Chemical Senses Vol. 29 No. 7 © Oxford University Press
2004; all rights reserved
Importance of Learning in the Response of Ewes to Male Odor
Station de Physiologie de la Reproduction et des Comportements, UMR 6175 INRA/CNRS/Université de Tours, 37380 Nouzilly, France
Correspondence to be sent to: C. Fabre-Nys, Station de Physiologie de la Reproduction et des Comportements, UMR 6175 INRA/CNRS/Université de Tours, 37380 Nouzilly, France. e-mail: fabre{at}tours.inra.fr
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Abstract |
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Exposure of anestrous ewes to a ram or its odor results in the activation of the luteinizing hormone (LH) secretion leading to reinstatement of cyclicity in most females. Sexual experience and learning have been suggested as important factors to explain the variability of the female responses. In experiment 1, we compared the behavioral and endocrine responses of four groups of anestrous females that differed in age (young or adult) and previous exposure to males [naive (no exposure) or experienced (courtship behavior for young and numerous mating for adults)]. Age did not seem to affect the LH response to males or their odor. In contrast, sexual experience was a critical factor: the proportion of females exhibiting an LH response to male odor was significantly higher in experienced than in naive ewes. Sexual experience affected the response to male odor, but did not have an effect on responses to the male himself. A second experiment investigated whether the LH response to male odor could result from an associative learning process. Accordingly, we tested the effectiveness of a conditioned stimulus (lavender odor) previously associated with the male, in inducing the endocrine response. The results indicate that the odor of lavender activated LH secretion only in ewes that have been previously exposed to scented males. This demonstrates that ewes are able to learn the association between a neutral odor and their sexual partner.
Key words: luteinizing hormone, olfactory cues, sheep, social stimuli
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Introduction |
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Social stimuli are known to influence reproductive behavior and neuroendocrine function in a variety of vertebrate species. In mammals, olfactory cues can mimic most effects of the interactions between conspecifics or between sexual partners.
Physiological changes induced by sexual chemosignals are frequently stereotyped
responses (Keverne, 1986
). In several
species, male odors accelerate puberty in young females that have never been in contact
with males, for example: mouse (Vandenbergh,
1969); prairie vole (Carter et
al., 1980); hamster (Reasner and
Johnston, 1988); and cow (Izard and
Vandenbergh, 1982). In hamsters, chemosignals in female vaginal secretions
induce an increase of testosterone in sexually naive males (Pfeiffer and Johnston, 1994). Naive male mice also
reflexively release luteinizing hormone (LH) and testosterone pulses after encountering a
female or her urinary pheromones (Macrides et
al., 1975;
Maruniak and Bronson, 1976). In some
cases, chemosignals may also induce stereotyped behavioral responses. For example,
sexually naive males hamster are attracted to female vaginal secretions and attempt to
copulate with anaesthetized surrogates scented with these secretions (Murphy, 1973;
Macrides et al., 1977,
1984).
However, most behavioral responses elicited by sexual pheromones are facilitated by
previous sexual experience. In many species, chemical signals serve as sexual
attractants, induce sexual arousal, appetitive and precopulatory postures and mating
behavior but these responses are preferentially expressed by sexually experienced
individuals. In adult male rats, mice and dogs, sexual experience results in a preference
for estrous over nonestrous females odors (Carr
et al., 1965;
Doty and Dunbar, 1974;
Hayashi and Kimura, 1974). In mice,
the presentation of female urine elicits vocalizations only in sexually experienced males
(Dizinno et al., 1978). The
role of learning in the development of behavioral response to olfactory cues has been
also demonstrated using conditioning paradigms. A conditioned cue (a neutral odor
associated with mating with a receptive female) induces sexual partner preferences
(Kippin and Pfaus, 2001a,b) and
elicits males vocalizations (Nyby et
al., 1978).
The role of experience is not limited to the treatment of social and sexual olfactory
cues. On the contrary, learning processes are generally required for the identification
of environmental odors that can be either associated with a reward or an aversive
stimulus (Schoenbaum et al.,
1998;
Tronel and Sara, 2002). These
artificial learned odors are principally detected by the main olfactory system, which is
usually considered as a general molecular analyser of an enormous variety of odorants
(Mori et al., 2000).
