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The Neural Basis of Romantic Love Andreas Bartels and Semir
Zeki [Figures & tables referenced in this article are
available at http://www.neuroscience.unizh.ch/e/pdf/PaperIshai.pdf#search=%22The%20neural%20basis%20of%20romantic%20love%22]
Key words: Anterior cingulate; Attachment; Emotion; fMRI;
Friendship; Galvanic skin response; Insula; Love; Striatum INTRODUCTION Romantic
love, celebrated throughout the ages as one of the most overwhelming of all
affective states, has been the inspiration for some of the loftiest
achievements of man- kind. Characteristically directed towards a single
person, it is a complex sentiment involving erotic, cognitive, emotional and
behavioural components [1 - 3], which are difficult if not impossible to
disentangle. Hence any study of `romantic love' is a study of a sentiment
with several components, some of which, like the erotic one, can also act
independently of the others; the converse is not true, in that all the above
components constitute essential ingredients of romantic love. Visual input plays
a leading role in arousing and sustaining romantic love and yet nothing is
known of the neural mechanisms underlying this complex sentiment. This,
together with the high position that romantic love assumes in the lives of
most, even if transiently, prompted this imaging study. Given its uniqueness,
we hypothesised that there may be special systems or pathways for romantic
love. Past
neuro-imaging studies of emotions have charted brain areas responsible for
producing an emotional state, or those responsible for recognising one; here
we concentrate on the former. Negative affective states such as fear, anger,
anxiety and sadness [4 - 10] have been studied more extensively than positive
ones such as happiness [5,6], sexual arousal [11,12] or `pleasant' states
provoked by visual stimulation [8,9,13]; here we concentrate on the latter.
We wanted to chart the neural correlates of this affective state when it is
generated by a visual input which is emotionally neutral to an external
observer. An abstract of our results has been published [14]. MATERIALS AND METHODS Subjects and stimuli: Volunteers who professed to be `truly, deeply and
madly in love' were recruited by posters and via the Internet. Out of 70 who
had replied (75% of whom were female), 17 normal subjects were selected by
means of short written statements describing how much they were in love and
by an interview (11 female; all right handed except for one male subject;
ages 21 - 37, media 23, mean 24.5 years). Eleven countries and several ethnic
groups were represented. All gave informed written con- sent. Prior or after
the scan the galvanic skin response was measured in response to the pictures
(see later). After the scan, subjects filled in the short version of the
'passionate love scale' (PLS) [15], thought to be a reliable means of
quantifying this complex sentiment. The PLS asks subjects to rate the truth
of statements such as: `For me, XXX is the perfect romantic partner' by means
of ratings from 1 to 9, with 9 being the maximum. In a slight modification of
the PLS, we asked our subjects to give ratings corresponding to the time when
we scanned them. Their high mean scores of 7.55 0.97 were higher than the
highest scores reported in the original version (7.36 for women at the
`exclusive dating' stage of their relationship [15]). During the scan each
subject viewed coloured pictures of the faces of four people on a neutral
background: their boy- or girlfriend and three friends of same sex as their
loved partner. All four were of similar age, and the duration of friendship
(4.3 5.2 years, median 3 years) was not shorter than the one of the loving
relationships (2.4 1.7 years, median 2.3 years). Ten subjects provided one
picture per person, seven provided two. Pictures were shown for 17.36 s (4
TRs) each, in nine random permutations of the four people. Sequences were
counterbalanced across subjects and lasted 10 min 25 s. Subjects were
instructed to view the pictures, to think of the viewed person and to relax.
