Evidence for adaptive design in human gaze preference

Many studies have investigated the physical cues that influence face preferences. By contrast, relatively few studies have investigated the effects of facial cues to the direction and valence of others' social interest (i.e. gaze direction and facial expressions) on face preferences. Here we found that participants demonstrated stronger preferences for direct gaze when judging the attractiveness of happy faces than that of disgusted faces, and that this effect of expression on the strength of attraction to direct gaze was particularly pronounced for judgements of opposite-sex faces (study 1). By contrast, no such opposite-sex bias in preferences for direct gaze was observed when participants judged the same faces for likeability (study 2). Collectively, these findings for a context-sensitive opposite-sex bias in preferences for perceiver-directed smiles, but not perceiver-directed disgust, suggest gaze preference functions, at least in part, to facilitate efficient allocation of mating effort, and evince adaptive design in the perceptual mechanisms that underpin face preferences.     

Prolonged visual experience in adulthood modulates holistic face perception

Background

Using the well-known composite illusion as a marker of the holistic perception of faces, we tested how prolonged visual experience with a specific population of faces (4- to 6-year-old children) modulates the face perception system in adulthood.

Methodology/Principal Findings

We report a face composite effect that is larger for adult than children faces in a group of adults without experience with children faces (“children-face novices”), while it is of equal magnitude for adults and children faces in a population of preschool teachers (“children-face experts”). When considering preschool teachers only, we observed a significant correlation between the number of years of experience with children faces and the differential face composite effect between children and adults faces. Participants with at least 10 years of qualitative experience with children faces had a larger composite face effect for children than adult faces.

Conclusions/Significance

Overall, these observations indicate that even in adulthood face processes can be reshaped qualitatively, presumably to facilitate efficient processing of the differential morphological features of the frequently encountered population of faces.     

Facial Trustworthiness Judgments in Children with ASD Are Modulated by Happy and Angry Emotional Cues

Appearance-based trustworthiness inferences may reflect the misinterpretation of emotional expression cues. Children and adults typically perceive faces that look happy to be relatively trustworthy and those that look angry to be relatively untrustworthy. Given reports of atypical expression perception in children with Autism Spectrum Disorder (ASD), the current study aimed to determine whether the modulation of trustworthiness judgments by emotional expression cues in children with ASD is also atypical. Cognitively-able children with and without ASD, aged 6–12 years, rated the trustworthiness of faces showing happy, angry and neutral expressions. Trust judgments in children with ASD were significantly modulated by overt happy and angry expressions, like those of typically-developing children. Furthermore, subtle emotion cues in neutral faces also influenced trust ratings of the children in both groups. These findings support a powerful influence of emotion cues on perceived trustworthiness, which even extends to children with social cognitive impairments.     

Perception of Social Cues of Danger in Autism Spectrum Disorders

Intuitive grasping of the meaning of subtle social cues is particularly affected in autism spectrum disorders (ASD). Despite their relevance in social communication, the effect of averted gaze in fearful faces in conveying a signal of environmental threat has not been investigated using real face stimuli in adults with ASD. Here, using functional MRI, we show that briefly presented fearful faces with averted gaze, previously shown to be a strong communicative signal of environmental danger, produce different patterns of brain activation than fearful faces with direct gaze in a group of 26 normally intelligent adults with ASD compared with 26 matched controls. While implicit cue of threat produces brain activation in attention, emotion processing and mental state attribution networks in controls, this effect is absent in individuals with ASD. Instead, individuals with ASD show activation in the subcortical face-processing system in response to direct eye contact. An effect of differences in looking behavior was excluded in a separate eye tracking experiment. Our data suggest that individuals with ASD are more sensitive to direct eye contact than to social signals of danger conveyed by averted fearful gaze.     

Dogs Evaluate Threatening Facial Expressions by Their Biological Validity – Evidence from Gazing Patterns

