Eye Region Of Faces Research Articles

Less attention to emotional faces is associated with low empathy and prosociality in 12-to 20-month old infants.

The development of empathy and prosocial behavior begins in infancy and is likely supported by emotion processing skills. The current study explored whether early emerging deficits in emotion processing are associated with disruptions in the development of empathy and prosociality. We investigated this question in a large, diverse sample of 147, 11- to 20-month-old infants (42% female; 61% Black; 67% low socioeconomic status). Infants completed two observational tasks assessing prosocial helping and one task assessing empathy and prosocial comforting behavior. Infants also completed an eye-tracking task assessing engagement and disengagement with negative emotional faces. Infants who attended less to angry, sad, and fearful faces (i.e., by being slower to look at and/or quicker to look away from negative compared to neutral faces) engaged in fewer helping behaviors, and effect sizes were larger when examining infants' attention toward the eye regions of faces. Additionally, infants who were quicker to look away from the eye regions of angry faces, but not the whole face, displayed less empathy and comforting behaviors. Results suggest that as early as 12months of age, infants' decreased attention toward negative emotional faces, particularly the eye regions, is associated with less empathy and prosociality during a developmental period in which these abilities are rapidly maturing.

Tryptophan-rich diet is negatively associated with depression and positively linked to social cognition

The essential amino acid tryptophan (TRP) is discussed as a potential protective factor for physical and mental health. Besides positive effects via the microbiota of the gut on many physiological processes, TRP is the precursor of the neurotransmitter serotonin (5-HT), thereby playing a role for affective disorders. The present study investigated the effects of a TRP-rich diet on depressiveness and on one of its endophenotypes, impaired social cognition, in a population based sample. N = 482 subjects participated in an online study, assessing the ability to properly recognize emotional states from the eye region of faces (Reading the Mind in the Eye Test, RMET) and asking for subjective ratings of condemnability in a moral judgment task. Moreover, the habitual TRP intake was measured. It was hypothesized that a low-TRP diet is associated with higher depressiveness and worse performance in the social cognition tasks. The main hypotheses could be supported. However, contrary to the expectations, the effect of TRP on social cognition was not mediated by depressiveness. Results show that a tryptophan-rich diet is a potential protective factor against depression and is positively related to functioning in social cognition.

Delayed gaze shifts away from others’ eyes in children and adolescents with social anxiety disorder

BackgroundSocial anxiety disorder (SAD) is linked to atypical attention to other's eyes. Empirical literature about this phenomenon in childhood and adolescence is scarce. Previous studies in adults have suggested that SAD may be characterized by either rapid avoidance of eye contact, or by impaired shifting of attention away from eyes once eye contact has been established. SAD has also been linked to quick orienting towards eyes, indicating vigilant monitoring of perceived threat. MethodsIn the largest eye-tracking study of youth with SAD to date, 10 to 17 year-olds with SAD (n = 88) and healthy controls (n = 62) were primed to look at either the eyes or the mouth of human faces. The latency and likelihood of a first gaze shift from, or to the eyes, was measured. ResultsIndividuals with SAD were slower to shift their gaze away from the eye region of faces than controls, but did not differ in orienting toward eyes. LimitationsParticipants were assessed once after the onset of SAD symptoms, meaning that the longitudinal predictive value of delayed gaze shifts from others’ eyes could not be examined. ConclusionsYouth with SAD may be impaired in shifting attention from other's eyes. This could contribute to the experience of eye contact as aversive, and may be a maintaining factor of childhood SAD.

