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Transcript of Current Visual Pathway Research
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Current visual scanpath research: a review of investigations into the
psychotic, anxiety, and mood disorders
Wei Lin Toha,b,, Susan L. Rossella,b,c, David J. Castlea,d
aDepartments of Behavioural Science and Psychiatry, The University of Melbourne, Melbourne, VIC, Australiab
Cognitive Neuropsychology Laboratory, Monash Alfred Psychiatry Research Centre, School of Psychology and Psychiatry, Faculty of Medicine,
Nursing, and Health Sciences, Monash University, Melbourne, VIC, AustraliacBrain Sciences Institute, Swinburne University of Technology, Melbourne, VIC, Australia
dDepartment of Psychiatry, St Vincent's Mental Health, Melbourne, VIC, Australia
Abstract
The human visual system is comprised of an array of complex organs, which jointly decode information from visible light to construct a
meaningful representation of the surrounding environment. The study of visual scanpaths transpired in a bid to enhance our understanding of
the role of eye movements underpinning adaptive functioning as well as psychopathology and was further aided by the advent of modern eye-
tracking techniques. This review provides a background to the nature of visual scanpaths, followed by an overview and critique of eye
movement studies in specific clinical populations involving the psychotic, anxiety, and mood disorders, and concludes with suggested
directions for future research. We performed a Medline and PsycInfo literature search, based on variations of the terms visual scanpath,
eye-tracking,and eye movements,in relation to articles published from 1986 to the present. Eye-tracking studies in schizophrenia mostly
concurred with the existence of a restricted scanning strategy, characterized by fewer number of fixations of increased durations, with
shorter scanpath lengths, and a marked avoidance of salient features, especially in relation to facial emotion perception. This has been
interpreted as likely reflecting dual impairments in configural processing as well as gestalt perception. Findings from the anxiety and mood
disorders have conversely failed to yield coherent results, with further research warranted to provide corroborating evidence and overcome
identified methodological limitations. Future studies should also look toward applying similar techniques to related disorders as well as
conducting parallel neuroimaging investigations to elucidate potential neurobiological correlates. 2010 Elsevier Inc. All rights reserved.
For the eye altering, alters all.- William Blake, 1757-1827.
The eye bestows the gift of sight, allowing us to make
sense of and navigate through our world. Though
positioned at the gateway to the human visual system, it
forms but one of an array of complex organs, including the
optic nerves and chiasm, lateral geniculate nucleus, and
visual cortex, which jointly decode information fromvisible light to construct a meaningful representation of
the surrounding environment. Accordingly, we are able to
perform intricate tasks, such as ident ifying objects,
perceiving color, and estimating distances, all crucial to
our everyday functioning. Despite these concrete opera-
tions, it is most often the psychological manifestation of
visual information, or visual perception, which is key in
shaping our behaviors and cognition. This review is aimed
at providing a background to the nature of visual scanpaths,
with key consideration to the special case of face
perception, followed by an overview and critique of eye
movement studies in healthy and specific clinical popula-tions involving the psychotic, anxiety, and mood disorders.
We conclude with suggested directions for future research.
1. Physiology of eye movements
The act of seeing is initiated when light enters the cornea
at the front window of the eye and passes through the pupil,
which either contracts or dilates, thereby controlling the
Available online at www.sciencedirect.com
Comprehensive Psychiatry xx (2011) xxx xxxwww.elsevier.com/locate/comppsych
Corresponding author at: Monash Alfred Psychiatry Research Centre,
Prahran VIC 3004, Australia. Tel.: +61 3 9076 8650.
E-mail address:[email protected](W.L. Toh).
0010-440X/$ see front matter 2010 Elsevier Inc. All rights reserved.
doi:10.1016/j.comppsych.2010.12.005
http://dx.doi.org/10.1016/j.comppsych.2010.12.005http://dx.doi.org/10.1016/j.comppsych.2010.12.005http://dx.doi.org/10.1016/j.comppsych.2010.12.005mailto:[email protected]://dx.doi.org/10.1016/j.comppsych.2010.12.005http://dx.doi.org/10.1016/j.comppsych.2010.12.005mailto:[email protected]://dx.doi.org/10.1016/j.comppsych.2010.12.005http://dx.doi.org/10.1016/j.comppsych.2010.12.005http://dx.doi.org/10.1016/j.comppsych.2010.12.005 -
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amount of light reaching the sensitive foveal membrane
located at the center of the retina[1]. This produces a series
of neural impulses, firing along the optic nerves, to be
ultimately managed in a hierarchical fashion by various parts
of the visual system located in the brain. As the fovea forms
the focus point of the eye, it yields enhanced image
resolution, allowing it to distinguish much more color and
visual detail, whereas the rest of the retina mainly comprises
basic light detectors that act to facilitate efficient peripheral
vision. Therefore, to process a visual scene in its entirety,
voluntary shifts of the eye have to take place to acquire,
fixate, and track the stimulus. By rotating the eye in the
horizontal and vertical planes, different points of interest
may be visually processed. These eye rotations are quantified
in terms of degrees of visual angle, with several successive
rotations required for a complete scan of the visual scene.
Depending on whether the visual stimulus is in motion or
stationary, research has focused on investigating 2 respective
classes of eye movements, namely, smooth pursuit vs
saccades, the latter of which forms the sole interest of thecurrent review.
1.1. The visual scanpath
Early proponents devised the notion of the visual
scanpath in an attempt to provide an integrated account of
how the human visual system was engaged in the formation
of internal memory links that facilitated the processes of
learning and recognition. Accordingly, Hochberg [2]
introduced the idea of a schematic map, representing the
synthesis of sensory information, afforded by successive
foveal glimpses, into an overall percept. This was laterexpanded upon by Noton and Stark [3] in their scanpath
hypothesis, which proposed pattern recognition as a serial
process involving the uptake of sensory details via a fixed
order sequence of eye movements during initial stimulus
detection as well as subsequent reidentification. In this way,
fixed and characteristic scanpaths permitted each individual
feature of the stimulus to be processed visually and laid
down as a corresponding memory trace. The internal
representation of the stimulus was thus thought to be made
up of an alternating progression of sensory and memory
traces accompanied by parallel motor shifts, forming what
was termed afeature ring. Consequently, the reproduction of
successive eye movements in a replica of the originalscanpath promoted verification of ensuing feature memories,
thereby indicating successful pattern recognition.
