Do Emotional Faces Automatically Attract Attention? - CSU, Chico

Emotion 2007, Vol. 7, No. 2, 285–295

Copyright 2007 by the American Psychological Association 1528-3542/07/$12.00 DOI: 10.1037/1528-3542.7.2.285

Attention for Emotional Faces Under Restricted Awareness Revisited: Do Emotional Faces Automatically Attract Attention? Ernst H. W. Koster, Bruno Verschuere, Benjamin Burssens, Roel Custers, and Geert Crombez Ghent University, Belgium Theoretical models of attention for affective information have assigned a special status to the cognitive processing of emotional facial expressions. One specific claim in this regard is that emotional faces automatically attract visual attention. In three experiments, the authors investigated attentional cueing by angry, happy, and neutral facial expressions that were presented under conditions of limited awareness. In these experiments, facial expressions were presented in a masked (14 ms or 34 ms, masked by a neutral face) and unmasked fashion (34 ms or 100 ms). Compared with trials containing neutral cues, delayed responding was found on trials with emotional cues in the unmasked, 100-ms condition, suggesting stronger allocation of cognitive resources to emotional faces. However, in both masked and unmasked conditions, the hypothesized cueing of visual attention to the location of emotional facial expression was not found. In contrary, attentional cueing by emotional faces was less strong compared with neutral faces in the unmasked, 100-ms condition. These data suggest that briefly presented emotional faces influence cognitive processing but do not automatically capture visual attention. Keywords: attention, faces, emotion, spatial cueing, time-course

volved in emotion processing and attention (e.g., Lidell et al., 2005; Pourtois, Grandjean, Sander, & Vuilleumier, 2004; Schupp et al., 2004; Whalen et al., 2001). Moreover, in patients with unilateral neglect, there is also strong evidence to suggest that emotional facial expressions capture attention even when presented in the contralesional hemifield (e.g., Vuilleumier, 2000). However, the idea that emotional faces could be processed without attentional resources was challenged by elegant studies, demonstrating that a minimal degree of attention is required for emotional processing of faces (Holmes, Vuilleumier, & Eimer, 2003; Pessoa, Kastner, & Ungerleider, 2002). A specific question in this the context is whether peripheral emotional faces automatically capture visual attention. Brainimaging studies indicate that preattentive processing of emotional compared with neutral faces results, among others, in increased responding in several areas of the visual cortex, which is thought to reflect enhanced attentional orienting to emotional faces (Pessoa et al., 2002). For instance, a recent study event-related fMRI study by Pourtois, Schwartz, Seghier, Lazeyras, and Vuilleumier (2006) indicated that when emotional faces were briefly (100 ms) presented as exogenous cues requiring shifts of attention, fearful faces, relative to happy faces, were associated with distinct neural structures involved in the control of spatial attention. However, these specific neuropsychological activities are not always accompanied by enhanced attentional orienting to emotional facial expressions in behavioral tasks (e.g., Pourtois et al., 2006). Close examination of the empirical data from behavioral data reveals that attentional orienting to emotional faces is not frequently found in normal participants. In this study, we examine automatic cueing of spatial attention by emotional faces in a behavioral task. We start with an overview of the available empirical

Theoretical models of attention for affective information ¨ hman, 1993; O ¨ hman, & Mineka, 2001) have assigned a (O special status to the cognitive processing of emotional facial expressions. It has been argued that faces pose a special class of stimuli with high social and biological relevance. Even before conscious identification, emotional (especially fear-relevant) faces are linked to activation of brain structures (i.e., amygdala) ¨ hman, & Dolan, involved in emotion processing (Morris, O 1998, 1999). In the domain of fear, such findings have been taken as empirical evidence that face processing may involve an innate or biologically prepared dedicated cerebral module that is capable of encoding facial features preattentively (for re¨ hman, Flykt, & Lundqvist, 2000; O ¨ hman & views, see O Mineka, 2001). In this regard, it has been argued that threatening faces are more easily associated with aversive stimuli (e.g., ¨ hman & Dimberg, 1978) and automatically capture attention O ¨ hman, 2002). (O These theoretical predictions have instigated a lively empirical debate on automatic processing of emotional facial expressions. Initial studies using measures such as functional MRI (fMRI) and event-related potentials (ERP) generally confirm that briefly presented emotional, particularly fearful, faces are associated with heightened activation of neural structures in-

Ernst H. W. Koster, Bruno Verschuere, Benjamin Burssens, Roel Custers, and Geert Crombez, Department of Psychology, Ghent University, Belgium. The authors thank Jan De Houwer for useful comments and Els De Bruycker for aid in the data collection. Ernst Koster is a postdoc fellow of the Fund for Scientific Research-Flanders (FWO), Belgium. Correspondence concerning this article should be addressed to Ernst H. W. Koster, Ghent University, Department of Psychology, Henri Dunantlaan 2, B-9000, Gent, Belgium. E-mail: [email protected] 285

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behavioral data on attentional orienting to emotional facial expressions.

task may not be the most suitable task to examine attentional orienting to emotional information.

