The positive affect behavioral data

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Sex causes positive affect. Some people would even say that few things cause a positive affect as intense as that experienced at orgasm. This positive affect produced by the execution of copulatory behaviors is what we understand with sexual reward. The role of affect shall not be underestimated. It is generally believed that positive incentive stimuli activate approach behavior because they induce some fraction of the affect produced by the event they predict. The odor of a receptive female rat, for example, activates approach behaviors in most male rats. Approach to the incentive is normally followed by copulatory acts culminating in ejaculation. Ejaculation is associated with a rather long-lasting positive affect in the male and in the female receiving it, as we soon will see. The female's odor predicts a proximate positive affect. The quality of predictor of positive affect is fundamental for all positive incentives.

It seems that the simple exposure to an incentive, without any further interaction with it, can produce positive affect. A male or a female rat will approach an inaccessible conspecific of the opposite sex day after day and week after week, even when sexual interaction never occurs. It seems as if the stimuli emitted by the potential sexual partner are intrinsically rewarding. The same can happen with food. A hungry rat may approach an inaccessible food pellet, day after day and week after week, even if she is never allowed to taste it. These approach behaviors would be completely unexplainable if we did not assume that the simple exposure to the incentives have some rewarding consequence. What is lacking at this moment is experimental support for the notion that the simple exposure to an incentive is rewarding. Please observe that there is no reason to believe that such an exposure could be used for reinforcing learning. Here we have a good example of the importance of distinguishing reward from reinforcement.

Even if the rewarding properties of the exposure to a sexual incentive have not been experimentally established, we know that the execution of copulatory acts until ejaculation is rewarding, meaning that it induces positive affect. We do not, regrettably, have any objective data from the human showing that the execution of sexual acts until orgasm produces positive affect. Perhaps we can trust introspective data on this matter. In other mammalian species, however, we have experimental data confirming the belief that sex is rewarding. I will first explain how we can look into the mind of a rat and figure out if he or she feels good or not, and after that I will turn to the data.

Many years ago scientists became interested in searching for the causes of drug addiction. I ignore why such a search seemed interesting, but one of the hypotheses that appeared stated that some people get addicted to drugs because they experience positive affect, or pleasure to use more vulgar language, after taking the drugs. In order to test the hypothesis in animal models, a procedure able to detect affective consequences of drugs was needed. A procedure able to do that was soon described (Beach, 1957a, 1957b). However, its routine use turned out to be rather impractical and it did not have much success. A more user friendly variant of the original procedure was described some years later (Rossi and Reid, 1976) and now it became a success. It has been used in hundreds of studies since then and it continues to be popular among those interested in positive affect and drug addiction. It has also been adapted for use with natural stimuli/events supposed to induce positive affect. Several reviews listing all the drugs and events employed as source of positive affect are available (Schechter and Calcagnetti, 1993, 1998; Bardo et al., 1995; Tzschentke, 1998).

The basic setup consists of two compartments differing in several stimulus modalities, usually odor, color and texture. For example, one compartment may have a floor covered with sawdust smelling of pine and black walls, while the other may have a steel grid floor, white walls and an odor of diluted vinegar. When affective consequences of a drug are the matter of interest, the drug is usually administered just before the subject is confined to one of these compartments. A following day, the drug vehicle is administered and the subject is then confined to the other compartment. The alternating drug and vehicle administrations are usually repeated a couple of times. At the test, the subjects are allowed to move freely between the compartments and the time spent in each of them is recorded. No drug is given before the test session.

The idea behind the procedure is that potential affective consequences of the drug become associated with the environmental cues present in the compartment through classical conditioning. Consequences of the vehicle injection should be associated with the corresponding compartment. If successful, the conditioning procedure should have transformed the initially neutral environmental cues in the compartment associated with drug administration into conditioned positive incentives. At test, these cues should activate approach behavior like any incentive. The cues in the compartment associated with vehicle administration should, at least in the ideal situation, remain neutral even after conditioning. Thus, at test, the experimental subjects should spend more time in the drug-associated compartment than in the vehicle-associated compartment. If that should happen to occur, then we would say that they show a conditioned place preference. An identical procedure may be employed for studying drugs or stimuli/events having aversive effects. In that case, a conditioned place aversion is produced.

