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1.  Neural bases of gaze and emotion processing in children with autism spectrum disorders 
Brain and Behavior  2011;1(1):1-11.
Abnormal eye contact is a core symptom of autism spectrum disorders (ASD), though little is understood of the neural bases of gaze processing in ASD. Competing hypotheses suggest that individuals with ASD avoid eye contact due to the anxiety-provoking nature of direct eye gaze or that eye-gaze cues hold less interest or significance to children with ASD. The current study examined the effects of gaze direction on neural processing of emotional faces in typically developing (TD) children and those with ASD. While undergoing functional magnetic resonance imaging (fMRI), 16 high-functioning children and adolescents with ASD and 16 TD controls viewed a series of faces depicting emotional expressions with either direct or averted gaze. Children in both groups showed significant activity in visual-processing regions for both direct and averted gaze trials. However, there was a significant group by gaze interaction such that only TD children showed reliably greater activity in ventrolateral prefrontal cortex for direct versus averted gaze. The ASD group showed no difference between direct and averted gaze in response to faces conveying negative emotions. These results highlight the key role of eye gaze in signaling communicative intent and suggest altered processing of the emotional significance of direct gaze in children with ASD.
PMCID: PMC3217668  PMID: 22398976
Autism; facial expression; functional magnetic resonance imaging; gaze; developmental neuroimaging
2.  Perception of Social Cues of Danger in Autism Spectrum Disorders 
PLoS ONE  2013;8(12):e81206.
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.
PMCID: PMC3852523  PMID: 24324679
3.  Variation in the human cannabinoid receptor CNR1 gene modulates gaze duration for happy faces 
Molecular Autism  2011;2:10.
From an early age, humans look longer at preferred stimuli and also typically look longer at facial expressions of emotion, particularly happy faces. Atypical gaze patterns towards social stimuli are common in autism spectrum conditions (ASC). However, it is unknown whether gaze fixation patterns have any genetic basis. In this study, we tested whether variations in the cannabinoid receptor 1 (CNR1) gene are associated with gaze duration towards happy faces. This gene was selected because CNR1 is a key component of the endocannabinoid system, which is involved in processing reward, and in our previous functional magnetic resonance imaging (fMRI) study, we found that variations in CNR1 modulate the striatal response to happy (but not disgust) faces. The striatum is involved in guiding gaze to rewarding aspects of a visual scene. We aimed to validate and extend this result in another sample using a different technique (gaze tracking).
A total of 30 volunteers (13 males and 17 females) from the general population observed dynamic emotional expressions on a screen while their eye movements were recorded. They were genotyped for the identical four single-nucleotide polymorphisms (SNPs) in the CNR1 gene tested in our earlier fMRI study.
Two SNPs (rs806377 and rs806380) were associated with differential gaze duration for happy (but not disgust) faces. Importantly, the allelic groups associated with a greater striatal response to happy faces in the fMRI study were associated with longer gaze duration at happy faces.
These results suggest that CNR1 variations modulate the striatal function that underlies the perception of signals of social reward, such as happy faces. This suggests that CNR1 is a key element in the molecular architecture of perception of certain basic emotions. This may have implications for understanding neurodevelopmental conditions marked by atypical eye contact and facial emotion processing, such as ASC.
PMCID: PMC3155489  PMID: 21714860
4.  Eye contact influences neural processing of emotional expressions in 4-month-old infants 
Eye gaze is a fundamental component of human communication. During the first post-natal year, infants rapidly learn that the gaze of others provides socially significant information. In addition, infants are sensitive to several emotional expressions. However, little is known regarding how eye contact influences the way the infant brain processes emotional expressions. We measured 4-month-old infants’ brain electric activity to assess neural processing of faces displaying neutral, happy and angry emotional expressions when accompanied by direct and averted eye gaze. The results show that processing of angry facial expressions was influenced by eye gaze. In particular, infants showed enhanced neural processing of angry expressions when these expressions were accompanied by direct eye gaze. These results show that by 4 months of age, the infant detects angry emotional expressions, and the infant brain processes their relevance to the self.
PMCID: PMC2555439  PMID: 18985122
infants; EEG; eye gaze; social cognition; ERP
5.  Atypical Functional Connectivity of the Amygdala in Childhood Autism Spectrum Disorders during Spontaneous Attention to Eye-Gaze 
Autism Research and Treatment  2012;2012:652408.
