A sexually receptive female rat will quietly approach a male and within a rather short distance of him (about one body length) she will turn away and make a short, fast run and then suddenly stop with her hind quarters raised. This behavior pattern is called solicitation (McClintock et al., 1982; McClintock and Anisko, 1982). It is a very important part of the female's copulatory behavior in seminatural conditions, like those used by Martha McClintock in her very elegant studies. A most interesting observation is that more than 90% of sexual interactions are initiated by a female solicitation (McClintock and Adler, 1978). The male initiated only 3% of the interactions. In the remaining 7% it was unclear who the initiator was. This is true not only for the initial mounting episode, but also for the entire sequence of mounts with and without intromissions leading to ejaculation. It appears, then, that the female is in control of the pace of copulatory interactions from the first mount until the end of copulation, in addition to being in control of the initiation of copu-latory behavior. I occasionally give talks on sex behavior to lay audiences and in these talks I find it amusing to emphasize this fact. It is not unusual that a male listener spontaneously and loudly remarks that it is not only among rats that the female is in command.
In the standard mating test arena there is not room enough for the female to display solicitation behavior and she loses most of her control of the copulatory interaction. This is very important to remember, because most studies of female rat sexual behavior have been performed in small arenas. In small arenas, where there is no way for the female to run away from the male, it appears that the male controls the interaction. Under these circumstances, the female's behavior is limited to responding to the male's mounts with lordosis, a concave dorsiflexion associated with raised hindquarters. This is achieved by extension of the hind legs. Simultaneously, the tail is turned sideward. The resulting body posture exposes the vaginal opening and makes it possible for the male to achieve intromission. In addition to lordosis, the female may respond to the male's approaches with short runs followed by a sudden stop, or she may even make short hops. These behaviors are identical to parts of the solicitation behavior described above. What is usually missing in small spaces is the initial approach to the male and the turning away from him at some distance. Nevertheless, the short runs and hops, called darting or hop-darting in the scientific literature, are frequently confounded with and used as synonyms for the entire sequence of solicitation. Another frequent behavior displayed by the female is ear wiggling. She is, in reality, not wiggling the ears but shaking and turning the head at a rather high frequency (Pfaff et al., 1973). To the human observer it looks like she wiggles her ears, therefore the name given to the behavior. Ear wiggling is often associated with hop-darting, but may also occur independently of this behavior. All three behaviors were termed proceptive in a classic 1976 paper by Frank Beach (Beach, 1976) and that name has been universally used ever since.
A female displaying lordosis in response to a male's mount or an experimenter's fingers is said to be sexually receptive. A huge amount of data has established that the display of lordosis is dependent on ovarian hormones. It would not be unreasonable to pose that, for all practical and scientific purposes, it is absolutely hormone-dependent. Furthermore, in 1958, it was shown that the ovarian hormones act in the brain when predisposing the female for the behavior. George Harris and Richard Michael implanted minute amounts of estrogen into the hypothalamus of ovariec-tomized cats and found that the implanted females responded with lordosis to a male's mounts while control females did not (Harris et al., 1958). They also presented data showing that the hormone had not leaked out from the site of implantation to the circulation (Harris and Michael, 1964). The unequivocal conclusion was that ovarian hormones act within the brain to predispose the female for displaying lordosis in response to mount. This was the first clear-cut demonstration of a central nervous action of hormones in the control of a complex behavior. Data from rabbits (Davidson and Sawyer, 1961) and ewes (Signoret, 1970) soon confirmed that lordosis and sexual receptivity are under the control of estrogens acting in the hypothalamus. The fact that lordosis is a behavior controlled by hormones acting in the brain has made it attractive for those interested in central nervous hormone actions. In the early 1970s, Don Pfaff at the Rockefeller University in New York set out on a series of brilliant studies aiming at a careful description of the lordosis in female rats. He analyzed the stimulus control and found that tactile stimulation of the flanks and perineal region triggered lordosis. He employed electrophysiological techniques in order to determine the sensory pathways involved in the transmission of the tactile stimulation, determined the exact brain sites for estrogen actions and described the pathways for the output from these sites to the muscles in the back underlying the lordosis posture. Summaries, some pretty extensive, of this extraordinary work have been published at irregular intervals and I strongly encourage readers to treat themselves to the intellectual delight provoked by reading these (Pfaff et al., 1973; Pfaff, 1980, 1999). That the processes underlying lordosis in rats are not unique for this species has been demonstrated in a series of studies in cats (van der Horst and Holstege, 1998). Here, I will not give any detailed picture of the intricacies of lordosis. It is sufficient to mention that one or another kind of lordosis posture as a fundamental element of copulatory behaviors is widespread among female mammals. A comparative analysis of lordosis among rodents was published many years ago by Don Dewsbury (Diakow and Dewsbury, 1978) and it is still unsurpassed in its clarity of description, although some teleology has infiltrated the conclusions.