Therefore, the visual scanpath may be seen as a map that
traces the direction and extent of eye movements during
viewing of a complex visual stimulus and comprises a
sequence of fixations and saccades [4]. Fixations may be
defined as consecutive gaze points within 1 of the visual
field held with a duration of at least 200 milliseconds,
though specific criteria may vary. These represent points of
attention, where the fovea is directed and held stationary
over a specific position on a visual scene, during which
stimulus input is processed in detail. In contrast, saccades
denote rapid voluntary movements between fixations, which
shift the fovea from one particular point of interest to
another. During this time, parallel cognitive processes use
parafoveal and peripheral retinal information to establish the
location of the next fixation[5]. Moreover, external features
of the stimulus, in conjunction with the operation of inner
schematic beliefs, also influence and shape the overall
scanpath pattern[6]. Fixation attention is thus dictated by a
combination of broader top-down cognitive factors, such as
expectations, goals, and memory, to name a few, as well as
specific bottom-up processes, involving visual sensory
input. However, as coarse discrimination occurs rapidly,
whereas the perception of finer details are governed by
later-stage processes of selective attention, the visual
scanpath is largely held as a marker of controlled attention
and reappraisal, rather than an automatic uptake of sensory
information [7]. In other words, visual scanning may be
characterized more as a top-down process regulated by
higher order cognition.
1.2. What is video-oculography?
Historically, insights into visual scanning arose from
direct observation. With the advent of modern eye-tracking
procedures, eye movements can be accurately recorded in a
number of ways. The most popular approach is video-
oculography, involving monocular monitoring of the gaze
direction via infrared light reflecting off the dominant cornea
and pupil [1]. Reflections from these 2 points permit
determination of the spatial position of the eye gaze, which
is recorded by miniature video cameras in terms of an x
-y
coordinate system. The development of novel techniques for
direct detection of the fovea with improved accuracy is also
underway [8]. The main advantages of video-oculography
are its noninvasiveness, robustness, compatibility with a
range of participants, and comprehensive data yield. Recent
technological advances have further enhanced data sampling
rates and gaze resolution, thereby addressing past key
criticisms of this method. Two classes of scanpath
characteristics are typically sampled, namely, spatial and
temporal parameters. At this point, a list of common
scanpath parameters is provided to orientate the reader to a
discussion of significant eye-tracking studies presented in
the following sections. Accordingly, scanpath length refersto the summed distances traveled by the eye during scanning
and is typically measured in degrees of visual angle. It has
also variously been labeled eye scanning length or saccade
amplitude. The number of fixations may intuitively be
defined as the frequency of stationary gaze points acquired
during scanning, whereas fixation durations represent the
time period of these fixations, usually denoted in milli-
seconds. The product of the number of fixations and related
durations thus yields total dwell time. Of late, researchers in
the field have also derived a series of spatial-temporal
indices, for instance, denoting the ratio of fixations to salient
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stimulus features, thereby facilitating a more comprehensive
analysis of scanpath data. In this way, eye movement
recordings are believed to provide an objective, online
psychophysiological indicator of sensory processing and
visuospatial cognition.
1.3. The special case of face perception
There is no doubt that faces constitute a psychologically
unique category of stimuli, with a special significance in
our everyday lives, ranging from conveying information
about the emotional states of significant others [9] to acting
as a potential source of knowledge for our attributions[10].
In fact, early studies have long established that we
recognize human faces with greater ease and accuracy,
compared with other forms of pictorial representation, such
as aeroplanes [11] or canine faces [12]. Models of face
processing have likewise posited a discrete pathway for the
treatment of facial stimuli. For instance, Walker-Smith et al
[13]elaborated on the scanpath hypothesis by proposing analternative feature network, involving the initial registration
of an overall face percept, followed by targeted foveal
interest to pertinent regions so as to insert the details of
salient features into a general face framework. Similarly,
Bruce and Young [14] postulated the involvement of
several separable functional components in face processing,
involving structural encoding, recognition of individuality,
and affect analysis, to name a few.
Although a review of contemporary theories of face
processing is not within the scope of the current review, it is
important to note that there are several robust lines of
evidence corroborating the special case of face perception,namely: (i) the ontogeny of face processing, stemming from
research demonstrating innate face preference and categori-
zation abilities in newborn infants [15]; (ii) the clinical
condition of prosopagnosia, characterized by an exclusive
impairment in face recognition[16]; (iii) the face inversion
effect, describing a significant disruption of recognition for
inverted relative to upright faces[17]; and (iv) neuroimaging
studies, pinpointing specialized brain structures, such as the
fusiform face area, as selectively engaged in face perception
[18]. Accordingly, it may be suggested that humans adopt
global or holistic strategies for scanning faces, simulta-
neously perceiving facial features in parallel[19]. Moreover,
configural representation, or the interrelations amonginternal facial features, is crucial in the formation of a
meaningful global structure [20]. In other words, the
perceptibility of faces is profoundly enhanced when salient
features are aligned into a well-defined overall form or
gestalt [21]. In fact, the gestalt theory of visual perception
elucidates how humans perceive individual components of
complex visual stimuli, such as faces, as an organized whole.
At this point, it is sufficient to note that gestalt perception lies
in contrast to sequential processing, where disparate
elements of visual stimuli are processed in a serial, piecemeal
manner (for a full review of gestalt principles, see Bruce et al
[22]). The significance of facial gestalts will be further
discussed in later sections.
