Phil. Trans. R. Soc. B (2006) 361, 2173–2186
doi:10.1098/rstb.2006.1938
Published online 13 November 2006

Romantic love: a mammalian brain
system for mate choice
Helen E. Fisher1,*, Arthur Aron2 and Lucy L. Brown3
1

Department of Anthropology, Rutgers University, 131 George Street, New Brunswick,
NJ 08901-1414, USA
2
Department of Psychology, State University of New York, Stony Brook, NY 11794, USA
3
Department of Neuroscience, Department of Neurology, Albert Einstein College of Medicine,
New Haven, CT 06519-130, USA
Mammals and birds regularly express mate preferences and make mate choices. Data on mate choiceamong mammals suggest that this behavioural ‘attraction system’ is associated with dopaminergic
reward pathways in the brain. It has been proposed that intense romantic love, a human crosscultural universal, is a developed form of this attraction system. To begin to determine the neuralmechanisms associated with romantic attraction in humans, we used functional magnetic resonanceimaging (fMRI) to study 17 people who were intensely ‘in love’. Activation specific to the beloved
occurred in the brainstem right ventral tegmental area and right postero-dorsal body of the caudate
nucleus. These and other results suggest that dopaminergic reward and motivation pathways
contribute to aspects of romantic love. We also used fMRI to study 15 men and women who had justbeen rejected in love. Preliminary analysis showed activity specific to the beloved in related regions of
the reward system associated with monetary gambling for uncertain large gains and losses, and inregions of the lateral orbitofrontal cortex associated with theory of mind, obsessive/compulsive
behaviours and controlling anger. These data contribute to our view that romantic love is one of thethree primary brain systems that evolved in avian and mammalian species to direct reproduction. The
sex drive evolved to motivate individuals to seek a range of mating partners; attraction evolved tomotivate individuals to prefer and pursue specific partners; and attachment evolved to motivate
individuals to remain together long enough to complete species-specific parenting duties. These three
behavioural repertoires appear to be based on brain systems that are largely distinct yet interrelated,
and they interact in specific ways to orchestrate reproduction, using both hormones andmonoamines. Romantic attraction in humans and its antecedent in other mammalian species playa primary role: this neural mechanism motivates individuals to focus their courtship energy on
specific others, thereby conserving valuable time and metabolic energy, and facilitating mate choice.
Keywords: mate choice; romantic love; dopamine; oxytocin; vasopressin; evolution

1. ROMANTIC LOVE: A MAMMALIAN BRAIN
SYSTEM FOR MATE CHOICE
Individuals of many species exhibit mate preferences
and focus their courtship energy on these favoured
conspecifics. The phenomenon of ‘courtship attraction’ is so common in nature that the ethologicalliterature regularly uses several terms to describe it,
including ‘female choice’, ‘mate preference’, ‘individual preference’, ‘favouritism’, ‘sexual choice’ and‘selective proceptivity’ (Andersson 1994). Charles
Darwin regarded this phenomenon, what has become
known as ‘mate choice’, as a central aspect ofintersexual selection, the type of sexual selection bywhich individuals of one sex evolve traits that attract
members of the opposite sex (Darwin 1871/n.d).
Mammalian and avian species (as well as otherspecies) have evolved many physical and behaviouralcharacteristics by means of mate choice. The peacock’s* Author for correspondence (helenfisher@helenfisher.com).
One contribution of 14 to a Theme Issue ‘The neurobiology of social
recognition, attraction and bonding’.

tail feathers are the standard example. But investigations have focused on the traits that ‘display
producers’ have evolved to attract mates. The corresponding neural mechanism by which ‘display choosers’ become attracted to these traits and focus theirmating energy on particular preferred individuals,
thereby making a mate choice, has not been defined.
Therefore, it has been proposed (Miller 2000; Fisher
et al. 2002a,b) that two aspects of intersexual selection
evolved in tandem: (i) traits that evolved in the ‘display
producer’ to attract mates, and (ii) corresponding
neural mechanisms in the ‘display chooser’, theviewer of the display, that evolved to enable him/her
to discriminate between various displays, become
attracted to some and pursue these specific preferredindividuals.
Several brain systems most probably operate intandem to orchestrate mate choice, including theneural systems for sensory perception, memory, andcognitive and emotional responses. But the specificbrain mechanism discussed in this review is the neuralmechanism that motivates the display chooser to pursue
a preferred mating partner, the courtship attraction

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Romantic lovesystem. Courtship attraction is characterized in
mammals by increased energy, focused attention,obsessive following, affiliative gestures, possessive
mate guarding and motivation to win a preferredmating partner (Fisher 2004).
A number of groups have reported that the basic
human motivations and emotions arise from distinct
systems of neural activity and that these brain systems
derive from mammalian precursors (Davidson 1994;
Panksepp 1998). Thus, it is parsimonious to suggestthat a mammalian brain mechanism for courtship
attraction is also active in Homo sapiens. Moreover,because human romantic love (also known as passionate love, obsessive love and ‘being in love’) is auniversal human phenomenon ( Jankowiak & Fischer
1992), because romantic love’s central characteristic ismate preference and because ‘being in love’ exhibits
many of the other traits associated with mammalian
courtship attraction, it has been hypothesized thathuman romantic love is a developed form of thismammalian neural mechanism for mate choice (Fisher
1998). In most species, courtship attraction is brief,
lasting only for minutes, hours, days or weeks; inhumans, intense early stage romantic love can last
12–18 months (Marazziti et al. 1999) or more.
This review discusses the present evidence for thisbrain system in mammals and humans, focusing on
recent neuroimaging studies of romantic love inhumans (Bartels & Zeki 2000, 2004; Aron et al.
2005; Fisher et al. 2005a,b). It examines how thisbrain system varies from the sex drive and how itchanges across time (Aron et al. 2005). It also discusses
preliminary data on neural mechanisms associated withromantic rejection (Fisher et al. 2005a,b). Finally, it
proposes that this brain system is one of the three
primary mating drives which interact in many ways andwhich have evolved in mammalian and avian species todirect various aspects of reproduction. (i) The sex drive
evolved to motivate individuals to seek copulation witha range of partners, (ii) courtship attraction/romantic
love evolved to enable ‘display choosers’ to focus theirmating energy on specific mates, thereby conserving
courtship time and metabolic energy, and (iii) partner
attachment evolved to motivate mating individuals toremain together long enough to perform speciesspecific parental duties (Fisher 1998).

2. MAMMALIAN COURTSHIP ATTRACTION‘It was evidently a case of love at first sight, for she swam
about the new-comer caressingly...with overtures ofaffection’ (Darwin 1871/n.d.). Darwin was describing afemale Mallard duck. Blackbirds, thrush, black grouse,
pheasants, these and many other birds, were reported as‘fell in love with one another’ (Darwin 1871/n.d.).
A myriad of other descriptions of courtship attraction have been reported by ethologists (Andersson
1994). Gladikas (1995) reports of a free-ranging
orangutan living in the Tanjung Putting Reserve,
Borneo, ‘The object of TP’s adoration was Priscilla. I thought that TP would have chosen a more comely
female. But . TP was smitten with her . He couldn’t
take his eyes off her. He didn’t even bother to eat, so
enthralled was he by her balding charms’. Housing
Phil. Trans. R. Soc. B (2006)

conditions are likely to alter the display of mate
preferences among laboratory animals when notpresented with a choice, but free-ranging individuals
regularly exhibit sexual favouritism.
Yet despite hundreds of ethological descriptions ofcourtship attraction in a wide array of mammalian andavian species, ethologists have traditionally lumped thismotivation/emotion system together with the sex drive.
However, there are exceptions. Beach (1976) made a
distinction between the sex drive and the courtship
attraction, writing that the occurrence of copulation
depended as much on individual affinities and aversions as upon the presence or absence of sex hormones
and that proceptive and receptive behaviour in thefemale may depend upon different anatomical andneurochemical systems in the brain. Hutchison &Hutchison (1983) proposed that courtship entailed asequence of choices, each requiring different
mechanisms, and they questioned whether the sex
hormones had any specific role in the establishment
and expression of mating preferences. Pfaff (2002)
distinguishes between the hormone-dependent facilitation of sexual arousal and the expression of approachand other courtship behaviours, regarding these as
distinct aspects of mating behaviour and physiology.
Kendrick & Dixson (1986) have shown that anteromedial hypothalamic lesions block proceptivity but
not receptivity in the female common marmoset.
Finally, Goodall (1986) reported that males of many
primate species ‘show clear-cut preferences for particular females, which may be independent of cycle stage’.
Various neurochemical mechanisms have also been
associated with courtship attraction. Darwin
hypothesized that female mate preferences arose fromtheir innate sense of beauty. But he (understandably)offered no hypothesis regarding which specific neuralmechanisms might be involved (Darwin 1871/n.d.).
Miller (2000) noted that several faculties must have
evolved to discern and respond to the courtship traits ofdisplay producers, referring to this constellation ofneural mechanisms as ‘mental machinery’ and ‘sexual
choice equipment’. Miller (2000) also distinguishedbetween ‘cold choosers’, such as insects that become
attracted to ornamental displays without any sensationof pleasure, and ‘hot choosers’, animals whose choiceof mates is directed by subjective feelings of pleasure;and he proposed that the endorphins may be involvedin the mate choices of hot choosers. Beach (1976)
suggested that the monoamines were involved in mate
preference, saying, ‘The mating behaviour of female
rats treated with monoamine receptor blocking agentsindicates that lordotic behaviour and soliciting
behaviour may be mediated by anatomically andpossibly neurochemically distinct systems’.
Present research supports Beach’s hypothesis. Whena female laboratory-maintained prairie vole (Microtus
ochrogaster) is mated with a male, she forms a distinct
preference for him associated with a 50% increase in
dopamine in the nucleus accumbens (Gingrich et al.
2000). When a dopamine antagonist is injected into theaccumbens, the female no longer prefers this partner
and when a female is injected with a dopamine agonist,she begins to prefer the conspecific that is present at thetime of infusion, even if she has not mated with thisRomantic love
male (Wang et al. 1999; Gingrich et al. 2000). An
increase in central dopamine is also associated withcourtship attraction in female sheep (Fabre-Nys 1997,1998). In male rats, too, increased striatal dopamine
release has been shown in response to the presence of a
receptive female rat (Robinson et al. 2002; Montague
et al. 2004).
Recent data on several peptides also suggest that
central dopamine plays a role in regulating mate
preference. Kendrick & Dixson (1985) showed that inmarmosets, luteinizing hormone-releasing hormone
specifically facilitated female proceptive behaviours,
and oxytocin and vasopressin have been shown tofacilitate social recognition in mammalian species.
All of these peptides facilitate monoamine release(Kendrick 2000). Therefore, it has been suggested
that mate preference may be influenced as these
peptides rewire brain circuits so that sensory andother stimuli from specific individuals have morepotent effects on monoamine release, particularly
release of dopamine in brain reward centres (Limet al. 2004).
The extensive ethological literature on sexuallydimorphic traits that evolved to attract mates, inconjunction with the above physiological data on
mate preference in several species, suggests thatintersexual selection involves interactions between thedisplay traits of display producers and a brain system
for mate preference in display choosers, courtship
attraction. Moreover, the data suggest that the brain
system for courtship attraction is distinct from, yet
operates in tandem with, the sex drive to orchestrate
proceptivity in birds and mammals. Finally, thedopaminergic reward pathways may be involved.