Lordosis is not a major component of copulatory behavior in women. In fact, it is not a component at all. Likewise, some ungulates like the ewe does not display lordosis in response to male mounts. A sexually receptive ewe displays an extremely quiet copulatory behavior. She just stands still when the male mounts. When non-receptive, ewes always run away from the male and he never gets an opportunity to perform a mount. The point I would like to make here is that, although the stimulus control as well as the endocrine mechanisms and the brain sites crucial for lordosis are well known, this knowledge may not be of vast usefulness when we want to talk about copulatory behavior in women and perhaps not even when our interest is focused on some species where lordosis is not part of female copulatory behavior.
Lordosis is not the only behavior characteristic of a sexually receptive female rat. I already mentioned that the female controls the pace of sexual interaction when given the opportunity to do so. This opportunity is, as I also mentioned, lost in small spaces like those habitually employed in the laboratory. Observations of sexual interaction among wild rats in natural environments, for example garbage deposits, have shown that a receptive female is pursued by a band of male rats. One of the pursuing males may suddenly be the object of a female solicitation, which normally is followed by a mount with or without intromission/ejaculation. After such an interaction the female frequently makes herself unavailable for the pursuing males in some way or another, for example by disappearing in a burrow (Steiniger, 1950; Calhoun, 1962; Robitaille and Bouvet, 1976). The males will wait outside until the female comes out again. Another copulatory interaction will take place and the female will again disappear for a while. This appears to go on until the female's sexual receptivity vanishes.
A situation similar to the wild can easily be created in the laboratory. All that is needed is an observation arena arranged so that there is a section to which only the female has access. One solution is to put an elevated platform somewhere in the arena to which the female has free access while the male is prevented from acceding to it. Another is to tether the male in one corner while the female is left free to move around. A third is to introduce a physical barrier dividing the arena. If the barrier has an opening and if the female is smaller than the male, then the opening can be adjusted so that only the female can pass. The bigger male gets stuck if he tries to penetrate the opening. In all these arrangements, the female is guaranteed to be able to escape from the male whenever she likes. At the same time, the male is always accessible in case the female would like to return to him. In situations of this kind, it is typical to see the female approach the male, who rapidly mounts with or without intromission. Now and then the female disappears to her private area. She soon returns, there is another mount with or without intromission, the female escapes again, she returns after a while, there is another mount with or without intromission, and so on. This come-and-go behavior on the female's part is called pacing. Paced mating tests have become rather popular and quite a lot is known about the factors controlling the female's behavior. Paramount among these factors is the amount of sensory sexual stimulation received by the female. After a mount without intromission, it is rather unusual for the female to escape. In fact, the probability of escape is no larger than it would have been if no sexual interaction had occurred (Ellingsen and Agmo, 2004). After a mount with intromission it is more likely that the female escapes and after an ejaculation she almost always escapes. If sensory feedback from the vagina is eliminated by section of the pudendal and pelvic nerves, then there is no difference between a mount with and without intromission and there is no difference between an intromission and an ejaculation (Erskine, 1992).
Besides determining the probability of female escape, the amount of sensory stimulation also determines the duration of the female's escapes. In the case of escape after a mount, she will return very fast. If she escaped after an intromission, she will take some more time before returning. The longest absence follows an ejaculation. The proportion of mounts with and without intromission/ejaculation followed by escape as well as the duration of escapes have been attributed many meanings. Some would say that the smaller the proportion of escapes and the faster the returns are, the more sexually motivated is the female. Both effects may be interpreted as indicating that the female wants to be close to the male in case he would like to mount. This, in turn, must be indicative of high sexual motivation. On the contrary, if the proportion of escapes is high and the return is slow, then we may say that the female does not want to be close to the male, hence she is not sexually motivated. All this sounds very nice, but before making claims of this kind it would be convenient to try to figure out the mechanisms determining the female's escape.