Oxytocin biases eye-gaze to dynamic and static social images and the eyes of fearful faces: associations with trait autism

A key functional effect of intranasal oxytocin with potential therapeutic relevance for autism-spectrum disorder is its reported facilitation of attention towards social stimuli, notably the eye region of faces. In the current randomized placebo-controlled within-subject experiment on 40 healthy males, we investigated the robustness of this facilitation of attention by intranasal oxytocin (24IU) towards social cues. Eye-tracking measures of preference for dynamic and static social vs. non-social stimuli were taken in four different paradigms where autistic individuals tend to exhibit reduced interest in social stimuli. Additionally, we investigated whether oxytocin increases attention towards the eyes relative to other salient face regions in an emotional face paradigm. Results showed that the time spent viewing both dynamic and static social vs. non-social stimuli was negatively associated with trait autism and significantly increased following intranasal oxytocin. For face stimuli, oxytocin primarily increased gaze towards the eyes of fearful expression faces but not for other face emotions. Overall, our findings demonstrate that oxytocin significantly shifts gaze preference towards social vs. non-social stimuli and to the eyes of fearful faces. Importantly, oxytocin appears generally to shift attention more towards salient social stimuli of particular relevance in the context of autism providing further support for its potential therapeutic use in autism-spectrum disorder.

Fixation-pattern similarity analysis reveals adaptive changes in face-viewing strategies following aversive learning.

Animals can effortlessly adapt their behavior by generalizing from past aversive experiences, allowing to avoid harm in novel situations. We studied how visual information was sampled by eye-movements during this process called fear generalization, using faces organized along a circular two-dimensional perceptual continuum. During learning, one face was conditioned to predict a harmful event, whereas the most dissimilar face stayed neutral. This introduced an adversity gradient along one specific dimension, while the other, unspecific dimension was defined solely by perceptual similarity. Aversive learning changed scanning patterns selectively along the adversity-related dimension, but not the orthogonal dimension. This effect was mainly located within the eye region of faces. Our results provide evidence for adaptive changes in viewing strategies of faces following aversive learning. This is compatible with the view that these changes serve to sample information in a way that allows discriminating between safe and adverse for a better threat prediction.

Remediating functional activation in the face perception network in autism and 22q11.2 deletion syndrome

Introduction: Vis-à-Vis (VAV), an online enrichment program targeting skills that underlie social abilities (looking at the eye region of faces, emotion comprehension & recognition and visuo-spatial working memory) was administered to children and adolescents with autism spectrum disorder (ASD), 22q11.2 deletion syndrome (22q11DS)) and developmental delay (DD). Differential functional activation throughout the brain and in regions related to face processing were measured before and after remediation.
 Methods: Participants with ASD (N=16), 22q11DS (N=12), and DD (N=9) completed a functional localizer task consisting of pictures of faces and tools before undertaking the 12-week VAV program (PreR). The same fMRI task was administered immediately after VAV, at post-remediation (PostR), and again three months later (Break). A group of healthy controls (N=10) was scanned, but not given VAV, to provide a baseline comparison for patients’ results. Functional neuroimaging data was analysed for category-specific brain activity.
 Results: The ASD and the 22q11DS groups both showed atypical activation to faces at PreR compared to controls. Whereas activation in 22q11DS at PostR and Break resembled that of controls in bilateral superior temporal gyrus, insula, bilateral precentral gyrus, right lingual gyrus and right middle frontal cortex. Unlike the 22q11DS group, the ASD group’s activation did not resemble that of controls at PostR or Break. Significant clusters in the ASD group were limited to left insula and right lingual gyrus at PostR, and right superior frontal gyrus at Break. Nevertheless, a significant relationship between increased BOLD response between PreR and PostR in the right fusiform gyrus and improvement on the VAV games teaching participants to focus on the eyes was observed in both groups. This relationship was not present in the DD group.
 Conclusions: These results support hypo-activation in response to faces in ASD and 22q11DS and differential cerebral activation in face processing networks following cognitive remediation.

