attentional biases for angry faces: relationships to trait anger and anxiety

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Attentional biasesfor angry faces:Relationships to traitanger and anxietyJack Van Honk a , Adriaan Tuiten a ,Edward de Haan a , Marcel vann deHout b & Henderickus Stam ca University of Utrecht, TheNetherlandsb University of Maastricht, TheNetherlandsc University of Calgary, Alberta, CanadaPublished online: 09 Sep 2010.

To cite this article: Jack Van Honk , Adriaan Tuiten , Edward de Haan ,Marcel vann de Hout & Henderickus Stam (2001) Attentional biases forangry faces: Relationships to trait anger and anxiety, Cognition andEmotion, 15:3, 279-297, DOI: 10.1080/02699930126112

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Attentional biases for angry faces: Relationships totrait anger and anxiety

Jack van Honk, Adriaan Tuiten, and Edward de HaanUniversity of Utrecht, The Netherlands

Marcel van den HoutUniversity of Maastricht, The Netherlands

Henderickus StamUniversity of Calgary, Alberta, Canada

In two experiments selective attention to angry faces was investigated in relation totrait anger and anxiety. A pictorial emotional Stroop task comparing colour-naming latencies for neutral and angry faces was employed. In Experiment 1 usingan unmasked task, individuals scoring high on trait anger showed an attentionalbias for angry faces. In Experiment 2, unmasked and masked versions of the taskwere used. Individuals were selected on low and high trait anxiety, but there wasno indication of a relation between attentional bias scores and anxiety. Whenindividuals were subsequently reallocated to groups on the basis of trait angerscores, the high anger group showed an attentional bias for angry faces in theunmasked and the masked task. Results are discussed in relation to recent neu-robiological findings from our laboratory, as reflecting an evolutionary-evolved,content-specific response to the facial expression of anger.

The assumption that anxiety is associated with selective attention for cuesrelated to threat is now supported by an abundant amount of evidence (for areview, see Williams, Watts, McLeod, & Mathews, 1997). It has been arguedthat this form of biased processing may play an important role in the etiologyand maintenance of emotional disorders. That is, more attention to threateningcues in the environment results in increased perception of danger (Williams,Mathews, & MacLeod, 1996), and a vicious circle is entered in which theseanxiety-produced attentional biases further enhance anxious mood, and so on(OÈ hman, 1997).

COGNITION AND EMOTION, 2001, 15 (3), 279–297

Correspondenc e should be addressed to Jack van Honk at the Department of Psychonomics ,Psychological Laboratory, Utrecht University, Heidelberglaan 2, 3584 CS Utrecht, The Netherlands;e-mail: [email protected]

# 2001 Psychology Press Ltdhttp://www.tandf.co.uk/journals/pp/02699931.html DOI:10.1080/0269993004200222

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Attentional biases for threat have been most frequently demonstrated usingthe modified Stroop colour-naming task: The emotional Stroop task. The task isto name the colour of a word as fast as possible while ignoring the meaning.Mathews and MacLeod (1985) were the first to demonstrate that, relative tonormal controls, anxiety-disordered patients are slower in colour-naming threatcompared to neutral words. This initial demonstration was followed by anincreasing number of experiments demonstrating these attentional biases forthreat in different anxiety disorders. Furthermore, attentional biases were foundin nonclinical high-anxious populations and under subliminal (masked) condi-tions (see Williams et al., 1997). Typically, a slowdown in colour-naming threatcues is observed in high-anxious individuals, whereas low-anxious individualsare often faster on threat cues.

To explain the pattern of findings in emotional Stroop research by addressingunderlying mechanisms, Williams et al. (1996) adapted the Cohen, Dunbar, andMcClelland (1990) parallel distributed processing (PDP) model. In the Williamset al. PDP model, activation of units representing threat is strengthened by a‘‘tag’’ through learning or biological preparedness. Competition is crucial in thenetwork, cues tagged with threat receive priority in processing over nontaggedstimuli. The advantage given to threat-tagged cues automatically increases thechance that a resource allocation mechanism (RAM) is triggered. If RAM istriggered, attentional bias occurs. In high trait anxious individuals, naming thecolour of the cue is slowed down because RAM allocates resources to the threatvalue of the cue. In contrast, in low trait anxious individuals, RAM directsresources away from the threat value of the cue, speeding up its colour naming.

Although evidence for attentional biases for threat is extensive, a limitationis the near exclusive use of word stimuli in emotional Stroop research. Thisposes a problem for evolutionary oriented explanations in terms of actionreadiness in threatening situations (e.g., Mathews & MacLeod, 1994). Thenecessity of rapid detection and attentional allocation to threatening materialseems in that fashion somewhat questionable (McNally, 1995). Moreover, bythe use of threat words a confounding factor might be introduced by the like-lihood that these are more frequently used by high anxious individuals (Brad-ley et al. 1997).

