Event-related potentials modulated by the perception of sexual dimorphism: The influence of attractiveness and sex of faces.

Sexual dimorphism has been proposed as one of the facial traits to have evolved through sexual selection and to affect attractiveness perception. Even with numerous studies documenting its effect on attractiveness and mate choice, the neurophysiological correlates of the perception of sexual dimorphism are not yet fully understood. In the present study, event-related potentials (ERPs) were recorded during visualisation of faces that had been previously transformed in shape to appear more masculine or more feminine. The participants' task consisted of judging the attractiveness of half of the total number of faces, and performing a sex discrimination task on the other half. Both early and late potentials were modulated by the sex of faces, whereas the effect of the sexually dimorphic transform was mainly visible in the P2 (positive deflection around 200 ms after stimulus onset), EPN (early posterior negativity) and LPP (late positive potential) components. There was an effect of sexual dimorphism on P2 and EPN amplitudes when female participants visualised male faces, which may indicate that masculinity is particularly attended to when viewing opposite sex members. Also, ERP results seem to support the idea of sex differences in social categorisation decisions regarding faces, although differences were not evident on behavioural results. In general, these findings contribute to a better understanding of how humans perceive sexually dimorphic characteristics in other individuals' faces and how they affect attractiveness judgements.

The shared neural basis of empathy and facial imitation accuracy.

Empathy involves experiencing emotion vicariously, and understanding the reasons for those emotions. It may be served partly by a motor simulation function, and therefore share a neural basis with imitation (as opposed to mimicry), as both involve sensorimotor representations of intentions based on perceptions of others' actions. We recently showed a correlation between imitation accuracy and Empathy Quotient (EQ) using a facial imitation task and hypothesised that this relationship would be mediated by the human mirror neuron system. During functional Magnetic Resonance Imaging (fMRI), 20 adults observed novel 'blends' of facial emotional expressions. According to instruction, they either imitated (i.e. matched) the expressions or executed alternative, pre-prescribed mismatched actions as control. Outside the scanner we replicated the association between imitation accuracy and EQ. During fMRI, activity was greater during mismatch compared to imitation, particularly in the bilateral insula. Activity during imitation correlated with EQ in somatosensory cortex, intraparietal sulcus and premotor cortex. Imitation accuracy correlated with activity in insula and areas serving motor control. Overlapping voxels for the accuracy and EQ correlations occurred in premotor cortex. We suggest that both empathy and facial imitation rely on formation of action plans (or a simulation of others' intentions) in the premotor cortex, in connection with representations of emotional expressions based in the somatosensory cortex. In addition, the insula may play a key role in the social regulation of facial expression.

It is all in the face: carotenoid skin coloration loses attractiveness outside the face.

Recently, the importance of skin colour for facial attractiveness has been recognized. In particular, dietary carotenoid-induced skin colour has been proposed as a signal of health and therefore attractiveness. While perceptual results are highly consistent, it is currently not clear whether carotenoid skin colour is preferred because it poses a cue to current health condition in humans or whether it is simply seen as a more aesthetically pleasing colour, independently of skin-specific signalling properties. Here, we tested this question by comparing attractiveness ratings of faces to corresponding ratings of meaningless scrambled face images matching the colours and contrasts found in the face. We produced sets of face and non-face stimuli with either healthy (high-carotenoid coloration) or unhealthy (low-carotenoid coloration) colour and asked participants for attractiveness ratings. Results showed that, while for faces increased carotenoid coloration significantly improved attractiveness, there was no equivalent effect on perception of scrambled images. These findings are consistent with a specific signalling system of current condition through skin coloration in humans and indicate that preferences are not caused by sensory biases in observers.

Adaptation improves face trustworthiness discrimination.