Children with social anxiety disorder show blunted pupillary reactivity and altered eye contact processing in response to emotional faces: Insights from pupillometry and eye movements

Cognitive models and adult research associate social anxiety disorder (SAD) with hypervigilant-avoidant processing of social information, such as eye contact. However, processing biases in childhood SAD remain mostly unexplored. We examined 10- to 13-year-old children’s eye contact processing and pupil dilation in response to happy, neutral, and angry faces in three groups: SAD (n = 31), mixed anxiety disorders (MAD; n = 30), and healthy controls (HC; n = 32). Compared to HC, SAD children showed faster first fixations on the eye region of neutral faces and shorter first fixation durations on the eye region of all faces. No differences between the two clinical groups emerged in eye movement results. SAD girls showed reduced pupil dilation in response to happy and angry faces compared to MAD and to happy faces compared to HC. SAD boys showed reduced pupil dilation in response to neutral faces compared to HC. Dimensionally, reduced pupil dilation was linked to social anxiety severity while eye movements were correlated with mixed anxiety and depressive severity.Results suggest that hypervigilant-avoidant eye contact processing and a blunted pupillary reactivity characterize children with SAD. Both transdiagnostic and disorder-specific processing biases are relevant for the understanding of childhood SAD.

Gaze behavior to faces during dyadic interaction.

A long-standing hypothesis is that humans have a bias for fixating the eye region in the faces of others. Most studies have tested this hypothesis with static images or videos of faces, yet recent studies suggest that the use of such "nonresponsive" stimuli might overlook an influence of social context. The present study addressed whether the bias for fixating the eye region in faces would persist in a situation that allowed for social interaction. In Experiment 1, we demonstrate a setup in which a duo could engage in social interaction while their eye movements were recorded. Here, we show that there is a bias for fixating the eye region of a partner that is physically present. Moreover, we report that the time 1 partner in a duo spends looking at the eyes is a good predictor of how long the other partner looks at the eyes. In Experiment 2, we investigate whether participants attune to the level of eye contact instigated by a partner by having a confederate pose as one of the partners. The confederate was subsequently instructed to either fixate the eyes of the observer or scan the entire face. Gaze behaviour of the confederate did not affect gaze behaviour of the observers. We conclude that there is a bias to fixate the eyes when partners can engage in social interaction. In addition, the amount of time spent looking at the eyes is duo-dependent, but not easily manipulated by instructing the gaze behaviour of 1 partner. (PsycINFO Database Record

The cognitive and neural basis of developmental prosopagnosia.

Developmental prosopagnosia (DP) is a severe impairment of visual face recognition in the absence of any apparent brain damage. The factors responsible for DP have not yet been fully identified. This article provides a selective review of recent studies investigating cognitive and neural processes that may contribute to the face recognition deficits in DP, focusing primarily on event-related brain potential (ERP) measures of face perception and recognition. Studies that measured the face-sensitive N170 component as a marker of perceptual face processing have shown that the perceptual discrimination between faces and non-face objects is intact in DP. Other N170 studies suggest that faces are not represented in the typical fashion in DP. Individuals with DP appear to have specific difficulties in processing spatial and contrast deviations from canonical upright visual-perceptual face templates. The rapid detection of emotional facial expressions appears to be unaffected in DP. ERP studies of the activation of visual memory for individual faces and of the explicit identification of particular individuals have revealed differences between DPs and controls in the timing of these processes and in the links between visual face memory and explicit face recognition. These observations suggest that the speed and efficiency of information propagation through the cortical face network is altered in DP. The nature of the perceptual impairments in DP suggests that atypical visual experience with the eye region of faces over development may be an important contributing factor to DP.

Don't look at my teeth when I smile: Teeth visibility in smiling faces affects emotionality ratings and gaze patterns.

Research on facial emotion processing has offered inconclusive results on whether certain emotional expressions, like happiness, are detected faster over others. A source of discrepancy among studies could stem from differences in physically salient features (e.g., teeth visibility), which are often left uncontrolled in this field of research. In Study 1, happy faces from the Karolinska Database Emotional Databse with visible, normal teeth unexpectedly obtained lower scores on intensity and prototypicality than the same faces with covered teeth. In Study 2, an eye-tracking methodology revealed that although faces with normal teeth drew participants' initial attention, participants spent more time looking at the eye region in faces with covered teeth, a region that previous research had found to be more informative of emotion than the mouth region. Overall, these results suggest that advantages often associated with certain emotional faces might be partially due to artifacts that should be systematically controlled for in future studies. (PsycINFO Database Record

Spatial limitations in averaging social cues.