3. HUMAN ROMANTIC LOVEIt was appropriate to investigate this brain system in
Homo sapiens for several reasons. Foremost, intenseromantic love is a cross-cultural universal. In a surveyof 166 societies, Jankowiak & Fischer (1992) foundevidence of romantic love in 147 of them. No negative
data were found; in the 19 remaining cultures,
anthropologists had failed to ask the appropriatequestions; all were cases of ethnographic oversight.
Jankowiak & Fischer (1992) concluded that romantic
love constitutes a ‘human universal . or near universal’.
Moreover, romantic love is associated with a specific
set of physiological, psychological and behaviouraltraits (Tennov 1979; Hatfield & Sprecher 1986; Shaver
et al. 1987; Hatfield et al. 1988; Harris & Christenfeld
1996; Fisher 1998; Gonzaga et al. 2001); and most ofthese traits are also characteristic of mammalian
courtship attraction, including increased energy, focused
attention, obsessive following, affiliative gestures,
possessive mate guarding, goal-oriented behaviours
and motivation to win a preferred mating partner(Fisher et al. 2002a,b; Fisher 2004).
Romantic love begins as an individual starts toregard another individual as special and unique. The
lover then focuses his/her attention on the beloved,
aggrandizing the beloved’s worthy traits and overlooking or minimizing his/her flaws. The lover
expresses increased energy, ecstasy when the love affair
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H. E. Fisher and others2175

is going well and mood swings into despair during timesof adversity. Adversity and barriers heighten romantic
passion, what has been referred to as ‘frustration
attraction’ (Fisher 2004). The lover suffers ‘separation
anxiety’ when apart from the beloved and a host of
sympathetic nervous system reactions when with the
beloved, including sweating and a pounding heart.
Lovers are emotionally dependent; they change theirpriorities and daily habits to remain in contact with
and/or impress the beloved. Smitten humans also
exhibit empathy for the beloved; many are willing tosacrifice, even die for this ‘special’ other. The lover
expresses sexual desire for the beloved, as well as
intense sexual possessiveness, mate guarding. Yet thelover’s craving for emotional union supersedes his/hercraving for sexual union with the beloved. Most
characteristic, the lover thinks obsessively about the
beloved, ‘intrusive thinking’. Rejected lovers firstexperience a phase of protest, during which they try
to win back the beloved and often feel abandonment
rage; then they move into the second stage of rejection,
associated with resignation and despair. Romantic loveis also involuntary, difficult to control and generally
impermanent.
Since romantic love shares many characteristics
with mammalian courtship attraction, it has been
hypothesized that this human preference system
would also be associated with the monoamines,
specifically elevated activity of central dopamine
and/or central norepinephrine (Liebowitz 1983; Fisher
1998).

4. ROMANTIC LOVE: FUNCTIONAL MAGNETICRESONANCE IMAGING RESEARCH
To investigate the constellation of neural correlates
associated with romantic love, Fisher, Aron, Brown andcolleagues recruited 10 women and 7 men who wereintensely in love. The age range was 18–26 years(MZ20.6; medianZ21); the reported duration of ‘being
in love’ was 1–17 months (MZ7.4; medianZ7). Eachparticipant was orally interviewed in a semi-structured
format to establish the duration, intensity and range of
his/her feelings of romantic love. Each also completed
the Passionate Love Scale (PLS), a 9-point Likert scale
self-report questionnaire which measures traits commonly associated with romantic love (Hatfield &Sprecher 1986; Cronbach’s alpha for questionnairereliability in this studyZ0.81; Cronbach 1951).
A preliminary investigation had identified a photograph of the beloved as an effective stimulus for eliciting
feelings of intense romantic love (Mashek et al. 2000).
Thus, the protocol employed photographs and consisted of four tasks presented in an alternating block
design: for 30 s, each participant viewed a photo of his/her beloved (positive stimulus); for the following 40 s,each performed a countback distraction task; for thefollowing 30 s, each viewed a photograph of anemotionally neutral acquaintance (neutral stimulus);
and for the following 20 s, each performed a similarcountback task. The countback task involved viewing alarge number, such as 8421, and mentally counting
backwards (beginning with this number) in incrementsof seven. We included the countback task to decrease

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Romantic lovethe carry-over effect after the participant viewed thepositive stimulus because it is difficult to quell intense
feelings of romantic love. This four-part sequence (or acounterbalanced version beginning with the neutral
stimulus) was repeated six times; the total stimulus
protocol was 720 s (12 min). Pre-scanning instructions
were to think about a non-sexual euphoric experience
with the beloved; post-scanning interviews establishedthat the participants had engaged in romantic thinking
and feeling.
Group activation specific to the beloved occurred inseveral regions, including the right ventral tegmental
area (VTA) localized in the region of A10 dopamine
cells (Aron et al. 2005). The VTA is a central region of
the brain’s reward system (Wise 1996; Schultz 2000;
Martin-Soelch et al. 2001), associated with pleasure,general arousal, focused attention and motivation to
pursue and acquire rewards (Schultz 2000; Delgado
et al. 2000; Elliot et al. 2003).
The VTA sends projections to several brain
regions (Gerfen et al. 1987; Oades & Halliday 1987;
Williams & Goldman-Rakic 1998), including thecaudate nucleus where we also found group activations,specifically in the right medial and postero-dorsal body(Aron et al. 2005). The caudate plays a role in reward
detection and expectation, the representation of goals
and the integration of sensory inputs to prepare foraction (e.g. Schultz 2000; Martin-Soelch et al. 2001;
Lauwereyns et al. 2002; O’Doherty et al. 2002). Zald
et al. (2004) found that predictable monetary reward
presentation caused dopamine release in the medial
caudate body where we found activation.
Using functional magnetic resonance imaging(fMRI), Bartels & Zeki (2000) also investigated brain
activity in 17 men and women who reported being‘truly, deeply and madly in love’. Eleven were women;
all looked at a photograph of his/her beloved, as well as
photographs of three friends of similar age, sex andlength of friendship. But the participants in that study
had been in love substantially longer than those in ourstudy (28.8 months versus 7.4 months t[32]Z4.28,
p!0.001). They were also less intensely in love. Thiswas established because both study groups were(serendipitously) administered the same questionnaire
on romantic love, the PLS (respective scores were 7.55
versus 8.54, t[31]Z3.91, p!0.001). In spite of thesedifferences in protocol, Bartels & Zeki (2000, 2004)
found activity in regions of the ventral tegmental area
and caudate nucleus, as we did.
These data are consistent with the above animal
literature, suggesting that mesolimbic dopamine
pathways in the reward system of the brain play a rolein the pleasurable feelings, focused attention,
motivation and goal-oriented behaviours associatedwith romantic love. However, activation of subcortical
dopaminergic pathways of the VTA and caudate
nucleus may comprise only the ‘general arousal’component (Pfaff 1999) of this brain system for mate
preference and mate pursuit (Fisher 2004).
Other neurotransmitters are likely to be involved,
including glutamate in the mesocortical system, owing
to their role in the release of dopamine in the VTA(Legault & Wise 1999) and/or their fast signals in theprefrontal cortex regarding reward (Lavin et al. 2005).
Phil. Trans. R. Soc. B (2006)

Central norepinephrine may also be associated withcourtship attraction (Fisher 1998). This was
hypothesized because increased activity of norepinephrine generally produces alertness, energy,
sleeplessness and loss of appetite (Coull 1998; Robbins
et al. 1998), increased attention (Posner & Peterson
1990) and increased memory for new stimuli (Griffin &Taylor 1995), some of the primary characteristics ofhuman romantic love (Tennov 1979; Hatfield &Sprecher 1986; Fisher 2004). As norepinephrine isalso associated with peripheral sympathetic nervous
system responses, including increased heart rate,
sweating and trembling, central norepinephrine may
contribute to these aspects of romantic love/courtship
attraction as well (Fisher 1998).
The above data suggest that mammalian courtship
attraction and human romantic love are associated withdopaminergic reward pathways in the brain. These dataalso support the hypothesis that romantic love isdistinct from the sex drive (Aron & Aron 1991; Fisher
1998).