We already know that the amount of sensory stimulation is the critical factor. What we do not know is which kind of sensory stimulation the female responds to. It is most likely that penile insertion causes distension of the vagina for the duration of the insertion. It is also likely that the ejaculatory plug causes vaginal distension that outlasts the penile insertion that was associated with ejaculation. The rat's semen coagulates within seconds of ejaculation and forms a solid plug that is somehow attached to the cervix. This plug is big enough to distend at least the deeper parts of the vagina. One possible cause for the females' habit of escaping from the male after intromissions and ejaculation may be this vaginal distension. The more intense distension caused by ejaculation (penis + ejaculatory plug enhance the degree of distension and the continued presence of the ejaculatory plug enhances the duration of distension) can easily explain the increased likelihood of escape after ejaculation compared to intromission, and also the longer duration of absence from the male after ejaculation. If this reasoning were correct, than stretch receptors in the vaginal wall would be critical. There is some evidence for the existence of such receptors. Inflation of an intravaginal balloon activates sensory neurons in the pudendal nerve in cats (Cueva-Rolon et al., 1994). The firing of these neurons declines very slowly during sustained vaginal distension, suggesting that the sensory receptors do not adapt to this kind of stimulation. On the contrary, receptors responding to a moving probe adapted rather fast. Similar results have been reported from rats (Katter et al., 1996). Ejaculation should cause sustained vaginal distension while the intromitting penis should be similar to a moving probe. Thus, ejaculation should produce long-lasting activity in sensory receptors while the activity should be short lasting after intromission. The duration of sensory stimulation thereby seems to be associated with the duration of the female's escape from the male. The electrophys-iological data nicely substantiate the hypothesis that vaginal distension can be the stimulus causing female withdrawal from the male.
Another hypothesis is that penile insertion is painful to female rats. The argument for this is that vaginocervical stimulation produces an analgesic response (Komisaruk and Wallman, 1977; Komisaruk and Whipple, 1995) and analgesic responses are typically associated with painful events. According to this point of view, the female escapes from the male because of vaginal pain. This is not an unlikely hypothesis. Most of those who have spent some time observing copulating rats have noticed that the female often vocalizes when being penetrated and she may also turn against an insistent male and reject his approaches with a certain lack of politeness or even with outright violence if the male should dare to try to mount shortly after having performed an intromission. In addition to this kind of anecdotal observation, there are experimental data suggesting that vaginal distension is aversive to rats. In a series of quite ingenious studies, rats were first subjected to tail pinch. They could terminate this noxious stimulation by introducing the head into a small tube located in front of them. All the rats learned to do so after a few trials. The interpretation of this was that the rats had learned to stop an aversive stimulus by the operant response of introducing the head into the tube. In the next phase, tail pinch was replaced with uterine or vaginal distension produced by a gradual increase of pressure in an intrauterine or intravaginal balloon. Exactly as in the first phase of the experiment, the stimulus could be stopped by introducing the head into the tube. All the rats responded to even moderate increases in pressure in the intravaginal balloon while the intrauterine balloon produced a much weaker response (Berkley et al., 1995). The conclusion drawn, that vaginal distension is aversive, does not seem unwarranted. In a subsequent study, it was reported that the response to intravaginal pressure increases depended on the estrous cycle. It was at a minimum around estrus/proestrus, exactly the period in which a cycling female is sexually receptive (Bradshaw et al., 1999). The conclusion was that vaginal distension is least aversive at the moment in which it is most likely to occur, that is during copulation, a behavior strictly limited to the period of proestrus/estrus.
Whether we want to interpret the female's response to the balloon as a pain response or not is probably a matter of taste. Personally, I prefer to call it a response to an aversive stimulus. According to basic concepts of learning theory, the head-introducing response was acquired because it stopped an aversive stimulus, tail pinching or distension of internal genitals. If these stimuli had not been aver-sive, a response stopping them would not have been learned. The fact that the females learned constitutes the proof that these stimuli are aversive. I will not enter into an analysis of the apparent circular nature of this reasoning. Learning theorists have solved the problem long ago and any good textbook in the field of learning will provide convincing arguments for the validity of the relationship between the acquisition of responses ending a stimulus and an aversive internal state produced by such a stimulus. The intimate nature of the emotional experience associated with the presence of the aversive stimulus is impossible to determine, but since the stimuli employed appear painful to a human observer, we imagine that they are also painful for rats.
A completely different explanation for the copulatory behavior of the female rat has been proposed in an extraordinary well-written chapter by Komisaruk and Whipple (2000). They suggest that a sexual interaction produces a momentary reduction of sexual motivation. The degree of reduction is determined by the intensity of vaginocervical stimulation, being least after a mount and largest after an ejaculation. If sexual motivation is momentarily reduced, then the female has no need to remain in proximity of the male and could as well escape. When sexual motivation spontaneously recovers after a few moments, she will return to the male for another sexual interaction. This intriguing proposal accounts for all known experimental facts in a very elegant way. Furthermore, it is no way incompatible with the vaginal distension hypothesis presented above. Indeed, it can be maintained that the origin of the reduction of sexual motivation is the sensory stimulation received from vaginal stretch receptors. For the sake of fairness, it must be mentioned that Komisaruk and Whipple (2000), at difference to myself, regard the aversive stimulation/pain hypothesis as a more viable alternative.
