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1 This article was downloaded by: [Michigan State University] On: 16 September 2009 Access details: Access Details: [subscription number ] Publisher Psychology Press Informa Ltd Registered in England and Wales Registered Number: Registered office: Mortimer House, Mortimer Street, London W1T 3JH, UK The Quarterly Journal of Experimental Psychology Publication details, including instructions for authors and subscription information: Early detection and avoidance of threatening faces during passive viewing Mark W. Becker a ; Brian Detweiler-Bedell b a Michigan State University, East Lansing, MI, USA b Lewis & Clark College, Portland, OR, USA First Published on: 09 March 2009 To cite this Article Becker, Mark W. and Detweiler-Bedell, Brian(2009)'Early detection and avoidance of threatening faces during passive viewing',the Quarterly Journal of Experimental Psychology,62:7, To link to this Article: DOI: / URL: PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: This article may be used for research, teaching and private study purposes. Any substantial or systematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material.

2 THE QUARTERLY JOURNAL OF EXPERIMENTAL PSYCHOLOGY 2009, 62 (7), Short article Early detection and avoidance of threatening faces during passive viewing Mark W. Becker Michigan State University, East Lansing, MI, USA Brian Detweiler-Bedell Lewis & Clark College, Portland, OR, USA To evaluate whether there is an early attentional bias towards negative stimuli, we tracked participants eyes while they passively viewed displays composed of four Ekman faces. In Experiment 1 each display consisted of three neutral faces and one face depicting fear or happiness. In half of the trials, all faces were inverted. Although the passive viewing task should have been very sensitive to attentional biases, we found no evidence that overt attention was biased towards fearful faces. Instead, people tended to actively avoid looking at the fearful face. This avoidance was evident very early in scene viewing, suggesting that the threat associated with the faces was evaluated rapidly. Experiment 2 replicated this effect and extended it to angry faces. In sum, our data suggest that negative facial expressions are rapidly analysed and influence visual scanning, but, rather than attract attention, such faces are actively avoided. Keywords: Emotion; Eye tracking; Threat; Attention; Fear. Sparse attentional capacity severely limits the number of objects that can be apprehended at any instant (Becker & Pashler, 2005). Thus it would seem important for attention to be allocated to the most relevant aspects of a visual scene. This has led a number of researchers to suggest that attention is preferentially allocated to sources of potential threat within the environment (e.g., Lundqvist & Öhman, 2005). Indeed, it is been suggested that subcortical projections leading to the amygdala allow for the rapid evaluation of the threatening stimuli, and, based on that evaluation, attention may be allocated preferentially to such stimuli (LeDoux, 2000; however, see Cowey, 2004). Given the clear evolutionary advantage of such a system, it has been suggested that this mechanism is phylogenetically old and should be present in all people (Mogg & Bradley, 1998). Although this theory is intuitively appealing, a number of findings have begun to challenge this view. Recent neuroimaging (Bishop, Jenkins, & Correspondence should be addressed to Mark W. Becker, Department of Psychology, Michigan State University, East Lansing, MI 48824, USA. becker54@msu.edu # 2009 The Experimental Psychology Society 1257 DOI: /

3 BECKER AND DETWEILER-BEDELL Lawrence, 2007; Pessoa, 2005) and electrophysiological (Holmes, Vuilleumier, & Eimer, 2003) studies suggest that the amygdala is activated by threat only in conditions of low load; when a primary task is made more demanding, the amygdala does not seem to react to an incidental threatening stimulus. This finding challenges the automatic nature of the amygdala s response, thereby limiting the extent to which the amygdala can act as a rapid, automatic alarm system. Although these findings limit the situations under which this system may function, they are still broadly consistent with the view that there is a bias to orient attention towards threatening stimuli, provided that adequate resources are available to support the evaluation of the threatening stimuli by the amygdala. Behavioural research, however, has begun to challenge the claim that there is a default bias to attend preferentially to threatening stimuli. Although there are a number of reports suggesting that threatening objects (Öhman, Flykt, & Esteves, 2001) and faces (Lundqvist & Öhman, 2005) capture attention, other researchers have failed to replicate these results (Koster, Verschuere, Burssens, Custers, & Crombez, 2007). In addition, a number of reports comparing anxious or phobic participants to typical participants