After the scan, they were asked to report their emotional experience while
viewing the different pictures, and each confirmed having felt being in love
when seeing the partner (see below). A decay of emotional response was
reported for the last few repeats of the nine four-people cycles. We therefore
analyzed the fMRI data not only for all nine repeats, but also for the first
six (first 6 min 57 s). The results were the same for both and all data shown
here are for the first six repeats for all 17 subjects. After
the scan, subjects were asked to rate feelings of love and sexual arousal on
a scale from 1 to 9, with 9 being the maximum, when viewing the loved partner
and when viewing friends. As expected, sexual arousal was one of the
components of the feelings when viewing the loved partner, but the feelings
of love were clearly dominant, scoring nearly twice as much as sexual arousal
for lovers compared to friends (Fig. 1): feelings of love: loved partner 7.46
1.1, friends 3.2 1.3; sexual arousal: loved partner 4.4 2.2, friends 1.4 0.7.
They were also asked to report any other associations or imagery during the
scan, to either friends or loved partner. No common imagery or associations
emerged. Electro-galvanic skin response (GSR): On a separate day before or after the scan the GSR
to the pictures was measured ( n ˆ 15) (Fig. 2).
Pictures were presented in a pseudorandom sequence, for 10 s with no gap
between pictures; GSRs to the first two were discarded to minimize
novelty/adaptation effects, leaving 15 pictures of the loved partner and 17
pictures of friends. The normalized GSR response to a picture was given by
the peak GSR 1 - 4 s after the picture presentation (the GSR in response to
the picture), from which the baseline (minimum GSR within the 2 s following a
picture presentation) was subtracted. This
paradigm could have been optimized, e.g. by using a similar sequence as in
the scanner, where each person was shown with equal probability, while here
each category (friends/loved partner) occurred with equal probability. This
would almost certainly have led to even higher GSRs to pictures of the loved
partner. Moreover, GSR is extremely unspecific, and any emotion or even
association, whether positive or negative, may lead to an enhanced GSR.
Applying GSR to pictures of people known to the subjects, each of which
elicits specific associations, seems therefore a rather risky approach to
detecting a very specific emotion. In spite of these factors, all working
against a positive result, we found that, for the group of subjects as a
whole, the GSR to pictures of the loved partner was significantly higher than
that to pictures of friends ( t-test, p , 0.0025), confirming objectively a
differential emotional response to the partner compared to the friends. Image acquisition and analysis: Data for all 17 subjects were acquired in a 2 T
Siemens Vision MRI scanner and analysed using SPM99 (www.fil.ion.ucl.ac.uk)
[16], as de- scribed elsewhere [17]. Activity in the whole head was measured
using an echo-planar imaging sequence (EPI) that acquired 48 transverse slices
(2.5 mm thickness, 0.5 mm gap), each subtending 64 3 64 voxels of 3 3 3 mm.
Repetition time (TR) of each whole-brain acquisition was 4.341 s, echo time
(TE) 40 ms. Data were smoothed with a Gaussian kernel of 10 mm full width at
half maximum. All four viewed people were modelled using a multiple
regression analysis and contrast images for the comparisons lover vs. friends
and friends vs. lover were calculated. In a second level (random effects)
analysis a t-test was applied to the 17 contrast images of all subjects to
obtain those areas that were commonly activated across the whole group,
making the results presented here valid for the population that the subjects
are representative of. This type of analysis reveals the regions that are
commonly activated in all subjects, and therefore the common denominator of
regions involved in love. The RESULTS No
visual area in the occipital lobe or in the fusiform gyrus, which is involved
in various aspects of visual face recognition, including attention to faces
[20], was activated or deactivated. Instead, the blood oxygen level dependent
signal (BOLD) specific to viewing pictures of the loved partner revealed
activity focally restricted to two main cortical areas remote from the visual
brain, the middle insula, mainly on the left, and the anterior cingulate
cortex bilaterally (p, 0.001, uncorrected, random effects analysis); with a lowered
threshold ( p , 0.005), bilateral activation in the
posterior hippocampus became apparent. There were also prominent activations
in two subcortical parts of the cerebrum, the head of the caudate nucleus and
the putamen, both stronger on the left, and in sites in the cerebellum ( p ,
0.001, uncorrected, random effects analysis) (Table
1; Fig. 3a, b). The regions apparent in the reverse contrast (friends vs.