5. THE SEX DRIVE
The sex drive is characterized by the urge for sexual
gratification. It is associated with the androgens andoestrogens in non-primate mammalian species andprimarily with the androgens in many primates,
especially humans (Edwards & Booth 1994; Sherwin
1994; Van Goozen et al. 1997). Humans with higher
circulating levels of testosterone tend to engage in moresexual activity (Edwards & Booth 1994; Sherwin
1994). Women tend to feel more sexual desire during
and around ovulation, when testosterone activity
increases (Van Goozen et al. 1997). Both sexes havefewer sexual fantasies, masturbate less regularly andengage in less intercourse as levels of the androgens
decline with age (Edwards & Booth 1994).
The balance between the androgens, oestrogens andother bodily systems, as well as childhood and adultexperiences and a host of other biological andenvironmental factors play a role in when, where andhow often individuals express the sex drive (Nyborg
1994). Nevertheless, the androgens are central to thesex drive and these gonadal and adrenal hormones havenot been associated with human romantic love. Moreover, when humans self-administer androgens to boost
sex drive, they do not report that they fall in love. These
two neural systems do not always act in tandem in
Homo sapiens.
Several fMRI studies support the hypothesis that thesex drive is associated with specific networks of brain
activation and that these networks are largely distinct
from those associated with human romantic love/
mammalian courtship attraction. Arnow et al. (2002)
reports that when young male heterosexual subjects
look at erotic video material while wearing a custombuilt pneumatic pressure cuff around the penis, theirsexual arousal is associated with strong activations in
the right subinsular region, including the claustrum,
left caudate and putamen, right middle occipital/
middle temporal gyri, bilateral cingulate gyrus, rightsensorimotor and pre-motor regions, and righthypothalamus.

Romantic love
Using fMRI, Beauregard et al. (2001) measured
brain activation in men as they viewed erotic film
excerpts. Activations occurred in limbic and paralimbic
structures, including the right amygdala, rightanterior temporal pole and hypothalamus. Using
fMRI, Karama et al. (2002) also recorded brain activity
while men and women viewed erotic film excerpts.
Activity increased in the anterior cingulate, medial
prefrontal cortex, orbitofrontal cortex, insula andoccipitotemporal cortices, as well as in the amygdala
and ventral striatum. Men showed activation in thethalamus and significantly greater activation than
women in the hypothalamus, specifically in a sexuallydimorphic area associated with sexual arousal andbehaviour. Animal studies also indicate that several
brain structures are associated with the sex drive andsexual expression, including the medial amygdala,medial preoptic area, paraventricular nucleus andperiaqueductal gray (PAG; Heaton 2000), as well as
the septum and the ventromedial hypothalamus(Dixson 1998).
Although the neural regions associated with the sex
drive overlap those associated with courtship attraction, these two neural systems show many differences,suggesting that the primary brain system for the sex
drive is distinct from the brain system associated withhuman romantic love (Aron & Aron 1991; Fisher
1998). Anecdotal behavioural data in humans support
this hypothesis. (i) The sex drive is focused on a specificgoal, sexual union with another, and romantic love isfocused on a different goal, emotional union withanother. (ii) The sex drive is often expressed towards a
range of individuals and romantic love is focused on one
particular individual. (iii) The sex drive is often
temporarily quelled when satisfied and romantic love
does not decrease with coitus and often persists
unabated for months, even years. (iv) Most liberated
adults have engaged in coitus with individuals forwhom they felt no romantic love and many have also
been ‘in love’ with someone with whom they have hadno physical contact.
Several lines of investigation indicate that the sex
drive and the courtship attraction/romantic love are
distinct neural systems, designed to orchestratedifferent aspects of the reproductive process. The sex
drive enables individuals to initiate courtship andmating with a range of partners; courtship attraction/
romantic love motivates them to focus their matingenergy on specific individuals, thereby conserving timeand metabolic energy.
Nevertheless, the brain systems for the sex drive andthe courtship attraction regularly interact to coordinate
mammalian mate choice.

6. THE SEX DRIVE AND MATE PREFERENCE:
INTERACTIONS
The biological relationships between the sex drive andthe courtship attraction are most likely dose dependentand variable, depending on which brain regions are
involved and many other biological and environmental
factors. However, data suggest that these brain systems
have a positive correlation.
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2177

Animal studies indicate that elevated activity of
dopaminergic pathways can stimulate a cascade ofreactions, including the release of testosterone andoestrogen (Wenkstern et al. 1993; Kawashima &Takagi
1994; Ferrari & Giuliana 1995; Hull et al. 1995, 1997,
2002; Szezypka et al. 1998; Wersinger & Rissman
2000). Likewise, increasing levels of testosterone andoestrogen promote dopamine release (Hull et al. 1999;
Auger et al. 2001; Becker et al. 2001; Appararundaram
et al. 2002; Creutz & Kritzer 2002; Pfaff 2005). When amale rat is placed in an adjacent cage, where he can seeor smell an oestrous female, activity of central
dopamine increases and contributes to sexual arousaland pursuit of the female (West et al. 1992; Wenkstern
et al. 1993; Hull et al. 1995, 1997, 2002). When thebarrier is removed and the male is allowed to copulate,activity of dopamine continues to rise in the medialpreoptic area (Hull et al. 1995). When dopamine isinjected into specific brain regions of the male rat, theinfusion stimulates copulatory behaviour (Ferrari &Giuliana 1995). Blocking the activities of central
dopamine in rats diminishes several proceptive sexual
behaviours, including hopping and darting (Herbert
1996). Finally, electrochemical studies in male rats
show increased dopamine release in the dorsal and theventral striatum in response to the presence of a
receptive female rat (Robinson et al. 2002; Montague
et al. 2004). Pfaff (2005) reports that in male rats,
dopamine increases male sexual behaviour in at least
three ways: it increases sexual arousal and courtshipbehaviour; it potentiates the motor acts of mounting;and it facilitates genital responses to stimulation.
This positive relationship between elevated activityof central dopamine, elevated sex steroids and elevatedsexual arousal and sexual performance (Herbert 1996;
Fiorino et al. 1997; Liu et al. 1998; Pfaff 2005) also
occurs in humans (Walker et al. 1993; Clayton et al.
2000; Heaton 2000). When individuals exhibiting
hypoactive sexual desire disorder are treated withdopamine-enhancing medications, libido improves(Segraves et al. 2001). When patients suffering fromdepression take drugs that elevate central dopamine
activity, their sex drive often improves (Walker et al.
1993; Ascher et al. 1995; Coleman et al. 1999). In fact,
since elevated activity of central serotonin is inhibitory
to the sex drive (Rosen et al. 1999; Montejo et al. 2001),
some patients taking serotonin-enhancing antidepressants supplement this therapy with medications thatelevate the activity of dopamine (and norepinephrine)
solely to maintain or elevate sexual appetite and arousal(Walker et al. 1993; Ascher et al. 1995; Coleman et al.
1999; Rosen et al. 1999).
Animal studies indicate that norepinephrine is also
positively linked with sexual motivation and sexual
arousal (Van Bockstaele et al. 1989; Clayton et al. 2002;
Fraley 2002; Pfaff 2005). When a female prairie vole is
exposed to a drop of male urine on the upper lip,
norepinephrine in the olfactory bulb contributes to therelease of oestrogen and concomitant proceptive
behaviour (Dluzen et al. 1981). The reverse also
occurs; oestradiol and progesterone contribute to therelease of norepinephrine in the hypothalamus to
produce lordosis in rats (Etgen et al. 1999). Moreover,when ovariectomized, sexually receptive female rats

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H. E. Fisher and others

Romantic lovereceive injections of oestrogen and are then permitted
to mate, copulation produces the release of norepinephrine in the lateral ventromedial hypothalamus(Etgen & Morales 2002). Drug users attest to thispositive chemical relationship between norepinephrine
and the sex drive. In the right oral dose, amphetamines(norepinephrine and dopamine agonists) enhancesexual desire (Buffum et al. 1988).
The complex interaction between these catecholamines and gonadal hormones suggests why the sex
drive and the courtship attraction have traditionallybeen lumped into a single behavioural category,proceptivity. Instead, these distinct neural systems
appear to work in tandem to enable display choosers
to explore an array of mating partners, focus theircourtship attention on preferred individuals and thensustain attraction and sexual arousal long enough tocomplete species-specific mating behaviours.

7. PARTNER ATTACHMENT
The full array of brain systems associated with courtship, mating and parenting and the interactions
between these brain systems need further investigation(Fisher & Thomson in press). Nevertheless, theavailable literature suggests that at least three distinct,
yet interrelated neural systems play a role in reproduction: the sex drive, courtship attraction and partner
attachment. Each of these motivation/emotion systems
is associated with a different behavioural repertoire,each is associated with a different and dynamic
constellation of neural correlates and each evolved todirect a different aspect of reproduction (Fisher 1998).
The relationship between courtship attraction/romantic love and the sex drive has been discussed above, andpartner attachment is considered next.
Partner attachment, or pairbonding, in birds andmammals is characterized by mutual territory defence
and/or nest building, mutual feeding and grooming,
maintenance of close proximity, separation anxiety,shared parental chores and affiliative behaviours. The
ethological literature commonly infers that this constellation of attachment behaviours associated withpairbonding evolved primarily to motivate mating
partners to sustain an affiliative connection longenough to complete species-specific parental duties.
This parental attachment system has been associatedwith the activity of the neuropeptides, oxytocin (OT) in
the nucleus accumbens and arginine vasopressin (AVP)in the ventral pallidum (Carter 1992; Winslow et al.
1993; Wang et al. 1994; Carter et al. 1997; Young et al.
1998; Lim & Young 2004; Lim et al. 2004), although
the brain’s opioid system (Moles et al. 2004) and otherneural systems are involved as well (Kendrick 2000).
Bowlby (1969, 1973) and Ainsworth et al. (1978)
proposed that, to promote survival of the young,
primates have evolved an innate attachment systemdesigned to motivate infants to seek comfort and safety
from their primary caregiver, generally their mother.
More recently, researchers have emphasized that this
attachment system remains active throughout their lifeand serves as a foundation for attachment between
spouses as they raise children (Hazan & Shaver 1987;
Hazan & Diamond 2000). Data from the Demographic
Phil. Trans. R. Soc. B (2006)