Adaptation to facial characteristics, such as gender and viewpoint, has been shown to both bias our perception of faces and improve facial discrimination. In this study, we examined whether adapting to two levels of face trustworthiness improved sensitivity around the adapted level. Facial trustworthiness was manipulated by morphing between trustworthy and untrustworthy prototypes, each generated by morphing eight trustworthy and eight untrustworthy faces, respectively. In the first experiment, just-noticeable differences (JNDs) were calculated for an untrustworthy face after participants adapted to an untrustworthy face, a trustworthy face, or did not adapt. In the second experiment, the three conditions were identical, except that JNDs were calculated for a trustworthy face. In the third experiment we examined whether adapting to an untrustworthy male face improved discrimination to an untrustworthy female face. In all experiments, participants completed a two-interval forced-choice (2-IFC) adaptive staircase procedure, in which they judged which face was more untrustworthy. JNDs were derived from a psychometric function fitted to the data. Adaptation improved sensitivity to faces conveying the same level of trustworthiness when compared to no adaptation. When adapting to and discriminating around a different level of face trustworthiness there was no improvement in sensitivity and JNDs were equivalent to those in the no adaptation condition. The improvement in sensitivity was found to occur even when adapting to a face with different gender and identity. These results suggest that adaptation to facial trustworthiness can selectively enhance mechanisms underlying the coding of facial trustworthiness to improve perceptual sensitivity. These findings have implications for the role of our visual experience in the decisions we make about the trustworthiness of other individuals.

Cross-cultural variation in women's preferences for cues to sex- and stress-hormones in the male face.

Women in the UK prefer the faces of men with low levels of the stress hormone cortisol, and the relationship is moderated by the sex hormone testosterone. In a Latvian sample, however, women's preferences were not affected by cortisol, and the interaction with testosterone differed from that of the UK. To further explore cross-cultural variation in preferences for facial cues to sex- and stress-hormones, we tested the preferences of women from 13 countries for facial composites constructed to differ in combinations of the hormones. We found significant relationships between a measure of societal development (the United Nations human development index 2011) and preferences for cues to testosterone in the face, and the interaction between preferences for cues to testosterone and cortisol. We also found a significant relationship between preferences for cues to testosterone and a societal-level measure of parasite stress. We conclude that societal-level ecological factors influence the relative value of traits revealed by combinations of sex- and stress-hormones.

Face structure predicts cooperation: men with wider faces are more generous to their in-group when out-group competition is salient.

Male facial width-to-height ratio appears to correlate with antisocial tendencies, such as aggression, exploitation, cheating, and deception. We present evidence that male facial width-to-height ratio is also associated with a stereotypically male prosocial tendency: to increase cooperation with other in-group members during intergroup competition. We found that men who had wider faces, compared with men who had narrower faces, showed more self-sacrificing cooperation to help their group members when there was competition with another group. We propose that this finding makes sense given the evolutionary functions of social helpfulness and aggression.

Cues to sex- and stress-hormones in the human male face: functions of glucocorticoids in the immunocompetence handicap hypothesis.

The stress-linked version of the immunocompetence handicap hypothesis has been proposed to account for inconsistencies in relationships between testosterone and immune response. The model has received some support from studies demonstrating roles of stress hormones in relationships between testosterone, immune function and secondary sexual ornamentation. Such work, however, has relied on artificial elevation of testosterone so may not reflect relationships in natural populations. We created human male facial stimuli on the basis of naturally co-occurring levels of salivary testosterone and the stress hormone cortisol. In Study 1 we tested female preferences for male faces with cues to combinations of the hormones across the menstrual cycle, and in Study 2 we tested perceptions of health and dominance in a novel set of facial stimuli. Females preferred cues to low cortisol, a preference that was strongest during the fertile phase of the menstrual cycle. The effects of cortisol on attractiveness and perceived health and dominance were contingent upon level of testosterone: the effects of the stress hormone were reduced when testosterone was high. We propose explanations for our results, including low cortisol as a cue to a heritable component of health, attractiveness as a predictor of low social-evaluative threat (and, therefore, low baseline cortisol) and testosterone as a proxy of male ability to cope efficiently with stressors.

Evidence for the stress-linked immunocompetence handicap hypothesis in human male faces.

