Eyes and Autism
Atypical Eye Gaze Behavior in Autism Spectrum Disorders
By Jisu Lee
Emory Class of 2020
From a neonatal period, eyes serve as important receptors for social and communicative information.1 Accordingly, avoidance of eye contact with others can lead to absence of constant social and emotional learning opportunities, which can adversely influence future social cognitive development.2 Unlike neurotypically developing children who preferentially look at other people’s eyes and socially salient information, children with autism prefer to direct their eye gaze on less socially relevant features of the environment.3 Later in adolescence and adulthood, atypical eye gaze behavior also poses significant challenges for individuals with autism to navigate real-world social situations.4 Thus, eye-tracking technology has received considerable research and clinical attention in the past decades to examine altered looking patterns in individuals with autism. A central goal of this paper is to examine how people with Autism Spectrum Disorder (ASD) may understand and interpret social world differently from neurotypical individuals displayed by their atypical eye gaze behaviors. Throughout the paper, three research questions: “How does atypical eye gaze behavior in autism relate to altered social engagement?” “What is the current debate on insisting eye contact to individuals with ASD?” and “What are the implications of the eye-tracking technology in the field of autism research?” will be addressed.
The perception of faces and knowledge that faces can reveal internal states of other people are essential skills for typical social development.5 Particularly, the ability to process information about eyes and eye-gaze direction is vital because it allows joint attention 6 and eye contact, establishing the primary mode of communicative context and social interaction.5 Typically developing newborns look longer at eyes than at other features of the face,7 show preferential attention to faces with mutual gaze,5 and demonstrate the ability to imitate facial expressions of others.8 However, research has shown that individuals with autism display social communication deficits from a young age, characterized by impaired eye contact, gaze following, joint attention, and imitative behaviors. 9,10
Atypical visual fixation patterns, such as lack of eye contact with others during critical periods of development and looking at other aspects of the environment, indicate an altered route for learning about the social world.3 Diminished attention to social cues, such as eyes and faces, may disturb language learning process 11 and language deficit may negatively impact the ability to navigate the social environment.12 Furthermore, Pelphrey and colleagues (2002) found that adults with autism significantly looked more at nonsocial features of the face, such as chin or hairline as opposed to eyes, than neurotypical participants.13 In another study, where eye tracker technology was used during an interactive conversation, children with ASD fixated more often on the mouth than eyes during emotional conversations compared to topics that were less affective.14 The researcher of the study, Hutchins suggests that for individuals with ASD, talking about emotions is like “driving in a snowstorm” because it is very draining for their executive function and requires great effort. Thus, children with ASD are susceptible to miss out on a wealth of meaningful social cues provided through the eyes during conversational exchanges.14
There has been two contrasting explanations for reduced eye contact in autism: one is gaze aversion – avoiding others’ eyes due to negative emotional arousal – and another is gaze indifference – reduced eye contact from failure to understand that eyes are engaging or socially informative.16 Research has shown that when two-year-olds with autism were directly cued to look at the eyes, they did not look away faster than typically developing children and did not display gaze aversion with implicit social cues for eye contact.16 This finding contradicts the statement that children are actively avoiding eye contact due to aversion, but rather support the gaze indifference theory – insensitivity to grasp social significance in eye contact. On the other hand, making eye contact can be a distressful and sensory-taxing encounter for older individuals with ASD, and most neurotypical people are likely to interpret their avoidance of eye contact as rude or antisocial.15 When sixteen people with autism were asked to share their reasons for difficulties in eye contact, many answered that they feel overloaded processing information, anxious, physically painful, and unnatural to make eye contact with other people.15 While some older individuals with ASD report discomfort in making eye contact, research have implied that early intervention on learning social cues can help individuals meet social expectations for eye contact.17
As most first-person accounts of anxiety or aversion from eye-looking are reported in older children and adults, age consideration is crucial when examining eye gaze behaviors and responses. In fact, atypical autonomic and amygdala activity in response to eye gaze has been founded for older individuals with ASD. 18, 19 However, the aberrant affective responses to eye gaze may derive from developmental outcomes. For example, anxiety in people with ASD is found to be more prevalent with higher mean age,20 moderated by improved cognitive functioning.21 These findings suggest that reduced eye gaze in young children with ASD is unlikely a response from anxiety or hyperarousal, and that reduction of eye gazes at later ages may be due to atypical development of social brain networks.16 In this sense, autonomic hyperactivity in older population with ASD from eye-looking are secondary symptoms that develop from atypical learning processes.16
In therapeutic and educational contexts, interventions have targeted eye gaze behaviors based on the belief that lack of eye contact disturbs meaningful learning and acquisition of more advanced social skills.22 To meet this goal, researchers have conducted studies on applied behavior analysis, peer modeling, role-play, and imitation activities, from which they only found minor to moderate improvements in joint attention and eye-looking behaviors.22, 23, 24 The article by Stewart mentions that teachers and parents commonly use verbal cues, such as “Look at me,” repeatedly and forcefully to grab the attention of those with ASD who are not engaging in mutual gaze.25 In fact, many individuals with autism seem to become more proficient at eye-looking as they constantly learn about the social expectations regarding eye contact and get more comfortable in social situations.25 However, Stewart argues that the society needs to recognize how sensory, motor, and emotional abnormalities in ASD can influence the capacity to understand social situations and expectations. The article provides an account by a teacher who had a student with autism. Although the student only looked out the window and did not seem to pay attention, he was able to explain everything the teacher had said in class. Another account by a person with ASD reported that he can concentrate better at other people’s words without having to make eye contact. These examples from the article suggest that some individuals with autism struggle to receive and process information from multiple sensory inputs in addition to challenges with interpreting social cues.