We examined functional connectivity of the amygdala in preadolescent children with Autism Spectrum Disorders (ASDs) during spontaneous attention to eye-gaze in emotional faces. Children responded to a target word (“LEFT/RIGHT”) printed on angry or fearful faces looking in a direction that was congruent, incongruent, or neutral with the target word. Despite being irrelevant to the task, gaze-direction facilitated (Congruent > Neutral) or interfered with (Incongruent > Congruent) performance in both groups. Despite similar behavioral performance, amygdala-connectivity was atypical and more widespread in children with ASD. In control children, the amygdala was more strongly connected with an emotional cognitive control region (subgenual cingulate) during interference, while during facilitation, no regions showed greater amygdala connectivity than in ASD children. In contrast, in children with ASD the amygdala was more strongly connected to salience and cognitive control regions (posterior and dorsal cingulate) during facilitation and with regions involved in gaze processing (superior temporal sulcus), cognitive control (inferior frontal gyrus), and processing of viscerally salient information (pregenual cingulate, anterior insula, and thalamus) during interference. These findings showing more widespread connectivity of the amygdala extend past findings of atypical functional anatomy of eye-gaze processing in children with ASD and challenge views of general underconnectivity in ASD.
PMCID: PMC3544253  PMID: 23326662
6.  Visual disengagement in the infant siblings of children with an Autism Spectrum Disorder (ASD) 
Children with Autism Spectrum Disorders (ASDs) are impaired in visually disengaging attention in both social and non-social contexts, impairments that may, in subtler form, also affect the infant siblings of children with an ASD (ASD-sibs). We investigated patterns of visual attention (gazing) in six-month-old ASD-sibs (n = 17) and the siblings of typically developing children (COMP-sibs; n =17) during the Face-to-Face/Still-Face Protocol (FFSF), in which parents are sequentially responsive, nonresponsive, and responsive to their infants. Throughout the protocol, ASD-sibs shifted their gaze to and from their parents' faces less frequently than did COMP-sibs. The mean durations of ASD-sibs’ gazes away from their parents' faces were longer than those of COMP-sibs. ASD-sibs and COMP-sibs did not differ in the mean durations of gazes at their parents' faces. In sum, ASD-sibs showed no deficits in visual interest to their parents’ faces, but greater interest than COMP-sibs in non-face stimuli.
PMCID: PMC2860749  PMID: 18805943
autism spectrum disorders; siblings; at-risk; disengagement; early deficits
7.  The shared signal hypothesis and neural responses to expressions and gaze in infants and adults 
Event-related potentials were recorded from adults and 4-month-old infants while they watched pictures of faces that varied in emotional expression (happy and fearful) and in gaze direction (direct or averted). Results indicate that emotional expression is temporally independent of gaze direction processing at early stages of processing, and only become integrated at later latencies. Facial expressions affected the face-sensitive ERP components in both adults (N170) and infants (N290 and P400), while gaze direction and the interaction between facial expression and gaze affected the posterior channels in adults and the frontocentral channels in infants. Specifically, in adults, this interaction reflected a greater responsiveness to fearful expressions with averted gaze (avoidance-oriented emotion), and to happy faces with direct gaze (approach-oriented emotions). In infants, a larger activation to a happy expression at the frontocentral negative component (Nc) was found, and planned comparisons showed that it was due to the direct gaze condition. Taken together, these results support the shared signal hypothesis in adults, but only to a lesser extent in infants, suggesting that experience could play an important role.
PMCID: PMC2840839  PMID: 19858107
ERP; facial expressions; gaze; shared signal hypothesis
8.  Neural correlates of “social gaze” processing in high-functioning autism under systematic variation of gaze duration☆ 
NeuroImage : Clinical  2013;3:340-351.
Direct gaze is a salient nonverbal signal for social interest and the intention to communicate. In particular, the duration of another's direct gaze can modulate our perception of the social meaning of gaze cues. However, both poor eye contact and deficits in social cognitive processing of gaze are specific diagnostic features of autism. Therefore, investigating neural mechanisms of gaze may provide key insights into the neural mechanisms related to autistic symptoms. Employing functional magnetic resonance imaging (fMRI) and a parametric design, we investigated the neural correlates of the influence of gaze direction and gaze duration on person perception in individuals with high-functioning autism (HFA) and a matched control group. For this purpose, dynamically animated faces of virtual characters, displaying averted or direct gaze of different durations (1 s, 2.5 s and 4 s) were evaluated on a four-point likeability scale. Behavioral results revealed that HFA participants showed no significant difference in likeability ratings depending on gaze duration, while the control group rated the virtual characters as increasingly likeable with increasing gaze duration. On the neural level, direct gaze and increasing direct gaze duration recruit regions of the social neural network (SNN) in control participants, indicating the processing of social salience and a perceived communicative intent. In participants with HFA however, regions of the social neural network were more engaged by averted and decreasing amounts of gaze, while the neural response for processing direct gaze in HFA was not suggestive of any social information processing.