The stress-linked immunocompetence handicap hypothesis (SL-ICHH) of sexual selection incorporates a role of the stress hormone corticosterone (C; cortisol in humans) in relationships between testosterone (T), immunity and secondary sexual trait expression. In support of this, C has been shown to mediate and moderate relationships between T and immune response and to be inversely related to attractiveness in some avian species. We predicted that female preferences for cues to T in human male faces would be contingent upon co-occurring cortisol levels. In study 1, we tested relationships between T and cortisol and attractiveness, masculinity and health ratings of raw male faces. We found cortisol to be inversely related to attractiveness. In study 2, we tested female preferences for male faces that were parametrically manipulated on the basis of cues to naturally co-occurring levels of T and cortisol across the menstrual cycle. Women preferred cues to low cortisol in general and in the fertile phase of the cycle, and there was an interaction between T and cortisol in general and in the non-fertile phase. Results were consistent with the SL-ICHH but not the original immunocompetence handicap model: females expressed preferences for cues to cortisol but not for cues to T, except in interaction with the stress hormone. Results inform the SL-ICHH by demonstrating female preferences for low cortisol and the nature of its interaction with T in humans, as well as indicating the traits that may be signalled by different combinations of the hormones including immune response, current health and resource acquisition characteristics.

Valid facial cues to cooperation and trust: male facial width and trustworthiness.

Decisions about whom to trust are biased by stable facial traits such as attractiveness, similarity to kin, and perceived trustworthiness. Research addressing the validity of facial trustworthiness or its basis in facial features is scarce, and the results have been inconsistent. We measured male trustworthiness operationally in trust games in which participants had options to collaborate for mutual financial gain or to exploit for greater personal gain. We also measured facial (bizygomatic) width (scaled for face height) because this is a sexually dimorphic, testosterone-linked trait predictive of male aggression. We found that men with greater facial width were more likely to exploit the trust of others and that other players were less likely to trust male counterparts with wide rather than narrow faces (independent of their attractiveness). Moreover, manipulating this facial-width ratio with computer graphics controlled attributions of trustworthiness, particularly for subordinate female evaluators.

The cutest little baby face: a hormonal link to sensitivity to cuteness in infant faces.

We used computer image manipulation to develop a test of perception of subtle gradations in cuteness between infant faces. We found that young women (19-26 years old) were more sensitive to differences in infant cuteness than were men (19-26 and 53-60 years old). Women aged 45 to 51 years performed at the level of the young women, whereas cuteness sensitivity in women aged 53 to 60 years was not different from that of men (19-26 and 53-60 years old). Because average age at menopause is 51 years in Britain, these findings suggest the possible involvement of reproductive hormones in cuteness sensitivity. Therefore, we compared cuteness discrimination in pre- and postmenopausal women matched for age and in women taking and not taking oral contraceptives (progestogen and estrogen). Premenopausal women and young women taking oral contraceptives (which raise hormone levels artificially) were more sensitive to variations of cuteness than their respective comparison groups. We suggest that cuteness sensitivity is modulated by female reproductive hormones.

Sex-contingent face aftereffects depend on perceptual category rather than structural encoding.

Many studies have used visual adaptation to investigate how recent experience with faces influences perception. While faces similar to those seen during adaptation phases are typically perceived as more 'normal' after adaptation, it is possible to induce aftereffects in one direction for one category (e.g. female) and simultaneously induce aftereffects in the opposite direction for another category (e.g. male). Such aftereffects could reflect 'category-contingent' adaptation of neurons selective for perceptual category (e.g. male or female) or 'structure-contingent' adaptation of lower-level neurons coding the physical characteristics of different face patterns. We compared these explanations by testing for simultaneous opposite after effects following adaptation to (a) two groups of faces from distinct sex categories (male and female) or (b) two groups of faces from the same sex category (female and hyper-female) where the structural differences between the female and hyper-female groups were mathematically identical to those between male and female groups. We were able to induce opposite aftereffects following adaptation between sex categories but not after adaptation within a sex category. These findings indicate the involvement of neurons coding perceptual category in sex-contingent face aftereffects and cannot be explained by neurons coding only the physical aspects of face patterns.

Salience of emotional displays of danger and contagion in faces is enhanced when progesterone levels are raised.

Findings from previous studies of hormone-mediated behavior in women suggest that raised progesterone level increases the probability of behaviors that will reduce the likelihood of disruption to fetal development during pregnancy (e.g. increased avoidance of sources of contagion). Here, we tested women's (N=52) sensitivity to potential cues to nearby sources of contagion (disgusted facial expressions with averted gaze) and nearby physical threat (fearful facial expressions with averted gaze) at two points in the menstrual cycle differing in progesterone level. Women demonstrated a greater tendency to perceive fearful and disgusted expressions with averted gaze as more intense than those with direct gaze when their progesterone level was relatively high. By contrast, change in progesterone level was not associated with any change in perceptions of happy expressions with direct and averted gaze, indicating that our findings for disgusted and fearful expressions were not due to a general response bias. Collectively, our findings suggest women are more sensitive to facial cues signalling nearby contagion and physical threat when raised progesterone level prepares the body for pregnancy.