The article by Stewart also implies that educators should consider and address the different learning styles of students. Just as how different people process, store, and carry out information in a dissimilar way, teachers need to acknowledge and respect that students with autism have unique styles of learning. For example, the student, who always looked out the window but displayed a good knowledge on the academic material, likely learned more effectively with auditory input. Although people may strongly encourage eye contact with that student, it is questionable whether he would gain meaningful social cues during that encounter and perceive the intended message. In other words, individuals with ASD may make efforts to look at the eyes of another person but not be able to comprehend the underlying social message. Thus, educators and therapists would need to consider the atypical ways that individuals with ASD learn information to accommodate and develop effective strategies.
Eye tracking device has long been used in psychology and neuroscience experiments to understand how humans process visual information. In the past two decades, many researchers have been using the eye tracking technology to study how people with ASD orient to different aspects of social scenes compared to neurotypical individuals.26 For example, Klin, Jones and Schultz (2002) measured the gaze of participants as they watched emotional scenes from the movie, Who’s Afraid of Virginia Woolf? which reflects complex social situations that people may encounter in daily life.27 The study discovered that individuals with autism looked at the actors’ mouths or irrelevant features in the periphery of the scene rather than the eyes. The study offered valuable information on how visual fixation patterns in autism are characterized by mouths, bodies, and objects and less on the eyes. Moreover, increased fixation on mouths predicted greater social competence, implying that individuals with ASD may achieve better understanding of social information via viewing the mouth rather than the eyes.
Unlike previous eye tracking studies, Norbury and colleagues (2009) discovered no significant difference in viewing patterns between teenagers with ASD and typically developing peers.1 However, researchers predicted that the typical viewing patterns of participants with ASD may be attributed to the learning outcome as all of their participants were enrolled in a full-time social skills training that emphasized eye contact. Nevertheless, typical viewing patterns evident in some participants with ASD do not necessarily imply that they are acquiring the same meaning from a visual stimuli as neurotypical subjects. This study also found that eye movement measures were not associated with social competence, contradicting the commonly accepted belief that eye contact is a vital precursor for successful communication. Another consistent finding that greater fixations to the mouth were associated with higher communication skills indicates that mouth may offer more explicit and reliable social communicative cues than the eyes for people on the autism spectrum.