Yearbooks of the United Nations on 97 societies
suggest the prevalence of this attachment system inhumans. Approximately 93.1% of women and 91.8%
of men marry by age 49 (Fisher 1992). Pairbonding
and attachment behaviours are central aspects of themulti-part human reproductive strategy (Fisher 1992).
Hatfield (1988) refers to feelings of attachment ascompanionate love, which she defines as ‘a feeling ofhappy togetherness with someone whose life has
become deeply entwined with yours’. Extensive
research has been done on this attachment system inadults (Fraley & Shaver 2000), but this literature does
not regularly distinguish between feelings of attachment and feelings of romantic love (Aron et al. 2006).
However, cross-cultural and historical data indicatethat people in other societies and centuries do
distinguish between feelings of romantic love andattachment.
Nisa, a !Kung Bushman woman of the Kalahari
Desert, Botswana, reported, ‘When two people are first
together, their hearts are on fire and their passion isvery great. After a while, the fire cools and that’s how it
stays. They continue to love each other, but it’s in adifferent way–-warm and dependable’ (Shostak 1981).
The Taita of Kenya say that love comes in two forms, anirresistible longing, a ‘kind of sickness’, and a deep
enduring affection for another (Bell 1995). In Korea,‘sarang’ is a word close to the western concept ofromantic love, while ‘chong’ is more like feelings oflong-term attachment; Abigail Adams, wife of America’s second president, distinguished these feelings
when writing to John Adams in 1793, ‘Years subdue
the ardor of passion, but in lieu thereof friendship andaffection deep-rooted subsists, which defies the ravagesof time’ (McCullough 2001).
Current brain imaging investigations in humans andanimal studies indicate some of the neural correlates ofthis attachment mechanism. These data also suggestthat the neural correlates for attachment are distinct
from those for early-stage intense romantic love inhumans and courtship attraction in other mammalian
species, yet these two brain systems interact.

8. NEUROIMAGING AND ANIMAL STUDIESOF ATTACHMENT
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 timecompared with our participants who were in love foran average of 7.4 months (Aron et al. 2005); theirsubjects were less passionately in love (Aron et al.
2005). Their participants also exhibited activity inseveral brain regions where our subjects showed none,
including the anterior cingulate cortex and midinsular cortex.
These varying results stimulated us to examine thesubset 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).

Romantic loveThus, we confirmed Bartels & Zeki’s (2000) findingsthat the anterior cingulate and insular cortex are
involved in longer term love relationships.
More relevant to this discussion, we also foundactivation in the ventral putamen/pallidum (Aron et al.
2005). Activity in this region, associated with a specificdistribution pattern of vasopressin (V1a) receptors, hasbeen 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 theventral 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 inthe ventral pallidum, specifically associated withvasopressin, is evident in other pairbonding/attachingmammals.
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 ofinfusion; and Lim, Murphy and Young report thatwhen 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 differencesin the V1 receptor gene of socially monogamous malevoles (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 tocohabit with her, even though they had not mated withthis female. Lim, Young and colleagues report thatwhen they transfected this genetic variant (the monogamous version) into the pallidum of meadow voles, anasocial promiscuous species, vasopressin receptors
were upregulated; each male also began to fixate on aparticular female and mate exclusively with her, eventhough other females were available (Lim et al. 2004).
The activities of central oxytocin and vasopressin
have been associated with both partner preference andPhil. Trans. R. Soc. B (2006)

H. E. Fisher and others2179

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 andother pairbonding creatures engage in sex, copulation
triggers the activity of vasopressin in the ventral
pallidum and oxytocin in the nucleus accumbens andfacilitates 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 V1areceptor for vasopressin in the ventral pallidum) mostprobably feel attraction, but do not associate thispleasurable feeling with their specific mating partner sothey do not initiate a longer term attachment. In
species that do not form these bonds, this relationshipwith dopamine reward centres is much weaker(Kendrick 2000).
Like the brain systems for the sex drive and thecourtship attraction, the neural mechanism for
attachment is complex, flexible, varies in its thresholdand intensity and is most likely integrated with manyother 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 workin tandem in a pairbonding species, motivating
individuals to prefer a specific mating partner andalso motivating them to form an attachment to thismate. 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 lovesupport 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 eachlooked at a photo of her own infant, an infant withwhom 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 regionsthat differed from those associated with romantic love,
including the lateral orbitofrontal cortex and the PAG.
Maternal love also activated some brain regions thatwere 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 loveoverlapped in brain areas rich in oxytocin andvasopressin receptors, including the substantia nigra(Bartels & Zeki 2004).
The neural flexibility of these brain systems forreproduction and their interactions with one anotherand other brain systems are complex (Kendrick 2000).
For example, central dopamine (and norepinephrine)
can stimulate the release of oxytocin and vasopressin inneurohypophyseal tissues (Kendrick et al. 1992;
Ginsberg et al. 1994; Galfi et al. 2001); but increasing

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H. E. Fisher and others

Romantic loveactivity of central dopamine can also inhibit release ofcentral oxytocin (Seybold et al. 1978; Vizi & Volbekas
1980). Increasing activity of central oxytocin canstimulate release of norepinephrine and dopamine(Kendrick 2000) or interfere with dopamine andnorepinephrine 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 thisgene region is subject to a number of polymorphismsthat contribute to variability in the strength of monogamous bonding in male prairie voles (Hammock &Young 2005). The Homo sapiens version of this genehas similar polymorphisms, which might contributeto individual differences in human monogamous
pairbonding as well.
The above data suggest that the mammalianattachment system is distinct from, yet interacts with,
the neural mechanisms for courtship attraction and thesex drive. This flexible, combinatorial system would
provide individuals of myriad species with the range ofmotivations, 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.

9. REJECTION IN LOVE
Romantic love is expressed in many graded forms, but
it has two extremes: love that is returned and love that is
rejected. To understand the range of neuralmechanisms associated with mate choice, Fisher,Aron, Brown and colleagues used fMRI to study 10
women and 5 men who were still very much in love but
had recently been rejected by their romantic partner(Fisher et al. 2005a,b). We used the same protocol aswith our happily in-love subjects (Aron et al. 2005).
Rejected participants alternately viewed a photographof their abandoning beloved (positive stimulus) and aphotograph of a familiar, emotionally neutral individual (neutral stimulus), interspersed with a distraction–
attention task.
Preliminary analysis of the positive–neutral contrast
showed significant group effects in the right nucleus
accumbens/ventral putamen/pallidum, lateral orbitofrontal cortex and anterior insular/operculum cortex(Fisher et al. 2005a,b). We then compared these data on
rejected lovers with the results from our study of 17
happily in-love individuals (Aron et al. 2005). Rejected
lovers expressed significantly greater activity in theventral striatum/putamen/pallidum than did those who
were happily in love (figure 1).
Other studies have shown that the nucleus accumbens/ventral pallidum/putamen region where we foundactivity becomes more active as an individual chooses ahigh-risk investment associated with big gains or big
losses, making it an uncertain gain (Kuhnen &Knutson 2005), or anticipates a money reward (Zaldet al. 2004); data from rat studies are consistent with
the idea that the nucleus accumbens core is importantfor choices for uncertain rewards and delayed
reinforcement (e.g. Cardinal & Howes 2005); activity
Phil. Trans. R. Soc. B (2006)

–10

–8

–6

Figure 1. Three axial sections through the human brain at
2 mm intervals show a consistent activation difference
between a group happily in love and a group in love but
recently rejected (yellow colour, p!0.01). Those who wererecently rejected show greater activation in the right ventral
putamen–pallidum and accumbens core (side definition isradiological convention) than those who were happily in love.
These regions have been associated with reward, especiallyuncertain large gains and losses in gambling, and uncertain
reinforcement in rats. (Figure data from Aron et al. 2005 anda preliminary report, Fisher et al. 2005a,b).

in the nucleus accumbens has also been associated withpairbond formation and maintenance in prairie voles(Lim et al. 2004). The region of the anterior insula/
operculum cortex where we found activity has been
associated with skin and muscle pain and with anxiety(Schreckenberger et al. 2005). The region of the lateralorbitofrontal cortex where we found activity has been
associated with theory of mind (Vollm et al. 2006),
evaluating punishers (Kringelbach & Rolls 2004),
implementing appropriate adjustments in behaviour(Ridderinkhof et al. 2004), obsessive/compulsive
behaviours (Evans et al. 2004) and with controlling
anger in recently abstinent cocaine-dependent individuals (Goldstein et al. 2005).
These results suggest that brain systems associatedwith reward and motivation remain active in recently
romantically rejected men and women, but differ intheir precise location. These preliminary results alsosuggest that neural regions associated with risk-taking
for big gains or losses, physical pain, obsessive/compulsive behaviours, ruminating on the intentions andactions of the rejecter, evaluating options, and emotion
regulation increase in their activity when someone isrejected by a beloved.
Our study is the second investigation of romantic
rejection. Najib et al. (2004) studied nine women who
were ‘actively grieving’ over a recent romantic breakup. Our preliminary comparisons uncovered nocommonalities; in fact, in several regions where wefound activations, they found deactivations. Since our
subjects regularly reported anger and hope for reconciliation, while subjects in the Najib et al. (2004) study
more regularly reported acceptance, we suspect that
our subjects were in the initial stage of romantic
rejection, the protest phase, while their participants
were largely in the subsequent resignation/despair
phase.
The combined aforementioned data may contributeunderstanding to the high cross-cultural rates ofstalking, homicide, suicide and clinical depression
associated with rejection in love (Meloy & Fisher
2005).

