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Romantic love is a universal human experience (Jankowiak and Fischer, 1992), yet is almost indescribable; doing so has been the subject of art for centuries. From Jankowiak and Fischer's (1992) review of ethnographic studies, it is clear romantic love has no cultural bounds and so likely to have its roots in human biology. Therefore, while appreciation of romantic love is usually the domain of the artist, this essay aims to explore and critically review scientific understanding of the phenomenon of romantic love, elucidating its biological components. Love comes in many forms, and in this essay the term romantic love is used to distinguish it from other forms of love, the exploration of which is beyond the scope of this essay, although research into motherly love provides useful comparisons. The conclusion will highlight where evidence overlaps, to illustrate the most likely biological components of romantic love, but ultimately show the needs for further work in this emerging field of research.
Animal Models and the Endocrinology of Romantic Love
Before the advent of functional Magnetic Resonance Imaging (fMRI) and other methods of brain imaging, most research into the biology of social attachment and bonding has been through the prairie vole. This species is a suitable model for human romantic love because they form close family units, and unlike other species of vole, form monogamous pair bonds (Carter et al., 1995). Studies on these animals show the importance of the substances oxytocin and vasopressin in pair bonding, naturally released in voles and humans during sex (Hiller, 2004). These hormones when externally administered (or testosterone and oestrogen, which act to increase synthesis and release of oxytocin and vasopressin) also encourage pair bonding in both sexes of the prairie vole in a dose dependent manner (Carter et al., 1995), whereas oxytocin receptor antagonists prevent it (Carter, 1998). A suggested explanation is oxytocin acts on the nucleus acuumbens and vasopressin on the ventral pallidum, to stimulate dopamine release from these neural areas and reward the formation and continuation of the pair bond (Fisher et al., 2006). This is evidenced further in that dopamine antagonists hinder pair bonding (Carter, 1998). This research is relevant to humans, as dopamine release, for example via cocaine use, produces a euphoric experience similar to that in romantic love (Fisher et al., 2002).
Both oxytocin and vasopressin also have unique roles in pair bonding. Vasopressin might be causative of monogamous sexual behaviour; which is present only in the prairie vole and not other species can be explained by increased expression of the vasopressin receptor in the ventral pallidum of the prairie vole. The genetic basis for monogamous behaviour is further indicated by evidence that polymorphisms of the vasopressin receptor gene alter the male prairie vole's faithfulness to one sexual partner (Fisher et al., 2006). Oxytocin might have a unique role in promoting social contact by reducing stress, through inhibition of the hypothalamic-pituitary-adrenal (HPA) axis. Carter, (1998) suggests this effect is specific to certain species of animal, theorising the presence of a unique oxytocin receptor. A human parallel of oxytocin released in nursing mothers decreases cortisol secretion (a hormone released in the response to stress) (Hiller, 2004), possibly through deactivation of the amygdala and hypothalamus (Debiec, 2005). However, it may not be this simple, the roles of oxytocin and vasopressin are complicated further with the knowledge that they can bind to each other's receptors (Carter, 1998).
Marazziti and Canale, (2004) provide further evidence of stress related to pair bonding in humans, finding plasma cortisol concentrations significantly higher in those who recently (previous 6 months) had fallen in love compared to those in long, stable relationships (mean of 5 years) or who were single. Marazziti and Canale, (2004) also found that Follicular Stimulating Hormone (FSH) and testosterone were significantly lower in men who had recently fallen in love versus male controls, while testosterone was significantly higher in women who had recently fallen in love versus female controls. These results, particularly those for FSH and cortisol, demonstrate stress associated with falling in love. The purpose of such stress might be a way of encouraging social contact, which is then rewarded by oxytocin and its anxiolytic effect (Esch and Stefano, 2005). However in Marazziti and Canale's (2004) study, there was a lack of suitable defining criteria of those 'in love', other than obsessive thoughts, and so these results may reflect only a sub-section of those who have fallen in love. However, it is further evidence of the suitability of studying the prairie vole for human behaviour.
