Beyond Traditional Clinical Measurements for ...

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Beyond Traditional Clinical Measurements for Screening Fears and Phobias Pedro J. Rosa, Francisco Esteves, and Patrícia Arriaga

Index Terms— Attentional orienting, eye movements, eye tracking (ET), fear, pupil response, snakes, subliminal exposure.

I. I NTRODUCTION

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Specific phobias can be comparable with other mental disorders since they tend to interfere on social activities and to reduce productivity at work [5]. According to prominent models of anxiety (e.g., attentional control model, model of attentional bias, and information-processing model), the development and maintenance of specific phobia is highly dependent on cognitive processes, especially on attentional mechanisms [6]–[8]. Attentional processes are vital because one function of anxiety is the quick detection of threat, enabling an organism’s rapid reaction to the feared stimulus [9]. According to these models, attention tends to be biased toward feared stimuli. In fact, research with nonclinical samples has suggested that attentional orienting is facilitated by concern-related as opposed to unconcern-related stimuli [10]–[12]. However, this attentional bias seems to be more pronounced in phobic individuals [13], [14]. This distinctive priority by the attention system for potential threat can lead people to an irrational and noncontrolled fear response [15] which may become dysfunctional when it is particularly intense and frequent, and lead to the development of an anxiety disorder [9]. The higher the level of anxiety is (currently or permanently), the more likely the fear defense system become activated and trigger physiological components of fear response, such as skin conductance, cardiac changes, and electrical activity produced by skeletal muscles [16]. This may explain the sensitiveness of threat detection mechanism in phobics. Öhman and Soares [17] advocate that preattentive automatic analysis of potentially threatening cues may be sufficient to activate the fear defense system and trigger the physiological component of fear response. This may explain why individuals with specific phobias, such as snake phobia, tend to show an exaggerated perception of danger and increased physiological arousal responses even when they know that the object of the phobia is harmless (e.g., tiny or plastic snakes). The main goals of the clinical assessment of specific phobias are to establish an accurate diagnosis, frame a treatment plan, and evaluate psychotherapeutic progress and outcome. To reach a comprehensive assessment for specific phobias, three components are used: 1) a clinical interview; 2) self-report measures (questionnaires, monitoring diaries); and 3) behavioral assessment [18]. However, psychophysiological and behavioral measures, which are often used in academic research and reliable correlates of biased threat processing, are seldom used in clinical practice [19]. The main reasons for this unattractiveness are related to considerable costs and training investments required for this kind of

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Abstract— The use of eye movements is a usual method of measuring attentional and emotional response in laboratory. However, when it comes to clinical practice, it is seldom applied. Two studies were conducted to examine whether extraocular and intraocular movements can be used as indices of attentional bias and autonomic activation. In the first study, a free-viewing task, combined with subliminal exposure, showed that highfear individuals tend to orient more their attention toward the visual space where threat-stimuli (snakes) were presented. The findings suggest a reflexive overt attentional orienting bias for subliminal snakes in comparison with subliminal control stimuli. The differentiation between participants with high and low fear of snakes suggested that a disposition to fear snakes affects the initial ocular saccades. In the second study, participants were instructed to discriminate a sign that was randomly displayed at the center of the display while subliminal images were peripherally presented. The results revealed larger pupil dilation for threatening stimuli subliminally presented; again, high-fear individuals showed larger pupillary dilations, independently of the stimulus category. Our results are in line with the assumption that a predisposition to fear is relevant for extraocular and intraocular movements when exposed to threat stimuli. These findings suggest that eye measurements, combined with subliminal exposure techniques, could be a reliable and nonintrusive aid tool to be used for the assessment and treatment of fear and phobias.

NXIETY disorder impacts approximately 18% (i.e., approximately 40 million) adults in the United States [1], and phobias are the most common anxiety disorders [2]. However, specific phobias such as animal phobia (e.g., snake phobia) are not the primary motive for seeking treatment [3]. This might be related to the perception that this specific phobia is simple to overcome, rarely capturing the focus of clinical attention [4].

Manuscript received February 13, 2015; revised May 7, 2015; accepted May 16, 2015. This work was supported by the Fundação Para a Ciência e Tecnologia of Portugal through the FCT-MCTES Project under Grant SFRH/BD/46965/2008. The Associate Editor coordinating the review process was Dr. Zheng Liu. P. J. Rosa is with the School of Psychology and Life Sciences/COPELABS (ULHT), Lisbon 1749-024, Portugal, and also with the ISCTE–University Institute of Lisbon, Lisbon 1649-026, Portugal (e-mail: [email protected]). F. Esteves is with the Department of Social Sciences, Mittuniversitetet, Östersund 831 25, Sweden (e-mail: [email protected]). P. Arriaga is with the Department of Psychology, ISCTE–University Institute of Lisbon, Lisboa 1649-026, Portugal (e-mail: [email protected]). Color versions of one or more of the figures in this paper are available online at http://ieeexplore.ieee.org. Digital Object Identifier 10.1109/TIM.2015.2450292

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(extraocular and intraocular) vary as a function of the level of fear, validating the use of ET 2.0 for screening and assessing the treatment effectiveness in specific phobias. In our first study, we investigate attentional orienting processes in a freeviewing task while snakes were simultaneously presented with control images (neutral stimuli) at very short exposure times. The number of valid saccade endpoints (hits) in the areas, where the subliminal stimuli were exposed [areas of interest (AoI)], was used as an index of reflexive overt attentional orienting [44]. We expected that participants with high FS would show a pronounced attentional bias toward the snake area. In the second study, as the confrontation with the concerned/feared stimulus tends to elicit a series of changes in a specific neural circuit, resulting in physiological arousal, we expected larger pupil dilation in the participants with high FS when snakes are presented subliminally in comparison with control stimuli [45]. FS was measured because snakes are one of the most feared stimuli by humans and a common object of phobias [46]. II. S TUDY I A. Method

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equipment (e.g., stimuli presentation software, psychophysiological recording unit, and EEG cap) [19]. Also important, in the laboratory context, that the patient needs to be fully attached with sensors and cables, which creates an artificial context and may increase the individual’s anxiety. Besides, behavioral measures such as reaction times, often measured by the use of key-press responses, may reflect more than simply biased attentional processes [20], [21]. Furthermore, self-report data, when used in isolation, are highly susceptible to exogenous influences, sustaining the use of complementary measurements [22]. To overcome the above limitations, eye movement recording or eye tracking (ET) can be a nonintrusive approach [23]. ET has been successfully applied in clinical [11], [13] and medical domains [24]–[26] as it allows researchers to obtain measures closely related to attention and emotion [12], [20], [27]. The most recent generations of ET systems, which use relatively low-cost cameras [28], [29], allowing a quick calibration process [30] with motion correction algorithms for large head movement [31], [32] and an accurate estimation of the point of regard [33], [34], are called in this paper as ET 2.0 (in analogous with Web 2.0). Several ET.2.0 systems with different pattern recognition algorithms, accuracy levels, performance, and cost have been applied to study a wide variety of phenomena related to attention and vision [35], [36]. Recent studies using ET 2.0 have shown that initial ocular saccades are influenced by supraliminal and subliminal emotional content [37]–[40]. However, little is yet known about this in free-viewing tasks. As far as we know, no studies using ET 2.0 have applied subliminal stimuli competition during a video presentation in a spontaneous viewing activity. Despite the use of a wide spectrum of technological particularities in ET 2.0 systems [35], [36], as well as a large set of techniques [31], [32] and paradigms [11]–[14], it is still unclear whether the human attentional system is sensitive to threatening stimuli (snakes) when control stimuli are competing subliminally. Furthermore, and given that pupil dilates with sympathetic activity [41], it can be seen as a reliable and nonintrusive measure of emotional arousal [42]. Despite being a physiological component of arousal, it is not a common index used in subliminal exposure. If emotions and pupil size variation are reliably associated with each other, then ET 2.0 would offer a possibility for nonintrusive monitoring of emotion-related reactions during subliminal exposure to emotional stimuli. To the best of our knowledge, the only study that specifically recorded the pupil response during subliminal exposure is the work by Bijleveld et al. [43]. Their data indicate that valuable subliminal rewards led to larger pupil dilation in comparison with nonvaluable rewards. In this paper, we attempted to extend prior visual attention paradigms and techniques by combining subliminal visual competition with ET. With our approach, we intend to provide reliable eye measurements that can be used as a proxy for emotional/affective disorders. Taking these prior studies into consideration, the aim of this paper is the assessment of fear of snakes (FS) by recording the eye movements toward different stimuli. In two studies, we aim to support the hypothesis that eye movements

