Studies in nonhuman mammals

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I defined habituation as a decrease in the intensity of a response because of repeated exposure to a constant stimulus caused by processes in the central nervous system and unrelated to sensory adaptation or effector fatigue. In male rats and other male mammals, prolonged exposure to a sexually receptive female and the associated execution of copulatory behavior leads eventually to an end of sexual activity. It is said that the animal is sexually exhausted. The cause of the disappearance of sexual behavior can obviously be that the male is physically exhausted, in other words fatigue in the effector systems. Another cause may be that his sensory organs have adapted and no longer register the stimuli emitted by the female. If we replace the original female partner with a new one, the male will reinitiate copulation. This phenomenon has been termed the Coolidge effect in honor of the 30th president of the USA, Calvin Coolidge. It is not entirely clear how the term was established, but there is a little anecdote that seems to be in the public domain and which I can tell. It is said that the president and his wife visited a farmer who had a substantial number of hens but only one rooster. The following conversation is said to have occurred.

Mrs Coolidge: Does the rooster copulate more than once each day?

Farmer: Dozens of times.

Mrs Coolidge: Please tell that to the president.

President Coolidge: Same hen every time?

Farmer: Oh no, Mr President, a different one each time.

President Coolidge: Tell that to Mrs Coolidge.

Whether the anecdote is true or not is unimportant. It is good enough either way. To return to more serious matters: by replacing the female with a new one we have removed a constant stimulus (the original female) and introduced a new one, at least somewhat different from the first (provided rats have some capacity for recognition of individuals, which in fact they seem to have). Remember that habituation is specific to a particular stimulus. Now, since the male starts to copulate again, he cannot have suffered from fatigue in effector systems. If he had been physically exhausted, a change of female should have no effect. Adaptation and disadaptation of sensory receptors is certainly a possibility, but it seems quite remote. There is, actually, no reason to believe that a new female would have an immediate effect on receptor adaptation. Dishabituation because of the introduction of a new stimulus is probably the most convincing explanation for the reactivation of behavior. The Coolidge effect can be considered as evidence for the existence of habituation of sexual responses in male rats. A similar effect has been described in some other rodents (reviewed in Dewsbury, 1981) and in rams (Beamer et al., 1969), bulls (Bailey et al., 2005) and in the male rhesus monkey (Michael and Zumpe, 1978), suggesting that habituation/disha-bituation of sexual responses is widespread among male mammals.

As is so frequently the case with phenomena of sexual behavior, there are very few data on a Coolidge effect in females. One study (Krames, 1971) exposed females to a new male when the original male had ceased to copulate, with the purpose of determining if the female accepted as many ejaculations from the new partner as she had with the original one. She did. The authors did not care much about the females' behavior, since they were interested in finding out whether the Coolidge effect in males could be attributed to changes in female behavior rather than to exhaustion/habituation of the male. They reasoned that the male might stop copulating because of reduced sexual motivation on the part of the female. This reasoning could be tested by replacing the original male with a new one. If the new male performed as many ejaculations as the original male had done, then it could be concluded that changes in female behavior was not the cause of cessation of male behavior. This observation is certainly interesting, but it does not tell us anything about a possible existence of a Coolidge effect in females, although some scientists cite this paper as evidence for that.

Something most similar to a Coolidge effect has been reported in female hamsters, though. In an interesting experiment, hamsters copulated until they no longer displayed lordosis in response to the male's mounts, or until they actively fought him away. At that moment, some of the females were given a new male. They started to display lordosis again (Lisk and Baron, 1982). This appears to be equivalent to what has been reported in males. However, the display of lordosis in response to the male's mount is not at all the same as actively to search sexual contact. The male Coolidge effect is exactly that and not the display of a somatic reflex in response to stimulation provided by the partner. Although suggestive, it is not self-evident that the hamster data show that the female actively seeks sexual contact with the new male in the way a male pursues and mounts a new female.