Emanuele et al., (2006), by looking at plasma levels of neurotrophins, showed that Nerve Growth Factor (NGF) was significantly higher in those who recently fell in love (previous 6 months), compared to those in a longer relationship or controls, positively correlating with Passionate Love Scale (PLS) scores. The PLS is a validated and reliable measure of the intensity of falling in love, (Hatfield and Sprecher, 1986). It is commonly used, featuring in most of the studies yet to be mentioned (Aron et al., 2005; Bartels and Zeki, 2000; Bartels and Zeki, 2004; Kim et al., 2009; Ortigue et al., 2007; Zeki, 2007). Previous studies show that NGF acts as a mediator of behaviour, emotion and anxiety in the brain, as well as endocinological functions, such as the release of vasopressin and activation of the HPA axis (Emanuele et al., 2006). If NGF is an inducer of the HPA axis, it is not surprising that Emanuele et al.'s (2006) study, and Marazziti and Canale's (2004) study examining the stress hormones have similar results, that become non-significant when retested 12-24 months later. Deductions about the significance of these results are limited by the fact that the researchers requested only a single blood sample upon which their findings are based, failing to eliminate the natural variability of hormonal levels. Multiple samples taken over the same time frame would make this evidence more robust. Despite flaws, these results support the social psychology research, which categorises romantic love as two distinct stages of experience; for example, Sternburg's Triangular theory of love, which depicts the movement from a relationship of passion, to one balanced with intimacy and commitment. (The Psychology of Love, 1988). This is reflected in the biology: initial stress and changes in behaviour and emotion, followed by a return to normal behaviour, possibly mediated by oxytocin.
Neuroimaging in romantic love
The two-stages of romantic love might also be reflected in the results of neuroimaging studies. Both Aron et al., (2005) and Bartels and Zeki, (2000) employed a similar method of utilising fMRI contrasting neural areas active when viewing pictures of their loved ones against pictures of their friends of the same sex, age, and with a similar length of friendship as their relationship with their loved one (Aron et al., 2005; Bartels and Zeki, 2000). The participants were chosen by analysing written statements on their relationship, interviews, and scores on the Passionate Love Scale (PLS) (Aron et al., 2005; Bartels and Zeki, 2000). The key difference between the two studies was that Bartels and Zeki's, (2000) study was conducted on those who had been in a relationship for longer (median 3 years versus median of 7 months) and had lower mean PLS scores (7.55 vs. 8.54) (Aron et al., 2005). Bartels and Zeki's (2000) study found greater activity when viewing photos of loved ones in the putamen (involved in reward), in the hypothalamus, (possibly indicating erotic arousal), and in the bilateral posterior hippocampus. Whereas Aron et al., (2005) didn't find these areas activated, instead found activation in the septum, which is involved in emotion, reward and (along with the ventral pallidum) pair bonding in prairie voles. Moreover, the ventral tegmental area (mentioned below), ventral pallidum, hippocampus and hypothalamus are all areas known to be rich in receptors for oxytocin and vasopressin (Bartels and Zeki, 2004; Carter, 1998), further implicating the involvement of these substances in social bonding and attachment.
These studies also indicated similar areas of activation, probably common neurological components to both stages of romantic love. Both Aron et al., (2005) and Bartels and Zeki, (2000) found greater activity in the ventral tegmental area and caudate nucleus, dopamine rich areas involved in a goal orientated motivation, reward and pleasure as well as in focused attention (Aron et al., 2005; Bartels and Zeki, 2000; Bartels and Zeki, 2004; Fisher et al., 2006). In addition, Aron et al., (2005) demonstrated that activity in the medial insula, right anterior cingulate cortex and the ventral pallidum positively correlated with length of time in relationship, while activity in the left posterior cingulate cortex was negatively correlated, reflecting Bartels and Zeki's (2000) results which found these areas were activated (except for the left posterior which was deactivated, the significance of which is discussed later). The medial insula is probably involved in emotional processing of sensory inputs (Bartels and Zeki, 2000; Bartels and Zeki, 2004), whereas the anterior cingulate is implicated in obsessive thinking, emotional processing of happy states, attention of own and assessing other's emotional states (Aron et al., 2005). Both these areas were active when using subliminal priming (flashes loved one's names) rather than a picture (Ortigue et al., 2007) and in Cheng et al.'s (2010) study, which asked participants was to imagine their loved one (versus a stranger) in pain, thought to demonstrate increased empathy with the loved one.
