Parity of female goats does not influence their estrous and ovulatory responses to the male effect.

The objective of the present study was to determine whether parity is a factor that influences the estrous and ovulatory responses of female goats when they are stimulated by males that show increased sexual activity. To stimulate sexual activity, four adult male goats were subjected to photoperiodic treatment for 2.5 months comprising long days, with the treatment commencing on 1 November. On 14 April at 1,900 h, a group of multiparous females (n=21) and a group of 16 months-old nulliparous females (n=19) were exposed to four bucks (two per group) for 15 days. Throughout the study period, the estrous behavior of these female goats was detected twice on a daily basis. Ovulations of the female goats were determined by ecography on days 7 and 18 after exposure to males. The sexual behavior of males was recorded twice every day from 0800 to 0900 h and from 1730 to 1,830 h during the first 4 days after introduction in the pen of females. The total cumulative proportion of multiparous females that had ovulations (100%) and displayed estrous behavior (100%) during the 15 days of exposure to males did not differ (P>0.05) from that of nulliparous females (100% and 95%, respectively). The interval between introduction of males and onset of estrous behavior did not differ (P>0.05) between multiparous (1.9+/-0.1 days) and nulliparous (1.7+/-0.2 days) females. The proportion of females displaying a short estrous cycle was greater (P<0.05) in multiparous (13/21, 62%) than in nulliparous (5/19, 26%) females. Duration of these shorter than typical estrous cycles did not differ (P>0.05) between groups (multiparous: 5.2+/-0.3 days, nulliparous: 4.5+/-0.1 days). The number of anogenital sniffings was greater (P<0.001) in males exposed to nulliparous than in those exposed to multiparous females. In contrast, the number of mounting attempts was greater (P<0.01) in males that were introduced to multiparous than in those that were introduced to nulliparous does. The number of flehmen, nudging, self-marking with urine, and mounts was not different (P>0.05) between males that were in contact with multiparous and nulliparous females. These results indicate that regardless of parity, female goats respond to male introduction if they are stimulated by males that were previously exposed to artificial long days to increase their sexual behavior.

Sexual behavior in ewes and other domestic ruminants.

Similarities as well as differences across species in the control of sexual behavior are helping to fully understand the subtle relations between physiology and eco-ethological constraints and how the brain integrates such information. We will illustrate this with sexual behavior in domestic ruminants and especially ewes. Females of these species like humans, but unlike rodents, have a long luteal phase. A prolonged exposure to progesterone (Pg) before the preovulatory estradiol rise is necessary for estrous behavior to be displayed. Estradiol action and receptor localization is very similar to that observed in other species. But not too surprisingly, the role of Pg is rather different with a priming effect not observed in rodents. However, as in rodents, Pg also has an inhibitory effect, is necessary for the display of proceptivity and is responsible for the timing of the different periovulatory events. These steroids act on the central nervous system in similar areas across mammalian species to regulate estrous behavior. Steroid fluctuations during the estrous cycle cause changes in catecholaminergic activity in the hypothalamus. Interestingly, these neurotransmitters seem to have very similar effects in ewes and rats as illustrated by the norepinephrine rise after male-female interactions observed in both species. Similar comparisons can be made regarding the action of some neuropeptides, including oxytocin and GnRH, and more integrative processes like sexual differentiation and modulation of reproduction by social interactions. Data on sheep, goats and cows will be compared with those of rodents.

Neural pathways involved in the endocrine response of anestrous ewes to the male or its odor.

