Brain Research 988 (2003) 139–145
www.elsevier.com / locate / brainres
Research report
Medial preoptic area dopaminergic responses to female pheromones
develop during puberty in the male Syrian hamster
Kalynn M. Schulz a , Heather N. Richardson a,c , Russell D. Romeo a,c , John A. Morris c ,
Keith J. Lookingland b,c , Cheryl L. Sisk a,c , *
a
b
Department of Psychology, Michigan State University, East Lansing, MI 48824, USA
Department of Pharmacology and Toxicology, Michigan State University, East Lansing, MI 48824, USA
c
Neuroscience Program, Michigan State University, East Lansing, MI 48824, USA
Accepted 15 July 2003
Abstract
Chemosensory cues from receptive females do not elicit similar reactions before and after puberty in male hamsters. While pheromones
facilitate a complex display of reproductive behavior in adults, prepubertal males do not engage in these same behaviors. Dopamine (DA)
released from the medial preoptic area (MPOA) in response to a receptive female or her odors is an important component of the neural
events underlying adult male rat sexual behavior. The current experiment investigated whether increased dopaminergic activity occurs in
the adult male hamster MPOA in response to female pheromones, and if so, whether this response is absent in prepubertal males, which
¨ prepubertal and adult male hamsters were exposed to cotton swabs with or without pheromone from an
do not mate. Sexually naıve
estrous female for 0, 5, 15, or 25 min, after which brains were collected and frozen on dry ice. The MPOA was micropunched from frozen
coronal sections (500 mm), and concentrations of DA and its primary metabolite DOPAC were determined by high-performance liquid
chromatography–electrochemical detection. DOPAC was used as an index of dopaminergic activity. DOPAC levels significantly increased
in adults after 15 min exposure to pheromone. In contrast, MPOA DOPAC concentrations did not increase in prepubertal males exposed to
pheromone. These data demonstrate that the neural processing of sexually relevant chemosensory stimuli matures during puberty. The
absence of a DA response to female pheromones prior to puberty may contribute to the inability of prepubertal males to display
reproductive behavior.
2003 Elsevier B.V. All rights reserved.
Theme: Neural basis of behaviour
Topic: Monoamines and behaviour
Keywords: Dopamine; Pheromone; Reproductive behavior; Puberty; Medial preoptic area
1. Introduction
Puberty is the developmental stage during which male
rodent reproductive behaviors emerge. In the adult male
Syrian hamster, full expression of reproductive behavior
relies on both the presence of gonadal steroid hormones
and exposure to female pheromones [10,26]. These
pheromonal cues and steroidal signals are integrated within
a forebrain neural circuit consisting of the medial
*Corresponding author. Department of Psychology and Neuroscience
Program, 108 Giltner Hall, Michigan State University, East Lansing, MI
48824, USA. Tel.: 11-517-355-5253; fax: 11-517-352-2744.
E-mail address: sisk@msu.edu (C.L. Sisk).
0006-8993 / 03 / $ – see front matter 2003 Elsevier B.V. All rights reserved.
doi:10.1016 / S0006-8993(03)03358-4
amygdala (Me), the bed nucleus of the stria terminalis
(BNST) and nuclei within the medial preoptic area
(MPOA) [26]. While the neural circuitry underlying
chemosensory processing and the hormonal regulation of
reproductive behavior are well studied in the adult male
Syrian hamster, how these steroid-sensitive circuits develop during puberty to permit the expression of adult
behavior is not clear.
Unlike adults, prepubertal males do not mate with a
receptive female, even when treated with adult levels of
gonadal steroids [9,16,20]. Surprisingly, differences in
neural responses to steroid hormones do not seem to
account for these behavioral differences. For example, both
testosterone and dihydrotestosterone increase brain an-
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K.M. Schulz et al. / Brain Research 988 (2003) 139–145
drogen receptor immunoreactivity in prepubertal and adult
castrates [9,16]. Testosterone is also capable of increasing
hypothalamic aromatase activity both before and after
puberty [19]. Estrogen receptor immunoreactivity is similar in pre- and postpubertal males, and estrogen treatment
increases progesterone receptors before and after puberty
[17,20]. Thus, many of the neural responses to steroid
hormones that are important for the display of male
reproductive behavior are in place before puberty, even
though the behavior is not expressed until after puberty.