Appropriate response to companions’ emotional signals is important for all social creatures. The emotional expressions of humans and non-human animals have analogies in their form and function, suggesting shared evolutionary roots, but very little is known about how animals other than primates view and process facial expressions. In primates, threat-related facial expressions evoke exceptional viewing patterns compared with neutral or positive stimuli. Here, we explore if domestic dogs (Canis familiaris) have such an attentional bias toward threatening social stimuli and whether observed emotional expressions affect dogs’ gaze fixation distribution among the facial features (eyes, midface and mouth). We recorded the voluntary eye gaze of 31 domestic dogs during viewing of facial photographs of humans and dogs with three emotional expressions (threatening, pleasant and neutral). We found that dogs’ gaze fixations spread systematically among facial features. The distribution of fixations was altered by the seen expression, but eyes were the most probable targets of the first fixations and gathered longer looking durations than mouth regardless of the viewed expression. The examination of the inner facial features as a whole revealed more pronounced scanning differences among expressions. This suggests that dogs do not base their perception of facial expressions on the viewing of single structures, but the interpretation of the composition formed by eyes, midface and mouth. Dogs evaluated social threat rapidly and this evaluation led to attentional bias, which was dependent on the depicted species: threatening conspecifics’ faces evoked heightened attention but threatening human faces instead an avoidance response. We propose that threatening signals carrying differential biological validity are processed via distinctive neurocognitive pathways. Both of these mechanisms may have an adaptive significance for domestic dogs. The findings provide a novel perspective on understanding the processing of emotional expressions and sensitivity to social threat in non-primates.     

Shyness in Early Infancy: Approach-Avoidance Conflicts in Temperament and Hypersensitivity to Eyes during Initial Gazes to Faces

‘Infant shyness’, in which infants react shyly to adult strangers, presents during the third quarter of the first year. Researchers claim that shy children over the age of three years are experiencing approach-avoidance conflicts. Counter-intuitively, shy children do not avoid the eyes when scanning faces; rather, they spend more time looking at the eye region than non-shy children do. It is currently unknown whether young infants show this conflicted shyness and its corresponding characteristic pattern of face scanning. Here, using infant behavioral questionnaires and an eye-tracking system, we found that highly shy infants had high scores for both approach and fear temperaments (i.e., approach-avoidance conflict) and that they showed longer dwell times in the eye regions than less shy infants during their initial fixations to facial stimuli. This initial hypersensitivity to the eyes was independent of whether the viewed faces were of their mothers or strangers. Moreover, highly shy infants preferred strangers with an averted gaze and face to strangers with a directed gaze and face. This initial scanning of the eye region and the overall preference for averted gaze faces were not explained solely by the infants’ age or temperament (i.e., approach or fear). We suggest that infant shyness involves a conflict in temperament between the desire to approach and the fear of strangers, and this conflict is the psychological mechanism underlying infants’ characteristic behavior in face scanning.     

Holistic gaze strategy to categorize facial expression of varying intensities

Using faces representing exaggerated emotional expressions, recent behaviour and eye-tracking studies have suggested a dominant role of individual facial features in transmitting diagnostic cues for decoding facial expressions. Considering that in everyday life we frequently view low-intensity expressive faces in which local facial cues are more ambiguous, we probably need to combine expressive cues from more than one facial feature to reliably decode naturalistic facial affects. In this study we applied a morphing technique to systematically vary intensities of six basic facial expressions of emotion, and employed a self-paced expression categorization task to measure participants' categorization performance and associated gaze patterns. The analysis of pooled data from all expressions showed that increasing expression intensity would improve categorization accuracy, shorten reaction time and reduce number of fixations directed at faces. The proportion of fixations and viewing time directed at internal facial features (eyes, nose and mouth region), however, was not affected by varying levels of intensity. Further comparison between individual facial expressions revealed that although proportional gaze allocation at individual facial features was quantitatively modulated by the viewed expressions, the overall gaze distribution in face viewing was qualitatively similar across different facial expressions and different intensities. It seems that we adopt a holistic viewing strategy to extract expressive cues from all internal facial features in processing of naturalistic facial expressions.     

Watch Out! Magnetoencephalographic Evidence for Early Modulation of Attention Orienting by Fearful Gaze Cueing

Others’ gaze and emotional facial expression are important cues for the process of attention orienting. Here, we investigated with magnetoencephalography (MEG) whether the combination of averted gaze and fearful expression may elicit a selectively early effect of attention orienting on the brain responses to targets. We used the direction of gaze of centrally presented fearful and happy faces as the spatial attention orienting cue in a Posner-like paradigm where the subjects had to detect a target checkerboard presented at gazed-at (valid trials) or non gazed-at (invalid trials) locations of the screen. We showed that the combination of averted gaze and fearful expression resulted in a very early attention orienting effect in the form of additional parietal activity between 55 and 70 ms for the valid versus invalid targets following fearful gaze cues. No such effect was obtained for the targets following happy gaze cues. This early cue-target validity effect selective of fearful gaze cues involved the left superior parietal region and the left lateral middle occipital region. These findings provide the first evidence for an effect of attention orienting induced by fearful gaze in the time range of C1. In doing so, they demonstrate the selective impact of combined gaze and fearful expression cues in the process of attention orienting.     

