Social Visual Attention Research Articles

Sex differences in social brain neural responses in autism: temporal profiles of configural face-processing within data-driven time windows

Face-processing timing differences may underlie visual social attention differences between autistic and non-autistic people, and males and females. This study investigates the timing of the effects of neurotype and sex on face-processing, and their dependence on age. We analysed EEG data during upright and inverted photographs of faces from 492 participants from the Longitudinal European Autism Project (141 neurotypical males, 76 neurotypical females, 202 autistic males, 73 autistic females; age 6–30 years). We detected timings of sex/diagnosis effects on event-related potential amplitudes at the posterior–temporal channel P8 with Bootstrapped Cluster-based Permutation Analysis and conducted Growth Curve Analysis (GCA) to investigate the timecourse and dependence on age of neural signals. The periods of influence of neurotype and sex overlapped but differed in onset (respectively, 260 and 310 ms post-stimulus), with sex effects lasting longer. GCA revealed a smaller and later amplitude peak in autistic female children compared to non-autistic female children; this difference decreased in adolescence and was not significant in adulthood. No age-dependent neurotype difference was significant in males. These findings indicate that sex and neurotype influence longer latency face processing and implicates cognitive rather than perceptual processing. Sex may have more overarching effects than neurotype on configural face processing.

Visual social attention in SYNGAP1-related intellectual disability.

SYNGAP1-ID is a neurodevelopmental disorder caused by a mutation of the SYNGAP1 gene. Characterized by moderate to severe developmental delay, it is associated with several physical and behavioral issues as well as additional diagnoses, including autism. However, it is not known whether social cognitive differences seen in SYNGAP1-ID are similar to those previously identified in idiopathic or other forms of autism. This study therefore investigated visual social attention in SYNGAP1-ID. Eye movements were recorded across three passive viewing tasks (face scanning, pop-out, and social preference) of differing social complexity in 24 individuals with SYNGAP1-ID and 12 typically developing controls. We found that SYNGAP1-ID participants looked at faces less than the controls, and when they did look at faces, they had less time looking at and fewer fixations to the eyes. For the pop-out task, where social and nonsocial objects (Phone, car, face, bird, and face-noise) were presented in an array, those with SYNGAP1-ID spent significantly less time looking at the phone stimulus as well as fewer fixations to the face compared with the typically developing controls. When looking at two naturalistic scenes side by side, one social in nature (e.g., with children present) and the other not, there were no differences between the SYNGAP1-ID group and typically developing controls on any of the examined eye tracking measures. This study provides novel findings on the social attention of those with SYNGAP1-ID and helps to provide further evidence for using eye tracking as an objective measure of the social phenotype in this population in future clinical trials.

Social impairment in survivors of pediatric brain tumors via reduced social attention and emotion-specific facial expression recognition.

Survivors of pediatric brain tumors (SPBT) experience significant social challenges, including fewer friends and greater isolation than peers. Difficulties in face processing and visual social attention have been implicated in these outcomes. This study evaluated facial expression recognition (FER), social attention, and their associations with social impairments in SPBT. SPBT (N=54; ages 7-16) at least 2years post treatment completed a measure of FER, while parents completed measures of social impairment. A subset (N=30) completed a social attention assessment that recorded eye gaze patterns while watching videos depicting pairs of children engaged in joint play. Social Prioritization scores were calculated, with higher scores indicating more face looking. Correlations and regression analyses evaluated associations between variables, while a path analysis modeling tool (PROCESS) evaluated the indirect effects of Social Prioritization on social impairments through emotion-specific FER. Poorer recognition of angry and sad facial expressions was significantly correlated with greater social impairment. Social Prioritization was positively correlated with angry FER but no other emotions. Social Prioritization had significant indirect effects on social impairments through angry FER. Findings suggest interventions aimed at improving recognition of specific emotions may mitigate social impairments in SPBT. Further, reduced social attention (i.e., diminished face looking) could be a factor in reduced face processing ability, which may result in social impairments. Longitudinal research is needed to elucidate temporal associations between social attention, face processing, and social impairments.