Differences in the neural processing of female pheromones may account for prepubertal and adult differences
in reproductive behavior. In adults, exposure to the pheromone-containing vaginal secretions of a female elicits an
increase in plasma concentrations of testosterone 1 h later
[18]. While this increase in testosterone is not required for
the display of reproductive behavior, it is nevertheless a
clear index of the activation of the hypothalamic–pituitary–gonadal axis by pheromonal exposure. Interestingly,
prepubertal males do not exhibit an increase in testosterone
after exposure to female pheromones, which suggests that
the ability to detect and / or process female pheromones is
immature prior to pubertal maturation [18]. It is apparent,
however, that prepubertal males do detect female pheromones, since like adults, they display increased expression
of the immediate-early gene product Fos within cell groups
of the Me, BNST, and MPOA after exposure to pheromones [18]. This finding further suggests that differences
between prepubertal and adult pheromonal processing are
downstream of the initial pheromonal activation of cell
groups that mediate mating behavior.
DA release in the MPOA also occurs in response to
female chemosensory cues, and this response is important
for the expression of male rodent reproductive behavior
[6]. For instance, microinjections of the DA receptor
antagonist cis-flupenthixol into the MPOA impair ejaculatory behavior in rats, and decrease the percentage of trials
in which males choose a female partner over a male
partner [25]. Conversely, the DA receptor agonist apomorphine increases reproductive behavior in castrated rats
[21]. Apomorphine also decreases both the latency to
ejaculate and the length of time between ejaculations in
male Syrian hamsters [3]. Microdialysis studies have
confirmed that gonad-intact male rats release DA into the
MPOA when they are exposed to the odors, sights, and
sounds of an estrous female through a screen, and that
copulation is accompanied by further increases in MPOA
DA [6]. These data demonstrate that the integration of
pheromonal and steroidal information in the mating circuitry results in DA release in the MPOA, which in turn
stimulates reproductive behavior. We hypothesize that the
inability of prepubertal males to engage in copulatory
behavior is related to the immaturity of hypothalamic
dopaminergic systems.
Preliminary data suggest that MPOA dopaminergic
activity increases in response to female pheromones in
male hamsters, as it does in rats [12]. One objective of this
study was to confirm and extend the observation that male
hamster dopaminergic activity is increased within the
MPOA in response to female chemosensory cues (experiment 1). The primary goal of this study was to determine
whether DA responses to female pheromones occur prior
to puberty (experiment 2). Prepubertal and adult hamsters
were exposed to the vaginal secretions of estrous females,
after which concentrations of DA and its primary metabolite DOPAC were measured in tissue extracts of the MPOA
and the adjacent periventricular nucleus (PeVN). DOPAC
is the primary metabolite of DA, and serves as an index of
the activity of DA neurons [11]. We report here that female
pheromones elicit increased dopaminergic activity in adult
but not in prepubertal males, which may account for the
inability of prepubertal males to engage in reproductive
behavior.
2. Materials and methods
2.1. Animals
Male Syrian hamsters were obtained from Charles River
Laboratories (Kingston, NY, USA), singly housed in clear
polycarbonate cages, and allowed at least 7 days to
acclimate to their new environment before tests were
conducted. The animals were maintained on a 14-h / 10-h
light–dark schedule (lights out at 12.00 h) at 2162 8C.
Food (Teklad Rodent Diet No. 8640; Harlan, Madison, WI,
USA) and water were available ad libitum. All animals
were treated in accordance with the NIH Guide for the
Care and Use of Laboratory Animals, and the protocols
were approved by the Michigan State University All
University Committee for Animal Use and Care.
2.2. Experimental procedures
2.2.1. Experiment 1
Two groups of adults (66 days of age) were exposed to
cotton swabs in their home cages starting 1 h into the dark
phase of the light–dark cycle. The control group was
exposed to a clean (blank) cotton swab, and the experimental group was exposed to a cotton swab containing
the vaginal secretions of an estrous female. Animals were
decapitated 15 min after introduction of the swab to the
home cage. Brains were removed, frozen on aluminum foil
placed on dry ice, and stored at 280 8C until sectioned.
