Fearful Eyes Research Articles

Revisiting the Watching Eyes Effect: How Emotional Expressions, Sex, and Age of Watching Eyes Influence Stereotypical Statement Endorsement

Abstract The watching eyes effect has been shown to influence prosocial and antisocial behaviors. However, the eye characteristics which induce this effect remain unclear. This study explored how emotional expressions (anger, fear, happy, neutral), age (old, young), and sex (male, female) of eye images affect antisocial behavior, measured by stereotype endorsement. Participants rated their endorsement of 36 stereotype statements about race, gender, and religion topics, each paired with an eye image. Our findings indicated that stereotype endorsement did not differ significantly between neutral eye images and control flower images. We then used neutral eyes as control images to evaluate stereotype endorsement when being watched by eyes with other expressions. When comparing endorsement across age and sex in each expression, the data revealed higher endorsement for angry old male eyes and for happy young eyes (males and females), and lower endorsement for fearful eyes, except for old fearful female eyes. Therefore, varying the emotional expression, sex, and age of the eye images used in the watching eyes effect paradigm influences stereotype endorsement. To further unravel the underlying mechanisms behind the watching eyes effect, we encourage future research to explore how varying characteristics of the eyes affect responses/behaviors like stereotype endorsement.

Prioritized Identification of Fearful Eyes during the Attentional Blink Is Not Automatic.

The eye region conveys considerable information regarding an individual's emotions, motivations, and intentions during interpersonal communication. Evidence suggests that the eye regions of an individual expressing emotions can capture attention more rapidly than the eye regions of an individual in a neutral affective state. However, how attentional resources affect the processing of emotions conveyed by the eye regions remains unclear. Accordingly, the present study employed a dual-target rapid serial visual presentation task: happy, neutral, or fearful eye regions were presented as the second target, with a temporal lag between two targets of 232 or 696 ms. Participants completed two tasks successively: Task 1 was to identify which species the upright eye region they had seen belonged to, and Task 2 was to identify what emotion was conveyed in the upright eye region. The behavioral results showed that the accuracy for fearful eye regions was lower than that for neutral eye regions under the condition of limited attentional resources; however, accuracy differences across the three types of eye regions did not reach significance under the condition of adequate attentional resources. These findings indicate that preferential processing of fearful expressions is not automatic but is modulated by available attentional resources.

Perceptual load-independent modulation of the facilitated processing of emotional eye regions

Although the eye region has been found to convey sufficient information for emotional recognition and interpersonal communication, little is known regarding the extent to which the prioritized processing of emotional eye regions relies on available attentional resources. To address this issue, the present study used a dual-target rapid serial visual presentation task in which the perceptual load levels of the first target (T1), as well as the valence of the second target (T2), were manipulated. In addition to the traditional event-related potential (ERP) analysis method, the mass univariate statistics approach was employed. Behaviorally, both happy and fearful eye regions were recognized more accurately than neutral eye regions, regardless of the T1 perceptual load. ERP findings revealed an enhanced N170 amplitude for fearful eye regions compared to neutral eye regions, confirming the preferential and automatic processing of fearful signals at the early sensory stage. The late positive potential component exhibited enhanced responses to fearful and happy eye regions, suggesting the amplified representation consolidation in working memory. Collectively, these findings indicate that isolated eye regions are processed automatically to a higher degree owing to their perceptual and motivational significance.

Eye-size effects in the dot-probe task: Greater sclera exposure predicts delayed disengagement from fearful faces.

Fearful facial expressions are nonverbal and biologically salient signals of potential threat that automatically hold, capture, and direct observers' attention. They are characterized by enlarged eye whites and dilated pupils, and fearful eyes alone are sufficient to capture attention. The morphological properties of the eye region, such as sclera exposure, are thought to play an important role in nonverbal communication. Specifically, increased sclera exposure associated with fearful expressions has been shown to moderate how observers' shift their attention toward the direction of another's gaze. Yet, the extent to which variability in sclera exposure possibly impacts the capture and hold of attention by fearful faces is untested. To address this, a sample of 249 adults completed a dot-probe task of selective attention with fearful and neutral faces. The results suggested that (1) fearful faces were prioritized over neutral faces (i.e., they captured and held attention), (2) greater sclera exposure at target locations facilitated reaction times, and (3) attention was held by greater sclera exposure of fearful faces at task irrelevant locations resulting in delayed disengagement. Collectively, the results indicate that fearful facial expressions and sclera exposure modulate spatial attention through independent and interactive mechanisms. Sclera exposure appears to be an important facilitator of nonverbal communication and perhaps represents an understudied variable in social cognition more broadly.

