mystery of yawning
Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal

mise à jour du
27 mars 2011
Brain Research

Heterosexual, autosexual and social behavior of adult male rhesus monkeys with medial preoptic-anterior hypothalamic lesions

Slimp JC, Hart BL,Goy RW.

Wisconsin Regional Primate Research Center, University of Wisconsin, Madison, Wise


Bilateral radiofrequency lesions were made in the medial preoptic-anterior hypothalamic (MP-AH) area of 6 adult male rhesus monkeys; 5 sham-lesioned subjects served as controls. Behavioral analysis consisted of observations on copulatory behavior, yawning, masturbation and some aspects of social behavior. MP-AH lesions reduced or completely eliminated the display of manual contacts of the partner, mounts, intromissions and ejaculations without interfering with masturbation. Yawning, a sexually dimorphic behavior, was not affected either. Measures of several social behaviors indicated no evidence of social withdrawal or other aberrance of social interactions, which might have led to the decline in heterosexual behavior. The results with regard to copulatory behavior were consistent with the effects of MP-AH lesions in rats, cats and dogs.
In rhesus monkeys it appears as though the MP-AH region is specifically involved in the mediation of heterosexual copulation and is not vital to the performance of other forms of male sexual activity such as masturbation. Also the MP-AH is not critical for the display of all sexually dimorphic behaviors. The types of behavioral changes in MP-AH lesioned subjects differed to some extent from those following castration, indicating that the effects of the lesions cannot be explained as basically that of functional castration.
Several neuroanatomical loci have been shown to be involved in the display of male sexual behavior. However, the single most critical region for the display of male sexual behavior appears to be the medial preoptic-anterior hypothalamic (MP-AH) continuum. This assumption is based upon several experimental approaches in rats and an extension of some of the basic findings in rodents to carnivores. Electrical stimulation of this brain area has been found to moderately facilitate mating activity in male rats in general and to dramatically increase mating activity in a few individuals. Stimulation of other forebrain areas, especially along the path of the medial forebrain bundle, has facilitated sexual activity in some instances, but there is no report of the dramatic increase as reported by MP-AH stimulation. In several non-primates, lesions of the MP-AH area have been shown to eliminate completely or markedly reduce male copulatory behavior. This is true of the rat, cat and dog. Typically the most severely affected males showed little mounting behavior and no intromissions or ejaculations.
Work on the neural correlates of' sexual behavior of primates is quite limited and none of the studies have specifically investigated the effects of bilateral MP-AH lesions on sexual behavior. Lesion studies on non-human primates have been limited to an examination of the effect of removal of the temporal lobes and amygdala where such lesions have been found to increase sexual activity. In restrained monkeys, electrical stimulation of several regions of the brain has revealed that the MP-AH locus is one of the most effective sites for evoking penile erection or ejaculation.
In freely moving rhesus monkeys mounting of ovariectomized (non-estrogen treated) females accompanied by intromissions and thrusting could be induced by electrical stimulation of a few sites in the dorsolateral preoptic area, dorsal portion of the lateral hypothalamus and ventral portion of the dorsomedial nucleus of the hypothalamus. Stimulation of the rostral putamen evoked penile erection in the restrained monkey, but in the freely moving monkey mounting, intromissions and thrusting were evoked by electrical stimulation only in the presence of an estrogenprimed female.
Interestingly, stimulation of the medial preoptic and some hypothalamic areas including dorsal, lateral and posterior regions, produced penile erection in the restrained monkey, but did not induce mounting in the freely moving animal.
Of the work in primates some clinical studies on human male patients relates most closely to the non-primate studies on the effects of MP-AH lesions. In a series of patients convicted of sexual offenses including pedophilic homosexuality and violent hypersexuality unilateral lesions were placed in areas extending from the ventromedial nucleus of the hypothalamus rostrally to the medial preoptic area. Patients receiving these lesions were reported to have experienced a lessening of the tendency towards abnormal behavior as well as a reduction in sexual interest. In earlier work on human patients. Meyers performed bilateral lesions of the ansa lenticularis to relieve abnormal motor signs but found that his patients suffered complete loss of sexual interest and even inability to achieve erection. The procedure used by Meyers was believed by him to have possibly damaged the anterior hypothalamus and medial forebrain bundle which carries nerve fibers to and from the MP-AH area.
The involvement of the MP-AH region in the display of male sexual behavior in a variety of mammalian species is well established. However, little attention has been given to its involvement in various types of sociosexual behavior other than heterosexual copulation. For example, lesions of the amygdala, which reportedly increase sexual activity in monkeys, also lead to disturbances of social behavior involving withdrawal from social interactions, alteration in dominance relationships, and increased social fear. Thus, MP-AH lesions could have an effect on social interactions which in turn could be altering sexual behavior.
