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Truly, Madly, Deeply

Ae fond kiss, and then we sever;

Ae fareweel, and then for ever!

Deep in heart-wrung tears I'll pledge thee,

Warring sighs and groans I'll wage thee.

'Ae Fond Kiss'

The poets speak of falling in love as though it was a kind of anguish - a sense of exhilaration tinged with loss, of yearning for what might have been. What on earth creates this extraordinary feeling? And why does it so often take us by surprise? One possible answer that got neuroscientists very excited a few years ago centred on the role of the neurohormone oxytocin. Its proper biological function originated in the management of water balance, but somehow during the course of mammalian evolution it became tangled up in the processes associated with reproduction, including both giving birth and lactation. It's not hard to see how a neurochemical implicated in managing water balance within the body should become involved in lactation. After all, that's just another form of water balance, since the water converted into milk has to be replaced to avoid the mother becoming too dehydrated. And then, perhaps, it's but a small step from that to the essential precondition for lactation, namely the birth process. It's yet another nice example of how evolution often exploits something that evolved for one function for some entirely different, but vaguely related, purpose.

Oxytocin really hit the headlines in the early 1990s as a result of a series of studies on an obscure group of North American voles - tiny, mouse-like, burrow-living rodents that scutter about in the undergrowth. The key finding was that females of two species of vole that differed in their mating systems also differed markedly in the number of receptor sites for oxytocin in their brains. Although both species' brains released equal quantities of oxytocin, one species seemed to be much more responsive to it. Unusually for such a small mammal, that species - the prairie vole - also happens to be monogamous: after mating, the male stays with the female right through until the pups have been weaned some forty-five days later. The montane vole, whose females are less responsive to oxytocin, is promiscuous and the male does not stay with the female after they have mated. The rather too obvious conclusion was that oxytocin must be involved in the processes that underpin pairbonding behaviour, and in the popular press it was soon dubbed the 'monogamy hormone' - or the 'cuddle hormone' because it made it possible for voles (which are otherwise usually quite aggressive towards each other) to huddle together in their burrows. In short, oxytocin seemed to make a prairie vole female more tolerant of the continuing close proximity of the male with whom she had mated, to the point where she would allow him to share her burrow. Here, then, in one simple chemical process lay the elixir of life. Or so it seemed.

Love hormones?

The starting point for much of the interest in oxytocin had been the discovery that it was released in large quantities during mating, and particularly, in human females, during orgasm. Given oxytocin's role in the processes of birthing and lactation, it was, perhaps, not too surprising to find it also deeply involved in female orgasm. Its release at orgasm coincides with a great deal of mechanical stimulation of both the upper body (especially the breasts) and the reproductive tract, so it may be that it is all part and parcel of the same process of physical stimulation that triggers oxytocin release during birthing and suckling. Nonetheless, the fact that oxytocin is released in the wake of orgasm probably explains why many of the same sensations and emotions as are roused by birth and suckling also occur in this context. This apparent connection with sex led, naturally enough, to questions about its involvement in other aspects of romantic behaviour and pairbonding. If oxytocin is about bonding, then its job might simply be to strengthen the bond with whomever you happen to be involved with at the particular moment - baby in the first case, partner in the second. It's a cheap chemical trick to bypass your natural defences. Rational thought flies out of the window, and instead you get poleaxed whether you want to or not, your better judgement notwithstanding.

In rats, high doses of oxytocin give rise to a sedative-like effect, including lowered blood pressure and reduced locomotion. The physical stimulation of suckling itself (the process that triggers the release of oxytocin) is also associated with anti-stress effects, and there is evidence to suggest that oxytocin may be associated with physical touch: massage-like stroking of a rat's abdomen raises oxytocin levels and results in an analgesic effect associated with elevated pain thresholds. Similarly, in novel environments oxytocin-deficient female mice are more nervous and have higher physiological stress levels than genetically normal mice. These symptoms can be alleviated by injecting oxytocin directly into the rat's brain. Intriguingly, analogous effects have been reported for women: the frequency of hugs with the partner correlates with elevated oxytocin levels and lowered blood pressure (indicating greater calmness and reduced stress) during stressful situations. In addition, the release of oxytocin following natural birth is associated with changes in personality in women, including greater levels of calmness, sociability and - probably just as well - a greatly increased tolerance of monotony. It began to seem that in some mysterious way, oxytocin was involved in the very processes of social bonding itself. Whatever may be mediating this relationship (and it may actually involve other neurohormones, as I shall suggest below), it seems that hugs are good for you. In one study of couples, the best predictor of low levels of cortisol (the so-called stress hormone) was the frequency of intimacy: more time spent on intimacy had an immediate effect on cortisol levels each day.

Being willing to share a burrow or a home with a mate is, in the end, about trust, trust that they will not kill your pups (at least in the case of voles whose males have something of a bad reputation in this respect) or mistreat you. So it was perhaps no surprise when it was found that oxytocin also seems to play a role in facilitating trust even in humans: a whiff of oxytocin up the nose causes us to be more generous towards each other. This was demonstrated in a neat experiment in which subjects were asked to play the Trust Game. In this game, one player is given a sum of money and asked to share some, all or none of it with a second player. Whatever they give to the second player is doubled, and the second player is then invited to share some, all or none of the enlarged pot with the first player. The best strategy for the first player ought to be to hand over the whole pot to the second player. Providing the second player is honest and splits the enlarged pot with the first player, they both benefit to the maximum. But the risk is that the second player simply pockets the lot and does a runner. That way, player two gets a double bonus, and player one gets nothing. So most people try to hedge their bets and only give some of their pot to player two, keeping back a proportion for themselves so that at least they get something if it all goes pear-shaped.

But a whiff of oxytocin up the nose has a decidedly beneficial effect: on average, player one shared 17 per cent more of the initial pot with player two after a shot of oxytocin compared to when they were given a placebo spray with an inert chemical. What makes it clear that this is about trust is the fact that when the experiment was re-run with player one playing against a computer that responded randomly (and they knew they were playing against a computer), there was no difference between the oxytocin and placebo conditions in their willingness to share. In other words, it was not simply risk that player one was betting on, but malicious, sneaky, untrustworthy human behaviour.

Another study has claimed that oxytocin increases men's ability to correctly read social information in the eyes. However, the improvement in performance after a squirt of oxytocin up the nose was only a measly 3 per cent (something most people wouldn't consider biologically meaningful) and only worked at all in two-thirds of the men in the sample. Besides, the test of social skills used in the study wasn't, perhaps, the most sensitive: it is a test of knowing whether someone is looking directly at you rather than away from your eyes, and although a good test of autism (the psychological condition associated with the virtual absence of social skills), it isn't really a terribly good test of normal individuals' social or mindreading competences. Who knows what these results are actually telling us? More plausibly, however, in another study the same team found that oxytocin reduced amygdala activity in men when viewing photographs of faces exhibiting different emotions. The amygdala is normally involved in the management of our responses to negative emotions (fear, anxiety, anger), so it makes sense, given how it works in females, that it should dampen negative emotional responses even in men.

Although oxytocin is present in male brains, it doesn't seem to have quite the same dramatic effect that it has in female brains. Instead, the vole work suggests that males are responsive to a related but rather different neurohormone, vasopressin. Males of the monogamous prairie vole have more vasopressin receptors in the brain's ventral pallidum (part of the ancient limbic system whose main job is to...