Ghosts of Tao House

Ghosts of Tao House

Processing of emotions expressed through eye regions attenuates attentional blink

Despite of the crucial role of eye region in nonverbal communication, how and when the brain responds to affective signals projected from this region remains unclear. This study explored the temporal dynamics in the processing of emotionally valenced eye regions (happy, neutral, and fearful) and the influence of attentional resources using a dual-target rapid serial visual presentation task and event-related potential (ERP) technique. Behaviorally, the recognition accuracy of happy and fearful eye regions was higher than that for neutral eye regions in the deficient attentional resources condition (lag2), indicating reduced attentional blink for emotional eye regions. The ERP findings denote that fearful and happy eye regions modulated the N170. The early posterior negativity (EPN) was influenced by the interaction between lag and emotional valence, which was reflected by larger amplitudes for fearful rather than neutral eye regions in the lag2 condition. The amplitude of the late positive potential (LPP) also increased for the happy and fearful eye regions. These outcomes suggest that the human brain is highly sensitive to isolated eye regions. Moreover, fearful signals emitted from the eye region are processed automatically and are unaffected by attentional resource availability.

With Fearful Eyes: Exploring Relatives' Experiences With Out-of-Hospital Cardiac Arrest: A Qualitative Study.

Out-of-hospital cardiac arrest (OHCA) imposes significant consequences for a family, but little is known about relatives' experiences. Our aim was to explore relatives' experiences with the OHCA and the following months after. A qualitative approach using phenomenological-hermeneutic methodology was applied. Data consisted of semistructured interviews with 12 relatives of OHCA survivors. We analyzed data based on Paul Ricoeur's theory of interpretation. Relatives experienced OHCA as an abrupt and stressful event filled with imposing concerns for the cardiac arrest survivor. Relatives were fellow sufferers confronted with the possibility of bereavement, watching from the sideline with fearful eyes. After the OHCA, relatives experienced a troubled time with anxiety and edginess, monitoring the survivor for signs of a new cardiac arrest and trying to adapt to a new normality. Relatives' previous identities and positions within their families were disrupted. Relatives were challenged with the OHCA and the trajectory after it, experiencing a high level of distress and anxiety. Relatives took on an immense responsibility, always watching the survivor for potential symptoms of a new cardiac arrest. The cardiac arrest and the survivor's possible cognitive impairments gave rise to assuming a new authority as a relative. We advocate for a new family approach to relatives, acknowledging relatives' stress and central role in supporting cardiac arrest survivors.

What drives the attentional bias for fearful faces? An eye-tracking investigation of 7-month-old infants' visual scanning patterns.

Seven-month-old infants display a robust attentional bias for fearful faces; however, the mechanisms driving this bias remain unclear. The objective of the current study was to replicate the attentional bias for fearful faces and to investigate how infants' online scanning patterns relate to this preference. Infants' visual scanning patterns toward fearful and happy faces were captured using eye tracking in a paired-preference task, specifically exploring if the fear preference is driven by increased attention to particular facial features. Infants allocated increased attention toward the fearful face compared to the happy face overall, thus successfully replicating the attentional bias, and greater attention toward the fearful eyes was associated with a greater magnitude of the fear preference. The current findings suggest that the fearful eyes are a salient facial feature in capturing infants' attention toward the fearful face and that increased scanning of the fearful eyes may be one mechanism driving the overall fear preference. In addition, scanning patterns, and attention to critical features specifically, are highlighted as a strategy for examining the mechanisms underlying the development of emotion recognition abilities in infancy.

The effect of emotional information from eyes on empathy for pain: A subliminal ERP study.