•We investigate the neural processing of gaze direction and duration in HFA.•We use a combined categorical and parametric approach to analyze fMRI data.•The social neural network is not modulated by direct gaze cues in HFA.•Persons with HFA are impaired in using subtle aspects of gaze to understand others.
PMCID: PMC3815020  PMID: 24273718
Social gaze; Gaze duration; High-functioning autism; FMRI
9.  Visual attention to dynamic faces and objects is linked to face processing skills: a combined study of children with autism and controls 
Although the extant literature on face recognition skills in Autism Spectrum Disorder (ASD) shows clear impairments compared to typically developing controls (TDC) at the group level, the distribution of scores within ASD is broad. In the present research, we take a dimensional approach and explore how differences in social attention during an eye tracking experiment correlate with face recognition skills across ASD and TDC. Emotional discrimination and person identity perception face processing skills were assessed using the Let's Face It! Skills Battery in 110 children with and without ASD. Social attention was assessed using infrared eye gaze tracking during passive viewing of movies of facial expressions and objects displayed together on a computer screen. Face processing skills were significantly correlated with measures of attention to faces and with social skills as measured by the Social Communication Questionnaire (SCQ). Consistent with prior research, children with ASD scored significantly lower on face processing skills tests but, unexpectedly, group differences in amount of attention to faces (vs. objects) were not found. We discuss possible methodological contributions to this null finding. We also highlight the importance of a dimensional approach for understanding the developmental origins of reduced face perception skills, and emphasize the need for longitudinal research to truly understand how social motivation and social attention influence the development of social perceptual skills.
PMCID: PMC3622030  PMID: 23596436
autism; eye tracking; face processing; eyetracking; autism spectrum disorder; ASD
10.  The NIMH Child Emotional Faces Picture Set (NIMH-ChEFS): A new set of children’s facial emotion stimuli 
With emergence of new technologies, there has been an explosion of basic and clinical research on the affective and cognitive neuroscience of face processing and emotion perception. Adult emotional face stimuli are commonly used in these studies. For developmental research, there is a need for a validated set of child emotional faces. This paper describes the development of the NIMH Child Emotional Faces Picture Set (NIMH-ChEFS), a relatively large stimulus set with high quality, color images of the emotional faces of children. The set includes 482 photos of fearful, angry, happy, sad and neutral child faces with two gaze conditions: direct and averted gaze. In this paper we describe the development of the NIMH-ChEFS and data on the set’s validity based on ratings by 20 healthy adult raters. Agreement between the a priori emotion designation and the raters’ labels was high and comparable with values reported for commonly used adult picture sets. Intensity, representativeness, and composite “goodness” ratings are also presented to guide researchers in their choice of specific stimuli for their studies. These data should give researchers confidence in the NIMH-ChEFS’s validity for use in affective and social neuroscience research.
PMCID: PMC3342041  PMID: 22547297
face processing; emotion perception; face stimuli sets; developmental psychopathology; methodology
11.  It's all in the eyes: neural responses to socially significant gaze shifts 
Neuroreport  2007;18(8):763-766.
Gaze direction signals another's focus of social attention. Here we recorded ERPs to a multi-face display where a gaze aversion created three different social scenarios involving social attention, mutual gaze exchange, and gaze avoidance. N170 was unaffected by social scenario. P350 latency was shortest in social attention and mutual gaze exchange, whereas P500 was largest for gaze avoidance. Our data suggest that neural activity after 300ms post-stimulus may index processes associated with extracting social meaning, whereas that earlier than 300ms may index processing of gaze change independent of social context.
PMCID: PMC2794043  PMID: 17471062
social cognition; eyes; gaze shifts; N170; P350; ERPs; temporal cortex; STS
12.  Facial Expressions of Threat Influence Perceived Gaze Direction in 8 Year-Olds 
PLoS ONE  2012;7(11):e49317.
