Current Developmental Disorders Reports (2019) 6:37–44

https://doi.org/10.1007/s40474-019-00158-w

AUTISM SPECTRUM (A RICHDALE AND L LAWSON, SECTION EDITORS)

Eye-Tracking Research in Autism Spectrum Disorder: What Are We

Measuring and for What Purposes?
Taralee Hamner 1,2 & Giacomo Vivanti 1,2

Published online: 18 April 2019

# Springer Nature Switzerland AG 2019

Abstract
Purpose of Review The introduction of eye-tracking technology has enabled researchers in the field of autism spectrum disorder
(ASD) to “look through the eyes” of individuals with ASD. In the article, we review research in the area with a focus on (1) the
constructs that have been measured through eye-tracking paradigms, and (2) the application of this technology across different
purposes, including addressing basic science questions, facilitating diagnosis, and measuring intervention mechanisms and outcomes.
Recent Findings Most eye-tracking research to date has focused on quantifying differences in social attention between samples
with ASD and typical development. Other social constructs such as goal prediction, theory of mind, and joint attention have also
been investigated, but to a lesser degree. Similarly, cognitive constructs in non-social domains, such as working memory, visual
search, attentional disengagement, and habituation have been investigated through eye-tracking paradigms, but less frequently
than social attention. A modest but growing body of literature is focusing on the usefulness of eye-tracking to identify ASD
diagnostic markers and measure intervention outcomes, with promising yet inconclusive results.
Summary Eye-tracking technology is a feasible measurement tool to capture a range of psychological constructs and can be used
for a range of purposes relevant to both research and practice. However, the potential of eye-tracking for capturing processes
other than social attention and its relevance to diagnosis and intervention is still to be fully explored.

Keywords Autism . Eye-tracking . Visual attention . Social attention . Autism diagnosis . Autism intervention

Introduction “looking through the eyes” of those with ASD. Eye-tracking

technology uses the contrast between the pupil and the iris to
Autism spectrum disorder (ASD) is a neurodevelopmental locate the center of the pupil and infrared light to create a
disorder characterized by impairments in social communica- corneal reflection. The vector between these two features is
tion and the presence of restricted, repetitive, or stereotyped then used to compute gaze intersection with a surface, thus
behaviors [1], occurring in 1 in 59 individuals in the USA [2]. measuring the focus of attention, or where a person is looking.
For decades, scholars in the field have argued that in order to The measurement of what individuals attend to can reveal
answer questions about psychological processes and experi- important information on how stimuli are prioritized, experi-
ence of individuals with ASD, one should aim to understand enced, and processed.
the world from their point of view [3]. Since the turn of the Compared with behavioral paradigms, the use of eye-
century, the introduction of eye-tracking technology has tracking in ASD research has two main advantages. First, it
allowed researchers to gain insight on ASD as if they were provides a more objective and accurate measurement of atten-
tional patterns (e.g., measuring duration or latency of atten-
tional engagement with a stimulus with millisecond-level pre-
This article is part of the Topical Collection on Autism Spectrum cision). Second, given its non-invasive nature, and the possi-
bility to acquire valid data via passive viewing of visual dis-
* Giacomo Vivanti
plays, eye-tracking is optimally suited for individuals who
[email protected]
experience difficulties with following verbal instructions and
1
A.J. Drexel Autism Institute, Drexel University, 3020 Market Street, handling complex social and cognitive demands, such as those
Suite 560, Philadelphia, PA 19104-3734, USA with ASD [4, 5].
2
Department of Psychology, Drexel University, Following the pioneering works of Klin et al., Pelphrey
Philadelphia, PA 19104-3734, USA et al., and van der Geest et al., eye-tracking has been used

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38 Curr Dev Disord Rep (2019) 6:37–44

