Scent Marking, Sexual Behavior and Aggression in Male Gerbils: Comparative Analysis of Endocrine Control1
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AMER. ZOOL., 21:143-151 (1981)
Scent Marking, Sexual Behavior and Aggression in Male Gerbils:
Comparative Analysis of Endocrine Control1
PAULINE YAHR
^ Department of Psychobiology, University of California,
• Irvine, California 92717
SYNOPSIS. The aggressive, sexual, and scent marking behaviors of male gerbils (Meriones
unguiculatus) are sensitive to gonadal androgens, but androgens are not equally important
in the control of each behavior. In this species, territorial residency, prior aggressive
experience, and unidentified factors that contribute to large individual differences in
aggressiveness, influence the aggressive behavior of males at least as much as androgens
do. To the extent that androgens affect aggression between male gerbils, they act partially
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by altering aggressiveness and partially by altering production of aggression-eliciting cues.
The nature of these cues is unknown. Understanding the role of androgens in aggression
in this species is further complicated by the observation that castration can either increase
or decrease aggression depending on the age at which the surgery is performed. In
contrast, androgens play a primary role in the control of sexual behavior and scent mark-
ing. Both behaviors consistently decline following castration despite prior experience of
the males. Both behaviors are also controlled by the medial preoptic area-anterior hy-
pothalamus, an area of the brain often implicated in the control of male sociosexual
behaviors. It appears, though, that the sites, and possibly the mechanisms, of hormone
action underlying scent marking and sexual behavior differ. Studying both behaviors in
the same species, and whenever possible in the same individuals, is proving to be a useful
technique for identifying such differences between behaviors as their sensitivity to steroids
and to brain lesions.
INTRODUCTION marking behaviors by which males actively
Androgens secreted by the testes influ- distribute olfactory signals about their en-
ence many of the sociosexual behaviors of vironment (Thiessen and Rice, 1976). Ur-
males during development and/or adult- ine spraying by male cats (Felis domesticus)
hood. Androgens stimulate male copula- and the frequent leg-lift urination behav-
tory behavior in every vertebrate species ior of male dogs (Canis familiaris) are fa-
studied to date and androgen-dependent miliar examples of scent marking.
changes in aggressiveness are common- Male gerbils (Meriones unguiculatus)
place. Androgens also influence the com- scent mark by rubbing their bellies on ob-
munication patterns of males. The songs jects that protrude from the substrate.
of male birds (e.g., zebra finches, Poephila This marking response deposits odorous
guttata, and canaries, Serinus canarius) secretions from the male's ventral seba-
and the postural displays of male lizards ceous gland. Both the secretory activity of
(Anolis carolinensis) are examples of audi- the gland and the marking behavior are
tory and visual displays controlled by an- controlled by testicular androgens (Thies-
drogens (see reviews by Arnold, 1981; sen et al., 1968). After castration, the or-
Crews and Greenberg, 1981). In mam- angey secretion of the gland disappears
mals, androgens often affect olfactory and scent marking greatly decreases or
communication. Odors used as social sig- ceases entirely. Both scent gland activity
nals, such as the urinary pheromones of and marking behavior resume when cas-
male mice (Mus musculus), can vary with a trated males are given testosterone. In this
male's hormonal status (Bronson, 1971). review, I summarize progress my research
Androgens also influence specialized scent- group has made in relating the hormonal
basis of gerbil scent marking to the hor-
monal basis of two more traditionally-stud-
ied, androgen-sensitive behaviors, sexual
1
From the Symposium on SocialSignals—Comparativebehavior and aggression, that may be func-
and Endocrine Aspects presented at the Annual Meet- tionally related to scent marking in this
ing of the American Society of Zoologists, 27-30 De-
cember 1979, at Tampa, Florida. species.