Social visual attention as a treatment outcome: evaluating the social games for autistic adolescents (SAGA) intervention

A core feature of autism involves difficulty perceiving and interpreting eye gaze shifts as nonverbal communicative signals. A hypothesis about the origins of this phenotype is that it emerges from developmentally different social visual attention (SVA). We developed Social Games for Autistic Adolescents (SAGA; Scherf et al. BMJ Open 8(9):e023682, 2018) as a serious game intervention for autistic individuals to discover the significance of eye gaze cues. Previously, we demonstrated the effectiveness of SAGA to improve the perception and understanding of eye gaze cues and social skills for autistic adolescents (Griffin et al. JCPP Adv 1(3):e12041, 2021). Here, we determine whether increases in social visual attention to faces and/or target gazed-at objects, as measured via eye tracking during the same Gaze Perception task in the same study sample, moderated this improvement. In contrast to predictions, SVA to faces did not differentially increase for the treatment group. Instead, both groups evinced a small increase in SVA to faces over time. Second, Prior to the SAGA intervention, attention to faces failed to predict performance in the Gaze Perception task for both the treatment and standard care control groups. However, at post-test, autistic adolescents in the treatment group were more likely to identify the object of directed gaze when they attended longer to faces and longer to target objects. Importantly, this is the first study to measure social visual attention via eye tracking as a treatment response in an RCT for autism. NCT02968225

The use of eye-tracking technology as a tool to evaluate social cognition in people with an intellectual disability: a systematic review and meta-analysis

BackgroundRelatively little is known about social cognition in people with intellectual disability (ID), and how this may support understanding of co-occurring autism. A limitation of previous research is that traditional social-cognitive tasks place a demand on domain-general cognition and language abilities. These tasks are not suitable for people with ID and lack the sensitivity to detect subtle social-cognitive processes. In autism research, eye-tracking technology has offered an effective method of evaluating social cognition—indicating associations between visual social attention and autism characteristics. The present systematic review synthesised research which has used eye-tracking technology to study social cognition in ID. A meta-analysis was used to explore whether visual attention on socially salient regions (SSRs) of stimuli during these tasks correlated with degree of autism characteristics presented on clinical assessment tools.MethodSearches were conducted using four databases, research mailing lists, and citation tracking. Following in-depth screening and exclusion of studies with low methodological quality, 49 articles were included in the review. A correlational meta-analysis was run on Pearson’s r values obtained from twelve studies, reporting the relationship between visual attention on SSRs and autism characteristics.Results and conclusionsEye-tracking technology was used to measure different social-cognitive abilities across a range of syndromic and non-syndromic ID groups. Restricted scan paths and eye-region avoidance appeared to impact people’s ability to make explicit inferences about mental states and social cues. Readiness to attend to social stimuli also varied depending on social content and degree of familiarity. A meta-analysis using a random effects model revealed a significant negative correlation (r = −.28, [95% CI −.47, −.08]) between visual attention on SSRs and autism characteristics across ID groups. Together, these findings highlight how eye-tracking can be used as an accessible tool to measure more subtle social-cognitive processes, which appear to reflect variability in observable behaviour. Further research is needed to be able to explore additional covariates (e.g. ID severity, ADHD, anxiety) which may be related to visual attention on SSRs, to different degrees within syndromic and non-syndromic ID groups, in order to determine the specificity of the association with autism characteristics.

Effects of Transcranial Direct Current Stimulation on Social Attention Patterns and Emotion Recognition Ability in Male Adolescents with Autism Spectrum Disorder.

Autism Spectrum Disorder (ASD) is characterized by impairments in social cognition including emotion recognition (ER) abilities. Common symptoms include unusual patterns of visual social attention, which are investigated as early developmental biomarkers for ASD. Transcranial Direct Current Stimulation (tDCS) has shown promising results in influencing social functioning in individuals with ASD. However, the effects of tDCS on social attention patterns and ER ability in adolescents with ASD remain unclear. This double-blind, sham-controlled, randomized clinical trial examined the effects of repeated sessions of tDCS on gaze behavior and ER ability in 22 male adolescents diagnosed with ASD. Participants received either 20 min of 2 mA active tDCS or sham stimulation for 10 days and an intra-stimulation training. Social allocation patterns were assessed using eye-tracking paradigms, including ER tasks. Our results indicated no tDCS-specific effects. Both groups showed improvements in ER and more frequent, faster, and longer fixations on the eyes than the mouth, and on social than nonsocial areas. In tasks with low social content, fixating the mouth seemed to increase ER accuracy. Understanding the effects of tDCS on social functioning in adolescents with ASD holds promise for the development of targeted interventions to improve their social cognition abilities.

