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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.

Background

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).

Methods

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.

Results

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.

Conclusions

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.

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.

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.

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.

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.

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.

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.

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.

Background

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.

Methods

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.

Results

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.

Limitations

The small sample size may have affected our ability to detect additional group differences.

Conclusion

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.

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.

Highlights

► 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.

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.

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.

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.

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.

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.

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.

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.

Objective

To examine prospectively the emergence of behavioral signs of autism in the first years of life in infants at low and high risk for autism.

Method

A prospective longitudinal design was used to compare 25 infants later diagnosed with an autism spectrum disorder (ASD) with 25 gender-matched low-risk children later determined to have typical development. Participants were evaluated at 6, 12, 18, 24, and 36 months of age. Frequencies of gaze to faces, social smiles, and directed vocalizations were coded from video and rated by examiners.

Results

The frequency of gaze to faces, shared smiles, and vocalizations to others were highly comparable between groups at 6 months of age, but significantly declining trajectories over time were apparent in the group later diagnosed with ASD. Group differences were significant by 12 months of age on most variables. Although repeated evaluation documented loss of skills in most infants with ASD, most parents did not report a regression in their child’s development.

Conclusions

These results suggest that behavioral signs of autism are not present at birth, as once suggested by Kanner, but emerge over time through a process of diminishment of key social communication behaviors. More children may present with a regressive course than previously thought, but parent report methods do not capture this phenomenon well. Implications for onset classification systems and clinical screening are also discussed.

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.

Background

Visual behavior is known to be atypical in Autism Spectrum Disorders (ASD). Monitor-based eye-tracking studies have measured several of these atypicalities in individuals with Autism. While atypical behaviors are known to be accentuated during natural interactions, few studies have been made on gaze behavior in natural interactions. In this study we focused on i) whether the findings done in laboratory settings are also visible in a naturalistic interaction; ii) whether new atypical elements appear when studying visual behavior across the whole field of view.

Methodology/Principal Findings

Ten children with ASD and ten typically developing children participated in a dyadic interaction with an experimenter administering items from the Early Social Communication Scale (ESCS). The children wore a novel head-mounted eye-tracker, measuring gaze direction and presence of faces across the child's field of view. The analysis of gaze episodes to faces revealed that children with ASD looked significantly less and for shorter lapses of time at the experimenter. The analysis of gaze patterns across the child's field of view revealed that children with ASD looked downwards and made more extensive use of their lateral field of view when exploring the environment.

Conclusions/Significance

The data gathered in naturalistic settings confirm findings previously obtained only in monitor-based studies. Moreover, the study allowed to observe a generalized strategy of lateral gaze in children with ASD when they were looking at the objects in their environment.

This study used eye-tracking to examine visual attention to faces and objects in adolescents with autism spectrum disorder (ASD) and typical peers. Point of gaze was recorded during passive viewing of images of human faces, inverted human faces, monkey faces, three-dimensional curvilinear objects, and two-dimensional geometric patterns. Individuals with ASD obtained lower scores on measures of face recognition and social-emotional functioning but exhibited similar patterns of visual attention. In individuals with ASD, face recognition performance was associated with social adaptive function. Results highlight heterogeneity in manifestation of social deficits in ASD and suggest that naturalistic assessments are important for quantifying atypicalities in visual attention.

The amygdalae are involved in the perception of emotions such as happiness, anger and fear. Because of their proximity to the sinuses, the image signal intensity in T2* weighted fMRI data is often affected by signal loss due to through-slice dephasing, especially at high field strength. In this study, the feasibility of fMRI in the amygdalae at 7 Tesla was investigated. A paradigm based on the presentation of fearful faces was used for stimulation. Previously, opposite effects have been found for presentation of averted and direct gaze fearful faces. Here, we show that (1) sufficiently high temporal SNR values are reached in the amygdalae for detection of small BOLD signal changes and (2) that the BOLD signal in the amygdalae for presentation of a direct or averted gaze in a fearful face depends on stimulus duration.

The social motivation hypothesis of autism posits that infants with autism do not experience social stimuli as rewarding, thereby leading to a cascade of potentially negative consequences for later development. While possible downstream effects of this hypothesis such as altered face and voice processing have been examined, there has not been a direct investigation of social reward processing in autism. Here we use functional magnetic resonance imaging to examine social and monetary rewarded implicit learning in children with and without autism spectrum disorders (ASD). Sixteen males with ASD and sixteen age- and IQ-matched typically developing (TD) males were scanned while performing two versions of a rewarded implicit learning task. In addition to examining responses to reward, we investigated the neural circuitry supporting rewarded learning and the relationship between these factors and social development. We found diminished neural responses to both social and monetary rewards in ASD, with a pronounced reduction in response to social rewards (SR). Children with ASD also demonstrated a further deficit in frontostriatal response during social, but not monetary, rewarded learning. Moreover, we show a relationship between ventral striatum activity and social reciprocity in TD children. Together, these data support the hypothesis that children with ASD have diminished neural responses to SR, and that this deficit relates to social learning impairments.

Gaze avoidance is a hallmark behavioral feature of fragile X syndrome (FXS), but little is known about whether abnormalities in the visual processing of faces, including disrupted autonomic reactivity, may underlie this behavior. Eye tracking was used to record fixations and pupil diameter while adolescents and young adults with FXS and sex- and age-matched typically developing controls passively viewed photographs of faces containing either a calm, happy, or fearful expression, preceded by a scrambled face matched on luminance. Results provide quantitative evidence for significant differences in gaze patterns and increased pupillary reactivity when individuals with FXS passively view static faces. Such abnormalities have significant implications in terms of understanding causes of gaze avoidance observed in individuals with FXS.