143144 PAULINE YAHR
The long-term goal of our research is to in aggression vary with the context in
understand how androgens act on the which aggression occurs, the previous ag-
brain to control and coordinate androgen- gressive experience of the male, and the
dependent behaviors of males. Because we age at which castration is performed. In-
are interested in identifying general prin- dividual differences in aggressiveness are
ciples of androgen action, and in recogniz- large. #
ing their limitations, a comparative ap- Male gerbils are more aggressive toward
proach is essential. The comparative unfamiliar males intruding into their ter-
approach we selected is not the traditional ritories than they are toward unfamiliar
one. Rather than compare androgen con- males that they encounter in neutral areas
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trol of a single behavior across species or (Wechkin and Cramer, 1971). Our data in-
strains, we set out to compare androgen dicate that castration does not appreciably
control of scent marking, sexual behavior, reduce the aggressiveness of resident
and aggression within a species. Our strat- males toward intruders unless their inter-
egy was to develop a model system in actions are prolonged (Yahr et al., 1977).
which several androgen-sensitive behav- When males met in a series of brief (15-
iors could be studied simultaneously with- min) tests, castrated residents and gonad-
in individual males. This comparative ap- ally intact residents were equally likely to
proach would afford the advantage that attack intruders. No differences in attack
any differences observed between behav- latency, fight duration, or chasing were ap-
iors could not be attributed to differences parent. We obtained similar results when
in genotype, developmental history, or males remained together continuously for
amount of circulating hormone. several hours, either in a neutral arena or
Our strategic goal has been partially in one of the male's living space. However,
met. Comparisons of the scent-marking if males remained together for an entire
and sexual behaviors of male gerbils are day, the decreased aggressiveness of cas-
proving fruitful. In contrast, as discussed trates showed up clearly. When fighting in
below, androgens are much less important a neutral arena, 4 of 9 intact males killed
in determining the aggressive behavior of their intact male opponents within 24 hr.
this species. Hence gerbil aggression is a In the same setting, castrates never killed
less suitable model system for analyzing their opponents, whether the opponent
the neural actions of androgens. was an intact or a castrated male. When
fighting in their own territories, 6 of 8 in-
ANDROGENS AND AGGRESSION tact males killed intruders (these 6 males
When we began our research, little was killed 10 of the 18 intruders they faced),
known about hormonal influences on the whereas only 1 of 8 castrated residents
aggressive behavior of male gerbils. None- killed intruders. These data suggest that
theless, the data that were available were androgens stimulate male gerbils to per-
intriguing because of the contradictory re- severe in their attacks but do not shorten
sults obtained in different laboratories. the latency to initiate a fight.
Some researchers reported that castration The decrease in aggressiveness follow-
decreased aggressiveness in male gerbils ing castration was attenuated in males with
(Sayler, 1970; Lumia et al., 1975), as it does prior aggressive experience. When we
in many other species. Others obtained treated castrated male residents with tes-
just the opposite result, i.e., castration in- tosterone propionate, they became more
creased aggression (Anisko et al., 1973; aggressive toward intruding males. For ex-
Christenson etal., 1973). Our data provide ample, some castrates that had not killed
support for both of these disparate results. intruders previously did so after receiving
The behavioral changes that occur after testosterone injections. In contrast, castra-
castration result partially from changes in tion did not decrease the aggressiveness of
aggressiveness and partially from changes male residents that gained aggressive ex-
in production of aggression-inducing cues. perience while gonadally intact. In partic-
The magnitude and direction of changes ular, resident males that killed intrudersSCENT MARKING, MATING AND AGGRESSION 145
prior to castration continued to do so after only subjects to reach a criterion of attack-
castration. ing within 60 sec on 5 of 6 consecutive
Gonadal androgens also influence tests. In contrast, postpuberally castrated
aggression in this species by promoting males formed the least aggressive group.