Several cognitive emotion researchers have resorted to the use of ecologi-cally valid stimuli, emotional facial expressions. Experimental paradigmswere chosen in which vigilance is not reflected by deteriorated, but facilitatedperformance (i.e., speeded and probe detection tasks). Byrne and Eysenck(1995) investigated selective attention to angry faces using the ‘‘face in thecrowd’’ task. They found relatively more attention for angry faces in highcompared to low trait anxious individuals. More specifically, low trait anxiousindividuals were slow in detecting angry faces among happy faces, whereasno differences were found in high trait anxious individuals. Bradley et al.

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(1997) used a probe detection task. They found an attentional bias away fromangry faces (compared to neutral faces) in nondysphori c individuals (i.e.,those with low levels of anxiety and depression). When selecting more expli-citly on trait anxiety measures, Bradley, Mogg, Falla, and Hamilton (1998)finally demonstrated a true attentional bias towards angry faces in high traitanxious individuals, and this finding was replicated by the same researchgroup (Mogg & Bradley, 1999a). As can be seen, the pattern of results in thestudies assessing the relation between attentional biases for angry faces andtrait anxiety differs somewhat, likely due to the different populations exam-ined and paradigms used. Nevertheless, overall higher levels of trait anxietyare related to relatively greater attentional biases for angry faces in spatiallyoriented tasks.

Depending on the dominance relation between sender and receiver, angryfaces can, however, be met with anxiety and anger (Dimberg & OÈ hman,1996). When a threat is appraised as being dangerous it leads to anxiety, butwhen appraised as provoking it elicits anger (Beck, 1976). Thereupon, anxietymotivates flight or avoidance of the source of danger, whereas anger moti-vates aggressive removal of the source of provocation (Smith, Hugo, & Kap-pas, 1996). Whether a specific situation is perceived as being dangerous orprovocative requires a personal interpretation. Anger-prone people are morelikely to make the latter interpretation and react with anger. In fact, just asanxiety is now considered a stable temperamental trait, so is anger (i.e., traitanxiety and trait anger; Spielberger, 1988; Spielberger, Jacobs, Russell, &Crane, 1983). Thus, trait anger should also be capable of determining an indi-vidual’s attentional reaction to threat. Recently evidence was found whenEckhardt and Cohen (1997) used a variation of the emotional Stroop task.They showed that previously insulted individuals with high trait anger levelsattended towards provoking (i.e., anger-relevant) threatening words. Theangry face has a potentially provoking and dangerous threat value (Dimberg& Ohman, 1996), thus both anger and anxiety may motivate the attentionalresponse. In sum, selective attention to angry faces should also be expected inanger-prone individuals.

The main aim of our first study was to investigate the relation between traitanger and selective attention to angry faces, using a pictorial emotional Strooptask. Given that trait anger and trait anxiety tend to be positively correlated (seeDiener & Emmons, 1985), we controlled for this relation. The core hypothesiswas that high trait anger is associated with selective attention to angry facialexpressions, and that this selectivity cannot be attributed to the relation betweenselective attention and trait anxiety. Additionally, the fact that both trait anxietyand trait anger were measured in participants, allowed for testing selectiveattention to angry facial expressions in relation to trait anxiety while controllingfor trait anger.

ATTENTIONAL BIASES FOR ANGRY FACES 281

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EXPERIMENT 1

Methods

Participants. The Dutch trait version of the State Trait Anger Scale(STAS; Spielberger et al., 1983), the Dutch trait version of the (STAI) StateTrait Anxiety Inventory (Spielberger, 1988), and the Inadequacy (IN) scale ofthe Dutch Personality Inventory (Luteijn, Starren, & Van Dijk, 1975) wereadministered to 420 students (female-male ratio 320:100) at Utrecht Uni-versity—Pearsons r trait anger and trait anxiety: r(420) = 0.30, p < .001.From this pool, 42 individuals, 21 scoring high (minimum score 20) and 21scoring low (maximum score 15) on the trait version of the STAS (i.e., traitanger) were invited to participate. (Female-male ratio’s for the low and thehigh trait anger groups were 15:6 and 15:6.) Care was taken to excludeindividuals with a possible repressing coping style (i.e. extreme low scores onthe IN scale). Preselection of participants resulted in a low trait anger groupwith a mean score of 11.9 (SD = 1.4) on the trait version trait of the STAS.High trait anger individuals had a mean score of 25.0 (SD = 4.6) on theSTAS. Reallocation of participants to groups on basis of trait anxiety scores(i.e., median split = 37.5) resulted in a low trait anxiety group with a mean of32.2 (SD = 3.0) on the STAI. The high trait anxiety group showed a mean of46.3 (SD = 5.2). Participants had normal or corrected to normal vision andtheir mean age was 22.5 years. They received payment for their participationin the experiment.

