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.

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.

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.

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.

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.

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 'Ideal Homunculus': decoding neural population signals.

Information processing in the nervous system involves the activity of large populations of neurons. It is possible, however, to interpret the activity of relatively small numbers of cells in terms of meaningful aspects of the environment. 'Bayesian inference' provides a systematic and effective method of combining information from multiple cells to accomplish this. It is not a model of a neural mechanism (neither are alternative methods, such as the population vector approach) but a tool for analysing neural signals. It does not require difficult assumptions about the nature of the dimensions underlying cell selectivity, about the distribution and tuning of cell responses or about the way in which information is transmitted and processed. It can be applied to any parameter of neural activity (for example, firing rate or temporal pattern). In this review, we demonstrate the power of Bayesian analysis using examples of visual responses of neurons in primary visual and temporal cortices. We show that interaction between correlation in mean responses to different stimuli (signal) and correlation in response variability within stimuli (noise) can lead to marked improvement of stimulus discrimination using population responses.

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.

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.

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.

Imitation, mirror neurons and autism.

Various deficits in the cognitive functioning of people with autism have been documented in recent years but these provide only partial explanations for the condition. We focus instead on an imitative disturbance involving difficulties both in copying actions and in inhibiting more stereotyped mimicking, such as echolalia. A candidate for the neural basis of this disturbance may be found in a recently discovered class of neurons in frontal cortex, 'mirror neurons' (MNs). These neurons show activity in relation both to specific actions performed by self and matching actions performed by others, providing a potential bridge between minds. MN systems exist in primates without imitative and 'theory of mind' abilities and we suggest that in order for them to have become utilized to perform social cognitive functions, sophisticated cortical neuronal systems have evolved in which MNs function as key elements. Early developmental failures of MN systems are likely to result in a consequent cascade of developmental impairments characterised by the clinical syndrome of autism.

Perceptual asymmetries in judgements of facial attractiveness, age, gender, speech and expression.

Lateralization of perception of various facial attributes (age, attractiveness, gender, lip-reading and expression) was studied using chimaeric faces in which the sides of the face differed along one dimension (e.g. the left side was male and the right side female). Computer graphics were used to eliminate naturally occurring physical asymmetries (e.g. those present in the mouth during speech and spontaneous smiles) and obvious vertical mid-line joins in the photo-realistic chimaeric stimuli. Following previous studies, we found that subjects' judgements of gender and expression were influenced more by the left than the right side of the face (viewer's perspective). This left of face stimulus bias extended to judgements about facial attractiveness and facial age. This was not true of lip-reading stimuli; for these stimuli subjects were influenced more by the right than the left side of the face. Thus using free fixation, it appears possible to demonstrate in normal subjects that brain processes underlying judgements of facial speech display different lateralization from the judgements of other facial dimensions.

Event-related potentials and the matching of familiar and unfamiliar faces.

Event-related potentials (ERPs) were recorded from one midline and three pairs of lateral sites while subjects made same/different judgements on sequentially presented pairs of familiar or unfamiliar faces. During the interval between the first and second face, a slow wave was more negative-going over the right than the left hemisphere, particularly when the faces were familiar. Following the second face, two regions of the waveforms were more negative-going when this face did not match the identity of its predecessor. In the early region (less than 160 msec), this effect was confined to posterior electrode sites and familiar faces. In the later region (greater than 250 msec), the match/non-match effect was widespread across the scalp and was evident for both familiar and non-familiar faces, although in the latency range 350-450 msec (encompassing the "N400" component), it was greater in magnitude in the case of familiar stimuli. It is suggested that the slow wave asymmetries reflect the engagement of short-term memory mechanisms lateralized to the right hemisphere. The match/non-match differences are thought to reflect multiple processes, including the modulation of the "N400" component. The sensitivity of this component to the familiarity manipulation is consistent with the hypothesis that the amplitude of N400 reflects an item's compatibility with currently activated memory representations.

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.

Acute SSRI administration affects the processing of social cues in healthy volunteers.

Enhancement of serotonin neurotransmission plays an important role in the antidepressant response to agents presently available to treat depression. This response forms the major evidence for the role of serotonin in affective and social behaviour in humans. The present study investigated the effects of acute administration of the selective serotonin reuptake inhibitor (SSR1), citalopram (10 mg, i.v.) upon a measure of emotional processing in healthy female volunteers. Subjects completed a facial expression recognition task following infusion of citalopram or saline (between-subjects design, double-blind). Facial expressions associated with five basic emotions--happiness, sadness, fearfulness, anger and disgust--were displayed. Each face had been 'morphed' between neutral (0%) and each emotional standard (100%) in 10% steps, leading to a range of emotional intensities. Mood and subjective experience were also monitored throughout the testing session. Volunteers receiving citalopram detected a higher number of facial expressions of fear and happiness, with reduced response times, relative to those given the placebo. By contrast, changes in the recognition of other basic emotions were not observed following citalopram. Notable differences in mood were also not apparent in these volunteers. These results suggest that acute administration of antidepressant drugs may affect neural processes involved in the processing of social information. This effect may represent an early acute effect of SSRIs on social and emotional processing that is relevant to their therapeutic actions.

Responses of striatal neurons in the behaving monkey. 3. Effects of iontophoretically applied dopamine on normal responsiveness.

In order to analyse the functions of dopamine, the effects of the iontophoretic application of dopamine on the responsiveness of striatal neurons to their normal inputs were investigated in the behaving monkey. It was shown that many neurons in the putamen had responses related to movements, of for example the mouth. Iontophoretically applied dopamine decreased the spontaneous firing rates of 178 of 267 neurons (67%) tested in the putamen, caudate nucleus, and the adjacent prefrontal cortex which also receives a dopaminergic projection. Trifluoperazine, applied iontophoretically to block dopamine receptors, increased the spontaneous firing rates of some of the neurons in the prefrontal cortex, suggesting that under normal conditions in the behaving animal the release of dopamine holds the firing rates of these neurons at a low level. The median was 9 spikes/s in the present sample of striatal neurons. Application of dopamine decreased the magnitude of the movement-related responses of the striatal neurons; this decrease in the responses was of approximately the same magnitude in spikes per second as the decrease in the spontaneous firing rate of the neurons produced by the same current of dopamine. It is suggested that this type of effect of dopamine could influence the signal to noise ratio of processing within the striatum, and that changes in this signal to noise ratio produced by disturbances of dopaminergic function could contribute to the behavioral disorders produced by dysfunctions of the dopaminergic systems.