The direction of social attention from groups provides stronger cueing than from an individual. It has previously been shown that both basic visual features such as size or orientation and more complex features such as face emotion and identity can be averaged across multiple elements. Here we used an equivalent noise procedure to compare observers’ ability to average social cues with their averaging of a non-social cue. Estimates of observers’ internal noise (uncertainty associated with processing any individual) and sample-size (the effective number of gaze-directions pooled) were derived by fitting equivalent noise functions to discrimination thresholds. We also used reverse correlation analysis to estimate the spatial distribution of samples used by participants. Averaging of head-rotation and cone-rotation was less noisy and more efficient than averaging of gaze direction, though presenting only the eye region of faces at a larger size improved gaze averaging performance. The reverse correlation analysis revealed greater sampling areas for head rotation compared to gaze. We attribute these differences in averaging between gaze and head cues to poorer visual processing of faces in the periphery. The similarity between head and cone averaging are examined within the framework of a general mechanism for averaging of object rotation.

Social Attention in 47,XXY (Klinefelter Syndrome): Visual Scanning of Facial Expressions Using Eyetracking.

Boys and men with an extra X chromosome (47,XXY, Klinefelter syndrome) are at risk for problems in social functioning and have an increased vulnerability for autism spectrum disorders (ASD). In the search for underlying mechanisms driving this increased risk, this study focused on social attention, that is, spontaneous orientation toward facial expressions. Seventeen adults with 47,XXY and 20 non-clinical controls participated in this study. Social attention was measured using an eyetracking method that quantifies the visual scanning patterns of faces expressing different types of emotions (happy, fearful, angry, neutral) and their varying intensity levels (25%, 50%, 75%, 100%). Overall, the group with Klinefelter syndrome fixated less on the eye region of faces when compared to controls (Cohen's d 1.4), and did not show the typical tendency, as was found in the control group, to first fixate on the eyes when presented with a face (Cohen's d 1.0). There was no significant effect of type or intensity of emotion. Shorter looking times toward eyes showed a borderline significant correlation with self-reports of poorer social functioning, with 29% explained variance. These findings suggest a reduced tendency to rapidly and automatically attend to the eyes of others in individuals with 47,XXY. This may have impact on more complex social-cognitive abilities that build upon this. In addition to studies of behaviorally defined disorders such as ASD, studying individuals with Klinefelter syndrome provide insight into mechanisms underlying various "at risk" pathways of social dysfunction and the factors that mediate this risk.

Social attention and the ventromedial prefrontal cortex.

Imagine looking out over the patrons in a restaurant as one of them looks up from their plate of food and makes eye contact with you. The change in the visual image on your retina is miniscule, yet the knowledge gained is great. A tiny change in the movements of another person’s eyes lets you know instantly that they are looking at you, know that you are also looking at them, and feel a particular emotion or have a particular intention. In this issue of Brain, Wolf et al. (2014) describe three patients with focal lesions of the ventromedial prefrontal cortex (vmPFC) who show strikingly atypical patterns of fixation onto faces: they do not look at a person’s eyes, with implications for social decision-making. The eye region of faces is salient not only because it tells us where somebody else is directing their attention, but also because it informs us of their emotional state (the muscles around the eyes contribute substantially to certain emotional facial expressions, most particularly fear). Deficits in our ability to process this information may underlie aspects of paranoid schizophrenia (feeling as though somebody is watching you all the time) as well as autism spectrum disorders (where diminished eye contact is associated with social disengagement; Fig. 1). The ability to use our perception of another person’s gaze to guide our own attention emerges during specific stages of early development, and some aspects of this ability may be unique to humans (although dogs are also quite good at figuring out social attention signals). To understand these different facets of social attention, it is a high priority to elucidate the neural substrates involved.