Adults show reciprocal influences between the perception of gaze direction and emotional expression. These facilitate the understanding of facial signals, because the meaning of one cue can vary considerably depending on the value of the other. Here we ask whether children show similar reciprocal influences in the perception of gaze and expression. A previous study has demonstrated that gaze direction affects the perception of emotional expression in children. Here we demonstrate the opposite direction of influence, showing that expression affects the perception of gaze direction. Specifically, we show that the cone of gaze, i.e., range of gaze deviations perceived as direct, is larger for angry than neutral or fearful faces in 8 year-old children. Therefore, we conclude that children, like adults, show reciprocal influences in the perception of gaze and expression. An unexpected finding was that, compared with adults, children showed larger effects of expression on gaze perception. This finding raises the possibility that it is the ability to process cues independently, rather than sensitivity to combinations, that matures during development. Alternatively, children may be particularly sensitive to anger in adult faces.
PMCID: PMC3498150  PMID: 23166638
13.  Autism spectrum traits predict the neural response to eye gaze in typical individuals 
Neuroimage  2012;59(4-4):3356-3363.
Autism Spectrum Disorders (ASD) are neurodevelopmental disorders characterised by impaired social interaction and communication, restricted interests and repetitive behaviours. The severity of these characteristics are posited to lie on a continuum extending into the typical population, and typical adults' performance on behavioural tasks that are impaired in ASD is correlated with the extent to which they display autistic traits (as measured by Autism Spectrum Quotient, AQ). Individuals with ASD also show structural and functional differences in brain regions involved in social perception. Here we show that variation in AQ in typically developing individuals is associated with altered brain activity in the neural circuit for social attention perception while viewing others' eye gaze. In an fMRI experiment, participants viewed faces looking at variable or constant directions. In control conditions, only the eye region was presented or the heads were shown with eyes closed but oriented at variable or constant directions. The response to faces with variable vs. constant eye gaze direction was associated with AQ scores in a number of regions (posterior superior temporal sulcus, intraparietal sulcus, temporoparietal junction, amygdala, and MT/V5) of the brain network for social attention perception. No such effect was observed for heads with eyes closed or when only the eyes were presented. The results demonstrate a relationship between neurophysiology and autism spectrum traits in the typical (non-ASD) population and suggest that changes in the functioning of the neural circuit for social attention perception is associated with an extended autism spectrum in the typical population.
► Autistic spectrum might extend to typically developing (TD) individuals. ► We studied TD individuals with varying Autism Spectrum Quotient (AQ). ► AQ correlated with BOLD response to viewing variable vs. constant eye gaze. ► AQ did not correlate with response to directional control stimuli. ► Neurophysiology and autism spectrum traits are associated in non-AS individuals.
PMCID: PMC3315678  PMID: 22062191
Eye gaze; fMRI; Autism spectrum; Attention; Face perception
14.  Neural circuitry of emotional face processing in autism spectrum disorders 
Autism spectrum disorders (ASD) are associated with severe impairments in social functioning. Because faces provide nonverbal cues that support social interactions, many studies of ASD have examined neural structures that process faces, including the amygdala, ventromedial prefrontal cortex and superior and middle temporal gyri. However, increases or decreases in activation are often contingent on the cognitive task. Specifically, the cognitive domain of attention influences group differences in brain activation. We investigated brain function abnormalities in participants with ASD using a task that monitored attention bias to emotional faces.
Twenty-four participants (12 with ASD, 12 controls) completed a functional magnetic resonance imaging study while performing an attention cuing task with emotional (happy, sad, angry) and neutral faces.
In response to emotional faces, those in the ASD group showed greater right amygdala activation than those in the control group. A preliminary psychophysiological connectivity analysis showed that ASD participants had stronger positive right amygdala and ventromedial prefrontal cortex coupling and weaker positive right amygdala and temporal lobe coupling than controls. There were no group differences in the behavioural measure of attention bias to the emotional faces.
The small sample size may have affected our ability to detect additional group differences.
When attention bias to emotional faces was equivalent between ASD and control groups, ASD was associated with greater amygdala activation. Preliminary analyses showed that ASD participants had stronger connectivity between the amygdala ventromedial prefrontal cortex (a network implicated in emotional modulation) and weaker connectivity between the amygdala and temporal lobe (a pathway involved in the identification of facial expressions, although areas of group differences were generally in a more anterior region of the temporal lobe than what is typically reported for emotional face processing). These alterations in connectivity are consistent with emotion and face processing disturbances in ASD.