Other behaviors, like ear wiggling, displayed by female rats during copulation are poorly understood. For example, the potential effects of ear wiggling on the male have never been studied. One imaginative hypothesis saying that the vestibular stimulation produced by the head shaking and turning underlying ear wiggling facilitates lordosis has been put forth (Pfaff, 1999). Some convoluted electrophysio-logical evidence was presented in favor of that hypothesis, but it is far from compelling. Personally, I find it safest to propose that ear wiggling is an entirely meaningless behavior, affecting copulatory behaviors neither of the female displaying it nor of the male watching it. The proposal of a meaningless, reflex-like behavior is certainly offensive to those believing that nature is perfect. However, nature may be perfect only if so designed by a perfect creator. Evolution, through natural selection, may favor or disfavor alternative solutions, but there is no reason to believe that evolution ever has arrived at a perfect solution. Only a creationist conviction could justify the idea that behavior cannot be meaningless. Those of us believing in evolutionary theory have no problems with imperfections.
I have given a rather extensive account of the female rat's sexual behavior. As was the case with the male, the main reason is that the female rat is the only animal for which we have a considerable amount of excellent experimental data. The essential characteristic of female rat sexual behavior is the sequence of excitation-inhibition, manifested as approach-withdrawal behaviors. Incidentally, this aspect of female sexual behavior had been ignored for many years. It was not so long ago that it was discovered that the female likes to escape from the male after some sexual interactions when given the opportunity to do so (Peirce and Nuttall, 1961). By a simple change of observation procedure, the before then ignored aspects of female copulatory behavior were suddenly seen. Here we have an eloquent example of how the choice of behavioral procedure can determine what we will observe. It is also an excellent example of how decisive it may be to evaluate ecological validity of our procedures. With that I mean that the possibile behavioral repertoire expressed in the laboratory should be as similar as possible to that expressed in the wild. Please note that this reasoning applies to the study of spontaneous behaviors like sex, but it is perhaps entirely inadequate for other kinds of behaviors. The importance of strictly controlled environments for learning experiments has been eloquently expressed by one of the giants in that field (Spence, 1956). After this little digression we should return to our subject matter.
The sequence excitation-inhibition, approach-avoidance seen in female rats is identical to what we see in the male. After a mount, there is a short period of inactivity, after an intromission it is slightly longer and after an ejaculation it is longer still. The similarity in the temporal organization of sexual behavior in male and female rats is striking. There are, in fact, only two consistent, but most insignificant, differences: the period of inactivity in the male is shorter than in the female following an intromission and it is longer in the male than in the female following an ejaculation. We will later see that the similarities between males and females extend from behavior to neural control and endocrine regulation of sex behavior.
Female copulatory behavior has been described in many species other than rats, but in none of those does the precision and depth of analysis approach, in the slightest, those found in the rat. There is no need to make a detailed comparative analysis. Nevertheless, I would like to point out that copulatory behavior in the human female is fundamentally different from that of the female rat. This also applies to men and rats, so I will talk about both sexes at the same time. Copulatory behavior in women and men is not characterized by constant interchanges excitation-inhibition, approach-avoidance. In the human, copulatory behavior is a continuous process, as so elegantly described by Masters and Johnson in their now classical work (Masters and Johnson, 1966). This, in fact, applies to all primates and many other species. It would appear that rats and some other species have a rather peculiar behavior. Despite the indisputable difference between rat and human copula-tory behavior, we will discover that many experimental manipulations have similar effects in rats and humans. There are, for example, some drugs that reliably enhance the ejaculation latency in rats. They do exactly the same in men. More about the many similarities between rats and humans will appear in future chapters.
A crucial thing to observe here is that, when writing these accounts of copulatory behavior, I have made no mention of function. There is no teleology in this chapter.
The attentive reader should have noted that I have simply described behavior patterns and tried to show how these behavior patterns are under the control of specific stimuli. When trying to determine the stimulus control of a particular behavior we determine its external causation. As shown in the section on incentive motivational theory, the external stimulus must act on something in the central nervous system when producing behavior. It can, therefore, easily be argued that a complete understanding of a behavior is impossible until we have elucidated these central nervous mechanisms. However, there is no way to determine how incentive stimuli act in the central nervous system when controlling a particular behavior without knowing which these stimuli are. Moreover, we cannot unravel how an incentive stimulus acts without knowing the exact kind of behavioral responses it controls. Thus, without a careful description of behavior and the stimulus control of its occurrence and patterning, progress in neuroscience will be slow and precarious. These comments are obviously not limited to the neuroscience of sexual behavior but apply equally well to all areas of behavioral neuroscience.
On the preceding pages, there is a simple outline of copulatory behavior. We know a lot more than I have cared to describe, but I see no point in making everyone an expert in that behavior. Not even scientifically speaking. Likewise, I see no point in making everyone an expert in comparative psychology. I have tried to concentrate on some basic aspects, all of which will be important to master in order to appreciate many of the arguments that will appear throughout this book. We will now turn to copulatory behaviors in the human.
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