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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.
doi:10.1002/brb3.6
PMCID: PMC3217668  PMID: 22398976
Autism; facial expression; functional magnetic resonance imaging; gaze; developmental neuroimaging
2.  Brain function and gaze-fixation during facial emotion processing in fragile-X and autism 
This research focuses on the relationship between fragile X syndrome (FXS) and autism spectrum disorders (ASD). Both of these populations have a tendency to avoid looking others in the eye, along with difficulties in communication with others and tend to be socially withdrawn. While it is clear that FXS and ASD share some common abnormal behaviors, the underlying brain mechanisms associated with the social and emotional deficits in these groups remain unclear. We showed pictures of emotional and non-emotional human faces to these groups while in a magnetic resonance scanner (MRI). We collected images of brain function along with measures of where on the faces the individuals were looking (e.g. eyes or mouth). The FXS group showed a similar yet less abnormal pattern of where they were looking on the face compared to the ASD group. The FXS group also showed a similar pattern of decreased brain function in the area of the brain typically used when looking at faces, the fusiform gyrus (FG). The amount of activation in the FG was associated with how much time the FXS and ASD individuals looked at the eyes, the more they looked at the eyes, the greater the FG activation. The FXS group also displayed more brain activation than both the ASD group and a group of typically developing control subjects in brain areas that might suggest increased task difficulty for the FXS group. These group differences in brain activation are important as they suggest there is some overlap in areas of brain function in FXS and ASD when looking at faces, but that these two groups also have unique activation in other brain areas. These findings largely support the idea that ASD characteristics in FXS are associated with partially different patterns of brain activation when looking at human faces compared to individuals with ASD.
Objective:
Fragile X syndrome (FXS) is the most commonly known genetic disorder associated with autism spectrum disorder (ASD). Overlapping features in these populations include gaze aversion, communication deficits, and social withdrawal. Although the association between FXS and ASD has been well documented at the behavioral level, the underlying neural mechanisms associated with the social/emotional deficits in these groups remain unclear.
Method:
We collected functional brain images and eye-gaze fixations from 9 individuals with FXS and 14 individuals with idiopathic ASD, as well as 15 typically developing (TD) individuals, while they performed a facial-emotion discrimination task.
Results:
The FXS group showed a similar yet less aberrant pattern of gaze-fixations compared to the ASD group. The FXS group also showed fusiform gyrus (FG) hypoactivation compared to the TD control group. Activation in FG was strongly and positively associated with average eye fixation and negatively associated with ASD characteristics in the FXS group. The FXS group displayed significantly greater activation than both the TD control and ASD groups in the left hippocampus (HIPP), left superior temporal gyrus (STG), right insula (INS), and left post-central gyrus (PCG).
Conclusions:
These group differences in brain activation are important as they suggest unique underlying face-processing neural circuitry in FXS versus idiopathic ASD, largely supporting the hypothesis that ASD characteristics in FXS and idiopathic ASD reflect partially divergent impairments at the neural level, at least in FXS individuals without a co-morbid diagnosis of ASD.
doi:10.1002/aur.32
PMCID: PMC2679695  PMID: 19360673
fragile X syndrome; autism; face processing; brain function; fMRI
3.  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.
doi:10.1371/journal.pone.0081206
PMCID: PMC3852523  PMID: 24324679
4.  Variation in the human cannabinoid receptor CNR1 gene modulates gaze duration for happy faces 
Molecular Autism  2011;2:10.
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.
doi:10.1186/2040-2392-2-10
PMCID: PMC3155489  PMID: 21714860
5.  Early neural activation during facial affect processing in adolescents with Autism Spectrum Disorder☆ 
NeuroImage : Clinical  2014;7:203-212.
Impaired social interaction is one of the hallmarks of Autism Spectrum Disorder (ASD). Emotional faces are arguably the most critical visual social stimuli and the ability to perceive, recognize, and interpret emotions is central to social interaction and communication, and subsequently healthy social development. However, our understanding of the neural and cognitive mechanisms underlying emotional face processing in adolescents with ASD is limited. We recruited 48 adolescents, 24 with high functioning ASD and 24 typically developing controls. Participants completed an implicit emotional face processing task in the MEG. We examined spatiotemporal differences in neural activation between the groups during implicit angry and happy face processing. While there were no differences in response latencies between groups across emotions, adolescents with ASD had lower accuracy on the implicit emotional face processing task when the trials included angry faces. MEG data showed atypical neural activity in adolescents with ASD during angry and happy face processing, which included atypical activity in the insula, anterior and posterior cingulate and temporal and orbitofrontal regions. Our findings demonstrate differences in neural activity during happy and angry face processing between adolescents with and without ASD. These differences in activation in social cognitive regions may index the difficulties in face processing and in comprehension of social reward and punishment in the ASD group. Thus, our results suggest that atypical neural activation contributes to impaired affect processing, and thus social cognition, in adolescents with ASD.