During the non-breeding season, anestrous ewes do not experience ovarian cycles but exposure to a ram or its odor results in the activation of the luteinizing hormone secretion leading to ovulation. The aim of our work was to identify the neural pathways involved in this phenomenon. Using Fos immunocytochemistry, we examined the brain areas activated by the male or its fleece, in comparison with ewes exposed to the female fleece or the testing room (control group). In comparison with the control group, the male or its odor significantly increases Fos neuronal expression in the main and accessory olfactory bulbs, anterior olfactory nucleus, cortical and basal amygdala, dentate gyrus, ventromedial nucleus of the hypothalamus, piriform and orbitofrontal cortices. The main olfactory bulb, the cortical amygdala and the dentate gyrus are specifically more activated by the male odor than the female odor. Using a procedure of double labeling for Fos and gonadotropin-releasing hormone, we also compared the number of gonadotropin-releasing hormone neurons activated in the four groups of females. The male or its odor significantly increases the number and the proportion of gonadotropin-releasing hormone cells expressing Fos-immunoreactivity in the preoptic area and the organum vasculosum of the lamina terminalis, whereas no such induction of Fos-immunoreactivity was found in gonadotropin-releasing hormone neurons of ewes exposed to the female odor or the testing room. These findings emphasize the role of the main olfactory system in the detection and the integration of the ram odor, and also suggest the participation of the accessory olfactory system. Numerous structures widely distributed seem involved in the processing of the male olfactory cue to reach the gonadotropin-releasing hormone neurons.

Importance of learning in the response of ewes to male odor.

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.

The "male effect" in sheep and goats: a review of the respective roles of the two olfactory systems.

In sheep and goats, exposure of seasonally anestrous females to sexually active males results in activation of luteinizing hormone (LH) secretion and synchronized ovulation. This phenomenon is named "the male effect" and seems to constitute a major factor in the control of reproductive events. This effect depends mostly on olfactory cues and is largely mimicked by exposure to male fleece only. In sheep, preventing the vomeronasal organ (VNO) from functioning does not affect the female responses to male odor suggesting that, unlike in rodents, the accessory olfactory system does not play the major role in the perception of this pheromonal cue. Female responses also seem to depend on previous experience, an effect that is not common for pheromones and renders this model of special interest. The aim of the present report is to summarize our current knowledge concerning the "male effect" and in particular to clarify the respective roles of the two olfactory systems in the processes involved in this effect.

Inactivation of the olfactory amygdala prevents the endocrine response to male odour in anoestrus ewes.

Our aim was to study the role of the olfactory amygdala (medial and cortical nuclei) and the ventromedial nucleus of the hypothalamus (VMN) in the ability of the male odour or live males to induce a release of luteinizing hormone in anoestrus ewes. To achieve this, we temporarily blocked the activity of these structures by localized retrodialysis administration of the anaesthetic lidocaine. The effect of ram odour on the secretion of luteinizing hormone was completely blocked by inactivation of the cortical nucleus of the amygdala. In contrast, inactivation of part of the accessory olfactory system (the medial nucleus of the amygdala or the VMN) had no effect. In the presence of the male, lidocaine never impaired the endocrine response of the ewes. These results show that modulation of reproduction by the sexual partner even through pheromonal cues does not occur via the direct circuit of the accessory system. On the contrary, the cortical nucleus of the amygdala is absolutely necessary for the treatment of and/or the response to the male olfactory signal but this structure can be bypassed when other sensory cues are available.

Role of experience in the neuroendocrine control of ewes' sexual behavior.

We assessed the role of learning in the expression of female sexual behavior and evaluated the relative importance of age versus experience. Two studies were conducted with ovariectomized ewes submitted to steroid treatment that mimicked an estrus cycle. We compared behavioral (experiments 1 and 2), neurochemical (experiment 1), and endocrine (experiment 2) responses of sexually naive young and adult ewes versus sexually experienced adults when exposed to males. In a third study, we compared their performance in an instrumental learning test and the extent to which it was affected by stress. These experiments showed that proceptivity is affected both by age and sexual experience. In experiment 1 only experienced adults were proceptive and displayed an increase in hypothalamic norepinephrine. By the second estrus cycle (experiment 2) naive adults performed similarly to experienced adults but proceptive behavior was still inferior in young ewes. Receptivity was also different between groups but affected more by age than by sexual experience. All ewes mated during the first interaction with a male, although males' latency to ejaculation was shorter with experienced females than naive adults or naive young. Young ewes found food as readily as adults in experiment 3 but were more affected by stress. Together, these experiments show that both experience and age influence sexual activity and that sensitivity to stress may also be involved. This may contribute to the deficient reproductive performance that is often observed in young female mammals.