Romantic love
10. THE DRIVE TO LOVEThe psychological literature distinguishes between
emotions (affective states of feeling) and motivations(brain systems oriented around the planning andpursuit of a specific want or need). Aron has proposedthat romantic love is not primarily an emotion, but amotivation system designed to enable suitors to build
and maintain an intimate relationship with a preferredmating partner (Aron & Aron 1991; Aron et al. 1995).
The fMRI and animal experiments we have reviewed
above support Aron’s hypothesis. The VTA is directly
associated with motivation- and goal-oriented
behaviours, as is the caudate nucleus. Moreover, thecaudate nucleus has widespread afferents from all of thecortex except primary visual areas (Kemp & Powell1970; Selemon & Goldman-Rakic 1985; Saint-Cyr
et al. 1990; Eblen & Graybiel 1995; Flaherty &Graybiel 1995) and is organized to integrate diverse
sensory, motor and limbic functions (Brown 1992;
Parthasarathy et al. 1992; Eblen & Graybiel 1995;
Parent & Hazrati 1995; Parent et al. 1995; Brown et al.
1998; Haber 2003). Thus, regions of the caudate
nucleus could effectively integrate the behavioural andbiological actions associated with a complex state, suchas romantic love.
In fact, these findings suggest that romantic love isa primary motivation system, a fundamental humanmating drive (Fisher 2004). Pfaff (1999) defines adrive as a neural state that energizes and directs
behaviour to acquire a particular biological need tosurvive or reproduce and he reports that all drives areassociated with the activity of dopaminergic pathways
and a few other specific neural systems (as well asother neural systems specific to each individual drivestate). Romantic love has many characteristics incommon with drives (Fisher 2004). (i) Like drives,
romantic love is tenacious and emotions ebb and flow,(ii) romantic love is focused on a specific reward andemotions are associated with a range of phenomena
instead, (iii) romantic love is not associated with adistinct facial expression and the primary emotions
are all associated with specific facial expressions,(iv) romantic love is difficult to control and all of thebasic drives are difficult to control, and (v) humanromantic love and mammalian courtship attraction
are associated with dopamine-rich neural regions andall the basic drives are also associated with dopaminergic pathways. Drives lie along a continuum. Thirstis almost impossible to control, while the sex drive
can be redirected, even quelled. Romantic love isevidently stronger than the sex drive because when
one’s sexual overtures are rejected, people do not killthemselves or someone else. Instead, abandoned
lovers sometimes stalk, commit suicide or homicide
or fall into a clinical depression.
More investigations need to be made to understandthe flexibility, variability and durability of this neuralmechanism for mate choice, romantic love. Data could
be collected on how the neural mechanisms forromantic love vary in conjunction with specifictraumatic childhood experiences; how specific personality profiles affect the biological expression of romantic
love; how specific diseases, such as schizophrenia andParkinson’s disease, and addictions, such as cocaine,Phil. Trans. R. Soc. B (2006)

H. E. Fisher and others

2181

amphetamine and alcohol addiction, facilitate or
inhibit the biological expression of romantic love;
how the constellation of neural correlates associatedwith romantic love varies during the course of a longterm relationship; how the biology of romantic love
varies according to sexual orientation; and how thisbrain system varies in cultures with different marital
patterns and in different mammalian species withdiverse reproductive strategies. More research into
the brain mechanisms associated with romantic love
may also help to explain some of the basic principles ofbrain lateralization and lend further understanding of
the reward system and its interactions with cognitiveand emotional processes that together produce
complex behaviours.
It might also be valuable to investigate genderdifferences in the constellation of neural correlates
associated with early stage (and later stage) romantic
love. In a preliminary study of gender differences, we
did a between-subject analysis of our 10 women and 7
men who were happily in love. Although men andwomen were similar in many ways, we did find genderdifferences. Men tended to show more activity than
women in a region of the right posterior dorsal insulathat has been correlated with penile turgidity (Arnow
et al. 2002) and male viewing of beautiful faces (Aharon
et al. 2001). Men also showed more activity in regions
associated with the integration of visual stimuli(Narumoto et al. 2001). Women tended to show more
activity than men in regions associated with attention,
memory and emotion (Gray et al. 2002; Maddock et al.
2003; Velanova et al. 2003).
Extensive cross-cultural data indicate that courting
men respond more strongly than women to visualsignals of youth and beauty (Buss et al. 1990); hence,
we speculate that the above male activation pattern
evolved, in part, to enable ancestral men to respond tothe visual signals of women who could bear them viable
young (Fisher 2004). Cross-cultural data indicate thatwomen are more attracted than men to potential mates
who offer status and resources (Buss et al. 1990). To
calculate the reproductive value of a man, a woman
must remember the promises and provisioning recordof her potential partner. Thus, we speculate that theabove female activation pattern evolved, in part, toenable ancestral women to remember male behaviour
patterns and thus make adaptive long-term matechoices (Fisher 2004). But more research is necessary
to confirm this hypothesis, to establish the culturalvariables that contribute to gender differences and tofind more gender differences in the brain associatedwith romantic love.
We expect that human romantic love will be found toengage a wide range of varying, overlapping anddynamic brain systems, as would be appropriate of amulti-faceted phenomenon that has significant social,reproductive and genetic consequences. Nevertheless,the primary neural correlates associated with intense,
early-stage romantic love are likely to remain similar
across individuals and cultures, even among species,
because this neural mechanism evolved to direct a
crucial aspect of mammalian reproduction, matechoice.

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Romantic love

REFERENCES
Aharon, I., Etcoff, N., Ariely, D., Chabris, C. F., O’Connor,
E. & Breiter, H. C. 2001 Beautiful faces have variable
reward value: fMRI and behavioral evidence. Neuron 32,
537–551.
Ainsworth, M. D. S., Blehar, M. C., Waters, E. & Wall, S.
1978 Patterns of attachment: a psychological study of thestrange situation. Hillsdale, NJ: Erlbaum.
Andersson, M. 1994 Sexual selection. Princeton, NJ: Princeton University Press.
Appararundaram, S., Huller, J., Lakhlani, S & Jennes L. 2002
Ovariectomy-induced alterations of choline and dopaminetransporter activity in the rat brain. Society for Neuroscience
Abstract Viewer/Itinerary Planner: p.368.20.
Arnow, B. A., Desmond, J. E., Banner, L. L., Glover, G. H.,
Solomon, A., Polan, M. L., Lue, T. F. & Atlas, S. W. 2002
Brain activation and sexual arousal in healthy, heterosexual males. Brain 125, 1014–1023.
Aron, A. & Aron, E. N. 1991 Love and sexuality. In Sexuality
in close relationships (ed. K. McKinney & S. Sprecher),pp. 25–48. Hillsdale, NJ: Lawrence Erlbaum.
Aron, A., Paris, M. & Aron, E. N. 1995 Falling in love:prospective studies of self-concept change. J. Pers. Social
Psychol. 69, 1102–1112.
Aron, A., Fisher, H. E., Mashek, D. J., Strong, G., Li, H. F. &Brown, L. L. 2005 Reward, motivation and emotion
systems associated with early-stage intense romantic love:an fMRI study. J. Neurophysiol. 94, 327–337.
Aron, A., Fisher, H. E. & Strong, G. 2006 Romantic love. In
The Cambridge handbook of personal relationships (ed.
D. Perlman & A. Vangelisti). Cambridge, MA: Cambridge
University Press.
Ascher, J. A. et al. 1995 Bupropion: a review of its mechanismof antidepressant activity. J. Clin. Psychiatry 56, 396–402.
Auger, A. P., Meredith, J. M., Snyder, G. L. & Blaustein, J. D.
2001 Oestradiol increases phosphorylation of a dopamineand cyclic AMP-regulated phosphoprotein (DARPP-32)
in female rat brain. J. Neuroendocrinol. 13, 761–768.
Bartels, A. & Zeki, S. 2000 The neural basis of romantic love.
Neuroreport 11, 3829–3834.
Bartels, A. & Zeki, S. 2004 The neural correlates of maternal
and romantic love. NeuroImage 21, 1155–1166.
Beach, F. A. 1976 Sexual attractivity, proceptivity, andreceptivity in female mammals. Horm. Behav. 7, 105–138.
Beauregard, M., Levesque, J. & Bourgouin, P. 2001 Neuralcorrelates of conscious self-regulation of emotion.
J. Neurosci. 21, RC165.
Becker, J. B., Rudick, C. N. & Jenkins, W. J. 2001 The role ofdopamine in the nucleus accumbens and striatum during
sexual behavior in the female rat. J. Neurosci. 21,
3236–3241.
Bell, J. 1995 Notions of love and romance among the Taita of
Kenya. In Romantic passion: a universal experience? (ed.
W. Jankowiak). New York, NY: Columbia University
Press.
Bester-Meredith, J. K., Young, L. J. & Marler, C. A. 1999
Species differences in paternal behavior and aggression in
Peromyscus and their associations with vasopressin immunoreactivity and receptors. Horm. Behav. 36, 25–38.
Bowlby, J. 1969. Attachment and loss: attachment, vol. 1. New
York, NY: Basic Books.
Bowlby, J. 1973. Attachment and loss: separation, vol. 2. New
York, NY: Basic Books.
Brown, L. L. 1992 Somatotopic organization in rat striatum:
evidence for a combinational map. Proc. Natl Acad. Sci.
USA 89, 7403–7407.
Brown, L. L., Smith, D. M. & Goldbloom, L. M. 1998
Organizing principles of cortical integration in the rat
Phil. Trans. R. Soc. B (2006)