Highlights
•The ability to recognize and interpret emotions is central to social interaction.•Deficits in social interactions are hallmarks of autism spectrum disorder (ASD).•Adolescents with and without ASD completed an emotional face task in MEG.•MEG data showed atypical neural activity in ASD to both angry and happy faces.•Insula, cingulate, temporal and orbitofrontal activities were particularly affected in the ASD group.
doi:10.1016/j.nicl.2014.11.009
PMCID: PMC4300004  PMID: 25610782
Implicit face processing; Adolescents; Autism Spectrum Disorder; Magnetoencephalography; Affect processing; Anterior cingulate cortex
6.  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.
Highlights
•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.
doi:10.1016/j.nicl.2013.08.014
PMCID: PMC3815020  PMID: 24273718
Social gaze; Gaze duration; High-functioning autism; FMRI
7.  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.
doi:10.1155/2012/652408
PMCID: PMC3544253  PMID: 23326662
8.  Investigating Gaze of Children with ASD in Naturalistic Settings 
PLoS ONE  2012;7(9):e44144.
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.
doi:10.1371/journal.pone.0044144
PMCID: PMC3454390  PMID: 23028494
9.  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.
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.
doi:10.1016/j.neuroimage.2011.10.075
PMCID: PMC3315678  PMID: 22062191
Eye gaze; fMRI; Autism spectrum; Attention; Face perception
10.  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.
doi:10.1093/scan/nsl008
PMCID: PMC2555439  PMID: 18985122
infants; EEG; eye gaze; social cognition; ERP
11.  Elevated amygdala response to faces and gaze aversion in autism spectrum disorder 
Autism spectrum disorders (ASD) are often associated with impairments in judgment of facial expressions. This impairment is often accompanied by diminished eye contact and atypical amygdala responses to face stimuli. The current study used a within-subjects design to examine the effects of natural viewing and an experimental eye-gaze manipulation on amygdala responses to faces. Individuals with ASD showed less gaze toward the eye region of faces relative to a control group. Among individuals with ASD, reduced eye gaze was associated with higher threat ratings of neutral faces. Amygdala signal was elevated in the ASD group relative to controls. This elevated response was further potentiated by experimentally manipulating gaze to the eye region. Potentiation by the gaze manipulation was largest for those individuals who exhibited the least amount of naturally occurring gaze toward the eye region and was associated with their subjective threat ratings. Effects were largest for neutral faces, highlighting the importance of examining neutral faces in the pathophysiology of autism and questioning their use as control stimuli with this population. Overall, our findings provide support for the notion that gaze direction modulates affective response to faces in ASD.
doi:10.1093/scan/nst050
PMCID: PMC3871735  PMID: 23596190
fMRI; amygdala; face expressions; autism spectrum disorders; eye-tracking
12.  Gaze aversion as a cognitive load management strategy in autism spectrum disorder and Williams syndrome 
Background
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.
Methods
Two studies were conducted exploring the typicality of GA during face-to-face questioning in (a) ASD and (b) WS.
Results
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.
Conclusions
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.
doi:10.1111/j.1469-7610.2011.02481.x
PMCID: PMC3627297  PMID: 22029480
Eye contact; gaze; Williams syndrome; gaze aversion; autism spectrum disorder
13.  Facial Trustworthiness Judgments in Children with ASD Are Modulated by Happy and Angry Emotional Cues 
PLoS ONE  2014;9(5):e97644.
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.
doi:10.1371/journal.pone.0097644
PMCID: PMC4039438  PMID: 24878763
14.  Direct Gaze Elicits Atypical Activation of the Theory-of-Mind Network in Autism Spectrum Conditions 
Cerebral Cortex (New York, NY)  2013;24(6):1485-1492.