PMCID: PMC2834792  PMID: 20184808
15.  Predictive gaze cues affect face evaluations: The effect of facial emotion 
When we see someone change their direction of gaze, we spontaneously follow their eyes because we expect people to look at interesting objects. Bayliss and Tipper (2006) examined the consequences of observing this expectancy being either confirmed or violated by faces producing reliable or unreliable gaze cues. Participants viewed different faces that would consistently look at the target, or consistently look away from the target: The faces that consistently looked towards targets were subsequently chosen as being more trustworthy than the faces that consistently looked away from targets. The current work demonstrates that these gaze contingency effects are only detected when faces create a positive social context by smiling, but not in the negative context when all the faces held angry or neutral expressions. These data suggest that implicit processing of the reward contingencies associated with gaze cues relies on a positive emotional expression to maintain expectations of a favourable outcome of joint attention episodes.
PMCID: PMC2945961  PMID: 20885988
Eye gaze; Attention; Face processing; Social evaluation
16.  Face-to-face interference in typical and atypical development 
Developmental Science  2012;15(2):281-291.
Visual communication cues facilitate interpersonal communication. It is important that we look at faces to retrieve and subsequently process such cues. It is also important that we sometimes look away from faces as they increase cognitive load that may interfere with online processing. Indeed, when typically developing individuals hold face gaze it interferes with task completion. In this novel study we quantify face interference for the first time in Williams syndrome (WS) and Autism Spectrum Disorder (ASD). These disorders of development impact on cognition and social attention, but how do faces interfere with cognitive processing? Individuals developing typically as well as those with ASD (n = 19) and WS (n = 16) were recorded during a question and answer session that involved mathematics questions. In phase 1 gaze behaviour was not manipulated, but in phase 2 participants were required to maintain eye contact with the experimenter at all times. Looking at faces decreased task accuracy for individuals who were developing typically. Critically, the same pattern was seen in WS and ASD, whereby task performance decreased when participants were required to hold face gaze. The results show that looking at faces interferes with task performance in all groups. This finding requires the caveat that individuals with WS and ASD found it harder than individuals who were developing typically to maintain eye contact throughout the interaction. Individuals with ASD struggled to hold eye contact at all points of the interaction while those with WS found it especially difficult when thinking.
PMCID: PMC3627295  PMID: 22356183
17.  In the Eye of the Beholder: Reduced Threat-Bias and Increased Gaze-Imitation towards Reward in Relation to Trait Anger 
PLoS ONE  2012;7(2):e31373.
The gaze of a fearful face silently signals a potential threat's location, while the happy-gaze communicates the location of impending reward. Imitating such gaze-shifts is an automatic form of social interaction that promotes survival of individual and group. Evidence from gaze-cueing studies suggests that covert allocation of attention to another individual's gaze-direction is facilitated when threat is communicated and further enhanced by trait anxiety. We used novel eye-tracking techniques to assess whether dynamic fearful and happy facial expressions actually facilitate automatic gaze-imitation. We show that this actual gaze-imitation effect is stronger when threat is signaled, but not further enhanced by trait anxiety. Instead, trait anger predicts facilitated gaze-imitation to reward, and to reward compared to threat. These results agree with an increasing body of evidence on trait anger sensitivity to reward.
PMCID: PMC3281963  PMID: 22363632
18.  Watch Out! Magnetoencephalographic Evidence for Early Modulation of Attention Orienting by Fearful Gaze Cueing 
PLoS ONE  2012;7(11):e50499.
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.
PMCID: PMC3510181  PMID: 23209761
19.  Gaze aversion as a cognitive load management strategy in autism spectrum disorder and Williams syndrome 
During face-to-face questioning, typically developing children and adults use gaze aversion (GA), away from their questioner, when thinking. GA increases with question difficulty and improves the accuracy of responses. This is the first study to investigate whether individuals with autism spectrum disorder (ASD; associated with reduced sociability and atypical face gaze) and Williams syndrome (WS; associated with hypersociability and atypical face gaze) use GA to manage cognitive load during face-to-face interactions.
Two studies were conducted exploring the typicality of GA during face-to-face questioning in (a) ASD and (b) WS.