2.2.2. Experiment 2
Prepubertal (28 days of age) and adult (66 days of age)
males were exposed in their home cages to either blank or
pheromone-containing swabs starting 1 h into the dark
phase of the light–dark cycle. Animals were decapitated
either 5, 15, or 25 min following the introduction of the
swabs to the home cage (n58 each age / condition / time-
K.M. Schulz et al. / Brain Research 988 (2003) 139–145
point). Groups of age-matched males that were not exposed to a cotton swab served as time-zero controls. Trunk
blood was collected for determination of plasma testosterone concentrations, and brains were removed, frozen
on dry ice, and stored at 280 8C until sectioned.
2.3. Plasma testosterone radioimmunoassay
Plasma concentrations of testosterone were measured in
50 ml samples within a single assay using the Coat-ACount Total Testosterone Kit (Diagnostic Products, Los
Angeles, CA, USA). This assay has been previously
validated in our laboratory [14]. The intraassay C.V. was
9.2%, and the lower limit of detectability was 0.1 ng / ml.
2.4. Tissue microdissection
The MPOA and PeVN were located within the same 500
mm coronal section that was cut on a cryostat and thawmounted onto a glass slide. The coronal section containing
the MPOA and PeVN corresponds to Fig. 19 of Paxinos
and Watson [15]. The PeVN served as a control brain
region. All sections were stored on dry ice until tissue
punches were dissected. The MPOA (experiments 1 & 2),
and PeVN (experiment 2 only) were dissected using a
modification of the technique of Palkovits [13]. Tissue
samples were placed in 65 ml of 0.05 M sodium
phosphate / 0.03 M citrate buffer (pH 2.5) containing 15%
methanol and stored at 280 8C until extraction.
2.5. High-performance liquid chromatography ( HPLC)
Concentrations of neurotransmitters and their metabolites in tissue samples of the MPOA (experiments 1 & 2)
and PeVN (experiment 2) were determined by HPLC with
electrochemical detection as previously described [4]. On
the day of the assay, tissue samples were thawed, sonicated
for 3 s (Sonicator Cell Disruptor; Heat Systems Ultrasonic,
Plainview, NY, USA), and centrifuged for 30 s in a
Beckman Microfuge B. The supernatant was then drawn
off from each tissue sample and analyzed for DOPAC
(experiments 1 & 2), DA (experiments 1 & 2), norepinephrine (NE) (experiment 2), serotonin (5-HT) (experiment
2), and the serotonin metabolite 5HIAA (experiment 2) by
HPLC. NE, 5-HT, and 5HIAA were measured in the
MPOA in order to determine whether the activity of other
cell populations in the MPOA is altered after exposure to
pheromones. The remaining tissue pellets were dissolved
in 1.0 M NaOH and assayed for protein content [8].
A 50-ml volume of the supernatant was injected onto a
C 18 reversed-phase analytical column (5 mm spheres;
25034.6 mm; Biophase ODS; Bioanalytical Systems, West
Lafayette, IN, USA). The analytical column was protected
by a precolumn cartridge filter (5 mm spheres; 3034.6
mm). The HPLC column was coupled to a single
coulometric electrode-conditioning cell in series with dual
141
electrode analytical cells (ESA, Bedford, MA, USA). The
conditioning cell electrode was set at 10.40 V, and the
analytical electrodes were set at 10.12 V and 20.40 V,
relative to internal silver reference electrodes. The HPLC
mobile phase was composed of 0.1 M phosphate / citrate
buffer (pH 2.5) containing 0.1 mM EDTA, 0.035% sodium
octylsulfate, and 10–25% methanol. The quantities of
neurotransmitters and their metabolites in each sample
were determined by comparing peak heights (recorded
from the 20.40 V analytical electrode by a HewlettPackard Integrator, Model 3393A) with those obtained
from standards run on the same day.
2.6. Statistics
Although each treatment group consisted of eight animals (experiments 1 & 2), actual sample sizes for each
brain region analyzed varied due to occasional difficulties
during sectioning or microdissection, which prevented
tissue samples from a particular brain region or animal
from being analyzed. In all cases the final sample sizes
were $5. In experiment 1, a one-way analysis of variance
(ANOVA) was used to compare DOPAC and DA concentrations in the MPOA of adults after a 15 min exposure
to blank or pheromone containing swabs. Experiment 2
employed a three-way ANOVA to analyze the effects of
age, swab type, and duration of swab exposure on concentrations of DOPAC, DA, NE, 5-HT, and 5HIAA in the
MPOA and PeVN. Significant interactions were probed
using Tukey HSD post-hoc tests. Differences were considered significant when P,0.05.