Empirical Evidence on Attention to Emotional Facial Expressions

The Present Study

A first line of studies has investigated the “face-in-the-crowd” phenomenon using the visual search task This task is a wellestablished paradigm from experimental psychology to investigate the automatic versus controlled detection of stimuli (Treisman & Souther, 1985). In a typical version of this task, individuals are asked to indicate the presence of a target stimulus within an array of distracting stimuli. Hansen and Hansen (1988) developed an emotional variant of this task, including pictures of emotional faces to examine attention to angry faces. On half of the trials, one of the faces in the crowd displayed a different emotion than the other faces (i.e., a happy face in an angry crowd and an angry face in a happy crowd). It was found that individuals were faster to locate an angry face in a happy crowd than a happy face in an angry crowd. Because the time needed to detect an angry face in the happy crowd was not affected by the number of distracters, Hansen and Hansen concluded that angry faces were detected automatically. Replications with improved methodology and stimulus material indicate efficient, but not automatic, detection of angry compared with happy faces in the visual search paradigm (e.g., Eastwood, Smilek, & Merikle, 2001; Fox et al., 2000). However, the visual search task has been criticized on several grounds, including the difficulty in separating the attentional effects caused by the targets from the distracters (Koster, Crombez, Verschuere, & De Houwer, 2004a) and motor preparation as an alternative explanation for reaction time (RT) speeding to emotional faces (Flykt, 2006). Attention for emotional faces has also been investigated in the visual dot probe task (MacLeod, Mathews, & Tata, 1986). In this task, a picture pair comprised of one emotional and one neutral picture is displayed on a screen, with the two stimuli pictures presented at spatially separated locations. After a brief period, these pictures disappear and a small dot is presented at the location of one of the pictures. Systematically faster responding to the dot probe presented at the location previously occupied by the emotional stimulus indicates selective attention for emotional information. A couple of studies examined attention for emotional facial expressions presented for short durations. Three experiments by Mogg and Bradley (1999) revealed that 17-ms masked presentation of angry faces resulted in preferential attention to its location when it was presented in the left visual field. Results were less strong and absent when angry faces were presented at the right visual field or for 34 ms. These findings were not moderated by anxiety level. However, Fox, Russo, and Dutton (2002) conducted an experiment on attention to fearful and happy faces (17 ms, masked) in the dot probe that showed a slightly different pattern of results: Only the high anxious individuals showed attentional orienting toward the fearful faces. Again this effect was only found for threat presented in the left visual field. Thus, empirical data obtained in the dot probe task are still inconclusive. In addition, it has been argued that studies using the dot probe task do not allow distinguishing between the initial engagement of visual attention with and impaired disengagement of visual attention from threat (Fox, Russo, Bowles, & Dutton, 2001). Therefore, the dot probe

We set out to further investigate orienting of attention to emotional facial expressions in function of awareness and presentation duration of the emotional information. For this purpose, we presented masked and unmasked emotional facial expressions in a modified exogenous cueing task. In the original exogenous cueing paradigm (Posner, 1980), participants are asked to detect a visual target presented at a left or right peripheral location. On most of the trials, a stimulus precedes the target and validly cues at its spatial location (“valid” trials). On the remaining trials, the preceding stimulus is presented at the opposite spatial location of the target and thus invalidly cues the target’s location (“invalid” trials). In general, faster responding is found on valid trials compared to invalid trials, a finding that is referred to as the “cue validity” effect. In the emotional modification of this paradigm, the emotional value of the cue is varied (i.e., emotional vs. neutral), which allows investigating attentional engagement and disengagement effects as a function of cue valence. Facilitated attentional engagement by the emotional cue has been related to the attentional capture by emotional information and its initial detection. This effect is evidenced by reaction time benefits on valid trials containing emotional cues compared to valid trials containing neutral cues. Difficulty in disengaging attention from emotional information has been related to attentional holding by threat and is evidenced by slower responding on invalid trials containing emotional cues compared to invalid trials containing neutral cues (Fox et al., 2001). A number of studies have used the modified cueing task to investigate attention for schematic and real emotional expressions (Fox et al., 2001; Fox et al., 2002; Georgiou et al., 2005). In these studies faces were presented for 100 ms, 250 ms, and 600 ms, with 75% valid and 25% invalid trials. It was found that high anxious individuals had difficulty in disengaging from angry faces. In the low anxious participants, usually no preferential attention for emotional faces was observed. Provided the high social relevance of emotional facial expressions, models of attention would predict ¨ hman & Mineka, 2001). that faces attract attention in everyone (O Furthermore, it is surprising that attentional effects were restricted to disengagement as it has been shown that relevant cues also elicit attentional engagement effects in the modified cueing paradigm (e.g., Koster, Crombez, Van Damme, Verschuere, & De Houwer, 2004b, 2005). The absence of engagement effects may be related to the higher proportion of valid compared with invalid trials. That is, it might be difficult to find faster responding on valid emotional compared with valid neutral trials if orienting to the cues is task-relevant (cf. Mogg & Bradley, 1998). Enhanced attentional engagement has mainly been found in studies using a 50% valid/ invalid proportion (Koster et al., 2004b). In the present study, we further investigated the time-course of attentional orienting to emotional facial using the modified cueing paradigm in unselected participants. Several methodological issues are of key importance in the present study: The emotional facial expressions were presented in the periphery, to the left or right hemifield. In the experiments, the emotional facial expressions were presented under conditions of restricted awareness, using

ATTENTION FOR EMOTIONAL FACES

backward masking. In Experiments 1A and 2, the emotional faces were presented for 34 ms and subsequently masked by a neutral face for another 66 ms. Such masked presentation should be sufficient to impair conscious recognition of the emotional faces ¨ hman, 1993). In an unmasked condition, faces were (Esteves & O presented for 100 ms (Experiments 1–3). Previous studies have frequently employed jumbled faces as mask. However, with such a procedure it could be that the changes between the emotional face and the mask facilitated attentional capture. Therefore, we ¨ hman, used neutral faces as masking stimuli (cf. Esteves & O 1993). In order to prevent a biased comparison because of larger changes in the masked emotional presentations compared to the masked neutral presentations, the faces used as prime and mask in the neutral presentations had the opposite gender. Responding on the masked emotional faces was compared to responding on masked neutral faces. In Experiment 1B, we presented all faces unmasked to examine whether the masking procedure affected attentional processes. In Experiment 2, an awareness check indicated that individuals could differentiate above chance between emotional versus neutral expressions presented under masked conditions. Therefore, in Experiment 3 masked facial expressions were presented under conditions of more restricted awareness.

Experiment 1 In Experiment 1A, we examined whether emotional faces attracted visual attention to their location in masked and unmasked conditions. In order to examine whether the masking stimulus affected the attentional effects obtained in Experiment 1A, we tested whether similar results were obtained when cues were presented in an unmasked version but for similar durations in Experiment 1B.