Emotional Empathy in Children with Autism Spectrum Disorder: Evidence from Biofeedback Measurement and Eye Movements

Autism spectrum disorders(ASD) are considered as a series of pervasive developmental disorders, and characterized by deficits in social interaction, delays and deviance in communication, and repetitive behaviors, rituals and interests. Emotional empathy refers to unconscious experience of emotions consistent with and in response to those of others and imitation of the facial expression, induced by shared representations of perception and emotional contagion. Eye-tracking studies have demonstrated that the visual fixation patterns of children with autism in social situations differ from normal patterns. Children with autism do not seem to attend spontaneously to salient features of the social stimulus in the way that most people do. It is possible that this reflects an attentional style that limits empathic arousal. Children with autism, relative to typically developing children, focused less on the eye region of faces when viewing social stimulus, because they avoid eye contact with others in order to decrease arousal. Previous studies explored emotional empathic responses to affective stimuli in children with ASD, but their results are inconsistent. The present research was designed to investigate the emotional empathy and the face scanning patterns of children with ASD using biofeedback measurement and eye-tracking. Fifteen children with ASD, fifteen typically developing(TD) children, and fifteen children with intellectual disability(ID) viewed eighty emotional faces with happiness, sadness, fear and anger from the Chinese Facial Affective Picture System(each emotional category consists of twenty pictures). Facial electromyography(EMG) activity, eye movements and automatic physiological responses, including skin conductance(SCR), skin temperature(TEMP) and PLUS, were recorded during the experiment. Comparing with typically developing children, children with ASD demonstrated atypical processing patterns of emotional faces with reduced responses of automatic facial EMG, and automatic physiological(SCRs, TEMP, PLUS). This suggested that a failure to perceive emotional faces in children with ASD. Furthermore, results of eye-tracking showed that the children with ASD less viewed the eye areas than the typically developing children. At the same time, the fixation time and fixation counts of face for children with ASD were significantly less than the intellectual disability group and the typically children group. The fixation time of fear faces for children with ASD was significantly less than the happy faces and sad faces. This suggested that the limited eye gaze for emotional faces in children with ASD. The results suggest that a failure to orient to emotional relevant stimuli(four basic emotional faces: happiness, sadness, fear and anger) may be caused by the lower fixation time to the eye areas, and avoidance of emotional stimulus may become the default coping mechanism for some individuals with autism. In conclusion, the current study demonstrates deficits in emotional empathy and limited eye gaze in children with ASD, which may be contributing to their problems in the face scanning patterns.

Single-Neuron Correlates of Atypical Face Processing in Autism

People with autism spectrum disorder (ASD) show abnormal processing of faces. A range of morphometric, histological, and neuroimaging studies suggest the hypothesis that this abnormality may be linked to the amygdala. We recorded data from single neurons within the amygdalae of two rare neurosurgical patients with ASD. While basic electrophysiological response parameters were normal, there were specific and striking abnormalities in how individual facial features drove neuronal response. Compared to control patients, a population of neurons in the two ASD patients responded significantly more to the mouth, but less to the eyes. Moreover, we found a second class of face-responsive neurons for which responses to faces appeared normal. The findings confirm the amygdala's pivotal role in abnormal face processing by people with ASD at the cellular level and suggest that dysfunction may be traced to a specific subpopulation of neurons with altered selectivity for the features of faces.

Effects of eye gaze directions of facial images on looking behaviour and autonomic responses in adolescents with autism spectrum disorders

It has been suggested that atypical eye contact of individuals with autism spectrum disorders (ASDs) arises from an unusually high level of autonomic activity elicited by another person's gaze. The present study investigated visual fixation duration and autonomic reactivity (heart rate, skin conductance response) simultaneously, while adolescents looked towards photographs of neutral faces, with either direct eye gaze, averted eye gaze or closed eyes. Both cognitively able adolescents with ASD (n=31, mean age=16 years, mean IQ=104) and typically developing (TD) adolescents (n=34, mean age=16 years, mean IQ=108) looked significantly longer towards the eye region of faces with direct eye gaze compared with faces with averted eye gaze or closed eyes. The adolescents with ASD did not show higher levels of autonomic activity than TD adolescents while they were instructed to look at the eye region. This suggests that looking at the eye region of static faces does not particularly trigger high autonomic arousal in adolescents with ASD.

