Eyetracking of social preference choices reveals normal but faster processing in autism.
ABSTRACT: People with Autism Spectrum Disorder (ASD) have been reported to show atypical attention and evaluative processing, in particular for social stimuli such as faces. The usual measure in these studies is an explicit, subjective judgment, which is the culmination of complex-temporally extended processes that are not typically dissected in detail. Here we addressed a neglected aspect of social decision-making in order to gain further insight into the underlying mechanisms: the temporal evolution of the choice. We investigated this issue by quantifying the alternating patterns of gaze onto faces, as well as nonsocial stimuli, while subjects had to decide which of the two stimuli they preferred. Surprisingly, the temporal profile of fixations relating to choice (the so-called "gaze cascade") was entirely normal in ASD, as were the eventual preference choices. Despite these similarities, we found two key abnormalities: people with ASD made choices more rapidly than did control subjects across the board, and their reaction times for social preference judgments were insensitive to choice difficulty. We suggest that ASD features an altered decision-making process when basing choice on social preferences. One hypothesis motivated by these data is that a choice criterion is reached in ASD regardless of the discriminability of the options.
Project description:The present investigation describes three studies testing the hypothesis that children with Autism Spectrum Disorder (ASD) show an atypical preference for non-social stimuli. Preference for non-social and social stimuli was assessed using applications on a portable tablet computer. Twenty-eight children with ASD were matched on developmental age with the chronological age of 41 typically developing (TD) children. The non-social stimuli consisted of six different films of abstract moving geometric patterns. Social stimuli were six different films of the face of young adults (Study 1 and 3) or six films of different dogs' faces (Study 2). When given a choice between the non-social and social stimuli, children with ASD preferred the non-social stimuli. When the human faces were replaced with dogs' faces the participants with ASD continued to prefer the non-social stimuli. A high reinforcement value of non-social stimuli was also demonstrated when the non-social stimuli were presented alone, suggesting the preference for the non-social stimuli was not simply an avoidance of social stimuli. Whenever an infant prefers non-social stimuli over social stimuli, non-typical development in social communication and social interests may result, together with the development of high levels and frequently occurring stereotyped and repetitive behavior. These behaviors define Autism.
Project description:Background:Visual atypicalities in autism spectrum disorder (ASD) are a well documented phenomenon, beginning as early as 2-6 months of age and manifesting in a significantly decreased attention to the eyes, direct gaze and socially salient information. Early emerging neurobiological deficits in perceiving social stimuli as rewarding or its active avoidance due to the anxiety it entails have been widely purported as potential reasons for this atypicality. Parallel research evidence also points to the significant benefits of animal presence for reducing social anxiety and enhancing social interaction in children with autism. While atypicality in social attention in ASD has been widely substantiated, whether this atypicality persists equally across species types or is confined to humans has not been a key focus of research insofar. Methods:We attempted a comprehensive examination of the differences in visual attention to static images of human and animal faces (40 images; 20 human faces and 20 animal faces) among children with ASD using an eye tracking paradigm. 44 children (ASD n = 21; TD n = 23) participated in the study (10,362 valid observations) across five regions of interest (left eye, right eye, eye region, face and screen). Results:Results obtained revealed significantly greater social attention across human and animal stimuli in typical controls when compared to children with ASD. However in children with ASD, a significantly greater attention allocation was seen to animal faces and eye region and lesser attention to the animal mouth when compared to human faces, indicative of a clear attentional preference to socially salient regions of animal stimuli. The positive attentional bias toward animals was also seen in terms of a significantly greater visual attention to direct gaze in animal images. Conclusion:Our results suggest the possibility that atypicalities in social attention in ASD may not be uniform across species. It adds to the current neural and biomarker evidence base of the potentially greater social reward processing and lesser social anxiety underlying animal stimuli as compared to human stimuli in children with ASD.
Project description:Individuals' gaze behavior reflects the choice they will ultimately make. For example, people confronting a choice among multiple stimuli tend to look longer at stimuli that are subsequently chosen than at other stimuli. This tendency, called the gaze bias effect, is a key aspect of visual decision-making. Nevertheless, no study has examined the generality of the gaze bias effect in older adults. Here, we used a two-alternative forced-choice task (2AFC) to compare the gaze behavior reflective of different stages of decision processes demonstrated by younger and older adults. Participants who had viewed two faces were instructed to choose the one that they liked/disliked or the one that they judged to be more/less similar to their own face. Their eye movements were tracked while they chose. The results show that the gaze bias effect occurred during the remaining time in both age groups irrespective of the decision type. However, no gaze bias effect was observed for the preference judgment during the first dwell time. Our study demonstrated that the gaze bias during the remaining time occurred regardless of decision-making task and age. Further study using diverse participants, such as clinic patients or infants, may help to generalize the gaze bias effect and to elucidate the mechanisms underlying the gaze bias.