2. Visual scanpath research in nonclinical and
clinical populations
The present review was accomplished based on a Medline
and PsycInfo literature search, using the terms visual
scanpath, visual scanning, visual scan, eye-tracking,
and eye movements, with a follow-up of relevant
literature. Eye-tracking studies among a wide range of
clinical conditions, such as developmental [23] and
neurologic [24] disorders, were uncovered. To ensure
direction and definition, we confined ourselves to the
psychotic, anxiety, and mood disorders, with a particular
focus on articles published from 1986 to the present. This is
because articles before this time were greatly hampered by
existing technology limitations. To set the foundation for a
review of visual scanpath research in clinical populations,we will first discuss how explorations of eye movement
patterns in healthy individuals have contributed to our
knowledge of visual scanning. When perceiving a visual
image, typical eye movement parameters vary as a function
of the nature of the scene as well as actual task demands, for
example, categorization vs memory or recognition. In
general, most fixations will settle upon informative parts
of the scene, with the mean fixation duration and saccade
amplitude respectively tending toward 300 milliseconds and
4to5 [25]. The gist of a scene, however, is extracted almost
instantaneously and can take as little as 40 milliseconds. The
details derived are then used to orientate subsequent fixationsto appropriate points of interest, where further visual
information is acquired.
Owing to its ecologic validity and significance in day-to-
day human interactions, research has examined eye move-
ments in face processing, establishing a typical inverted
triangular pattern of scanning for neutral faces, with most
fixations being focused on salient facial features, notably the
eyes, but also the nose and mouth[13]. More recently, the
focus has turned to detecting differences in recognition
across a range of facial expressions, producing mixed
findings. Accordingly, Green et al [26] described an
extended scanning strategy, comprising increased fixations
of longer durations to salient facial features, along withlonger saccadic distances, but only in response to angry and
fearful emotions. These authors identified a vigilant
scanning strategy reflective of an evolutionary bias in the
appraisal of threat stimuli within a social context. In a
follow-up study, it was observed that schizotypy, or
delusion-proneness, was characterized by reduced number
of fixations to these negatively valenced emotions, likely
suggestive of a hypersensitive avoidance of threat [27].
Another study examining eye movements in schizotypy
uncovered a specific fear recognition deficit that was
believed to be unrelated to anomalies in oculomotor function
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or sustained visual attention[28]. In contrast, Hunt et al[29]
failed to uncover any selective orientation toward angry or
happy faces, whereas Calvo et al[30]reported an advantage
for disgusted, happy, and surprised expressions relative to
angry, fearful, and sad expressions, as shown by earlier
localizations, more efficient detection, and greater response
accuracies. Follow-up research attributed this search advan-
tage to the contribution of affective content and featural
uniqueness[31]. In related research, Bate et al[32]identified
a facilitatory interaction between facial familiarity and
emotion processing; happy expressions promoted the
processing of famous faces, and angry expressions promoted
the processing of novel faces.
Other research examining changes in visual scanning
across the lifespan has noted an age-related decline in
emotion recognition, especially for angry and fearful
expressions [33,34]. Older adults exhibited fewer overall
fixations, which were disproportionately focused on the
lower parts of the face, especially the mouth. These authors
theorized that typical frontal lobe atrophy associated withnormal aging may underlie these scanning styles. In a
separate study investigating sex differences, males were
found to adopt an increased gaze orientation to the nose and
mouth relative to females[35]. Both sexes were nevertheless
equally accurate in identifying facial emotions, though
females exhibited faster reaction times. Taken together,
these studies suggest that eye movements during face
processing in healthy individuals vary as a function of a
range of factors, including age, sex, or specific personality
traits, with negatively valenced emotions perhaps eliciting
more atypical scanning patterns. We will now turn to the
visual scanpath literature in relation to specific classes ofpsychiatric conditions.
2.1. The psychotic disorders
Most visual scanpath research in clinical populations has
focused on the psychotic disorders, especially schizophre-
nia. This disorder has a heterogeneous presentation and may
be classed into various subtypes, but is typically character-
ized by abnormalities in the perception and representation
of reality[36]. Its primary symptoms are bizarre or paranoid
delusions, auditory hallucinations, or grossly disorganized
speech or behavioral patterns, which cause clinically
significant distress and socio-occupational dysfunction. To
date, studies examining eye movements in schizophrenia
have generated fairly consistent findings involving gener-
alized visual scanning deficits. The following sections
provide an overview of this work, organized along a
number of themes, followed by key interpretations and
concluding remarks.
2.1.1. Early visual scanpath studies
A brief outline of early visual scanpath research is
provided, as these studies ignited interest in eye-tracking
investigations in schizophrenia and paved the way for future
inquiries. However, in light of the modern technological
advances in eye tracking, this early literature should be read
with caution. A preliminary study sought to compare the
scanpaths of partially remitted outpatients with schizophre-
nia to healthy controls using light fixation and visual letter
search tasks[37]. Though the schizophrenia group tended to
do worse, these results were not statistically significant, with
the exception of males with chronic unremitting schizophre-
nia who exhibited poor eye-tracking performances. Anom-
alously, patients with catatonic schizophrenia performed
better relative to healthy controls, whereas eye movement
parameters and clinical variables remained largely uncorre-
lated. In follow-up research, the same authors presented a
series of pictures depicting social scenes under free-viewing
conditions. Similarly, there were no observed differences in
fixation or saccade parameters across both populations. Two
discrete styles of visual scanningextensive vs mini-
malwere nevertheless identified and respectively related
to positive and negative schizophrenia symptoms [38].
Another early study also investigated eye movements in
chronic schizophrenia; findings included reduced number offixations of increased durations, amid a limited movement
range in response to a single picture display, as well as
significantly poorer performances during comparisons of a
series of geometric figures [39].
2.1.2. Faces and social scenes
Prominent disturbances in interpersonal communication
and social functioning serve as hallmark features in
schizophrenia. Given the importance of face perception
in social interactions, research exploring various aspects of
face processing in the disorder has uncovered a range of
pervasive deficits, involving judgments of facial attributes,familiarity and identity[40,41], and, most notably, emotion
recognition [42-44]. As a result, numerous studies have
analyzed visual scanpaths in response to facial emotions so
as to gain a better understanding of the nature of these
difficulties. With minor modifications, the basic method-
ology has relied on the presentation of a series of facial
images under free-viewing conditions. The expressions
portrayed were typically the entire range, or a subset, of
the 6 universal human emotions (ie, angry, disgusted,
fearful, happy, sad, and surprised), with a neutral face
serving as the control condition. Initial studies, however,
either relied solely on neutral faces [45-47] or failed to
analyze potential group differences in scanpath parametersacross discrete facial emotions [48-50]. However, on the
whole, virtually all studies have converged on the existence
of a restrictedscanning strategy adopted by schizophrenia
patients, characterized by fewer fixations of increased
durations, with shorter scanpath lengths, and a marked
avoidance of salient facial features, regardless of emotion
valence[45-47,51-53].