reduction of aggression-inducing cues, It is not clear why castration produced dif-
8 \., intact males elicit more aggression
than castrates do (Yahr et al., 1977). When
ferent effects on aggression when per-
formed before versus after puberty, but
we left intact males and castrates together the differences do not necessarily reflect
for a day in a neutral arena, only 1 of 11 changes in the neuroendocrine mecha-
intact males killed his castrated opponent. nisms underlying aggression. They could
As discussed above, deaths occurred in just as easily reflect differences in the way
nearly half of the cases when intact males intact male intruders behave toward dif-
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were paired. Thus intact males are less ferent types of residents. For example, in-
persistent when attacking castrates. Simi- truders may provoke attacks from females
larly, resident males were twice as likely to and prepuberal castrates by attempting to
attack and chase intact male intruders as mount them. Prepuberal castration may be
castrated intruders. This was true regard- more effective than postpuberal castration
less of the resident's gonadal status, indi- for eliminating secondary sex characteris-
cating that both castrated and intact male tics {e.g., odors) that distinguish males
residents are sensitive to the aggression-in- from females.
ducing cues that intact intruders produce. While the level of aggression male ger-
However, the importance of these aggres- bils display in a territorial context is influ-
sion-inducing cues also decreases as males enced to varying degrees by the males'
become more experienced fighters. When hormonal condition, the outcome of inter-
we exposed aggressively experienced male actions in this setting depends primarily on
residents (either castrated or intact) to in- territorial (residential) status (Yahr et al.,
tact, castrated, or scent-glandectomized in- 1977). We found that during brief en-
truders for a day, the residents attacked counters resident males were twice as likely
and chased the different types of intruders to dominate intruders as the reverse, and
indiscriminately. Intruders from each cat- this disparity increased when the interac-
egory were equally likely to be killed. tions were prolonged. Intruders, for ex-
The influence of castration on gerbil ample, never killed a resident male. The
aggression is modified not only by aggres- advantage to fighting in their own territory
sive experience, but also by the age at occurred independent of either the resi-
which castration is performed. Castration dent's or the intruder's hormonal state.
can actually increase the aggressiveness of Similar results have recently been re-
male gerbils if they are castrated prior to ported for rats (Rattus norvegicus; Christie
puberty (Yahr and Coquelin, 1980). In this and Barfield, 1979).
study, male or female residents encoun- As noted above, we originally hoped to
tered intact male intruders twice daily for study three androgen-sensitive social be-
up to 2 wk. All female residents were go- haviors, social signalling (scent marking),
nadally intact. The male residents either sexual behavior, and aggression, simulta-
remained intact, were castrated before pu- neously in male gerbils. Yet as our data
berty, or were castrated as adults. Each test indicate, several other factors, including
ended after 5 min, or earlier if a fight be- territorial residency, prior aggressive ex-
gan. Fights were infrequent under these perience, and age at castration, limit the
conditions, but group differences ap- role of androgens in the control of aggres-
peared among residents that initiated sion in this species. It seems, therefore,
fights against 2 or more intruders. The that straightforward analyses of androgen
most aggressive such fighters were females control of aggression between male gerbils
and prepuberally castrated males. They are not feasible until a test situation is de-
attacked more quickly and more often veloped in which hormonal variables make
than intact male residents and were the a larger contribution to aggression than146 PAULINE YAHR
• Shorn-operated control* often as paired or isolated males (Hull et
al, 1973; Yahr et al, 1980). The marking
frequencies of isolated males were related
to their sexual activity. Isolated males that
mounted scent marked 2-5 times as much
as sexually-inactive isolates. •
Scent marking and sexual behavior show
a similar dependence on testicular andro-
gens (Yahr et al., 1979). Like scent mark-
ing, sexual behavior gradually declines af-
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Weekly Tests After Surgery
ter castration, as illustrated in Figure 1.
