Edited by: Maurizio Codispoti, Università degli Studi di Bologna, Italy
Reviewed by: Andrea De Cesarei, Università degli Studi di Bologna, Italy; Laura Miccoli, Universidad de Granada, Spain
This article was submitted to Emotion Science, a section of the journal Frontiers in Psychology
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It is generally thought to be adaptive that fear relevant stimuli in the environment can capture and hold our attention; and in psychopathology attentional allocation is thought to be cue-specific. Such hypervigilance toward threatening cues or difficulty to disengage attention from threat has been demonstrated for a variety of stimuli, for example, toward evolutionary prepared animals or toward socially relevant facial expressions. Usually, specific stimuli have been examined in individuals with particular fears (e.g., animals in animal fearful and faces in socially fearful participants). However, different kinds of stimuli are rarely examined in one study. Thus, it is unknown how different categories of threatening stimuli compete for attention and how specific kinds of fears modulate these attentional processes. In this study, we used a free viewing paradigm: pairs of pictures with threat-related content (spiders or angry faces) or neutral content (butterflies or neutral faces) were presented side by side (i.e., spiders and angry faces, angry and neutral faces, spiders and butterflies, butterflies and neutral faces). Eye-movements were recorded while spider fearful, socially anxious, or non-anxious participants viewed the picture pairs. Results generally replicate the finding that unpleasant pictures more effectively capture attention in the beginning of a trial compared to neutral pictures. This effect was more pronounced in spider fearful participants: the higher the fear the quicker they were in looking at spiders. This was not the case for high socially anxious participants and pictures of angry faces. Interestingly, when presented next to each other, there was no preference in initial orientation for either spiders or angry faces. However, neutral faces were looked at more quickly than butterflies. Regarding sustained attention, we found no general preference for unpleasant pictures compared to neutral pictures.
Humans are exposed to a plethora of concurrent visual stimuli and attention is preferentially directed to the most menacing of them. This is thought to be adaptive because quick detection of danger promotes survival by initiating necessary behavioral responses (
Among all the visual stimuli that are encountered, faces are especially relevant social cues for us (
Although different kinds of threatening stimuli (fear-related animals and social stimuli) evoke comparable reactions compared to neutral stimuli, this does not mean that all threatening stimuli are the same. For example, in an earlier study we demonstrated that pictures of emotional scenes and pictures of faces can result in very different psychophysiological response patterns (
Similar response patterns to different evolutionary fear-relevant stimuli are noticeable in infants younger than 9 months (
Hence, there is considerable evidence that both, pictures of threatening animals and of emotional facial expressions trigger fear responses, avoidant behavior, they differ in fear learning and in fear conditioning.
Furthermore, no studies so far have addressed the specificity of attentional biases – is there a uniform bias to emotionally relevant pictures or is there a category specific bias? Are specific categories more dominant than others? Until now, the question how these types of stimuli compete for visual attention and whether specific fear (e.g., spider vs. face) can differentially modulate the underlying mechanisms of attentional biases remains still unanswered. In order to answer these questions, the main purpose of the present study was to examine whether angry faces and spiders elicit similar attentional biases (initial vigilance; difficulties to disengage).
Another important aspect we deal with in the present research is the time course of attention allocation to fear-related stimuli. This has also been tested in one
There is considerable evidence to support the notion that attentional biases are comprised of an initial hypervigilance for threat (
Face stimuli are frequently used to investigate the aforementioned attentional processes. For example, in an eye-tracking study,
Given the contradictory models for the sustained attention mentioned above, as well as the limited range of examined stimuli used in previous experiments, in the present study we directly compared faces and animals in a typical free viewing paradigm to identify attentional biases (in anxiety). Pairs of emotional (spiders, angry faces) and neutral (butterflies, neutral faces) visual stimuli were presented in one of several combinations: pictures of spiders and butterflies, angry and neutral faces, spiders and angry faces, butterflies, and neutral faces.