Eye contact plays a key role in social interaction and is frequently reported to be atypical in individuals with autism spectrum conditions (ASCs). Despite the importance of direct gaze, previous functional magnetic resonance imaging in ASC has generally focused on paradigms using averted gaze. The current study sought to determine the neural processing of faces displaying direct and averted gaze in 18 males with ASC and 23 matched controls. Controls showed an increased response to direct gaze in brain areas implicated in theory-of-mind and gaze perception, including medial prefrontal cortex, temporoparietal junction, posterior superior temporal sulcus region, and amygdala. In contrast, the same regions showed an increased response to averted gaze in individuals with an ASC. This difference was confirmed by a significant gaze direction × group interaction. Relative to controls, participants with ASC also showed reduced functional connectivity between these regions. We suggest that, in the typical brain, perceiving another person gazing directly at you triggers spontaneous attributions of mental states (e.g. he is “interested” in me), and that such mental state attributions to direct gaze may be reduced or absent in the autistic brain.
doi:10.1093/cercor/bht003
PMCID: PMC4014180  PMID: 23324559
autism; connectivity; eye gaze; theory-of-mind
15.  Neural circuitry of emotional face processing in autism spectrum disorders 
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.
doi:10.1503/jpn.090085
PMCID: PMC2834792  PMID: 20184808
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.
doi:10.1111/j.1467-7687.2011.01125.x
PMCID: PMC3627295  PMID: 22356183
17.  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.
doi:10.1093/scan/nsp037
PMCID: PMC2840839  PMID: 19858107
ERP; facial expressions; gaze; shared signal hypothesis
18.  Abnormal Activation of the Social Brain Network in Children with Autism Spectrum Disorder: An fMRI Study 
Psychiatry Investigation  2014;12(1):37-45.
Objective
The aim of this study is to investigate abnormal findings of social brain network in Korean children with autism spectrum disorder (ASD) compared with typically developing children (TDC).
Methods
Functional magnetic resonance imaging (fMRI) was performed to examine brain activations during the processing of emotional faces (happy, fearful, and neutral) in 17 children with ASD, 24 TDC.
Results
When emotional face stimuli were given to children with ASD, various areas of the social brain relevant to social cognition showed reduced activation. Specifically, ASD children exhibited less activation in the right amygdala (AMY), right superior temporal sulcus (STS) and right inferior frontal gyrus (IFG) than TDC group when fearful faces were shown. Activation of left insular cortex and right IFG in response to happy faces was less in the ASD group. Similar findings were also found in left superior insular gyrus and right insula in case of neutral stimulation.
Conclusion
These findings suggest that children with ASD have different processing of social and emotional experience at the neural level. In other words, the deficit of social cognition in ASD could be explained by the deterioration of the capacity for visual analysis of emotional faces, the subsequent inner imitation through mirror neuron system (MNS), and the ability to transmit it to the limbic system and to process the transmitted emotion.
doi:10.4306/pi.2015.12.1.37
PMCID: PMC4310919
Autism spectrum disorder; Social brain network; Social cognition; fMRI
19.  The perception and identification of facial emotions in individuals with Autism Spectrum Disorders using the Let’s Face It! Emotion Skills Battery 
Background
Although impaired social-emotional ability is a hallmark of autism spectrum disorder (ASD), the perceptual skills and mediating strategies contributing to the social deficits of autism are not well understood. A perceptual skill that is fundamental to effective social communication is the ability to accurately perceive and interpret facial emotions. To evaluate the expression processing of participants with ASD, we designed the Let's Face It! Emotion Skills Battery (LFI! Battery), a computer-based assessment composed of three subscales measuring verbal and perceptual skills implicated in the recognition of facial emotions.
Methods
We administered the LFI! battery to groups of participants with ASD and typically developing control (TDC) participants that were matched for age and IQ.
Results
On the NameGame labeling task, participants with ASD (N = 68) performed on par with TDC individuals (N = 66) in their ability to name the facial emotions of happy, sad, disgust and surprise and were only impaired in their ability to identify the angry expression. On the Matchmaker Expression task that measures the recognition of facial emotions across different facial identities, the ASD participants (N = 66) performed reliably worse than TDC participants (N = 67) on the emotions of happy, sad, disgust, frighten and angry. In the Parts/Wholes test of perceptual strategies of expression, the TDC participants (N = 67) displayed more holistic encoding for the eyes than the mouths in expressive faces whereas ASD participants (N = 66) exhibited the reverse pattern of holistic recognition for the mouth and analytic recognition of the eyes.