1) Participants: Fifty female students (Mage = 25.32 and SDage = 6.70) from two Portuguese universities volunteered to take part in this paper. Participants provided their written informed consent prior to entering the study. They were told that they were free to withdraw at any time and that confidentiality and anonymity of their individual data would be ensured. Female participants were chosen because they tend to report high and more frequently FS than men [46], [47]. 2) Materials and Procedure: A free viewing of a 4-min video segment, taken from the movie Koyaanisqatsi [48], was used as the experimental task. The particular features of this movie, with only landscapes, but no actors nor dialogs made it an adequate choice for a neutral stimulus and a mean to expose participants to a natural context in which subliminal stimuli were presented. Twenty pictures (10 snakes and 10 neutral, e.g., daily life objects) selected from the International Affective Picture System (IAPS) were used as subliminal stimuli [49]. Nonaffective features of the pictures, such as apparent contrast and luminance, were previously analyzed using ImageJ v1.47 software [50]. Twenty pairs of images were used, consisting of counterbalanced combinations of 10 snakes and 10 neutral pictures. Both snakes and control pictures had similar levels of luminance, t (18) = 0.56 and p = 0.58, and apparent contrast, t (18) = 0.78 and p = 0.44. All images were resized to a 320 × 256 resolution, using Photoshop TM CS3 software. These images were inserted randomly in the video (over layered) using MAGIX Movie Edition Pro-10 software. Altogether, 20 trials (2 randomized blocks × 10 pairs), with a duration of 1/60 s,1 were presented in the upper corners of the screen (one image per corner) while 1 Subliminality was pretested with two different presentation times (17 and 30 ms) with participants who did not take part in this paper. Half of the participants (5 in 10) noticed the stimuli’s content with a 30-ms presentation. However, with 17-ms presentation, none reported having seen any stimuli nor their content.

ROSA et al.: BEYOND TRADITIONAL CLINICAL MEASUREMENTS FOR SCREENING FEARS AND PHOBIAS

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Fig. 1. Video time sequence with two blocks of 10 trials each. Note that these example images were not among the experimental stimuli. Fig. 2. Proportion of hits in the AoI as a function of image type and FS. The error bars represent the standard errors of the mean.

B. Data Preparation Eye blinks, drifts, and outliers (±2 SD) were removed from raw gaze data and coded as missing values. To examine the number of hits immediately after the presentation of subliminal images, two rectangular AoI were drawn around each location where the stimuli were introduced on the screen. The following criteria were used to consider that a valid trial occurred: the endpoint of the initial saccade must have been within one of the AoI with saccade latency between 80 ms (5 frames) and 600 ms (35 frames) [54]. Considering the total number of valid trials for each participant, the percentage of hits in the two AoI was computed. The SNAQ median-split (Mdn = 13.5) was used to set apart participants with low FS (n = 29) from participants with high FS (n = 21). Data were analyzed with a mixed factorial analysis of variance (ANOVA). Greenhouse–Geisser corrected degrees of freedom were used to report significant levels. A Bonferroni correction was applied for pairwise comparisons.

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a movie sequence with 1280 × 1024 resolution was shown at 60 frames/s (see Fig. 1). The interstimulus interval (ISI) varied from 11 to 14 s to avoid expectation effects. The picture size was 7.69° × 6.26° of visual angle at a viewing distance of 60 cm. All participants were recruited from classrooms and invited to participate in the experiment. The experiment occurred in a single session, in an isolated laboratory room with constant illumination (42 lx). The true purpose of this paper was not fully disclosed beforehand. Instead, participants were informed that this paper was about how people watch a movie. This free-viewing instruction was given to avoid any top-down processes [51] and to control for anticipatory anxiety. Participants were told that the instructions would be provided on the computer screen at the beginning of the experiment. The instructions were as follows: A video will be presented. Please pay attention and try to remain still while the video is presented. At the end, some questions will be asked. The participants were instructed to always look at the screen to avoid ocular drifts. The stimuli were presented and the responses recorded on a Tobii-T60 ET System (Tobii Technology AB, Sweden), integrated into a thin-film transistor (TFT) 17-in monitor and connected to an Intel core2duo 6550 desktop computer. Gaze data were recorded binocularly at 60 Hz with an average accuracy of a 0.5 visual angle. After task completion, the stimuli unawareness was tested. Participants were also asked about the purpose of this paper, whether they thought any of the tasks performed had been related and whether anything about this paper seemed strange or suspicious to them. If participants mentioned that they saw pictures of snakes or any other content, they would be excluded from the experiment. Of the 50 participants, 28% (n = 14) mentioned having seen flashes, and of those, only 12% (n = 6) referred to having seen pictures. Therefore, no participants were excluded from analysis. Next, participants were instructed to fill out the Snake Anxiety Questionnaire (SNAQ) [52]. The SNAQ is a 30-item selfreport scale, with a dichotomy response format (true/false), which enables the assessment of the cognitive-verbal component of the FS. SNAQ has showed good reliability in [52] and [53], ranging Kuder-Richardson (KR)-20 values from 0.78 to 0.90. In this paper, the SNAQ had a KR-20 of 0.79. At the end, the participants were thanked, debriefed and dismissed.

C. Results

The proportion of hits was calculated based on the sum of hits in the AoI, divided by the number of valid trials. A 2 (image type: control versus snakes) × 2 (FS: low versus high) ANOVA showed a main effect of image on proportions of hits, F (1, 48) = 5.74, p = 0.021, and η2p = 0.11. Consistent with our hypothesis, a higher percentage of hits were found in the AoI where snakes were presented (M = 0.27) than in the AoI for control stimuli (M = 0.23), t (49) = 2.36, p < 0.001, and d = 0.35. A significant interaction between image and FS was also found, F (1, 48) = 9.37, and p = 0.004 and η2p = 0.16 (see Fig. 2). Simple main effects revealed that the proportion of hits for snakes was higher in participants with high FS (M = 0.32) than in participants with low FS (M = 0.23), t (48) = 2.36, p = 0.003, and d = 0.93. Furthermore, for participants with high FS, the proportion of hits for snakes (M = 0.32) was significantly higher than in the control AoI (M = 0.22), t (20) = 3.56, p = 0.001, and d = 0.98. There were no other significant effects (ps > 0.05). D. Discussion The results revealed that participants with high FS tend to orient their attention more toward the visual space where

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greater fear. To form two opposite balanced groups, those who responded with 1 or 2 on the FSS-II snake item and those who scored 6 or 7 were invited to participate in a further study. From the initial participants, only 51 (26 snake-fearful and 25 nonfearful) were chosen based on the mentioned criteria. Of these, 84.3% were females (n = 43) and 15.7% were males, ranging from 18 to 55 years old (M = 25.55 SD = 8.25). All the participants had normal or corrected vision and most were Portuguese (n = 38, 76%). 2) Materials and Procedure: In this experiment, in addition to the measurement of cognitive FS through SNAQ, the trait and state anxiety as well the level of fatigue were assessed. Trait and state anxiety were assessed through the State Trait Anxiety Inventory (STAI) [59]. The STAI has both state and trait scales with each scale consisting of 20 items (e.g., I feel nervous), evaluated on a four-point Likert response format scale (1 = almost never; 4 = almost always). Scores in both trait and state scales can range from 20 to 80, with higher scores reflecting higher levels of anxiety. This measure has shown good reliability in [60] and in this paper had a Cronbach’s alpha of 0.77 for the State and 0.85 for the Trait subscale. The KR-20 was of 0.66 for SNAQ. The level of fatigue was measured through the Pichot fatigue scale (le questionnaire de la fatigue) [61]. This is a short eight-item, easy to administer tool that measures the individual’s level of fatigue at the moment, consisting in a four-point Likert scale from 0 (not at all) to 4 (extremely). This fatigue scale presented a good internal consistency (α = 0.81). Due to its interference with attentional processes [62], [63], the level of fatigue was similar for both groups (low fear versus high fear) before the experiment, t (49) = −1.11 and p = 0.274. Sixty images were selected from IAPS [49] consisting of 20 negative (10 snakes + 10 other feared animals), 20 positive and 20 neutral. All images were converted to grayscale 8-bit portable network graphic (.png) image file format, controlled for luminance and apparent contrast and resized to 320 × 256 resolution, using ImageJ 1.47 software [50]. The image size was 7.69 × 6.26 of visual angle at a viewing distance of 60 cm. Stimuli were presented through Superlab 4.0 presentation software [64] for Windows in an Intel core2duo 6550 desktop computer, which was connected to a Tobii-T60 ET System (Tobii Technology AB, Sweden) and integrated into a 17-in TFT. Blanks and background were presented on a gray color (Red-Green-Blue: 150, 150, 150) to minimize differences in luminance during stimulus presentation. The eye tracker received the video signal through the Video Graphics Array capture card from the PC running Superlab program. The pupil diameter was binocularly measured with a temporal resolution of 60 Hz. Gaze data were used to control the locus of the participant’s overt visual attention while the pupil diameter was being recorded. Upon arrival at the laboratory of experimental psychology, each participant signed a consent form and was seated in a chair in a sound-proof room with a constant illumination (42 lx). The true purpose of this paper was masked to control for anticipatory anxiety. Each participant was instructed to count only the number of signs + and to ignore the o signs. One of the two following signs (0 or +) was randomly

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snakes are presented when exposed to two concurrent subliminal stimuli. Thus, the present findings suggest a reflexive attentional orienting bias for snakes presented subliminally as opposed to control stimuli. Because participants were not aware of stimuli, attentional orienting seemed to be activated by the subliminal threat-related stimuli. The selective sensitiveness of the fear defense system to concern-related stimuli is indicative of a quick detection of snakes, supporting the assumption that a subliminal attentional orienting bias, as prioritized processing, is facilitated to snakes, while other fear-irrelevant stimuli are inhibited [15], [55]. These results are in line with studies showing that individuals with high level of anxiety/fear have lower perceptive thresholds to their concern-related stimuli, thereby orienting their attention toward threat [11], [13], [20]. These results corroborate previous experimental studies, indicating that individuals with a specific fear tend to have exacerbated preattentive bias to the feared stimuli in complex visual contexts [56], [57]. However, it is important to address some potential limitations of this first study. First, the present findings cannot be generalized to males. A mixed male and female sample would give more robustness to our findings. Second, since snakes were only compared with control stimuli (pictures with neutral content), it is quite difficult to know whether this ocular behavior is specific to their concern-related stimuli or also occurs during other threatening stimuli (e.g., sharks or lions).