Materials. Stimuli were taken from Ekman and Friesen’s (1976) Pictures ofFacial Affect. In the experiment pictures of 10 different faces (5 female and 5male), each displaying a neutral and an angry expression, were used.Duplications of each model were made and coloured by placing a red, green,blue, or yellow transparent folio in front of the picture in the slide-frame. Anextra set of stimuli was prepared for practice trails. The stimuli were back-projected through a milk-coloured glass screen into the experimental room. Thescreen was located at 110 cm from the participant at eye level. The resultingslide image was 20 cm 6 30 cm. Two Kodak Carousels with Compur highspeed shutters and an Electronic Developments projection tachistoscope wereused for presentation. The timing was regulated by Test Point software on aLaser Pentium 133 personal computer. One trial consisted of a slide of a fixationpoint which was shown for 750 ms and followed by the target slide (the colouredneutral or angry face). A microphone connected to a voice level detector wasplaced in front of the participant. Initiation of vocal response was registered bythe computer’s clock and target presentation was subsequently terminated. 40neutral faces and 40 threat faces were presented in random order with therestriction that no more than two presentations of the same colour werepresented consecutively.

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Procedure. The colour-naming task was performed in a specially equippedexperimental room. All apparatus was placed outside the room to minimisesound disturbance. An intercom allowed participant and experimenter tocommunicate. Dimmed light was used throughout the experiment. Participantswere instructed to ignore the content of the image and name the colour asquickly as possible. The main task was preceded by 10 practice trials.

Results

Responses with colour-naming errors (which are rare in emotional Stroop tasks,here 1.1%) were eliminated. Outlier latencies below 300 ms and above 3000 ms(1.8%) were also excluded from analyses. In addition, latencies more than 3standard deviations above each participants’ mean (1.4%) were removed (cf.Bradley, Mogg, Millar, & White, 1995). Attentional-bias scores were computed(i.e., the individual mean response latencies for angry faces minus the individualmean response latencies for neutral faces). Note that positive attentional-biasscores are referred to as interference and negative scores as facilitation . Foranalysis we used an ANCOVA, with Group (high vs. low trait-anger) andGender (female vs. male) as between-subjects factors and attentional-bias scoresas the dependent measure. Trait anxiety was used as the covariate.

A second mixed-design ANCOVA was performed, using Group (low vs. hightrait anxiety), and Gender as between-subjects factors and attentional-bias scoresas the dependent measure. Here, trait anger was used as a covariate to separatethe contribution of anger. There were no significant effects due to Gender (allFs<1.1), this variable was therefore excluded from the final analyses. Finally,for significant effects on ANCOVAs, paired t-tests were assessed to determine ifattentional bias scores in low or high trait groups differed significantly fromzero. An alpha level of .05 two-tailed was used throughout for all statistical tests.

ANGER (preselected groups): Mean colour-naming latencies for neutral andangry faces were, respectively, 649.1 (SD = 91.8) and 652.4 (SD = 91.6). For thelow anger group, the mean colour naming latencies for neutral and angry faceswere, respectively, 628.9 (SD = 94.7) and 623.3 (SD = 98.2), and the meanattentional-bias scores were 75.6 (SD = 18.3). For the high anger group, meanlatencies were 669.3 (SD = 86.2) for neutral faces and 681.5 (SD = 76.0) forangry faces. The mean attentional bias scores were 12.1 (SD = 20.2). Thecovariate (i.e., trait anxiety) was not significant: F(1, 39) = .55. n.s.), but thecrucial effect for Group on attentional-bias scores was significant: F(1, 39) =6.0, p < 0.02. Removing the covariate from the analysis only marginally changedthis effect: F(1, 40) = 5.8, p < 0.025. Paired t-tests on colour-naming latencies ofneutral vs. angry faces indicated nonsignificant facilitation for the low traitanger group: t(21) = 71.1, n.s., but significant interference for the high traitanger group: t(21) = 2.3, p < .035. Thus, the high trait anger subject groupshowed an attentional bias for angry faces (see Figure 1).


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ANXIETY (median split groups): For the low anxiety group, the mean colour-naming latencies for neutral and angry faces were, respectively, 646.5 (SD =101.6) and 648.6 (SD = 100.6), and the mean attentional-bias scores were 2.1(SD = 24.7). For the high anxiety group, latencies were 651.7 (SD = 83.2) forneutral faces and 656.2 (SD = 84.0) for angry faces. The mean attentional-biasscores were 4.5 (SD = 16.5). The covariate (i.e., trait anger) was significant:F(1, 39) = 5.7, p < .025. The effect for Group on attentional-bias score effectwas, however, not significant: F(1, 39) = 0.1, n.s. When removing the covariatethis effect remained unchanged: F(1, 40) = 0.1, n.s. As data show in bothANCOVAs the influence of the covariates was negligible. Figure 1 shows thepattern of results for trait anger and anxiety groups.