Method Participants. Forty-nine undergraduate students participated for course credit. All participants had normal or corrected-tonormal vision. Materials. The Exogenous Cueing Task was programmed using the Inquisit Millisecond software package (Inquisit 1.32, 2001) and ran on a laptop computer with a 60 Hz, 15-inch color monitor. Inquisit measures response times with millisecond accuracy (De Clercq, Crombez, Roeyers, & Buysse, 2003). All stimuli were presented against a black background. On every trial, a white fixation cross was presented in the middle of the screen, flanked by two white rectangles (6 cm high by 8 cm wide; subtending 5.7° ⫻ 7.6°). The middle of these rectangles was 7.5 cm (7.2°) from the fixation cross. Cues and targets were presented in the middle of the rectangles. Cues consisted of emotional and neutral expressions taken from the Karolinska Directed Emotional ¨ hman, 1998). Faced (KDEF) database (Lundqvist, Flykt, & O These pictures were adjusted to exclude interference of background stimuli (hair, clothing). All pictures were digitized to the same size (326 ⫻ 326 pixels) as the white rectangles and were presented in color. On the basis of ratings on the clarity and intensity of the expressed emotion (Goeleven, De Raedt, Leyman, & Verschuere, 2005) we selected 45 pictures as cues: 15 angry, 15 happy, and 15 neutral expressions. Two additional neutral pictures were selected for the masking procedure with one male and one

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female face. Another 12 pictures with mixed emotional valence were selected for the practice phase.1 Targets were black squares (1.1 ⫻ 1.1 cm; subtending 1° ⫻ 1°). Responses were made by pressing one of two keys (target left: “q,” target right: “5”) with the left and right index finger on an AZERTY keyboard. Procedure. Participants were tested in small groups of a maximum four individuals in a quiet experiment room. In order to reduce any interference between individuals, computers were located in each corner of the room, and participants were instructed to refrain from interaction during the attentional task. At the start of the experiment, an informed consent form was administered. The sequence of events on a test trial consisted of a 500-ms presentation of the fixation cross and white rectangles. The fixation cross remained on screen during the rest of the trial sequence. Then, a pictorial cue appeared for either 34 ms in the masked condition or 100 ms in the unmasked condition. The 34-ms cue was masked by a neutral facial expression for 66 ms, ensuring that only the presentation duration of the cues varied but not the stimulus onset asynchrony (SOA). The target was presented 17 ms after cue offset and remained on screen until a response was made. Upon responding the next trial started immediately. Participants practiced the attentional task during 12 trials. The test phase consisted of 240 trials. Participants could take a short break after 120 trials. During the test phase, an equal amount of valid (left cue/left target and right cue/right target) and invalid (left cue/right target and right cue/left target) trials were presented. The cues were presented at random for 34 or 100 ms, at the left or right hemifield, with an equal number of presentations for each picture and trial type. Each cue picture was repeated about five times. The masking facial expression had the opposite gender as the preceding cue. Participants were at approximately 60-cm viewing distance from the computer screen to perform the cueing task. Instructions were presented on the computer screen. Participants were asked to respond as quickly as possible to the location of the target without sacrificing accuracy. They were informed that a cue preceded the presentation of the target and that the cue location was not predictive of target location, with some targets following at the cue position and some targets following at the opposite location of the cue.

Results Data preparation. On inspection of the data, results from one participant were removed from the analyses because an excessive number of errors and outliers (⬎20%). Trials with errors were discarded from analyses (M ⫽ 1.2%). In line with previous studies (Koster et al., 2004b), RTs smaller than 150 ms and RTs larger than 750 ms were considered outliers because of anticipatory and delayed responding, respectively. Furthermore, RTs deviating more than 3 SDs from the individual mean RT were excluded. Statistical analyses were run on 97.5% of the data. Overall effects. Reaction times were subjected to a 2 (presentation condition: masked, unmasked) ⫻ 3 (cue valence: angry, happy, neutral) ⫻ 2 (cue validity: valid, invalid) repeated measures 1

The exact picture numbers and their selection criteria for valence and arousal are available from the authors upon request.

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analysis of variance (ANOVA). If the higher-order interactions were significant, cue validity effects (reaction time on invalid trials minus reaction times on valid trials) were examined, which provide an easy measure of overall attention for the different cue types. Positive scores indicate attention toward a cue, whereas negative scores indicate attention away from the cue. At this point, we checked for the effects of threat presented at the left versus right visual field. Then, in order to examine our hypotheses related to the specific components of attention, attentional engagement and disengagement scores were calculated. The GreenhouseGeisser correction (with adjusted dfs) is reported if the sphericity assumption was violated. The mean reaction time data are depicted in Table 1. The 2 ⫻ 3 ⫻ 2 ANOVA revealed a significant main effects of presentation condition, F(1, 47) ⫽ 82.49, p ⬍ .001, with faster responding on pictures presented for unmasked faces (M ⫽ 353 ms) than for the masked faces (M ⫽ 368 ms). There also was a strong effect of cue validity, F(1, 47) ⫽ 16.92, p ⬍ .001, due to faster responding on valid (M ⫽ 355 ms) compared with invalid trials (M ⫽ 366 ms). The main effect of valence was also significant F(2, 94) ⫽ 110.49, p ⬍ .001, with faster responses on trials containing neutral faces (M ⫽ 343 ms) compared to angry (M ⫽ 368 ms) and happy faces (M ⫽ 370 ms). Of importance, there was a statistically significant three-way interaction between presentation condition ⫻ cue valence ⫻ cue validity, F(2, 94) ⫽ 17.97, p ⬍ .001, and the significant two-way interactions between presentation condition ⫻ cue validity, presentation condition ⫻ cue valence, and cue valence ⫻ cue validity could be subsumed under this effect. Mean cue validity effects in function of presentation condition and cue valence are depicted in Figure 1. In order to interpret the three-way interaction effect, separate ANOVAs for each presentation condition were performed. Masked condition. In this condition, there was a significant main effect of cue validity, F(1, 47) ⫽ 4.48, p ⬍ .05. No other effects were significant (cue valence ⫻ cue validity, F(1, 47) ⫽ 2.20, p ⫽ .13, other F ⬍ 1.0), indicating no differential cue of visual attention at this presentation condition.2 In the absence of this interaction, calculation of attentional engagement and disengagement indices is not warranted.

