On the importance of the distinction between approach behaviors and the execution of copulatory reflexes

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Sexual interaction, potentially leading to sperm deposit, is impossible at a distance. Two or more individuals need to be in close proximity before sperm transfer can occur. The establishment of the required proximity must inevitably precede the activation of copulatory behavior. The ways in which humans and other animals succeed in establishing this proximity is extremely variable. In fact, it is safe to propose that proximity is established by a series of entirely arbitrary behaviors as already pointed out in the previous section. Whereas copulatory behavior is very stereotyped in all mammals, with the exception of the human, behaviors leading to proximity are extremely varied. They are determined by an interplay between the specific context and individual experience. The importance of proximity as a requisite for copulation cannot be overestimated. For many animals, and perhaps particularly for the human, copulation is a far lesser problem than finding with whom to copulate. Despite this rather obvious fact, the stereotyped copulatory behavior has attracted scientists' attention far more than the intriguing and fundamental problems of the arbitrary behaviors employed for the establishment of proximity. One consequence is that we know far more about the regulation of copulatory reflexes than we know about the mechanisms determining behaviors leading to proximity. This state of affairs makes it possible to give a quite clear picture of copulatory behavior, whereas the present picture of behaviors associated with the establishment of proximity is confusing. That is one reason for beginning with an analysis of copulatory behavior. An old didactic principle is to begin with the simple and proceed with the complex. Another reason for beginning with copulatory behavior is that our discussion of proximity establishment frequently will refer to some or another aspect of copulatory behavior. Since most scientists have ignored the proximity establishment, we often need to make inferences based on observations of copulatory behavior and, to make these inferences meaningful, we need to have some basic knowledge of that behavior. However, it is also very important to keep in mind that there are fundamental differences between approaching and establishing contact with a potential mate and the ensuing (if all goes well) execution of copulatory reflexes.

One powerful reason for maintaining that sexual approach behaviors need to be classified and analyzed in a category different from the category of copulatory behaviors is the obvious and repeatedly mentioned distinction between arbitrary and stereotyped. This distinction has many consequences. One is that the arbitrary approach behaviors may be fundamentally molded by learning, basically operant conditioning. The stereotyped copulatory behaviors are far less moldable by experience and, when learning occasionally affects them, it appears to be because of classical rather than operant conditioning. A more extensive discussion of the role of learning is found in Chapter 7, but I find it necessary to anticipate this subject here because of its importance for keeping approach behaviors separate from copulation. Besides the differential role of learning, there are many other good reasons for the distinction between copulation and approach. These will appear in the following paragraphs.

Others may argue that the distinction between the establishment of proximity and actual copulatory behavior is artificial and unfounded in reality. It could be maintained, for example, that both aspects are necessarily associated with reproduction and represent, therefore, inseparable parts of a behavioral sequence. This argument loses its force when we consider the dichotomy stereotyped versus arbitrary behaviors and the consequences of this outlined in the preceding paragraph. Furthermore, it is likely that the nervous processes involved in approach are different from those involved in the execution of copulatory reflexes. Illustrations of this difference are the fact that some individuals will try to establish proximity while never initiating copulatory behavior (Stone et al., 1935) and that experimental treatments may affect proximity establishment but not copulatory behavior and vice versa. Examples of this will be found throughout this chapter.

Another argument against the distinction between proximity establishment and copulatory behavior could be that the establishment of proximity with a potential mate is not a sexual behavior at all. Animals may approach conspecifics in many non-sexual situations and the behavioral and neural mechanisms determining the approach behavior leading to the establishment of proximity may be common for non-sexual and sexual contacts. In keeping with this reasoning, there would be no need for including the proximity establishment in the category of sexual behaviors.