FIG. 1. Changes in ejaculatory behavior of male ger- Ejaculation disappeared first, followed by
bils after castration and during treatment with tes-
tosterone propionate (TP). TP was injected twice a intromission and mounting. This pattern
week in the doses specified in the figure. Figure taken of decline resembles that seen in other
from Yahr et al. (1979). species (Grunt and Young, 1953; Young,
1961; Davidson, 1966a). Injections of tes-
tosterone propionate (75 pig twice weekly)
they do in the test settings that we have prevented loss of sexual activity and main-
employed. tained copulatory behavior at the level of
intact males. This dose of testosterone pro-
HORMONAL CONTROL OF SEXUAL pionate did not restore sexual behavior
BEHAVIOR AND SCENT MARKING once it had ceased, but larger doses (600
Next we turned our attention to andro- ixg twice weekly) did. Thus gerbils resem-
gen control of male sexual behavior. Al- ble rats: more testosterone is needed after
though gerbils have been popular subjects castration to reinstate mating behavior
for research on social behavior for years, than is needed to maintain mating behav-
no data were available on the hormonal ior (Davidson and Bloch, 1969).
basis of male copulatory behavior. It ap- Testosterone propionate injections also
pears that this was due in part to difficul- prevented and reversed castration-in-
ties in inducing gerbils to copulate in sit- duced decreases in scent marking (see Fig-
uations where their behavior could be ure 2); however, the 75 //.g (twice weekly)
observed and quantified. Initially we were dose of testosterone propionate that fully
plagued with problems in obtaining a rea- maintained mating did not fully maintain
sonable number of males that would cop- scent marking in the same males. This was
ulate reliably, e.g., males that would cop- our first clue that scent marking and sex-
ulate to ejaculation in three of five ual behavior were differentially sensitive to
preliminary screening tests. By trying a va- testosterone. Which behavior is more sen-
riety of environmental manipulations, we sitive to testosterone varies with the exper-
have since found that male gerbils are imental paradigm.
most likely to copulate if they are housed When male gerbils were implanted sev-
with other males and if they are tested dur- eral weeks after castration with testoster-
ing the light rather than the dark phase of one contained in silastic capsules, so that
the cycle (Yahr et al, 1980). Males housed they were continuously exposed to hor-
in pairs or groups (of 4) were 3^1 times mone, both sexual behavior and scent
more likely to mount, intromit, and ejac- marking resumed as a function of hor-
ulate than isolated males. The percentage mone dose (capsule length), as shown in
of tests in which sexual behavior occurred Figure 3 (Yahr et al, 1979). However, less
and the level of sexual activity among testosterone was needed to reinstate scent
males that mounted were both higher in marking than to reinstate sexual behavior.
the light than in the dark. Ejaculation, in A dose of testosterone (2-mm capsules)
particular, was more likely to occur in the that reinstated ejaculation in only 57% of
light and in grouped males. In contrast, castrates elevated scent marking frequen-
grouped males scent marked only half as cies above precastration levels in the sameSCENT MARKING, MATING AND AGGRESSION 147
males. Males that reliably copulated to eja-
Sham-operated Controls
culation before castration rarely mounted
when given a lower dose of testosterone Castrates
(1-mm capsules), yet this dose reinstated
scent marking to 25% of precastration
Revels in a subset of these males that were
also reliable scent markers (i.e., that ob-
tained mean marking scores of at least five
marks per 5-min test) before castration. In
some males that regularly ejaculated but
rarely scent marked before castration, low Pre-op I 2 3 4 5 6 7 8 9 10 tl 12 13 14 15 16
doses of testosterone induced high mark- Weekly Tests After Surgery
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ing frequencies without reinstating mount- FIG. 2. Changes in scent marking frequency of male
ing. Thus it was easier to reinstate scent gerbils after castration and during treatment with tes-
marking than sexual behavior using hor- tosterone propionate (TP). TP was injected twice a
mone implants, whereas in the previous week in the doses specified in the figure. Data shown
study it was easier to maintain sexual be- are for males that averaged five or more marks per
test before castration. Figure taken from Yahr et al.
havior than scent marking with hormone (1979).