neostriatum: corticostriate map of the body surface is anordered lattice of curved laminae and radial points.
J. Comp. Neurol. 392, 468–488.
Buffum, J., Moser, C. & Smith, D. 1988 Street drugs andsexual function. In Handbook of sexology, vol. 6 (ed.
J. M. A. Sitsen) The pharmacology and endocrinology ofsexual function. New York, NY: Elsevier Science
Publishers.
Buss, D. M. et al. 1990 International preferences in selecting
mates: a study of 37 societies. J. Cross Cult. Psychol. 21,
5–47.
Cardinal, R. N. & Howes, N. J. 2005 Effects of lesions of theaccumbens core on choice between small uncertain
rewards in rats. BMC Neurosci. 6, 37–56.
Carter, C. S. 1992 Oxytocin and sexual behavior. Neurosci.
Biobehav. Rev. 1, 131–144.
Carter, C. S., DeVries, A., Taymans, S. E., Roberts, R. L.,
Williams, J. R. & Getz, L. L. 1997 Peptides steroids, andpair bonding. In The integrative neurobiology of affiliation,
vol. 807 (ed. C. S. Carter, I. I. Lederhendler & B.
Kirkpatrick), pp. 260–272. Annals of the New York
Academy of Sciences, New York, NY: The New York
Academy of Sciences.
Clayton, A. H. et al. 2000 Bupropion as an antidote to SSRIinduced sexual dysfunction. Poster presented at the New
Clinical Drug Evaluation Unit Program (NCDEU), Boca
Raton, FL.
Clayton, A. H., Pradko, J. F., Croft, H. A., Montano, C. B.,
Leadbetter, R. A., Bolden-Watson, C., Bass, K. I.,
Donahue, R. M., Jamerson, B. D. & Metz, A. 2002
Prevalence of sexual dysfunction among newer antidepressants. J. Clin. Psychiatry 63, 357–366.
Coleman, C. C., Cunningham, L. A., Foster, V. J., Batey,
S. R., Donahue, R. M. J., Houser, T. L. & Ascher, J. A.
1999 Sexual dysfunction associated with the treatment ofdepression: a placebo-controlled comparison of buproprion sustained release and sertraline treatment. Ann.
Clin. Psychiatry 11, 205–215.
Coull, J. 1998 Neural correlates of attention and arousal
Insights from electrophysiology, functional neuroimaging
and psychopharmacology. Prog. Neurobiol. 55, 343–361.
Creutz, L. M. & Kritzer, M. F. 2002 Estrogen receptorbeta immunoreactivity in the midbrain of adult rats:
regional, subregional, and cellular localization in the
A10, A9, and A8 dopamine cell groups. J. Comp. Neurol.
446, 288–300.
Cronbach, L. J. 1951 Coefficient alpha and the internal
structure of tests. Psychometrika 16, 297–334.
Darwin, C. 1871/n.d. The descent of man and selection
in relation to sex. New York, NY: The Modern Library/
Random House.
Davidson, R. J. 1994 Complexities in the search for emotionspecific physiology. In The nature of emotion: fundamental
questions (ed. P. Ekman & R. J. Davidson). New York, NY:
Oxford University Press.
Delgado, M. R., Nystrom, L. E., Fissell, C., Noll, D. C. &Fiez, J. A. 2000 Tracking the hemodynamic responses toreward and punishment in the striatum. J. Neurophysiol.
84, 3072–3077.
Dixson, A. F. 1998 Primate sexuality. Oxford, UK: Oxford
University Press.
Dluzen, D. E., Ramirez, V. D., Carter, C. S. & Getz, L. L.
1981 Male vole urine changes luteinizing hormonereleasing hormone and norepinephrine in female olfactorybulb. Science 212, 573–575.
Eblen, F. & Graybiel, A. M. 1995 Highly restricted origin of
prefrontal cortical inputs to striosomes in the macaquemonkey. J. Neurosci. 15, 5999–6013.

Romantic love
Edwards, J. N. & Booth, A. 1994 Sexuality, marriage, andwell-being: the middle years. In Sexuality across the life
course (ed. A. S. Rossi). Chicago, IL: University of Chicago
Press.
Elliott, R., Newman, J. L., Longe, O. A. & Deakin, J. W. F.
2003 Differential response patterns in the striatum andorbitofrontal cortex to financial reward in humans: aparametric functional magnetic resonance imaging study.
J. Neurosci. 23, 303–307.
Etgen, A. & Morales, J. C. 2002 Somatosensory stimuli
evoke norepinephrine release in the anterior ventromedial hypothalamus of sexually receptive female rats.
J. Neuroendocrinol. 14, 213–218.
Etgen, A. M., Chu, H. P., Fiber, J. M., Karkanias, G. B. &Morales, J. M. 1999 Hormonal integration of neurochemical and sensory signals governing female reproductive
behavior. Behav. Brain Res. 105, 93–103.
Evans, D. W., Lewis, M. D. & Iobst, E. 2004 The role of theorbitofrontal cortex in normally developing compulsivelike behaviors and obsessive–compulsive disorder. Brain
Cogn. 55, 220–234.
Fabre-Nys, C. 1997 Male faces and odors evoke differential
patterns of neurochemical release in the mediobasal
hypothalamus of the ewe during estrus: an insight into
sexual motivation. Eur. J. Neurosci. 9, 1666–1677.
Fabre-Nys, C. 1998 Steroid control of monoamines inrelation to sexual behaviour. Rev. Reprod. 3, 31–41.
Ferrari, F. & Giuliani, D. 1995 Sexual attraction andcopulation in male rats: effects of the dopamine agonist
SND 919. Pharmacol. Biochem. Behav. 50, 29–34.
Fiorino, D. F., Coury, A. & Phillips, A. G. 1997 Dynamicchanges in nucleus accumbens dopamine efflux during the
Coolidge effect in male rats. J. Neurosci. 17, 4849–4855.
Fisher, H. E. 1992 Anatomy of love: the natural history ofmonogamy, adultery and divorce. New York, NY: WW
Norton.
Fisher, H. 1998 Lust, attraction, and attachment inmammalian reproduction. Human Nature 9, 23–52.
Fisher, H. 2004 Why we love: the nature and chemistry ofromantic love. New York, NY: Henry Holt.
Fisher, H., Aron, A., Mashek, D., Strong, G., Li, H. &Brown, L. L. 2002a The neural mechanisms of matechoice: a hypothesis. Neuroendocrinol. Lett. 23(Suppl. 4),
92–97.
Fisher, H., Aron, A., Mashek, D., Strong, G., Li, H. &Brown, L. L. 2002b Defining the brain systems of lust,romantic attraction and attachment. Arch. Sexual Behav.
31, 413–419.
Fisher, H., Aron, A., Mashek, D., Strong, G., Li, H. &Brown, L. L. 2005a Motivation and emotion systems
associaed with romantic love following rejection: an fMRI
study. Program no. 660.7. Abstract Viewer/Itinerary
Planner. Washington, DC: Society for Neuroscience,
Online.
Fisher, H., Aron, A. & Brown, L. L. 2005b Romantic love: anfMRI study of a neural mechanism for mate choice.
J. Comp. Neurol. 493, 58–62.
Fisher, H. E. & Thomson, J. A. In press. Lust, attraction,
attachment: the neural mechanisms of mate choice andhow antidepressants jeopardize romantic love, attachment
and one’s genetic future. In Evolutionary cognitive neuroscience. Steven Platek (ed.). Cambridge, MA: MIT Press.
Flaherty, A. W. & Graybiel, A. M. 1995 Motor andsomatosensory corticostriatal projection magnificationsin the squirrel monkey. J. Neurophysiol. 74, 2638–2648.
Fraley, G. S. 2002 Immunolesion of hindbrain catecholaminergic projections to the medial hypothalamus attenuates penile reflexive erections and alters hypothalamic
peptide mRNA. J. Neuroendocrinol. 14, 345–348.
Phil. Trans. R. Soc. B (2006)

H. E. Fisher and others

2183

Fraley, R. C. & Shaver, P. R. 2000 Adult romantic
attachment: theoretical developments, emerging controversies and unanswered questions. Rev. Gen. Psychol. 4,
132–154.
Galfi, M., Janaky, T., Toth, R., Prohaszka, G., Juhasz, A.,
Varga, C. & Laszlo, F. A. 2001 Effects of dopamine anddopamine-active compounds on oxytocin and vasopressin
production in rat neurohypophyseal tissue cultures. Regul.
Pept. 98, 49–54.
Gerfen, C. R., Herkenham, M. & Thibault, J. 1987 The
neostriatal mosaic: II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems.
J. Neurosci. 7, 3915–3934.
Gingrich, B., Liu, Y., Cascio, C. Z. & Insel, T. R. 2000
Dopamine D2 receptors in the nucleus accumbens areimportant for social attachment in female prairie voles(Microtus ochrogaster). Behav. Neurosci. 114, 173–183.
Ginsberg, S. D., Hof, P. R., Young, W. G. & Morrison, J. H.
1994 Noradrenergic innervation of vasopressin- andoxytocin-containing neurons in the hypothalamic paraventricular nucleus of the macaque monkey: quantitative
analysis using double-label immunohistochemistry andconfocal laser microscopy. J. Comp. Neurol. 341, 476–491.
Gladikas, B. M. 1995 Reflections of Eden: my years with theOrangutans of Borneo. New York, NY: Little Brown andCompany.
Goldstein, R. Z., Alai-Klein, N., Leskovjan, A. C., Fowler,
J. S., Wang, G. J., Gur, R. C., Hitzemann, R. & Volkow,
N. D. 2005 Anger and depression in cocaine addiction:
association with the orbitofrontal cortex. Psychiatry Res.
138, 13–22.
Gonzaga, G. C., Keltner, D., Londahl, E. A. & Smith, M. D.
2001 Love and the commitment problem in romantic
relations and friendship. J. Pers. Soc. Psychol. 81, 247–262.
Goodall, J. 1986 The Chimpanzees of Gombe: patterns of
behavior. Cambridge, MA: The Belknap Press of Harvard
University Press.
Gray, J. R., Braver, T. S. & Raichle, M. E. 2002 Integration ofemotion and cognition in the lateral prefrontal cortex.
Proc. Natl Acad. Sci. USA 99, 4115–4120.
Griffin, M. G. & Taylor, G. T. 1995 Norepinephrine
modulation of social memory: evidence for a timedependent functional recovery of behavior. Behav.
Neurosci. 109, 466–473.
Haber, S. N. 2003 The primate basal ganglia: parallel andintegrative networks. J. Chem. Neuroanat. 26, 317–330.
Hammock, E. A. D. & Young, L. J. 2005 Microsatellite
instability generates diversity in brain and sociobehavioral
traits. Science 308, 1630–1634.
Harris, C. R. & Christenfeld, N. 1996 Gender, jealousy, andreason. Psychol. Sci. 7, 364–366.
Hatfield, E. 1988 Passionate and companionate love. In The
psychology of love (ed. R. J. Sternberg & M. S. L. Barnes).
New Haven, CT: Yale University Press.
Hatfield, E. & Sprecher, S. 1986 Measuring passionate lovein intimate relations. J. Adolesc. 9, 383–410.
Hatfield, E., Schmitz, E., Cornelius, J. & Rapson, R. L. 1988
Passionate love: how early does it begin? J. Psychol. Hum.
Sex. 1, 35–51.
Hazan, C. & Diamond, L. M. 2000 The place of attachment
in human mating. Rev. Gen. Psychol. 4, 186–204.
Hazan, C. & Shaver, P. R. 1987 Romantic love conceptualized as an attachment process. J. Pers. Social Psychol. 52,
511–524.
Heaton, J. P. 2000 Central neuropharmacological agents andmechanisms in erectile dysfunction: the role of dopamine.
Neurosci. Biobehav. Rev. 24, 561–569.
Herbert, J. 1996 Sexuality, stress and the chemicalarchitecture of the brain. Annu. Rev. Sex Res. 7, 1–44.