III. S TUDY II The second study addressed the limitations of the previous study using a mixed gender sample and four image categories instead of two. In the first study, we found that participants with high FS showed a higher percentage of ocular movements (initial saccades) toward areas where snakes were subliminally presented than control stimuli. However, the specificity of the ocular response to concern-related stimuli was impossible to examine. Therefore, a presentation of four categories of stimuli in this paper was focused on the specificity of the fear module using not only neutral pictures as controls but also positive and other threatening-related pictures. It was also of interest to test whether pupil reactivity could be taken as an index of emotional arousal when concern-related stimuli are subliminally presented. To our knowledge, there is no previous evidence whether snakes when presented subliminally are capable of affecting pupil size. We hypothesized that participants with a high level of FS would show larger pupil dilation those with low level of fear. Furthermore, it is expected that fear module operates as a specific fear detector, that is, snake stimuli lead to larger reactivity in comparison with other control stimuli in participants with high level of FS. A. Method

1) Participants: Initially, a sample of 147 undergraduate psychology students of a Portuguese University was screened through classroom announcements to first respond to the Fear Survey Schedule-II (FSS-II) [58]. The FSS-II lists 51 commonly feared objects and real life events. Participants rated their fear of each object and event on a 1 (none)–7 (terror) scale. One object listed is snake. Higher scores indicate


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Fig. 4. Mean pupil dilation as a function of fear group after controlling for the effect of trait anxiety level. The error bars represent the standard errors of the adjusted mean. Fig. 3. These same pictures were not among the experimental stimuli. This picture was not among the stimuli.

B. Data Preparation

C. Results

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presented at the center of the screen for 500 ms before image onset. Due to the fact that pupillary response is also sensitive to high cognitive demands, it was essential to conduct a simple discrimination task. Following two practice trials, 60 pictures were randomly displayed at one of the four screen corners of the screen for 17 ms through a Latin-square presentation. The ISI was randomized (8, 10, or 12 s) to avoid any expectation effects (see Fig. 3). Next, participants were instructed to fill out the SNAQ at home and to return them within a week at the Laboratory of Computing Psychology. Then, the participants were thanked and dismissed.

F (3, 36) = 108.59 and p < 0.001, presenting snakes (M = 6.11 and SD = 0.39) and other animals (M = 6.30 and SD = 0.44) higher mean arousal ratings compared with positive (M = 4.09 and SD = 0.50) and neutral images (M = 2.74 and SD = 0.65).

Eye blinks, drifts, and outliers (±2 SD) were identified from raw pupil data and linear interpolation was made on a trial by trial basis to estimate pupil size. Pupil artifacts were randomly distributed across experimental conditions. Pupil data were smoothed using a 10-Hz low-pass filter. The pupil size data were analyzed using a 1-s prestimulus baseline correction. The baseline pupil diameter was defined as the average of pupil diameter recorded during the 1 s (60 samples) that preceded the picture onset. Peak dilations were computed as the maximum baseline corrected pupil diameter in a 6-s window after image onset. Pupillary reactivity was calculated as the difference between pupil peak and pupil baseline. No difference in terms of age was found for both groups t (49) = −0.40 and p = 0.688. The low- and highfearful ones were also similar regarding gender composition, 2 (1) = 1.19 and p = 0.248. The SNAQ mean score χYates was significantly different between the low-fearful (M = 7.0 and SD = 4.15) and high-fearful (M = 22.20 and SD = 3.36) groups. For anxiety, the high-fearful group showed significantly a higher state anxiety level (M = 41.80 and SD = 12.25) than the low-fearful group (M = 32.65, and SD = 8.40, t (49) = −3, and 12 p = 0.003). A similar pattern was found for trait anxiety level, showing the high-fearful group a significantly higher trait anxiety level (M = 36.11; SD = 8.42) than the low-fearful group (M = 44.12; SD = 11.78, t (49) = −2, 80 p = 0.007). Rated arousal differed significantly between picture categories

Ten positive and 10 neutral images were randomly selected from the presented images (20 for each category) allowing a balanced mean comparison across the four picture categories. To control the effect of anxiety trait level on pupillary amplitude, a repeated-measure full factorial analysis of covariance (ANCOVA) with one within-subject factor (image type: snakes versus other feared animals versus pleasant versus neutral) × one between-subject factor (fear of snakes: low versus high) was performed. The linear mixedeffects models procedure in the Statistical Package for Social Sciences software version 22 was chosen due to the advantage of dealing with missing values and correlated within-subject errors [65]. Anxiety state level and arousal rating of images were not included as covariates in the model since they were not correlated with pupillary reactivity [66]. The covariate (anxiety trait level) was centered before the analysis as recommended in [67]. Missing data were completely at random (Little’s Missing Completely at Random test: χ2(578) = 248.82 and p > 0.05). Both factors were treated as fixed effects and the maximum likelihood method was used to estimate the covariance matrix (compound symmetry) [68]. Cohen’s f 2 effect size measure was manually computed based on the recommendations of Selya et al. [69]. Bonferroni correction was applied for pairwise comparison of adjusted means. The repeated-measures ANCOVA revealed a main effect of FS on pupillary reactivity after controlling for trait anxiety level, F (1, 50) = 4.509, p = 0.039, and f 2 = 0.02. As shown in Fig. 4 and consistent with our hypothesis, pupillary reactivity was higher in participants with high FS (M = 0.43) than in participants with low FS (M = 0.33). The results concerning the main effect of type of image on pupillary reactivity, after controlling for trait anxiety level, partially support our snake-specific response hypothesis. F(3, 150) = 3.15, p = 0.027, and f 2 = 0.07. A multiple mean comparison showed that pupillary reactivity was sig-

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IV. G ENERAL D ISCUSSION

Fig. 5. Mean pupil dilation as a function of the type of image after controlling for the effect of trait anxiety level. The error bars represent the standard errors of the adjusted mean.

D. Discussion

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nificantly higher to snakes (M = 0.41) than to neutral (M = 0.35), t (150) = 2.90, p = 0.025, and d = 0.24. However, no significant differences between snakes, feared animals, and positive images were found on pupillary reactivity (see Fig. 5). There was no significant interaction between FS and image type ( p > 0.10).

The findings of these two studies offer valuable insights into the relationship between fear and eye movements. In the first study, a free-viewing task showed that participants with high FS tend to orient more their attention toward snakes than control stimuli. These results validate the use of extraocular eye measurements for differentiation between participants with high and low FS. Furthermore, our results extend previous findings of enhanced spatial attention to threatening stimuli in phobic participants [21], [57], suggesting that when competing simultaneously with neutral stimuli in visual space, snakes take it all in terms of attentional orienting, probably due to being a fear-relevant stimuli. Both of our studies extend previous research by showing that subliminal exposure paradigms, when combined with ET 2.0 can offer valuable intraocular and extraocular indexes to differentiate low-feared from high-feared individuals. Data from the first study are in accordance with [7], which argue that fearful individuals typically show a wide attentional focus, enabling faster threat detection. In a similar vein, the higher sensitivity to snake stimuli by snake fearful individuals may also lead to scanning the environment for potential threat more than individuals with low FS [75]. These findings are also consistent with those of Calvo and Lang [10], who found a higher probability of an initial fixation on supraliminal emotional images when paired with neutral pictures. The differentiation between participants with high and low FS suggests that FS disposition moderates the programming and execution of the initial ocular saccades, indicating that eye movements, especially initial saccades are associated with the level of fear. In the second study, we used a simple discrimination task with a peripheral subliminal presentation. Contrary to what we expected, no specific fear response in participants with high FS was found in snake images. These results are dissonant with those of [17] where participants with high FS showed a sympathetic exacerbation to snakes images. It is possible that as the arousal of a stimulus increases, the stimulus becomes increasingly likely to trigger a sympathetic response regardless of the individual’s level of trait anxiety [76], [77]. This may reflect a stimulus response generalization, that is, a processing mechanism based on image features similarity between the emotionally laden stimuli [78]. Our findings also indicated that participants with high FS showed larger dilations while controlling for the trait-anxiety level. These results reinforce the link between the fear module and unspecific hypervigilance or heightened alertness even prior to detecting a threat stimulus [16], [17]. In this perspective, individuals with high FS are constantly scanning the visual field, enabling a quicker processing and detection for signs of potential threats in the visual periphery [75]. Paralleling a large body of [79], our results suggest that sympathetic responses are thought to be operated in a relatively rudimentary fashion, which might minimize false negatives and increase the number of false positives. Furthermore, trait anxiety explained some variation in pupillary reactivity, supporting the idea that may act as an additive factor for the prioritization of emotional information [7]. In addition, it can also be argued that the