Discussion

The first experiment confirmed our main hypothesis by revealing a significantrelation between trait anger and selective attention to angry faces. This effectprimarily depended on high trait anger participants slowing down significantlywhen colour naming angry faces. Interestingly, no significant effects were foundin relation to trait anxiety. Individuals were, however, preselected on low andhigh trait anger scores. In the spatially oriented (dot probe and speeded detec-tion) tasks, attentional biases for angry faces have been shown to be related toindividuals’ trait anxiety levels when preselection was based on anxiety levels.To investigate if anxiety-related attentional biases for angry faces might also beevidenced in the ‘‘focused’’ emotional Stroop task, we preselected participants

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Figure 1. Experiment 1: Mean attentional bias scores and SEM in preselected trait anger groupsand reallocated (median-split) trait anxiety groups (N = 42).

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on trait anxiety levels in the second experiment. Furthermore, for Experiment 2we constructed a subliminal (masked) condition, to investigate preconsciousattentional biases for angry faces.

In several classical conditioning experiments by OÈ hman and co-workers (seeDimberg & OÈ hman, 1996), superior conditioning for masked angry faces(compared to masked happy faces) was demonstrated. OÈ hman (1997) argues thatthis difference is due to angry faces possessing biologically prepared threateningfeatures, which are easily associated with fear. Automatic sympathetic activationby these features is held to be initiated without cortical processing through aneurobiological short-cut, the thalamic-amygdala pathway (see Ledoux, 1996).Crucial features of the angry facial expression are processed in parallel bysubcortical feature detectors, resulting in speeded activation of the arousalsystem. Under masked conditions, more complex perceptual analysis andappraisal is precluded, because this requires the slower neocortical loop.According to OÈ hman, masked exposure conditions may reveal underlying ten-dencies uncontaminated by conscious control, experimenter expectations, ordemand characteristics.

Although it seems unlikely for words to travel the subcortical route,1 astriking observation sometimes made in nonclinical high anxious individualswith the emotional Stroop task is the occurrence of attentional biases forthreatening words in the masked but not in the unmasked task (MacLeod &Hagen, 1992; MacLeod & Rutherford, 1992; Mogg, Kentish, & Bradley, 1993).A consciously mediated mood-controlling strategy in the unmasked task issuggested as responsible for the dissociation (see Williams et al., 1996, 1997).Interestingly, this dissociation between masked and unmasked task performancehas not yet been shown in clinically anxious individuals. The inability to controlStroop interference for unmasked threatening words may therefore indicatepsychopathology (Williams et al., 1996, 1997; but see Amir et al., 1996).

The main hypothesis tested in Experiment 2 was that high trait anxiety isassociated with selective attention to masked and unmasked angry facialexpressions and this selectivity cannot be attributed to a relation with traitanger. Experiment 2 also allows for an evaluation of the previously men-tioned consciously mediated mood-controlling strategies in relation to emo-tional faces. Furthermore, in the same manner as was done in Experiment 1with trait anxiety scores, trait anger scores were used for testing selectiveattention to masked and unmasked angry faces in relation to anger while con-trolling for trait anxiety.

1 It might be argued that, when highly learned, threatening words become or come to possessthreatening features, which gain access to the subcortical short-cut. However, OÈ hman (1993) arguesfor other, likely neocortical evaluation mechanisms, implicated in the unconscious processing ofthreatening words.


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EXPERIMENT 2

Methods

Participants. The Dutch trait version of the (STAS; Spielberger et al.,1983), the Dutch trait version of the (STAI; Spielberger, 1988), and the IN scaleof the (DPI; Luteijn et al., 1975) were administered to 350 students (female-maleratio 110 : 240) at Utrecht University—Pearsons r trait anxiety and trait anger:r(350) = 0.29, p < .001. From this pool, 42 participants, 21 scoring high(minimum score 40) and 21 scoring low (maximum score 30), on the traitversion of the STAI (i.e., trait anxiety) were invited to participate. (Female-maleratio for the low and the high trait anxiety groups were 6:15 and 6:15.) Possiblerepressors were again excluded (see Methods in Experiment 1). Low traitanxiety participants had a mean score of 25.0 (SD = 2.7) on the trait version ofthe STAI. High trait anxiety participants had a mean score of 47.7 (SD = 4.5) onthe STAI. Reallocation of participants to groups on the basis of a median split ontrait anger scores (median = 15.5) resulted in a low trait anger participant groupwith a mean score of 12.7 (SD = 1.3) on the STAS. The high trait anger grouphad a mean score of 18.3 (SD = 1.9) on the STAS. Participants had normal orcorrected to normal vision and their mean age was 22.8 years. They receivedpayment for participation.

Materials. The same materials were used as in Experiment 1, except for theinclusion of the masks. Furthermore, the supplemented subliminal version of theStroop task required a third Kodak carousel to display the mask. To constructslides of masking stimuli we cut, randomly reassembled, and rephotographedpictures of faces (see OÈ hman & Soares, 1993). The colours of the masks werecongruent with the colours of their targets, through placement of the sametransparent red, blue, green, and yellow folios in front of the picture in both slideframes. Initiation of vocal response was registered by the computer’s clock andtarget (or mask) presentation was subsequently terminated. Masked andunmasked tasks were presented blocked and these blocks were counterbalancedin both low and high trait anxiety participants.