In rodents, chemosignals inducing stereotyped physiological or behavioral changes are
essentially detected and integrated by the accessory olfactory system (Keverne, 1983, 1999;
Brennan, 2001). Lesion of the
vomeronasal organ (VNO) impairs dramatically the responses to conspecific odors
(Wysocki and Lepri, 1991). This
blockage mainly concerns the endocrine responses that are generally pre-programmed,
whereas sexual experience can compensate for the behavioral effects of VNO destruction.
In male hamsters, lesion of the VNO abolished copulatory behavior only in sexually naive
animals (Meredith, 1986). Destruction
of the VNO of male mice eliminates vocalizations in response to female urine but only in
sexually naive individuals (Bean,
1982).
During the non-breeding season, the ram or its fleece induce an immediate increase in
plasma LH by ewes (Knight et al.,
1983;
Martin et al., 1983). In
sheep, in contrast to rodents, male pheromone seems essentially detected by the main
olfactory system (Cohen-Tanoudji et al.,
1989;
Gelez and Fabre-Nys, 2004).
Furthermore, preliminary data suggest that the endocrine response induced by male odor
may be affected by sexual experience and could involve learning mechanisms
(Cohen-Tanoudji, unpublished data). This phenomenon, commonly called the ‘male
effect’, constitutes a major factor in the control of reproductive events in
ungulates, with physiological and ecological relevance and provides an original model for
studying the actions of olfactory cues.
The aim of our work was to assess the importance of learning in anestrous ewes’ responses to ram odor. To achieve this, we adopted two strategies. In experiment 1, we compared the behavioral and endocrine responses of females differing in sexual experience (naive or experienced) and age (young or naive). In experiment 2, we examined the capacity of a neutral conditioned stimulus (lavender odor) which had been previously associated with an adult male, to induce an LH increase.
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Materials and methods |
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Experiment 1
Animals
We used 49 Ile-de-France ewes in anestrus that differed in age and sexual experience:
young (1 year old) sexually naive ewes (n = 7); young (1 year old)
sexually experienced ewes (n = 19); adult (2–5 years old) sexually
naive ewes (n = 13); and adult (2–5 years old) sexually experienced
ewes (n = 10).
The young sexually experienced ewes were in contact with males for 2 weeks and only received male courtship but not mating. The adult sexually experienced ewes were multiparous. The two groups of sexually naive females were never previously exposed to males or their odors.
The females were housed by groups (four or five ewes per groups) in indoor pens which
had not previously contained rams, under a natural photoperiod. They were fed daily with
a constant diet of straw, maize, lucerne pellets and mineral supplements and had free
access to water. The ewes were diagnosed as seasonally anovulatory by persistent low
concentrations of circulating progesterone (<1 ng/ml) in weekly progesterone assays,
indicating the absence of a functional corpus luteum. These assays were performed with a
method adapted from
Terqui and Thimonier (1974).
Six sexually experienced adult, Ile-de-France rams, were used as stimuli. Fleece of 10 other Ile-de-France or Romanov rams and 10 Ile-de-France ewes was collected during the breeding season and stored at –20°C.
LH assay
Blood samples were centrifuged and plasmas were stored at –20°C.
Concentrations of LH were measured in duplicate samples of 100 µl plasma by the
radioimmunoassay (RIA) method of
Pelletier et al. (1968) as
modified by
Montgomery et al. (1985).
The sensitivity of the assay was 0.16 ± 0.05 ng/ml (four assays) standard
1051-CY-LH (i.e. 0.31 ng/ml NIH LH-S1). The intra-assay and inter-assay coefficients of
variation were 4.4 and 10.3%, respectively.
Behavioral data
For each stimulation, quantitative and qualitative data were recorded. During exposure
to the fleece, we recorded the number of olfactory investigations of the fleece, the
number of urine emissions, defecations, bleats, movements and the position of the animal
in the pen: immobile near or far from the fleece (Gelez and Fabre-Nys, 2004). During male stimulation, we
analysed both female and male sexual behaviors as previously described (Banks, 1964;
Fabre-Nys and Venier, 1987). We
recorded the number of male and female anogenital sniffs, male and female head sniffs,
male nudges followed by female immobilization, male nudges followed by female movements
and male mount attempts.
