Sex-specific norms code face identity.

Face identity aftereffects suggest that an average face, which is continuously updated by experience, functions as a norm for coding identity. Sex-contingent figural face aftereffects indicate that different norms are maintained for male and female faces but do not directly implicate them in coding identity. Here, we investigated whether sex-specific norms are used to code the identities of male and female faces or whether a generic, androgynous norm is used for all faces. We measured identity aftereffects for adapt-test pairs that were opposite relative to a sex-specific average and pairs that were opposite relative to an androgynous average. Identity aftereffects are generally larger for adapt-test pairs that lie opposite an average face, which functions as a norm for coding identity, than those that do not. Therefore, we reasoned that whichever average gives the larger aftereffect would be closer to the true psychological norm. Aftereffects were substantially and significantly larger for pairs that lie opposite a sex-specific than an androgynous average. This difference remained significant after correcting for differences in test trajectory length. These results indicate that, despite the common structure shared by all faces, identity is coded using sex-specific norms. We suggest that the use of category-specific norms may increase coding efficiency and help us discriminate thousands of faces despite their similarity as patterns.

The relation between anger and different forms of disgust: implications for emotion recognition impairments in Huntington's disease.

Initial reports of emotion recognition in Huntington's disease (HD) found disproportionate impairments in recognising disgust. Not all subsequent studies have found this pattern, and a review of the literature to date shows that marked impairments in recognising anger are also often seen in HD. However, the majority of studies have based their conclusions on a single test of facial expression recognition. In the current study we revisit this issue of emotion recognition in HD to address whether the pattern found on one test of facial expression recognition generalised to another, and to different modalities using tests of emotion recognition from facial expressions, vocal expressions, and short verbal vignettes. The results showed evidence of impairments in recognising anger, fear and disgust across the three domains, with recognition of anger the most severely impaired. Given work identifying different subtypes of disgust that are associated with different facial features, a second study examined the recognition of three disgust expressions that healthy participants reliably associate with unpleasant tastes, unpleasant smells, and a more general elaborated or expanded form of disgust that includes reactions to violations of moral standards. The results showed a disproportionate impairment in recognising faces associated with the expanded form, the subtype most closely aligned with anger. We conclude that the related emotions of disgust and anger associated with social disapproval are frequently impaired in HD and discuss factors that might cause one emotion to show more severe impairments than the other.

Leaving a bad taste in your mouth but not in my insula.

Previous research has implicated regions of anterior insula/frontal operculum in processing conspecific facial expressions of disgust. It has been suggested however that there are a variety of disgust facial expression components which relate to the disgust-eliciting stimulus. The nose wrinkle is predominantly associated with irritating or offensive smells, the mouth gape and tongue extrusion with distaste and oral irritation, while a broader range of disgust elicitors including aversive interpersonal contacts and certain moral offenses are associated primarily with the upper lip curl. Using functional magnetic resonance imaging, we show that activity in the anterior insula/frontal operculum is seen only in response to canonical disgust faces, exhibiting the nose wrinkle and upper lip curl, and not in response to distaste facial expressions, exhibiting a mouth gape and tongue protrusion. Canonical disgust expressions also result in activity in brain regions linked to social cognition more broadly, including dorsal medial prefrontal cortex, posterior cingulate cortex, temporo-parietal junction and superior temporal sulcus. We interpret these differences in relation to the relative functional and communicative roles of the different disgust expressions and suggest a significant role for appraisal processes in the insula activation to facial expressions of disgust.

Anxiety predicts a differential neural response to attended and unattended facial signals of anger and fear.