fail to demonstrate attentional capture by threatening objects (Caseras, Garner, Bradley, & Mogg, 2007) or faces (Fox, 2002) among typical participants. The failure to find evidence for attentional capture by threatening stimuli among nonanxious participants seems problematic for the theory that almost all people should have a bias to attend rapidly to such stimuli. There are, however, two ways that a proponent of the theory might discount these contrary results. First, one might argue that typical lab settings and stimuli are so innocuous that only participants who are especially sensitive to threat (e.g., phobic or anxious participants) will evaluate lab-based stimuli as threatening; nonanxious people will not perceive them as threatening. To evaluate this explanation, researchers have attempted to make the lab experience less innocuous by pairing subsets of their stimuli with loud noise bursts, thus conditioning a more powerful fear response among participants. Nevertheless, even under these conditions, results are mixed. Some researchers find that attention is captured by fear-conditioned stimuli (Koster, Crombez, Van Damme, Verschuere, & De Houwer, 2004), but others fail to observe such an effect (Stormark, Hugdahl, & Posner, 1999). Thus there is no clear evidence that the failure to find consistent effects is due to the stimuli not being threatening enough. Second, one might use the aforementioned neurophysiological findings to claim that disparate behavioural results arise because the cognitive load of the primary task varies across experiments. With low-load tasks, the warning system is activated, and one finds evidence for the rapid reorienting of attention towards threat. With high-load tasks, there are insufficient resources to activate the warning system, and one fails to find evidence for the rapid reorienting of attention towards threat. Consistent with this explanation, most behavioural experiments investigating this issue use tasks that require participants to make overt decisions and responses (e.g., visual search, Posner cueing, or dot probe tasks). These primary tasks may influence the likelihood of the threatening stimulus receiving adequate resources to activate the amygdala. In addition, the tasks impose attentional sets. These attentional sets may create their own biases to look toward or away from threatening objects. In sum, there may be a default attentional bias toward threat, but experimental tasks may interfere with the ability to find the effect either by imposing an attentional set that creates its own bias or by increasing the perceptual or attentional load to such an extent that the amygdala is not able to evaluate a stimulus as threatening. Alternatively, it is possible that the presumed default bias to attend to threatening stimuli may not exist within nonanxious people. In order to avoid potential task-related confounds and to evaluate whether there is a default bias to shift attention towards threatening stimuli, we investigated overt shifts of attention while participants performed a passive viewing 1258 THE QUARTERLY JOURNAL OF EXPERIMENTAL PSYCHOLOGY, 2009, 62 (7)

4 AVOIDANCE OF THREAT task. The lack of a primary task is the boundary condition of a low-load primary task. That is, removing explicit task demands should allow any default attentional bias, however slight, to exert its influence. Of course, in the absence of an explicit search or decision task, such a bias would have to be observed through participants eye movements. Thus we tracked participant s eye movements while they passively viewed displays. For several reasons, we chose to use facial expressions of emotion as the stimuli for this passive viewing task. Basic facial expressions of emotion are thought to be relatively universal (Ekman, 1973) and are detected via the low spatial frequencies that are available in the periphery (Vuilleumier & Pourtois, 2007). Moreover, they lead to rapid amygdala activation (Palermo & Rhodes, 2007; Sergerie, Chochol, & Armony, 2008; however, see Cowey, 2004) and can be detected subcortically (de Gelder, Vroomen, Pourtois, & Weiskrantz, 1999). All of these reasons suggest that facial expressions of emotion should be particularly effective, naturalistic stimuli in an investigation of how and to what extent potential threats influence visual attention. EXPERIMENT 1 Method Participants A total of 25 college undergraduates with normal or corrected-to-normal vision participated. Procedure Participants were told that we were interested in the eye movements that people make when looking at faces. They were asked to view a series of images depicting people s faces and to look at the images as they normally would. Thus the task was a passive viewing task with no explicit search instructions. A series of 64 images was shown to the participant. Each image was displayed for four seconds and was then replaced with a central fixation point. Participants had to maintain fixation on the central fixation