Experimental protocol
During the anestrous period, all females were isolated from males for at least 1 month
and were habituated to manipulation and bleeding during 1 week. They received a catheter
in the jugular vein that permits the collection of blood samples. Afterwards, the four
groups of females were randomly exposed to female fleece (control situation) or male
fleece, then to males. The stimulation consisted in introducing in the females’
pens an open box containing the fleece or a sexually active male. At least 2 or 3 days
separated each stimulation. For each stimulation, blood samples were collected every 15
min over 5 h. After 1 h, the fleece or the males were introduced in the females’
pens.
Experiment 2
Animals
We used 26 sexually naive young Ile-de-France ewes that were 10 months old at the
beginning of the experiment. Females were housed by groups in indoor pens and were fed
daily with a constant diet of straw, maize, lucerne pellets and mineral supplements and
had free access to water.
Behavioral data
As in experiment 1, quantitative and qualitative data were recorded: the number of
olfactory investigations of the fleece, urine emissions, defecations, bleats, movements
and the position of the animal in the pen: immobile near or far from the fleece.
Experimental protocol
During the breeding season, the ewes were placed for 2 weeks with: males scented
with lavender (MALELAV, n = 12); males not scented with
lavender (MALE, n = 7); or females scented with lavender (FEMLAV,
n = 7).
Each morning, the animals stimulus were perfumed with 200 ml of 1% lavender solution applied on the fleece. They then remained in contact with the females. The concentration of the lavender solution was chosen according to the results of preliminary trials in which six females were allowed to choose between a trough scented with lavender and containing food, a second empty unscented trough. Three concentrations of lavender solution were tested: 0.1, 1 and 10%. According to the results of the test choice, the concentration 1% was the concentration detected but not repulsive for ewes, and subsequently used.
After the 2 weeks of the odor conditioning procedure, all females were isolated from the males. Two months later, during the anestrous period, all females were habituated to manipulation and bleeding for 1 week. They received a catheter in the jugular vein. Afterwards, the three groups of ewes were randomly exposed to unscented female fleece or female fleece scented with 1% lavender solution. At least 2 or 3 days separated the two stimulus presentations. For each stimulation, blood samples were collected every 15 min over 5 h. After 1 h, an open box containing the fleece was introduced in the females’ pens.
Data analysis
Behavioral responses
For each group, the behavioral data were compared between the control situation
(exposure to female fleece) and the other stimulus conditions, and with the
non-parametric Wilcoxon test for related samples. For each stimulus, the behavioral data
were compared between groups with the Mann–Whitney U-test. Two-tailed
tests were used for all the analyses.
Endocrine responses
The increase of LH pulsatility was used to identify the female response (Martin et al., 1986). The pulses of LH
were defined as a rise of LH according to the following criteria established by
Goodman and Karsch (1980): (i) both
the increase and subsequent decrease in concentration had to exceed the sum of the assay
errors appropriate for the concentrations at the onset and the peak of the pulse; (ii)
the increase had to occupy no more than two sampling intervals and the decline had to
begin within two sampling intervals of attainment of the peak.
Ewes were considered as responsive to the stimulus if they presented an increased
frequency of LH pulses relative to the control situation (exposure to female fleece).
Proportions of responsive ewes were compared with the 
2 test.
The response latency corresponds to the interval between the stimulus presentation and the first LH pulse. The LH maximum was the highest LH level during the stimulation period. For each group, these three physiological parameters (number of pulses, response latency and LH maximum) were compared between the control situation and the other stimuli with the Wilcoxon test. These parameters were also compared using between groups Mann–Whitney U-test.
To assess the effect of age and sexual experience, we used a two factors analysis of variance (ANOVA).
One-tailed tests were used since preliminary data provide a basis for predicting an effect of sexual experience on endocrine responses. For all analyses, statistical significance was considered when P < 0.05.
All experimental procedures were performed in accordance with the local animal regulation (Authorization No. 006259 of the French Ministry of Agriculture, in accordance with ECC directive).