Table 1 Mean Reaction Times (in ms), Standard Deviations, and Cue Validity Indices (CVI) as a Function of Presentation Condition, Cue Valence and Cue Validity in Experiment 1A

Masked (34 ms)

Cue Valence

Cue Validity

Angry

Valid Invalid Valid Invalid Valid Invalid Valid Invalid Valid Invalid Valid Invalid

Happy Neutral Unmasked (100 ms)

Angry Happy Neutral

M 361 371 364 374 369 369 367 374 370 372 299 334

SD CVI 37 45 38 46 45 44 33 41 37 39 39 41

Figure 1. Mean cue validity indices (in ms) as a function of presentation conditions and cue valence in Experiments 1 to 3.

Unmasked condition. In line with the overall ANOVA, there were main effects of cue validity, F(1, 47) ⫽ 27.74, p ⬍ .001, and cue valence, F(2, 76) ⫽ 179.84, p ⬍ .001. More important, the interaction between cue validity ⫻ cue valence was also significant, F(2, 94) ⫽ 21.45, p ⬍ .001. In order to examine this interaction effect, cue validity indices were calculated for each cue valence. The cue validity effects are depicted together with the mean latencies in Table 1. Paired comparison t tests indicate that the cue validity was significantly larger for neutral pictures than for angry pictures, t(47) ⫽ 4.45, p ⬍ .001, and happy pictures, t(47) ⫽ 6.55, p ⬍ .001. The difference between angry and happy faces was not significant (t ⬍ 1.2). As clear from Table 1, responding to trials containing neutral cues was faster compared with trials containing emotional material. Provided that responding to the neutral cues provide the baseline to calculate attentional engagement and disengagement, these indices would be strongly distorted by the general facilitation on trials containing neutral cues (see Yiend & Mathews, 2001). Therefore, these indices are not presented here.3

Experiment 1B Method Participants. Twenty-four new undergraduate students participated for course credit. All participants had normal or correctedto-normal vision. Materials and procedure. The exogenous cueing task was similar to Experiment 1A, except for the masking procedure. In the present experiment all stimuli were presented unmasked for 34 and 100 ms, respectively. The experiment was run individually to exclude any interference between participants.

10 10 0 7 2 35

2 Previous studies have obtained differential effects in function of cue or target position under masked presentation conditions (e.g., Mogg & Bradley, 1999). An initial ANOVA including the factors cue position and target position instead of cue validity revealed no additional interactions involving spatial factors (Cue Valence ⫻ Cue Position ⫻ Target position, F(2, 96) ⫽ 2.17, p ⬎ 1.0; all other Fs ⬍ 2.2). Therefore, we report the ANOVAs using only cue validity as factor. 3 It is noteworthy that the cue validity index does not suffer from this problem because responding on valid trials is subtracted from responding to invalid trials within each valence.


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Results

Discussion

Data preparation. Trials with errors were discarded from analyses (M ⫽ 2.41%). Outliers were excluded. Statistical analyses were run on 95.9% of the data. Overall effects. The mean reaction time data are depicted in Table 2. The 2 ⫻ 3 ⫻ 2 ANOVA revealed a significant main effect of cue validity, F(1, 23) ⫽ 187.68, p ⬍ .001, with faster responding on valid trials (M ⫽ 349 ms) compared to invalid trials (M ⫽ 367 ms). There also was a main effect of valence, F(2, 46) ⫽ 187.68, p ⬍ .001. Individuals were slower to respond on trials containing emotional cues (angry faces: M ⫽ 368 ms; happy faces; M ⫽ 370 ms) compared with neutral (neutral faces; M ⫽ 336 ms). Of importance, there was a significant three-way interaction between presentation condition ⫻ cue valence ⫻ cue validity, F(2, 46) ⫽ 6.56, p ⬍ .01. Other interactions could be subsumed under this effect: presentation condition ⫻ cue valence, F(2, 46) ⫽ 183.00, p ⬍ .001; presentation condition ⫻ cue validity, F(1, 23) ⫽ 3.86, p ⫽ .06). In order to interpret the three-way interaction effect, separate ANOVA’s for each presentation condition were performed. 34-ms condition. The 2 ⫻ 2 ANOVA revealed a main effect of cue validity, F(1, 23) ⫽ 31.73, p ⬍ .001. There was trend effect of cue valence, F(2, 46) ⫽ 2.62, p ⬍ .08. No significant interaction was found between cue valence and cue validity (F ⬍ 1.0), indicating no enhanced attentional cue of visual attention by emotional faces at this presentation condition.4 100-ms condition. The 2 ⫻ 2 ANOVA revealed two main effects: cue validity, F(1, 23) ⫽ 13.40, p ⬍ .01 and cue valence, F(2, 46) ⫽ 321.85, p ⬍ .001. The interaction between cue valence and cue validity was significant, F(2, 46) ⫽ 9.13, p ⬍ .001. We further examined this interaction using the cue validity indices. The attentional cueing effect was significantly stronger for neutral faces than for angry faces, t(23) ⫽ 3.26, p ⬍ .01 and happy faces, t(23) ⫽ 3.71, p ⬍ .01 (see Table 2). Provided these effects, attentional engagement and disengagement indices were not calculated.

The results of Experiment 1 provided interesting results on the attentional cueing of visual attention by emotional facial expressions. There was a main effect of cue valence at the unmasked condition. That is, delayed responding was observed to emotional facial expressions compared to neutral facial expressions. This reaction time delay suggests that emotional faces did capture attention and demanded processing resources. However, this effect was not associated with stronger cueing of visual attention: First, in the masked condition visual attention was not attracted to the location of the emotional faces. Experiment 1B showed that the absence of effects was not because of the masking procedure. Second, in the unmasked condition, a stronger cue validity effect was found for neutral faces compared with emotional faces. These data provide disconfirming evidence for the idea that emotional faces capture visual attention more strongly than neutral faces. In fact, at the 100-ms cue presentation, even less attention was allocated to the emotional stimuli. In sum, the findings in Experiment 1 indicate dissociable effects of emotional cues on the allocation of attentional resources in general versus spatial attention. That is, the presentation of emotional faces led to delayed responding to the targets, yet emotional facial expressions failed to cue visual attention to their location more strongly than neutral faces.