point in order to begin the next trial. Each image consisted of four Ekman faces that appeared for four seconds at the corners of an imaginary square ( of visual angle from nose to nose) centred on fixation (Figure 1). The Ekman images were cropped into ovals (78 high 58 wide) depicting only the face. In each display, three of the faces were neutral, and the fourth depicted either happiness or fear. In half of the displays, all four images appeared in an upright orientation; in the remaining half, all four images appeared upside down in order to provide an experimental control with visual properties nearly equivalent to those of the corresponding experimental stimulus. The 64 images represented the complete counterbalancing of four Ekman models each displaying one of two emotions at each of four locations in each of two orientations. Eye-tracking procedures Participants were fitted with an EyeLinkII videobased eye tracker. The tracker sampled eye position at 500 Hz and recorded participants gaze along the x, y pixel coordinates of the screen. Prior to beginning the experimental trials, the eye tracker was individually calibrated by having the participant fixate a series of small bullseyes that appeared in nine positions distributed throughout the screen. The eye tracker was adjusted and recalibrated until the maximum tracking error across the nine positions was less than 0.4 degrees of visual angle. Between each trial participants had to fixate a central fixation point in order to verify that the calibration was still accurate and correct for any drift across trials. This ensured that the eye tracker s accuracy was maintained throughout the experiment. Results and discussion To evaluate whether overt attention was rapidly diverted to the emotional faces, we evaluated two dependent variables: the ordinal fixation number of the first fixation on the emotional face and the distance of the scan path made by the eye before it reached the emotional face. The ordinal fixation number of the first fixation was obtained by THE QUARTERLY JOURNAL OF EXPERIMENTAL PSYCHOLOGY, 2009, 62 (7) 1259

5 BECKER AND DETWEILER-BEDELL Figure 1. Example of the four types of displays used in Experiment 1. Left panels show a happy condition and its inverted control. Right panels show a fear condition and inverted control. counting the number of fixations made within a scene prior to first fixating on the emotional face. This indicates how many other locations received overt attentional deployments before the emotional face received attention. The scan path distance was derived by calculating the distance between each fixation and summing the distance travelled by the eye before its first fixation on the emotional face. This measured whether the eye traced a more or less direct path to the emotional face. Both are measures of the attentional priority given to the emotional face relative to the display s neutral faces. Two 2 2 repeated measure analyses of variance (ANOVAs) with two levels of facial emotion (fearful, happy) and two levels of display orientation (upright, inverted) were conducted, one with ordinal fixation number and one with scan path distance as the dependent variable. Rather than finding evidence for a rapid diversion of attention towards threat, both measures suggest that participants actively avoided an upright fearful face (Figure 2, top panels). The critical emotion by orientation interaction was significant for ordinal fixation number, F(1, 24) ¼ 5.82, p ¼.024, and for scan path distance, F(1, 24) ¼ 6.66, p ¼.016. These effects were driven by the fact that the participants avoided looking at the upright fearful face. A planned contrast comparing the upright fearful face to a combination of the three other conditions ordinal fixation number, F(1, 24) ¼ 11.36, p ¼.003; scan path distance, F(1, 24) 1260 THE QUARTERLY JOURNAL OF EXPERIMENTAL PSYCHOLOGY, 2009, 62 (7)

6 AVOIDANCE OF THREAT Figure 2. Top panels plot the data from Experiment 1, and bottom panels plot the data from Experiment 2. The leftward panels (A1 and A2) plot the mean ordinal fixation number of the first fixation on the emotional faces as function of facial expression and orientation. The middle panels (B1 and B2) plot the total distance the eye scanned prior to first fixating on the emotion faces. Error bars for Panels A and B are withinsubject error bars (Loftus & Masson, 1994). The rightward panels plot the percentage of first saccades, post stimulus onset, that ended on the emotional face for each condition. The dashed line is the chance probability of looking at a given face first. Error bars are 95% confidence intervals. ¼ 8.16, p ¼.009 or to only the upright happy face ordinal fixation number, F(1, 24) ¼ 10.91, p ¼.003; scan path distance F(1, 24) ¼ 7.18, p ¼.013 produced significant differences for both dependent measures. This pattern of results suggests that participants actively avoided the upright fearful face, leading to both later overt shifts of attention to the