extensively in the field of ASD to gain insight on atypical sensitive to the presence of non-social physical contingen-
information processing characteristic to the syndrome [6•, cies in the same social stimuli (such as audiovisual syn-
7•, 8•]. More recently, its application has been extended to chronies involving movement and non-social sounds)
the search for diagnostic markers and the measurement of [18]. Subsequent research using similar stimuli, however,
intervention outcomes [4, 9••]. In the reminder of the article, documented that reduced rather than increased attention to
we will provide a narrative overview of these different areas of audiovisual synchrony in infants at 10 months was pre-
inquiry in ASD eye-tracking research, discussing lessons dictive of an ASD diagnosis at 3 years of age [19]. As
learned and directions for future research. suggested by the study authors, atypical developmental
trajectories in ASD may contribute to these discrepant
Eye-Tracking Research Investigating the Nature findings, as infants with ASD may process multisensory
of Social Differences in ASD information differently early in development. In addition,
it has been suggested the earlier study introduced the con-
Most eye-tracking research in the field of ASD has attempted found of highly repetitive motion (i.e., clapping to “pat-a-
to quantify and explain social atypicalities of those with ASD cake”), which may cause a preferential bias in ASD.
focusing on the construct of social attention, i.e., allocation of Eye-tracking research has also been used to examine
attention to social features of a given scene. The construct of various constructs related to social cognition in ASD,
social attention, which has also been defined as “social including the ability to predict the behavior of others
orienting” [10] and “social visual engagement” [11], in eye- and understanding the mental states of others. For exam-
tracking research is commonly operationalized as the duration ple, Falck-Ytter, Krogh-Jespersen et al., and Vivanti
of attention to social versus non-social content of a stimulus et al. have used eye-tracking in predictive gaze para-
(for example, relative amount of attention to someone’s eyes digms that measured whether participants predictively
versus objects in the background). Two recent meta-analyses gazed towards an area or object that the agent in the
examining social attention in ASD [12•, 13] showed a medi- video was likely to act upon (e.g., an object that the
um effect in the magnitude of social attention difference be- agent was looking at and moving her hand towards, as
tween participants with and without ASD, with the ASD opposed to one that she was ignoring) [14, 20, 21, 22••,
groups exhibiting reduced attention to social stimuli. This 23]. Such predictive gaze paradigms are used to index
phenomenon was reported to increase in magnitude as the goal prediction, i.e., the ability to anticipate the behavior
social complexity of the stimuli increased, with differences of others. This research yielded mixed findings, with
remaining stable across development. Additional research Falck-Ytter reporting normative performance in toddlers
has shown that attention to faces in preschoolers with ASD with ASD, whereas Vivanti et al. and Krogh-Jespersen
is less modulated by social cues that increase social attention et al. documented reduced ability to anticipate the target
in individuals without ASD, including the presence of a direct of others’ actions in toddlers and preschoolers, which
versus averted gaze [14] and emotional versus neutral facial was related to reduced attention to social cues such as
expressions [15]. head turning and gaze direction.
Another line of eye-tracking research has examined Eye-tracking paradigms based on predictive gaze have
ASD-specific differences in visual attention to different also been used to study the theory of mind in young chil-
components within social stimuli. Initial research has sug- dren with ASD. In an eye-tracking version of the classic
gested that adults with ASD showed increased attention to false-belief task, Senju et al. documented that toddlers
the human mouth and decreased attention to human eyes with ASD failed to anticipate an agent’s behavior when
[6•]. However, subsequent research did not replicate this such behavior could only have been predicted if they had
finding [16] and provided indications that atypical face attributed a false belief to her (see also [25]), a pattern
scanning features are related to age. For example, consistent with the notion of a theory of mind impairment
Chawarska et al. documented that children with ASD [24]. However, more recently Cole et al. failed to replicate
showed increased attention to “outer” facial features this finding using a similar eye-tracking paradigm in
(i.e., hair, cheeks, chin) compared with typical peers at adults [26].
both 2 and 4 years of age. However, attention to “inner” Eye-tracking paradigms have also been used to examine
features (i.e., eyes, nose, mouth) was similar to typical joint attention in ASD, with research documenting ASD-
peers at age two, but significantly reduced at age four, specific impairments in response to joint attention as well
suggesting atypical developmental patterns [17•]. as initiations of joint attention in toddlers and preschoolers
Another eye-tracking study reported that toddlers (2 years [27, 28•]. Additionally, recent work by Bedford et al. has
of age) with ASD were less sensitive to animations documented early emerging differences in attentional en-
depicting social actions (e.g., an adult engaging in peek- gagement with objects looked at by others in at-risk infants
a-boo) compared with typical peers but abnormally who would later receive an ASD diagnosis [29].