Behavioural evidence indicates that individual differences in anxiety influence the response to facial signals of threat. Angry and fearful faces represent qualitatively different forms of threat. Fearful faces are thought to signal the presence of a significant, yet undetermined source of danger within the environment, referred to as 'ambiguous threat'. In contrast, angry faces represent a more direct form of threat, often used in face-to-face encounters to exert dominance. Given the inherent differences between anger and fear, we hypothesised that anxiety would modulate the amygdala response to angry faces to a greater extent when attended. Following previous research, we expected anxiety to show a stronger relationship with the amygdala response to unattended fearful faces. In an event-related fMRI study, we presented images of two houses and two faces (consisting of fearful, angry or neutral expressions) in horizontal and vertical pairs around a central fixation cross, with participants instructed to attend to either the face or house stimuli. The results showed that higher anxiety levels produced an increased right amygdala response to viewer directed angry facial expressions (versus neutral or fearful faces) only when attended. By contrast, increased anxiety was associated with a greater left amygdala response to fearful faces (versus neutral or angry faces) in the unattended condition, with only borderline evidence for attended fear (relative to neutral). Our findings demonstrate the striking effects of personality in a non-clinical population, and show how this can distinguish the neural coding of anger and fear faces.

Connectivity from the ventral anterior cingulate to the amygdala is modulated by appetitive motivation in response to facial signals of aggression.

For some people facial expressions of aggression are intimidating, for others they are perceived as provocative, evoking an aggressive response. Identifying the key neurobiological factors that underlie this variation is fundamental to our understanding of aggressive behaviour. The amygdala and the ventral anterior cingulate cortex (ACC) have been implicated in aggression. Using functional magnetic resonance imaging (fMRI), we studied how the interaction between these regions is influenced by the drive to obtain reward (reward-drive or appetitive motivation), a personality trait consistently associated with aggression. Two distinct techniques showed that the connectivity between the ventral ACC and the amygdala was strongly correlated with personality, with high reward-drive participants displaying reduced negative connectivity. Furthermore, the direction of this effect was restricted from ventral ACC to the amygdala but not vice versa. The personality-mediated variation in the pathway from the ventral anterior cingulate cortex to the amygdala provides an account of why signals of aggression are interpreted as provocative by some individuals more than others.

Disgust sensitivity predicts the insula and pallidal response to pictures of disgusting foods.

The anterior insula has been implicated in coding disgust from facial, pictorial and olfactory cues, and in the experience of this emotion. Personality research has shown considerable variation in individuals' trait propensity to experience disgust ('disgust sensitivity'). Our study explored the neural expression of this trait, and demonstrates that individual variation in disgust sensitivity is significantly correlated with participants' ventroanterior insular response to viewing pictures of disgusting, but not appetizing or bland, foods. Similar correlations were also seen in the pallidum and orofacial regions of motor and somatosensory cortices. Our results also accord with comparative research showing an anterior to posterior gradient in the rat pallidum reflecting increased 'liking' of foods [Smith, K. S. and Berridge, K. C. (2005) J. Neurosci., 25, 849-8637].

Impaired recognition of anger following damage to the ventral striatum.

Comparative neuropsychology has identified a role for the ventral striatum (VS) in certain forms of aggression. To address whether the homologous region in humans also contributes to the emotion anger, we studied a case series of four human subjects with focal lesions affecting the VS. All four demonstrated a disproportionate impairment in recognizing human signals of aggression. By contrast, a control group of individuals with damage to more dorsal basal ganglia (BG) regions showed no evidence of an anger impairment. Our findings demonstrate that the VS makes a significant contribution to coding signals of aggression in humans, and emphasize the importance of an approach to human affective neuroscience based on cross-species homologies. The results are discussed in relation to the ventral striatal dopamine system's role in the pursuit of biological resources in general. We propose that the role of the VS in the recognition of human signals of anger may reflect a more general role in the coordination of behaviour relevant to the acquisition and protection of valued resources, including detection of signals of conspecific challenge (anger).

Facial expression recognition across the adult life span.

