The positive affect neurotransmitters

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Neuroscientists and many others are convinced that psychic events, like mood states, are nothing more than processes within the brain. Such a conviction makes it legitimate to ask for the neurochemical substrates of, for example, mood states. Positive affect, or pleasure or happiness or whichever vulgar expression we prefer to use, is a theme attracting attention from people even outside the circle of neuro-scientists. Because of the double audience, it might be worth the trouble to make some comments on this topic here and now.

The only central nervous mechanisms we know something about in relation to sex-induced positive affect is transmitter release. Assuming that the execution of copulatory behaviors culminating in orgasm is an efficient affect-producing procedure, we can start by looking at the neurotransmitters whose release is enhanced around orgasm. This has been done in a couple of studies, but most of them have looked at one single transmitter. Knowing that we already have dozens of transmitters in the brain, and that new ones appear every year, it is unfortunate that attention has been so extremely focused on only one. Still worse, many studies have reported exactly the same data, which seems like a kind of waste. The reason for this uniformity in thought and work is that dominant prejudice at the time these studies were popular had it that the neurotransmitter dopamine was crucial for the experience of positive affect. It was even believed that the positive affect was localized to the nucleus accumbens, one of the projection areas of the mesolimbic dopamine system (Wise, 1982; Wise and Bozarth, 1987).

Dopamine is released from the moment a male or a female is exposed to an individual of the opposite sex until ejaculation. Thereafter release declines rapidly (Pfaus et al., 1990, 1995; Pleim et al., 1990; Phillips et al., 1991; Mermelstein and Becker, 1995). Dopamine is also released in rats subjected to tail pinch, foot-shock, aggressive encounters and similar unpleasant events (Doherty and Grattton, 1992; Tidey and Miczek, 1996; Takahashi et al., 1998; Ferrari et al., 2003). The variety of events able to enhance dopamine release in the accumbens was shown in an elegant experiment in 1986. Aggressive encounters, tail pinch and encounters with a female shared the capacity to release accumbens dopamine (Louilot et al., 1986). The fact that dopamine is released in all situations enhancing arousal and general activity, regardless of the kind of affective reaction associated with the enhanced arousal, suggests that dopamine in the nucleus accumbens subserves motor mechanisms. This notion stems from a brilliant paper concerning the function of the nucleus accumbens published in 1980 (Mogenson et al., 1980). All observations pointed in the direction of a function related to motricity. Thus, already in the mid-1980s, it was evident that dopamine release in the accumbens could not have much to do with positive affect. This has been pointed out many times since then (Robinson and Berridge, 1993; Salamone et al., 1997; Berridge and Robinson, 1998; Ikemoto and Panksepp, 1999). Despite the clear evidence to the contrary, the hypothesis of accumbens dopamine release as an event underlying positive affect continues to circulate in some badly informed textbooks and among many amateur scientists.

After excluding dopamine as a transmitter associated with positive affect, we need to find an alternative. This is easily done, since the endorphins had been implicated in reward states long before the contradictory dopamine data had started to accumulate (Belluzzi and Stein, 1977). In view of this, we evaluated the capacity of an opiate receptor antagonist to block the positive affect produced by ejaculation in male rats. To that end, the place preference procedure was used. Before each session, some rats were injected with naloxone, then allowed to ejaculate. Immediately thereafter they were placed in the place preference chamber. After a few sessions, the test was made. Control rats showed a robust place preference, but there was no trace of a preference in rats treated with naloxone. On the contrary, a group of rats injected with a dopamine antagonist displayed a clear place preference after conditioning (Agmo and Berenfeld, 1990). The conclusion was quite clear: the positive affect caused by sexual interaction is an opioid-dependent event. Similar data have been obtained in female rats (Paredes and Martinez, 2001). As was the case with the male, a dopamine antagonist does not block the positive affect induced by sexual interaction in female rats (Garcia-Horsman and Paredes, 2004). Exactly as in males, positive affect caused by sexual interaction is an opioid-dependent event.

After having shown that sexually induced positive affect is opioid dependent, it was quite natural to ask where in the brain the sex-induced opioid release could be localized. At the time, there was no procedure available to measure rapid changes in opioid release, so we had to employ indirect approaches. Some data already existing suggested that the medial preoptic area could be an important site. We proceeded to analyze a possible copulation-induced release in the preoptic area with help of the kindling procedure. Electrical kindling consists of the repeated application of short pulses of a current of low intensity to a brain site. The first couple of stimulations have no visible behavioral effect, but they excite neurons in the vicinity of the stimulation electrode. After several stimulations, the neuronal excitation is increased both in amplitude and duration and, eventually, behavioral manifestations are seen. When kindling is complete, the previously ineffective electrical stimulation produces full-blown convulsions. After a kindling-induced convulsive crisis, the rat remains immobile for a while. This state is called post-ictal behavioral depression. Administration of an opiate antagonist strongly reduces the duration of the post-ictal behavioral depression and it has become habitual to consider that state as opioid-dependent. We reasoned that kindling with the electrode placed in the preoptic area and determinations of the duration of the opioid-dependent post-ictal behavioral depression observed in completely kindled animals could be used as indirect evidence for opioid release during copulation. If opioids indeed were released during the execution of copulatory reflexes and especially at ejaculation, this release should enhance the duration of the post-ictal behavioral depression, and that enhancement should be blocked by an opiate antagonist. In line with this reasoning, we applied electrical stimulation to some rats 1 minute after ejaculation. Another day we applied an identical electrical stimulus in the absence of sexual activity. The post-ictal behavioral depression was dramatically prolonged when the stimulus was applied 1 min after ejaculation in rats with the electrode within the preoptic area. This increase was blocked by naloxone. In rats with the stimulating electrode in the basolateral amygdala, sexual activity did not modify the duration of the post-ictal behavioral depression, suggesting that the opioid release was specific to the preoptic area (Paredes et al., 1992). Recent studies employing far more sophisticated techniques have confirmed that sexual activity indeed releases opioids within the preoptic area (Coolen et al., 2004).

There is still one element missing from a complete picture of sexually induced positive affect. We know that it is opioid-dependent and we know that opioids are released in the preoptic area, but we do not know if opioid receptors within that area are involved in the generation of positive affect. This question was answered in a simple experiment many years ago. We administered an enkephalin to the pre-optic area before place preference conditioning. The results were quite clear. Even a very small dose of enkephalin produced place preference when infused into that area (Ágmo and Gómez, 1991). Finally, a group of rats were allowed to copulate until they had achieved one ejaculation after infusion of a minute amount of the opiate antagonist naloxone into the preoptic area. No place preference could be established, while controls as always showed a strong preference. Naloxone infused into the nucleus accumbens was, obviously, ineffective (Ágmo and Gómez, 1993). Taken together, all these data make it likely that the positive affect caused by sexual activities is dependent on opioid release in the preoptic area.

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