups for test sessions. Somatic changes were another example of physiological effects of DHT that were apparently unrelated to behavioral variables. A gain in weight was measured in all the treated subjects, including the female (NP 42) whose dominance standing was unaltered.
 
Although the results reaffirm earlier findings that DHT can effectively restore sexual behavior in castrated male rhesus monkeys (Phoenix, 1974), we are unable to state whether this hormone affects female receptivity, since pair tests were not used with the female groups. Sexual behavior in the triads was confounded with variables related to the social relationship between group members. In any event, the lack of noticeable alteration in female rhesus sexual behavior following administration of DHT is consistent with similar findings in female rats and rabbits (Beyer, McDonald, and VidaI, 1970; Beyer, Morali, and Cruz, 1971).
 
The importance of DHT per se for the regulation of sexual or aggressive behavior in rhesus monkeys remains in question. For example, no direct relationship has been found between plasma levels of DHT (or testosterone) and male rhesus monkey sexual behavior (Robinson, Scheffler, Eisele, and Goy, 1975). However, given the qualifications just discussed, our data indicate that an androgen-related mechanism is relevant to the endocrine basis of social aggression in both male and female rhesus monkeys. This conclusion must be further tempered by the caution that should attend the interpretation of the behavioral effects produced by pharmacological hormone dosages administered as replacement treatment in gonadectomized animals. At present, we propose that further investigation of the hormonal relationships to behavior should consider androgenic compounds, including DHT, as mediators of aggressive behavior, which, in unstable social groups, can promote alterations in group social structure.
 
« 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