Threshold-control. Through extensive piloting in our laboratory weestablished an objective threshold for the recognition of emotional expressionsfor our displays. These pilots indicated that a 30 ms masking interval effectivelyprecluded recognition of the emotional valence of targets in every participant.Note that perceptual thresholds are task-dependent (Van Selst & Merikle, 1993),and an emotional-neutral recognition procedure reflects the emotional Strooptask (Wells & Mathews, 1994). Nevertheless, in the present experiment, theeffect of the masking procedure was individually determined after the Strooptasks. A two alternative forced-choice (2AFC) emotional-neutral recognitionprocedure was used. In our 2AFC procedure, a random set of 30 masked faces

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was shown to the participants. In advance, they were explicitly told that 15neutral and 15 angry faces were in the set, and instructed to indicate (when indoubt by guessing), by pushing a button, whether the presented slide was aneutral or an emotional expression (see Kemp-Wheeler & Hill, 1988, for therationale behind this instruction).

Procedure. The procedures were identical to those in Experiment 1 with theexception of the presentation of the masked stimuli. The tasks, using 80 stimulimasked and 80 stimuli unmasked were presented blocked and counterbalancedacross participants. Stimuli were presented in a random order, with therestriction that no more than two presentations of the same colour werepresented consecutively. Both tasks were preceded by 10 practice trials, andthere was a 5 minute rest period between the two tasks.

Results

Responses with colour-naming errors (in both tasks < 1.2%) were eliminated.Outlier latencies below 300 ms and above 3000 ms (unmasked 1.4%; masked1.6%) were also excluded from analyses. In addition, latencies more than 3standard deviations above each participants’ mean (unmasked 1.2%; masked1.5%) were removed.

2AFC checks: Forced-choice checks indicated that masked presentationprecluded recognition of emotional valence of targets. Only 50.2% of overallresponses were correct (chance performance = 50%). The cut-off score was 19correct responses. None of the participants scored above this limit. Nonpara-metric tests for deviation from the expected value (cut-off point = 15), showedthat the deviation was not significant (binomial, two-tailed, p = .64).

Table 1 shows the mean colour-naming latencies for unmasked and maskedneutral and angry faces, together with the mean attentional bias for the pre-selected anxiety groups and the median-split anger groups.

TABLE 1Experiment 2: Means (and standard deviations) of colour-naming latencies (ms)

Low trait anxiety High trait anxiety Low trait anger High trait anger

Neutral faces 651.7 (93.3) 681.7 (118.8) 658.1 (101.7) 675.3 (113.1)Angry faces 656.8 (94.8) 688.1 (124.0) 658.3 (104.7) 686.6 (116.2)Attentional bias 5.1 (17.8) 6.6 (16.6) .2 (13.1) 11.3 (18.7)

Masked neutral faces 669.1 (111.8) 692.1 (114.2) 669.4 (104.0) 691.8 (119.5)Masked angry faces 674.2 (109.3) 695.5 (114.8) 667.4 (202.1) 702.3 (120.5)Attentional bias 5.2 (15.6) 3.4 (17.1) 72.0 (16.2) 10.5 (13.8)


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MANCOVA (between preselected anxiety groups): A MANCOVA was con-ducted, with Group (high vs. low trait anxiety), Gender (female vs. male), andTask order (masked-unmasked vs. unmasked-masked) as between-subjectsfactors. Masked and unmasked attentional-bias scores were used as dependentmeasures, and trait anger was used as covariate. There were no significanteffects involving Gender (all Fs < 1.2), and Task order (all Fs<1), these vari-ables were therefore excluded from analyses. The final results showed that thecovariate (i.e., trait anger) was significant in this analysis: F(1, 39) = 8.7,p < .002. There was a multivariate effect for Group on unmasked and maskedattentional bias: F(1, 39) = 0.6, n.s. This null finding did not depend on anger-anxiety relations. Although the effect of Anger (covariate) on attentional biasscores was highly significant: F(1, 39) = 18.4, p < .001, removing the covariatedid not change the pattern of results: F(1, 40) = 0.9, n.s.

MANCOVA (between median-split anger groups): A second MANCOVAwas conducted, with Group (high vs. low trait anger), Gender (female vs. male),and Task order (masked-unmasked vs. unmasked-masked) as between-subjectsfactors. Masked and unmasked attentional-bias scores were used as dependentmeasures, and trait anxiety as covariate. Again there were no significant effectsinvolving Gender (all Fs < 1.4), and Task order (all Fs<1), these variables weretherefore excluded from the final analyses.