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Curr Dev Disord Rep (2019) 6:37–44 39

Eye-Tracking Research Investigating the Nature Eye-tracking has also been used to examine repetitive be-
of Non-social Differences in ASD haviors in ASD, with research documenting increased atten-
tion to specific, non-social stimuli in children with ASD ver-
Eye-tracking studies have also sought to examine attentional sus typical controls, and an association between heightened
and cognitive processes that are not related to the social do- visual interest in objects and severity of repetitive behaviors in
main. For example, Joseph and colleagues used eye-tracking children (but not adults) with ASD [34, 42].
to document superior visual search (enhanced ability to dis- A recent area of eye-tracking research is the examination of
criminate between targets and distractors) in school-age chil- gender differences within the ASD population, with prelimi-
dren and adolescents with ASD, pointing to the usefulness of nary research suggesting that social attention might be less
eye-tracking research to understand strengths in addition to atypical in school-age females versus males with ASD [43•];
challenges in ASD [30•]. Interestingly, Gliga et al. document- a similar pattern was detected in infants at risk for ASD [44].
ed that advantages in visual search at 9 months predicted ASD Finally, eye-tracking technology has also been used to mea-
severity in toddlerhood [31]. Other eye-tracking research has sure physiological arousal through pupillometry (the measure-
documented superior performance in the embedded figures ment of pupil diameter and its dilation in response to different
test in ASD, indicating that school-aged children with ASD, stimuli). Preliminary evidence from this area of research in-
compared with typically developing peers, were faster at per- cludes atypical emotional reactivity in response to different
ceiving target figures that were embedded in larger shapes social stimuli in preschoolers ASD, such as emotional faces
[32] (see also [33] for additional eye-tracking evidence of [45, 46, 47••]. While this area of research is in its infancy. The
atypical global processing in ASD). relevance of eye-tracking pupillometry to index arousal re-
Eye-tracking research has also examined attention sponse as well as various brain processes is subject to increas-
shifting and disengagement in ASD, with recent research ing investigation [48, 49].
[34] documenting fewer shifts and longer disengagement Summarizing, eye-tracking research investigating the na-
time in response to pictures considered of high interest ture of ASD atypicalities has generally documented atypical-
(e.g., trains, cars) in adolescents and adults with ASD—a ities in how social information is processed, including differ-
finding consistent with earlier work linking atypical ences in how attention to social stimuli is allocated and mod-
shifting and disengagement to circumscribed interests in ulated by various cues. However, conflicting findings also
children with ASD [35]. Impairments in attentional disen- exist. Research on information processing in non-social do-
gagement have also been documented in eye-tracking re- mains is more limited and inconclusive. As outlined in the
search using the gap-overlap paradigm [36], although two discussion, the field would benefit from standardization and
recent eye-tracking studies found normative disengage- validation of eye-tracking paradigms to ensure precision of
ment in ASD [37, 38]. These different results might be in constructs measured and comparability of results between
part attributable to differences in the eye-tracking indexes studies.
of engagement/disengagement across studies (central
disengagement/peripheral saccade accuracy in [36] versus Early Identification and Diagnostic Markers
central disengagement peripheral saccade in [37, 38]).
Additional eye-tracking paradigms have been used to ex- In the past decade, eye-tracking has been used in longitudinal
amine habituation and response to invariant versus variable studies of infants at familial risk for ASD to investigate
stimuli. Recent research [39] has documented that whereas markers of early emerging atypicalities that might be informa-
preschoolers without ASD decreased their attention towards tive for early identification. A recent study in this area found
an invariant stimulus (repeated presentation of a square) and that newborns at high-risk for ASD showed atypical looking
increased their attention towards a variable stimulus (shapes) profiles evidenced by more time spent looking at inverted
over multiple trials, those with ASD showed a similar atten- faces and random motion compared to children not at risk,
tional decline in response to both the novel and repeating who showed a preference for non-inverted faces and biologi-
stimuli. Vernetti et al. also documented atypical fixation pat- cal motion [50]. However, a study by Jones and Klin using a
terns in response to invariant versus variable stimuli using similar design failed to identify differences in newborns at risk
social stimuli in toddlers with ASD [40]. for ASD. Rather, they documented that infants who went on to
Furthermore, Fanning et al. used eye-tracking to mea- receive an ASD diagnosis at 36 months showed normative
sure spatial working memory in preschoolers with ASD in attention to the eyes of a caregiver at 2 months of age, which
an adaptation of the classic A not B paradigm in which then declined through 6 months of age. Conversely, children
participants’ visual fixations to locations associated with not at risk for ASD showed an increase in eye looking over
previously presented stimuli were used as an index of this same period [51••].
working memory [41]. Results revealed normative perfor- Other studies found that at 6 months of age, high-risk in-
mance in the ASD group. fants who later received an ASD diagnosis showed reduced