Visual Search for Human Gaze Direction by a Chimpanzee (Pan troglodytes)

Background

Humans detect faces with direct gazes among those with averted gazes more efficiently than they detect faces with averted gazes among those with direct gazes. We examined whether this “stare-in-the-crowd” effect occurs in chimpanzees (Pan troglodytes), whose eye morphology differs from that of humans (i.e., low-contrast eyes, dark sclera).

Methodology/Principal Findings

An adult female chimpanzee was trained to search for an odd-item target (front view of a human face) among distractors that differed from the target only with respect to the direction of the eye gaze. During visual-search testing, she performed more efficiently when the target was a direct-gaze face than when it was an averted-gaze face. This direct-gaze superiority was maintained when the faces were inverted and when parts of the face were scrambled. Subsequent tests revealed that gaze perception in the chimpanzee was controlled by the contrast between iris and sclera, as in humans, but that the chimpanzee attended only to the position of the iris in the eye, irrespective of head direction.

Conclusion/Significance

These results suggest that the chimpanzee can discriminate among human gaze directions and are more sensitive to direct gazes. However, limitations in the perception of human gaze by the chimpanzee are suggested by her inability to completely transfer her performance to faces showing a three-quarter view.     

The Composite Task Reveals Stronger Holistic Processing in Children than Adults for Child Faces

Background

While own-age faces have been reported to be better recognized than other-age faces, the underlying cause of this phenomenon remains unclear. One potential cause is holistic face processing, a special kind of perceptual and cognitive processing reserved for perceiving upright faces. Previous studies have indeed found that adults show stronger holistic processing when looking at adult faces compared to child faces, but whether a similar own-age bias exists in children remains to be shown.

Methodology/Principal Findings

Here we used the composite face task – a standard test of holistic face processing – to investigate if, for child faces, holistic processing is stronger for children than adults. Results showed child participants (8–13 years) had a larger composite effect than adult participants (22–65 years).

Conclusions/Significance

Our finding suggests that differences in strength of holistic processing may underlie the own-age bias on recognition memory. We discuss the origin of own-age biases in terms of relative experience, face-space tuning, and social categorization.     

Cultural Modulation of Face and Gaze Scanning in Young Children

Previous research has demonstrated that the way human adults look at others’ faces is modulated by their cultural background, but very little is known about how such a culture-specific pattern of face gaze develops. The current study investigated the role of cultural background on the development of face scanning in young children between the ages of 1 and 7 years, and its modulation by the eye gaze direction of the face. British and Japanese participants’ eye movements were recorded while they observed faces moving their eyes towards or away from the participants. British children fixated more on the mouth whereas Japanese children fixated more on the eyes, replicating the results with adult participants. No cultural differences were observed in the differential responses to direct and averted gaze. The results suggest that different patterns of face scanning exist between different cultures from the first years of life, but differential scanning of direct and averted gaze associated with different cultural norms develop later in life.     

Facial Expression Training Optimises Viewing Strategy in Children and Adults

This study investigated whether training-related improvements in facial expression categorization are facilitated by spontaneous changes in gaze behaviour in adults and nine-year old children. Four sessions of a self-paced, free-viewing training task required participants to categorize happy, sad and fear expressions with varying intensities. No instructions about eye movements were given. Eye-movements were recorded in the first and fourth training session. New faces were introduced in session four to establish transfer-effects of learning. Adults focused most on the eyes in all sessions and increased expression categorization accuracy after training coincided with a strengthening of this eye-bias in gaze allocation. In children, training-related behavioural improvements coincided with an overall shift in gaze-focus towards the eyes (resulting in more adult-like gaze-distributions) and towards the mouth for happy faces in the second fixation. Gaze-distributions were not influenced by the expression intensity or by the introduction of new faces. It was proposed that training enhanced the use of a uniform, predominantly eyes-biased, gaze strategy in children in order to optimise extraction of relevant cues for discrimination between subtle facial expressions.     