3. Results
3.1. Experiment 1
3.1.1. DOPAC and DA in the MPOA
Adults exposed to a pheromone swab for 15 min had
significantly greater concentrations of MPOA DOPAC than
adults exposed to a blank swab for 15 min [F(1,12)57.45,
P,0.02]. No significant differences in MPOA DA concentrations were detected between males exposed to blank
and pheromone-containing swabs (Fig. 1).
3.2. Experiment 2
3.2.1. Plasma testosterone
There were no main effects of swab type or swab
duration on plasma testosterone, and these variables were
therefore collapsed to compare testosterone levels of
prepubertal and adult males. Adults had significantly
greater plasma concentrations of testosterone than did
prepubertal males [2.7360.215 vs. 0.4060.115 ng / ml,
respectively; F(1,123)591.18, P,0.0001].
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K.M. Schulz et al. / Brain Research 988 (2003) 139–145
Fig. 1. Pheromone exposure increases dopaminergic activity in the
MPOA of adult males. Mean concentrations (ng / mg protein) of DOPAC
and dopamine (DA) in medial preoptic area (MPOA) tissue punches of
adults exposed to blank or pheromone-containing swabs for 15 min. All
values are means6S.E.M. Asterisk indicates P,0.05. The number of
animals in each group is indicated.
3.2.2. DOPAC in the MPOA
The three-way ANOVA revealed a significant three-way
interaction between age, swab type, and swab duration
[F(3,81)54.66, P,0.01]. When exposed to pheromonecontaining swabs, adults exhibited significantly greater
DOPAC levels than prepubertal males [F(1,81)513.01,
P,0.001] (Fig. 2A and B). In contrast, no differences
between prepubertal and adult males were observed when
exposed to blank swabs [F(1,81)53.706, P.0.05] (Fig.
2C and D). Furthermore, when the DOPAC responses of
prepubertal and adult males were compared across the
Fig. 2. MPOA DOPAC increases in adult but not prepubertal males after
pheromone exposure. Mean concentrations (ng / mg protein) of DOPAC in
medial preoptic area (MPOA) tissue punches of prepubertal and adult
males exposed to blank or pheromone-containing swabs for 0, 5, 15, or 25
min. The asterisk indicates that adult males display significantly increased
DOPAC concentrations 15 min after pheromone exposure while prepubertal males do not. All values are means6S.E.M. The number of animals in
each group is indicated.
Fig. 3. MPOA DA levels in prepubertal and adult males. Mean concentrations (ng / mg protein) of dopamine (DA) in medial preoptic area
(MPOA) tissue punches of prepubertal and adult males exposed to blank
or pheromone-containing swabs for 0, 5, 15, or 25 min. Main effect bar
graph illustrates that adults exhibit overall higher concentrations of DA.
All values are means6S.E.M. Asterisk indicates P,0.05. The number of
animals in each group is indicated.
different pheromone-swab exposure durations, Tukey tests
revealed that adults had significantly greater concentrations
of DOPAC than prepubertal males after 15 min of exposure to a pheromone-swab [F(1,81)524.00, P,0.01], but
not after 0, 5, or 25 min exposure (Fig. 2A and B).
3.2.3. DA in the MPOA
Adults exhibited significantly greater overall concentrations of MPOA DA than prepubertal males [F(1,815
20.90), P,0.001] (main effect of age, Fig. 3). DA
concentrations were not significantly affected by the type
of swab presented, or the duration of swab exposure.
3.2.4. DA and DOPAC in the PeVN
Adults exhibited significantly greater overall concentrations of PeVN DA than prepubertal males [F(1,75)5
5.53, P,0.03] (main effect of age, Fig. 4). No changes in
Fig. 4. Prepubertal and adult male PeVN DA levels. Mean concentrations
(ng / mg protein) of dopamine (DA) in periventricular nucleus (PeVN)
tissue punches of prepubertal and adult males exposed to blank or
pheromone-containing swabs for 0, 5, 15, or 25 min. Main effect bar
graph illustrates the higher overall concentration of PeVN DA in adult
males. All values are means6S.E.M. Asterisk indicates P,0.05. The
number of animals in each group is indicated.