Visual Scan Paths and Recognition of Facial Identity in Autism Spectrum Disorder and Typical Development

BackgroundPrevious research suggests that many individuals with autism spectrum disorder (ASD) have impaired facial identity recognition, and also exhibit abnormal visual scanning of faces. Here, two hypotheses accounting for an association between these observations were tested: i) better facial identity recognition is associated with increased gaze time on the Eye region; ii) better facial identity recognition is associated with increased eye-movements around the face.Methodology and Principal FindingsEye-movements of 11 children with ASD and 11 age-matched typically developing (TD) controls were recorded whilst they viewed a series of faces, and then completed a two alternative forced-choice recognition memory test for the faces. Scores on the memory task were standardized according to age. In both groups, there was no evidence of an association between the proportion of time spent looking at the Eye region of faces and age-standardized recognition performance, thus the first hypothesis was rejected. However, the ‘Dynamic Scanning Index’ – which was incremented each time the participant saccaded into and out of one of the core-feature interest areas – was strongly associated with age-standardized face recognition scores in both groups, even after controlling for various other potential predictors of performance.Conclusions and SignificanceIn support of the second hypothesis, results suggested that increased saccading between core-features was associated with more accurate face recognition ability, both in typical development and ASD. Causal directions of this relationship remain undetermined.

Single-Unit Responses Selective for Whole Faces in the Human Amygdala

The human amygdala is critical for social cognition from faces, as borne out by impairments in recognizing facial emotion following amygdala lesions [1] and differential activation of the amygdala by faces [2-5]. Single-unit recordings in the primate amygdala have documented responses selective for faces, their identity, or emotional expression [6, 7], yet how the amygdala represents face information remains unknown. Does it encode specific features of faces that are particularly critical for recognizing emotions (such as the eyes), or does it encode the whole face, a level of representation that might be the proximal substrate for subsequent social cognition? We investigated this question by recording from over 200 single neurons in the amygdalae of seven neurosurgical patients with implanted depth electrodes [8]. We found that approximately half of all neurons responded to faces or parts of faces. Approximately 20% of all neurons responded selectively only to the whole face. Although responding most to whole faces, these neurons paradoxically responded more when only a small part of the face was shown compared to when almost the entire face was shown. We suggest that the human amygdala plays a predominant role in representing global information about faces, possibly achieved through inhibition between individual facial features.

Mental state decoding abilities in young adults with borderline personality disorder traits.

Previous studies have demonstrated that patients with borderline personality disorder (BPD) tend to misattribute malevolence to benign social stimuli, including facial expressions. Yet, facial emotion recognition studies examining those with BPD have yielded mixed results, with some studies showing impaired accuracy and others demonstrating enhanced accuracy in the recognition of emotions or mental states. The current study examined the ability to decode mental states from photographs of just the eye region of faces in a nonclinical sample of young adults who exhibited BPD traits (high BPD) compared with those who did not (low BPD). Group differences in mental state decoding ability depended on the valence of the stimuli. The high-BPD group performed better for negative stimuli compared with the low-BPD group, but did not perform significantly different from the low-BPD group for stimuli of neutral or positive valence. The high-BPD group also demonstrated a response bias for attributing negative mental states to facial stimuli. In addition, findings suggested that the group difference in accuracy for negative stimuli could not be explained by response bias, because the group difference in response bias for negative stimuli did not reach significance. These findings suggest that BPD traits may be associated with enhanced ability to detect negative emotions and a bias for attributing negative emotions to nonnegative social stimuli.

Hemispheric specialization for the processing of horizontal and vertical manipulations of the eye region in faces

Hemispheric specialization for the processing of horizontal and vertical manipulations of the eye region in faces