In Study 1, children with ASD increased their GA as question difficulty increased. In addition, they used most GA when thinking about their responses to questions, mirroring evidence from typically developing children. An important atypicality for participants with ASD was a significantly higher level of GA when listening to interlocutors. In Study 2, participants with WS showed typical patterns of GA in relation to question difficulty and across different points of the interaction.
Two different neuro-developmental disorders, both characterized by significant problems with executive control of attention and atypicalities of social interactions, exhibited generally typical patterns of GA. All groups used most GA while thinking about questions, and increased their GA as questions got harder. In addition, children with ASD showed elevated levels of GA while listening to questions, but not while thinking about or making their responses, suggesting that they sometimes fail to see the relevance of attending to visual cues rather than actively avoiding them. Results have important implications for how professionals interpret GA in these populations and for social skills training.
PMCID: PMC3627297  PMID: 22029480
Eye contact; gaze; Williams syndrome; gaze aversion; autism spectrum disorder
20.  Happy and fearful emotion in cues and targets modulate event-related potential indices of gaze-directed attentional orienting 
The goal of the present study was to characterize the effects of valence in facial cues and object targets on event-related potential (ERPs) indices of gaze-directed orienting. Participants were shown faces at fixation that concurrently displayed dynamic gaze shifts and expression changes from neutral to fearful or happy emotions. Emotionally-salient target objects subsequently appeared in the periphery and were spatially congruent or incongruent with the gaze direction. ERPs were time-locked to target presentation. Three sequential ERP components were modulated by happy emotion, indicating a progression from an expression effect to a gaze-by-expression interaction to a target emotion effect. These effects included larger P1 amplitude over contralateral occipital sites for targets following happy faces, larger centrally distributed N1 amplitude for targets following happy faces with leftward gaze, and faster P3 latency for positive targets. In addition, parietally distributed P3 amplitude was reduced for validly cued targets following fearful expressions. Results are consistent with accounts of attentional broadening and motivational approach by happy emotion, and facilitation of spatially directed attention in the presence of fearful cues. The findings have implications for understanding how socioemotional signals in faces interact with each other and with emotional features of objects in the environment to alter attentional processes.
PMCID: PMC2453519  PMID: 18626515
facial affect; positive psychology; evoked potentials; shared attention; social neuroscience
21.  Happy and fearful emotion in cues and targets modulate event-related potential indices of gaze-directed attentional orienting 
The goal of the present study was to characterize the effects of valence in facial cues and object targets on event-related potential (ERPs) indices of gaze-directed orienting. Participants were shown faces at fixation that concurrently displayed dynamic gaze shifts and expression changes from neutral to fearful or happy emotions. Emotionally-salient target objects subsequently appeared in the periphery and were spatially congruent or incongruent with the gaze direction. ERPs were time-locked to target presentation. Three sequential ERP components were modulated by happy emotion, indicating a progression from an expression effect to a gaze-by-expression interaction to a target emotion effect. These effects included larger P1 amplitude over contralateral occipital sites for targets following happy faces, larger centrally distributed N1 amplitude for targets following happy faces with leftward gaze, and faster P3 latency for positive targets. In addition, parietally distributed P3 amplitude was reduced for validly cued targets following fearful expressions. Results are consistent with accounts of attentional broadening and motivational approach by happy emotion, and facilitation of spatially directed attention in the presence of fearful cues. The findings have implications for understanding how socioemotional signals in faces interact with each other and with emotional features of objects in the environment to alter attentional processes.
PMCID: PMC2453519  PMID: 18626515
facial affect; positive psychology; evoked potentials; shared attention; social neuroscience
22.  Normal Gaze Cueing in Children with Autism Is Disrupted by Simultaneous Speech Utterances in “Live” Face-to-Face Interactions 
Autism Research and Treatment  2011;2011:545964.
Gaze cueing was assessed in children with autism and in typically developing children, using a computer-controlled “live” face-to-face procedure. Sensitivity to gaze direction was assessed using a Posner cuing paradigm. Both static and dynamic directional gaze cues were used. Consistent with many previous studies, using photographic and cartoon faces, gaze cueing was present in children with autism and was not developmentally delayed. However, in the same children, gaze cueing was abolished when a mouth movement occurred at the same time as the gaze cue. In contrast, typical children were able to use gaze cues in all conditions. The findings indicate that gaze cueing develops successfully in some children with autism but that their attention is disrupted by speech utterances. Their ability to learn to read nonverbal emotional and intentional signals provided by the eyes may therefore be significantly impaired. This may indicate a problem with cross-modal attention control or an abnormal sensitivity to peripheral motion in general or the mouth region in particular.