Eye-tracking technology has also been used to examine altered looking patterns in toddlers with ASD to develop biomarkers for ASD diagnosis at a young age when interventions are most helpful.3, 26 One of the first eye tracking studies on infants with autism was conducted in 2008 when researchers studied Helen, a 15-month-old child in two eye-tracking paradigms. In the first study, she was shown a video of a woman engaging in friendly cooing sounds. Helen looked significantly more at the mouth than eyes.26 In the another paradigm that used point-light animation to display biological motions, typically developing infants demonstrated preferential fixation toward the upright figure rather than the inverted animation.26 On the other hand, toddlers who had autism were able to preferentially look at the upright version of the animation only when it occurred with a clapping action of the figure. Thus, these eye tracking findings imply that while neurotypical controls were able to connect the dots, perceive those displays as human figures, and preferentially orient to biological motions, children with ASD failed to impose social meanings in the dots. Thus, robust studies on eye movements comparing children with ASD to neurotypical subjects have suggested eye gaze abnormalities to be a key diagnostic feature of ASD.27 As the eye tracking technology offers cheap and quantifiable measures of social understanding, many experts are testing new paradigms to develop a reliable diagnostic measure for ASD.26
Over the past years, watching videos of social interactions has been recognized to be a naturalistic paradigm compared to static images in eye tracking studies. However, researchers have sought to extend eye tracking studies in a more naturalistic environment. For instance, Noris and colleagues (2011) utilized a wearable eye-tracker called, WearCam, to gather gaze information from the child’s viewpoint and conducted a study in a semi-structured social situation.28 The results from WearCam showed that children with ASD exhibited downcast eye movement and engaged in looking at their lateral field of view compared to neurotypical subjects. Although data collected in naturalistic social settings offer benefits over original paradigms that used static photographs, it is important to consider significant limitations for these techniques. The primary impediment of such techniques is associated with the presence of a camera that has to be positioned on the participant’s head to track their eye gaze behavior.28 This may potentially influence the final study results as comorbid symptoms of anxiety are frequently manifested in children with ASD and can interfere with their gaze patterns. Researchers have also raised concerns that the eye-tracker equipment may contribute to increase in participants’ anxiety and and lead to their downcast gaze phenomenon. 28, 29 Despite limitations in wearable eye-tracker devices, future research in this technology will further advance our understanding of how children with ASD perceive the social world and provide another reliable measure of where and what children with ASD are looking at in their daily routines.29
Based on the implications from the eye-tracking studies, atypical eye gaze behaviors evident in ASD subjects demonstrate how individuals with autism process and understand the social world differently beginning at an early age. Although interventions and social skill training can improve eye contact behaviors in individuals with ASD,25 difficulties with eye contact persist throughout lifetime for most individuals.30 Even though the ability to engage in mutual gaze is essential to navigate the social scenes at work and school,17 lack of association between eye contact and social competence raises question on whether the significance of eyes in developing social skills has been overstated.1 Furthermore, researchers, clinicians, and educators should be encouraged to develop social and academic interventions that appreciate the neurodiversity of individuals with ASD. For example, it is important to understand how conventional social expectations, such as eye contact, may be interpreted differently or even disturb learning for some individuals with ASD. In short, eye contact is a natural and an effortless action for most neurotypical individuals, but those with ASD experience difficulty and distress by this action. Whether to insist that individuals engage in eye-looking are questions that will require ongoing review and understanding. However, respect for autistic forms of communication and self-expression will be the first steps to expand the definitions on what is normal and acceptable to create a welcoming society for all individuals.
References
1. Norbury CF, Brock J, Cragg L, Einav S, Griffiths H, Nation K. Eye-movement patterns are associated with communicative competence in autistic spectrum disorders. Journal of Child Psychology and Psychiatry. 2009;50(7):834-842. doi:10.1111/j.1469-7610.2009.02073.x.
2. Sasson NJ. The Development of Face Processing in Autism. Journal of Autism and Developmental Disorders. 2006;36(3):381-394. doi:10.1007/s10803-006-0076-3.
3. Jones W, Carr K, Klin A. Absence of Preferential Looking to the Eyes of Approaching Adults Predicts Level of Social Disability in 2-Year-Old Toddlers With Autism Spectrum Disorder. Archives of General Psychiatry. 2008;65(8):946. doi:10.1001/archpsyc.65.8.946.
4. Howlin P, Yates P. The Potential Effectiveness of Social Skills Groups for Adults with Autism. Autism. 1999;3(3):299-307. doi:10.1177/1362361399003003007.
5. Farroni T, Csibra G, Simion F, Johnson MH. Eye contact detection in humans from birth. Proceedings of the National Academy of Sciences. 2002;99(14):9602-9605. doi:10.1073/pnas.152159999.
6. Butterworth G, Jarrett N. What minds have in common is space: Spatial mechanisms serving joint visual attention in infancy. British Journal of Developmental Psychology. 1991;9:55–72.
7. Haith M, Bergman T, Moore M. Eye contact and face scanning in early infancy. Science. 1977;198(4319):853-855. doi:10.1126/science.918670.
8. Meltzoff A, Moore M. Imitation of facial and manual gestures by human neonates. Science. 1977;198(4312):74-78. doi:10.1126/science.897687.
9. Leekam S, Baron-Cohen S, Perrett D, Milders M, Brown S. Eye-direction detection: A dissociation between geometric and joint attention skills in autism. British Journal of Developmental Psychology. 1997;15(1):77-95. doi:10.1111/j.2044-835x.1997.tb00726.x.
10. Charman T, Swettenham J, Baron-Cohen S, Cox A, Baird G, Drew A. Infants with autism: An investigation of empathy, pretend play, joint attention, and imitation. Developmental Psychology. 1997;33(5):781-789. doi:10.1037/0012-1649.33.5.781.
11. Itier RJ, Alain C, Sedore K, McIntosh AR. Early face processing specificity: It’s in the eyes! Journal of Cognitive Neuroscience. 2007;19:1815–1826. doi: 10.1162/jocn.2007.19.11.1815.