Based on a variant of the standard paradigm, Williams
et al [47] displayed nondegraded and degraded neutral
faces, followed by a recognition task with dual levels of
complexity. Relative to healthy controls, schizophrenia
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patients exhibited scanpath disturbances that were most
marked for nondegraded faces, with reduced recognition
accuracies for the more difficult task condition. In follow-
up research, Loughland et al [52,53] administered an
added affect recognition task, using faces depicting happy,
neutral, and sad emotions. In the context of overall
restricted scanpaths, the eye movements of schizophrenia
patients were notably impoverished for happy faces, yet
with superior recognition accuracy, but conversely some-
what normalized in terms of increased attentional focus to
salient facial features for sad faces. These observations
were respectively interpreted in view of past research
documenting an emphasis on holistic processing for happy
faces[54]as well as an undue bias toward negative stimuli
in psychosis [55]. Using an inclusive range of facial
emotions, Bestelmeyer et al [51]suggested that the pattern
of spatial scanning characteristics observed may serve as a
unique biomarker, effectively distinguishing schizophrenia
from other disorders. In a similar vein, Nishiura et al [56]
examined the spatial distribution of gaze points and totalscanpath lengths during the presentation of smiling vs
crying baby faces and reported that schizophrenia patients
showed significant eye movement disturbances, which
were especially prominent in the left visual field for
smiling baby faces.
In contrast, other studies have focused on temporal
scanning parameters in an attempt to elucidate early vs later-
stage face processing. In this regard, schizophrenia patients
were found to exhibit reduced number of fixations of shorter
durations in relation to neutral faces, which were most
marked during the first 3 seconds directly following stimulus
presentation[45]. According to Rosse et al[48],preattentive
fixations may be defined as those less than or equal to 50.1
milliseconds and are believed to implicate configural
processing in an automatic manner due to their brevity of
operation. This is in contrast to serial search processes,
which necessitate longer scrutiny times to aid the sequential
perception of individual features. Using affect recognition
and gaze discrimination tasks, Rosse et al [48] thus
uncovered that schizophrenia patients displayed significantly
decreased preattentive fixations, which inversely correlated
with their clinical symptoms. In follow-up research involv-
ing the presentation of upright and inverted faces, it was
shown that the former drew significantly more preattentive
saccades from healthy controls, whereas the eye movementsof schizophrenia patients did not differ between orientations
[49]. In light of these findings, it was suggested that deficient
scanning strategies in schizophrenia are likely to reflect an
overreliance on sequential processing as a result of impaired
gestalt perception[48,49]. Individuals with the disorder are
not only believed to have difficulties forming an initial
facepercept but also fail in the global integration of stimuli
into a meaningful gestalt. In other words, they perceive faces
in a fragmented, serial manner, such that extraneous areas are
treated as equally critical as salient feature regions. Further
impairments in configural processing are also likely (eg,
Joshua and Rosell [57]), given an absence of the face
inversion effect.
To further enhance ecologic validity, a related area of
research has used social scenes. Using a sketch of a mother
with her child, Nieman et al [58]found that schizophrenia
patients tended to fixate more on both faces relative to
healthy controls, resulting in poorer performance in an
associated working memory task based on external features
of the drawing. More recently, Green et al [59] asked
participants to perform a mental state inference task during
the presentation of image pairs depicting target characters in
emotion-congruent social contexts vs those with limited
situational cues. Relative to healthy controls, schizophrenia
patients displayed longer fixation durations in context-
embedded situations, reduced saccadic activity in context-
free situations, as well as a larger proportion of total dwell
time viewing faces in both conditions. This failure to
perform rapid scanning and uptake of social contextual
information was further correlated with significant impair-
ments during mental state assessments. The findinginvolving augmented facial focus in social scenes is not
incongruent with the avoidance of salient facial features
documented in research using faces only. In particular, it
remains unclear whether this increased facial fixation
during social scene scans was directed at salient or
nonsalient facial regions. Therefore, though opposing
viewing strategies for faces and social scenes may osten-
sibly exist in schizophrenia, a more inclusive interpretation
points toward a restricted scanning strategy, encompassing a
local viewing bias. This interpretation was further supported
by de Wilde et al [60], who reported that schizophrenia
patients exhibited shorter scanpath lengths and increasedstaring behaviors, especially directed toward localized
details, based on social scenes depicted in Thematic
Apperception Test cards. In this sense, a greater focus on
the nonsalient features of faces and other visual stimuli in
social scenes at the expense of pertinent contiguous
information likely contributes toward misinterpretations of
real-life social interactions.
2.1.3. Geometric figures, objects, and line drawings
There has been a great deal of visual scanpath research in
schizophrenia that has used geometric figures. In particular, a
group of Japanese researchers has published a large series of
studies stemming from the late 1980s to the present based ona standardized experimental paradigm (see Akiyama et al
[61]for a review). In sum, this involved a brief presentation
of a unique S-shaped target figure, which participants were
asked to subsequently reproduce from memory. Two slightly
dissimilar figures were next displayed for comparison with
the original target, followed by a repetition of the drawing
memory task. A responsive search score (RSS) was
calculated as a function of the number of sections of the
figures fixated upon. This task was also administered to a
range of clinical populations with temporal lobe epilepsy
[62], frontal lobe lesions [63], and anxiety and/or mood
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disorders[64], to name a few. When schizophrenia patients
in acute, chronic, and remitted states were assessed[65-67],
it was concluded that the entire schizophrenia group
consistently exhibited the lowest RSS, with chronic patients
further displaying a significantly decreased mean eye
scanning length. It was thus suggested that these eye
movement parameters could potentially serve as a nosolog-
ically specific indicator for the disorder. Discriminant
analysis revealed that individuals with schizophrenia could
be differentiated from those without, with a sensitivity and
specificity of 76.7% and 81.4%, respectively [68]. This
methodology has since been replicated across global World
Health Organization collaborative research sites[69], most
recently with the aid of a digital computerized system to
handle extensive data loads[70].