K.M. Schulz et al. / Brain Research 988 (2003) 139–145
Fig. 5. Prepubertal and adult NE levels in the MPOA. Mean concentrations (ng / mg protein) of norepinephrine (NE) in medial preoptic
area (MPOA) tissue punches of prepubertal and adult males exposed to
blank or pheromone-containing swabs for 0, 5, 15, or 25 min. Main effect
bar graph illustrates that adult males exhibit overall greater concentrations
of norepinephrine (NE). All values are means6S.E.M. Asterisk indicates
P,0.05. The number of animals in each group is indicated.
DA concentration were observed with exposure to blank or
pheromone-containing swabs. No significant differences
were observed between prepubertal and adult PeVN concentrations of DOPAC, nor were there any significant
changes in DOPAC concentrations with exposure to blank
or pheromone containing swabs (data not shown).
3.2.5. NE in the MPOA
Analysis of MPOA NE concentrations revealed a main
effect of age, such that adults exhibited significantly
greater concentrations of NE than prepubertal males
[F(1,81510.97, P,0.01] (main effect of age, Fig. 5). NE
levels did not significantly vary with the type of swab or
with the duration of swab exposure.
Fig. 6. Prepubertal and adult 5-HT levels. Mean concentrations (ng / mg
protein) of serotonin (5-HT) in medial preoptic area (MPOA) tissue
punches of prepubertal and adult males exposed to blank or pheromonecontaining swabs for 0, 5, 15, or 25 min. No significant effects of age,
swab type, or time were observed for 5-HT levels in the MPOA. All
values are means6S.E.M. The number of animals in each group is
indicated.
143
Fig. 7. Prepubertal and adult levels of the serotonin metabolite 5HIAA.
Mean concentrations (ng / mg protein) of 5HIAA in medial preoptic area
(MPOA) tissue punches of prepubertal and adult males exposed to blank
or pheromone-containing swabs for 0, 5, 15, or 25 min. No significant
effects of age, swab type, or time were observed for 5HIAA levels in the
MPOA. All values are means6S.E.M. The number of animals in each
group is indicated.
3.2.6. 5 -HT and 5 HIAA in the MPOA
No differences were observed between prepubertal and
adult levels of 5-HT (Fig. 6) or 5HIAA (Fig. 7) in the
MPOA. Further, no significant changes in 5-HT or 5HIAA
concentrations were observed after exposure to a blank or
pheromone-containing swab.
4. Discussion
This study demonstrates that increased MPOA dopaminergic activity in response to female pheromones occurs
in males only after pubertal maturation. The failure of
prepubertal males to display increases in DOPAC in
response to female pheromones is the first direct demonstration of differences in the neural processing of sexually
relevant information between prepubertal and adult males,
and this difference may contribute to the inability of
prepubertal males to engage in mating behavior. Thus,
expression of reproductive behavior in adulthood likely
involves maturation of the hypothalamic DA system during
puberty. Furthermore, we have confirmed that increased
dopaminergic activity in the MPOA occurs in adult male
hamsters when presented with female odors [12]. Thus,
female sensory stimuli elicit MPOA DA responses in male
hamsters as well as in male rats [6].
Two important aspects of neural maturation during
puberty were elucidated in this study. First, the pubertal
development of increased dopaminergic activity in response to female chemosensory stimuli was demonstrated,
as indexed by increased DOPAC concentrations in adults,
but not prepubertal males, after exposure to pheromones.
Second, DA responses to chemosensory cues seem to be
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K.M. Schulz et al. / Brain Research 988 (2003) 139–145
specific to the MPOA, and MPOA responses to pheromones seem to be specific to dopaminergic activity. The
nearby PeVN did not show increased DOPAC concentrations in response to female sensory cues, and within the
MPOA, NE, 5HIAA, and 5-HT levels did not change with
exposure to pheromone. Interestingly, overall levels of DA
in the MPOA and PeVN were greater in adults, which
suggests that the hypothalamic DA system undergoes
general developmental changes during puberty. MPOA
norepinephrine levels were also significantly higher in
adults than prepubertal males. MPOA concentrations of
serotonin and its metabolite 5HIAA, however, did not
change with pubertal maturation. Thus, while both DA and
NE-producing neurons of the hypothalamus undergo maturational changes during puberty, only the DA neurons
terminating in the MPOA acquire responsiveness to pheromones.