There is only one study in female rodents that unequivocally shows a Coolidge effect. That study was performed by two undergraduate students in my laboratory a few years ago (Ágmo et al., 2002). They tested female rats in the pacing procedure. If a female maintained herself inaccessible to the male for a continuous period of more than 20 minutes following an ejaculation, we considered her to be sexually exhausted or to have habituated to the male. This occurred after having received between three and five ejaculations. The original male was either removed and then put back in the mating test cage (control) or he was removed and replaced by a new male (experimental). The females did not respond to the reintroduction of the original male in any particular way, but the new male rapidly provoked the display of proceptive behaviors and the female's return to the male compartment. The 'new' male was sometimes a rested male (no immediately preceding sexual activity) or a male that was in his fifth post-ejaculatory refractory interval when being put in the mating test cage. The availability of such males was assured by having several males copulating in another part of the observation room during the experiments with the females. Thus, it seems that the Coolidge effect exists also in female rats. The results of this experiment are shown in Figure 7.1. There are, to my knowledge, no other data in female non-human animals.

Although the Coolidge effect frequently, if not usually, is interpreted as a consequence of habituation to the original female, there is one alternative explanation that must be considered. The prolonged consumption of or commerce with a re-inforcer, like an extremely tasty sweet solution or a very funny computer game, leads to a reduction of its value. This effect has been well documented and is called

Control New male

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Control New male

FIGURE 7.1 (a) Number of proceptive behaviors per minute displayed after the introduction of a new male to sexually exhausted females compared to that observed when the original male was removed and then replaced. The recording of proceptive behaviors stopped when copulation was reinitiated. (b) Length of the latency to enter the male's area in sexually exhausted female rats when a new male had been introduced compared to that recorded when the original male was removed and then replaced. *, different from control, P < 0.05. (Data from an unpublished study by Turi, Ellingsen and Agmo.)

negative alliesthesia (Cabanac and Lafrance, 1990; Cabanac, 1992; Zhao and Cabanac, 1994). For example, if a human or a rat was asked to taste a small amount of a rather concentrated sucrose solution and then indicate the degree of pleasantness of the taste, they would rate it highly, at least the rats. Now, if we perform the same test immediately after having consumed a large amount of sucrose solution, both the human and the rat would rate the pleasantness of the taste far lower than prior to consumption. It is this reduction in pleasantness of a stimulus as a result of consumption or other commerce with it that is called negative alliesthesia. After prolonged copulation, the pleasantness of sex would be reduced and the incentive value of the stimulus indicating the availability of more sex would also be reduced. The decline in sexual activity after extensive copulation could, then, easily be explained by negative alliesthesia rather than habituation. The reactivation of copu-latory activity by a new female, however, cannot be accounted for by alliesthesia. In rats, copulatory behavior is stereotyped, meaning that the copulatory acts performed with one female are extremely similar to those performed with any other female. Thus, the introduction of a new female should have no effect, since that could not signal the availability of activities different from those already performed. Negative alliesthesia would not be affected by a change of female. Habitu-ation remains the most likely explanation.

If a Coolidge effect existed in the human, then we would have serious problems distinguishing alliesthesia from habituation. Human copulatory behaviors are not stereotyped. An example will illustrate the consequences of this. A man stops performing penile-vaginal intercourse after two ejaculations. The cessation of sexual activity may be attributed to either habituation or negative alliesthesia. Now, imagine that another woman appears and the man reinitiates sexual behavior with her. The only difference is that he performs cunnilingus on her rather than having penile-vaginal intercourse with her. The observation of the man's behavior seems unambiguous enough, but the explanation becomes quite intricate. First, we can maintain that the new woman was a new stimulus and, therefore, a cause of dishabituation. Sexual activity was consequently reinitiated. This coincides with our behavioral observations. Second, we can suggest that the new woman somehow signaled that she would not like penile-vaginal intercourse but rather cunnilingus. The negative alliesthesia affecting penile-vaginal intercourse would not affect the propensity to perform cunnilingus and the man would reinitiate sexual activity. In other words, the man can have reactivated his copulatory behavior either because of a new stimulus (dishabituation) or because he anticipated a new kind of sexual activity (disappearance of negative alliesthesia). The observed behavior is compatible with both explanations. One possible solution to this dilemma would be to ask the man.

The discussion of alliesthesia is slightly out of context here. Alliesthesia refers to the affective consequences of a stimulus or a behavior and this subject will be discussed in another section of this chapter. However, since alliesthesia is a potential explanation for the Coolidge effect, I considered it acceptable to mention it here. Furthermore, by applying the concept to human sexual behavior, I got an opportunity to remind the reader of the fundamental differences between copulatory behavior in the human and that of non-human animals. After this spontaneous digression from our main theme, I will immediately return to the issue of habituation.

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