Facial expressions are deeply tied to empathy, which plays an important role during social communication. The eye region is effective at conveying facial expressions, especially fear and sadness emotions. Further, it was proved that subliminal stimuli could impact human behavior. This research aimed to explore the effect of subliminal sad, fearful and neutral emotions conveyed by the eye region on a viewer's empathy for pain using event-related potentials (ERP). The experiment used an emotional priming paradigm of 3 (prime: subliminal neutral, sad, fear eye region information) × 2 (target: painful, nonpainful pictures) within-subject design. Participants were told to judge whether the targets were in pain or not. Results showed that the subliminal sad eye stimulus elicited a larger P2 amplitude than the subliminal fearful eye stimulus when assessing pain. For P3 and late positive component (LPC), the amplitude elicited by the painful pictures was larger than the amplitude elicited by the nonpainful pictures. The behavioral results demonstrated that people reacted to targets depicting pain more slowly after the sad emotion priming. Moreover, the subjective ratings of Personal Distress (PD) (one of the dimensions in Chinese version of Interpersonal Reactivity Index scale) predicted the pain effect in empathic neural responses in the N1 and N2 time window. The current study showed that subliminal eye emotion affected the viewer's empathy for pain. Compared with the subliminal fearful eye stimulus, the subliminal sad eye stimulus had a greater impact on empathy for pain. The perceptual level of pain was deeper in the late controlled processing stage.

The effect of emotionally valenced eye region images on visuocortical processing of surprised faces.

In this study, we presented pictorial representations of happy, neutral, and fearful expressions projected in the eye regions to determine whether the eye region alone is sufficient to produce a context effect. Participants were asked to judge the valence of surprised faces that had been preceded by a picture of an eye region. Behavioral results showed that affective ratings of surprised faces were context dependent. Prime-related ERPs with presentation of happy eyes elicited a larger P1 than those for neutral and fearful eyes, likely due to the recognition advantage provided by a happy expression. Target-related ERPs showed that surprised faces in the context of fearful and happy eyes elicited dramatically larger C1 than those in the neutral context, which reflected the modulation by predictions during the earliest stages of face processing. There were larger N170 with neutral and fearful eye contexts compared to the happy context, suggesting faces were being integrated with contextual threat information. The P3 component exhibited enhanced brain activity in response to faces preceded by happy and fearful eyes compared with neutral eyes, indicating motivated attention processing may be involved at this stage. Altogether, these results indicate for the first time that the influence of isolated eye regions on the perception of surprised faces involves preferential processing at the early stages and elaborate processing at the late stages. Moreover, higher cognitive processes such as predictions and attention can modulate face processing from the earliest stages in a top-down manner.

Boldness psychopathic traits predict reduced gaze toward fearful eyes in men with a history of violence

Research with developmental and adult samples has shown a relationship of psychopathic traits with reduced eye gaze. However, these relationships remained to be investigated among forensic samples. Here we examined the eye movements of male violent offenders during an emotion recognition task. Violent offenders performed similar to non-offending controls, and their eye movements varied with the emotion and intensity of the facial expression. In the violent offender group Boldness psychopathic traits, but not Meanness or Disinhibition, were associated with reduced dwell time and fixation counts, and slower first fixation latencies, on the eyes compared with the mouth. These results are the first to show a relationship of psychopathic traits with reduced attention to the eyes in a forensic sample, and suggest that Boldness is associated with difficulties in orienting attention toward emotionally salient aspects of the face.

Correction: The perceptual saliency of fearful eyes and smiles: A signal detection study.

[This corrects the article DOI: 10.1371/journal.pone.0173199.].

The perceptual saliency of fearful eyes and smiles: A signal detection study.

Facial features differ in the amount of expressive information they convey. Specifically, eyes are argued to be essential for fear recognition, while smiles are crucial for recognising happy expressions. In three experiments, we tested whether expression modulates the perceptual saliency of diagnostic facial features and whether the feature’s saliency depends on the face configuration. Participants were presented with masked facial features or noise at perceptual conscious threshold. The task was to indicate whether eyes (experiments 1-3A) or a mouth (experiment 3B) was present. The expression of the face and its configuration (i.e. spatial arrangement of the features) were manipulated. Experiment 1 compared fearful with neutral expressions, experiments 2 and 3 compared fearful versus happy expressions. The detection accuracy data was analysed using Signal Detection Theory (SDT), to examine the effects of expression and configuration on perceptual precision (d’) and response bias (c), separately. Across all three experiments, fearful eyes were detected better (higher d’) than neutral and happy eyes. Eyes were more precisely detected than mouths, whereas smiles were detected better than fearful mouths. The configuration of the features had no consistent effects across the experiments on the ability to detect expressive features. But facial configuration affected consistently the response bias. Participants used a more liberal criterion for detecting the eyes in canonical configuration and fearful expression. Finally, the power in low spatial frequency of a feature predicted its discriminability index. The results suggest that expressive features are perceptually more salient with a higher d’ due to changes at the low-level visual properties, with emotions and configuration affecting perception through top-down processes, as reflected by the response bias.