In addition, there were areas less active (deactivation) when viewing photos of those the participants were in love with. Aron et al., (2005) and Bartels and Zeki, (2000) found deactivations in the right prefrontal, right parietal and middle temporal lobes, the posterior cingulate cortex, posterior amygdala and medial prefrontal cortex. Aron et al., (2005) and Bartels and Zeki, (2000) suggested these results reflected the lack of negative emotions and depressive states in romantic love, reduced social criticism of the beloved, and shift from cognitive to emotional judgement. Bartels and Zeki, (2000) further evidenced an increased emotional response related to viewing pictures of their loved one, by demonstrating a significantly increased galvanic skin response.
The correlation between brain areas activated and length of time in relationship in Aron et al.'s (2005) study were based on cross-sectional data, therefore could be explained by other factors. To examine the temporal change further, Kim et al. (2009) conducted a longitudinal study over a six month period using a similar methodology to Aron et al's (2005) and Bartels and Zeki's (2000) studies. As well as a significant decrease in the passionate love score, Kim et al., (2009) found decreased activity in the caudate nucleus and increased activity in the anterior cingulate cortex over the six month period. This research demonstrates the temporal change in the biology of romantic love, and also confirms involvement of the anterior cingulate and caudate nucleus. However, the un-expected deactivation of the caudate nucleus brings the need for caution with the results, possibly due to differences in method, such as the participants being of Chinese ethnic origin, rather than European. Furthermore, involvement of the anterior cingulate and caudate nucleus may not be specific to romantic love, but maternal love as well (Bartels and Zeki, 2004). In fact, of the brain areas discussed thus far, comparing overlapping areas of maternal and romantic love (figure) indicated that the hippocampus, hypothalamus and ventral tegmental area were the only areas active specific to romantic love (Bartels and Zeki, 2004), areas are not reported on in Kim et al's study (Kim et al., 2009).
Figure: The overlapping areas of maternal and romantic love: Reproduced from Bartels and Zeki, (2004),pg 1158. Abbreviations: ac - anterior cingulate, hi - hippocampus, I - insula, C - caudate nucleus and S - striatum.
Critique and suggestions for future research
Therefore, the above results are not sufficient to start to build an accurate model of the biology of romantic love in humans, but their correlations do at least confirm its involvement. There is a need for further research to confirm which differences seen in these studies are due to methodology or biology, although such research may be limited by technology. Furthermore, while vasopressin and oxytocin have been implicated in romantic love, their exact role in humans is yet to be determined. There are questions still to be answered; for example, are genetic differences in the vasopressin receptor linked to humans being more faithful to their partners, as they are in voles? Do the hormones oxytocin and vasopressin induce the early romantic state? Similarly the exact role of nerve growth factor is yet to be determined. There is also a need for research into broader fields of romantic love; for example, are the same areas of the brain activated across different ethnicities and in homosexuals and heterosexuals who are in love?
To conclude, the biological components of romantic love are most likely the activation of the anterior cingulate, medial insula and caudate nucleus, and the hormones vasopressin and oxytocin. In addition, the prairie vole has been suggested as a good model for the endocrinological components of human attachment behaviour. Finally, the biological interpretation of romantic love reflects the psychological one, that of two distinct parts. The early, stressful, 'falling in love' phase characterised by a powerful, focused, motivating but rewarding drive to be with someone, rather than a specific emotion, and then later, a less emotionally intense phase associated with a strong biological mediated attachment to a particular person.
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