12. Durkin K, Conti-Ramsden G. Language, Social Behavior, and the Quality of Friendships in Adolescents With and Without a History of Specific Language Impairment. Child Development. 2007;78(5):1441-1457. doi:10.1111/j.1467-8624.2007.01076.x.
13. Pelphrey KA, Sasson NJ, Reznick JS, Paul G, Goldman BD, Piven J. Visual scanning of faces in autism. Journal of Autism and Developmental Disorders. 2002;32(4):249-261. doi:10.1023/a:1016374617369.
14. New study adds key piece to autism puzzle. ScienceDaily. https://www.sciencedaily.com/releases/2016/04/160404134228.htm. Published April 4, 2016. Accessed December 6, 2019.
15. McGlensey M. 16 People With Autism Describe Why Eye Contact Can Be Difficult. The Mighty. https://themighty.com/2016/02/why-eye-contact-can-be-difficult-for-people-with-autism/. Published December 6, 2019. Accessed December 6, 2019.
16. Moriuchi JM, Klin A, Jones W. Mechanisms of Diminished Attention to Eyes in Autism. American Journal of Psychiatry. 2017;174(1):26-35. doi:10.1176/appi.ajp.2016.15091222.
17. Bennie M. Should we insist on eye contact from children with autism? Autism Awareness. https://autismawarenesscentre.com/force-eye-contact-children-autism/. Published April 23, 2018. Accessed December 6, 2019.
18. Kylliäinen A, Hietanen JK. Skin Conductance Responses to Another Person’s Gaze in Children with Autism. Journal of Autism and Developmental Disorders. 2006;36(4):517-525. doi:10.1007/s10803-006-0091-4.
19. Kleinhans NM, Richards T, Weaver K, et al. Association between amygdala response to emotional faces and social anxiety in autism spectrum disorders. Neuropsychologia. 2010;48(12):3665-3670. doi:10.1016/j.neuropsychologia.2010.07.022.
20. Steensel FJAV, Bögels SM, Perrin S. Anxiety Disorders in Children and Adolescents with Autistic Spectrum Disorders: A Meta-Analysis. Clinical Child and Family Psychology Review. 2011;14(3):302-317. doi:10.1007/s10567-011-0097-0.
21. White SW, Oswald D, Ollendick T, Scahill L. Anxiety in children and adolescents with autism spectrum disorders. Clinical Psychology Review. 2009;29(3):216-229. doi:10.1016/j.cpr.2009.01.003.
22. Helgeson DC, Fantuzzo JW, Smith C, Barr D. Eye-contact skill training for adolescents with developmental disabilities and severe behavior problems. Edu Training Mental Retardation. 1989;1: 56–62.
23. Berler ES, Gross AM, Drabman RS. Social skills training with children: proceed with caution. Journal of Applied Behavior Analysis. 1982;15(1):41-53. doi:10.1901/jaba.1982.15-41.
24. Hwang B, Hughes C. Increasing Early Social-Communicative Skills of Preverbal Preschool Children with Autism through Social Interactive Training. Journal of the Association for Persons with Severe Handicaps. 2000;25(1):18-28. doi:10.2511/rpsd.25.1.18.
25. Stewart R. Indiana Institute on Disability and Community. IIDC. https://www.iidc.indiana.edu/pages/Should-We-Insist-on-Eye-Contact-with-People-who-have-Autism-Spectrum-Disorders. Accessed December 6, 2019.
26. Eye tracking: Autism Research News. Spectrum. https://www.spectrumnews.org/wiki/eye-tracking/. Accessed December 6, 2019.
27. Klin A, Jones W, Schultz R, Volkmar F, Cohen D. Visual Fixation Patterns During Viewing of Naturalistic Social Situations as Predictors of Social Competence in Individuals With Autism. Arch Gen Psychiatry.2002;59(9):809–816. doi: 10.1001/archpsyc.59.9.809
28. Noris B, Barker M, Nadel J, Hentsch F, Ansermet F, Billard A. Measuring gaze of children with autism spectrum disorders in naturalistic interactions. 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society. 2011. doi:10.1109/iembs.2011.6091325.
29. Noris B, Nadel J, Barker M, Hadjikhani N, Billard A. Investigating Gaze of Children with ASD in Naturalistic Settings. PLoS ONE. 2012;7(9). doi:10.1371/journal.pone.0044144.
30. Senju A, Johnson MH. Atypical eye contact in autism: Models, mechanisms and development. Neuroscience & Biobehavioral Reviews. 2009;33(8):1204-1214. doi:10.1016/j.neubiorev.2009.06.001.