This second study sought to determine whether pupil size, as an index of physiological arousal, could be affected when threatening images were subliminally presented. The findings suggest that pupil dilation was larger in the participants with high FS than in the participants with low FS. Thus, these results support the initial hypothesis that individual’s level of fear is involved in sympathetic response [16]. Higher pupillary reactivity to images subliminally presented shows concordance between self-reported FS (SNAQ) and physiological response, even after controlling for the trait anxiety level [70]. Moreover, when trait anxiety level was included as covariate in the statistical model, Cohen’s f 2 for FS decreases from 0.03 to 0.02. This suggests that trait anxiety level also appeared to explain some variation in pupillary reactivity [7]. Interestingly, snakes were expected to evoke larger amplitudes not only than neutral images but also than other emotionally valenced images. In the present experiment, the absence of any differential pupil response between negative and positive emotional content suggests a low sensitivity of the fear module to the hedonic valence of stimuli, but the pupil response shows an almost similar pattern to arousal ratings [71], [72]. This suggests that perhaps the fear module tends to respond primarily to more arousing stimuli. Thus, there was no statistical evidence that snakes led to higher pupillary reactivity in high-feared participants. Perhaps these less expressive results can be explained due a carry-over effect produced by the cognitive load in the discrimination task that preceded the subliminal exposure, obscuring larger pupil responses [73]. Thus, it is important to note that our results support the evidence for a differential preattentive processing for fearrelevant stimuli when compared to neutral [12], [16], [17] and that pupillary reactivity can be an important noninvasive index of fear level without conscious effort [74].


should rely on three aspects. First, phobic patients usually tend to avoid specific-concerning objects and situations in which they experience relatively high levels of anxiety. Our combined methodology could possibly reduce the unpleasantness in patients at early stages of the therapeutic program. Second, in exposure therapy interventions, ocular metrics, similar to other psychophysiological indexes, can serve as a therapeutic success index, complementing other measures such as self-report instruments. Third, since emotionally laden stimuli, even when presented subliminally, can still lead to emotional reactions, subliminal exposure feared stimuli may already reduce the phobia, while at the same time might prevent extreme and unpleasant emotional responses [83]. Despite the seldom use of ET 2.0 in clinical and medical practice, its use is promising for future years [26]. ET 2.0, due to its mobility and flexibility, allows clinicians to record eye movements in nonlaboratory clinical contexts. In fact, clinicians are able to set up a quick and portable eye analysis laboratory wherever patients are [35]. Moreover, other ocular indices such as blinks, vergence, and accommodation can be explored and they may be a rich source of data [84]. For instance, blink rate is quite sensitive to cognitive load and could be a good index of emotional suppression [85]. Empirical studies using emotional paradigms have shown that attentional biases in anxiety individuals commonly disappear following treatment [86], [87]. Similarly, future therapeutic applications using the paradigms and the methodology we have presented, combined with different types of ocular analysis [88], might also be important, especially when dealing with resistant children who are undergoing therapy for overcoming fears.

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high- and the low-fear groups did not differ sufficiently in terms of fear as they were defined by means of a median-split procedure. In other words, there is a possibility that a larger clinically meaningful difference in fear levels between both groups would lead to a specific response to snakes. The findings of the second study also underline the use of ET 2.0 combined with subliminal exposure for differentiation between participants with high and low levels of fear. Both studies offer new contributions to our understanding of the relation between eye movements and emotional fear response. The results have shown that subliminal exposure can be combined with ET 2.0 as an assessment aid tool for future studies on attention and emotion, especially in the clinical context. The simple tasks that we developed and grounded on previous empirical research findings and theory were sufficient to obtain reliable ocular measurements and to assess how the individual’s evaluative system reacts to fear and to control stimuli. The results showed that extraocular movements (initial saccades) and intraocular movements (pupil dilations) can be affected by emotional content and level of fear. Nevertheless, we must also be cautious in making firm conclusions about the attentional and emotional responses observed in these participants. Since humans use trichromatic color vision, it was our intention to present stimuli with high ecological validity, but the repeatability of studies using the same tasks is crucial. A higher methodological control of stimuli’s physical features, such as spatial frequency analysis through the fast Fourier transform, could be relevant to use in future studies [80]. One of the limitations of both experiments is that we did not assess the predisposition of participants to fear other animals beside snakes. This information might have helped to understand how large is the spectrum of fear and how this could be related to fear responses. Another limitation is related to the levels of anxiety participants might have experienced during the experiment. The reapplication of the Trait Anxiety Inventory [59] at the end of the experiment could be relevant to examine whether the subliminal presentation of fear stimuli might also increase the levels of state anxiety. On the whole, the results from our studies suggest that participants with a high level of fear tend to overtly orient attention toward threatening-stimuli and to show larger pupil dilation. Moreover, given that threatening stimuli subliminally presented tend to be accompanied by neural and physiological responses [17], [81], the use of subliminal exposure might be also relevant to help individuals overcome their phobias, as well as to understand its impact during exposure therapy. As shown by our studies, eye measurements when combined with subliminal exposure techniques can be a nonintrusive assessment aid tool with several applications in therapeutic and medical contexts. Based on these results, we also suggest that the use of ET 2.0, combined with subliminal exposure, could be cost effective methodology for a better screening of anxiety disorders. Since screening and treatment outcome measures for anxiety disorders have been based almost entirely on the cognitive– language dimensions, intraocular and extraocular measurements might complement the information [82]. The use of the presented combined methodology by therapists and clinicians

7

ACKNOWLEDGMENT

The authors would like to thank to A. F. Barata, C. Sottomayor, and F. Soares for their data collection. The participants were treated in accordance with the Ethical Principles of Psychologists and Code of Conduct. R EFERENCES

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Pedro J. Rosa was born in Lisbon, Portugal. He received the B.Sc. (Hons.) degree in psychology and the M.Sc. degree in psychology, psychotherapy, and counseling from the Universidade Lusófona de Humanidades e Tecnologias, Lisbon, in 2006 and 2008, respectively, and the Ph.D. degree in health psychology from the Instituto Universitário de Lisboa, Lisbon, in 2014. He is currently an Assistant Professor with the Universidade Lusófona de Humanidades e Tecnologias, Lisbon, and the Instituto Superior Manuel Teixeira Gomes, Portimão, Portugal. He is also an Invited Professor with the Universidad de San Buenaventura, Medellin, Colombia, and the Universidad de la Costa, Barranquilla, Colombia. He is part of the Grupo Internacional de Investigación Neuro-Conductual and is a Researcher with the Association for Research and Development in Cognitive and People-Centric Computing. His current research interests include the study of attentional and emotional processes to visual and auditory stimuli through eye tracking and psychophysiological recording. He is the mentor of the International Conference on Eye Tracking, Visual Cognition, and Emotion, in Portugal, and the founder of the First Meeting of Cognitive Oculometry, in Portugal, in 2015.

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Francisco Esteves received the Ph.D. degree in psychology and the Ph.D. degree in clinical psychology from the University of Uppsala, Uppsala, Sweden, in 1984 and 1994, respectively. His Ph.D. dissertation was entitled Emotional Facial Expressions and the Unconscious Activation of Physiological Responses. He was with the University Institute of Lisbon (ISCTE-IUL), Lisbon, Portugal, from 2005 to 2012. He is currently a Professor with Mid Sweden University, Sundsvall, Sweden, and a Visiting Professor with ISCTE/IUL.

Patrícia Arriaga received the Ph.D. degree in psychology and the M.Sc. degree in clinical psychology and psychopathology from the ISPA-University Institute, in 1996 and 2000, respectively, and the Ph.D. degree in social and organizational psychology from the Instituto Universitário de Lisboa (ISCTE-IUL), Lisbon, Portugal, in 2006. She received a post-doctoral fellowship from the Portuguese Foundation for Science and Technology to work with Granada University, Granada, Spain, and ISCTE-IUL from 2008 to 2009. She was hired as a Researcher by the Research Centre CIS-IUL (under Science 2008, an initiative by the FCT). She has held faculty positions with Lusófona University from 1996 to 2008, and with ISCTE-IUL. She is an Assistant Professor with ISCTE-IUL, and the Director of the master’s program in Science on Emotion. Her current research interests include basic (laboratory) and applied (healthcare settings) research on emotions, cognitive and interpersonal behavioral, combining subjective, and behavioral and psychophysiological measures.


