Current visual scanpath research: a review of investigations into the psychotic, anxiety, and mood disorders

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Comprehensive Psychiatry 52 (2011) 567 – 579 www.elsevier.com/locate/comppsych

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 b

a Departments of Behavioural Science and Psychiatry, The University of Melbourne, Melbourne, VIC, Australia Cognitive Neuropsychology Laboratory, Monash Alfred Psychiatry Research Centre, School of Psychology and Psychiatry, Faculty of Medicine, Nursing, and Health Sciences, Monash University, Melbourne, VIC, Australia c Brain Sciences Institute, Swinburne University of Technology, Melbourne, VIC, Australia d Department 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 eyetracking 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. © 2011 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 from visible light to construct a meaningful representation of the surrounding environment. Accordingly, we are able to perform intricate tasks, such as identifying objects, perceiving color, and estimating distances, all crucial to

our everyday functioning. Despite these concrete operations, 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 populations involving the psychotic, anxiety, and mood disorders. We conclude with suggested directions for future research.

1. Physiology of eye movements ⁎ 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 © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.comppsych.2010.12.005

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

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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 the current review.

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?

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 later expanded 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 a feature ring. Consequently, the reproduction of successive eye movements in a replica of the original scanpath 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

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 videooculography, 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 refers to 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 milliseconds. 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 an alternative 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 categorization 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, simultaneously perceiving facial features in parallel [19]. Moreover, configural representation, or the interrelations among internal 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

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[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 4° to 5° [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 fixations to appropriate points of interest, where further visual information is acquired. Owing to its ecologic validity and significance in day-today human interactions, research has examined eye movements 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 with longer 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 advantage 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 with normal 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 of psychiatric conditions. 2.1. The psychotic disorders Most visual scanpath research in clinical populations has focused on the psychotic disorders, especially schizophrenia. This disorder has a heterogeneous presentation and may be classed into various subtypes, but is typically characterized 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 generalized 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 schizophrenia 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 schizophrenia who exhibited poor eye-tracking performances. Anomalously, patients with catatonic schizophrenia performed better relative to healthy controls, whereas eye movement parameters and clinical variables remained largely uncorrelated. 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 scanning—“extensive” vs “minimal”—were 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 of fixations 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 methodology 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 parameters across discrete facial emotions [48-50]. However, on the whole, virtually all studies have converged on the existence of a “restricted” scanning 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 followup 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 somewhat 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 total scanpath 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 laterstage 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 involving the presentation of upright and inverted faces, it was shown that the former drew significantly more preattentive saccades from healthy controls, whereas the eye movements of 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 “face” percept 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

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(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 contextembedded situations, reduced saccadic activity in contextfree 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 impairments during mental state assessments. The finding involving 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 ostensibly 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 increased staring 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 on a 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 nosologically 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 landscapes 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 schizophrenia 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 but also 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 syndromes Traditional 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 correlations between scanpath aberrations and specific symptom or syndrome factors. An initial study proposed a rather simplistic theory relating extensive and restricted scanning styles to positive and negative symptoms respectively [38]. Though later research has reported minimal relations between eye movement parameters and symptom complexes [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 symptoms, 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 shorter durations 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 investigations into the area are necessary to elucidate further significant relationships. 2.1.6. The special role of delusions Delusions have 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 comparison 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 accuracies. 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 viewing times 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 impairments 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

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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, risperidonetreated 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 direct vision 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 schizophrenia 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 advantageous 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 significant frontal lobe dysfunction, alongside visuospatial working memory deficits [63,71,73]. Moreover, eye movement research in schizophrenia does carry direct therapeutic implications, in terms of the remediation of faulty facial emotion perception, with attendant benefits for the day-today social living of affected individuals. To this end, several training packages, to be delivered with the aid of eyetracking 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 improvements 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 when an 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), posttraumatic 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 and persistent 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 expressions, a “hyperscanning” strategy was uncovered, represented by reduced fixations in frequency and duration, as well as increased raw scanpath lengths [106,107]. Furthermore, it was demonstrated that individuals with SP displayed an active avoidance of salient facial features, especially the eyes, coupled with extensive scanning of nonsalient facial regions, 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 interactions. 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 attention [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 fearrelevant stimuli, resulting in shorter overall fixation durations. Other typical paradigms were saccadic (prosaccades 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 increased 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]. In a separate line of enquiry, Rinck and Becker [112] administered 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 taskirrelevant 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. Accordingly, 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 threat faces [117]. When presented with complex pictures depicting 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 from SP, with a dearth of relevant studies in other areas precluding further meaningful conclusions. In addition, existing research 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 to persevere 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

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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 schizophrenia. 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. These repeated fixations were hypothesized as underpinning elaborative processing of dysphoric stimuli, akin to a ruminative cognitive style partially liable for the maintenance of MDD. During repeated pretreatment and posttreatment 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 has been suggested as intermediate between that of schizophrenia 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 schizophrenia 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 performance 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 assist in the identification of specific endophenotypes underpinning 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 freeviewing 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 unequivocal 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 processing 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]. The other 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 methodological limitations, involving a lack of corroborating studies, limited sample sizes, skewed patient demographics, uncontrolled 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. References [1] Wade N, Tatler BW. The moving tablet of the eye: the origins of modern eye movement research. Oxford: Oxford University Press; 2005. [2] Hochberg J. In the mind's eye. In: Haber RN, editor. Contemporary theory and research in visual perception. New York: Rinehart and Winston; 1968. p. 70-99. [3] Noton D, Stark L. Scanpaths in eye movements during pattern perception. Science 1971;171:308-11. [4] Noton D, Stark L. Eye movements and visual perception. Scientific Am 1971;224:35-43.

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