Facial appearance is a cue to oestrogen levels in women.

Although many accounts of facial attractiveness propose that femininity in women's faces indicates high levels of oestrogen, there is little empirical evidence in support of this assumption. Here, we used assays for urinary metabolites of oestrogen (oestrone-3-glucuronide, E1G) and progesterone (pregnanediol-3-glucuronide, P3G) to investigate the relationship between circulating gonadal hormones and ratings of the femininity, attractiveness and apparent health of women's faces. Positive correlations were observed between late follicular oestrogen and ratings of femininity, attractiveness and health. Positive correlations of luteal progesterone and health and attractiveness ratings were marginally significant. Ratings of facial attributions did not relate to hormone levels for women wearing make-up when photographed. There was no effect of sex of rater on the relationships between oestrogen and ratings of facial appearance. These findings demonstrate that female facial appearance holds detectable cues to reproductive health that are considered attractive by other people.

Menstrual cycle, trait estrogen level, and masculinity preferences in the human voice.

Men with low testosterone (feminine men) invest in relationships and offspring more than men with high testosterone (masculine men). Women's attraction to testosterone dependent traits (e.g. masculine face shape) is enhanced during the late-follicular, fertile phase of the menstrual cycle. Attractive, feminine women have stronger preferences for masculine men as possible long-term partners than less attractive, masculine women. We manipulated 2 testosterone related vocal traits (voice pitch and apparent vocal-tract length) in voices to test if women prefer masculinized men's voices to feminized men's voices; masculinity preferences are enhanced at the fertile (late-follicular) menstrual cycle phase; the amount that masculinity preferences shift cyclically relates to average estrone-3-glucuronide concentration (the primary urinary metabolite of estrone, E3G). We found women displayed general masculinity preferences for men's voices; masculinity preferences were greater in the fertile (late-follicular) phase of the cycle than the non-fertile (early-follicular and luteal) phase; and this effect was most pronounced for women with low average E3G concentration. As feminine women (i.e. those with high average E3G levels) are most able to obtain investment even from masculine men, these women may not need to change their mating preference or strategy during the menstrual cycle as much as masculine women.

Commitment to relationships and preferences for femininity and apparent health in faces are strongest on days of the menstrual cycle when progesterone level is high.

Previous studies of changes in women's behavior during the menstrual cycle have offered insight into the motivations underpinning women's preferences for social cues associated with possible direct benefits (e.g., investment, low risk of infection) and indirect benefits (e.g., offspring viability). Here we sought to extend this work by testing for systematic variation in women's preferences for male and female faces and in their attitudes to their romantic relationship during the menstrual cycle. In Study 1, we found partnered women's reported commitment to their romantic relationship and preferences for femininity in male and female faces were strongest on days of the menstrual cycle when progesterone levels are increased (and fertility is low). Happiness in relationships did not change across the cycle. In Study 2, we found that the effect of cycle phase on women's preference for feminine faces was independent of increased attraction to apparent health in faces during the luteal phase. Collectively, these findings are further evidence that women's preferences for social cues associated with possible direct benefits and commitment to relationships are strongest during conditions characterized by raised progesterone level, while attraction to men displaying cues associated with possible indirect benefits is strongest when women are most fertile.

Menstrual cycle, pregnancy and oral contraceptive use alter attraction to apparent health in faces.

Previous studies demonstrating changes in women's face preferences have emphasized increased attraction to cues to possible indirect benefits (e.g. heritable immunity to infection) that coincides with periods of high fertility (e.g. the late follicular phase of the menstrual cycle). By contrast, here we show that when choosing between composite faces with raised or lowered apparent health, women's preferences for faces that are perceived as healthy are (i) stronger during the luteal phase of the menstrual cycle than during the late follicular, fertile phase, (ii) stronger in pregnant women than in non-pregnant women and (iii) stronger in women using oral contraceptives than in women with natural menstrual cycles. Change in preference for male faces was greater for short- than long-term relationships. These findings indicate raised progesterone level is associated with increased attraction to facial cues associated with possible direct benefits (e.g. low risk of infection) and suggest that women's face preferences are influenced by adaptations that compensate for weakened immune system responses during pregnancy and reduce the risk of infection disrupting foetal development.