Influence of Ethnic Group-Membership and Gaze Direction on the Perception of Emotions. A Cross-Cultural Study between Germany and China

Emotional facial expressions provide important nonverbal cues in human interactions. The perception of emotions is not only influenced by a person’s ethnic background but also depends on whether a person is engaged with the emotion-encoder. Although these factors are known to affect emotion perception, their impact has only been studied in isolation before. The aim of the present study was to investigate their combined influence. Thus, in order to study the influence of engagement on emotion perception between persons from different ethnicities, we compared participants from China and Germany. Asian-looking and European-looking virtual agents expressed anger and happiness while gazing at the participant or at another person. Participants had to assess the perceived valence of the emotional expressions. Results indicate that indeed two factors that are known to have a considerable influence on emotion perception interacted in their combined influence: We found that the perceived intensity of an emotion expressed by ethnic in-group members was in most cases independent of gaze direction, whereas gaze direction had an influence on the emotion perception of ethnic out-group members. Additionally, participants from the ethnic out-group tended to perceive emotions as more pronounced than participants from the ethnic in-group when they were directly gazed at. These findings suggest that gaze direction has a differential influence on ethnic in-group and ethnic out-group dynamics during emotion perception.     

Reading faces: differential lateral gaze bias in processing canine and human facial expressions in dogs and 4-year-old children

Sensitivity to the emotions of others provides clear biological advantages. However, in the case of heterospecific relationships, such as that existing between dogs and humans, there are additional challenges since some elements of the expression of emotions are species-specific. Given that faces provide important visual cues for communicating emotional state in both humans and dogs, and that processing of emotions is subject to brain lateralisation, we investigated lateral gaze bias in adult dogs when presented with pictures of expressive human and dog faces. Our analysis revealed clear differences in laterality of eye movements in dogs towards conspecific faces according to the emotional valence of the expressions. Differences were also found towards human faces, but to a lesser extent. For comparative purpose, a similar experiment was also run with 4-year-old children and it was observed that they showed differential processing of facial expressions compared to dogs, suggesting a species-dependent engagement of the right or left hemisphere in processing emotions.     

Tuning to the Positive: Age-Related Differences in Subjective Perception of Facial Emotion

Facial expressions aid social transactions and serve as socialization tools, with smiles signaling approval and reward, and angry faces signaling disapproval and punishment. The present study examined whether the subjective experience of positive vs. negative facial expressions differs between children and adults. Specifically, we examined age-related differences in biases toward happy and angry facial expressions. Young children (5–7 years) and young adults (18–29 years) rated the intensity of happy and angry expressions as well as levels of experienced arousal. Results showed that young children—but not young adults—rated happy facial expressions as both more intense and arousing than angry faces. This finding, which we replicated in two independent samples, was not due to differences in the ability to identify facial expressions, and suggests that children are more tuned to information in positive expressions. Together these studies provide evidence that children see unambiguous adult emotional expressions through rose-colored glasses, and suggest that what is emotionally relevant can shift with development.     

Atypicalities in Perceptual Adaptation in Autism Do Not Extend to Perceptual Causality

A recent study showed that adaptation to causal events (collisions) in adults caused subsequent events to be less likely perceived as causal. In this study, we examined if a similar negative adaptation effect for perceptual causality occurs in children, both typically developing and with autism. Previous studies have reported diminished adaptation for face identity, facial configuration and gaze direction in children with autism. To test whether diminished adaptive coding extends beyond high-level social stimuli (such as faces) and could be a general property of autistic perception, we developed a child-friendly paradigm for adaptation of perceptual causality. We compared the performance of 22 children with autism with 22 typically developing children, individually matched on age and ability (IQ scores). We found significant and equally robust adaptation aftereffects for perceptual causality in both groups. There were also no differences between the two groups in their attention, as revealed by reaction times and accuracy in a change-detection task. These findings suggest that adaptation to perceptual causality in autism is largely similar to typical development and, further, that diminished adaptive coding might not be a general characteristic of autism at low levels of the perceptual hierarchy, constraining existing theories of adaptation in autism.     