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
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Experiment 1
Response to male odor
Behavioral responses. In both groups of experienced ewes, the number of
olfactory investigations and the number of times they ‘ate’ the fleece were
significantly higher during exposure to the male fleece rather than the female fleece
(P < 0.05, Figure
1A). The naive adult ewes also
displayed a significantly higher number of olfactory investigations of the male fleece
(P < 0.05) whereas the young naive ewes smelled similarly the male and female
fleeces (Figure
1A).
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The sexually experienced ewes (young and adult) urinated significantly more during exposure to the male fleece than during exposure to the female fleece (P < 0.05, Figure 1B). This was not the case for the naive females, although the naive adult ewes tended to urinate more in the presence of the male fleece (P = 0.07, Figure 1B).
Other quantitative or qualitative behavioral data (bleats, movements, defecations, time spent near the fleece) did not significantly differ among two stimuli nor 4 groups of females.
Endocrine responses. The proportions of ewes exhibiting an increase of LH in response to the male odor differed significantly among four groups of females. The proportion of responsive females was significantly higher in experienced (24/29) than in naive ewes (8/20, P < 0.05, Table 1). The significant effect of experience was confirmed by the comparison of these proportions between groups of the same age (Table 1).
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Sexual experience had a significant effect on LH responses [F(4,25) = 4.15, P < 0.05]. The experienced ewes, regardless of their age, exhibited a significantly greater number of LH pulses during exposure to the male odor than during exposure to the female fleece (P < 0.05, Table 1). No significant increase of LH pulses was detected in naive females. Furthermore, the ram odor elicited a significantly higher number of LH pulses in the two groups of experienced ewes than in the groups of naive ewes (P < 0.05, Table 1). The response latency was also significantly shorter for the experienced ewes (P < 0.05, Table 1).
Response to male
Behavioral responses. The young ewes investigated the male significantly more
than did the experienced females (number of olfactory investigation of the male head or
anogenital part, P < 0.05, Figure
2A). The number of male nudges
followed by female avoidance was significantly higher in young than in adult ewes
(P < 0.05, Figure
2B). Experienced adults ewes remained
immobile following male nudges significantly more often than ewes of the three other
groups (P < 0.05, Figure
2B).
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Endocrine responses. The proportion of ewes exhibiting an increase of LH in response to males did not differ significantly among four groups of females. During exposure to males, the number of LH pulses, the response latency and the maximum concentration of LH did not differ significantly among four groups (Table 1).
For all groups of females the number of LH pulses and the maximum concentration of LH were significantly higher during exposure to males than during exposure to the female fleece (P < 0.05, Table 1).
The responses to the males and their fleece were also compared. In both groups of naive ewes, the actual male induced a significantly higher number of LH pulses than did the presentation of only male fleece (P < 0.05, Table 1). Furthermore, the naive females presented a significantly shorter response latency in the presence of males than in the presence of their fleece (P < 0.05, Table 1). In contrast, no differences were observed in experienced ewes responses to these two stimuli.
Experiment 2
Behavioral responses
All females of the MALELAV and MALE groups were stimulated by males during the
conditioning period in the breeding season. However, because of their young age, none of
them was receptive and accepted mating. Rather, they were only exposed to male courtship:
olfactory investigations, nudges and attempts to mount.
During the anestrous period, the females that have been previously exposed to lavender (MALELAV and FEMLAV groups) displayed significantly more olfactory investigations oriented to the scented than the unscented fleece (P < 0.05, Figure 3A). In contrast, the ewes of the MALE group investigated both fleeces in a similar manner. Only the MALELAV ewes tended to urinate more during exposure to the lavender scented fleece than in presence of the unscented fleece (P = 0.06, Figure 3B).
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Endocrine responses
The proportion of ewes exhibiting an increase of LH in response to the lavender odor differed significantly among three groups of females (P < 0.05, Table 2). The proportion of responsive females was significantly higher in the MALELAV group than in the MALE group (P < 0.05, Table 2). The proportion of responsive ewes did not differ between the MALELAV FEMLAV groups.