Interpersonal Threat Sensitivity in Borderline Personality Disorder: An Eye-Tracking Study.

Threat sensitivity is a prominent predictor of interpersonal dysfunctions in borderline personality disorder (BPD), leading to intense, aversive feelings of threat and eventually dysfunctional behaviors, such as aggression. In the present study, BPD patients and healthy volunteers classified angry, fearful, neutral, and happy faces presented for 150 ms or 5,000 ms to investigate initial saccades and facial scanning. Patients more often wrongly identified anger, responded slower to all faces, and made faster saccades towards the eyes of briefly presented neutral faces and slower saccades away from fearful eyes compared with healthy volunteers. Latency of initial saccades and fixation duration correlated negatively with the patients' aggressiveness. Supporting previous results, BPD patients did not experience general deficits in facial emotion processing, but a specific hypersensitivity for and deficits in detailed evaluation of threat cues, which was particularly enhanced in aggressive patients. Interventions might benefit from relocating attention towards positive information and detailed evaluation of social cues.

Identification of Emotional Facial Expressions: Effects of Expression, Intensity, and Sex on Eye Gaze.

The identification of emotional expressions is vital for social interaction, and can be affected by various factors, including the expressed emotion, the intensity of the expression, the sex of the face, and the gender of the observer. This study investigates how these factors affect the speed and accuracy of expression recognition, as well as dwell time on the two most significant areas of the face: the eyes and the mouth. Participants were asked to identify expressions from female and male faces displaying six expressions (anger, disgust, fear, happiness, sadness, and surprise), each with three levels of intensity (low, moderate, and normal). Overall, responses were fastest and most accurate for happy expressions, but slowest and least accurate for fearful expressions. More intense expressions were also classified most accurately. Reaction time showed a different pattern, with slowest response times recorded for expressions of moderate intensity. Overall, responses were slowest, but also most accurate, for female faces. Relative to male observers, women showed greater accuracy and speed when recognizing female expressions. Dwell time analyses revealed that attention to the eyes was about three times greater than on the mouth, with fearful eyes in particular attracting longer dwell times. The mouth region was attended to the most for fearful, angry, and disgusted expressions and least for surprise. These results extend upon previous findings to show important effects of expression, emotion intensity, and sex on expression recognition and gaze behaviour, and may have implications for understanding the ways in which emotion recognition abilities break down.

A face versus non-face context influences amygdala responses to masked fearful eye whites.

The structure of the mask stimulus is crucial in backward masking studies and we recently demonstrated such an effect when masking faces. Specifically, we showed that activity of the amygdala is increased to fearful facial expressions masked with neutral faces and decreased to fearful expressions masked with a pattern mask—but critically both masked conditions discriminated fearful expressions from happy expressions. Given this finding, we sought to test whether masked fearful eye whites would produce a similar profile of amygdala response in a face vs non-face context. During functional magnetic resonance imaging scanning sessions, 30 participants viewed fearful or happy eye whites masked with either neutral faces or pattern images. Results indicated amygdala activity was increased to fearful vs happy eye whites in the face mask condition, but decreased to fearful vs happy eye whites in the pattern mask condition—effectively replicating and expanding our previous report. Our data support the idea that the amygdala is responsive to fearful eye whites, but that the nature of this activity observed in a backward masking design depends on the mask stimulus.

Empathy in youths: Change in patterns of eye gaze and brain activity with the manipulation of visual attention to emotional faces