Other researchers have also used a variety of diagrams,
including the Wechsler Adult Intelligence Scale picture
completion task[71], Rey-Osterrieth Complex Figure[46],
smiley faces and scene drawings[72], Rorschach inkblots
[58,73], Benton Visual Retention Test [74], natural land-scapes and fractal patterns [51,75], as well as static linear
segments [76]. It was generally found that schizophrenia
patients exhibited the predicted restricted viewing strategy
relative to healthy controls. There were, however, a few
exceptions, with Manor et al [46] and Cocchi et al [76]
reporting comparable fixation dynamics across schizophre-
nia and healthy control groups. On the whole, the evidence
seems to denote the existence of visuospatial working
memory deficits in schizophrenia, superimposed upon a
faulty oculomotor processing system.
2.1.4. Trait vs state markers
A recurring argument relates to whether deficits in visual
scanning in schizophrenia would more accurately serve as a
trait or state marker. The evidence concerning this dispute
tends to be mixed and primarily derives from 2 sources,
namely, longitudinal and family studies. Accordingly, a line
of research has tracked the stability of scanpath deficits over
the longitudinal course of the disorder by monitoring
schizophrenia patients across acute, chronic, and remitted
states. Several researchers observed that scanpath anomalies
tended to be transient, with relative normalization of eye
movement patterns following improvements in clinical
symptoms [38,77,78]. Other studies have conversely
reported these deficits as not only persisting over time butalso being largely unrelated to changes in psychopathology
and medication status[50,67]. More recently, Kallimani et al
[79] studied the effect of change in clinical status on eye
movement dysfunction using a wide range of oculomotor
tasks and deduced that saccadic parameters were stable at
both individual and group levels, whereas fixation dynamics
tended to be more state dependent. In a separate attempt to
resolve this conflict, other studies have explored the
existence of comparable scanning difficulties in first-degree
relatives of schizophrenia probands. In support of the trait
hypothesis, Loughland et al [80] suggested that relatives
exhibited an attenuated form of the typical restricted
scanning strategy, compounded by a distinct pattern of
increased staring toward happy expressions as well as an
extreme avoidance of salient facial features, especially for
sad expressions (the latter of which was even more marked
than in schizophrenia patients). Several authors have equally
proposed that eye movement dysfunction may serve as an
endophenotype for schizophrenia, corroborating its use as a
specific biological trait marker[81,82]. In contrast, de Wilde
et al [60] reported that unaffected siblings of probands did
not differ from healthy controls on scanpath variables to
Thematic Apperception Test cards, thereby creating concern
about using eye movement parameters as a potential
vulnerability marker. On the whole, support for the trait
hypothesis appears marginally stronger, but further research
elucidating the unique contributions of specific spatial and
temporal scanpath parameters is crucial to clarify the trait vs
state debate.
2.1.5. Symptoms and syndromesTraditional theories of schizophrenia have proposed
diverse classification schemes, ranging from Schneiderian
first-rank symptoms [83] to positive symptoms (eg,
delusions, hallucinations, or thought disorder) vs negative
symptoms (eg, blunted affect, alogia, or anhedonia) [84]
as well as Liddle's [85] 3-factor model, comprising the
dimensions of psychomotor poverty, disorganization, and
reality distortion. Some researchers have thus assumed
investigations from the perspective of uncovering correla-
tions between scanpath aberrations and specific symptom
or syndrome factors. An initial study proposed a rather
simplistic theory relating extensive and restricted scanningstyles to positive and negative symptoms respectively
[38]. Though later research has reported minimal relations
between eye movement parameters and symptom com-
plexes[47,53], associations between staring behaviors and
negative symptoms have been found [56,64,66,73]. For
example, Streit et al [50] detected narrow and constrained
staring behaviors in line with signs of affective flattening.
In addition, Obayashi et al [67] described a correlation
between mean eye scanning length and negative symp-
toms, which was further suggested as a possible
sensitivity index for chronicity. In terms of Liddle's [85]
model, Loughland et al [53] found that psychomotor
poverty was associated with decreased fixations of shorterdurations for happy faces, whereas disorganization was
similarly associated with reduced foveal attention, but
extended raw scanpath lengths for happy faces. However,
the sparse and random nature of these observations has
precluded meaningful interpretations; systematic investiga-
tions into the area are necessary to elucidate further
significant relationships.
2.1.6. The special role of delusions
Delusionshave typically been seen as a central feature of
schizophrenia and may be defined as erroneous beliefs,
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involving a misinterpretation of reality, routinely sustained
with high levels of conviction, despite clear evidence to the
contrary [36]. Several researchers have thus proposed
exploring information processing biases possibly underlying
delusions using visual scanpaths [86-88]. An initial com-
parison of eye movements among deluded and nondeluded
schizophrenia patients and healthy controls used single and
paired facial stimuli [77,78]. Relative to other groups, the
deluded patients used a staring strategy, with decreased
fixations of longer durations directed disproportionately at
nonsalient feature areas, despite similar recognition accura-
cies. Subsequent symptom improvement, however, initiated
relative normalization of viewing strategies during follow-up
assessment. Expanding upon their research protocol, the
same authors presented neutral, ambiguous, or overtly
threatening social scenes to schizophrenia patients bearing
either persecutory or nonpersecutory delusions[89]. Relative
to other groups, the schizophrenia patients with persecutory
delusions exhibited an atypical scanning pattern only for
ambiguous scenes, with significantly increased viewingtimes for nonthreatening foreground areas. Inappropriate
threat appraisal within a social context was hence theorized
as linked to the presence of persecutory delusions. In a later
study, Green et al[90]administered a standard facial affect
paradigm to deluded and nondeluded schizophrenia patients,
with the former demonstrating respectively increased and
decreased fixations to happy and fearful emotions. This
occurred in the context of an overall restricted scanning
strategy to negatively valenced emotions across both
schizophrenia groups, suggestive of a vigilance-avoidance
style of attention operating across early and later stages of
information processing.