In dogs, MP-AH lesions that alter male sexual behavior do not affect dominance relationships but do markedly reduce sexually dimorphic urine marking behavior. Thus one might propose that the MP-AH region is involved in the mediation of sexually dimorphic behaviors other than sexual responses.
Another consideration is that previous studies dealing with MP-AH lesions have yielded little information regarding the question of the effects on the animal's capability to achieve erection and ejaculation in a context other than copulation with a female partner. Although in dogs MP-AH lesions did not block erection and ejaculation, as elicited manually by the experimenter, study of a species in which masturbation typically occurs would provide a direct answer to this question.
The rhesus monkey is an ideal animal in which to pursue these considerations. There is a great deal of descriptive and analytical data available dealing with sexual behavior. The copulatory pattern of the adult rhesus male includes several elements such as manual contact (placing two hands on the hips of the partner), mount with or without pelvic thrusting, erection, intromission and ejaculation, which can be scored independently. In addition to various aspects of copulatory behavior, yawning is a sexually dimorphic behavior which frequently occurs in mating tests. Finally, since masturbation is a normal part of a rhesus monkey's behavioral repertoire both in the laboratory and in the natural environment, possible changes in this behavior can be observed along with an analysis of changes in heterosexual copulation.
The approach of the present study was to examine the role of the MP-AH area in sociosexual behavior through the observation of lesion effects on several behavioral categories. Heretofore, analysis of MP-AH lesions in male animals has been restricted mostly to heterosexual copulatory behavior.
Sexual behavior
It could be proposed that copulatory behavior and masturbation are different behavioral expressions of male sexuality. The results of the present study indicate that lesions of the MP-AH region do not affect both of these behavioral measures equally. Even though heterosexual copulation was reduced or eliminated, masturbation was apparently undisturbed, since the occurrence of seminal material in the home cage drop pans and the frequency of video-taped masturbation by lesioned males were equal to that of sham-lesioned males. The difference in the effects of MP-AH lesions on masturbation and heterosexual copulation suggests that the MP-AH area is specifically involved with sexual behavior directed towards a partner and is not a neural locus for all forms of sexual behavior.
Recovery of function with regard to copulatory performance in lesioned subjects was observed during the second through fifth months in 4 of the 6 males, varying from 100% in one male to 5 of all tests in another. The level of recovery of ejaculatory ability appeared to stabilize by the end of the sixth month and no more recovery apparent at 16 months, suggesting that the degree of remaining deficit was permanent .
These observations on impairment of copulatory behavior by MP-AH lesions are consistent with those from rats. cats and dogs. In all species studied some animals have shown partial or complete recovery of copulatory behavior and others have undergone permanent elimination of copulawry ability.
An analysis of the effects of the MP-AH lesions on heterosexual behavior revealed that components of sexual behavior such as intromission and ejaculation. which occur after contact and mounting, were more reduced than the earlier components. Normally, the number of tests with ejaculation are less than the number of tests with intromission, and those with intromission less than those with mounts or contacts. As shown in Fig. 2, this trend was greatly enhanced by MP-AH lesion. The lesioned males also failed to engage in a second copulatory series when they did ejaculate. These data illustrate that often a copulatory series was begun but not carried through. Whenever ejaculation did occur postoperatively in lesioned subjects with an impairment in sexual behavior, there were significantly more contacts, mounts and intromissions prior to ejaculation and a longer intromission and ejaculatory latency than in sham-lesioned subjects, suggesting that more sexual stimulation was required for lesioned males to attain ejaculation. This effect is in agreement with a recent report") that, in male rats. MP-AH lesions interfere with the copulatory mechanism as well as the mechanism for initiating sexual behavior.
Although the copulatory responses of mounting, intromission and ejaculation were altered by MP-AH lesions, yawning during mating, which is also a sexually dimorphic behavior, was not affected. Thus it is evident that the lesion did not reduce or impair sexually dimorphic behavior in general.
Comparison with effects of castration
Serum levels of testosterone in MP-Al-l-lesioned males were monitored at periodic intervals by radioimmunoassay. The levels of testosterone in MP-AH- lesioned males were found to be comparable to sham-lesioned males (unpublished observations). Thus the changes in sexual activity cannot be explained by interference with the gonadotropin control of testosterone secretion. It is possible that the lesions did destroy androgen sensitive neurons in the basal forebrain, resulting in a type of functional castration. Therefore, a comparison with the effects of castration is of interest.