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40 Curr Dev Disord Rep (2019) 6:37–44

spontaneous attention to social scenes [52••] and were less examined in the ASD field. For example, Murias et al. docu-
focused on the inner features of a face when the face was mented that eye-tracking-derived measures of social attention
speaking compared with infants who did not develop ASD were correlated with social outcome measures that are typical-
[53]. Additionally, as previously mentioned, eye-tracking re- ly used in ASD intervention trials, including caregiver reports
search by Falck-Ytter et al. documented reduced orienting to of adaptive behavior and ASD symptoms [62]. Recent work
audiovisual synchrony during the observation of biological by Dawson and colleagues documented changes in eye-
motion in 10-month-old infants was predictive of receiving tracking measures of social attention in a group of children
an ASD diagnosis [19]. Interestingly, an association between receiving a novel therapy based on autologous cord blood
preference for synchrony in toddlerhood and language abili- infusion [9••]. These changes were associated with changes
ties has been recently documented in children with and with- in parent-reported socialization measures, pointing to the use-
out ASD who were matched on language abilities [54], sug- fulness of eye-tracking markers as endpoints in clinical trials.
gesting that attentional responsivity to audiovisual synchrony A recent trial on bumetanide (a diuretic acting on GABAergic
might be an important factor for communication development inhibition) has used eye-tracking to document increase dura-
in typical and atypical social development. tion of attention to eyes during viewing of dynamic emotional
Further eye-tracking research has reported similar gaze fol- faces as well as improved face perception in ASD following
lowing patterns in 10-month old high- and low-risk infants in intervention [63•, 64].
response to an agent turning both her head and eyes to direct Additionally, Vivanti et al. documented the utility of eye-
attention, whereas the high-risk group was under-responsive tracking measures in predicting intervention response, with
to an “eyes-only condition” and relied more on collecting findings showing that an eye-tracking measure of goal antic-
information from head movements [55•] (see also [14, 23] ipation was associated with communication changes follow-
for similar results in older samples). Gaze following abnor- ing 1 year of early intervention in young children with ASD
malities during infancy detected through eye-tracking was [22••]. Finally, eye-tracking has been used to test hypotheses
shown to predict later ASD symptomatology [29, 56]. relevant to early intervention theories. For example, Trembath
This preliminary research highlights the potential for eye- et al. tested the long-held assumption that children with ASD
tracking to capture early deviations in social processes in ASD learn better in response to visually presented instructions
that are difficult to measure through behavioral observation, (such as pictures) compared with verbal instruction, finding
with recent findings showing robust concordance between little evidence for a “visual learning style” in ASD [65].
eye-tracking and clinical judgment of ASD risk, symptoms, While the use of eye-tracking technology in this area is in
and attentional patterns [13, 57]. Importantly, however, some its infancy, this preliminary work holds promise in testing
eye-tracking research reported no differences during infancy treatment theories and providing an objective measurement
in children later diagnosed with ASD compared with children of intervention mechanisms and outcomes (e.g., changes in
who do not develop ASD [58, 59]. Variability in eye-tracking social engagement and social cognition).
stimuli and indexes might contribute to such differences,
pointing to the need for validation of paradigms before the
usefulness of eye-tracking for early identification of ASD Discussion
can be fully ascertained.
Challenges and Future Directions
Intervention Science
In summary, the introduction of eye-tracking in the field of
Whereas most literature on ASD early intervention focuses on ASD has contributed critical advances in the characterization
broad measures of cognitive, language, and adaptive function- of social (and, to a lesser degree, non-social) information pro-
ing to establish treatment effects, there is an increasing em- cessing in children with ASD. Progress enabled by eye-
phasis in the field on the need for a better measurement of the tracking includes increased measurement precision as well
social processes that are engaged and shaped by intervention as the possibility to test attentional and cognitive processes
[60]. Eye-tracking technology affords a high degree of preci- in younger and more impaired children with ASD, who have
sion in the measurement of constructs relevant to early inter- been historically under-represented in experimental behavior-
vention mechanisms and outcomes, such as social attention/ al paradigms requiring compliance with verbal instructions
orienting and social cognitive constructs (e.g., goal prediction, (e.g., the classic theory of mind tests).
theory of mind), thus holding the potential to provide an ob- Importantly, however, it appears that the field has yet to
jective marker of treatment change. fully exploit the potential of eye-tracking to address questions
The feasibility of eye-tracking technology as a sensitive on the nature of ASD and implications for diagnosis and treat-
measure to treatment response has been recently shown in ment. First, eye-tracking research reviewed in this article sug-
the typically developing literature [61] and is currently gests that social attention is a frequently measured construct,