It could be argued that we do not know if conditioned place preference really is a behavioral expression of drug-induced positive affect. Initially, the arguments in favor of an explanation in terms of affect were based on anthropomorphism. All drugs known to produce positive affect in the human can be used for conditioning place preference, while drugs perceived as neutral in humans are ineffective. Likewise, all compounds having aversive effects in the human produce a conditioned place aversion. I have criticized the use of anthropomorphisms, and I must accordingly consider the preceding reasoning as faulty. Rather I maintain that learning theory excludes any explanation other than conditioning of positive affect. What else producing approach behavior could possibly be conditioned in this particular situation? Many experimental controls have been employed over the years and all alternative explanations have been ruled out.

A natural stimulus/event may replace a drug for producing positive affect. We tested the affective consequences of the execution of copulatory behavior in male rats many years ago. The basic idea was that copulation until ejaculation should induce a positive affect outlasting the sexual interaction itself. Conversations with colleagues and friends had convinced me that the pleasure of having an orgasm did not dissipate instantaneously. Supposing this to be true, we could replace the injection of a drug causing positive affect with an opportunity to copulate until ejaculation. This we did. Male rats were allowed to ejaculate once with a sexually receptive female. Immediately after ejaculation, we introduced the male into one of the compartments of a place preference box. On alternate days, the male was taken directly from its home cage and placed in another compartment. We repeated this three times and then we performed the test. It turned out that the males preferred the compartment associated with the after-effects of ejaculation. Another group of males were exposed to a non-receptive female for a time equal to that needed for achieving one ejaculation in the first group and the animals were then placed in the place preference compartment. At test, this group displayed no preference. This simple experiment suggests that the execution of copulatory behavior indeed induces a state of positive affect in male rats (Agmo and Berenfeld, 1990). Similar results have later been reported by others (Martinez and Paredes, 2001; Camacho et al., 2004).

While copulation has been believed to produce positive affect in males long before any experimental demonstration existed, it was for a long time discussed whether this was the case also in females. In my discussion of paced mating in the female rat, I mentioned that scientists have been fascinated by possible aversive consequences of sexual interaction. The proposal that sex was aversive to the female rat was made seriously and experimental data were interpreted as supporting it. I already insinuated that this idea coincided nicely with typical social prejudice dominant at the time. Many groups were still maintaining that sex was a conjugal obligation, which women had to endure for the sake of preservation of the species. The idea that women could find any pleasure in sexual acts was reserved for prostitutes, nymphomaniacs and other perverts. In that context, the rat data came in very handy. However, we now know that copulatory acts produce as much positive affect in females as they do in males. This has convincingly been shown in the conditioned place preference procedure. Female rats were allowed to copulate until the male ejaculated, some in a procedure where the male controlled sexual interactions, some in the pacing procedure. It turned out that only paced mating produced positive affect (Paredes and Alonso, 1997; Martinez and Paredes, 2001). Male-controlled mating was affectively neutral, producing neither preference nor aversion in the procedure. These data could easily be interpreted in a feminist way, saying that they demonstrate that females enjoy sex only when they, and not the male, are in control. Some more recent data do not coincide with the feminist view. In two nicely controlled studies, it was reported that the execution of copulatory acts was rewarding for female rats regardless of the mating procedure employed (Meerts et al., 2005; Meerts and Clark, 2006; Yamada et al., 2006). Thus, with or without control, females show positive affect after copulating.

We are now in a position to conclude that experimental data show that sexual activity can induce a state of positive affect in male and female rats. It can be assumed that this is also the case in other mammals, including the human.

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