Table 2 Mean Reaction Times (in ms), Standard Deviations, and Cue Validity Indices (CVI) as a Function of Cue Valence and Cue Validity at 34- and 100-ms Picture Presentation in Experiment 1B

Unmasked (34 ms)

Cue Valence

Cue Validity

Angry



Angry Happy Neutral

M 349 370 349 372 344 367 376 379 377 380 300 333

Given the interesting and somewhat surprising findings of Experiment 1, we tried to replicate the results of Experiment 1A. An awareness check was included to examine whether participants were able to determine the emotional valence of masked emotional faces. In previous studies, awareness of masked emotional stimuli was assessed by determining the percentage of correctly identified features of the emotional stimuli (e.g., Mogg & Bradley, 1999). However, this type of awareness check is highly sensitive to response bias (Swets, 1964; Macmillan & Creelman, 1991). Therefore, Signal Detection Theory (SDT) was applied to provide a measure of awareness. Participants performed a recognition task and SDT was applied to check whether individuals could reliably detect the masked emotional facial expressions.

Method

SD CVI 32 45 34 45 29 41 33 41 41 39 42 42

Experiment 2

21 23 23 3

Participants. Twenty-four new undergraduate students participated for course credit. All participants had normal or correctedto-normal vision. Materials and procedure. The exogenous cueing task was programmed similar to Experiment 1, with cue presentations of 34 and 100 ms. Awareness check. In order to check for awareness of the masked emotional facial expression a recognition task was administered after the cueing task. In this task only the masked emotional faces were presented under similar conditions as in the attention task. More specifically, pictures were presented randomly to the

3 33

4 An ANOVA that included cue position and target position as withinsubjects factor did not reveal any interactions of valence with spatial location (all Fs ⬍ 1.0). This also holds for Experiments 2 and 3.

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left and right location with trial duration and picture size similar to the attention task. Instead of responding to the target, participants were now asked to judge whether they had seen an emotional face (a “yes-no” format). Participants were informed that they might be able to recognize this by small changes and that they could guess if they were unsure. In order to prevent any extreme response biases, participants were informed that emotional faces would be presented more often than neutral faces. There were 10 practice trials and 80 test trials. In the test phase each facial expression was presented about twice.

Results Data preparation. Trials with errors were discarded from analyses (M ⫽ 0.92%). Outliers were removed following the procedure of Experiment 1. Statistical analyses were run on 97.9% of the data. Overall effects. The 2 (presentation condition) ⫻ 3 (cue valence) ⫻ 2 (cue validity: valid, invalid) repeated measures ANOVA revealed three main effects of presentation condition, F(1, 23) ⫽ 20.34, p ⬍ .001, cue valence, F(2, 46) ⫽ 40.45, p ⬍ .001, and cue validity, F(1, 23) ⫽ 10.20, p ⬍ .01. Responding on unmasked trials (M ⫽ 347 ms) was faster than on masked trials (M ⫽ 357 ms), responding to neutral cues (M ⫽ 336 ms) was faster than to happy (M ⫽ 360 ms) and angry cues (M ⫽ 360 ms), and responding on valid trials (M ⫽ 346 ms) was faster than on invalid trials (M ⫽ 358 ms). There was a significant two-way interaction between presentation condition and cue valence, F(2, 46) ⫽ 14.14, p ⬍ .001, that could be subsumed under the three way interaction of presentation condition ⫻ cue valence ⫻ cue validity, F(2, 46) ⫽ 7.26, p ⬍ .01. All other effects were nonsignificant (cue valence ⫻ cue validity, F(1.62, 37.0) ⫽ 2.24, p ⬎ .1; other Fs ⬍ 1.5). The three-way interaction was followed-up by analyses for masked and unmasked conditions, separately. Masked condition. In the masked condition, the cue valence x cue validity ANOVA revealed the cue validity effect, F(1, 23) ⫽ 6.20, p ⬍ .05, with faster responding on valid (M ⫽ 352 ms) compared with invalid trials (M ⫽ 362 ms). Notably, there also was a main effect of cue valence, F(2, 46) ⫽ 3.63, p ⬍ .05, with faster responding on neutral cues (M ⫽ 352 ms) compared with happy (M ⫽ 361 ms) and angry cues (M ⫽ 358 ms). The interaction between cue valence and cue validity was nonsignificant (F ⬍ 1.3). Unmasked condition. In this condition, main effects of cue valence, F(2, 46) ⫽ 35.50, p ⬍ .001, and cue validity were found, F(1, 23) ⫽ 9.78, p ⬍ .01. Again, there was faster responding on valid (M ⫽ 340 ms) compared with invalid trials (M ⫽ 355 ms), and faster responding on neutral cues (M ⫽ 321 ms) compared with happy (M ⫽ 359 ms) and angry cues (M ⫽ 363 ms). The two-way interaction between cue valence and cue validity was significant, F(2, 46) ⫽ 7.91, p ⬍ .01. Analysis of the cue validity indices clearly show a larger cueing effect for neutral cues compared with the angry, t(23) ⫽ 2.94, p ⬍ .01, and happy cues, t(23) ⫽ 3.87, p ⬍ .01 (see Table 3). Attentional engagement and disengagement scores are not presented because of overall faster responding to trials containing neutral cues. Awareness check. The proportion Hits and False alarms were converted into the nonparametric indices of sensitivity (A’) and

Table 3 Mean Reaction Times (in ms), Standard Deviations, and Cue Validity Indices (CVI) as a Function of Cue Valence and Cue Validity at Masked and Unmasked Conditions in Experiment 2

Masked (34 ms)

Cue Valence

Cue Validity

Angry



Angry Happy Neutral

M 355 361 353 370 349 354 359 366 356 362 305 336

SD CVI 39 38 36 45 38 40 27 39 36 41 27 43

6 17 5 7 6 31

response bias (B”) (Macmillan & Creelman, 1991). Scores of A’ range from 0 to 1, with a score of 0.5 indicating sensitivity at chance level. Scores of B” range from ⫺1 to 1, with a score of 0 indicating no response bias. Despite our instructions, two participants indicated that they had not seen an emotional face. Their scores did not allow calculation of signal detection measures and were excluded from analyses. We compared mean A’ to sensitivity at chance level (0.5) using a one-sample t test. Mean A’ was .68 (SD ⫽ .07), which differed significantly from 0.5, t(21) ⫽ 11.35, p ⬍ .001, indicating that detection of the emotional stimuli is above chance. Mean B” was tested against a neutral response criterion (0). Mean B” ⫽ .04 (SD ⫽ .47) was not different from 0 (t ⬍ 1), indicating a neutral response criterion.

