mise à jour du
20 novembre 2005
Hormones and Behavior
Androgen-induced yawning in rhesus monkey females
is reversed with a nonsteroidal anti-androgen
Franklynn C. Graves, Kim Wallen
Department of Psychology Emoty University, Atlanta, USA
Yerkes National Primate Research Center; Emory University, Atlanta, USA


In the adult rhesus monkey, yawning is an androgen-dependent sexually dimorphic behavior with males yawning more frequently than do females reflecting sex differences in circulating androgens. Studies in a variety of species indicate that yawning is mediated by various neurochemicals including dopamine, serotonin, and oxytocin. In rhesus monkeys, exogenous androgen reliably induces yawning in females to male-like levels. This study investigated whether flutamide, a nonsteroidal anti-androgen, reverses yawning induced by exogenous androgen administration in adult female rhesus monkeys. Six adult female rhesus monkeys were given chronic DHT alone and in combination with daily injections of flutamide and observed for yawning behavior. Treatment with DHT alone significantly increased yawning from 0.3 yawns per 30 min at the pretreatment baseline to 4.7 yawns per 30 min. Concurrent administration of flutamide significantly reduced the rate of yawning to 1.9 yawns per 30 min. These data indicate that flutamide is an effective tool for blocking the central effects of androgens in rhesus monkey females and that androgens regulate yawning similarly in both males and females. 

Across several macaque species, yawning is a sexually dimorphic behavior (Hadidian, 1980; Goy and Resko, 1972; Troisi et al., 1990). Intact adult male rhesus monkeys yawn at significantly higher rates than do adult females (Goy and Resko, 1972). One hypothesis for this sex difference is that males use this behavior as social dominance display (Darwin, 1872), a notion not supported empirically (Deputte. 1994). Yawning does appear to reflect social context as Deputte (1994) noted that male macaques were more likely to yawn in social situations associated with increased psychological tension. A second hypothesis is that this sex difference stems from underlying sex differences in the brain, the hormonal environment, or another biological system.
The sex difference in yawning does not appear until after males are fully post-pubertal, increasing at puberty when testosterone levels are rising (Hadidian, 1980; Troisi et al., 1990). During experiments testing hormonal effects on sexual behavior, it was noted that in fully adult males, castration almost completely eliminates male yawning (Phoenix et al., 1973). The administration of testosterone replacement to castrated males restores yawning rates to those comparable to that seen in intact males (Phoenix et al., 1973). Further, this increase in castrated males occurs in a dose-dependent fashion (Phoenix and Chambers, 1986). Data such as these led Phoenix (1976) to state "yawning is one of the most reliable behavioral indicators of injected testosterone and dihydrotestosterone ... an increase in male sexual behavior is always accompanied by an increase in yawning and vice versa."

Female rhesus monkeys rarely, if ever, yawn. However, administration of exogenous androgens, either testosterone or the nonaromatizable androgen, dihydrotestosterone (DHT), can induce yawning in adult females (Goy and Resko, 1972; Johnson and Phoenix, 1976; Wallen and Goy, 1977). Taken together, these findings suggest that in adult macaques, yawning is a behavior which both males and females are capable of displaying that is strongly regulated by androgens.

More recently, the link between male yawning and androgens has been tested using androgen receptor blockers. Deputte and colleagues (1994) investigated the effects of hydroxyflutamide, the active metabolite of flutamide, on yawning in adult male rhesus monkeys. This study found that hydroxyflutamide injections were as effective as the withdrawal of testosterone in reducing the rates of yawing whether testosterone was given at physiological or supraphysiological levels. Interestingly, under both testosterone conditions, flutamide injections took longer to have an effect than did androgen withdrawal. The present study tested whether the nonsteroidal anti-androgen flutamide was capable of blocking the behavioral effects of exogenous androgen administration in female rhesus monkeys. If the behavioral effects of flutamide in females parallel that seen in males, it would support the notion that yawning is under similar control in both sexes and that the sex difference in yawning reflects differences in circulating androgens and not differences in the organization of male and female brains.

(....) macaque


This study replicates and extends previous work with androgens and yawning in rhesus monkeys. Rates of yawning were very low during the baseline period, consistent with previous data from 20 h of observations in this setting (Graves et al., 2002). DHT, a nonaromatizable androgen, significantly increased rates of yawning in adult females as was seen in Wallen and Goy (1977). Flutamide blocked this effect, reducing the rate of yawning in females treated with both DHT and flutamide concomitantly. Deputte and colleagues (1994) observed a return of yawn rates to baseline levels with hydroxyflutamide in males, unlike the present flutamide treatment in females, which did not return yawn levels completely to baseline. However, in the Deputte study a longer period of anti-androgen was given and yawning rates did not return to baseline until the end of this extended treatment, suggesting that with extended treatment yawning rates may have returned completely to baseline levels. The results of this study extend the work of Deputte and colleagues (1994), indicating that behavioral effects of androgens in females, as in males, are reversible with an androgen receptor blocker.

Flutamide has received wide use as a nonsteroidal antiandrogen for the treatment of hormonally dependent prostatic cancer. However, it has not been clear whether flutamide is as active centrally as it is peripherally (cf. Gray, 1977). The present findings, as well as those of Deputte and colleagues (1994), show that rates of yawning, a centrally mediated behavior, are reduced by flutamide. These data suggest that in both males and females flutamide crosses the blood brain barrier and is capable of exerting influence on central structures through interactions with androgen receptors. Whether central concentrations are as high as those produced peripherally cannot be resolved from our data.

Following castration, adult male rhesus monkeys show a marked decline in yawning as well as sexual behavior (Phoenix et al., 1973). Since flutamide effectively reduces yawning in adult males (Deputte et al., 1994), one would expect to see a similar decline in sexual behavior. Although this has not been investigated in males, there has been one study of the effect of flutamide on female sexual behavior. Administration of flutamide to cycling females in pair tests did not alter their sexual behavior, unlike its effect on yawning in the present study (Johnson and Phoenix, 1978), suggesting that female sexual behavior is not androgen mediated as some have suggested (e.g., Baum et al., 1977). In conclusion, flutamide appears to be an effective tool for blocking the central effects of androgens in rhesus monkey females. Yawning provides a simple behavioral endpoint for assessing central androgenic activity. The similarity of the behavioral effects of flutamide in males and females more strongly supports the hypothesis that yawning is controlled by similar brain mechanisms in both sexes and that the sex difference in yawning reflects differences in circulating androgens and not differences in the organization of male and female brains.


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« 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  
credit photo : "Asif A. Ghazanfar and Aristides Arrenberg"
Max Planck Institute for Biological Cybernetics
Tuebingen; Germany.
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