injections. These differences in the sensi-
tivity of scent marking and sexual behavior
to testosterone across studies may reflect
differences in the treatment paradigm Wilson, 1968). It is presumed that dihy-
(maintenance or reinstatement), the form drotestosterone is not aromatized within
of hormone administration (injections or the brain because it is not aromatized by
capsules), or the dose-response curves for human placental microsomes (Ryan, 1960),
the two behaviors. the standard assay system for assessing
Differential sensitivity of scent marking aromatization. If testosterone activates
and sexual behavior to hormonal stimula- sexual behavior or scent marking via 5a-
tion is also apparent when other steroid reduction, then dihydrotestosterone should
hormones are substituted for testosterone be more potent behaviorally than testos-
(Yahr and Stephens, unpublished data). terone. If aromatization is essential, dihy-
Our analysis of the effects of different ste- drotestosterone should be ineffective,
roids was motivated by an interest in the whereas estradiol should be more potent
role of metabolism in androgen action on than testosterone. 19-Nortestosterone was
the brain and behavior. According to one selected for study because it is converted
currently popular hypothesis, testosterone to estrogen 20% as efficiently as testoster-
is a prohormone that stimulates male sex- one in placental microsomes (Ryan, 1959).
ual behavior via its metabolism to estrogen Thus estradiol, testosterone, 19-nortestos-
(aromatization) within the brain (see re- terone, and dihydrotestosterone represent
view by Adkins, 1981). To test the role of a graded series in terms of the amount of
aromatization in androgen control of sex estrogen available either directly or via
and scent marking in male gerbils, we aromatization.
studied the behavioral effects of estrogen All of the steroids maintained and rein-
and of androgens that vary in their ability stated scent marking in castrated males
to be metabolized to estrogens. More spe- and few significant differences between
cifically, we compared the behavioral ef- groups emerged. None of the steroids was
fects of dihydrotestosterone, 19-nortestos- more potent than testosterone. This sug-
terone, testosterone, and estradiol. gests that neither aromatization nor 5a-re-
Dihydrotestosterone, a 5a-reduced me- duction alone can account for the stimu-
tabolite of testosterone, is the active form latory effects of testosterone on scent
of testosterone for promoting growth of marking, although it is possible that the
tissues in the male reproductive tract (An- doses of hormone used (2- and 5-mm cap-
derson and Liao, 1968; Bruchovsky and sules) were too large to adequately distin-148 PAULINE YAHR
but ejaculatory behavior ceased in most
1
estradiol-treated castrates within 5 wk.
•o 25 loo- The decline in ejaculations may reflect an
80 inability of estradiol to maintain penile re-
2 20
£ IS-
* k
1I 1 60
1
g
1—|
flexes and morphology, as has been re-
ported for rats (Sodersten, 1975; Haijfe
1979). However, estradiol proved less et-
2 10 ilT 40 fective than either testosterone or 19-nor-
= 5-
'i testosterone in restoring mounting behav-
« 20-
ior. Castrates given 2-mm capsules of
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estradiol mounted in only 8% of their tests.
2 mm 5 mm 10
T
Length of Silastic Capsule of T
I mm 2 mm 5mm |0mm
When the estradiol dose was increased (5-
Length of Silastic Capsule of T
mm capsules), mounting still occurred in
Fic. 3. Dose-response relationships for reinstate- only 33% of the tests. Thus gerbils differ
ment by testosterone (T) of ejaculatory behavior and considerably from rats which resume
scent marking in castrated male gerbils. Asterisks in-
dicate mean marking scores before castration. Mark- mounting much more readily in response
ing scores shown are for males that averaged five or to estradiol than in response to testoster-
more marks per test before castration. All males cop- one (Baum and Vreeburg, 1973).