1

Beyond Traditional Clinical Measurements for Screening Fears and Phobias Pedro J. Rosa, Francisco Esteves, and Patrícia Arriaga

Index Terms— Attentional orienting, eye movements, eye tracking (ET), fear, pupil response, snakes, subliminal exposure.

I. I NTRODUCTION

A

Specific phobias can be comparable with other mental disorders since they tend to interfere on social activities and to reduce productivity at work [5]. According to prominent models of anxiety (e.g., attentional control model, model of attentional bias, and information-processing model), the development and maintenance of specific phobia is highly dependent on cognitive processes, especially on attentional mechanisms [6]–[8]. Attentional processes are vital because one function of anxiety is the quick detection of threat, enabling an organism’s rapid reaction to the feared stimulus [9]. According to these models, attention tends to be biased toward feared stimuli. In fact, research with nonclinical samples has suggested that attentional orienting is facilitated by concern-related as opposed to unconcern-related stimuli [10]–[12]. However, this attentional bias seems to be more pronounced in phobic individuals [13], [14]. This distinctive priority by the attention system for potential threat can lead people to an irrational and noncontrolled fear response [15] which may become dysfunctional when it is particularly intense and frequent, and lead to the development of an anxiety disorder [9]. The higher the level of anxiety is (currently or permanently), the more likely the fear defense system become activated and trigger physiological components of fear response, such as skin conductance, cardiac changes, and electrical activity produced by skeletal muscles [16]. This may explain the sensitiveness of threat detection mechanism in phobics. Öhman and Soares [17] advocate that preattentive automatic analysis of potentially threatening cues may be sufficient to activate the fear defense system and trigger the physiological component of fear response. This may explain why individuals with specific phobias, such as snake phobia, tend to show an exaggerated perception of danger and increased physiological arousal responses even when they know that the object of the phobia is harmless (e.g., tiny or plastic snakes). The main goals of the clinical assessment of specific phobias are to establish an accurate diagnosis, frame a treatment plan, and evaluate psychotherapeutic progress and outcome. To reach a comprehensive assessment for specific phobias, three components are used: 1) a clinical interview; 2) self-report measures (questionnaires, monitoring diaries); and 3) behavioral assessment [18]. However, psychophysiological and behavioral measures, which are often used in academic research and reliable correlates of biased threat processing, are seldom used in clinical practice [19]. The main reasons for this unattractiveness are related to considerable costs and training investments required for this kind of

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Abstract— The use of eye movements is a usual method of measuring attentional and emotional response in laboratory. However, when it comes to clinical practice, it is seldom applied. Two studies were conducted to examine whether extraocular and intraocular movements can be used as indices of attentional bias and autonomic activation. In the first study, a free-viewing task, combined with subliminal exposure, showed that highfear individuals tend to orient more their attention toward the visual space where threat-stimuli (snakes) were presented. The findings suggest a reflexive overt attentional orienting bias for subliminal snakes in comparison with subliminal control stimuli. The differentiation between participants with high and low fear of snakes suggested that a disposition to fear snakes affects the initial ocular saccades. In the second study, participants were instructed to discriminate a sign that was randomly displayed at the center of the display while subliminal images were peripherally presented. The results revealed larger pupil dilation for threatening stimuli subliminally presented; again, high-fear individuals showed larger pupillary dilations, independently of the stimulus category. Our results are in line with the assumption that a predisposition to fear is relevant for extraocular and intraocular movements when exposed to threat stimuli. These findings suggest that eye measurements, combined with subliminal exposure techniques, could be a reliable and nonintrusive aid tool to be used for the assessment and treatment of fear and phobias.

NXIETY disorder impacts approximately 18% (i.e., approximately 40 million) adults in the United States [1], and phobias are the most common anxiety disorders [2]. However, specific phobias such as animal phobia (e.g., snake phobia) are not the primary motive for seeking treatment [3]. This might be related to the perception that this specific phobia is simple to overcome, rarely capturing the focus of clinical attention [4].

Manuscript received February 13, 2015; revised May 7, 2015; accepted May 16, 2015. This work was supported by the Fundação Para a Ciência e Tecnologia of Portugal through the FCT-MCTES Project under Grant SFRH/BD/46965/2008. The Associate Editor coordinating the review process was Dr. Zheng Liu. P. J. Rosa is with the School of Psychology and Life Sciences/COPELABS (ULHT), Lisbon 1749-024, Portugal, and also with the ISCTE–University Institute of Lisbon, Lisbon 1649-026, Portugal (e-mail: [email protected]). F. Esteves is with the Department of Social Sciences, Mittuniversitetet, Östersund 831 25, Sweden (e-mail: [email protected]). P. Arriaga is with the Department of Psychology, ISCTE–University Institute of Lisbon, Lisboa 1649-026, Portugal (e-mail: [email protected]). Color versions of one or more of the figures in this paper are available online at http://ieeexplore.ieee.org. Digital Object Identifier 10.1109/TIM.2015.2450292

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(extraocular and intraocular) vary as a function of the level of fear, validating the use of ET 2.0 for screening and assessing the treatment effectiveness in specific phobias. In our first study, we investigate attentional orienting processes in a freeviewing task while snakes were simultaneously presented with control images (neutral stimuli) at very short exposure times. The number of valid saccade endpoints (hits) in the areas, where the subliminal stimuli were exposed [areas of interest (AoI)], was used as an index of reflexive overt attentional orienting [44]. We expected that participants with high FS would show a pronounced attentional bias toward the snake area. In the second study, as the confrontation with the concerned/feared stimulus tends to elicit a series of changes in a specific neural circuit, resulting in physiological arousal, we expected larger pupil dilation in the participants with high FS when snakes are presented subliminally in comparison with control stimuli [45]. FS was measured because snakes are one of the most feared stimuli by humans and a common object of phobias [46]. II. S TUDY I A. Method

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equipment (e.g., stimuli presentation software, psychophysiological recording unit, and EEG cap) [19]. Also important, in the laboratory context, that the patient needs to be fully attached with sensors and cables, which creates an artificial context and may increase the individual’s anxiety. Besides, behavioral measures such as reaction times, often measured by the use of key-press responses, may reflect more than simply biased attentional processes [20], [21]. Furthermore, self-report data, when used in isolation, are highly susceptible to exogenous influences, sustaining the use of complementary measurements [22]. To overcome the above limitations, eye movement recording or eye tracking (ET) can be a nonintrusive approach [23]. ET has been successfully applied in clinical [11], [13] and medical domains [24]–[26] as it allows researchers to obtain measures closely related to attention and emotion [12], [20], [27]. The most recent generations of ET systems, which use relatively low-cost cameras [28], [29], allowing a quick calibration process [30] with motion correction algorithms for large head movement [31], [32] and an accurate estimation of the point of regard [33], [34], are called in this paper as ET 2.0 (in analogous with Web 2.0). Several ET.2.0 systems with different pattern recognition algorithms, accuracy levels, performance, and cost have been applied to study a wide variety of phenomena related to attention and vision [35], [36]. Recent studies using ET 2.0 have shown that initial ocular saccades are influenced by supraliminal and subliminal emotional content [37]–[40]. However, little is yet known about this in free-viewing tasks. As far as we know, no studies using ET 2.0 have applied subliminal stimuli competition during a video presentation in a spontaneous viewing activity. Despite the use of a wide spectrum of technological particularities in ET 2.0 systems [35], [36], as well as a large set of techniques [31], [32] and paradigms [11]–[14], it is still unclear whether the human attentional system is sensitive to threatening stimuli (snakes) when control stimuli are competing subliminally. Furthermore, and given that pupil dilates with sympathetic activity [41], it can be seen as a reliable and nonintrusive measure of emotional arousal [42]. Despite being a physiological component of arousal, it is not a common index used in subliminal exposure. If emotions and pupil size variation are reliably associated with each other, then ET 2.0 would offer a possibility for nonintrusive monitoring of emotion-related reactions during subliminal exposure to emotional stimuli. To the best of our knowledge, the only study that specifically recorded the pupil response during subliminal exposure is the work by Bijleveld et al. [43]. Their data indicate that valuable subliminal rewards led to larger pupil dilation in comparison with nonvaluable rewards. In this paper, we attempted to extend prior visual attention paradigms and techniques by combining subliminal visual competition with ET. With our approach, we intend to provide reliable eye measurements that can be used as a proxy for emotional/affective disorders. Taking these prior studies into consideration, the aim of this paper is the assessment of fear of snakes (FS) by recording the eye movements toward different stimuli. In two studies, we aim to support the hypothesis that eye movements