In both hamster and rat, the MPOA has a greater
concentration of NE than DA (current study, and Ref. [7]).
Because DA is a precursor of NE, both DA and DOPAC
may be produced by noradrenergic neurons. Therefore, it is
possible that the DOPAC measured in tissue punches of the
MPOA originated from noradrenergic neurons, and not DA
neurons. However, we conclude that the changes in
DOPAC concentration observed in the current study are the
result of increased dopaminergic activity. The relative
levels of DA, DOPAC, and NE in this study most closely
resemble what is typical for DA neuron activation, and not
noradrenergic activation. Specifically, when noradrenergic
MPOA neurons are activated, DOPAC and DA concentrations increase significantly while NE decreases significantly [24]. This pattern is observed because when
noradrenergic neurons are activated, the rate of DA
synthesis exceeds the rate of DA uptake and conversion to
NE by DA b-hydroxylase [24]. Therefore, precursor DA
accumulates in the cytoplasm and is metabolized to
DOPAC by monoamine oxidase in the mitochondria
[1,5,22]. Given that no changes in concentrations of NE
across experimental groups were observed in the current
study, and only a slight (non-significant) increase in DA
was observed after exposure to pheromone, we conclude
that DOPAC concentrations measured in the MPOA reflect
the activity of DA neurons and not NE neurons.
While adults displayed greater plasma concentrations of
testosterone than prepubertal males, neither age group
displayed increased plasma concentrations of testosterone
after exposure to pheromone swabs. This stands in contrast
with previously published work in which adult but not
prepubertal males displayed increased plasma testosterone
concentrations 60 min after exposure to female pheromones [18]. Most likely, the different results of these two
studies are attributable to differences in the time between
exposure to the pheromone swab and euthanasia of animals. In the present study, 0–25 min passed between swab
exposure and animal sacrifice, which may not have been
sufficient time for increases in plasma testosterone concentrations to be observed.
What are the relationships among testosterone, DA
responses to pheromones, and expression of male reproductive behavior? One week after removal of endogenous testosterone via castration, some, but not all, male rats
cease to copulate with a female [6]. Castrates that do not
engage in sexual behavior also fail to release DA in the
MPOA when exposed to an estrous female. However,
castrates that do engage in sexual behavior also release DA
in the MPOA in anticipation of and during copulation [6].
These results indicate that DA release is more closely tied
to the expression of male reproductive behavior than are
circulating testosterone levels, and that circulating testosterone is not required for the DA response to female
sensory stimuli. Thus, it seems likely that the absence of a
DA response to female pheromones in prepubertal males is
not due to their low levels of circulating testosterone.
Furthermore, if DA release is the critical neural response
for the induction of reproductive behavior, then we predict
that DA responses to pheromones would not occur in
prepubertal males treated with testosterone, because testosterone treated prepubertal males do not display mating
behavior.
The factors responsible for the pubertal increase in DA
responses to pheromones are presently unknown. One
possibility is that gonadal hormones, acting specifically
during the time of puberty, program or organize DA
responses to female sensory stimuli. If this is the case, then
depriving males of hormones during puberty via prepubertal gonadectomy should reduce dopaminergic activity and
mating behavior in testosterone treated adult males. While
we know that prepubertal gonadectomy of male hamsters
compromises the activation of mating behavior by testosterone in adulthood [23], we do not know whether this
attenuation of reproductive behavior is due to a reduction
in the MPOA DA response to female pheromones. Alternatively, pubertal maturation of hypothalamic dopaminergic systems may not depend on the presence of
testosterone during pubertal development. For instance,
Andersen et al. [2] reported that the overproduction and
subsequent pruning of striatal DA receptors that occurs
during puberty in male rats does not depend on gonadal
hormones. Future experiments will determine whether the
hypothalamic DA system is a target for organization by
gonadal hormones during puberty, or if the maturation of
MPOA DA responses to female pheromones is a developmentally timed steroid-independent process.
Acknowledgements
We thank Jane Venier for her expert technical assistance.
This work was supported by a grant from the National
Science Foundation IBN 99-85876.
K.M. Schulz et al. / Brain Research 988 (2003) 139–145
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