Seeing emotion with your ears: emotional prosody implicitly guides visual attention to faces

Interpersonal communication involves the processing of multimodal emotional cues, particularly facial expressions (visual modality) and emotional speech prosody (auditory modality) which can interact during information processing. Here, we investigated whether the implicit processing of emotional prosody systematically influences gaze behavior to facial expressions of emotion. We analyzed the eye movements of 31 participants as they scanned a visual array of four emotional faces portraying fear, anger, happiness, and neutrality, while listening to an emotionally-inflected pseudo-utterance (Someone migged the pazing) uttered in a congruent or incongruent tone. Participants heard the emotional utterance during the first 1250 milliseconds of a five-second visual array and then performed an immediate recall decision about the face they had just seen. The frequency and duration of first saccades and of total looks in three temporal windows ([0-1250 ms], [1250-2500 ms], [2500-5000 ms]) were analyzed according to the emotional content of faces and voices. Results showed that participants looked longer and more frequently at faces that matched the prosody in all three time windows (emotion congruency effect), although this effect was often emotion-specific (with greatest effects for fear). Effects of prosody on visual attention to faces persisted over time and could be detected long after the auditory information was no longer present. These data imply that emotional prosody is processed automatically during communication and that these cues play a critical role in how humans respond to related visual cues in the environment, such as facial expressions.     

Young infants' neural processing of objects is affected by eye gaze direction and emotional expression

Eye gaze is an important social cue which is used to determine another person's focus of attention and intention to communicate. In combination with a fearful facial expression eye gaze can also signal threat in the environment. The ability to detect and understand others' social signals is essential in order to avoid danger and enable social evaluation. It has been a matter of debate when infants are able to use gaze cues and emotional facial expressions in reference to external objects. Here we demonstrate that by 3 months of age the infant brain differentially responds to objects as a function of how other people are reacting to them. Using event-related electrical brain potentials (ERPs), we show that an indicator of infants' attention is enhanced by an adult's expression of fear toward an unfamiliar object. The infant brain showed an increased Negative central (Nc) component toward objects that had been previously cued by an adult's eye gaze and frightened facial expression. Our results further suggest that infants' sensitivity cannot be due to a general arousal elicited by a frightened face with eye gaze directed at an object. The neural attention system of 3 month old infants is sensitive to an adult's eye gaze direction in combination with a fearful expression. This early capacity may lay the foundation for the development of more sophisticated social skills such as social referencing, language, and theory of mind.     

Atypical gaze patterns in children and adults with autism spectrum disorders dissociated from developmental changes in gaze behaviour

Eye tracking has been used to investigate gaze behaviours in individuals with autism spectrum disorder (ASD). However, traditional analysis has yet to find behavioural characteristics shared by both children and adults with ASD. To distinguish core ASD gaze behaviours from those that change with development, we examined temporo-spatial gaze patterns in children and adults with and without ASD while they viewed video clips. We summarized the gaze patterns of 104 participants using multidimensional scaling so that participants with similar gaze patterns would cluster together in a two-dimensional plane. Control participants clustered in the centre, reflecting a standard gaze behaviour, whereas participants with ASD were distributed around the periphery. Moreover, children and adults were separated on the plane, thereby showing a clear effect of development on gaze behaviours. Post hoc frame-by-frame analyses revealed the following findings: (i) both ASD groups shifted their gaze away from a speaker earlier than the control groups; (ii) both ASD groups showed a particular preference for letters; and (iii) typical infants preferred to watch the mouth rather than the eyes during speech, a preference that reversed with development. These results highlight the importance of taking the effect of development into account when addressing gaze behaviours characteristic of ASD.     

情绪面孔对听觉通道短时距内隐知觉的影响

时间知觉是人类的一项基本能力.日常生活经验表明时间知觉容易受到情绪的影响.但是在前人的研究中,这些影响往往伴随着主动注意和外显的运动反应.这里关注的是不伴随主动注意和外显运动反应的内隐时间知觉是否受到情绪面孔的影响.被试在主动完成一个由情绪面孔组成的视觉辨别任务的同时,被动地听一系列声音刺激.声音刺激的刺激启动异步时间(stimulus onset asynchrony,SOA)中,80%是标准SOA(800ms),20%是偏差SOA(400,600 ms).对频繁出现的标准SOA和偶尔出现的偏差SOA诱发的事件相关电位(event-related potential,ERP)进行记录.2个短的偏差SOA(400和600ms)引发了2个变化相关的ERP成分:失匹配负波(the mismatch negativity,MMN)和P3a.代表对无规律变化早期检测的MMN波幅受到了情绪面孔的影响.与愉快和中性面孔相比,恐惧面孔降低了MMN波幅.对于400ms偏差SOA,与恐惧面孔和中性面孔相比,愉快面孔增加了P3a波幅.该ERP研究提示听觉通道的内隐时间知觉受到情绪面孔的影响,恐惧面孔降低了内隐时间知觉的准确性.