partner) were interpreted as deactivations specific to viewing the loved
partners (Table 1; Fig. 4). Cortically, these were concentrated in the right
prefrontal, parietal, and middle temporal cortex, and in the posterior
cingulate gyrus and medial prefrontal cortex. Subcortically, there was a
deactivation in the posterior amygdaloid region. When data from males and
females were analysed separately, both had the same activation and
deactivation patterns as found for the whole group. However, the limited
number of male subjects did not allow for a statistical population comparison
between the genders. We
further analysed each subject with an independent component analysis ( DISCUSSION In
this study, we used a novel way of studying the neural bases of affective
states in a broader sense. Previous studies have induced emotions through the
use of visual scenes, or, less commonly, through autobiographic events. As
well, they have compared positive emotional states with negative ones. Here
we have for the first time tried to explore the neural correlates of personal
relationships; in addition, we have compared two positive emotional states.
This study is therefore an initial attempt to explore the neurological bases
of one of the most important ingredients in human interaction, that of
personal relationships, which we hope future studies will extend. Given
the complexity of the sentiment of romantic love, it was not surprising to
find that the activity was within regions of the brain found to be active in
other emotional states, even if the pattern of activity evoked here is
unique. This raises the question of the degree of overlap in sites of
activity between this and previous studies. The cortical and sub-cortical
structures involved are large and many previously reported activations lie in
subdivisions of these structures which are distinct from ours. Where there is
a suspected overlap of activation (see later), its extent is difficult to
determine from the anatomical information available in many previous studies.
What seems to be certain is that, even allowing for possible overlap, the
pattern of activation obtained here was nevertheless unique, both in the
identity and combination of sites involved. To us, the surprise was to find
that the activity was restricted to so few areas with such a small spatial
extent, given that romantic love involves several not easily dissociable
components. Faces, familiarity and attention: By restricting the experiment to views of faces
alone, we hoped to minimize the differences in visual stimulation, and thus
concentrate on a difference in emotional attachment. This approach may be
complicated by two potentially confounding variables, of familiarity and
attention. Even though all the faces were highly familiar to our subjects, it
is not unreasonable to assume that the face of a loved person is likely to be
more familiar than that of friends. But imaging studies reassure us that
familiarity with a face leads to heightened activity within the part of the
visual cortex specialized for face processing in the fusiform gyrus, and
other areas not activated here [22]. Similarly, it is plausible to suppose
that the loved face attracts more of the subject’s attention than the faces
of friends. But previous studies show that attention to faces or even
features associated with them leads to increased activity in the fusiform
gyrus and in other, non- visual areas, none of which were activated here
[20]. We thus conclude that neither variable influenced our results. Activations: The insula is related to a variety of emotional
functions [23]. Lesions in it can have severe emotional consequences, among
them those related to the interpretation of visual input. Imaging studies of
various negative emotional experiences have localized activity to a region of
the anterior insula that is distinct from our medial one [23]. Interestingly,
attractiveness of unfamiliar faces was reported to correlate positively with
blood flow in the left insula [24], in a region that does seem to overlap
with ours. The
large anterior cingulate cortex consists of several functionally distinct
components [25]; several of its sub-divisions play an important role in
emotional function. Whilst previous imaging experiments involving different
emotions have attributed activity to 'the anterior cingulate', they almost
certainly activated different subdivisions within it. In particular, the
anterior cingulate cortex includes regions implicated in happy states [6], attention
to one's own emotional state and especially social interactions which involve
assessing one's own and other people's emotions and states of mind [25,26].