2.1.7. Implications and conclusions
Thus far, research examining visual scanpaths in
schizophrenia has revealed fairly consistent findings,
indicative of generalized scanning deficits of a restricted
nature, characterized by fewer fixations of increased
durations, with shorter scanpath lengths, and a marked
avoidance of salient features across a range of visual stimuli.
This has been interpreted as likely reflecting dual impair-
ments in configural processing as well as gestalt perception
[48,49,57]. However, methodological limitations of existing
studies remain to be addressed. As mentioned, early studies
were confined by the technical restrictions of the time,meaning their measurement methods and data accuracy are
debatable (eg, [37-39]. Though this has largely been
remedied by current advances in eye-tracking technology,
some later studies have been fraught with other forms of
inconsistencies. First, the quality of visual stimuli used has
varied. Two superior examples include images of facial
emotion from Ekman and Friesen[91]as well as Mazurski
and Bond[92], though the sharper definition offered by the
former perhaps surpasses the realistic colors of the latter.
Second, inadequate participant matching was common, for
instance, with Rosse et al [48] using cocaine use disorder
patients as control participants. These disparities have made
it difficult to perform comparisons across studies, or derive
firm overall conclusions.
Another source of discrepancy relates to the medication
status of patients. Most studies have suggested that
antipsychotic medications have minimal impact on eye
movements[38,50,93], but de Wilde et al [60]has asserted
that typical antipsychotic chlorpromazine may ameliorate
scanning deficits. Only a single study to date has explicitly
investigated the effects of atypical (risperidone) vs typical
(haloperidol) antipsychotic medication on facial affect
recognition in schizophrenia [94]. Notably, risperidone-
treated patients displayed a relatively normalized pattern of
foveal attention to the salient facial features of happy and
neutral expressions, along with a concomitant recognition
accuracy comparable to healthy controls. However, caution
must be applied in interpreting these findings, because
comparisons between these 2 drugs are fraught with potential
complications. In particular, haloperidol is known for its
extrapyramidal adverse effects, which could include directvision disturbances (eg, pupil dilation, blurred or double
vision), movement problems (eg, ataxia, tardive dyskinesia)
as well as general concentration and memory difficulties
[95], all of which would clearly exert a considerable
detrimental impact on scanning performance. Future research
should therefore focus on examining the latent effects of
atypical antipsychotics on eye-tracking function, with special
notice to the length and dosage of administration as well as
possible side effect profiles.
On a more positive note, the involvement of schizophre-
nia patients across differing illness stages, ranging from
those experiencing a recent onset[58,75]to acute, chronic,and remitted populations [66], as well as other forms of
psychoses, including those induced by methamphetamine
[96,97] or cannabis [75] is encouraging. This is advanta-
geous because gathering eye-tracking statistics over the
course of various psychotic disorders will allow tracking of
fluctuations in eye movement dysfunction. Such progress
has been augmented by neuroimaging studies [98,99],
facilitating the identification of significant neurobiological
correlates. The extensive array of tasks, in conjunction with
neuropsychological assessments, have further corroborated a
cognitive profile for schizophrenia, represented by signifi-
cant frontal lobe dysfunction, alongside visuospatial work-
ing memory deficits [63,71,73]. Moreover, eye movementresearch in schizophrenia does carry direct therapeutic
implications, in terms of the remediation of faulty facial
emotion perception, with attendant benefits for the day-to-
day social living of affected individuals. To this end, several
training packages, to be delivered with the aid of eye-
tracking technology, have been offered [100-102]. In
particular, the Micro-Expression Training Tool developed
by Russell et al[101]fostered a more adaptive face-viewing
strategy in terms of increased fixations and dwell times
within salient feature regions as well as associated improve-
ments in emotion recognition. In the future, the utility of
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these techniques may be enhanced via integration with other
key therapeutic elements within a comprehensive cognitive
remediation program.
2.2. The anxiety disorders
A small number of studies have sought to examine
potential eye movement dysfunction in anxious individuals.When persons with varying levels of trait anxiety were
exposed to angry and happy faces, all participants initially
oriented their gaze more toward angry faces, but only
persons with high trait anxiety exhibited ensuing avoidance
behaviors[103]. Using positive, neutral, and threat images,
another study conversely showed that participants with high
trait anxiety did display early preferential attention for
affective stimuli, but also experienced difficulties in
subsequent disengagement, as evidenced by increased
fixation times[104]. In a separate investigation, Calvo and
Avero[105]found that high trait anxiety had a facilitatory
effect on the reading of posttarget words conveying a
congruent threat event, but a converse inhibitory effect whenan incongruent threat event was being described. This was
interpreted as indicative of a controlled selective bias toward
threat prediction in individuals with elevated levels of trait
anxiety. There has also been preliminary research exploring
visual scanpaths in certain anxiety disorders, including
phobias, obsessive-compulsive disorder (OCD), posttrau-
matic stress disorder (PTSD), and generalized anxiety
disorder (GAD), each of which is reviewed, in turn, in the
following subsections.
2.2.1. Social phobia and specific phobias
Social phobia (SP) is characterized by a marked andpersistent fear of social situations and its attendant prospect
of negative evaluation by others, often provoking a
significant anxiety response [36]. Most visual scanpath
research in the anxiety disorders has focused on SP,
ostensibly because of a classic avoidance of eye contact
exhibited in social situations. Using the standard facial affect
paradigm, involving angry, happy, neutral, and sad expres-
sions, a hyperscanning strategy was uncovered, repre-
sented by reduced fixations in frequency and duration, as
well as increased raw scanpath lengths [106,107]. Further-
more, it was demonstrated that individuals with SP displayed
an active avoidance of salient facial features, especially the
eyes, coupled with extensive scanning of nonsalient facialregions, which was most marked for negatively valenced
emotions. This was construed as a hypervigilance to social
threat, resulting in a diminished ability to acquire ample
information for the accurate interpretation of social interac-
tions. In an assessment of socially anxious individuals,
Meyer [28], on the other hand, found that their affect
recognition performance did not differ from that of healthy
controls. More recently, Wieser et al [108] investigated
visual scanpaths in SP using a novel and ecologically valid
approach, which entailed the presentation of animated movie
clips, depicting neutral faces bearing either a direct or
averted gaze, to individuals with differing levels of social
anxiety. Regardless of gaze orientation, high socially
anxious participants were found to fixate more on the eye
regions, and moreover, responded to direct gazes with
increased physiological arousal in terms of more pronounced
cardiac acceleration. These disparate findings, involving
significant gaze avoidance [106,107] vs preferential atten-
tion [108] to social threat, may perhaps be reconciled by
considering differences in illness severity; individuals with
SP may be inclined to use avoidance as a coping mechanism,
whereas socially anxious persons may be predisposed to seek
out and misjudge instances of interpersonal threat.