Background & aim: Understanding the emotional state of others is fundamental to effective social interaction and the development of empathy. Critical information is conveyed via the eyes, and reduced attention to the eyes is associated with poorer emotion recognition and empathic deficits in individuals with disorders affecting social cognition such as autism or some types of conduct problems. Deliberately redirecting attention to the eyes may be a way of improving behaviour. However, the effects of directing attention on brain activity during emotional processing has not been studied previously. Our aim was to determine whether manipulation of visual attention in youths affects their eye gaze patterns and brain responses to expression of emotions in others. Method: Eighteen typically developing male youths aged 8-16 performed an implicit facial emotion processing task while viewing different facial expressions (fearful, neutral, happy), presented in three separate blocks under three different instructions: undirected, eye-gaze and mouth-gaze. Eye tracking (dwell time) and functional-MRI data were acquired concurrently as measures of visual attention and brain response, respectively. Results: Eye tracking indicated that the youths attended more to the eyes than the mouth in the undirected condition. Redirecting attention to the eyes and mouth significantly increased attention to these areas. Compared to undirected, directing attention to the fearful eyes also produced a greater increase in attention than neutral eyes. Attention directed to eyes elicited greater brain activity in frontal regions than undirected attention. Discussion & conclusions: The undirected eye gaze patterns indicate natural orienting to eyes in healthy youths, which can be effectively altered with instruction. Directing attention to fearful eyes engaged attention relatively longer than neutral, consistent with the threat value of fearful faces. These data also demonstrate that manipulation of visual attention modulates activity in frontal regions, perhaps reflecting greater engagement of executive function due to attentional demands. Understanding attentional manipulation effects in a healthy sample will inform ongoing work addressing potentially perturbed response patterns in a conduct problem cohort.

Beware the eyes behind the mask: The capture and hold of selective attention by backward masked fearful eyes

Fearful facial expressions are important social indicators of environmental threat. Among the various features of a fearful face, the eyes appear to be particularly important for recognizing and responding to these social cues. One way in which fearful faces facilitate observers’ behavior is by automatically capturing attention. This is true for both consciously and nonconsciously processed fearful faces. Recent research suggests that consciously processed fearful eyes alone are sufficient to capture observers’ attention. However, it is unknown as to whether or not nonconsciously processed, backward masked, fearful eyes are sufficient to facilitate spatial attention. To test this possibility, two dot-probe experiments with masked fearful eye stimuli were performed. In Experiment 1, we found that, relative to scrambled eyes, masked fearful eyes facilitate attentional orienting and delay attentional disengagement. In Experiment 2, we replicated this effect when comparing backward masked fearful to neutral eyes. Thus, the data suggest that nonconscious fearful eyes facilitate spatial attention through facilitated orienting and delayed disengagement.

The developmental emergence of unconscious fear processing from eyes during infancy

From early in life, emotion detection plays an important role during social interactions. Recently, 7-month-old infants have been shown to process facial signs of fear in others without conscious perception and solely on the basis of their eyes. However, it is not known whether unconscious fear processing from eyes is present before 7months of age or only emerges at around 7months. To investigate this question, we measured 5-month-old infants’ event-related potentials (ERPs) in response to subliminally presented fearful and non-fearful eyes and compared these with 7-month-old infants’ ERP responses from a previous study. Our ERP results revealed that only 7-month-olds, but not 5-month-olds, distinguished between fearful and non-fearful eyes. Specifically, 7-month-olds’ processing of fearful eyes was reflected in early visual processes over occipital cortex and later attentional processes over frontal cortex. This suggests that, in line with prior work on the conscious detection of fearful faces, the brain processes associated with the unconscious processing of fearful eyes develop between 5 and 7months of age. More generally, these findings support the notion that emotion perception and the underlying brain processes undergo critical change during the first year of life. Therefore, the current data provide further evidence for viewing infancy as a formative period in human socioemotional functioning.

Genetic variation in CD38 and breastfeeding experience interact to impact infants’ attention to social eye cues

Attending to emotional information conveyed by the eyes is an important social skill in humans. The current study examined this skill in early development by measuring attention to eyes while viewing emotional faces in 7-mo-old infants. In particular, we investigated individual differences in infant attention to eyes in the context of genetic variation (CD38 rs3796863 polymorphism) and experiential variation (exclusive breastfeeding duration) related to the oxytocin system. Our results revealed that, whereas infants at this age show a robust fear bias (increased attention to fearful eyes), their attention to angry and happy eyes varies as a function of exclusive breastfeeding experience and genetic variation in CD38. Specifically, extended exclusive breastfeeding duration selectively enhanced looking preference to happy eyes and decreased looking to angry eyes. Importantly, however, this interaction was impacted by CD38 variation, such that only the looking preferences of infants homozygous for the C allele of rs3796863 were affected by breastfeeding experience. This genotype has been associated with reduced release of oxytocin and higher rates of autism. In contrast, infants with the CA/AA genotype showed similar looking preferences regardless of breastfeeding exposure. Thus, differences in the sensitivity to emotional eyes may be linked to an interaction between the endogenous (CD38) and exogenous (breastfeeding) availability of oxytocin. These findings underline the importance of maternal care and the oxytocin system in contributing to the early development of responding to social eye cues.