The Brain Reaction to Viewing Faces of Opposite- and Same-Sex Romantic Partners

Citation: Zeki S, Romaya JP ( The Brain Reaction to Viewing Faces of Opposite- and Same-Sex Romantic Partners Semir Zeki 0 John Paul Romaya 0 Angela Sirigu, CNRS, France 0 Wellcome Laboratory of Neurobiology, University College London , London , United Kingdom We pursued our functional magnetic resonance imaging (fMRI) studies of the neural correlates of romantic love in 24 subjects, half of whom were female (6 heterosexual and 6 homosexual) and half male (6 heterosexual and 6 homosexual). We compared the pattern of activity produced in their brains when they viewed the faces of their loved partners with that produced when they viewed the faces of friends of the same sex to whom they were romantically indifferent. The pattern of activation and de-activation was very similar in the brains of males and females, and heterosexuals and homosexuals. We could therefore detect no difference in activation patterns between these groups. - The work reported here is a continuation of our previous work on brain systems and networks that are critical for the sentiment of romantic love [1,2]. It was inspired by a reading of the world literature of love, both Western and Oriental, in which similar sentiments are expressed, whether in the same or opposite sex context. In extending our work, we therefore considered it interesting to compare the pattern of brain activity evoked in opposite- and same-sex lovers when they view the pictures of those they love. Passionate romantic love, commonly triggered by a visual input, is an all-consuming and disorienting state that pervades almost every aspect of a lovers life. Yet human brain imaging studies [1,2,3,4] show that the neural correlates of viewing the face of a loved person are limited to only a few, though richly connected, brain regions. This limitation made it plausible to suppose that we could detect any differences relatively easily. Differences between homosexual and heterosexual brains have been described, specifically in the size of hypothalamic [5] or suprachiasmatic [6] nuclei, or in the degree of lateralization between the two groups of men [7], or in hemispheric asymmetries and differential activation patterns between homosexual and heterosexual brains. But such differential activations as have been described have been in response to sexually arousing stimuli [8], not in response to the sentiment of love. Given the profound similarity in the sentiment of love expressed in the opposite- or same-sex contexts, we hypothesised that we would see no differences when females or males, or heterosexual or homosexual subjects, viewed the face of their loved partners. This would amount to a negative result but one that is nevertheless of considerable significance. Materials and Methods Ethics Statement Informed written consent was obtained from all participants and the study was approved by the University College London Research Ethics Committee. Subjects 28 healthy subjects (equally divided between male and female and heterosexual and homosexual) were recruited through advertisements requesting volunteers who were passionately in love. All reported being in a sexual relationship with their lover. Their age varied from 19 to 47 years (mean 26.3 , ssd 6.4) and length of relationship from 4 months to 23 years (mean 3.7, ssd 4.4). Two subjects were left handed. Subjects were drawn from West European, East European, American, Oriental and Asian backgrounds, within which there were further cultural subgroupings, for example, British, Italian, Portuguese, etc within the West European grouping. Of the 28 subjects who were scanned, 4 were excluded for the following reasons: one showed strong artefacts in her scanned image, another subsequently reported deep underlying problems in the relationship, a third fell asleep shortly after scanning commenced and the fourth subsequently reported thinking of her lover throughout the scanning session, even when neutral faces were being displayed. Later analysis of the individual results from these four excluded subjects displayed very little or no activation for the contrast Loved vs. Neutral. During a first visit to the laboratory, some two weeks prior to scanning, each subject provided 68 picture portraits of their lover and a similar number of portraits of other friends of the same sex as their lover towards whom they had neutral feelings, all pictures being matched as far as possible for expression and general appearance. The experiment was explained to the subject and an example stimulus using random anonymous faces was demonstrated. Each subject completed a Passionate Love Scale (PLS) [9] questionnaire, to attempt to quantify their feelings about their lover. Age and length of relationship were recorded for each subject. During scanning sessions subjects heart-rate and respiration were continuously recorded, providing physiological measurements that were subsequently incorporated into the first level analysis for each subject (see File S1: Physiological noise correction). We also recorded eye gaze position to monitor subjects attention and galvanic skin response (GSR) but did not use these measurements in the analysis since in this, as in our past studies, we have found the GSR to be an unpredictable and unreliable metric [1]. Directly after scanning, each subject again completed the PLS questionnaire, in order to re-quantify their feelings immediately after the scanning. Subjects were also interviewed to assess whether they had experienced any difficulties (such as that experienced by the excluded subject who reported thinking of her lover throughout the experiment). Subsequent to the experiments, each subject also gave a Kinsey rating of their sexual orientation, on a scale of 0 (exclusively heterosexual) to 6 (exclusively homosexual) [10] (see Table 1). Of the 24 subjects, 50% were exclusively either heterosexual or homosexual. The remaining 50%, whose ratings fell in between, nevertheless declared their relationship to be either heterosexual or homosexual. Stimuli Stimuli were generated using Cogent 2000 and Cogent Graphics (http://www.vislab.ucl.ac.uk/cogent.php). Photographic images provided by each subject were digitized, converted to grayscale and edited to remove superfluous features such as earrings, scarves etc. Background detail was replaced with a flat mid-grey tone and images were normalized in terms of visual area and average brightness. Spatial frequency and contrast were also roughly normalized (see File S1: Preprocessing of face images). Subjects were exposed to two stimulus sessions but in two subjects the second session was not used, for the following reasons: one subject fell asleep during the second session while for the other the second session was invalid due to technical reasons. The session began with a flat grey background (intensity 6.4 cd/m2) (blank condition) which was present for 26 s, during which the first six brain volumes were discarded to allow T1 (...truncated)