A limited number of studies have also used eye-tracking
to investigate spider phobia. Rinck and Becker [109]
presented categories of animal pictures (including spiders)
and reported that spider phobic participants more often
directed their initial fixation toward spider pictures,
followed by a rapid shift of attention away from the fear-
relevant stimuli, resulting in shorter overall fixation
durations. Other typical paradigms were saccadic (prosac-cades vs antisaccades) and visual search tasks. In terms of
the former, Trippe et al [110] presented participants with
pairs of fear-provoking spider pictures alongside neutral
pictures, with instructions to fixate on a target category.
Participants exhibited significantly more errors and in-
creased latencies during prosaccades to spider pictures, but
were quicker to perform antisaccades from spider pictures,
signifying a propensity for threat avoidance. In another
study, it was conversely established that spider phobic
participants not only fixated more quickly on fear-relevant
targets but also displayed longer latencies when asked to
turn their attention away from those images [111]. I n aseparate line of enquiry, Rinck and Becker [112] admin-
istered a range of visual search tasks and observed that
spider phobic participants displayed faster detection and
increased attentional disruption to spider pictures. Likewise,
another visual search task conducted amid an array of task-
irrelevant distractors revealed greatest fixation durations for
spider distractors [113]. On the whole, it remains unclear
whether the mechanisms of initial attentional capture
followed by active avoidance or delayed disengagement
of attention from threat stimuli chiefly underpins spider
phobia. Additional research is thus warranted to clarify the
temporal pattern of eye movement dysfunction in both SP
and specific phobias.
2.2.2. Other anxiety disorders
Scant eye-tracking research has been conducted in other
anxiety disorders, with the exception of a few studies
devoted to OCD, PTSD, and GAD. Before proceeding, it is
important to delineate key differences amongst these
disorders, though each is primarily characterized by
excessive and overwhelming feelings of anxiety. Accord-
ingly, OCD is defined by the manifestation of recurrent
thoughts, images, or impulses experienced as inappropriate
or intrusive, thereby prompting repetitive behaviors or
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mental rituals aimed at neutralizing the distress, but
performed in an excessive or irrational manner [36]. In
contrast, PTSD typically develops as a cluster of disturbing
symptoms following an extreme traumatic stressor, whereas
GAD is experienced as undue anxiety and worry over a
range of concerns, attended by somatic symptoms. In an
exploratory eye movement analysis, reduced RSS, number
of fixations, and total scanpath lengths were found in OCD
and significantly correlated with specific clinical symptoms
[114]. Differences in eye-tracking performance between
medicated and nonmedicated OCD groups have also been
observed [115]. However, Kojima et al [64] found no
significant differences between OCD patients and healthy
controls in this regard. In a separate study, PTSD participants
showed increased initial fixations to threat stimuli and
greater overall skin conductance orienting responses in
relation to a display of disorder-specific threat and nonthreat
words[116]. In an investigation of the direction and latency
of initial gazes to pairs of emotional faces, GAD participants
were found to fixate more quickly and frequently on threatfaces[117]. When presented with complex pictures depict-
ing potential, latent, direct threat, or nonthreat themes,
Freeman et al [118] reported that individuals with GAD
failed to exhibit any atypical scanning strategies. At present,
it appears that a consistent and coherent account of eye
movement dysfunction in these anxiety disorders is missing.
Moreover, a lack of corroborating studies and certain
methodological limitations (outlined in the next section)
render these results tentative at best.
2.2.3. Implications and conclusions
On the whole, the most convincing evidence pertaining to
eye-tracking anomalies in the anxiety disorders comes fromSP, with a dearth of relevant studies in other areas precluding
further meaningful conclusions. In addition, existing re-
search tends to suffer from a range of methodological
limitations. Foremost, small participant numbers diminished
the power of the studies, making it less likely for significant
effects to be statistically detected. Some studies, moreover,
used skewed participant groups, for instance, involving
subclinical populations[111]or solely females[108]. Other
inconsistencies include uncontrolled medication status in
almost all studies as well as comorbidity with additional
anxiety disorders and/or secondary depressive conditions
[118]. However, it remains a worthwhile endeavor topersevere with further eye-tracking research into the anxiety
disorders, because preliminary findings from SP show
promise for clinical applications, akin to the cognitive
remediation treatments offered in schizophrenia.