Discussion The results of Experiment 2 again showed an overall delay in responding to targets cued by emotional faces compared with neutral faces. In addition, Experiment 2 showed no cueing of spatial attention by emotional facial expressions presented under conditions of restricted awareness and in the unmasked condition emotional faces even attracted less attention than neutral faces. Thus, the pattern of results is similar to the results of the first experiment. One discrepancy between both experiments is that in Experiment 2 delayed responding was found in both the masked and unmasked condition, whereas this effect was only found in the unmasked condition of Experiment 1. At present there is no clear explanation for this difference. It is unclear why the emotional facial expressions failed to attract visual attention. One explanation could be that preattentive effects have been obscured by stimuli presented close to awareness (Mogg & Bradley, 1999). The awareness check showed that individuals could detect above chance level whether an emotional face had been presented. In this situation, controlled attentional processes might have interfered with the automatic processes caused by presentation of emotional stimuli (Greenwald, Klinger, & Schuh, 1995). In Experiment 3 we examined attentional cueing by emotional faces under conditions of more restricted awareness.

Experiment 3 An experiment was conducted to examine the unexpected findings with regard to the cueing of spatial attention by emotional


faces. It could be argued that the findings might be due to the masking procedure, which did not fully prevented conscious awareness of the emotional faces. In previous studies, such conditions led to reduced attentional orienting to emotional information (Mogg & Bradley, 1999). In order to examine cueing of visual attention by emotional faces under conditions of more restricted awareness, the presentation duration of the faces in the masked condition was decreased to 14 ms. This duration was based on previous work by Williams et al. (2004) suggesting that backwardly masked facial expressions presented for less than 20 ms could not be differentiated above chance from a blank screen. A slightly modified awareness check was administered to examine whether participants noticed differences in stimulus change between the emotional and nonemotional trials. Such differences in stimulus change could affect the attentive processing of the masked faces.

Method Participants. Nineteen undergraduate students participated for course credit. All participants had normal or corrected-to-normal vision. Exogenous cueing task. The cognitive tasks were run on a PC with a 72-Hz, 15-in. Cathode Ray Tube (CRT) screen. This leads to slightly different presentation durations compared to Experiment 1 and 2 but allows more precise stimulus presentation (Wiens et al., 2004). The attentional task was similar to Experiment 1 except for the presentation durations: Pictorial cues appeared for either 14 ms or 100 ms. The 14-ms cue was masked by a neutral facial expression for 83 ms, ensuring that only the presentation duration of the cues varied but not he SOA. The target was presented 14 ms after cue offset and remained on screen until a response was made. Participants were tested individually. Awareness check. After the attention task, participants performed an awareness check. Participants were presented a detection task instead of the recognition task administered in Experiment 2. The present awareness check examined whether participants were able to detect changes in the stimuli due to the masking procedure. This methodology was based on Maxwell and Davidson (2004) who demonstrated that change detection was the most stringent criterion to determine awareness. The emotional faces were presented in a similar fashion as in the attention task. That is, faces were presented randomly at the left or right in a masked or unmasked fashion location. Participants were presented with the choice to indicate whether they saw a single picture or a backwardly masked picture. Participants were instructed that faces could constitute of a single picture or a backwardly masked picture. They were asked to indicate after each face presentation whether they saw a single or a backwardly masked face. Participants were informed that they might be able to recognize this by small changes (e.g., flickering) and that they could guess if they were unsure. In order to prevent any extreme response biases participants were informed that both presentation conditions would appear equally often. This task consisted of a practice and test phase with equal trial numbers as the attention task. The advantage of presenting masked and unmasked stimuli is that it is possible to calculate hits and false alarms that allow application of SDT.

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Results Exogenous cueing task. Trials with errors were discarded from analyses (M ⫽ 3.4%). After removal of the outliers, statistical analyses were run on 95.0% of the data. Reaction times were subjected to a 2 (presentation condition: masked/unmasked) ⫻ 3 (cue valence: angry, happy, neutral) ⫻ 2 (cue validity: valid, invalid) repeated measures ANOVA. The mean reaction time data are depicted in Table 4. The 2 ⫻ 3 ⫻ 2 ANOVA revealed the basic cue validity effect, F(1, 18) ⫽ 11.69, p ⬍ .01, with faster responding on valid cues (M ⫽ 342) than on invalid cues (M ⫽ 356 ms). Of importance, there was a statistically significant three-way interaction between presentation condition ⫻ cue valence ⫻ cue validity, F(2, 36) ⫽ 5.62, p ⬍ .01. A marginally significant interaction between cue valence and cue validity, F(1.5, 26.7) ⫽ 2.97, p ⫽ .08, could be subsumed under this interaction. All other effects were not significant (presentation ⫻ cue validity, F(1, 18) ⫽ 2.97, p ⫽ .1, all other Fs ⬍ 1.3). In order to interpret the three-way interaction effect, separate ANOVAs for each presentation condition were performed. Masked condition. In this condition, there was only a significant main effect of cue validity, F(1, 18) ⫽ 23.65, p ⬍ .001 with shorter RTs on valid (M ⫽ 340 ms) compared to invalid (M ⫽ 357 ms) trial types. No other effects were significant (Fs ⬍ 1.0), indicating no differential cueing effects at this presentation condition. Unmasked condition. The interaction between cue validity ⫻ cue valence was significant, F(1.4, 25.4) ⫽ 8.27, p ⬍ .01. The main effect of cue valence approached significance, F(1, 18) ⫽ 3.16, p ⫽ .09, with slower responding to trials containing angry cues (M ⫽ 353 ms) compared with happy (M ⫽ 347 ms) and neutral cues (M ⫽ 349). In order to examine this interaction effect, cue validity indices were calculated. The cue validity effects are depicted in Table 4. Paired comparison t tests indicate that the cue validity effect was significantly larger for neutral pictures than for angry pictures, t(19) ⫽ 3.17, p ⬍ .01, and happy pictures, t(19) ⫽ 3.96, p ⬍ .01. The difference between angry and happy faces was not significant (t ⬍ 1.4). Awareness check. The probability of hits and false alarms were converted to A’ and B” scores. Mean A’ ⫽ .59 (SD ⫽ .08), was significantly different from 0.5, t(18) ⫽ 5.03, p ⬍ .001, Table 4 Mean Reaction Times (in ms), Standard Deviations, and Cue Validity Indices (CVI) as a Function of Cue Valence and Cue Validity at Masked and Unmasked Presentation in Experiment 3

