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.
INTRODUCTION
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.
DISCUSSION
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.