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The ewes of the MALELAV group showed a significantly greater number of LH pulses and a high LH maximum during exposure to the scented fleece than during exposure to the unscented fleece (P < 0.05, Table 2). No differences were found for the ewes of the FEMLAV and the MALE groups.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
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Our results show that a large proportion of sexually naive ewes, which have never previously been in contact with a male, do not exhibit an endocrine response during their first exposure to ram fleece. The fact that experienced ewes are more sensitive to the male odor demonstrates that sexual experience facilitates the response to this chemosignal. This markedly differs from other species. Indeed, in most mammals, the effects of olfactory cues on neuroendocrine secretions are independent of previous sexual experience and do not require learning mechanisms. The male odor accelerates sexual maturation in young females which have never been in contact with males, for example: mouse (Vandenbergh, 1969
); prairie
vole (Carter et al., 1980);
hamster (Reasner and Johnston, 1988);
and cow (Izard and Vandenbergh,
1982). Sexually naive males exhibit a reflexive increase of testosterone
during their first exposure to female urine or vaginal secretion, for example: mouse
(Maruniak and Bronson, 1976) and
hamster (Pfeiffer and Johnston,
1994). The male effect in sheep therefore constitutes the first demonstration
that the action of an olfactory message eliciting a physiological response, is
facilitated by previous experience.
The response to the ram odor may result in part from a reflex processes since some
naive females are able to exhibit an endocrine response. However, the facilitatory effect
of sexual experience indicates the involvement of more complex mechanisms. Our results
show that a neutral conditioned stimulus can mimic the effect of the ram odor, suggesting
that the LH response may be due to associative olfactory learning. It is possible that
ewes have to learn the association between their sexual partner and its odor to assign a
‘meaning’ to the male chemosignal. Similar conditioning paradigms have been
extensively used to reproduce behavioral changes induced by chemosignals. For example,
when mating occurs with female scented with an artificial odor, subsequent exposure to
this odor induces vocalizations by male mice (Nyby et al., 1978) and rats develop a preference
for sexual partner treated with this scent (Kippin and Pfaus, 2001a,b). In contrast, conditioned
endocrine responses are difficult to obtain (Keverne, 1986), and they have only been demonstrated in one
study.
Graham and Desjardins (1980) showed
that male rats exhibit an increase in circulating levels of LH and testosterone in
response to an artificial odor (methylsalicylate) which had been previously paired with a
receptive female during mating. An important difference between this work and ours is
that the young ewes in our experiments were not receptive during the conditioning
procedure and they did not accept mating. This same difference exists for other forms of
associative olfactory learning occurring in natural conditions. In female mice, the
memorization of the odor of the stud male at the time of mating leads to pregnancy block
when the female is subsequently exposed to urinary pheromones of a strange male
(Brennan and Keverne, 1997). In sheep,
learning the newborn lambs’ odor enables the mothers to recognize and accept
suckling only their own offspring (Lévy
et al., 1991). In these examples, learning processes are triggered
by the vaginocervical stimulation arising from either mating or parturition, resulting in
major synaptic changes in the olfactory bulbs (Kendrick et al., 1992;
Keverne et al., 1993;
Brennan et al., 1995). Our
results show that in the context of the male effect, sexual experience limited to
males’ courtship appears sufficient for responsiveness to the ram odor, suggesting
that vaginal stimulation is not indispensable to learn the meaning of the male olfactory
cue. What ewes exactly learn and associate during these incomplete sexual interactions
remains an open question.
In the presence of males, naive ewes exhibited an LH response similar to those of the experienced females. In our protocol, all ewes were first exposed to the male fleece then to males. It is possible that the first olfactory stimulation facilitated the subsequent response to males themselves. However, a more likely explanation is that males constitute a sufficiently powerful stimulation that does not require prior sexual experience.
In some species, the attractiveness of odor of the sexual partner is not dependent on
learning, for example: hamster (Johnston,
1974) and mouse (Jemiolo et
al., 1991;
Moncho-Bogani et al., 2002).
Our results show that the ram odor does not possess innate attractive properties, since
naive young ewes displayed similar olfactory investigations of both male and female
fleeces. However, the naive adult ewes smelled the male fleece significantly more than
the female fleece. This result may be explained by the past experience of the females.