Masked (14 ms)

Cue Valence

Cue Validity

Angry



Angry Happy Neutral

M

SD CVI

344 358 339 359 338 354 356 351 346 349 336 362

35 14 38 32 20 36 39 16 39 35 ⫺5 36 42 3 34 44 26 40

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indicating that detection of changes in the masked condition was slightly but significantly above chance. Mean B” ⫽ .09 (SD ⫽ .15) did not differ significantly from zero (t ⬍ 1), indicating a neutral response criterion. Analyses did not reveal differential sensitivity or response bias as a function of cue valence (Fs ⬍1). One individual showed above chance awareness of the masked emotional facial expression (0.83). However, exclusion of this persons’ data did not change the attentional effects.

Discussion In this experiment, we examined whether the absence of attentional cueing by emotional faces under masked conditions was due to near-threshold awareness. A test of awareness, using the stringent criterion of change detection, indicated that individuals still had some awareness of stimulus changes in the masking condition. This effect was unexpected given that previous studies indicate that backwardly masked facial expressions presented for shorter durations than 20 ms cannot be detected (Williams et al., 2004). In our studies, the backwardly masked faces were presented in peripheral vision, which even further impairs detection. Despite that stimulus detection was slightly above chance, no differences were found in detection emotional versus neutral faces. This suggests that the masking procedure was effective in disrupting the processing of stimulus valence. The results of Experiment 3 were similar to the previous findings obtained in Experiment 1–2. Again, we found delayed responding for the emotional stimuli compared with neutral stimuli at 100-ms cue presentation. Moreover, emotional faces did not cue spatial attention more strongly than neutral expressions. In fact, at the 100-ms cue presentation, neutral faces cued attention more strongly than emotional faces.

General Discussion From an evolutionary perspective it has been argued that processing of emotional facial expressions has a special status ¨ hman & Mineka, 2001). There is a wealth of neuropsycholog(O ical data suggesting that emotional facial expressions can be processed preattentively and activates structures involved in the orienting of attention. However, data from empirical research do not support this conclusion unequivocally. This study was aimed to further elucidate whether emotional facial expressions attract visual attention in function of awareness and presentation duration of the faces. There were three main findings: (1) Delayed responding was found on trials with emotional cues in the unmasked condition (Experiments 1–3); (2) In both masked and unmasked conditions, the hypothesized cueing of visual attention to the location of emotional facial expression was not found (Experiments 1–3); (3) Attentional cueing by emotional faces was reduced compared with neutral faces in the unmasked condition (Experiments 1–3). These effects are discussed in turn.

Delayed Responding to Emotional Facial Expressions The most reliable finding in the present series of experiments was that responding to trials containing emotional cues was slower than responding to trials containing neutral cues. This effect was present in Experiment 1–3 in the unmasked, 100-ms

condition. This effect was only found once under masked conditions (Experiment 2). The response interference observed on trials containing emotional cues seems in line with a number of emotion theories and previous studies. In theoretical models on emotion, action tendency is an important element of an emotion and the processing of the emotional information is partly dependent on this action tendency (e.g., Lang, Bradley, & Cuthbert, 1997). For instance, processing fear-relevant information is organized to facilitate rapid appraisal and responding to potential threat in the environment. Therefore, it is not surprising that the presence of an emotional stimulus causes interferes with responding to a target that has no association with the emotional stimulus. In line with our findings, it has been found that unmasked (but not masked) presented emotional faces are associated with elevated autonomic arousal (Williams et al., 2004). Although the interference effect did not occur with very brief (14, 34 ms) masked presentation of the cues (except for Experiment 2), it is clear that 100 ms cue presentation was sufficient to instigate this behavioral effect. In previous studies on attention for emotional expressions, similar effects have been interpreted as indicating that emotional faces capture processing resources (Bindemann, Burton, Hooge, Jenkins, & De Haan, 2005). Thus, results of this study may indicate a dissociable effect of emotional cues on spatial attention versus the allocation of attentional resources in general. That is, emotional facial expressions did not attract attention to their location but the presentation of emotional faces led to delayed responding to the targets. However, it should be noted that the interference effect is not necessarily due to attentional effects but could also be explained by other effects such as response-preparation. For instance, it has been found that threatening stimuli can facilitate or delay responding and, thus, can influence interpretation of attentional tasks relying on reaction time measurement (Flykt, 2006).

Absence of Facilitated Cueing by Emotional Faces A preliminary issue to address is whether the null findings in the masked conditions are due to insufficient power. To ascertain that the absence of enhanced attentional orienting to emotional faces at the masked condition was a genuine effect, we calculated the number of participants necessary to obtain a significant two-way interaction between cue valence and cue validity in the exogenous cueing task. Using GPOWER (Erdfelder, Faul, & Buchner, 1996) we determined the number of participants needed to establish a reliable (power ⬎ .7) cue validity by cue valence interaction effect. All experiments had sufficient participants if the effect size is large (ƒ2 ⫽ .35). Only Experiment 1A had sufficient participants to find significant effects if the effect size is medium (power of ƒ2 ⫽ .74). If the effect size is small (ƒ2 ⫽ .02), over 400 participants would be required to find effects. Thus, our experiments could only detect a medium-large effect. A recent study on attentional cueing by threat signals in a nonselected sample, indicated that emotional cueing might result in large effect sizes (ƒ2 ⫽ .66;


