The role of ovarian hormones in nonprimate female mammals

All those interested in non-human sexual behavior and particularly those interested in the sexual behavior of rodents have noticed that females are not like males. While one of the main attributes of the male character is its constancy, females are highly unstable. This is evident in, for example, female rats. One day, a female may display intense hopping, darting and ear wiggling as soon as approached by a male, and his tender mounts activate the most beautiful of lordoses. Twelve hours later, the same female may abstain from all reactions to the male's approaches, and if he would dare to mount he would be kicked in his face with a back paw. If he didn't understand the message but continued to mount, it is most likely that the female would turn on her back and push the male away with all four paws. If that did not put him off, the female would not hesitate to bite. Four or five days later, the female will again display hopping, darting, ear wiggling and lordosis in response to the male while all rejective behaviors will be suppressed. Such rapid and extremely systematic variations in the female's propensity to engage in sexual interactions and the associated changes in response to the male's approaches contrast dramatically to the male rat's behavior. He will try to copulate with any female at any time from puberty until well into old age and he systematically responds to a female's invitation with cordiality and enthusiasm. One rare exception might occur if the male were already sexually exhausted. Then he would probably respond with indifference. Misbehaviors like biting are, however, extremely unlikely.

The causes of the systematic variations in female sexual behavior have intrigued scientists, and probably also laymen, for a very long time. However, it was not until the 1920s that experimental studies of the physiological underpinnings of female sexual behavior became popular. In a classic paper, Long and Evans (1922) described not only the regular variation in female rat sexual behavior, but also the equally regular changes in vaginal cytology. Both these events were soon found to depend on secretions from the ovaries (Allen and Doisy, 1923). The Danish endocrinologist, Axel Hemmingsen, published a splendid, detailed study of the behavioral and physiological effects of ovarian, more precisely follicular, hormones in 1933. When he began his research in rats and mice in 1924, the chemical structure of the follicular hormones was unknown. At that time the hormones were normally obtained from follicular extracts and the active material that was isolated from such extracts was called oestrin. In order to evaluate carefully the actions of oestrin on female sexual responses, Hemmingsen devised a set of behavioral criteria for determining the intensity of these responses. The lowest intensity was described in the following way:

The female runs away from the male, defends herself violently with one of the hind legs, or rises breast to breast to the male, or rolls on her back, or rises her hind legs, making mounting impossible. Quivering of the ears is entirely absent (Hemmingsen, 1933, p. 119).

This is a very poetic description of what we now would consider behaviors typical of a non-receptive female. An intermediate intensity of sexual behavior was described in this way: 'When mounted, the female shows both lordosis and quivering of the ears'. A slightly more intense reaction to the male occurs when: 'quivering of the ears is provoked by the male smelling at the vagina, but not by the mere presence of a male'. The highest level of sexual excitability was expressed as:

spontaneous quivering of the ears (perhaps also the darting movements?) is seen even if there are only other normal females present (perhaps also if the female is alone?) (Hemmingsen, 1933, p. 123).

These behavioral criteria for quantifying the intensity of sexual behavior, and the magnitude of the oestrin effect, were based on careful cinematographic analyses of female rat sexual behavior. More than 70 years after its publication in a rather obscure journal, it is a real intellectual treat to read this brilliant paper. I have made this rather extensive mention of it only to pay tribute to an almost forgotten pioneer in the field of behavioral endocrinology.

The crucial role of follicular hormones for female sexual behavior is not limited to rats and mice. I will not review the huge amount of data that has been accumulated over the years, but it appears to be quite obvious that these hormones are necessary for the display of sexual behavior in most mammals. Possible exceptions include some primates, like the human, as we will see in a couple of paragraphs. However, follicular hormones are not the only ovarian products that are involved in female sexual behavior. Although the follicular hormones, i.e. estradiol, estrone or estriol, can activate complete female rat sexual behavior if administered in doses large enough, the addition of a small dose of progesterone renders a small, otherwise ineffective, dose of estradiol capable of activating all aspects of sex behavior (Beach, 1942b). In rats, estrogens usually need to be administered at least 24 hours before progesterone in order for the latter hormone to be effective. It is now known that estrogens activate the gene coding for the progesterone receptor, something resulting in a huge increase in the number of cytosolic progesterone receptors (see, for example, Scott et al., 2002 and references therein). I will not describe the molecular actions of estrogens, or of progesterone, but it can be interesting to remember that the sequential actions of estrogens and progesterone appear to be important for female sexual behavior in many rodents. In other mammals, for example the ewe, the most efficient order of hormone administration is the reverse. If progesterone is given for a few days before estrogen treatment, then the estrogen dose needed to induce receptivity is reduced (Robinson, 1954, 1955; Caraty et al., 2002). The molecular mechanisms underlying this are not known. In other species, female sexual behaviors are activated exclusively by estradiol and progesterone may have an inhibitory rather than facilitatory action. This is the case in rabbits and cats, for example (Michael and Scott, 1964; Beyer et al., 1969; Beyer and McDonald, 1973). Thus, it is quite important to keep in mind that the hormone treatment regimen most efficient in rats is not necessarily so in females of other mammalian species.

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