The covariate (trait anxiety) was not significant: F(1, 39) = 0.6, n.s. Themultivariate effect for Group on unmasked and masked attentional-bias scoreswas significant, F(1, 39) = 7.4, p < .003. Removal of the covariate changed thiseffect only marginally: F(1, 40) = 6.9, p <.004. Univariate tests (without thecovariate) showed that for both unmasked and masked data, the effect for Groupon attentional-bias scores was significant: F(1, 40) = 4.9, p <.035, and F(1, 40) =7.3, p <.015, respectively.

For unmasked data, paired t-tests over neutral versus angry faces revealednonsignificant interference for the low trait anger group: t(20) = 0.1, n.s.Interference in the high trait anger group reached significance: t(20) = 2.7, p =.015; the high trait anger group showed an attentional bias for angry faces.Figure 2 shows the pattern of results for the anxiety and the anger groups. Formasked data these paired t-tests indicated nonsignificant facilitation for the lowtrait anger group: t(20) = 70.5, n.s. Interference in the high trait anger groupwas highly significant: t(20) = 3.5, p < .005; the high anger group showed anattentional bias for masked angry faces.

GENERAL DISCUSSION

The results of the present experiments indicate that selective attention to angryfaces—as measured by an emotional Stroop task—is related to trait anger andnot to trait anxiety. The primary hypothesis for Experiment 2 was not supported,even when participants were preselected on trait anxiety significant results were

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exclusively related to trait anger. Furthermore, these anger-related attentionalbiases for angry faces were present even on a preconscious level. How do thesedata relate to current models of attentional bias for threat?

To explain inreconcilable experimental findings, Mathews and Mackintosh(1998) recently revised the Williams et al. (1996) model. A serious problem forthe Williams et al. model was the demonstration of attentional biases for highlyaversive stimuli irrelevant of anxiety level. Individual differences seem tobecome apparent only when one uses mild threat cues, such as words and faces.In the newly developed cognitive model, the critical role of competition inattentional bias is more strongly emphasised. When competing representationsdrawing on common resources are involved, the inhibition of threat (which isrequired for efficient responding to the designated target) is argued to be defi-cient in anxious populations. Additionally, for severe threat cues it is suggestedthat activation levels which make the execution of competing processes possibleare exceeded. Moreover, Mathews and Mackintosh (1998) join with OÈ hman(1993) in seeking compatibility with Ledoux’s (1996) neural model of fear in therat, wherein the amygdala plays a crucial role by integrating sources of threa-tening information from cortical and subcortical routes. Both routes are stillsuggested to be functional in humans, resulting in automatic subcortical threatappraisal or analyses of crude stimulus features that become integrated withcortically processed and more detailed contextual and memory information.With respect to the present experiments, the Mathews and Mackintosh model is

Masked Unmasked

Figure 2. Experiment 2: Mean attentional bias scores and SEM in preselected trait anxiety groupsand reallocated (median-split) trait anger groups for masked and unmasked data (N = 42).


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exclusively concerned with attentional bias due to activation of the amygdala interms of implicating a fear- or anxiety-driven response. When coupled withpunishment, angry faces may indeed become easily associated with fear(OÈ hman, 1997). However, when not aversively conditioned, amygdala-drivenattentional and physiological responses to angry faces need not indicate, nor tobe amplified by fear or anxiety. Converging evidence from lesion and stimu-lation studies in primates and humans provides stronger evidence for theamygdala being implicated in aggressive acts in social and socially threateningcontexts (for reviews, see Aggleton, 1992; Kling & Brothers, 1992). Amygda-lectomy, in fact, primarily reduces social aggression and induces loss of socialrank. However, concerning our results, for what adaptive reason should angerproneness and no anxiety proneness motivate a vigilant response to the facialdisplay of anger?

The adaptive functions of anger are related to self-defence, dominance, andthe regulation of social and interpersonal behaviours (Lemerise & Dodge, 1993).During social conflict, anger is associated with heightened approach and low-ered withdrawal tendencies (Harmon-Jones & Allen, 1998), and makes offensiveforms of aggression to others more likely (Lemerise & Dodge, 1993). Althoughaggression is the means by which lower animals, like rodents, tend to dominate,in higher primates, such as humans, competition is mostly restricted to thesymbolic level wherein the facial display of anger plays a pivotal role. Athreatening gaze, while keeping direct eye contact reflects dominance, whereasaverting the eyes or gaze from threatening individuals symbolises submissionand prevents aggression (Mazur & Booth, 1998). Social relations are establishedand maintained by submissive gestures towards the dominant individual dis-playing anger (OÈ hman, 1986). Anger proneness is arguably associated withdominance in social systems, and thus with dominance display in sociallythreatening encounters. Hence, allocation of attention towards the angry facemay be most prominent for those who are anger prone.