Koster et al., 2004b)5. Thus, it seems safe to conclude that the present experiments indicate that emotional faces do not capture visual attention in a strong way. Another important question is whether the absence of enhanced attentional cueing effects could be explained by specific features of the exogenous cueing task. Although previous studies have found emotional modulation of attentional cueing (Fox et al., 2001, 2002; Koster et al., 2004b; Yiend & Mathews, 2001), specific features of the exogenous cueing task may partially explain the null-findings. The absence of enhanced attentional cueing by emotional faces compared to neutral faces might be related to the sudden onset of the cues. It has been demonstrated that stimuli that are abruptly presented capture attention regardless of their emotional valence (Yantis, 1996). It could be that, especially at very brief presentation durations, the process of attentional engagement to the cue is related to this abrupt onset and not influenced directly by emotional valence. In addition, it may be that facial expressions, even if they are neutral, already provide a highly salient stimulus. A possibility worth considering is that the realistic neutral facial expressions presented for a short duration, captured attention in order to facilitate conscious appraisal of these stimuli as emotional/nonemotional. This could explain why emotional facial expressions failed to elicit enhanced attentional orienting on top of these effects. However, this explanation does not fit with earlier studies using the KDEF pictures, demonstrating facilitated processing of emotional faces (e.g., Schupp et al., 2004).

Reduced Attention for Emotional Faces In Experiment 1–3, we consistently found reduced attention for emotional faces at the 100-ms cue presentation condition. There are a few studies that have previously found reduced attention for emotional information compared with neutral information at brief presentation of stimulus material (Mackintosh & Mathews, 2003). An important question is what drives these effects. One possibility is that with brief cue presentations, the presentation of a salient cue directly followed by a target is associated with impaired target detection because of an attentional blink effect. That is, several recent studies in the context of attentional blink have demonstrated that the presentation of emotional stimuli in a stream of pictures can impair the detection of subsequent targets (Most, Chun, Widders, & Zald, 2005). In these studies, pictures are shown very briefly (⬍100 ms) in a rapid serial visual presentation (RSVP) and the presentation of an emotional stimulus impairs the detection of a target that is presented within about the next 500 ms. This effect may explain the pattern of findings, with the absence of cueing effects for emotional faces in the masked condition and reduced attention for emotional faces in the unmasked condition. Provided that attentional capture by emotional stimuli is thought to underlie the enhanced attentional blink effect, it remains unclear whether the data of Experiment 1–3 can be regarded as a failure to find attentional cueing effects by emotional faces. The occurrence of an emotion-induced blindness effect with impaired detection of the target after presentation of an emotional cue could be a plausible explanation. Although not reported in detail, we conducted another control experiment examining this possibility, using a short and somewhat longer SOA (100 ms and 250 ms) that did not support the attentional blink explanation. The logic of this experiment was that

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presenting picture for the same duration (14 ms and 100 ms), but at a longer SOA allowed more time between cue offset and target appearance, which reduces the potential effects of attentional blink effects. In previous work with the spatial cueing task we have observed that fear-conditioned stimuli presented for 200 ms and SOA ⫽ 214 ms cued visual attention to their location (Koster et al., 2004b, 2005). Presenting the same stimulus material for a longer duration in this control experiment revealed that even under those conditions no significantly stronger cue validity effect emerged for emotional faces. This provides some evidence against that the idea that an attentional blink effect masked an enhanced cue validity effect for emotional faces. However, these data do not exclude the possibility that an attentional blink effect is associated with the reversed cue validity effect for emotional faces. Another explanation for the reduced attention effect could rely on attentional control settings. It has been demonstrated that topdown attentional control can override attentional capture by irrelevant stimuli (Folk, Remington, & Johnston, 1992). Attentional control settings may have been applied in the modified Posner task in an attempt to exclude interference of the emotional cues on target responding. Such a strategy could affect attentional capture in this particular task easily because of the task requirements: Only a single cue is presented that is irrelevant to target detection. Therefore, it would be useful to examine whether the same pattern of responding arises in tasks where threatening stimuli are presented in a less predictable way and interfere more strongly with target responding. How do the findings of the experiments fit in the debate on automatic attention for emotional faces? Combined with the neuropsychological data, the delayed responding on trials with emotional faces suggests that even brief (100 ms) presentation of peripheral emotional faces is sufficient to demand attention and cognitive resources. This means that peripherally presented emotional information can be processed highly efficiently. The absence of attentional effects for the backwardly masked emotional faces may be in line with recent findings that at least some degree of attention is necessary for emotion processing to occur (Pessoa et al., 2002). It could be that peripheral presented faces needs to be processed to a certain degree before enhanced shifts of visual attention for emotional stimuli are found. It may be that differential attentional orienting for emotional versus nonemotional stimuli is only observed at slightly longer durations or with more ecologically valid stimulus displays (multiple stimuli). In fact, there are a number of studies examining attention for emotional faces combining a dot probe task (multiple stimuli) with neuropsychological measures (Armony & Dolan, 2002; Pourtois et al., 2004). These studies indicate that brief presentation of emotional faces capture attention as evidenced by the behavioral data and neuropsychological responding. This work should be extended to backwardly masked emotional facial expressions. A surprising effect in the present studies was the absence of facilitated detection of emotional information in the awareness checks. There is some evidence to suggest that negative emotional expression can be detected more efficiently than neutral expres5

This effect-size was obtained at the acquisition phase for the Cue valence ⫻ Cue validity interaction. This study was selected as it is one of the few studies on attention for emotional information in nonselected samples.

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sions, even when presented peripherically (Calvo & Esteves, 2005). These effects were found with presentation durations of even 25 ms, which is quite similar to the presentation duration of the cues presented under masked conditions in the present experiments. It appears that the masking procedure eliminated the enhanced threat detection. It could be that the presentation of a new (masking) stimulus caused the threat-relevant information in visuospatial working memory to be removed. Clearly, these ideas warrant further study. In conclusion, in three experiments we found that the presentation of brief emotional faces led to an interference effect but did not automatically attract visual attention to their location. These data argue against the claim that emotional facial expressions cue visual attention in an automatic, bottom-up fashion, that is, without awareness of the emotional faces. Instead, attending to emotional faces might be susceptible to top-down attentional influences, such as attentional control settings (see Mathews & Mackintosh, 1998; Pessoa et al., 2002). The findings of the present studies could be of importance in stimulating further research on the conditions for enhanced attentional capture by emotional stimuli.

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Received January 26, 2006 Revision received December 15, 2006 Accepted December 18, 2006 䡲