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Curr Dev Disord Rep (2019) 6:37–44 41

and findings of social attention differences in ASD appears to understood, leaving open the question of the degree to which
be robust. However, eye-tracking research focused on other biological wiring drives social visual engagement and social
constructs is less abundant and has resulted in more inconsis- visual engagement shapes biological connections, and how
tent findings, pointing to the need for more examination of the two processes interact in early development. Recent re-
constructs other than social attention. Research reviewed in search has started to shed light on the hardwired constraints
this article suggests that a range of psychological processes and neonatal transitions of visual social attention, but more
(e.g., theory of mind, response to joint attention, working research is needed to clarify the relative contribution of bio-
memory) can be measured through eye-tracking adaptations logical programming and experience (e.g., social attention
of behavioral paradigms, most commonly using anticipatory history) on ASD atypicalities detected through eye-tracking
gaze to stimuli/locations to examine what children expect to [68•, 69•].
see based on how previous information is processed. This Our review has also highlighted how the relevance of
window into information processing could be exploited fur- eye-tracking to the diagnosis of ASD is still unclear.
ther, through replication of existing studies and development Although initial eye-tracking findings of reduced social
of eye-tracking tasks tapping into cognitive constructs that are attention in ASD had sparked optimism on the possibility
difficult to measure with precision through standard cognitive that atypical eye-tracking patterns could provide an early
tests, especially in younger and non-verbal children with diagnostic signature for ASD, many studies could not
ASD. identify a link between eye-tracking patterns in infants
Furthermore, this line of research would benefit from an and a later diagnosis of ASD [58, 59]. The few studies
increased focus on factors that modulate differences in eye- that documented eye-tracking abnormalities in infants lat-
tracking measures between ASD and other groups (e.g., anx- er diagnosed with ASD have not yet identified a universal
iety disorders, attention-deficit/hyperactivity disorder, other and specific eye-tracking marker to support the early di-
neurodevelopmental disorders), and within the ASD group, agnosis of ASD [51••, 52••]. For example, Pierce et al.
i.e., the circumstances/conditions under which eye-tracking (2016) documented abnormal visual preference for geo-
patterns in ASD are most abnormal, and how these differ metric shapes compared with social stimuli in young chil-
among different subgroups within the ASD population (for dren with ASD, but such atypical eye-tracking pattern had
example, individuals showing optimal versus suboptimal re- very low sensitivity for ASD, although it demonstrated
sponse to specific interventions). Knowledge in this area high specificity [70]. These results led the authors to pro-
would provide critical insight on how the allocation of atten- pose that performance on the task could be a potential
tion in ASD is impacted by different stimuli in different indi- biomarker for a specific ASD subtype.
viduals and how such abnormalities might be minimized It is possible that our ability to identify eye-tracking
through treatment. markers of ASD might be hindered by poor ecological
Additionally, more research is needed on the behavioral validity of stimuli presented through eye-tracking devices,
and neuropsychological correlates of eye-tracking measures. as visual displays might fail to enable bodily engagement
For example, recent research has used EEG and MRI to mea- with the child, possibly resulting in the failure to fully
sure neural responses to social stimuli believed to be disrupted capture the core social engagement impairments that char-
in ASD and targeted by treatment [66, 67]. Eye-tracking pat- acterize ASD [71]. This limitation has been recently
terns in response to social stimuli, including both fixation time targeted by eye-tracking research measuring viewing pat-
and pupil dilation response, could provide a sensitive and less terns in live interactions with caregivers or confederates
invasive and costly measure of social processing changes [55•]; studies using eye-wear technology (e.g., glasses)
targeted in the intervention. Additionally, eye-tracking pat- that records participants’ viewing pattern as they go about
terns might capture intervention-related changes (for example, their day or are worn by an examiner to detect gaze pat-
increased engagement with social stimuli) before those chang- terns during social interactions [72•, 73]. Future research
es are reflected in structure-functioning reorganization detect- should capitalize on such ecologically valid eye-tracking
able through neuroimaging. However, the use of eye-tracking approaches to identify markers relevant to the diagnosis
as an “intermediate” marker to measure social processing re- of ASD.
quires further investigation on the association between brain Another challenge in the field is that much research on
imaging-derived and eye-tracking-derived responses to social eye-tracking signatures of ASD in infancy has focused on
stimuli. In particular, the study of behavioral and infants who are at high risk to develop ASD by virtue of
neurofunctional correlates of eye-tracking measures would having an older sibling with ASD—a population that might
benefit from the adoption of a developmental perspective. differ in terms of underlying genetic or biological risk fac-
For example, the developmental interplay between visual en- tors compared with other populations at high risk for ASD
gagement with social information and neural activation/ (e.g., children who are born premature), and compared
processing in response to social stimuli remains poorly with children with idiopathic ASD and ASD associated

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42 Curr Dev Disord Rep (2019) 6:37–44

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