In fact, mechanisms responsible for this kind of behavior could be better understood if they were analyzed independently from sexual behaviors, according to this point of view. Since the actions or motor patterns of which approach behavior consists are extremely variable, there is no way to distinguish patterns leading to sexual proximity from patterns leading to other kinds of proximity. As examples of situations where proximity of different kinds are established and maintained for some time through the action of forward locomotion, I can mention social and sexual approach between rats. Laboratory rats are gregarious and they like to be close to other rats when given the opportunity (Latané and Glass, 1968; Latané, 1969; Latané et al., 1973; Âgmo et al., 2004) even though no sexual interaction will take place. This kind of proximity may conveniently be called social. In this context, one rat typically reduces the distance to another rat by forward locomotion and, since the other rat may be moving around, this forward locomotion may continue for a rather long period of time. Likewise, forward locomotion is involved in sexual approach and it is also used for maintaining contact during actual copulation. The muscular activity, i.e. the motor patterns, involved in both social and sexual approaches may be identical. Considering the impossibility of distinguishing behaviorally one kind of approach from another, it is impossible to consider the establishment of sexual proximity as anything different from the establishment of other kinds of proximity. To make the point in slightly different language: animals, including humans, may search to establish proximity with conspecifics without any ensuing copulatory behavior employing exactly the same motor patterns as those used for the establishment of sexual proximity, making it ludicrous to propose a particular behavioral category of 'the establishment of sexual contact'. Moreover, social approach behaviors may be modified by operant learning in exactly the same way as sexual approach behaviors are.

The reasoning exposed above could easily be rejected by stating that the finality or purpose or function of the behaviors is different when sexual and social proximity are sought. According to my own opinion, expressed quite clearly before, this argument has no sense. Fortunately, there are scientifically sound arguments for maintaining that the establishment of sexual contact is determined by factors different from those involved in the establishment of social contact. Instead of advancing a teleological argument, I advance empirical observations concerning the causation of these approaches. They go like this:

1 If sexual approach were dependent on gonadal hormones in the same way as copulatory behaviors are, and if social approach were independent of such hormones, then it could be concluded that sexual and social approach are at least partially controlled by different central nervous mechanisms. In fact, castrated males approach a sexually receptive female less than intact males and ovariec-tomized females approach an intact male less than sexually receptive females. At the same time, social approach is not modified by gonadal hormones. Intact and castrated males approach an ovariectomized female (a social incentive) with the same intensity and sexually receptive and non-receptive females approach a castrated male (another social incentive) with equal intensity (Agmo, 2003; Agmo et al., 2004). If the establishment of proximity to a potential mate can be experimentally separated from other kinds of proximity establishment, then it seems most useful to consider it a unique behavioral category. Furthermore, since it is dependent on gonadal hormones, it seems reasonable to consider it as part of sexual behavior. 2 We have shown that continuous sexual interaction with a sexually receptive female for 4 hours significantly reduces the intensity of the males' approach towards a sexual incentive while leaving that towards a social incentive unaffected. Likewise, a female rat shows reduced approach towards an intact male immediately after having received three ejaculations while approach towards a castrated male did not differ from that shown when the females were unmated (Agmo et al., 2004; Spiteri and Agmo, 2006). Similar data have been obtained in an entirely different procedure (Sloan and Latane, 1974). All these observations convincingly show that the mechanisms determining the intensity of sexual approach are different from those determining social approach.

I would like to propose that the central motive state determining the behavioral impact of sexual incentives (conspecifics with which sexual interactions may occur) is different from that determining the impact of social incentives (conspecifics with which social but not sexual interaction may occur). We have already seen that some behavioral data support this proposal. Concerning the neural control of social versus sexual approach, it has been found that preoptic lesions eliminating copulatory behaviors and reducing approach to a sexually receptive female fail to modify social interactions (e.g. Paredes et al., 1993a). Finally, some drugs modify a sexual incentive approach while not affecting, or having opposite effects on, a social incentive approach (Viitamaa et al., 2006). There is, then, ample evidence for a behavioral, anatomical and neurochemical separation of mechanisms determining sexual approach and mechanisms determining social approach.

The preceding arguments are entirely based on data from rats. However, as we will see in the appropriate section, sexual proximity establishment has been experimentally studied in a few other species. Results from these studies support the notions outlined above. For the moment we will abandon the question of how to understand this part of sexual behavior and proceed with an introduction to the scientific study of copulatory behavior. This may prove to be more exciting than would be expected.

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