Notably, in humans, interpersonal dominance and (the anger disorder) anti-social behaviour are related to high basal levels of the gonadal hormone tes-tosterone (Mazur & Booth, 1998). In agreement with our explanation, werecently demonstrated that, when compared to individuals with low testosteronelevels, individuals with high testosterone levels scored higher on the anger scaleof the Profile of Mood States and attended more towards angry faces in anemotional Stroop task (Van Honk et al., 1999). Moreover, when we adminis-tered testosterone in a double-blind placebo controlled design, the relationbetween testosterone and a vigilant physiological response to the angry faceproved to be causal (Van Honk et al., in press).

Anxiety proneness, but especially social anxiety, is associated with thesubmissive pole in the social system (OÈ hman, 1986; Sapolsky, 1990). Note thatthe largely symbolic nature of primate dominance interactions decreases thechance of being injured or killed during these encounters. In established primate

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groups there is a constant display of anger to consolidate positions but overtaggression seldomly occurs. Flight thus has low adaptive value, threats andhumiliations must be endured, because advantages are gained from living inclose social groups (OÈ hman, 1996). Ethological evidence shows that submissive,socially anxious primates have high basal levels of the stress hormone cortisol,and display avoiding reflexes (i.e., gaze aversion) towards threatening con-specifics to forestall attack (OÈ hman, 1986; Sapolsky, 1990). In agreement, wefound attentional biases away from masked angry faces in individuals with highbasal cortisol levels (Van Honk et al., 1998). This finding was designated as apreconsciously initiated, submissive, avoidant reflex. Additionally, in con-sidering Experiment 2 in the present study it revealed that our preselectionshould perhaps have been based on social anxiety levels, with the hypothesisedpattern of attentional bias reversed.

Interestingly, in an unpublished dot-probe study by Yuen (1994) such anattentional bias away from angry faces was shown in socially anxious indivi-duals. This finding was recently replicated by Mansell, Clark, Ehlers, and Chen(1999). However, in the Mansell et al. dot-probe study the effect was restrictedto a condition of social evaluative threat, wherein socially anxious individualsalso showed an attentional bias away from happy faces. In the nonthreat con-dition Mansell et al. replicated Bradley et al. (1998) and Mogg and Bradley(1999a) by showing an attentional bias towards angry faces in high trait anxiousindividuals.

By employing masked and unmasked neutral, happy, and angry faces in apictorial emotional Stroop task, we recently showed that individuals with higherlevels of social anxiety selectively attend away from angry faces only, in themasked task exclusively (Van Honk, Putman, Hermans, & Tuiten, 2000). Thiseffect is in concordance with our findings on basal cortisol levels, and furthersupports the above noted explanation in terms of submission motives. Further-more, in the Van Honk et al. (2000) study, we replicated the present subliminalfindings. Individuals scoring high on trait anger showed attentional biasestowards masked angry faces. Thus in the latter study, as in the Van Honk et al.(1998) study, findings were restricted to the masked task. This lends additionalsupport to the suggestion that the effects in unmasked tasks may be countered bystrategic task-related efforts (Williams et al., 1996; Mathews & Mackintosh,1998) or confounded by ‘‘the whims of consciousness’’ (OÈ hman, 1997).

Admittedly, the evolutionary explanation of the present results is somewhatweakened by the Eckhard and Cohen (1997) findings, described in the intro-duction. Relationships between trait anger and selective attention to both anger-provoking words and angry facial expression leave open an explanation in termsof a processing bias for concern-related information (see Williams et al., 1996).However, there is no evidence that socially anxious individuals attend awayfrom threatening words in the emotional Stroop task. They attend towardsthreatening words in a nonthreat condition (Hope, Rapee, Heimberg, & Dom-


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beck, 1990; Mattia, Heimberg, & Hope, 1993), and this effect seems to dis-appear under social-evaluative threat (Amir et al., 1996).

A further provocative finding in the Van Honk et al. (2000) study was on self-report measures of the behavioural activation system (BAS) and the behaviouralinhibition system (BIS) (Carver & White, 1994). It is commonly suggested that ahighly reactive BIS implicates anxiety proneness and produces hypervigilance toenvironmental threat (e.g., Mathews & Mackingtosh, 1998; Mogg & Bradley,1998). Our research, however, indicated that high BAS/low BIS was mostpredictive of the vigilant attentional response towards the masked angry face(Van Honk et al., 2000). At an extreme, high BAS/low BIS stands for thepsychopathic, antisocial personality who tends to react with inappropriate anger(Cole & Zahn-Waxler, 1992), and is constantly seeking rewards while beinginsensitive to punishment (Gray, 1994). In these individuals lack of anxiety (lowBIS) amplifies the potency for socially destructive behaviour (high BAS)(Carver & White, 1994; Keltner, Moffitt, & Stouthamer-Loeber, 1995). Withrespect to our BIS-BAS findings, the amplification of vigilance through thereduction of anxiety does not match recent cognitive theoretical accounts ofselective attention to threat (see Mathews & Mackingtosh, 1998; and Mogg &Bradley, 1998).