Functional maturation in visual pathways predicts attention to the eyes in infant rhesus macaques: Effects of social status

Differences in looking at the eyes of others are one of the earliest behavioral markers for social difficulties in neurodevelopmental disabilities, including autism. However, it is unknown how early visuo-social experiences relate to the maturation of infant brain networks that process visual social stimuli. We investigated functional connectivity (FC) within the ventral visual object pathway as a contributing neural system. Densely sampled, longitudinal eye-tracking and resting state fMRI (rs-fMRI) data were collected from infant rhesus macaques, an important model of human social development, from birth through 6 months of age. Mean trajectories were fit for both datasets and individual trajectories from subjects with both eye-tracking and rs-fMRI data were used to test for brain-behavior relationships. Exploratory findings showed infants with greater increases in FC between left V1 to V3 visual areas have an earlier increase in eye-looking before 2 months. This relationship was moderated by social status such that infants with low social status had a stronger association between left V1 to V3 connectivity and eye-looking than high status infants. Results indicated that maturation of the visual object pathway may provide an important neural substrate supporting adaptive transitions in social visual attention during infancy.

Effects of social complexity and gender on social and non-social attention in male and female autistic children: A comparison of four eye-tracking paradigms.

Eye tracking has long been used to characterize differences in social attention between autistic and non-autistic children, but recent work has shown that these patterns may vary widely according to the biological sex of the participants and the social complexity and gender-typicality of the eye tracking stimuli (e.g., barbies vs. transformers). To better understand effects of sex, social complexity, and object gender-typicality on social and non-social gaze behavior in autism, we compared the visual attention patterns of 67 autistic (ASD) and non-autistic (NA) males (M) and females (F) (ASD M=21; ASD F=18; NA M=14; NA F=14) across four eye tracking paradigms varying in social complexity and object gender-typicality. We found consistency across paradigms in terms of overall attention and attention to social stimuli, but attention to objects varied when paradigms considered gender in their stimulus design. Children attended more to gendered objects, particularly when the gender-typicality of the object matched their assigned sex. These results demonstrate that visual social attention in autism is affected by interactions between a child's biological sex, social scene complexity, and object gender-typicality and have broad implications for the design and interpretation of eye tracking studies.

Abnormal visual attention to simple social stimuli in 4-month-old infants at high risk for Autism

Despite an increasing interest in detecting early signs of Autism Spectrum Disorders (ASD), the pathogenesis of the social impairments characterizing ASD is still largely unknown. Atypical visual attention to social stimuli is a potential early marker of the social and communicative deficits of ASD. Some authors hypothesized that such impairments are present from birth, leading to a decline in the subsequent typical functioning of the learning-mechanisms. Others suggested that these early deficits emerge during the transition from subcortically to cortically mediated mechanisms, happening around 2–3 months of age. The present study aimed to provide additional evidence on the origin of the early visual attention disturbance that seems to characterize infants at high risk (HR) for ASD. Four visual preference tasks were used to investigate social attention in 4-month-old HR, compared to low-risk (LR) infants of the same age. Visual attention differences between HR and LR infants emerged only for stimuli depicting a direct eye-gaze, compared to an adverted eye-gaze. Specifically, HR infants showed a significant visual preference for the direct eye-gaze stimulus compared to LR infants, which may indicate a delayed development of the visual preferences normally observed at birth in typically developing infants. No other differences were found between groups. Results are discussed in the light of the hypotheses on the origins of early social visual attention impairments in infants at risk for ASD.

Assessment of the Autism Spectrum Disorder Based on Machine Learning and Social Visual Attention: A Systematic Review

The assessment of autism spectrum disorder (ASD) is based on semi-structured procedures addressed to children and caregivers. Such methods rely on the evaluation of behavioural symptoms rather than on the objective evaluation of psychophysiological underpinnings. Advances in research provided evidence of modern procedures for the early assessment of ASD, involving both machine learning (ML) techniques and biomarkers, as eye movements (EM) towards social stimuli. This systematic review provides a comprehensive discussion of 11 papers regarding the early assessment of ASD based on ML techniques and children’s social visual attention (SVA). Evidences suggest ML as a relevant technique for the early assessment of ASD, which might represent a valid biomarker-based procedure to objectively make diagnosis. Limitations and future directions are discussed.