Conclusion
In summary, findings from Let's Face It! Emotion Skills Battery show that participants with ASD were able to label the basic facial emotions (with the exception of angry expression) on par with age- and IQ-matched typically developing participants. However, participants with ASD were impaired in their ability to generalize facial emotions across different identities and a tendency to recognize the mouth feature holistically and the eyes as isolated parts.
doi:10.1111/j.1469-7610.2012.02571.x
PMCID: PMC3505257  PMID: 22780332
ASD; Computer-based assessment; Facial emotions; Perceptual skills; Social communication
20.  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.
doi:10.1177/1362361308094504
PMCID: PMC2860749  PMID: 18805943
autism spectrum disorders; siblings; at-risk; disengagement; early deficits
21.  The Interaction Between Gaze and Facial Expression in the Amygdala and Extended Amygdala is Modulated by Anxiety 
Behavioral evidence indicates that angry faces are seen as more threatening, and elicit greater anxiety, when directed at the observer, whereas the influence of gaze on the processing of fearful faces is less consistent. Recent research has also found inconsistent effects of expression and gaze direction on the amygdala response to facial signals of threat. However, such studies have failed to consider the important influence of anxiety on the response to signals of threat; an influence that is well established in behavioral research and recent neuroimaging studies. Here, we investigated the way in which individual differences in anxiety would influence the interactive effect of gaze and expression on the response to angry and fearful faces in the human extended amygdala. Participants viewed images of fearful, angry and neutral faces, either displaying an averted or direct gaze. We found that state anxiety predicted an increased response in the dorsal amygdala/substantia innominata (SI) to angry faces when gazing at, relative to away from the observer. By contrast, high state anxious individuals showed an increased amygdala response to fearful faces that was less dependent on gaze. In addition, the relationship between state anxiety and gaze on emotional intensity ratings mirrored the relationship between anxiety and the amygdala/SI response. These results have implications for understanding the functional role of the amygdala and extended amygdala in processing signals of threat, and are consistent with the proposed role of this region in coding the relevance or significance of a stimulus to the observer.
doi:10.3389/fnhum.2010.00056
PMCID: PMC2906373  PMID: 20661452
emotion; anxiety; fMRI; face processing; amygdala; expression; gaze
22.  Reduced gaze aftereffects are related to difficulties categorising gaze direction in children with autism 
Neuropsychologia  2013;51(8):1504-1509.
Perceptual mechanisms are generally flexible or “adaptive”, as evidenced by perceptual aftereffects: distortions that arise following exposure to a stimulus. We examined whether adaptive mechanisms for coding gaze direction are atypical in children diagnosed with an autism spectrum condition. Twenty-four typical children and 24 children with autism, of similar age and ability, were administered a developmentally sensitive eye-gaze adaptation task. In the pre-adaptation phase, children judged whether target faces showing subtle deviations in eye-gaze direction were looking leftwards, rightwards or straight-ahead. Next, children were adapted to faces gazing in one consistent direction (25° leftwards/rightwards) before categorising the direction of the target faces again. Children with autism showed difficulties in judging whether subtle deviations in gaze were directed to the left, right or straight-ahead relative to typical children. Although adaptation to leftward or rightward gaze resulted in reduced sensitivity to gaze on the adapted side for both groups, the aftereffect was significantly reduced in children with autism. Furthermore, the magnitude of children's gaze aftereffects was positively related to their ability to categorise gaze direction. These results show that the mechanisms coding gaze are less flexible in autism and offer a potential new explanation for these children's difficulties discriminating subtle deviations in gaze direction.
Highlights
•Adaptive mechanisms are fundamental for perceptual coding.•We found adaptation to gaze direction was significantly attenuated in autism.•The degree of adaptation was also linked to children's gaze acuity.•This study provides potential evidence for the functional benefits of adaptation.
doi:10.1016/j.neuropsychologia.2013.03.021
PMCID: PMC3708125  PMID: 23583965
Autism; Gaze; Adaptation; Aftereffect; Vision
23.  Effect of Familiarity on Reward Anticipation in Children with and without Autism Spectrum Disorders 
PLoS ONE  2014;9(9):e106667.
Background
Previous research on the reward system in autism spectrum disorders (ASD) suggests that children with ASD anticipate and process social rewards differently than typically developing (TD) children—but has focused on the reward value of unfamiliar face stimuli. Children with ASD process faces differently than their TD peers. Previous research has focused on face processing of unfamiliar faces, but less is known about how children with ASD process familiar faces. The current study investigated how children with ASD anticipate rewards accompanied by familiar versus unfamiliar faces.