Out of sight but not out of mind: the neurophysiology of iconic memory in the superior temporal sulcus.

Iconic memory, the short-lasting visual memory of a briefly flashed stimulus, is an important component of most models of visual perception. Here we investigate what physiological mechanisms underlie this capacity by showing rapid serial visual presentation (RSVP) sequences with and without interstimulus gaps to human observers and macaque monkeys. For gaps of up to 93 ms between consecutive images, human observers and neurones in the temporal cortex of macaque monkeys were found to continue processing a stimulus as if it was still present on the screen. The continued firing of neurones in temporal cortex may therefore underlie iconic memory. Based on these findings, a neurophysiological vision of iconic memory is presented.

Are the perceptual biases found in chimeric face processing reflected in eye-movement patterns?

Studies of patients with focal brain lesions and neuroimaging indicate that face processing is predominantly based on right hemisphere function. Additionally, experiments using chimeric faces, where the left and the right-hand side of the face are different, have shown that observers tend to bias their responses toward the information on the left. Here, we monitored eye-movements during a gender identification task using blended face images for both whole and chimeric (half female, half male) faces [Neuropsychologia 35 (1997) 685]. As expected, we found a left perceptual bias: subjects based their gender decision significantly more frequently on the left side of the chimeric faces. Analysis of the first saccade showed a significantly greater number of left fixations independent of perceptual bias presumably reflecting the tendency to first inspect the side of the face better suited to face analysis (left side of face/right hemisphere). On top of this though, there was a relationship between response and fixation pattern. On trials where participants showed a left perceptual bias they produced significantly more left saccades and fixated for longer on the left. In contrast, for trials where participants showed a right perceptual bias there was no reliable difference between the number, or total fixation duration, on the left or the right. These results demonstrate that on a trial-by-trial basis subtle differences in the extent of left or right side scanning are related to the perceptual response of the participant, although an overall initial fixation bias to the left occurs irrespective of response bias.

A region of right posterior superior temporal sulcus responds to observed intentional actions.

Human adults and infants identify the actions of another agent based not only on its intrinsic perceptual features, but critically on the contingent relationship between its motion path and the environmental context [Trends Cogn. Sci. 7 (1995) 287; Cognition 72 (2003) 237]. Functional neuroimaging studies of the perception of agents and intentional actions, on the other hand, have mostly focussed on the perception of intrinsic cues to agency, like a face or articulated body motion (e.g. [J. Neurosci. 17 (1997) 4302; Neuroimage 8 (1998) 221; Trends Cogn. Sci. 4 (2000) 267; Nat. Neurosci. 3 (2000) 80; Neuroimage 13 (2001) 775; Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 11656; Neuron 35 (2002) 1167; Neuron 34 (2002) 149, Neuroscience 15 (2003) 991; J. Neurosci. 23 (2003) 6819; Philos. Trans. R Soc. Lond. B. Biol. Sci. 358 (2003) 435]. Here we describe a region of the right posterior superior temporal sulcus that is sensitive not to articulated body motion per se, but to the relationship between the observed motion and the structure of the surrounding environment. From this and other aspects of the region's response, we hypothesize that this region is involved in the representation of observed intentional actions.

Female condition influences preferences for sexual dimorphism in faces of male humans (Homo sapiens).

In some species, female condition correlates positively with preferences for male secondary sexual traits. Women's preferences for sexually dimorphic characteristics in male faces (facial masculinity) have recently been reported to covary with self-reported attractiveness. As women's attractiveness has been proposed to signal reproductive condition, the findings in human (Homo sapiens) and other species may reflect similar processes. The current study investigated whether the covariation between condition and preferences for masculinity would generalize to 2 further measures of female attractiveness: other-rated facial attractiveness and waist-to-hip ratio (WHR). Women with high (unattractive) WHR and/or relatively low other-rated facial attractiveness preferred more "feminine" male faces when choosing faces for a long-term relationship than when choosing for a short-term relationship, possibly reflecting diverse tactics in female mate choice.