2184

H. E. Fisher and others

Romantic love

Hull, E. M., Du, J., Lorrain, D. S. & Matuszewich, L. 1995
Extracelular dopamine in the medial preoptic area:
implicatons for sexual motivation and hormonal control
of copulation. J. Neurosci. 15, 7465–7471.
Hull, E. M., Du, J., Lorrain, D. S. & Matuszewick, L. 1997
Testosterone, preoptic dopamine, and copulation in malerats. Brain Res. Bull. 44, 327–333.
Hull, E. M., Lorrain, D. S., Du, J., Matuszewick, L., Lumley,
L. A., Putnam, S. K. & Moses, J. 1999 Hormone–
neurotransmitter interactions in the control of sexual
behavior. Behav. Brain Res. 105, 105–116.
Hull, E., Meisel, R. & Sachs, B. D. 2002 Male sexual
behavior. In Hormones, brain, and behavior (ed. D. W. Pfaff,
A. P. Arnold, A. M. Etgen, S. E. Fahrbach & R. T. Rubin),pp. 1–139. Boston, MA: Academic Press.
Hutchison, J. B. & Hutchison, R. E. 1983 Hormonal
mechanisms of mate choice in birds. In Mate choice (ed.
P. Bateson), pp. 389–405. Cambridge: Cambridge
University Press.
Jankowiak, W. R. & Fischer, E. F. 1992 A cross-cultural
perspective on romantic love. Ethnology 31, 149.
Karama, S., Lecours, A. R., Leroux, J. M., Bourgouin, P.,
Beaudoin, G., Joubert, S. & Beauregard, M. 2002 Areas ofbrain activation in males and females during viewing of
erotic film excerpts. Hum. Brain Mapp. 16, 1–13.
Kawashima, S. & Takagi, K. 1994 Role of sex steroids on thesurvival, neuritic outgrowth of neurons, and dopamine
neurons in cultured preoptic area and hypothalamus.
Horm. Behav. 28, 305–312.
Kemp, J. M. & Powell, T. P. 1970 The cortico-striate
projection in the monkey. Brain 93, 525–546.
Kendrick, K. M. 2000 Oxytocin, motherhood and bonding.
Exp. Physiol. 85S, 111S–124S.
Kendrick, K. M. & Dixson, A. F. 1985 Luteinizing hormone
releasing hormone enhances proceptivity in a primate.
Neuroendocrinology 41, 449–453.
Kendrick, K. M. & Dixson, A. F. 1986 Anteromedial
hypothalamic lesions block proceptivity but not receptivity
in the female common marmoset (Callithrix jacchus). Brain
Res. 375, 221–229.
Kendrick, K. M., Keverne, E. B., Hinton, M. R. & Goode,J. A. 1992 Oxytocin, amino acid and monoamine releasein the region of the medial preoptic area and bed nucleusof the stria terminalis of the sheep during parturition andsuckling. Brain Res. 569, 199–209.
Kovacs, G. & Telegdy, G. 1983 Effects of oxytocin, desglycinamide-oxytocin and anti-oxytocin serum on thealpha-MPT-induced disappearance of catecholamines in
the rat brain. Brain Res. 268, 307–314.
Kovacs, G. L., Sarnyai, Z., Barbarczi, E., Szabo, G. &Telegdy, G. 1990 The role of oxytocin-dopamineinteractions in cocaine-induced locomotor hyperactivity.
Neuropharmacology 29, 365–368.
Kringelbach, M. L. & Rolls, E. T. 2004 The functional
neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog.
Neurobiol. 72, 341–372.
Kuhnen, C. M. & Knutson, B. 2005 The neural basis offinancial risk taking. Neuron 47, 763–770.
Lauwereyns, J., Takikawa, Y., Kawagoe, R., Kobayashi,S., Koizumi, M., Coe, B., Sakagami, M. & Hikosaka,O. 2002 Feature-based anticipation of cues thatpredict reward in monkey caudate nucleus. Neuron
33, 463–473.
Lavin, A., Nogueira, L., Lapish, C. C., Wightman, R. M.,
Phillips, P. E. M. & Seamans, J. K. 2005 Mesocortical
dopamine neurons operate in distinct temporal domains
using multimodal signaling. J. Neurosci. 25, 5013–5023.
Phil. Trans. R. Soc. B (2006)

Legault, M. & Wise, R. A. 1999 Injections of N-methylD-asparate into the ventral hippocampus increase extraceullular dopamine in the ventral tegmental area andnucleus accumbens. Synapse 31, 241–249.
Liebowitz, M. R. 1983 The chemistry of love. Boston, MA:
Little Brown.
Lim, M. M. & Young, L. J. 2004 Vasopressin-dependentneural circuits underlying pair bond formation in themonogamous prairie vole. Neuroscience 128, 35–45.
Lim, M. M., Murphy, A. Z. & Young, A. J. 2004 Ventral
striatopallidal oxytocin and vasopressin V1a receptors in
the monogamous prairie vole (Microtus ochrogaster).
J. Comp. Neurol. 468, 555–570.
Liu, Y.-C, Sachs, B. D. & Salamone, J. D. 1998 Sexual
behavior in male rats after radiofrequency or dopaminedepleting lesions in nucleus accumbens. Pharmacol.
Biochem. Behav. 60, 585–592.
Maddock, R. J., Garrett, A. S. & Buonocore, M. H. 2003
Posterior cingulate cortex activation by emotional words:
fMRI evidence from a valence decision task. Hum. Brain
Mapp. 18, 30–41.
Marazziti, D., Akiskal, H. S., Rossi, A. & Cassano, G. B. 1999
Alteration of the platelet serotonin transporter in romantic
love. Psychol. Med. 29, 741–745.
Martin-Soelch, C., Leenders, K. L., Chevalley, A. F.,
Missimer, J., Kunig, G., Magyar, S., Mino, A. &Schultz, W. 2001 Reward mechanisms in the brain andtheir role in dependence: evidence from neurophysiological and neuroimaging studies. Brain Res. Rev. 36,
139–149.
Mashek, D., Aron, A. & Fisher, H. E. 2000 Identifying,evoking, and measuring intense feelings of romantic love.
Rep. Res. Social Psychol. 24, 48–55.
McCullough, D. 2001 John Adams. New York, NY: Simonand Schuster.
Meloy, J. R. & Fisher, H. 2005 Some thoughts on theneurobiology of stalking. Forensic Sci. 50, 1472–1480.
Miller, G. 2000 The mating mind: how sexual choice shaped theevolution of human nature. New York, NY: Doubleday.
Moles, A., Kieffer, B. L. & D’Amato, F. R. 2004 Deficit inattachment behavior in mice lacking the u-opioid receptor
gene. Science 304, 1983–1985.
Montague, P. R., McClure, S. M., Baldwin, R. P., Phillips,
P. E., Budygin, E. A., Stuber, G. D., Kilpatrick, M. R. &Wightman, R. M. 2004 Dynamic gain control of
dopamine delivery in freely moving animals. J. Neurosci.
24, 1754–1759.
Montejo, A. L., Llorca, G., Izquierdo, J. A. & RicoVallademoros, F. 2001 Incidence of sexual dysfunction
associated with antidepressant agents: a prospective
multicenter study of 1022 outpatients. J. Clin. Psychiatry62, 1020.
Najib, A., Lorberbaum, J. P., Kose, S., Bohning, D. E. &George, M. S. 2004 Regional brain activity in womengrieving a romantic relationship breakup. Am. J. Psychiatry
161, 2245–2256.
Narumoto, J., Okada, T., Sadato, N., Fukui, K. & Yonekura,Y. 2001 Attention to emotion modulates fMRI activity inhuman right superior temporal sulcus. Brain Res. Cogn. 12,
225–231.
Nyborg, H. 1994 Hormones, sex and society. Westport, CT:
Praeger.
Oades, R. D. & Halliday, G. M. 1987 Ventral tegmental(A10) system: neurobiology. 1. Anatomy and connectivity.
Brain Res. 434, 117–165.
O’Doherty, J. P., Deichmann, R., Critchley, H. D. & Dolan,
R. J. 2002 Neural responses during anticipation of a
primary taste reward. Neuron 33, 815–826.