The locus activated in our study is small and localized to a ventral region
distinct from the regions activated in most studies mentioned above, which
are often restricted to dorsal parts of the anterior cingulate (BA 32), which
is unfortunately not usually distinguished from the more ventral region (BA
24) involved here. The distinction between the (dorsal) region of the
anterior cingulate activated in many studies of emotion and the ventral one
activated here argues for functional subdivisions related to emotions within
the anterior cingulate too. The
two subcortical zones activated, the caudate nucleus and putamen, are also
amongst the most commonly activated regions in studies involving both
positive [11 -13,24,27,28] and negative emotions [5,6,8] (see also [29]),
probably in different subdivisions. Both have been considered to be part of
the extrapyramidal motor system, raising the question whether the activity we
observed is related to increased motor planning or
imagery associated with a loved person. This is unlikely because studies on
motor imagery, mental rotation and motor execution typically do not activate
either structure, while activating other regions not implicated in this study
[30]. In contrast, it is note- worthy that dopamine release due to success in
a video game has been localised to a broad region in the striatum that
overlaps at least with the activity reported here in the putamen [31].
Collectively, these results call for a re- appraisal of the role of the
putamen and the caudate in emotional states and as parts of the
extrapyramidal motor system. Deactivations: In charting the neural basis of so complex an
emotion, the deactivations are also important, since the nature and strength
of the emotion itself may be dictated in part at least by a complex balance
between the two. The widespread deactivations that we have observed have their
counterpart in previous studies which have shown that happiness correlates
with deactivations in the right pre- frontal and bilateral parietal and
temporal cortices [5]. Conversely, it is striking to note that sadness and
depression correlate with activation in some of the cortical regions
deactivated in our study, especially the right prefrontal cortex [10], whose
artificial inactivation by means of transcranial magnetic stimulation has
proven to result in successful treatment against depression [32]. The
posterior cingulate cortex is one of the most commonly activated region in
emotional studies [29], but its exact function remains poorly understood. The
deactivation of the amygdaloid region is of special interest, since activity
in it correlates with fear, sadness and aggression, and is thought to mediate
emotional learning [33]; activity in it increases from the most happy to the
most fearful facial expression viewed [28]. This differential response is
further emphasised by our results which show that, within experienced
positive emotions, the amygdaloid region is more active when viewing friends
than the loved partner. Studies of sexual arousal: Sexual arousal is of course never far from
romantic love, making it especially interesting to consider the degree to
which the two are neuronally entangled. Two studies on sexual arousal [11,
12] reported no activations that overlapped with ours, but both activated
regions adjacent to ours in the anterior cingulate gyrus, one in the left
caudate nucleus and the right insula [11], and the other in the right globus
pallidus [12]. Deactivations were reported in the posterior cingulate cortex
[11] and in the right hemisphere [12], the latter overlapping with ours in BA
8. It is however striking that studies of cocaine-
and muopioid agonist-induced euphoria have shown increased activity in foci
that seem to overlap with all foci activated in our study: the anterior
cingulate cortex [27, 34], the insula, the caudate nucleus and the putamen
[27]. This suggests a potentially close neural link between romantic love and
euphoric states. CONCLUSION We
have tried to identify the cortical activity associated with the state of
romantic love, by comparing one positive emotion (romantic love) with another
one (friendship). Our stimuli were emotionally indistinguishable to an
external observer: the difference between the partner and friends was an
emotional one, apparent to the subject concerned alone. By showing that a
unique set of interconnected areas becomes active when humans view the face
of someone who elicits a unique and characteristic set of emotions, we have
shown that underlying one of the richest experiences of mankind is a
functionally specialised system of the brain. It is perhaps surprising that
so complex and over- whelming a sentiment should correlate differentially
with activity in such restricted regions of the brain, and fascinating to
reflect that the face that launched a thousand ships should have done so
through such a limited expanse of cortex. Given the complexity of the
sentiment of romantic love, and its capacity to exhilarate, arouse and
disturb and thus influence so much of our behaviour, it would be surprising
if these areas act in isolation. The widespread cortical connections of the
areas differentially activated here is no doubt a means of recruiting more
areas during this complex emotional state, with a pattern of activity that
may differ between individuals and situations, which future studies will no
doubt unravel. Given the uniqueness of the pattern of activity evoked, it is
not unreasonable to suppose that other unique emotional states will correlate
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Our work is supported by the Wellcome Trust London; A.B. is supported by the
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