ulated to ejaculation in at least 2 of 3 precastration
tests. Figure taken from Yahr et at. (1979). The levels of mounting behavior in-
duced in gerbils by estradiol were actually
lower than those induced by implants of
dihydrotestosterone. Dihydrotestosterone
guish their effects on marking behavior. (2-mm capsules) did not maintain mount-
In contrast, the steroids differed consid- ing behavior after castration. Yet castrates
erably in their effects on mating. given 2- and 5-mm capsules of dihydrotes-
Testosterone and 19-nortestosterone tosterone in a reinstatement paradigm
were the most potent steroids for stimu- mounted in 17% and 56% of their tests,
lating sexual behavior. When administered respectively. In terms of reinstating eja-
in 2-mm capsules implanted at castration, culation, dihydrotestosterone was roughly
these steroids maintained ejaculation fre- as potent as testosterone. When given in 2-
quency at 109% and 93% of precastration and 5-mm capsules, dihydrotestosterone
levels, respectively. They also reinstated restored ejaculation frequencies to 22%
sexual activity once it had ceased in the and 55% of precastration levels, respec-
absence of hormonal stimulation, although tively, compared to 8% and 67% for tes-
19-nortestosterone was more potent than tosterone. Thus to some extent gerbils re-
testosterone in this paradigm. Within semble guinea pigs {Cavia porcellus) and
three to five weeks after implantation of rhesus monkeys (Macaca mulatto) in terms
19-nortestosterone in 2-mm capsules, eja- of their ability to respond to dihydrotes-
culation frequencies of castrates returned tosterone (Alsum and Goy, 1974; Phoenix,
to 109% of precastration values. Ejacula- 1974).
tion frequencies of castrates given testos- Our comparisons of the behavioral ef-
terone returned to only 8% of precastra- fects of different steroids must be tem-
tion levels in the same time. A larger dose pered by the fact that they are released
of testosterone (5-mm capsules) boosted from silastic capsules at different rates.
ejaculation frequencies to 67% of precas- (They are, of course, also released at dif-
tration levels. The observation that 19-nor- ferent rates from oil depots produced by
testosterone reinstated sexual behavior at subcutaneous injections.) Nonetheless, it
a lower dose than testosterone seems in- seems difficult to account for all of the data
compatible with the notion that androgens on the basis of differential release rates.
act via their estrogenic metabolites. The release of estradiol would have to be
Estradiol (2-mm capsules) maintained very low to be less than the amount of es-
high levels of mounting after castration, as tradiol produced by aromatization of tes-
predicted by the aromatization hypothesis, tosterone within the brain since the con-SCENT MARKING, MATING AND AGGRESSION 149
version ratio is less than 0.1% (Naftolin et 5
4 0
al., 1975). Similarly, if 19-nortestosterone 3
acted via aromatization yet is more potent 2
• TP in Am POA
than testosterone, it must be released more II
0
than five times as rapidly as testosterone 9
^iven that it is aromatized only one-fifth as 8 /
well. 7
6
/ v \
/ \ «TP in Pos! POA
Xv
5
NEURAL CONTROL OF SEXUAL BEHAVIOR 4 -^ /
AND SCENT MARKING 3 ,, ~y \ f.. Js>~=-—"TPinLotPOA
2
The medial preoptic area-anterior hy- 1
* * • • - - « . > < _ /
^-tf''^*'^
* ' " ^ "
T P
^»---*Cholesterol
' " " " '
P O a
pothalamus mediates androgen control of 0 e ^
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Pre Post I 2 3 4 5 6 7 8 9 1
male copulatory behavior in various ver- Castration
Test Periods offer Brain Implants
tebrate species, including lizards, frogs FIG. 4. Changes in scent marking frequencies of cas-
(Rana pipiens), ring doves (Streptopelia ri- trated male gerbils after implantation of testosterone
soria), rats, cats, dogs and rhesus monkeys propionate (TP) into either the anterior (Ant), middle
(Davidson, 19666; Heimer and Larsson, (Mid), or posterior (Post) portion of the medial
1966; Slimp et al, 1968; Barfield, 1971; preoptic area (POA), or into the lateral preoptic area
Hart, 1974; Hart et al., 1974; Wada and (Lat POA). Controls received cholesterol implants at
the same locations.