Social-Pragmatic Inferencing, Visual Social Attention and Physiological Reactivity to Complex Social Scenes in Autistic Young Adults

This study examined social-pragmatic inferencing, visual social attention and physiological reactivity to complex social scenes. Participants were autistic young adults (n = 14) and a control group of young adults (n = 14) without intellectual disability. Results indicate between-group differences in social-pragmatic inferencing, moment-level social attention and heart rate variability (HRV) reactivity. A key finding suggests associations between increased moment-level social attention to facial emotion expressions, better social-pragmatic inferencing and greater HRV suppression in autistic young adults. Supporting previous research, better social-pragmatic inferencing was found associated with less autistic traits.

Looking for a Deal?

Whereas social visual attention has been examined in computer-mediated (e.g., shared screen) or video-mediated (e.g., FaceTime) interaction, it has yet to be studied in mixed-media interfaces that combine video of the conversant along with other UI elements. We analyzed eye gaze of 37 dyads (74 participants) who were tasked with negotiating the price of a new car (as a buyer and seller) using mixed-media video conferencing under competitive or cooperative negotiation instructions (experimental manipulation). We used multidimensional recurrence quantification analysis to extract spatio-temporal patterns corresponding to mutual gaze (individuals look at each other), joint attention (individuals focus on the same elements of the interface), and gaze aversion (an individual looks at their partner, who is looking elsewhere). Our results indicated that joint attention predicted the sum of points attained by the buyer and seller (i.e., the joint score). In contrast, gaze aversion was associated with faster time to complete the negotiation, but with a lower joint score. Unexpectedly, mutual gaze was highly infrequent and unrelated to the negotiation outcomes and none of the gaze patterns predicted subjective perceptions of the negotiation. There were also no effects of gender composition or negotiation condition on the gaze patterns or negotiation outcomes. Our results suggest that social visual attention may operate differently in mixed-media collaborative interfaces than in face-to-face interaction. As mixed-media collaborative interfaces gain prominence, our work can be leveraged to inform the design of gaze-sensitive user interfaces that support remote negotiations among other tasks.

Comorbidity Matters: Social Visual Attention in a Comparative Study of Autism Spectrum Disorder, Attention-Deficit/Hyperactivity Disorder and Their Comorbidity.

Autism Spectrum Disorder (ASD) and Attention-Deficit/Hyperactivity Disorder (ADHD) represent two common neurodevelopmental disorders with considerable co-occurrence. Their comorbidity (ASD + ADHD) has been included in the latest diagnostic guidelines (DSM-V, 2013). The present study focuses on social visual attention that i) is a main aspect of social attention reflecting social cognition and ii) its atypicalities have been suggested as a potential biomarker for ASD. Considering the possible shared background of both disorders and their comorbidity, it is important to compare such traits directly. Here, 73 children and adolescents paired for age and IQ diagnosed with ASD (N = 12), ADHD (N = 21), comorbid ASD + ADHD (N = 15), and “typically developing” (TD) controls (N = 25), were shown static real-life social scenes while their gaze movements were recorded with eye-tracking. Scenes with two levels of social complexity were presented: low complexity (one person depicted) and high (four interacting individuals). Gaze fixation variables were investigated. Fixation duration on faces was significantly reduced only in ASD + ADHD which also required longer time to fixate all faces at least once. Fixation duration on faces in ASD was reduced, compared to TD, only when looking at scenes with high versus low social complexity. ADHD individuals did not differ from TD. Concluding, the observed alterations of social visual attention support the existence of possible dysfunctional particularities differentiating ASD, ADHD, and ASD + ADHD, which can be revealed with the new method of eye-tracking technique. The objective gaze measurements provided contribute to the development of biomarkers enabling early diagnosis, amelioration of care and further interventions specified for each group.

Visual Attention Patterns Differ in Dog vs. Cat Interactions With Children With Typical Development or Autism Spectrum Disorders.