Project description:Reduced attentional preference for faces and symptoms of social anxiety are common in autism spectrum disorders (ASDs). The neuropeptide oxytocin triggers anxiolytic functions and enhances eye gaze, facial emotion recognition and neural correlates of face processing in ASD. Here we investigated whether a single dose of oxytocin increases attention to faces in ASD. As a secondary question, we explored the influence of social anxiety on these effects. We tested for oxytocin's effects on attention to neutral faces as compared to houses in a sample of 29 autistic individuals and 30 control participants using a dot-probe paradigm with two different presentation times (100 or 500 ms). A single dose of 24 IU oxytocin was administered in a randomized, double-blind placebo-controlled, cross-over design. Under placebo, ASD individuals paid less attention to faces presented for 500 ms than did controls. Oxytocin administration increased the allocation of attention toward faces in ASD to a level observed in controls. Secondary analyses revealed that these oxytocin effects primarily occurred in ASD individuals with high levels of social anxiety who were characterized by attentional avoidance of faces under placebo. Our results confirm a positive influence of intranasal oxytocin on social attention processes in ASD. Further, they suggest that oxytocin may in particular restore the attentional preference for facial information in ASD individuals with high social anxiety. We conclude that oxytocin's anxiolytic properties may partially account for its positive effects on socio-cognitive functioning in ASD, such as enhanced eye gaze and facial emotion recognition.
Project description:Importance:Enhanced selective attention toward nonsocial objects and impaired attention to social stimuli constitute key clinical features of autism spectrum disorder (ASD). Yet, the mechanisms associated with atypical selective attention in ASD are poorly understood, which limits the development of more effective interventions. In typically developing individuals, selective attention to social and nonsocial stimuli is associated with the informational value of the stimuli, which is typically learned over the course of repeated interactions with the stimuli. Objective:To examine value learning (VL) of social and nonsocial stimuli and its association with selective attention in preschoolers with and without ASD. Design, Setting, and Participants:This case-control study compared children with ASD vs children with developmental delay (DD) and children with typical development (TD) recruited between March 3, 2017, and June 13, 2018, at a university-based research laboratory. Participants were preschoolers with ASD, DD, or TD. Main Outcomes and Measures:Procedure consisted of an eye-tracking gaze-contingent VL task involving social (faces) and nonsocial (fractals) stimuli and consisting of baseline, training, and choice test phases. Outcome measures were preferential attention to stimuli reinforced (high value) vs not reinforced (low value) during training. The hypotheses were stated before data collection. Results:Included were 115 preschoolers with ASD (n?=?48; mean [SD] age, 38.30 [15.55] months; 37 [77%] boys), DD (n?=?31; mean [SD] age, 45.73 [19.49] months; 19 [61%] boys), or TD (n?=?36; mean [SD] age, 36.53 [12.39] months; 22 [61%] boys). The groups did not differ in sex distribution; participants with ASD or TD had similar chronological age; and participants with ASD or DD had similar verbal IQ and nonverbal IQ. After training, the ASD group showed preference for the high-value nonsocial stimuli (mean proportion, 0.61 [95% CI, 0.56-0.65]; P?<?.001) but not for the high-value social stimuli (mean proportion, 0.51 [95% CI, 0.46-0.56]; P?=?.58). In contrast, the DD and TD groups demonstrated preference for the high-value social stimuli (DD mean proportion, 0.59 [95% CI, 0.54-0.64]; P?=?.001 and TD mean proportion, 0.57 [95% CI, 0.53-0.61]; P?=?.002) but not for the high-value nonsocial stimuli (DD mean proportion, 0.52 [95% CI, 0.44-0.59]; P?=?.64 and TD mean proportion, 0.50 [95% CI, 0.44-0.57]; P?=?.91). Controlling for age and nonverbal IQ, autism severity was positively correlated with enhanced learning in the nonsocial domain (r?=?0.22; P?=?.03) and with poorer learning in the social domain (r?=?-0.26; P?=?.01). Conclusions and Relevance:Increased attention to objects in preschoolers with ASD may be associated with enhanced VL in the nonsocial domain. When paired with poor VL in the social domain, enhanced value-driven attention to objects may play a formative role in the emergence of autism symptoms by altering attentional priorities and thus learning opportunities in affected children.
Project description:Gaze direction is a common social cue implying potential interpersonal interaction. However, little is known about the neural processing of social decision making influenced by perceived gaze direction. Here, we employed functional magnetic resonance imaging (fMRI) method to investigate 27 females when they were engaging in an economic exchange game task during which photos of direct or averted eye gaze were shown. We found that, when averted but not direct gaze was presented, prosocial vs. selfish choices were associated with stronger activations in the right superior temporal gyrus (STG) as well as larger functional couplings between right STG and the posterior cingulate cortex (PCC). Moreover, stronger activations in right STG was associated with quicker actions for making prosocial choice accompanied with averted gaze. The findings suggest that, when the cue implying social contact is absent, the processing of understanding others' intention and the relationship between self and others is more involved for making prosocial than selfish decisions. These findings could advance our understanding of the roles of subtle cues in influencing prosocial decision making, as well as shedding lights on deficient social cue processing and functioning among individuals with autism spectrum disorder (ASD).