1) Participants: Fifty female students (Mage = 25.32 and SDage = 6.70) from two Portuguese universities volunteered to take part in this paper. Participants provided their written informed consent prior to entering the study. They were told that they were free to withdraw at any time and that confidentiality and anonymity of their individual data would be ensured. Female participants were chosen because they tend to report high and more frequently FS than men [46], [47]. 2) Materials and Procedure: A free viewing of a 4-min video segment, taken from the movie Koyaanisqatsi [48], was used as the experimental task. The particular features of this movie, with only landscapes, but no actors nor dialogs made it an adequate choice for a neutral stimulus and a mean to expose participants to a natural context in which subliminal stimuli were presented. Twenty pictures (10 snakes and 10 neutral, e.g., daily life objects) selected from the International Affective Picture System (IAPS) were used as subliminal stimuli [49]. Nonaffective features of the pictures, such as apparent contrast and luminance, were previously analyzed using ImageJ v1.47 software [50]. Twenty pairs of images were used, consisting of counterbalanced combinations of 10 snakes and 10 neutral pictures. Both snakes and control pictures had similar levels of luminance, t (18) = 0.56 and p = 0.58, and apparent contrast, t (18) = 0.78 and p = 0.44. All images were resized to a 320 × 256 resolution, using Photoshop TM CS3 software. These images were inserted randomly in the video (over layered) using MAGIX Movie Edition Pro-10 software. Altogether, 20 trials (2 randomized blocks × 10 pairs), with a duration of 1/60 s,1 were presented in the upper corners of the screen (one image per corner) while 1 Subliminality was pretested with two different presentation times (17 and 30 ms) with participants who did not take part in this paper. Half of the participants (5 in 10) noticed the stimuli’s content with a 30-ms presentation. However, with 17-ms presentation, none reported having seen any stimuli nor their content.


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Fig. 1. Video time sequence with two blocks of 10 trials each. Note that these example images were not among the experimental stimuli. Fig. 2. Proportion of hits in the AoI as a function of image type and FS. The error bars represent the standard errors of the mean.

B. Data Preparation Eye blinks, drifts, and outliers (±2 SD) were removed from raw gaze data and coded as missing values. To examine the number of hits immediately after the presentation of subliminal images, two rectangular AoI were drawn around each location where the stimuli were introduced on the screen. The following criteria were used to consider that a valid trial occurred: the endpoint of the initial saccade must have been within one of the AoI with saccade latency between 80 ms (5 frames) and 600 ms (35 frames) [54]. Considering the total number of valid trials for each participant, the percentage of hits in the two AoI was computed. The SNAQ median-split (Mdn = 13.5) was used to set apart participants with low FS (n = 29) from participants with high FS (n = 21). Data were analyzed with a mixed factorial analysis of variance (ANOVA). Greenhouse–Geisser corrected degrees of freedom were used to report significant levels. A Bonferroni correction was applied for pairwise comparisons.

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a movie sequence with 1280 × 1024 resolution was shown at 60 frames/s (see Fig. 1). The interstimulus interval (ISI) varied from 11 to 14 s to avoid expectation effects. The picture size was 7.69° × 6.26° of visual angle at a viewing distance of 60 cm. All participants were recruited from classrooms and invited to participate in the experiment. The experiment occurred in a single session, in an isolated laboratory room with constant illumination (42 lx). The true purpose of this paper was not fully disclosed beforehand. Instead, participants were informed that this paper was about how people watch a movie. This free-viewing instruction was given to avoid any top-down processes [51] and to control for anticipatory anxiety. Participants were told that the instructions would be provided on the computer screen at the beginning of the experiment. The instructions were as follows: A video will be presented. Please pay attention and try to remain still while the video is presented. At the end, some questions will be asked. The participants were instructed to always look at the screen to avoid ocular drifts. The stimuli were presented and the responses recorded on a Tobii-T60 ET System (Tobii Technology AB, Sweden), integrated into a thin-film transistor (TFT) 17-in monitor and connected to an Intel core2duo 6550 desktop computer. Gaze data were recorded binocularly at 60 Hz with an average accuracy of a 0.5 visual angle. After task completion, the stimuli unawareness was tested. Participants were also asked about the purpose of this paper, whether they thought any of the tasks performed had been related and whether anything about this paper seemed strange or suspicious to them. If participants mentioned that they saw pictures of snakes or any other content, they would be excluded from the experiment. Of the 50 participants, 28% (n = 14) mentioned having seen flashes, and of those, only 12% (n = 6) referred to having seen pictures. Therefore, no participants were excluded from analysis. Next, participants were instructed to fill out the Snake Anxiety Questionnaire (SNAQ) [52]. The SNAQ is a 30-item selfreport scale, with a dichotomy response format (true/false), which enables the assessment of the cognitive-verbal component of the FS. SNAQ has showed good reliability in [52] and [53], ranging Kuder-Richardson (KR)-20 values from 0.78 to 0.90. In this paper, the SNAQ had a KR-20 of 0.79. At the end, the participants were thanked, debriefed and dismissed.

C. Results

The proportion of hits was calculated based on the sum of hits in the AoI, divided by the number of valid trials. A 2 (image type: control versus snakes) × 2 (FS: low versus high) ANOVA showed a main effect of image on proportions of hits, F (1, 48) = 5.74, p = 0.021, and η2p = 0.11. Consistent with our hypothesis, a higher percentage of hits were found in the AoI where snakes were presented (M = 0.27) than in the AoI for control stimuli (M = 0.23), t (49) = 2.36, p < 0.001, and d = 0.35. A significant interaction between image and FS was also found, F (1, 48) = 9.37, and p = 0.004 and η2p = 0.16 (see Fig. 2). Simple main effects revealed that the proportion of hits for snakes was higher in participants with high FS (M = 0.32) than in participants with low FS (M = 0.23), t (48) = 2.36, p = 0.003, and d = 0.93. Furthermore, for participants with high FS, the proportion of hits for snakes (M = 0.32) was significantly higher than in the control AoI (M = 0.22), t (20) = 3.56, p = 0.001, and d = 0.98. There were no other significant effects (ps > 0.05). D. Discussion The results revealed that participants with high FS tend to orient their attention more toward the visual space where

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greater fear. To form two opposite balanced groups, those who responded with 1 or 2 on the FSS-II snake item and those who scored 6 or 7 were invited to participate in a further study. From the initial participants, only 51 (26 snake-fearful and 25 nonfearful) were chosen based on the mentioned criteria. Of these, 84.3% were females (n = 43) and 15.7% were males, ranging from 18 to 55 years old (M = 25.55 SD = 8.25). All the participants had normal or corrected vision and most were Portuguese (n = 38, 76%). 2) Materials and Procedure: In this experiment, in addition to the measurement of cognitive FS through SNAQ, the trait and state anxiety as well the level of fatigue were assessed. Trait and state anxiety were assessed through the State Trait Anxiety Inventory (STAI) [59]. The STAI has both state and trait scales with each scale consisting of 20 items (e.g., I feel nervous), evaluated on a four-point Likert response format scale (1 = almost never; 4 = almost always). Scores in both trait and state scales can range from 20 to 80, with higher scores reflecting higher levels of anxiety. This measure has shown good reliability in [60] and in this paper had a Cronbach’s alpha of 0.77 for the State and 0.85 for the Trait subscale. The KR-20 was of 0.66 for SNAQ. The level of fatigue was measured through the Pichot fatigue scale (le questionnaire de la fatigue) [61]. This is a short eight-item, easy to administer tool that measures the individual’s level of fatigue at the moment, consisting in a four-point Likert scale from 0 (not at all) to 4 (extremely). This fatigue scale presented a good internal consistency (α = 0.81). Due to its interference with attentional processes [62], [63], the level of fatigue was similar for both groups (low fear versus high fear) before the experiment, t (49) = −1.11 and p = 0.274. Sixty images were selected from IAPS [49] consisting of 20 negative (10 snakes + 10 other feared animals), 20 positive and 20 neutral. All images were converted to grayscale 8-bit portable network graphic (.png) image file format, controlled for luminance and apparent contrast and resized to 320 × 256 resolution, using ImageJ 1.47 software [50]. The image size was 7.69 × 6.26 of visual angle at a viewing distance of 60 cm. Stimuli were presented through Superlab 4.0 presentation software [64] for Windows in an Intel core2duo 6550 desktop computer, which was connected to a Tobii-T60 ET System (Tobii Technology AB, Sweden) and integrated into a 17-in TFT. Blanks and background were presented on a gray color (Red-Green-Blue: 150, 150, 150) to minimize differences in luminance during stimulus presentation. The eye tracker received the video signal through the Video Graphics Array capture card from the PC running Superlab program. The pupil diameter was binocularly measured with a temporal resolution of 60 Hz. Gaze data were used to control the locus of the participant’s overt visual attention while the pupil diameter was being recorded. Upon arrival at the laboratory of experimental psychology, each participant signed a consent form and was seated in a chair in a sound-proof room with a constant illumination (42 lx). The true purpose of this paper was masked to control for anticipatory anxiety. Each participant was instructed to count only the number of signs + and to ignore the o signs. One of the two following signs (0 or +) was randomly

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snakes are presented when exposed to two concurrent subliminal stimuli. Thus, the present findings suggest a reflexive attentional orienting bias for snakes presented subliminally as opposed to control stimuli. Because participants were not aware of stimuli, attentional orienting seemed to be activated by the subliminal threat-related stimuli. The selective sensitiveness of the fear defense system to concern-related stimuli is indicative of a quick detection of snakes, supporting the assumption that a subliminal attentional orienting bias, as prioritized processing, is facilitated to snakes, while other fear-irrelevant stimuli are inhibited [15], [55]. These results are in line with studies showing that individuals with high level of anxiety/fear have lower perceptive thresholds to their concern-related stimuli, thereby orienting their attention toward threat [11], [13], [20]. These results corroborate previous experimental studies, indicating that individuals with a specific fear tend to have exacerbated preattentive bias to the feared stimuli in complex visual contexts [56], [57]. However, it is important to address some potential limitations of this first study. First, the present findings cannot be generalized to males. A mixed male and female sample would give more robustness to our findings. Second, since snakes were only compared with control stimuli (pictures with neutral content), it is quite difficult to know whether this ocular behavior is specific to their concern-related stimuli or also occurs during other threatening stimuli (e.g., sharks or lions).