Carver and White’s BIS/BAS scales have recently been linked to prefrontalbrain asymmetry, as measured by electroencephalography (EEG). The BIS scalepredicts greater relative right prefrontal activation, whereas the BAS scalepredicts greater relative left prefrontal activation (Sutton & Davidson, 1997;Harmon-Jones & Allen, 1997). In concordance, fearful behaviour and theexpression of the emotion fear are associated with relatively more right pre-frontal activity (Coan, Allen, & Harmon-Jones, 1999; Kalin, Larson, Shelton, &Davidson, 1998), whereas for anger proneness and the expression of angerevidence shows relatively more left prefrontal activity (Coan et al., 1999;Harmon-Jones & Allen, 1998). It may therefore be suggested that the left pre-frontal cortex is involved in the vigilant response to the angry face.

In striking contrast to the latter suggestion, Mogg and Bradley (1999b) used amasked dot-probe task and demonstrated that allocation of attention towards theangry face was most strong in the left visual field, suggestive of right hemi-sphere involvement. However, the reversed pattern was found when using lowfrequency repetitive transcranial magnetic stimulation (rTMS) of the left and theright prefrontal cortex (PFC) in a within-subjects emotional Stroop design(d’Alfonso, Van Honk, Hermans, Postma, & De Haan, 2000). rTMS is a tech-nique capable of disrupting local processing in neural networks in the brain.When applied to a specific area of the cortex, low frequency rTMS produces aperiod of cortical inactivity, a temporary ‘‘virtual brain lesion’’ (see Pascual-Leone, Bartres-Faz, & Keenan, 1999). Thus, right PFC rTMS results in the leftPFC being (temporarily) relatively more active and vice versa. d’Alfonso et al.hypothesised that right compared to left prefrontal inactivation would result in a

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significant increase in selective attention towards angry faces. Results showedthe expected significant effect of stimulation position, which was due to indi-viduals showing positive attentional bias scores (vigilance) when the right PFCwas inactivated and negative attentional bias scores (avoidance) when the leftPFC was inactivated. Thus, attentional biases towards angry faces as measuredby an emotional Stroop task may causally depend on the left prefrontal cortexbeing relatively more active.

As a prudent explanation for these different findings on hemispheric lateri-alisation and personality traits it might be suggested that the dot-probe task (atleast in Bradley and Mogg’s case) demonstrates general negative valenceeffects, while the pictorial emotional Stroop task shows content-specificresponses to the angry face. Evidence shows that not only the attentionalresponse towards the angry face (d’Alfonso et al., 2000), but also the recognition(Suburi & McKeever, 1977), and as mentioned the experience and expression ofanger (Harmon-Jones & Allen, 1998; Coan et al., 1999) are associated with theleft hemispheric approach system (Davidson, 1998). It seems that right hemi-spheric contribution only becomes evident in the case of aversive conditioning(e.g., Johnson & Hughdahl, 1993). However, during aversive conditioning theangry face becomes associated with punishment, and the right hemisphere—which is, with the exclusion of an anger-related affect, more generally involvedin negative affect—is implicated in withdrawal and sensitivity to punishment(Davidson, 1998). High trait anxious individuals are extremely sensitive tosignals of punishment, and generally preoccupied with threats in their envir-onment (Mathews & Mackintosh, 1998; Williams et al., 1996). Hence, a generalnegative affect explanation for the Bradley and Mogg findings concurs withtheir demonstrations of right hemispheric lateralisation, and with their repeateddemonstrations of attentional bias for angry faces in high trait anxious indivi-duals.2

In conclusion, the present study demonstrates that attentional biases formasked and unmasked angry faces—as measured by an emotional Stroop task—are related to trait anger and not to trait anxiety. To our knowledge this is thefirst study to report evidence of a relation between trait anger and preconsciousprocessing of threat. Given a recent replication (Van Honk et al., 2000) thisfinding seems reliable. In addition, we have shown that individuals withendocrine and self-reported indications of social anxiety show avoidant atten-tional responses to masked angry faces (Van Honk et al., 1998, 2000). Vigilant

2 Bradley et al. (1998) found an attentional bias away from happy faces in high trait anxiousindividuals, but as partial correlations showed this effect was due to increased depression in thisgroup. In a clinically anxious group, Bradley et al. (1999) found an attentional bias towards happyfaces, which was strongest by the end of the experiment. They suggested that anxious individualsappraised the happy face as threatening, fearing its invitation to social engagement . This suggestionconcurs with our argument for a negative valence effect. We thank an anonymous referee of anearlier version of this paper for inspiring this explanation in terms of negative valence.


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attentional and physiological responses to angry faces were evidently mediatedby testosterone (Van Honk et al., 1999, in press), a hormone which has beenassociated with anger, aggression, and dominance behaviour in humans (Mazur& Booth, 1998). It is argued that dominance and submission motives can explainthese observed vigilant and avoidant responses to angry faces.

Manuscript received 22 March 1999Revised manuscript received 6 October 2000

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attentional biases for angry faces: relationships to trait anger and anxiety

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