Visual social attention is an important part of the social life of many species, including humans, but its patterning may vary between species. Studies on human–pet relationships have revealed that visual attention is also part of such interspecific interactions and that pets are sensitive to the human visual attentional state. It has been argued that domestication and/or repeated experiences with humans have shaped and refined these decoding abilities. Little is known on how the species’ evolutionary history may play a role in determining visual attention patterns during interactions, nor how the human’s own social skills may influence the animal’s attention patterns in human–animal interactions. In the present study, we investigated the visual attention patterns directed to the partner in dog–child and cat–child interactions in their home environment. We also compared these patterns between a group of children with autism spectrum disorders (ASD) and children with typical development. We found that the attention patterns differed according to species, with dogs displaying more gazes and cats more glances toward their human interlocutor, while children showed gazes toward both species. Only slight differences were observed according to the developmental status of children: ASD children displayed much more visual attention with their pet cat than with their pet dog and the same amount of visual attention toward their pet, whatever the species, as typically developing (TD) children. Because humans rely a lot upon visual communication in their own social encounters, where direct gazes play a major role from early on, they may be especially sensitive to the gazing behavior of their dogs. People with ASD, with a less typical pattern of interaction, may be more comfortable with the less “invasive” short glances of cats. These results suggest not only that interspecific communication has to be associated with processing and storing the other species’ ways of communicating in order to be successful but also that visual attention patterns during interactions, even when interspecific, are, for a large part, the result of the species’ own evolutionary history.

Diminished social attention in pediatric brain tumor survivors: Using eye tracking technology during naturalistic social perception.

The etiology of pediatric brain tumor survivor (PBTSs) social difficulties is not well understood. A model of social competence for youth with brain disorder and evidence from youth with autism spectrum disorder (ASD) suggests that diminished social attention may underlie social deficits in PBTSs. This study used eye tracking technology to compare visual social attention in PBTSs, youth with ASD, and typically developing (TD) youth. Participants included 90 age-, gender-, and IQ-matched youth (N = 30 per group). PBTSs were at least 5 years from diagnosis and 2 years from the completion of tumor-directed therapy. Participants' eye gaze patterns were recorded while watching an established social play paradigm that presented videos of children engaging in either interactive or parallel play. Group differences in proportional gaze duration toward social versus nonsocial areas of interest were compared. Medical correlates of social attention in PBTSs were evaluated. Groups significantly differed in gaze preference across conditions, with PBTSs looking less at social areas of interest than TD youth and in a manner comparable to youth with ASD. Among PBTSs, multimodal tumor-directed therapy was associated with reduced gaze preference for faces. This study provides the first evidence of disrupted social attention in PBTSs, with parallels to the social attention deficits observed in ASD. Findings offer a new way to conceptualize the social difficulties of PBTSs and could guide interventions aimed at improving PBTS social adjustment by increasing visual attention to socially relevant information during social interactions. (PsycINFO Database Record (c) 2020 APA, all rights reserved).

The Characteristics of Intelligence Profile and Eye Gaze in Facial Emotion Recognition in Mild and Moderate Preschoolers With Autism Spectrum Disorder.

Childhood autism spectrum disorder (ASD) can easily be misdiagnosed, due to the nonspecific social and communicational deficits associated with the disorder. The present study attempted to profile the mental development and visual attention toward emotion among preschool children with mild or moderate ASD who were attending mainstream kindergartens. A total of 21 children (17 boys and 4 girls) diagnosed with mild or moderate ASD selected from 5,178 kindergarteners from the Xi’an city were recruited. Another group of 21 typically developing (TD) children who were matched with age, gender, and class served as controls. All children were assessed using the Griffiths Mental Development Scales–Chinese (GDS-C), and their social visual attention was assessed during watching 20 ecologically valid film scenes by using eye tracking technique. The results showed that ASD children had lower mental development scores in the Locomotor, Personal-Social, Language, Performance, and Practical Reasoning subscales than the TD peers. Moreover, deficits in recognizing emotions from facial expressions based on naturalistic scene stimuli with voice were found for ASD children. The deficits were significantly correlated with their ability in social interaction and development quotient in ASD group. ASD children showed atypical eye-gaze pattern when compared to TD children during facial emotion expression task. Children with ASD had reduced visual attention to facial emotion expression, especially for the eye region. The findings confirmed the deficits of ASD children in real life multimodal of emotion recognition, and their atypical eye-gaze pattern for emotion recognition. Parents and teachers of children with mild or moderate ASD should make informed educational decisions according to their level of mental development. In addition, eye tracking technique might clinically help provide evidence diagnosing children with mild or moderate ASD.

