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Facial expressions are an increasingly used tool to assess emotional experience and affective state during experimental procedures in animal models. Previous studies have successfully related specific facial features with different positive and negative valence situations, most notably in relation to pain. However, characterizing and interpreting such expressions remains a major challenge. We identified seven easily visualizable facial parameters on mouse profiles, accounting for changes in eye, ear, mouth, snout and face orientation. We monitored their relative position on the face across time and throughout sequences of positive and aversive gustatory and somatosensory stimuli in freely moving mice. Facial parameters successfully captured response profiles to each stimulus and reflected spontaneous movements in response to stimulus valence, as well as contextual elements such as habituation. Notably, eye opening was increased by palatable tastants and innocuous touch, while this parameter was reduced by tasting a bitter solution and by painful stimuli. Mouse ear posture appears to convey a large part of emotional information. Facial expressions accurately depicted welfare and affective state in a time-sensitive manner, successfully correlating time-dependent stimulation. This study is the first to delineate rodent facial expression features in multiple positive valence situations, including in relation to affective touch. We suggest using this facial expression assay might provide mechanistic insights into emotional expression and improve the translational value of experimental studies in rodents on pain and other states.

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In classical rodent anxiety models, females usually display lower anxiety than males, whereas anxiety disorders are more prevalent in women. Perhaps this contradiction is caused by the use of behavioural models with low external validity. Therefore, we analysed immediate reactions to a sudden 90-dB white noise in a semi-natural environment. We observed mixed-sex groups of rats for the 60 seconds preceding noise onset and the first 60 seconds of exposure. White noise elicited fear-specific behaviours hiding alone and huddling. It also increased exploratory and ambulatory behaviours, although only in the burrow zone farthest from the open area. Thus, in a semi-natural environment, white noise enhanced motor activity as a product of fear-induced general arousal. Then, we compared male and female sexual, social, exploratory and anxiety-related behaviour, and found little sex difference. This absence of behavioural effect, also observed in other studies, might be a result of our study design, a familiar environment with an ecologically relevant social context. Fear and anxiety responses are modulated by oestrogens through the activation of oestrogen receptors α and ß. Thus, in a third part of out study, we analysed how treatment with either oil, oestradiol benzoate (EB), an agonist to the oestrogen receptor α (propylpyrazoletriol [PPT]) or ß (diarylpropionitrile [DPN]) influenced female behaviour. The effect of treatment was limited, both EB and PPT stimulated motor activity in the open area before white noise, probably because of sexual activity. PPT increased the probability of fleeing from the noise, and decreased the latency to do so, which is consistent with a pattern of anxiogenic properties found in previous studies. Contrary to reports in classical procedures, we failed to detect any effect of DPN on immediate fear reactions in a semi-natural environment.

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Gonadally intact female rats display sexual behaviors only during a portion of the estrus cycle. In standard experimental setups, the on- and offset of sexual behavior is gradual. However, in naturalistic settings, it is almost instantaneous. We assessed the changes in sociosexual behaviors at the beginning and end of behavioral estrus in ovariectomized females treated with ovarian hormones. Rats were housed in a seminatural environment, in groups of three males and four females. We scored female and male behavior during the 8 min preceding and following the first and last lordosis of behavioral estrus. Immediately before the first lordosis, there was a sharp increase in female paracopulatory behaviors whereas the end of estrus was marked by a sudden decrease in these behaviors. There was no systematic change in other female behavior patterns. These data suggest that the display of female paracopulatory behaviors plays a key role. Both during transition into and out of behavioral estrus, most behavioral changes occurred within one minute. The rapid changes must be unrelated to ovarian hormone fluctuations in these ovariectomized females. Perhaps they can be explained in terms of hormone-induced, dynamic (chaotic) changes in the function of critical structures within the brain.

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Sexual behavior is activated by motivation. An overwhelming majority of experimental studies of the intricacies of sexual motivation has been performed in rodents, most of them in rats. Sometimes it is desirable to generalize results obtained in this species to other species, particularly the human. It is hoped that studies of the neurobiology of rodent sexual behavior may shed light on the central nervous mechanisms operating in the human, and the search for efficient pharmacological treatments of human sexual dysfunctions relies partly on studies performed in rodents. Then the issue of generalizability of the rodent data to the human becomes crucial. We emphasize the importance of distinguishing between copulatory acts, behavior involving the genitals, and the preceding event, the establishment of physical contact with a potential mate. Comparisons between the structure of copulatory behavior in rats and humans show abysmal differences, but there may be some similarity in the underlying mechanisms. The endocrine control of sex behavior is shortly mentioned, and we also compare the effects of the few drugs known to affect both rodent and human copulatory behavior. The stimuli activating sexual motivation, often called desire in the human literature, are examined, and the sexual approach behaviors in rats and humans are compared. There is a striking similarity between these species in how these behaviors respond to drugs. It is then shown that the intensity of sexual approach is unrelated to the intensity of copulatory behavior. Even though the approach is a requisite for copulation, an activity that requires at least two individuals in close physical contact, these two aspects of sexuality do not covary. This is similar to the role of the testosterone in men and male rats: although the hormone is needed for sex behavior, there is no correlation between serum testosterone concentration and the intensity of copulation. It is also pointed out that human sexual behavior is mostly determined by social conventions, whereas this is not the case in rats and other rodents. It is concluded that some observations in rats can be generalized to the human, but extreme caution must be exercised.