The naive adult ewes were housed with several groups of conspecifics and had been in
contact with the odors of numerous different females. Thus, they had a greater
‘social experience’ than the young naive ewes that only encountered the
females of their living group. Therefore, for the naive adult ewes that are habituated to
meet unfamiliar female odors, the male fleece may be perceived as a really novel odor
eliciting a particular interest. In contrast, for the young females, both fleeces may
represent novel odors. The difference between young and adult naive females may also be
due to different emotional and/or attentive state. In previous work, we showed that naive
adult ewes acquired a level of proceptivity (corresponding to the time spent in
interaction with males in a test choice) similar to that of experienced adults, more
rapidly than young ewes (Gelez et al.,
2004a). The young ewes did not exhibit lower learning capacity than adult
females, but higher levels of stress that may explain their difficulty in focusing their
attention on males (Gelez et al.,
2004a). In anestrous young ewes, a similar reaction might occur during
exposure to the male fleece and could mask the attractiveness of this cue. This
explanation may also apply to the endocrine responses. Only the ewes exhibiting a low
level of stress during exposure to the male fleece might present an endocrine response,
and the facilitative action of sexual experience could result in a lower stress response
to the olfactory cue.
In contrast to to naive females, the experienced ewes urinated more during exposure
to the ram fleece than during exposure to the female fleece. Furthermore, the MALELAV
females that have been previously exposed to males perfumed with lavender, urinated more
in presence of the scented than the unscented fleece. These results suggest that the
emission of urine is not a pre-programmed response but rather a response to an identified
stimulus. The emission of urine in the presence of the ram or the lavender odor suggests
that the females learned the association between the ram and its odor or between the ram
and the artificial odor. In ungulates, the emission of urine by females is frequent
during sexual interactions and is commonly followed by male flehmen (Banks, 1964;
Ladewig et al., 1980). In
most breeds, the females urinate more in response to male courtship when they are in
anestrus rather than in estrus (Stevens et
al., 1982;
Bland and Jubilan, 1987). In this
manner, females may signal to the males their physiological state since rams are able to
distinguish between urine of anestrous and estrous females (Blissitt et al., 1990). In another breed of sheep
(Romanov) and in goats, however, females urinate more in the presence of males when they
are in estrus (Fabre-Nys, personal observation). This behavior can serve to attract males
and stimulate their sexual arousal, and may considered a sign of proceptivity similar
vaginal marking by females hamster (Johnston,
1979). This same explanation is not applicable to our results since in the
context of the male effect, ewes are in anestrus. The exact significance of female urine
emission remains therefore unclear.
The involvement of learning processes in both endocrine and behavioral responses to
the ram odor may related to the neural mechanisms mediating detection and integration of
this chemosignal and the respective roles of both olfactory systems. In rodents, the
neural pathway supporting the action of olfactory cues inducing neuroendocrine changes,
involve direct connections with a limited number of synapses between the accessory
olfactory bulb and the hypothalamic structures (Keverne, 1983;
Brennan and Keverne, 1997). This
pathway that bypasses cognitive centers of the brain, like the cortical areas, may
account for pre-programmed and stereotyped responses. In contrast, the ram odor acts
primarily through the main olfactory system: the destruction of the olfactory epithelium
or the inactivation of the cortical amygdala, first relay of the main olfactory bulb,
completely blocks the LH response to male odor (Gelez et al., 2004b;
Gelez and Fabre-Nys, 2004). The
demonstration of learning processes is consistent with the preponderant role of the main
olfactory system in the action of the ram odor, since cortical structures belonging to
this pathway can proceed to an elaborate cognitive processing of the olfactory message.
It is interesting to note that all other chemosignals that are integrated by the main
olfactory system and require learning mechanisms, concern only behavioral responses, for
example: pig (Dorries et al.,
1997) and ferret (Kelliher et
al., 1998). In comparison, the ram odor constitutes an original model of
action of a primer pheromone. This may correspond to a strategy of reproduction to adapt
efficiently the ewes’ endocrine state to their changing environmental conditions,
since in artiodactyls contrary to laboratory rodents, the risk of predation accentuates
the importance of the reproductive events synchronization between sexual partners.
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Acknowledgements |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
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The authors thank Richard Porter for his correction of English and his valuable comments on the manuscript and Odile Moulin for her help with the illustrations.
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TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
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Accepted May 2, 2004
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