Social complexity and the early social environment affect visual social attention to faces.

Diminished attention to socially relevant information appears to be an early emerging risk factor associated with autism spectrum disorders (ASD). However, inconsistencies across studies suggest that atypicalities in visual social attention in infants at high-risk for ASD during the first postnatal year may be subtle and more apparent under certain contexts. Here we explore factors that may moderate developmental trajectories in attention to faces, including the social complexity of the dynamic visual stimuli used to measure visual social attention and the early social environment of the infant as indexed by parental affectedness of ASD-related traits. Across infants at both high (HR) and low risk for ASD, attention to faces increased during the first postnatal year, with overall greater attention being allocated to schematic faces in the simpler video stimulus. Moreover, greater parental affectedness of ASD-related traits was associated with reduced developmental gains in attention to faces. For HR infants, greater attention to faces was positively associated with social communicative competence, including better joint attention skills and lower social impairments. Altogether, our findings highlight the importance of considering developmental level when selecting stimuli to longitudinally examine visual social attention, and the clinical relevance of including measures of infant's social environment in understanding early markers of ASD risk. Autism Res 2019, 12: 445-457 © 2019 International Society for Autism Research, Wiley Periodicals, Inc. LAY SUMMARY: Attention to faces is an important means for infants to learn about the social world. The complexity of the social scene and an infant's early social environment both affect the amount of time infants at high- and low-risk for ASD look at faces during the first postnatal year. For infants at high-risk for ASD, greater attention to faces was associated with better social skills. Understanding an infant's social environment may have a positive impact on social communicative development.

Mechanisms of impairments in visual social attention in autism spectrum disorders

Atypical visual social attention and cortical activation have been documented in autism spectrum disorders, yet the source of this deficit remains unclear. We tried to review three perspectives about mechanisms of such impairments: atypical sensory processing, social deficit and Bayesian model. Among these perspectives, Bayesian model is a comprehensive one that explains abnormal social attention in ASD group in a bottom-up and top-down manner. It is unknown, however, whether Bayesian model can be recognized as a unified model that accounts for abnormal social attention in individuals with ASD. Finally, we offered some insights to future studies on social attention in ASD. Future research should test different theories from various levels and find effective behavioral and neurocognitive markers for early diagnosis. It is a priority to take advantage of these theories or hypotheses to develop intervention and treatment tools, which may help to ameliorate ASD group’s social attention, and further, social functioning.

Oxytocin, vasopressin, and primate behavior: Diversity and insight.

It has become increasingly clear that the nonapeptide hormones oxytocin and vasopressin have more diverse behavioral and physiological effects across species and across individuals than was initially recognized. To reflect this variation, we would like to introduce our Special Issue, entitled Oxytocin and Vasopressin in Primate Behavior, by celebrating the diversity that is found across the articles within it. While every article directly addresses the topic of this Special Issue, they also vary in many characteristics: the species studied, the methods used, and the perspectives taken. By highlighting the interesting ways in which these articles differ from one another, we can gain unique insights into the subject that ties them together: our understanding of oxytocin and vasopressin and the behavior of primates. Nonhuman primates are critical intermediates between rodents and humans and are the best models for human biology and behavior, especially with respect to complex cognitive social constructs, such as visual social attention, face processing, and vocal communication. While rodent studies have laid an important and foundational framework for our understanding of nonapeptides, brains, and behavior, these studies cannot fully recapitulate human phenomena. Therefore, we hope the articles presented here contribute to a greater understanding on the role of oxytocin and vasopressin in primate physiology and behavior and help to further advance the application of this knowledge to human biology.

Improving sensitivity to eye gaze cues in autism using serious game technology: study protocol for a phase I randomised controlled trial

IntroductionAutism spectrum disorder (ASD) is characterised by impairments in social communication. Core symptoms are deficits in social looking behaviours, including limited visual attention to faces and sensitivity to eye gaze...