III. S TUDY II The second study addressed the limitations of the previous study using a mixed gender sample and four image categories instead of two. In the first study, we found that participants with high FS showed a higher percentage of ocular movements (initial saccades) toward areas where snakes were subliminally presented than control stimuli. However, the specificity of the ocular response to concern-related stimuli was impossible to examine. Therefore, a presentation of four categories of stimuli in this paper was focused on the specificity of the fear module using not only neutral pictures as controls but also positive and other threatening-related pictures. It was also of interest to test whether pupil reactivity could be taken as an index of emotional arousal when concern-related stimuli are subliminally presented. To our knowledge, there is no previous evidence whether snakes when presented subliminally are capable of affecting pupil size. We hypothesized that participants with a high level of FS would show larger pupil dilation those with low level of fear. Furthermore, it is expected that fear module operates as a specific fear detector, that is, snake stimuli lead to larger reactivity in comparison with other control stimuli in participants with high level of FS. A. Method

1) Participants: Initially, a sample of 147 undergraduate psychology students of a Portuguese University was screened through classroom announcements to first respond to the Fear Survey Schedule-II (FSS-II) [58]. The FSS-II lists 51 commonly feared objects and real life events. Participants rated their fear of each object and event on a 1 (none)–7 (terror) scale. One object listed is snake. Higher scores indicate


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Fig. 4. Mean pupil dilation as a function of fear group after controlling for the effect of trait anxiety level. The error bars represent the standard errors of the adjusted mean. Fig. 3. These same pictures were not among the experimental stimuli. This picture was not among the stimuli.

B. Data Preparation

C. Results

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presented at the center of the screen for 500 ms before image onset. Due to the fact that pupillary response is also sensitive to high cognitive demands, it was essential to conduct a simple discrimination task. Following two practice trials, 60 pictures were randomly displayed at one of the four screen corners of the screen for 17 ms through a Latin-square presentation. The ISI was randomized (8, 10, or 12 s) to avoid any expectation effects (see Fig. 3). Next, participants were instructed to fill out the SNAQ at home and to return them within a week at the Laboratory of Computing Psychology. Then, the participants were thanked and dismissed.

F (3, 36) = 108.59 and p < 0.001, presenting snakes (M = 6.11 and SD = 0.39) and other animals (M = 6.30 and SD = 0.44) higher mean arousal ratings compared with positive (M = 4.09 and SD = 0.50) and neutral images (M = 2.74 and SD = 0.65).

Eye blinks, drifts, and outliers (±2 SD) were identified from raw pupil data and linear interpolation was made on a trial by trial basis to estimate pupil size. Pupil artifacts were randomly distributed across experimental conditions. Pupil data were smoothed using a 10-Hz low-pass filter. The pupil size data were analyzed using a 1-s prestimulus baseline correction. The baseline pupil diameter was defined as the average of pupil diameter recorded during the 1 s (60 samples) that preceded the picture onset. Peak dilations were computed as the maximum baseline corrected pupil diameter in a 6-s window after image onset. Pupillary reactivity was calculated as the difference between pupil peak and pupil baseline. No difference in terms of age was found for both groups t (49) = −0.40 and p = 0.688. The low- and highfearful ones were also similar regarding gender composition, 2 (1) = 1.19 and p = 0.248. The SNAQ mean score χYates was significantly different between the low-fearful (M = 7.0 and SD = 4.15) and high-fearful (M = 22.20 and SD = 3.36) groups. For anxiety, the high-fearful group showed significantly a higher state anxiety level (M = 41.80 and SD = 12.25) than the low-fearful group (M = 32.65, and SD = 8.40, t (49) = −3, and 12 p = 0.003). A similar pattern was found for trait anxiety level, showing the high-fearful group a significantly higher trait anxiety level (M = 36.11; SD = 8.42) than the low-fearful group (M = 44.12; SD = 11.78, t (49) = −2, 80 p = 0.007). Rated arousal differed significantly between picture categories

Ten positive and 10 neutral images were randomly selected from the presented images (20 for each category) allowing a balanced mean comparison across the four picture categories. To control the effect of anxiety trait level on pupillary amplitude, a repeated-measure full factorial analysis of covariance (ANCOVA) with one within-subject factor (image type: snakes versus other feared animals versus pleasant versus neutral) × one between-subject factor (fear of snakes: low versus high) was performed. The linear mixedeffects models procedure in the Statistical Package for Social Sciences software version 22 was chosen due to the advantage of dealing with missing values and correlated within-subject errors [65]. Anxiety state level and arousal rating of images were not included as covariates in the model since they were not correlated with pupillary reactivity [66]. The covariate (anxiety trait level) was centered before the analysis as recommended in [67]. Missing data were completely at random (Little’s Missing Completely at Random test: χ2(578) = 248.82 and p > 0.05). Both factors were treated as fixed effects and the maximum likelihood method was used to estimate the covariance matrix (compound symmetry) [68]. Cohen’s f 2 effect size measure was manually computed based on the recommendations of Selya et al. [69]. Bonferroni correction was applied for pairwise comparison of adjusted means. The repeated-measures ANCOVA revealed a main effect of FS on pupillary reactivity after controlling for trait anxiety level, F (1, 50) = 4.509, p = 0.039, and f 2 = 0.02. As shown in Fig. 4 and consistent with our hypothesis, pupillary reactivity was higher in participants with high FS (M = 0.43) than in participants with low FS (M = 0.33). The results concerning the main effect of type of image on pupillary reactivity, after controlling for trait anxiety level, partially support our snake-specific response hypothesis. F(3, 150) = 3.15, p = 0.027, and f 2 = 0.07. A multiple mean comparison showed that pupillary reactivity was sig-

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IV. G ENERAL D ISCUSSION

Fig. 5. Mean pupil dilation as a function of the type of image after controlling for the effect of trait anxiety level. The error bars represent the standard errors of the adjusted mean.

D. Discussion

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nificantly higher to snakes (M = 0.41) than to neutral (M = 0.35), t (150) = 2.90, p = 0.025, and d = 0.24. However, no significant differences between snakes, feared animals, and positive images were found on pupillary reactivity (see Fig. 5). There was no significant interaction between FS and image type ( p > 0.10).

The findings of these two studies offer valuable insights into the relationship between fear and eye movements. In the first study, a free-viewing task showed that participants with high FS tend to orient more their attention toward snakes than control stimuli. These results validate the use of extraocular eye measurements for differentiation between participants with high and low FS. Furthermore, our results extend previous findings of enhanced spatial attention to threatening stimuli in phobic participants [21], [57], suggesting that when competing simultaneously with neutral stimuli in visual space, snakes take it all in terms of attentional orienting, probably due to being a fear-relevant stimuli. Both of our studies extend previous research by showing that subliminal exposure paradigms, when combined with ET 2.0 can offer valuable intraocular and extraocular indexes to differentiate low-feared from high-feared individuals. Data from the first study are in accordance with [7], which argue that fearful individuals typically show a wide attentional focus, enabling faster threat detection. In a similar vein, the higher sensitivity to snake stimuli by snake fearful individuals may also lead to scanning the environment for potential threat more than individuals with low FS [75]. These findings are also consistent with those of Calvo and Lang [10], who found a higher probability of an initial fixation on supraliminal emotional images when paired with neutral pictures. The differentiation between participants with high and low FS suggests that FS disposition moderates the programming and execution of the initial ocular saccades, indicating that eye movements, especially initial saccades are associated with the level of fear. In the second study, we used a simple discrimination task with a peripheral subliminal presentation. Contrary to what we expected, no specific fear response in participants with high FS was found in snake images. These results are dissonant with those of [17] where participants with high FS showed a sympathetic exacerbation to snakes images. It is possible that as the arousal of a stimulus increases, the stimulus becomes increasingly likely to trigger a sympathetic response regardless of the individual’s level of trait anxiety [76], [77]. This may reflect a stimulus response generalization, that is, a processing mechanism based on image features similarity between the emotionally laden stimuli [78]. Our findings also indicated that participants with high FS showed larger dilations while controlling for the trait-anxiety level. These results reinforce the link between the fear module and unspecific hypervigilance or heightened alertness even prior to detecting a threat stimulus [16], [17]. In this perspective, individuals with high FS are constantly scanning the visual field, enabling a quicker processing and detection for signs of potential threats in the visual periphery [75]. Paralleling a large body of [79], our results suggest that sympathetic responses are thought to be operated in a relatively rudimentary fashion, which might minimize false negatives and increase the number of false positives. Furthermore, trait anxiety explained some variation in pupillary reactivity, supporting the idea that may act as an additive factor for the prioritization of emotional information [7]. In addition, it can also be argued that the