2.3. The mood disorders
A small amount of research has explored visual scanpaths
in the mood disorders, chiefly major depressive disorder
(MDD). Key features of the disorder include depressed mood
and/or loss of interest or pleasure in nearly all activities,
accompanied by a constellation of cognitive and somatic
symptoms[36]. Only half of the studies were actually aimed
at examining eye movements in MDD per se, whereas the
remaining research used mood disordered participants as a
psychiatric control group in eye-tracking studies of schizo-
phrenia. Of the former, Eizenman et al[119]presented MDD
participants with a competing array of visual images
depicting differing themes of dysphoria, neutral, social,
and threat, and reported that MDD participants exhibited
increased fixation durations and dwell times for dysphoric
images. This was interpreted as not merely suggesting a
general eye movement bias toward negatively valenced
information as demonstrated by Caseras et al [120], but
rather a selective allocation of attention to specific content
portraying loss and sadness. In follow-up research, Kellough
et al[121]used a similar paradigm but extended the exposure
time to 30 seconds (instead of the 10.5 seconds in the
original study) to examine the time course of such biased
attention. Though the MDD participants likewise focused
more attention on the dysmorphic images, this was found to
be due to a significantly greater number of fixations. Theserepeated fixations were hypothesized as underpinning
elaborative processing of dysphoric stimuli, akin to a
ruminative cognitive style partially liable for the mainte-
nance of MDD. During repeated pretreatment and posttreat-
ment assessments, existing eye movement dysfunctions was
found to remain largely unchanged, despite improvements in
clinical symptoms, thereby alluding to the trait-like nature of
these anomalies [122]. As mentioned, other studies in the
area pertained to a comparison between MDD and
schizophrenia samples and will thus only be summarized
briefly. Although no distinct scanning style has been isolated
for the disorder, the eye-tracking performance in MDD hasbeen suggested as intermediate between that of schizophre-
nia and healthy controls, especially in terms of fixation
frequency [64,123], though David et al [124] found no
differences between schizophrenia and MDD patients. On
the other hand, Loughland et al [52]administered face and
affect recognition tasks to mood disordered participants and
concluded that their functioning was superior to schizophre-
nia patients and equal with healthy controls, except for a
marked avoidance of salient facial features across all
emotions, particularly for degraded faces.
Once again, these studies have suffered from a range of
methodological limitations, including a lack of corroborating
research, limited sample sizes, skewed participant groups(eg, involving only young adults[121]or mixed unipolar and
bipolar affective patients [52]), uncontrolled medication
status, and undiagnosed comorbidities, thereby rendering
any present conclusions speculative, in anticipation of
further investigations.
3. Directions for future research
In terms of suggested directions for future research, 2
main avenues appear to deserve further exploration. First,
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eye-tracking techniques may be productively applied to a
range of other psychological disorders, notably those keenly
involving elements of social perception. This has already
been initiated for conditions, such as the autism spectrum
disorders [125], and remains to be applied to other
disorders, such as body dysmorphic disorder (BDD). In
particular, relevant findings in BDD will help to inform
existing debates in terms of its nosologic classification,
which has long been disputed. At present, BDD is
categorized as a somatoform disorder [36], but various
arguments have been made toward its reclassification
amongst the newly conceptualized obsessive-compulsive
spectrum disorders, anxiety disorders, or even psychotic
disorders (see Toh et al [126]for a comprehensive review).
Distinct similarities and differences in eye-tracking perfor-
mance in BDD relative to OCD, schizophrenia, and other
psychiatric disorders would therefore shed further light on
these prevailing nosologic debates. Such a bottom-up
approach will also permit a more detailed delineation of
potential domains of executive dysfunction, for instance,involving attentional biases or deficits in visual organization
and processing. Second, concurrent neuroimaging studies
will facilitate investigations into potential neurologic
deficits, upon the detection of eye movement dysfunction.
More specifically, parallel brain imaging techniques will
help to isolate functional and structural cerebral anomalies,
which likely contribute toward eye-tracking deficits. This
has been previously attempted in schizophrenia [98,99]and
forms the next logical step for related studies of similar
conditions. In this way, linking behavioral disturbances with
underlying neurobiological correlates should in turn not
only advance existing etiologic formulations but also assistin the identification of specific endophenotypes underpin-
ning related psychological disorders.
To facilitate such future research and overcome the
existing methodological inconsistencies, which have
plagued visual scanpath research to date, it would be prudent
to recommend a standardized set of experimental tasks,
naturally with the option of modifications beyond this fixed
paradigm. In line with the findings of the current review,
relevant stimuli used should include emotional faces as well
as geometric figures. For the standardized facial affect
paradigm, the general consensus has been that 5- to
10-second presentations of a series of facial images depicting
the entire range of the 6 universal human emotions (ie, angry,disgusted, fearful, happy, sad, and surprised), along with a
neutral face serving as the control condition under free-
viewing conditions would suffice. The best available stimuli
for this task is probably the set of facial images by Ekman et
al[91], though these ideally require updating, with inclusion
of full color. In terms of the geometric figure, the wide
assortment used thus far in research precludes an unequi-
vocal decision, but perhaps the Rey-Osterrieth Complex
Figure, with its well-documented validity and reliability
[127], would be a sound choice. Additional novel research
thereafter involving the use of complex social scenes as well
as digitalized moving images would serve as a constructive
adaptation. On the whole, such a systematic approach will
certainly add to the growing body of knowledge concerning
how attentional allocation and visual anomalies contribute
toward the etiology and maintenance of a range of
psychiatric presentations.
4. Conclusion
Advances in modern eye-tracking techniques have
rendered this line of research especially fruitful. Studies
analyzing visual scanpaths in schizophrenia have been fairly
well documented, converging on generalized scanning
deficits of a restricted nature, characterized by fewer
fixations of increased durations, with shorter scanpath
lengths, and a marked avoidance of salient features across
a range of visual stimuli, but notably in relation to facial
emotion perception[45-47,51-53]. There is thus an emerging
consensus involving dual impairments in configural proces-sing as well as gestalt perception. In other words, individuals
with the disorder are not only unable to form significant
connections between discrete portions of a face but also fail
to integrate it into a meaningful global structure. Added
research is nevertheless essential to clarify the trait vs state
debate and to elucidate the contributions of specific
symptoms and syndromes and, in particular, delusions. In
relation to the anxiety disorders, explorations into SP have
proposed a hyperscanning strategy, represented by reduced
number of fixations of shorter durations and increased
scanpath lengths, coupled with a respective avoidance and
scrutiny of salient and nonsalient facial features, most
evident for negatively valenced emotions [106,107]. Theother anxiety disorders offered a less coherent picture,
necessitating further investigations. From the perspective of
the mood disorders, the most striking finding related to
disproportionate foveal attention to dysphoric images,
analogous to the classic ruminative thinking style frequently
underlying MDD [119,121]. However, existing methodo-
logical limitations, involving a lack of corroborating studies,
limited sample sizes, skewed patient demographics, uncon-
trolled participant comorbidities, and medication status, need
to be overcome. Future endeavors could yield valuable
clinical utility, in light of treatment applications already
evident for schizophrenia.
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