Castration in the rhesus results in a variable but gradual decline in intromissive and ejaculatory performance. Some animals, though continuing to mount, are apparently incapable of intromission or ejaculation. Yawning during mating tests also declines, as well as does the occurrence of ejaculatory plugs in the home cage. Direct observation of masturbation frequency has not been made in the studies involving castration, and the disappearance of seminal material from the drop pans could reflect just the cessation of secretion of seminal material from accessory sexual organs.
In contrast to castration, MP-AH lesions greatly reduced mounting and eliminated or reduced intromission and ejaculation as soon as subjects were tested postoperatively. Importantly, yawning was not affected by MP-AH lesions. One would not expect to see masturbation continue in castrated animals as it did in lesioned subjects, but there are no direct observations to support this. The behavioral effects of MP-AH lesions are therefore not what one would expect from a type of functional castration resulting either from interference with gonadal androgen secretion or from removing some androgen target tissue in the basal forebrain.
Social behavior
in lesioned animals there were no increases in the frequency of threat display or aggression and grooming actually increased. Low frequencies of aggression and the presence of grooming behavior are considered characteristics of stable social interactions. The continuing interaction with partners by the lesioned males indicates that sexual deficits were not secondary to some gross social maladjustment. The subjects continued to lever press for access to females, which presumably indicated a predisposition for social interactions with another animal. Analysis of lever pressing tests revealed no preference for the EB-treated females by either sham or lesioned males. The continuation of positive social interactions in the subjects of the present study contrasts with the signs of general social withdrawal in rhesus monkeys following amygdaloid lesions.
The present study was not specifically designed to test the effects of MP-AH lesions on female sexual reponses, but some interesting observations were recoided. Presenting, which is a part of the male rhesus monkey's behavioral repertoire", is normally displayed to other males; presenting is rarely displayed to females. The subjects of this study were not paired with other males, and the occurrence of presenting therefore depended upon the degree to which this behavior was displayed to females, especially when the female partner contacted or attempted to mount the male. In contrast to sham-lesioned subjects, 5 lesioned males (all except the one with complete recovery of copulatory behavior) showed an increase in the number of contacts by the female and the number of presentations when contacted. The presenting by the lesioned males and subsequent mounting by female partners could have been due to an increased tendency of the males to assume a feminine role. However, it is possible that these female partners were using contact and mounting behavior as a type of sexual solicitation for these relatively sexually inactive males.
Analysis of lesions and recovery of function
The most effective anterior-posterior locus for the impairment of heterosexual behavior is best described as the junction of the medial preoptic and anterior hypothalamic area at the posterior edge of the anterior commissure (Fig. 5). In the dorsoventral plane, lesions located anywhere between the optic chiasm and the anterior commissure had pet manent behavioral effects.
This lesion site is in the same atea which has resulted in marked reduction or elimination of copulatory behavior in rats, cats and dogs. In fact, the same interior brain landmarks (posterior edge of the antetior commissure, the region between the anterior commissure and optic chiasm and the medial tissue along the walls of the third ventricle), as revealed by X-ray ventriculography, were found to be the most effective lesion sites for eliminating copulatory behavior in cats and dogs. As in the previous work on rats, cats and dogs, large MP-AH lesions were the only ones resulting in elimination of copulatory responses.
The variability in lesion effects could be related to differences in vertical placement of the lesions, rather than minor differences in anterior-posterior or lateral placement, or to the volume of the lesioned area. The three most effective lesions were the three largest, and in the male with no long-term behavioral deficits it was the smallest. While the variability in lesion effects could be explained on an anatomical basis, another possible explanation is that individual differences in preoperative copulatory performance may have determined postoperative performance. The male with the best preoperative copulatory performance, in terms of numbers of ejaculations and the shortest latency to ejaculation, was the male showing the least deficit following MP-AH lesion. The two males with the longest latency to ejaculation and the fewest number of ejaculations preoperatively were the two males with no postoperative ejaculations. Hence, there was a tendency for the degree of preoperative copulatory performance to be related to the effectiveness of the lesion.
In the present study animals were tested 16 months after surgery, but recovery of function only occurred between the second and fifth months. The absence of any further recovery beyond the sixth postoperative month indicates that the MP-AH lesion effect on sexual behavior is permanent once initial recovery occurs. This lack of recovery is also evident in recent work on male rats where the effects of MP-AH lesions are evident within about one month after lesioning with no further recovery apparent for as long as 8 months after surgery.