Methods
The stimulus preceding negativity (SPN) of the event-related potential (ERP) was utilized to measure reward anticipation. Participants were 6- to 10-year-olds with (N = 14) and without (N = 14) ASD. Children were presented with rewards accompanied by incidental face or non-face stimuli that were either familiar (caregivers) or unfamiliar. All non-face stimuli were composed of scrambled face elements in the shape of arrows, controlling for visual properties.
Results
No significant differences between familiar versus unfamiliar faces were found for either group. When collapsing across familiarity, TD children showed larger reward anticipation to face versus non-face stimuli, whereas children with ASD did not show differential responses to these stimulus types. Magnitude of reward anticipation to faces was significantly correlated with behavioral measures of social impairment in the ASD group.
Conclusions
The findings do not provide evidence for differential reward anticipation for familiar versus unfamiliar face stimuli in children with or without ASD. These findings replicate previous work suggesting that TD children anticipate rewards accompanied by social stimuli more than rewards accompanied by non-social stimuli. The results do not support the idea that familiarity normalizes reward anticipation in children with ASD. Our findings also suggest that magnitude of reward anticipation to faces is correlated with levels of social impairment for children with ASD.
doi:10.1371/journal.pone.0106667
PMCID: PMC4153666  PMID: 25184524
24.  Attention to Eye Contact in the West and East: Autonomic Responses and Evaluative Ratings 
PLoS ONE  2013;8(3):e59312.
Eye contact has a fundamental role in human social interaction. The special appearance of the human eye (i.e., white sclera contrasted with a coloured iris) implies the importance of detecting another person's face through eye contact. Empirical studies have demonstrated that faces making eye contact are detected quickly and processed preferentially (i.e., the eye contact effect). Such sensitivity to eye contact seems to be innate and universal among humans; however, several studies suggest that cultural norms affect eye contact behaviours. For example, Japanese individuals exhibit less eye contact than do individuals from Western European or North American cultures. However, how culture modulates eye contact behaviour is unclear. The present study investigated cultural differences in autonomic correlates of attentional orienting (i.e., heart rate) and looking time. Additionally, we examined evaluative ratings of eye contact with another real person, displaying an emotionally neutral expression, between participants from Western European (Finnish) and East Asian (Japanese) cultures. Our results showed that eye contact elicited stronger heart rate deceleration responses (i.e., attentional orienting), shorter looking times, and higher ratings of subjective feelings of arousal as compared to averted gaze in both cultures. Instead, cultural differences in the eye contact effect were observed in various evaluative responses regarding the stimulus faces (e.g., facial emotion, approachability etc.). The rating results suggest that individuals from an East Asian culture perceive another's face as being angrier, unapproachable, and unpleasant when making eye contact as compared to individuals from a Western European culture. The rating results also revealed that gaze direction (direct vs. averted) could influence perceptions about another person's facial affect and disposition. These results suggest that cultural differences in eye contact behaviour emerge from differential display rules and cultural norms, as opposed to culture affecting eye contact behaviour directly at the physiological level.
doi:10.1371/journal.pone.0059312
PMCID: PMC3596353  PMID: 23516627
25.  Eye contact with neutral and smiling faces: effects on autonomic responses and frontal EEG asymmetry 
In our previous studies we have shown that seeing another person “live” with a direct vs. averted gaze results in enhanced skin conductance responses (SCRs) indicating autonomic arousal and in greater relative left-sided frontal activity in the electroencephalography (asymmetry in the alpha-band power), associated with approach motivation. In our studies, however, the stimulus persons had a neutral expression. In real-life social interaction, eye contact is often associated with a smile, which is another signal of the sender's approach-related motivation. A smile could, therefore, enhance the affective-motivational responses to eye contact. In the present study, we investigated whether the facial expression (neutral vs. social smile) would modulate autonomic arousal and frontal EEG alpha-band asymmetry to seeing a direct vs. an averted gaze in faces presented “live” through a liquid crystal (LC) shutter. The results showed that the SCRs were greater for the direct than the averted gaze and that the effect of gaze direction was more pronounced for a smiling than a neutral face. However, in this study, gaze direction and facial expression did not affect the frontal EEG asymmetry, although, for gaze direction, we found a marginally significant correlation between the degree of an overall bias for asymmetric frontal activity and the degree to which direct gaze elicited stronger left-sided frontal activity than did averted gaze.
doi:10.3389/fnhum.2012.00122
PMCID: PMC3343319  PMID: 22586387
motivation; facial expression; gaze direction; skin conductance response; electroencephalography; social cognition

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