Romantic love
Panksepp, J. 1998 Affective neuroscience: the foundations ofhuman and animal emotions. New York, NY: Oxford
University Press.
Parent, A. & Hazrati, L. N. 1995 Functional anatomy of
the basal ganglia. I. The cortico-basal ganglia-thalamocortical loop. Brain Res. Brain Res. Rev. 20, 91–127.
Parent, A., Cote, Y. & Lavoie, B. 1995 Anatomy of primate
basal ganglia. Prog. Neurobiol. 46, 131–197.
Parthasarathy, H. B., Schall, J. D. & Graybiel, A. M. 1992
Distributed but convergent ordering of corticostriatal
projections: analysis of the frontal eye field and the
supplementary eye field in the macaque monkey.
J. Neurosci. 12, 4468–4488.
Pfaff, D. W. 1999 DRIVE: neurobiological and molecularmechanisms of sexual motivation. Cambridge, MA: The
MIT Press.
Pfaff, D. W. 2005 Brain arousal and information theory.
Cambridge, MA: Harvard University Press.
Pfaff, D., Frohlich, J. & Morgan, M. 2002 Hormonal andgenetic influences on arousal – sexual and otherwise.
Trends Neurosci. 25, 45–50.
Pitkow, L. J., Sharer, C. A., Ren, X., Insel, T. R., Terwilliger,
E. F. & Young, L. J. 2001 Facilitation of affiliation andpair-bond formation by vasopressin receptor gene transfer
into the ventral forebrain of a monogamous vole.
J. Neurosci. 21, 7392–7396.
Posner, M. & Petersen, S. 1990 The attention system of thehuman brain. Annu. Rev. Neurosci. 13, 25–42.
Ridderinkhof, K. R., van den Wildenberg, W. P.,
Segalowitz, S. J. & Carter, C. S. 2004 Neurocognitive
mechanisms of cognitive control: the role of prefrontal
cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain
Cogn. 56, 129–140.
Robbins, T., Granon, S., Muir, J., Durantou, P., Harrison, A.
& Everitt, B. 1998 Neural systems underlying arousal andattention: implications for drug abuse. Ann. NY Acad. Sci.
846, 222–237.
Robinson, D. L., Heien, M. L. & Wightman, R. M. 2002
Frequency of dopamine concentration transients increases
in dorsal and ventral striatum of male rats during introduction of conspecifics. J. Neurosci. 22, 10 477–10 486.
Rosen, R. C., Lane, R. M. & Menza, M. 1999 Effects ofSSRIs on sexual function: a critical review. J. Clin.
Psycopharmacol. 19, 67–85.
Saint-Cyr, J. A., Ungerleider, L. G. & Desimone, R. 1990
Organization of visual cortical inputs to the striatum andsubsequent outputs to the pallido-nigral complex in themonkey. J. Comp. Neurol. 298, 129–156.
Schreckenberger, M., Siessmeier, T., Viertmann, A.,
Landvogt, C., Buchholz, H. G., Rolke, R., Treede, R. D.
& Bartenstein, F. 2005 The unpleasantness of tonic pain is
encoded by the insular cortex. Neurology 64, 1175–1183.
Schultz, W. 2000 Multiple reward signals in the brain. Nat.
Rev. Neurosci. 1, 199–207.
Schwarzberg, H., Kovacs, G. L., Szabo, G. & Telegdy, G.
1981 Intraventricular administration of vasopressin andoxytocin affects the steady-state levels of serotonin,
dopamine and norepinephrine in rat brain. Endocrinol.
Exp. 15, 75–80.
Segraves, R. T., Croft, H., Kavoussi, R., Ascher, J. A., Batey,
S. R., Foster, V. J., Bolden-Watson, C. & Metz, A. 2001
Bupropion sustained release (SR) for treatment of
hypoactive sexual desire disorder (HSDD) in nondepressed women. J. Sex Marital Ther. 27, 303–316.
Selemon, L. D. & Goldman-Rakic, P. S. 1985 Longitudinal
topography and interdigitation of corticostriatal projections in the rhesus monkey. J. Neurosci. 5, 776–794.
Phil. Trans. R. Soc. B (2006)

H. E. Fisher and others

2185

Seybold, V. S., Miller, J. W. & Lewis, P. R. 1978 Investigationof a dopaminergic mechanism for regulating oxytocin
release. J. Pharmacol. Exp. Ther. 207, 605–610.
Shaver, P., Schwartz, J., Kirson, D. & O’Connor, C. 1987
Emotion knowledge: further exploration of a prototype
approach. J. Pers. Soc. Psychol. 52, 1061–1086.
Sherwin, B. B. 1994 Sex hormones and psychological
functioning in postmenopausal women. Exp. Gerontol.
29, 423–430.
Shostak, M. 1981 Nisa: the life and words of a !Kung woman.
Cambridge, MA: Harvard University Press.
Szezypka, M. S., Zhou, Q. Y. & Palmiter, R. D. 1998
Dopamine-stimulated sexual behavior is testosterone
dependent in mice. Behav. Neurosci. 112, 1229–1235.
Tennov, D. 1979 Love and limerence: the experience of being inlove. New York, NY: Stein and Day.
Van Bockstaele, E. J., Pieribone, V. A. & Aston-Jones, G.
1989 Diverse afferents converge on the nucleus paragigantocellularis in the rat ventrolateral medulla: retrograde and anterograde tracing studies. J. Comp. Neurol.
290, 561–584.
Van de Kar, L. D., Levy, A. D., Li, Q. & Brownfield, M. S.
1998 A comparison of the oxytocin and vasopressin
responses to the 5-HT1A agonist and potential anxiolytic
drug alnespirone (S-20499). Pharmacol. Biochem. Behav.
60, 677–683.
Van Goozen, S., Wiegant, V. M., Endert, E., Helmond, F. A.
& Van de Poll, N. E. 1997 Psychoendocrinologicalassessment of the menstrual cycle: the relationshipbetween hormones, sexuality, and mood. Arch. Sex.
Behav. 26, 359–382.
Velanova, K., Jacoby, L. L., Wheeler, M. E., McAvoy, M. P.,
Petersen, S. E. & Buckner, R. L. 2003 Functionalanatomic correlates of sustained and transient processing
components engaged during controlled retrieval.
J. Neurosci. 23, 8460–8470.
Vizi, E. S. & Volbekas, V. 1980 Inhibition by dopamine ofoxytocin release from isolated posterior lobe of the
hypophysis of the rat: disinhibitory effect of betaendorphin/enkephalin. Neuroendocrinology 31, 46–52.
Vollm, B. A., Taylor, A. N., Richardson, P., Corcoran, R.,
Stirling, J., McKie, S., Deakin, J. F. & Elliott, R. 2006
Neuronal correlates of theory of mind and empathy: afunctional magnetic resonance imaging study in a
nonverbal task. Neuroimage 29, 90–98.
Walker, P. W., Cole, J. O. & Gardner, E. A. 1993
Improvement in fluoxetine-associated sexual dysfunction
in patients switched to bupropion. J. Clin. Psychiatry 54,
459–465.
Wang, Z. X., Ferris, C. F. & De Vries, G. J. 1994 The role of
septal vasopressin innervation in paternal behavior inprairie voles (Microtus ochrogaster). Proc. Natl Acad. Sci.
USA 91, 400–404.
Wang, Z., Toloczko, D., Young, L. J., Moody, K., Newman,
J. D. & Insel, T. R. 1997 Vasopressin in the forebrain ofcommon marmosets (Calithrix jacchus): studies with in situ
hybridization, immunocytochemistry and receptor autoradiography. Brain Res. 768, 147–156.
Wang, Z., Yu, G., Cascio, C., Liu, Y., Gingrich, B. & Insel,
T. R. 1999 Dopamine D2 receptor-mediated regulation ofpartner preferences in female prairie voles (Microtus
ochrogaster): a mechanism for pair bonding? Behav.
Neurosci. 113, 602–611.
Wenkstern, D., Pfaus, J. G. & Fibiger, H. C. 1993 Dopaminetransmission increases in the nucleus accumbens of malerats during their first exposure to sexually receptive female
rats. Brain Res. 618, 41–46.
Wersinger, S. R. & Rissman, E. F. 2000 Dopamine activates
masculine sexual behavior independent of the estrogen
receptor alpha. J. Neurosci. 20, 4248–4254.

2186

H. E. Fisher and others

Romantic love

West, C. H. K., Clancy, A. N. & Michael, R. P. 1992
Enhanced responses of nucleus accumbens neurons inmale rats to novel odors associated with sexually receptive
females. Brain Res. 585, 49–55.
Williams, S. M. & Goldman-Rakic, P. S. 1998 Widespreadorigin of the primate mesofrontal dopamine system. Cereb.
Cortex 8, 321–345.
Williams, J. R., Insel, T. R., Harbaugh, C. R. & Carter, C. S.
1994 Oxytocin administered centrally facilitates formationof a partner preference in female prairie voles (Microtus
ochrogaster). J. Neuroendocrinol. 6, 247–250.
Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R. &Insel, T. R. 1993 A role for central vasopressin in pairbonding in monogamous prairie voles. Nature 365, 545–548.
Wise, R. A. 1996 Neurobiology of addiction. Curr. Opin.
Neurobiol. 6, 243–251.

Phil. Trans. R. Soc. B (2006)

Young, L. J. 1999 Oxytocin and vasopressin receptors andspecies-typical social behaviors. Horm. Behav. 36,
212–221.
Young, L. J., Winslow, J. T., Nilsen, R. & Insel, T. R. 1997
Species differences in V1a receptor gene expression inmonogamous and nonmonogamous voles: behavioral
consequences. Behav. Neurosci. 111, 599–605.
Young, L. J., Wang, Z. & Insel, T. R. 1998 Neuroendocrinebases of monogamy. Trends Neurosci. 21, 71–75.
Young, L. J., Lim, M. M., Gingrich, B. & Insel, T. R. 2001
Cellular mechanisms of social attachment. Horm. Behav.
40, 133–138.
Zald, D. H., Boileau, I., El-Dearedy, W., Gunn, R.,
McGlone, F., Dichter, G. S. & Dagher, A. 2004
Dopamine transmission in the human striatum during
monetary reward tasks. J. Neurosci. 24, 4105–4112.