This second study sought to determine whether pupil size, as an index of physiological arousal, could be affected when threatening images were subliminally presented. The findings suggest that pupil dilation was larger in the participants with high FS than in the participants with low FS. Thus, these results support the initial hypothesis that individual’s level of fear is involved in sympathetic response [16]. Higher pupillary reactivity to images subliminally presented shows concordance between self-reported FS (SNAQ) and physiological response, even after controlling for the trait anxiety level [70]. Moreover, when trait anxiety level was included as covariate in the statistical model, Cohen’s f 2 for FS decreases from 0.03 to 0.02. This suggests that trait anxiety level also appeared to explain some variation in pupillary reactivity [7]. Interestingly, snakes were expected to evoke larger amplitudes not only than neutral images but also than other emotionally valenced images. In the present experiment, the absence of any differential pupil response between negative and positive emotional content suggests a low sensitivity of the fear module to the hedonic valence of stimuli, but the pupil response shows an almost similar pattern to arousal ratings [71], [72]. This suggests that perhaps the fear module tends to respond primarily to more arousing stimuli. Thus, there was no statistical evidence that snakes led to higher pupillary reactivity in high-feared participants. Perhaps these less expressive results can be explained due a carry-over effect produced by the cognitive load in the discrimination task that preceded the subliminal exposure, obscuring larger pupil responses [73]. Thus, it is important to note that our results support the evidence for a differential preattentive processing for fearrelevant stimuli when compared to neutral [12], [16], [17] and that pupillary reactivity can be an important noninvasive index of fear level without conscious effort [74].


should rely on three aspects. First, phobic patients usually tend to avoid specific-concerning objects and situations in which they experience relatively high levels of anxiety. Our combined methodology could possibly reduce the unpleasantness in patients at early stages of the therapeutic program. Second, in exposure therapy interventions, ocular metrics, similar to other psychophysiological indexes, can serve as a therapeutic success index, complementing other measures such as self-report instruments. Third, since emotionally laden stimuli, even when presented subliminally, can still lead to emotional reactions, subliminal exposure feared stimuli may already reduce the phobia, while at the same time might prevent extreme and unpleasant emotional responses [83]. Despite the seldom use of ET 2.0 in clinical and medical practice, its use is promising for future years [26]. ET 2.0, due to its mobility and flexibility, allows clinicians to record eye movements in nonlaboratory clinical contexts. In fact, clinicians are able to set up a quick and portable eye analysis laboratory wherever patients are [35]. Moreover, other ocular indices such as blinks, vergence, and accommodation can be explored and they may be a rich source of data [84]. For instance, blink rate is quite sensitive to cognitive load and could be a good index of emotional suppression [85]. Empirical studies using emotional paradigms have shown that attentional biases in anxiety individuals commonly disappear following treatment [86], [87]. Similarly, future therapeutic applications using the paradigms and the methodology we have presented, combined with different types of ocular analysis [88], might also be important, especially when dealing with resistant children who are undergoing therapy for overcoming fears.

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high- and the low-fear groups did not differ sufficiently in terms of fear as they were defined by means of a median-split procedure. In other words, there is a possibility that a larger clinically meaningful difference in fear levels between both groups would lead to a specific response to snakes. The findings of the second study also underline the use of ET 2.0 combined with subliminal exposure for differentiation between participants with high and low levels of fear. Both studies offer new contributions to our understanding of the relation between eye movements and emotional fear response. The results have shown that subliminal exposure can be combined with ET 2.0 as an assessment aid tool for future studies on attention and emotion, especially in the clinical context. The simple tasks that we developed and grounded on previous empirical research findings and theory were sufficient to obtain reliable ocular measurements and to assess how the individual’s evaluative system reacts to fear and to control stimuli. The results showed that extraocular movements (initial saccades) and intraocular movements (pupil dilations) can be affected by emotional content and level of fear. Nevertheless, we must also be cautious in making firm conclusions about the attentional and emotional responses observed in these participants. Since humans use trichromatic color vision, it was our intention to present stimuli with high ecological validity, but the repeatability of studies using the same tasks is crucial. A higher methodological control of stimuli’s physical features, such as spatial frequency analysis through the fast Fourier transform, could be relevant to use in future studies [80]. One of the limitations of both experiments is that we did not assess the predisposition of participants to fear other animals beside snakes. This information might have helped to understand how large is the spectrum of fear and how this could be related to fear responses. Another limitation is related to the levels of anxiety participants might have experienced during the experiment. The reapplication of the Trait Anxiety Inventory [59] at the end of the experiment could be relevant to examine whether the subliminal presentation of fear stimuli might also increase the levels of state anxiety. On the whole, the results from our studies suggest that participants with a high level of fear tend to overtly orient attention toward threatening-stimuli and to show larger pupil dilation. Moreover, given that threatening stimuli subliminally presented tend to be accompanied by neural and physiological responses [17], [81], the use of subliminal exposure might be also relevant to help individuals overcome their phobias, as well as to understand its impact during exposure therapy. As shown by our studies, eye measurements when combined with subliminal exposure techniques can be a nonintrusive assessment aid tool with several applications in therapeutic and medical contexts. Based on these results, we also suggest that the use of ET 2.0, combined with subliminal exposure, could be cost effective methodology for a better screening of anxiety disorders. Since screening and treatment outcome measures for anxiety disorders have been based almost entirely on the cognitive– language dimensions, intraocular and extraocular measurements might complement the information [82]. The use of the presented combined methodology by therapists and clinicians

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ACKNOWLEDGMENT

The authors would like to thank to A. F. Barata, C. Sottomayor, and F. Soares for their data collection. The participants were treated in accordance with the Ethical Principles of Psychologists and Code of Conduct. R EFERENCES

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Pedro J. Rosa was born in Lisbon, Portugal. He received the B.Sc. (Hons.) degree in psychology and the M.Sc. degree in psychology, psychotherapy, and counseling from the Universidade Lusófona de Humanidades e Tecnologias, Lisbon, in 2006 and 2008, respectively, and the Ph.D. degree in health psychology from the Instituto Universitário de Lisboa, Lisbon, in 2014. He is currently an Assistant Professor with the Universidade Lusófona de Humanidades e Tecnologias, Lisbon, and the Instituto Superior Manuel Teixeira Gomes, Portimão, Portugal. He is also an Invited Professor with the Universidad de San Buenaventura, Medellin, Colombia, and the Universidad de la Costa, Barranquilla, Colombia. He is part of the Grupo Internacional de Investigación Neuro-Conductual and is a Researcher with the Association for Research and Development in Cognitive and People-Centric Computing. His current research interests include the study of attentional and emotional processes to visual and auditory stimuli through eye tracking and psychophysiological recording. He is the mentor of the International Conference on Eye Tracking, Visual Cognition, and Emotion, in Portugal, and the founder of the First Meeting of Cognitive Oculometry, in Portugal, in 2015.

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Francisco Esteves received the Ph.D. degree in psychology and the Ph.D. degree in clinical psychology from the University of Uppsala, Uppsala, Sweden, in 1984 and 1994, respectively. His Ph.D. dissertation was entitled Emotional Facial Expressions and the Unconscious Activation of Physiological Responses. He was with the University Institute of Lisbon (ISCTE-IUL), Lisbon, Portugal, from 2005 to 2012. He is currently a Professor with Mid Sweden University, Sundsvall, Sweden, and a Visiting Professor with ISCTE/IUL.

Patrícia Arriaga received the Ph.D. degree in psychology and the M.Sc. degree in clinical psychology and psychopathology from the ISPA-University Institute, in 1996 and 2000, respectively, and the Ph.D. degree in social and organizational psychology from the Instituto Universitário de Lisboa (ISCTE-IUL), Lisbon, Portugal, in 2006. She received a post-doctoral fellowship from the Portuguese Foundation for Science and Technology to work with Granada University, Granada, Spain, and ISCTE-IUL from 2008 to 2009. She was hired as a Researcher by the Research Centre CIS-IUL (under Science 2008, an initiative by the FCT). She has held faculty positions with Lusófona University from 1996 to 2008, and with ISCTE-IUL. She is an Assistant Professor with ISCTE-IUL, and the Director of the master’s program in Science on Emotion. Her current research interests include basic (laboratory) and applied (healthcare settings) research on emotions, cognitive and interpersonal behavioral, combining subjective, and behavioral and psychophysiological measures.