Project description:A key functional effect of intranasal oxytocin with potential therapeutic relevance for autism-spectrum disorder is its reported facilitation of attention towards social stimuli, notably the eye region of faces. In the current randomized placebo-controlled within-subject experiment on 40 healthy males, we investigated the robustness of this facilitation of attention by intranasal oxytocin (24IU) towards social cues. Eye-tracking measures of preference for dynamic and static social vs. non-social stimuli were taken in four different paradigms where autistic individuals tend to exhibit reduced interest in social stimuli. Additionally, we investigated whether oxytocin increases attention towards the eyes relative to other salient face regions in an emotional face paradigm. Results showed that the time spent viewing both dynamic and static social vs. non-social stimuli was negatively associated with trait autism and significantly increased following intranasal oxytocin. For face stimuli, oxytocin primarily increased gaze towards the eyes of fearful expression faces but not for other face emotions. Overall, our findings demonstrate that oxytocin significantly shifts gaze preference towards social vs. non-social stimuli and to the eyes of fearful faces. Importantly, oxytocin appears generally to shift attention more towards salient social stimuli of particular relevance in the context of autism providing further support for its potential therapeutic use in autism-spectrum disorder.
Project description: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.
Project description:Social interaction in individuals with Autism Spectrum Disorder (ASD) is characterized by qualitative impairments that highly impact quality of life. Bayesian theories in ASD frame an understanding of underlying mechanisms suggesting atypicalities in the evaluation of probabilistic links within the perceptual environment of the affected individual. To address these theories, the present study explores the applicability of an innovative Bayesian framework on social visual perception in ASD and demonstrates the use of gaze transitions between different parts of social scenes. We applied advanced analyses with Bayesian Hidden Markov Modeling (BHMM) to track gaze movements while presenting real-life scenes to typically developing (TD) children and adolescents (N = 25) and participants with ASD and Attention-Deficit/Hyperactivity Disorder (ASD+ADHD, N = 15) and ASD without comorbidity (ASD, N = 12). Regions of interest (ROIs) were generated by BHMM based both on spatial and temporal gaze behavior. Social visual perception was compared between groups using transition and fixation variables for social (faces, bodies) and non-social ROIs. Transition variables between faces, namely gaze transitions between faces and likelihood of linking faces, were reduced in the ASD+ADHD compared to TD participants. Fixation count to faces was also reduced in this group. The ASD group showed similar performance to TD in the studied variables. There was no difference between groups for non-social ROIs. Our study provides an innovative, interpretable example of applying Bayesian theories of social visual perception in ASD. BHMM analyses and gaze transitions have the potential to reveal fundamental social perception components in ASD, contributing thus to amelioration of social-skill interventions.
Project description:Although previous research has characterized the important role for spatial and affective pre-cues in the control of visual attention, less is known about the impact of pre-cues on preference formation. In preference formation, the gaze cascade phenomenon suggests that the gaze serves both to enhance and express "liking" during value-based decision-making. This phenomenon has been interpreted as a type of Pavlovian approach toward preferred objects. Decision-making here reflects a process of gradual commitment in which the gaze functions as a precursor to choice; by this account, overt attention produces a necessarily positive, additive effect on the value of the attended object. The implication is that drawing attention to an object should initiate, and therefore promote, preference formation for that object. Alternatively, information-integration models of attention propose that attention produces a multiplicative effect on the value of the attended object, implying that negative information can impede preference formation. To pitch the gradual-commitment hypothesis against the information-integration hypothesis, we conducted four experiments that combined the spatial-cueing paradigm with a value-based choice paradigm. In each trial in all experiments, subjects were presented with an irrelevant, peripheral pre-cue for a duration of 500 ms, followed by a 500 ms blank, and then a pair of abstract images (one at the pre-cued position; one in the opposite hemifield). The subjects were asked to choose their preferred abstract image by pressing the corresponding button. We manipulated the type of pre-cues (images of faces versus foods; with varying affective associations) and the time constraints (a deadline of 1,500 ms versus self-paced). Overall, the choice data showed a clear pattern of influence from the pre-cues, such that, given a deadline, abstract images were chosen less often if they had been preceded by a pre-cue with a negative affective association (both for face and food images). Analyses of the gaze data showed the emergence of significant gaze biases in line with the subjects' choices. Taken together, the data pattern provided support for the information-integration hypothesis, particularly under urgency. When tasked with a speeded preference choice, subjects showed affective disengagement following pre-cues that carried a negative association.