As discussed earlier, using fMRI, Bartels & Zeki (2000)
studied 17 men and women who were in love. However, their subjects were in love for an average of 28.8 months, a considerably longer period of time compared with our participants who were in love for an average of 7.4 months (Aron et al. 2005
); their subjects were less passionately in love (Aron et al. 2005
). Their participants also exhibited activity in several brain regions where our subjects showed none, including the anterior cingulate cortex and mid-insular cortex.
These varying results stimulated us to examine the subset of our subjects in longer relationships, specifically those who were in love between 8 and 17 months. In our subset of individuals in longer relationships, several regions showed activations, including the right anterior and posterior cingulate cortex, and right mid-insular cortex (Aron et al. 2005
). Thus, we confirmed Bartels & Zeki's (2000)
findings that the anterior cingulate and insular cortex are involved in longer term love relationships.
More relevant to this discussion, we also found activation in the ventral putamen/pallidum (Aron et al. 2005
). Activity in this region, associated with a specific distribution pattern of vasopressin (V1a) receptors, has been linked with pairbonding and attachment behaviours in monogamous prairie voles (Lim & Young 2004
; Lim et al. 2004
), monogamous California mice and monogamous marmosets, whereas promiscuous white-footed mice and promiscuous rhesus monkeys do not express pairbonding/attachment behaviours or this distribution of V1a receptors in the ventral pallidum (Wang et al. 1997
; Young et al. 1997
; Bester-Meredith et al. 1999
; Young 1999
). Hence, activity in the ventral pallidum is greater in longer term human relationships than in shorter ones and activity in the ventral pallidum, specifically associated with vasopressin, is evident in other pairbonding/attaching mammals.
But vasopressin activity in the ventral pallidum also affects partner preference, a central characteristic of mammalian courtship attraction and human romantic love. Lim & Young (2004)
report that arginine vasopressin antagonists infused into the ventral pallidum prevented partner preference formation among male prairie voles. Yet they also report that V1aR activation in this region is necessary for pairbond formation (Lim & Young 2004
Activity of central oxytocin in the nucleus accumbens also contributes to both pairbonding and partner preference (Lim et al. 2004
). Williams et al. (1994)
report that when oxytocin was administered intracerebroventricularly, ovariectomized female prairie voles preferred the partner who was present at the time of infusion; and Lim, Murphy and Young report that when an oxytocin receptor (OTR) antagonist is infused directly into the nucleus accumbens of a female prairie vole, this antagonist blocks partner preference formation (Young et al. 2001
; Lim et al. 2004
). Yet they also conclude that among monogamous prairie voles, OTRs and vasopressin V1a receptors (V1aR) in the ventral forebrain play critical roles in the formation of pairbonds.
Research on the genetic basis of pairbonding also lumps partner preference and attachment behaviours. Pitkow et al (2001)
reported that structural differences in the V1 receptor gene of socially monogamous male voles (as opposed to asocial promiscuous voles) increased levels of the expression of this receptor in the ventral pallidum; moreover, these males also exhibited heightened levels of social affiliation. They formed a preference for a specific female and began to cohabit with her, even though they had not mated with this female. Lim, Young and colleagues report that when they transfected this genetic variant (the monogamous version) into the pallidum of meadow voles, an asocial promiscuous species, vasopressin receptors were upregulated; each male also began to fixate on a particular
female and mate exclusively with her, even though other females were available (Lim et al. 2004
The activities of central oxytocin and vasopressin have been associated with both partner preference and attachment behaviours, while dopaminergic pathways have been associated more specifically with partner preference. So Lim et al. (2004)
integrate these data, proposing that when monogamous prairie voles and other pairbonding creatures engage in sex, copulation triggers the activity of vasopressin in the ventral pallidum and oxytocin in the nucleus accumbens and facilitates dopamine release in these reward regions, which motivates males and females to prefer a current mating partner and initiates attachment/pairbonding behaviours. Moreover, males of promiscuous species (who lack one link in this chain for encoding the V1a receptor for vasopressin in the ventral pallidum) most probably feel attraction, but do not associate this pleasurable feeling with their specific mating partner so they do not initiate a longer term attachment. In species that do not form these bonds, this relationship with dopamine reward centres is much weaker (Kendrick 2000
Like the brain systems for the sex drive and the courtship attraction, the neural mechanism for attachment is complex, flexible, varies in its threshold and intensity and is most likely integrated with many other brain systems (Kendrick 2000
), probably including the opioids (Moles et al. 2004
). Nevertheless, the above data suggest that the neural systems for courtship attraction and partner attachment work in tandem in a pairbonding species, motivating individuals to prefer a specific mating partner and also motivating them to form an attachment to this mate. These data also suggest that courtship attraction and partner attachment can operate independently in non-monogamous species, enabling individuals to prefer specific mating partners yet avoid long-term attachments.
Data on the neural correlates of maternal love support the proposition that feelings of attachment and feelings of romantic love are distinct yet interrelated neural systems. Bartels & Zeki (2004)
used fMRI to measure brain activity in mothers while each looked at a photo of her own infant, an infant with whom she was acquainted, an adult best friend and an adult acquaintance. They then compared these data on the neural mechanisms associated with maternal attachment with their data on the neural correlates of (later stage) romantic love (Bartels & Zeki 2000
). Maternal love activated several specific brain regions that differed from those associated with romantic love, including the lateral orbitofrontal cortex and the PAG. Maternal love also activated some brain regions that were the same as those activated by romantic love, including regions of the medial insula, anterior cingulate gyrus and caudate nucleus. Finally, activity associated with maternal love and romantic love overlapped in brain areas rich in oxytocin and vasopressin receptors, including the substantia nigra (Bartels & Zeki 2004
The neural flexibility of these brain systems for reproduction and their interactions with one another and other brain systems are complex (Kendrick 2000
). For example, central dopamine (and norepinephrine) can stimulate the release of oxytocin and vasopressin in neurohypophyseal tissues (Kendrick et al. 1992
; Ginsberg et al. 1994
; Galfi et al. 2001
); but increasing activity of central dopamine can also inhibit release of central oxytocin (Seybold et al. 1978
; Vizi & Volbekas 1980
). Increasing activity of central oxytocin can stimulate release of norepinephrine and dopamine (Kendrick 2000
) or interfere with dopamine and norepinephrine pathways (Schwarzberg et al. 1981
; Kovacs & Telegdy 1983
; Kovacs et al. 1990
; Van de Kar et al. 1998
). Finally, a small microsatellite repeat sequence in the gene coding for V1aR controls its density of expression in the ventral pallidum and this gene region is subject to a number of polymorphisms that contribute to variability in the strength of monogamous bonding in male prairie voles (Hammock & Young 2005
). The Homo sapiens
version of this gene has similar polymorphisms, which might contribute to individual differences in human monogamous pairbonding as well.
The above data suggest that the mammalian attachment system is distinct from, yet interacts with, the neural mechanisms for courtship attraction and the sex drive. This flexible, combinatorial system would provide individuals of myriad species with the range of motivations, emotions and behaviours necessary to pursue their species-specific reproductive strategy.
These data on attachment and romantic love also lend perspective to another aspect of reproduction, rejection in love.