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Estrogens receptors (ER) are involved in several sociosexual behaviors and fear responses. In particular, the ERα is important for sexual behaviors, whereas ERß modulates anxiolytic responses. Using shRNA directed either against the ERα or the ERß RNAs (or containing luciferase control) encoded within an adeno-associated viral vector, we silenced these receptors in the ventromedial nucleus of the hypothalamus (VMN) and the central amygdala (CeA). We exposed ovariectomized female rats, sequentially treated with estradiol benzoate and progesterone, to five stimuli, previously reported to elicit positive and negative affect. The subjects were housed in groups of 4 females and 3 males in a seminatural environment for several days before hormone treatment. We analyzed the frequency of a large number of behavior patterns. In addition, we performed analyses of co-occurrence in order to detect changes in the structure of behavior after infusion of the vectors. Silencing the ERα in the VMN disrupted lordosis and showed some anxiolytic properties in aversive situations, whereas silencing of the ERß in this structure had no effect. This was also the case after silencing the ERα in the CeA. Silencing of the ERß in this structure increased risk assessment, an expression of anxiety, and increased olfactory exploration of the environment. We hypothesize that the ERß in the CeA has an important role in the well-established anxiolytic effects of estrogens, and that it may modulate arousal level. Furthermore, it seems that the ERα in the VMN is anxiogenic in aversive or threatening situations, in agreement with other studies.

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The behavioral effects of putative anxiolytic and anxiogenic drugs are usually evaluated in highly standardized tests. Here, we determined the effects of such drugs in rats housed in mixed sex groups in a seminatural environment. Sexually receptive female Wistar rats were treated with either the anxiolytic drug chlordiazepoxide (2 mg/kg), the anxiogenic drug yohimbine (1 mg/kg), or saline (1 ml/kg). Different emotional challenges eliciting purportedly positive affect (lavender odor, Mozart's music, chocolate flavored food) or negative affect (white noise, fox odor) were then introduced into the seminatural environment. A co-occurrence analysis revealed that music was rather aversive to the rats, as were white noise and fox odor. Lavender and chocolate exposure decreased classical indicators of fear. White noise suppressed sexual behaviors and caused avoidance of the open area. Yohimbine increased sexual receptivity during lavender exposure, decreased the latency to flee the white noise, and increased self-grooming regardless of the emotional challenge. Chlordiazepoxide was effective only during exposure to white noise, and increased the frequency of hiding alone. The modest effects of the drugs in the seminatural environment may be the result of social buffering and rats experiencing a high degree of controllability over their environment.

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Estrogen receptors (ERs) are involved in sexual as well as non-sexual behaviors. In the present study we assessed the effects of stimuli inducing positive or negative affect on sociosexual, exploratory and fear-related behaviors of female rats housed in groups (4 females, 3 males) in a seminatural environment. Ovariectomized females were treated with oil, 17ß­estradiol benzoate (EB, 18 µg/kg), the ERα agonist propylpyrazoletriol (PPT), or the ERß agonist diarylpropionitrile (DPN) (both 2 × 10 mg/rat). On the test day, the females were exposed to a sequence of events consisting of lavender odor, Mozart's Sonata for Two Pianos K448, chocolate pellets, white noise and fox odor (2,3,5­Trimethyl­3­thiazoline, TMT). All these events are known to induce positive or negative affect. Behavior was carefully observed from the video record. White noise suppressed sexual behaviors and reduced the time spent in the open area of the environment. TMT had no consistent effect whereas exposure to music caused avoidance of the open area. Exposure to chocolate increased exploratory and social behavior. Lavender odor enhanced exploratory behavior. PPT and EB stimulated sexual behaviors, whereas DPN was ineffective. Co-occurrence analyses of the sequence of behavioral patterns revealed that PPT and EB consistently belonged to clusters different from oil and DPN, whereas DPN was separate from oil only under fear-inducing experimental conditions. These data, from a procedure with external validity, confirm that the ERα is crucial for sexual behaviors, that these behaviors are reduced under stressful conditions, and that the ERß may have some role in fear-related behaviors.

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Sexual attraction has two components: Emission of sexually attractive stimuli and responsiveness to these stimuli. In rodents, olfactory stimuli are necessary but not sufficient for attraction. We argue that body odors are far superior to odors from excreta (urine, feces) as sexual attractants. Body odors are produced by sebaceous glands all over the body surface and in specialized glands. In primates, visual stimuli, for example the sexual skin, are more important than olfactory. The role of gonadal hormones for the production of and responsiveness to odorants is well established. Both the androgen and the estrogen receptor α are important in male as well as in female rodents. Also in primates, gonadal hormones are necessary for the responsiveness to sexual attractants. In males, the androgen receptor is sufficient for sustaining responsiveness. In female non-human primates, estrogens are needed, whereas androgens seem to contribute to responsiveness in women.

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Female mate choice is often investigated in terms of reproductive success in order to understand how male characteristics contribute to sexual attractiveness. Previous studies have found that females rats prefer mating with their first encounter rather than males visited subsequently, suggesting that the rewarding value of this first encounter is enough to reinforce mating with the first partner. Using a multiple chambers paradigm, we allowed female rats to copulate freely with three males placed each in a different chamber. Then, we switched the males' position, and let the female interact with them freely again within the same session. We tested whether female mate choice was relying rather on a preferred male rat or on a preferred mating location. The results showed that females spent most time with the male in the chamber of 1st entry in the beginning, but as soon as male rats switched chambers, the female rat continued to copulate with the new male in the same chamber of 1st entry, instead of mating with her previously preferred male rat. This suggests that the male preference is an artefact of location preference. Therefore, female mate choice seems to be rather random than the consequence of an individual choice based on male characteristics. This finding, although contradictory with the intuitive feeling that mate choice is a crucial feature in sexual and reproductive behavior, is supported by several recent observations. In the coming years, behavioral neuroscience should bring light to the brain processes at work in random mate choice.

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