We report three experiments investigating the recognition of emotion from facial expressions across the adult life span. Increasing age produced a progressive reduction in the recognition of fear and, to a lesser extent, anger. In contrast, older participants showed no reduction in recognition of disgust, rather there was some evidence of an improvement. The results are discussed in terms of studies from the neuropsychological and functional imaging literature that indicate that separate brain regions may underlie the emotions fear and disgust. We suggest that the dissociable effects found for fear and disgust are consistent with the differential effects of ageing on brain regions involved in these emotions.

Acquired theory of mind impairments in individuals with bilateral amygdala lesions.

Studies in humans suggest that the amygdala plays a role in processing social information. A key component of social information processing is what developmental psychologists call "theory of mind": the ability to infer others' mental states. Recent studies have raised the possibility that the amygdala is involved in theory of mind, showing amygdala activation during a theory of mind task, or showing impairment on theory of mind tasks in a patient with amygdala damage acquired in childhood. Here, we present the first evidence of theory of mind deficits following amygdala damage acquired in adulthood. Two participants, D.R. and S.E., with acquired bilateral amygdala damage showed difficulties with two theory of mind tasks, "Recognition of Faux Pas" (for D.R., z=-5.17; for S.E., z=-1.83) and "Reading the Mind in the Eyes" (for S.E., z=-1.91; for D.R., z=-1.4). The items on which D.R. and S.E. made errors on these tasks were uncorrelated with the items that control participants found most difficult, indicating that these deficits cannot be attributed solely to the cognitive difficulty of the tasks. These results indicate that the amygdala's critical role in theory of mind may not be just in development, but also in "on-line" theory of mind processing in the adult brain.

Reading the mind from eye gaze.

Baron-Cohen [Mindblindness: an essay on autism and theory of mind. Cambridge, MA: MIT Press, 1997] has suggested that the interpretation of gaze plays an important role in a normal functioning theory of mind (ToM) system. Consistent with this suggestion, functional imaging research has shown that both ToM tasks and eye gaze processing engage a similar region of the posterior superior temporal sulcus (STS). However, a second brain region associated with ToM, the medial prefrontal (MPF) cortex, has not been identified by previous eye gaze studies. We discuss the methodological issues that may account for the absence of MPF activation in these experiments and present a PET study that controls for these factors. Our experiment included three conditions in which the proportions of faces gazing at, and away from, the participant, were as follows: 100% direct [0% averted], 50% direct-50% averted, and 100% horizontally averted [0% direct]. Two control conditions were also included in which the faces' gaze were averted down, or their eyes were closed. Contrasts comparing the gaze conditions with each of the control conditions revealed medial frontal involvement. Parametric analyses showed a significant linear relationship between increasing proportions of horizontally averted gaze and increased rCBF in the MPF cortex. The opposite parametric analysis (increasing proportions of direct gaze) was associated with increased rCBF in a number of areas including the superior and medial temporal gyri. Additional subtraction contrasts largely confirmed these patterns. Our results demonstrate a considerable degree of overlap between the medial frontal areas involved in eye gaze processing and theory of mind tasks.

Face and emotion processing in frontal variant frontotemporal dementia.

Lavenu et al. [Alzheimer Dis. Assoc. Disorder 5 (1999) 96] have shown that patients with frontotemporal dementia (FTD) show impaired recognition of facial expressions. It is not clear, however, whether these deficits arise from an impairment affecting face processing generally, emotion processing generally, or facial expression recognition alone. We address this issue by testing six patients with frontal variant frontotemporal dementia (fvFTD) on a series of face perception tasks (including facial identity and facial expression recognition), and a test of vocal emotion recognition. In general, the fvFTD participants showed impaired recognition of facial expressions in the context of preserved recognition of facial identity. In addition, however, deficits were also observed for the vocal emotion recognition task. These results are consistent with the idea that fvFTD affects the recognition of emotional signals from multiple modalities rather than facial expression processing alone. It is plausible that the emotion recognition impairments observed contribute to the abnormal social behaviour that is characteristic of this condition.