PMCID: PMC3420531  PMID: 22937251
23.  Anxiety and Sensitivity to Gaze Direction in Emotionally Expressive Faces 
Emotion (Washington, D.C.)  2007;7(3):478-486.
This study investigated the role of neutral, happy, fearful, and angry facial expressions in enhancing orienting to the direction of eye gaze. Photographs of faces with either direct or averted gaze were presented. A target letter (T or L) appeared unpredictably to the left or the right of the face, either 300 ms or 700 ms after gaze direction changed. Response times were faster in congruent conditions (i.e., when the eyes gazed toward the target) relative to incongruent conditions (when the eyes gazed away from the target letter). Facial expression did influence reaction times, but these effects were qualified by individual differences in self-reported anxiety. High trait-anxious participants showed an enhanced orienting to the eye gaze of faces with fearful expressions relative to all other expressions. In contrast, when the eyes stared straight ahead, trait anxiety was associated with slower responding when the facial expressions depicted anger. Thus, in anxiety-prone people attention is more likely to be held by an expression of anger, whereas attention is guided more potently by fearful facial expressions.
PMCID: PMC2757723  PMID: 17683204
emotion; facial expression; gaze direction; anxiety; attentional orienting
24.  How Do We Update Faces? Effects of Gaze Direction and Facial Expressions on Working Memory Updating 
The aim of the study was to investigate how the biological binding between different facial dimensions, and their social and communicative relevance, may impact updating processes in working memory (WM). We focused on WM updating because it plays a key role in ongoing processing. Gaze direction and facial expression are crucial and changeable components of face processing. Direct gaze enhances the processing of approach-oriented facial emotional expressions (e.g., joy), while averted gaze enhances the processing of avoidance-oriented facial emotional expressions (e.g., fear). Thus, the way in which these two facial dimensions are combined communicates to the observer important behavioral and social information. Updating of these two facial dimensions and their bindings has not been investigated before, despite the fact that they provide a piece of social information essential for building and maintaining an internal ongoing representation of our social environment. In Experiment 1 we created a task in which the binding between gaze direction and facial expression was manipulated: high binding conditions (e.g., joy-direct gaze) were compared to low binding conditions (e.g., joy-averted gaze). Participants had to study and update continuously a number of faces, displaying different bindings between the two dimensions. In Experiment 2 we tested whether updating was affected by the social and communicative value of the facial dimension binding; to this end, we manipulated bindings between eye and hair color, two less communicative facial dimensions. Two new results emerged. First, faster response times were found in updating combinations of facial dimensions highly bound together. Second, our data showed that the ease of the ongoing updating processing varied depending on the communicative meaning of the binding that had to be updated. The results are discussed with reference to the role of WM updating in social cognition and appraisal processes.
PMCID: PMC3459018  PMID: 23060832
biological binding; social cognition; appraisal; gaze direction; facial expression; facial dimensions; working memory
25.  No Differences in Emotion Recognition Strategies in Children with Autism Spectrum Disorder: Evidence from Hybrid Faces 
Autism Research and Treatment  2014;2014:345878.
Emotion recognition problems are frequently reported in individuals with an autism spectrum disorder (ASD). However, this research area is characterized by inconsistent findings, with atypical emotion processing strategies possibly contributing to existing contradictions. In addition, an attenuated saliency of the eyes region is often demonstrated in ASD during face identity processing. We wanted to compare reliance on mouth versus eyes information in children with and without ASD, using hybrid facial expressions. A group of six-to-eight-year-old boys with ASD and an age- and intelligence-matched typically developing (TD) group without intellectual disability performed an emotion labelling task with hybrid facial expressions. Five static expressions were used: one neutral expression and four emotional expressions, namely, anger, fear, happiness, and sadness. Hybrid faces were created, consisting of an emotional face half (upper or lower face region) with the other face half showing a neutral expression. Results showed no emotion recognition problem in ASD. Moreover, we provided evidence for the existence of top- and bottom-emotions in children: correct identification of expressions mainly depends on information in the eyes (so-called top-emotions: happiness) or in the mouth region (so-called bottom-emotions: sadness, anger, and fear). No stronger reliance on mouth information was found in children with ASD.
PMCID: PMC3909988  PMID: 24527213

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