Dataset Information

Look me in the eyes: constraining gaze in the eye-region provokes abnormally high subcortical activation in autism.

ABSTRACT: Individuals with Autism Spectrum Disorder (ASD) seem to have difficulties looking others in the eyes, but the substrate for this behavior is not well understood. The subcortical pathway, which consists of superior colliculus, pulvinar nucleus of the thalamus, and amygdala, enables rapid and automatic face processing. A specific component of this pathway - i.e., the amygdala - has been shown to be abnormally activated in paradigms where individuals had to specifically attend to the eye-region; however, a direct examination of the effect of manipulating the gaze to the eye-regions on all the components of the subcortical system altogether has never been performed. The subcortical system is particularly important as it shapes the functional specialization of the face-processing cortex during development. Using functional MRI, we investigated the effect of constraining gaze in the eye-region during dynamic emotional face perception in groups of participants with ASD and typical controls. We computed differences in activation in the subcortical face processing system (superior colliculus, pulvinar nucleus of the thalamus and amygdala) for the same stimuli seen freely or with the gaze constrained in the eye-region. Our results show that when constrained to look in the eyes, individuals with ASD show abnormally high activation in the subcortical system, which may be at the basis of their eye avoidance in daily life.

SUBMITTER: Hadjikhani N

PROVIDER: S-EPMC5466661 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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Publications

Look me in the eyes: constraining gaze in the eye-region provokes abnormally high subcortical activation in autism.

Hadjikhani Nouchine N Åsberg Johnels Jakob J Zürcher Nicole R NR Lassalle Amandine A Guillon Quentin Q Hippolyte Loyse L Billstedt Eva E Ward Noreen N Lemonnier Eric E Gillberg Christopher C

Scientific reports 20170609 1

Individuals with Autism Spectrum Disorder (ASD) seem to have difficulties looking others in the eyes, but the substrate for this behavior is not well understood. The subcortical pathway, which consists of superior colliculus, pulvinar nucleus of the thalamus, and amygdala, enables rapid and automatic face processing. A specific component of this pathway - i.e., the amygdala - has been shown to be abnormally activated in paradigms where individuals had to specifically attend to the eye-region; ho ...[more]

PMID: 28600558

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Project description:BackgroundShifts in eye gaze communicate social information that allows people to respond to another's behavior, interpret motivations driving behavior, and anticipate subsequent behavior. Understanding the social communicative nature of gaze shifts requires the ability to link eye movements and mental state information about objects in the world. Autism spectrum disorder (ASD) is characterized by atypical sensitivity to eye gaze cues, which impacts social communication and relationships. We evaluated whether reduced visual attention to faces explains this difficulty in ASD.MethodsWe employed eye-tracking technology to measure visual attention to faces and gazed-at objects in a 4-alternative forced choice paradigm in adolescents with ASD and typically developing (TD) adolescents. Participants determined the target object that an actor was looking at in ecologically rich scenes. We controlled for group differences in task engagement and data quality.ResultsIn the Gaze Following task, adolescents with ASD were relatively impaired (Cohen's d = 0.63) in the ability to identify the target object. In contrast to predictions, both groups exhibited comparable fixation durations to faces and target objects. Among both groups, individuals who looked longer at the target objects, but not faces, performed better in the task. Finally, among the ASD group, parent SSIS-Social Skills ratings were positively associated with performance on the Gaze Following task. In the Gaze Perception task, there was a similar pattern of results, which provides internal replication of the findings that visual attention to faces is not related to difficulty interpreting eye gaze cues. Together, these findings indicate that adolescents with ASD are capable of following gaze, but have difficulty linking gaze shifts with mental state information.LimitationsAdditional work is necessary to determine whether these findings generalize to individuals across the full autism spectrum. New paradigms that manipulate component processes of eye gaze processing need to be tested to confirm these interpretations.ConclusionsReduced visual attention to faces does not appear to contribute to atypical processing of eye gaze cues among adolescents with ASD. Instead, the difficulty for individuals with ASD is related to understanding the social communicative aspects of eye gaze information, which may not be extracted from visual cues alone.