fearful face and longer scan paths to the face. Importantly, we found clear evidence that the negative faces were evaluated rapidly. The bias to avoid a fearful face occurred as early as the first eye movement post stimulus onset (Figure 2). Given that there were four faces in the display, the chance odds of making the saccade to a particular face were.25. Single sample t tests show that the observed probability of making the first saccade to an upright happy face, t(24) ¼ 0.89, p ¼.380, inverted happy face, t(24) ¼ 0.53, p ¼.603, and inverted fearful face, t(24) ¼ 21.92, p ¼.067, were within error of this chance value. However, the odds of making the first saccade to the upright fearful face was significantly below chance, t(24) ¼ 3.73, p ¼.001, suggesting that the bias to avoid the fearful face began even before the first eye movement was made away from the central fixation point (e.g., within the first 300 ms of the display). In summary, Experiment 1 suggests that threat is evaluated rapidly and results in active avoidance of, rather than overt attention towards, a fearful face. EXPERIMENT 2 Conceivably, proponents of the view that attention is allocated rapidly to potential threats might argue that a fearful face is not the source of threat per se, suggesting that in such a context the threat would be located elsewhere in the display. Under this explanation, the rapid detection of fear should THE QUARTERLY JOURNAL OF EXPERIMENTAL PSYCHOLOGY, 2009, 62 (7) 1261

7 BECKER AND DETWEILER-BEDELL result in a rapid shift of attention not toward the fearful face, but away from it toward the object eliciting the fear. To test this explanation in Experiment 2, we replicated the previous experiment while including an additional 32 trials in which a single angry face was paired with three neutral faces (the 32 additional displays completely mirrored the set of angry and happy images). Like fear, anger is associated with threat. Unlike fear, the angry person is the source of threat. Thus, under the alternative explanation of Experiment 1, we should find rapid shifts of attention towards the angry faces but away from the fearful ones. A total of 25 undergraduates, who did not participate in Experiment 1, participated in this second study. Results and discussion Two 3 2 ANOVAs were run, one for each dependent variable (Figure 2, bottom panels). There was a significant main effect of emotion ordinal fixation number, F(2, 48) ¼ 4.50, p ¼.016; scan path distance, F(2, 48) ¼ 5.27, p ¼.009 and a significant emotion by orientation interaction ordinal fixation number, F(2, 48) ¼ 3.58, p ¼.035; scan path distance, F(2, 48) ¼ 3.11, p ¼.054. The main effect of orientation was not significant ordinal fixation number, F(1, 24) ¼ 2.99, p ¼.096; scan path distance, F(1, 24), 1. To further investigate how these effects related to the different emotional conditions, we first eliminated the angry condition and replicated the analyses that were performed for Experiment 1. These analyses confirmed the finding that participants actively avoided the upright fearful face. For both the ordinal fixation number data and the scan path distance data, there was a significant emotion by orientation interaction ordinal, F(1, 24) ¼ 5.97, p ¼.022; scan path, F(1, 24) ¼ 5.92, p ¼.023. A planned contrast comparing the upright fearful face to the three other conditions was significant ordinal, F(1, 24) ¼ 8.88, p ¼.007; scan path, F(1, 24) ¼ 8.27, p ¼.008 and the upright fearful face was fixated less directly than the upright happy face ordinal, F(1, 24) ¼ 7.01, p ¼.014; scan path, F(1, 24) ¼ 8.17, p ¼.009. This pattern of results replicated those of Experiment 1, clearly demonstrating that people actively avoid looking at a fearful face. Next we examined whether attention would be allocated rapidly to an angry face a face that both indicates and is the source of potential threat. Instead of finding evidence that people rapidly shifted overt attention towards the angry face, we once again found that participants avoided the angry faces, regardless of whether they appeared upright or inverted. A 2 2 ANOVA comparing the happy and angry conditions found a main effect of emotion ordinal, F(1, 24) ¼ 9.91, p ¼.004; scan path, F(1, 24) ¼ 8.57, p ¼.007 but no main effect of orientation (both Fs, 1) nor an emotion by orientation interaction ordinal, F(1, 24) ¼ , p ¼.235; scan path, F(1, 24) ¼ 3.467, p ¼.075. Planned comparisons (two-tailed paired t tests) between the upright angry condition and the upright happy condition revealed that the angry face was fixated later than the happy face in terms of both ordinal fixation number, t(24) ¼ 3.179, p ¼.004, and scan path distance, t(24) ¼ 4.08, p,.001. The upright angry condition did not differ significantly from the upright fearful face on either measure (both p..27). These data suggest that participants treat an upright angry face very similarly to an upright fearful face. That is, they avoid making overt shifts of attention to it. Participants