Taken together, the main purpose of our study was to examine whether spiders and angry faces elicit similar attentional biases (initial vigilance; difficulties to disengage) when directly compete for attentional resources. In order to achieve this, we use eye-tracking as an advantageous measure to investigate these attentional biases (
Seventy participants (11 men) were recruited via newspaper advertisements from the general population and from the student population of the University of Mannheim. Their age ranged from 18 to 51 years (
Thirty-two pictures of male angry and neutral faces from the Karolinska Directed Emotional Faces set (
Examples of experimental category combinations, trial sequences, and block order counterbalanced across participants. (Block A) Spiders and butterflies, (Block B) angry and neutral faces, (Block C) spiders and angry faces, and (Block D) butterflies and neutral faces. The codes for the KDEF faces used in the figure are: am10nes, am10ans, am21ans, am21nes, am23nes, am24ans, bm10nes, bm23nes, bm31ans, and bm31nes.
After arrival at the laboratory, participants completed a set of questionnaires. To check for fear of spiders we used the FAS (German version of the Fear of Spiders Questionnaire; FSQ:
Participants were instructed to simply look at the pictures that appear on the screen. The procedures of the experiment were approved by the ethics committee of the University of Mannheim.
Eye movements were recorded with an SMI RED250 eye-tracking device (SMI, Teltow, Germany), which has a sampling rate of 250 Hz and tracking resolution of 0.03°. A frame around each picture was the area of interest (AOI) for the analysis in BeGaze (SMI, Teltow, Germany).
Trials without saccades, or without proper fixation on the fixation cross, were deleted from further analyses. We then calculated the entry viewing time for each picture. Entry time was defined as the average duration after picture onset when the first fixation on the picture was recorded. Second, we calculated the number of fixations (fixation count) as an index of the total time that participants spent looking at a specific picture (number of all fixations for all subjects divided by number of subjects).
Self-report data were analyzed with separate 2 × 2 ANOVAs for the mean valence and arousal ratings with Emotion (fear-related vs. neutral) and Type of Stimuli (animals vs. faces) as within subject’s factor. In a second step questionnaire scores of fear of spiders and social anxiety were included separately as covariates in ANCOVA analyses. Afterward, we conducted
More specifically we analyzed entry time with a 2 × 2 analysis of variance (ANOVA) for the four different block types (spiders and butterflies, angry and neutral faces, spiders and angry faces, and butterflies and neutral faces), with the factors Position of each picture (left or right) and Emotion (fear-related or neutral) for the first two blocks, and Position of each picture (left or right) and Type of Stimuli (animal stimuli or face stimuli) for the last two blocks. Furthermore, separate analyses of covariance (ANCOVA) including the questionnaire scores of fear of spiders and social anxiety as covariate were conducted to investigate the influence of individual differences (spider fear and social anxiety). We used an ANCOVA so that we had no loss in power (
We then analyzed the number of fixations index based on a ratio analysis. As fear-related and neutral pictures appeared in pairs, raw data of fixation counts were not independent. Therefore, we computed preference ratios as suggested by
Regarding the self-report ratings, we conducted separate ANOVAs for the mean valence and arousal ratings with a 2 × 2 design with Emotion (fear-related vs. neutral) and Type of Stimuli (animals vs. faces) as within subject’s factor.
In order to test the effects of individual’s particular extend of a specific fear/anxiety we then included questionnaire scores of fear of spiders and social anxiety were also included as covariates in an ANCOVA analysis separately
The ANOVA for the mean valence rating showed a significant main effect of Emotion,
In the ANCOVA with fear of spiders as a covariate the main effect of Emotion covaried with fear of spiders,
The ANOVA for the mean arousal rating showed a significant main effect of Emotion,
Furthermore, in the ANCOVA with fear of spiders as a covariate, there was an interaction of Emotion with fear of spiders
When we compared spiders with angry faces, spiders were rated as more negative
Moreover, no interaction of Social Anxiety and Emotion was found
The mean entry time varied as a function of Emotion,
Mean entry time for the four blocks.
Furthermore, a main effect of Position emerged,
In the overall ANOVA with mean entry time and Emotion [again, for Block 2 the Type of Stimulus factor was kept constant (see the “Data Analyses” section)] there was a main effect of Emotion
Illustration of covariation between Emotion and fear level.