Project description:Eye gaze is a ubiquitous cue in child-caregiver interactions, and infants are highly attentive to eye gaze from very early on. However, the question of why infants show gaze-sensitive behavior, and what role this sensitivity to gaze plays in their language development, is not yet well-understood. To gain a better understanding of the role of eye gaze in infants' language learning, we conducted a broad systematic review of the developmental literature for all studies that investigate the role of eye gaze in infants' language development. Across 77 peer-reviewed articles containing data from typically developing human infants (0-24 months) in the domain of language development, we identified two broad themes. The first tracked the effect of eye gaze on four developmental domains: (1) vocabulary development, (2) word-object mapping, (3) object processing, and (4) speech processing. Overall, there is considerable evidence that infants learn more about objects and are more likely to form word-object mappings in the presence of eye gaze cues, both of which are necessary for learning words. In addition, there is good evidence for longitudinal relationships between infants' gaze following abilities and later receptive and expressive vocabulary. However, many domains (e.g., speech processing) are understudied; further work is needed to decide whether gaze effects are specific to tasks, such as word-object mapping or whether they reflect a general learning enhancement mechanism. The second theme explored the reasons why eye gaze might be facilitative for learning, addressing the question of whether eye gaze is treated by infants as a specialized socio-cognitive cue. We concluded that the balance of evidence supports the idea that eye gaze facilitates infants' learning by enhancing their arousal, memory, and attentional capacities to a greater extent than other low-level attentional cues. However, as yet, there are too few studies that directly compare the effect of eye gaze cues and non-social, attentional cues for strong conclusions to be drawn. We also suggest that there might be a developmental effect, with eye gaze, over the course of the first 2 years of life, developing into a truly ostensive cue that enhances language learning across the board.

Project description:BackgroundAvoidance to look others in the eye is a characteristic symptom of Autism Spectrum Disorders (ASD), and it has been hypothesised that quantitative monitoring of gaze patterns could be useful to objectively evaluate treatments. However, tools to measure gaze behaviour on a regular basis at a manageable cost are missing. In this paper, we investigated whether a smartphone-based tool could address this problem. Specifically, we assessed the accuracy with which the phone-based, state-of-the-art eye-tracking algorithm iTracker can distinguish between gaze towards the eyes and the mouth of a face displayed on the smartphone screen. This might allow mobile, longitudinal monitoring of gaze aversion behaviour in ASD patients in the future.ResultsWe simulated a smartphone application in which subjects were shown an image on the screen and their gaze was analysed using iTracker. We evaluated the accuracy of our set-up across three tasks in a cohort of 17 healthy volunteers. In the first two tasks, subjects were shown different-sized images of a face and asked to alternate their gaze focus between the eyes and the mouth. In the last task, participants were asked to trace out a circle on the screen with their eyes. We confirm that iTracker can recapitulate the true gaze patterns, and capture relative position of gaze correctly, even on a different phone system to what it was trained on. Subject-specific bias can be corrected using an error model informed from the calibration data. We compare two calibration methods and observe that a linear model performs better than a previously proposed support vector regression-based method.ConclusionsUnder controlled conditions it is possible to reliably distinguish between gaze towards the eyes and the mouth with a smartphone-based set-up. However, future research will be required to improve the robustness of the system to roll angle of the phone and distance between the user and the screen to allow deployment in a home setting. We conclude that a smartphone-based gaze-monitoring tool provides promising opportunities for more quantitative monitoring of ASD.

Dataset Information

Look me in the eyes: constraining gaze in the eye-region provokes abnormally high subcortical activation in autism.

Publications

Look me in the eyes: constraining gaze in the eye-region provokes abnormally high subcortical activation in autism.

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