also seemed to avoid the inverted angry face. The inverted angry face was looked at later than the upright happy face, t(24) ¼ 2.52, p ¼.038, for ordinal fixation number; t(24) ¼ 2.25, p ¼.034, for scan path distance, but did not differ from the upright angry or upright fearful conditions for either dependent measure (all ps..13). The finding that people actively avoid both the upright and the inverted angry faces may suggest that these faces were avoided based on their lowlevel visual salience, rather than their emotional content. Although we cannot rule out this saliency-based explanation, we think it is unlikely. For this explanation to hold, one must assume that the angry face was less salient than the three neutral faces in the display. Given that saliency is determined by how disparate an object s visual 1262 THE QUARTERLY JOURNAL OF EXPERIMENTAL PSYCHOLOGY, 2009, 62 (7)

8 AVOIDANCE OF THREAT features are relative to the other features in a display, it seems unlikely that the face expressing a unique emotion would be the least salient. Instead, we favour the interpretation that the angry face is avoided because it continues to be associated with threat, even when inverted. Regardless of how one interprets the inverted angry condition, our data are quite clear that an upright angry face does not attract early attention. Similar to Experiment 1, the active avoidance developed fairly rapidly. People made fewer initial eye movements towards the upright fearful, t(24) ¼ 2.70, p ¼.013, upright angry, t(24) ¼ 2.76, p ¼.011, and inverted angry faces, t(24) ¼ 2.02, p ¼.054, than one would have expected by chance (Figure 2). Taken together, the results from Experiments 1 and 2 suggest that potential threat (either fearful face or angry faces) is evaluated rapidly but that overt attention actively avoids the threatening stimuli rather than being drawn to them. SUMMARY In two experiments we tracked eye movements while participants passively viewed displays consisting of one emotional face among three neutral faces in order to test the theory that fearful and angry facial expressions are evaluated rapidly and should cause a rapid shift of attention toward such stimuli. Although the passive viewing task should have been very sensitive to default attentional biases, we found no evidence that overt attention was biased toward fearful or angry faces. Instead, people tended to actively avoid looking at these faces. This avoidance was evident very early in scene viewing (i.e., within 300 ms of display onset), suggesting that the threat associated with the faces was evaluated rapidly while the faces were still in the periphery. Thus, our main findings are that negative facial expressions are rapidly analysed, but rather than attract attention, they are actively avoided. Importantly, in our experiment, participants had no primary task, and thus our findings cannot be explained based on task-related attentional sets biasing attention away from threat or the primary task load impairing the ability of the amygdala to evaluate the threat. Instead, it appears that the threat was evaluated rapidly, but this evaluation led to avoidance rather than attraction. We believe this passive viewing task is a very sensitive test of the theory that there is a persistent, underlying bias to attend toward threatening stimuli. One could imagine that such a bias exists, but will not manifest itself under situations in which short-term goals supersede this underlying bias. However, in our passive viewing task, there were no short-term goals to compete with such bias, and it therefore should have manifested itself, if it existed. Our failure to find such a bias is strong evidence against the view that there is an underlying bias to orient towards threat in a rapid and reflexive manner. Instead, our results are consistent with a growing body of literature that fails to find a default tendency for attention to be preferential allocated towards threat in typical participants (Bar-Haim, Lamy, Pergamin, Bakermans-Kranenburg, & van IJzendoorn, 2007), and it is consistent with an emerging view that the bias among typical participants may, in fact, be away from threatening stimuli towards positive stimuli (Frewen, Dozois, Joanisse, & Neufeld, 2008). REFERENCES Original manuscript received 6 November 2008 Accepted revision received 8 December 2008 First published online 9 March 2009 Bar-Haim, Y., Lamy, D., Pergamin, L., Bakermans- Kranenburg, M. J., & van IJzendoorn, M. H. (2007). Threat-related attentional bias in anxious and nonanxious individuals: A meta-analytic study. Psychological Bulletin, 133, Becker, M. W., & Pashler, H. (2005). Awareness of the continuously visible: Information acquisition during preview. Perception & Psychophysics, 67, Bishop, S. J., Jenkins, R., & Lawrence, A. D. (2007). Neural processing of fearful faces: Effects of anxiety THE QUARTERLY JOURNAL OF EXPERIMENTAL PSYCHOLOGY, 2009, 62 (7) 1263

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