Gorbman, 1977; Morgantaler and Crews,
1978; Wheeler and Crews, 1978). This
area of the brain also controls various pat-
terns of social signalling in males. For ex- after castration, but implants into the mid-
ample, lesions that impair copulatory be- dle portion of the medial preoptic area or
havior also disrupt assertion and challenge into the lateral preoptic area did not.
displays in male lizards and eliminate uri- These data are shown in Figure 4.
nary scent marking in male dogs and cats In contrast, the middle portion of the
(Hart, 1974; Hart and Voith, 1978; Wheel- medial preoptic area seems critical for the
er and Crews, 1978). Implanting testoster- display of sexual behavior in male gerbils.
one directly into the medial preoptic area- This conclusion is based on the effects of
anterior hypothalamus stimulates display lesions in the medial preoptic area-ante-
behavior in lizards, mate-calling in frogs, rior hypothalamus (Yahr et al., unpub-
and scent marking in gerbils (Thiessen et lished data). These lesions eliminated or
al., 1973; Wada and Gorbman, 1977; Mor- severely impaired mating behavior in go-
gantaler and Crews, 1978). We were inter- nadally intact males. After lesioning, most
ested in determining whether the medial males (13/17) stopped ejaculating and
preoptic area-anterior hypothalamus con- nearly half (7/17) never mounted. Those
trols sexual behavior in male gerbils and that did mount did so much less often after
whether the cells mediating androgen con- lesioning than before. These deficits were
trol of scent marking and sexual behavior neither prevented nor reversed by admin-
were the same. Our data indicate that dif- istration of exogenous testosterone, indi-
ferent, although possibly overlapping, cell cating that the behavioral decrements were
populations in this region control the two not due to decreased gonadotropin and
behaviors. hence testicular androgen secretion. Le-
The most important areas for mediating sions that eliminated mounting were clus-
androgen control of scent marking are the tered in the middle portion of the medial
anterior aspect of the medial preoptic preoptic area.
area, near the diagonal band of Broca, and Interestingly, the same lesioned males
the posterior aspect of the medial preoptic showed only temporary decreases in the
area, near the anterior hypothalamus frequency of scent marking. Even this tem-
(Yahr et al., unpublished data). Testoster- porary decline did not occur in males im-
one implants into these portions of the planted with silastic capsules of testoster-
preoptic area induced marking behavior one at lesioning. Since the lesions generally150 PAULINE YAHR
spared the most anterior and the most pos- golian gerbil (Meriones unguiculatus). Physiol. Be-
terior aspects of the medial preoptic area hav. 10:989-994.
Christie, M. H. and R. J. Barfield. 1979. Effect of
(i.e., the areas implicated in the control of castration and home cage residency on aggres-
scent marking), this may account for the sive behavior in rats. Horm. Behav. 13:85-91.
sparing of scent marking function. This Crews, D and N. Greenberg. 1981. Function and
possibility gains support from the obser- causation of social signals in lizards. Amer. Zoofe
vation that the few males that seemed to 21:273-294.
suffer permanent disruption of scent Davidson, J. M. 1966a. Characteristics of sex behav-
iour in male rats following castration. Anim. Be-
marking, despite hormone therapy, had hav. 14:266-272.
lesions that included one or the other of Davidson, J. M. 1966ft. Activation of the male rat's
Downloaded from https://academic.oup.com/icb/article/21/1/143/134137 by guest on 23 January 2021
these sites. These data suggest that gerbils sexual behavior by intracerebral implantation of
differ from lizards, dogs, and cats in that androgen. Endocrinology 79:783-794.
Davidson, J. M. and G. J. Bloch. 1969. Neuroen-
different neural loci control social signal- docrine aspects of male reproduction. Biol. Re-
ling and sexual behavior. Perhaps more prod. 1 (Suppl.):67-92.
discrete lesions within the medial preoptic Grunt, J. A. and W. C. Young. 1953. Consistency of
area-anterior hypothalamus would reveal sexual behavior patterns in individual male
specificity of function in these other guinea pigs following castration and androgen
therapy. J. Comp. Physiol. Psychol. 46:138-144.
species as well. Hart, B. L. 1974. Medial preoptic-anterior hypotha-
lamic area and the sociosexual behavior of male
ACKNOWLEDGMENTS dogs: A comparative neuropsychological analy-
sis. J. Comp. Physiol. Psychol. 86:328-349.
The research summarized here was sup- Hart, B. L. 1979. Activation of sexual reflexes of
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