Furthermore, a main effect of Position emerged,
For the overall ANOVA with mean entry time and Type of Stimulus [in Blocks 3 and 4 the Emotion factor was held constant (see “Data Analysis” section)] was not found to have an effect on the entry time — we found no differences between spiders and angry faces,
Interaction of emotion with reported levels of fear for the third block (spiders vs. angry faces).
The mean entry time varied as a function of Type of Stimulus [(in Block 4, same like in Block 3, Emotion factor was held constant (see “Data Analysis” section)] suggesting that neutral faces are looked at faster than butterflies,
The overall ANOVA for the preference ratio of number of fixations with the within-subject factor Position did not reveal any main effects:
The overall ANOVA for the preference ratio of number of fixations with the within-subject factor Position did not reveal any main effects:
The preference ratio of the number of fixations did not vary as a function of Position:
The overall ANOVA for the preference ratio of number of fixations with the within-subject factor Position did not reveal any main effects:
Attentional biases have been documented for fear-related animals (such as spiders) and emotional facial expressions (such as angry faces) but they have rarely been pitted against each other in one experiment. This is the first eye-tracking study to directly compare how threatening animal stimuli and social stimuli compete for visual attention. We recorded eye-movements during a free viewing task with pictures from different categories (animals and human faces), displaying emotional (spiders, angry faces) or neutral (butterflies, non-emotional faces) information. Our findings support an attentional preference toward threat, thus, this replicates previous findings in a more complex context. Overall, fear-related stimuli captured initial attention more than neutral pictures. As for the comparison between categories (animal vs. faces), there were no obvious differences in the initial allocation of attention or in sustained attention.
Eye-tracking methodology provides a useful tool to investigate attentional biases (see
In addition, typical left bias was also observed in our study, which may represent the common reading direction. Pictures on the left were detected faster than the ones on the right, independent of stimulus type. A left bias for processing emotional information has been found before (
Regarding sustained attention, fixation count data do not differ for spiders or faces. More fixations were observed for face stimuli compared to spider pictures in Block 3 but this did not reach significance. Similar to other studies (
Regarding the neutral category, butterflies were rated as more positive than neutral faces which can also be seen in the normative ratings of the few pictures depicting butterflies in the IAPS collection (
One reason for the differences in eye movements in participants with fear of spiders and social anxiety could be that social anxiety is generally considered to be more complex than specific phobias. Attentional biases in general in fear of spiders can be explained in terms of preparedness while social anxiety can be seen as a result of perceived dominance (
Our results support the above-mentioned notion in that fear of spiders correlates with the observed initial hypervigilance but this is not the case for social anxiety. This suggests that distinct mechanisms may be underlying the two fears. It will be fruitful for the understanding of both fear domains to disentangle the specific mechanisms in future research. One plausible reason for the differences may in part be due to the intensity of reported fear in our sample. When each one of our groups is compared to normative controls, spider fearful participants report higher levels of spider fear compared to socially anxious participants who score lower on social anxiety (For spider fear:
Taken together, the present research is one of the few examples of a direct comparison of different kinds of emotional stimuli. Furthermore, it sheds light on how different categories of threat cues compete for visual attention and how attentional biases are manifested in the context of anxiety. The results suggest that both spiders and angry human faces preferentially guide attentional processes and they seem to be ingrained in our defense system as evolutionary fear-relevant stimuli.
EB contributed to the conceptualization and design of the work, data collection, data analysis, writing of the manuscript, and final approval. AG contributed to the conceptualization, programming, design, data analysis, revisions, and final approval. FB contributed to the conceptualization, data analysis, revisions, and final approval. AW contributed to the conceptualization, data analysis, and final approval. GA contributed to the conceptualization, funding, data analysis, continuous revisions, and final approval.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The reviewer ADC and handling Editor declared their shared affiliation.
We also included STAI State and Trait scores in the analysis. STAI State did not have any significant effect on the results. While STAI Trait correlates with emotion in the first block. To check whether the effect we find in the first block is due to spider fear or general negative affect we conducted a correlation and regression analysis with FAS scores and STAI Trait scores as potential predictors. The stepwise regression reveals that when the predictor FAS is held constant, the STAI-T is not significant (