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Cognitive Therapy and Research, Vol. 27, No. 5, October 2003 ( C© 2003), pp. 489–504

Threat-Evoked Anxiety Disrupts Spatial WorkingMemory Performance: An Attentional Account

Aureliu Lavric,1,4 Gina Rippon,2 and Jeremy R. Gray3

It is proposed that threat-evoked anxiety and spatial Working Memory (WM) relyon a common visuospatial attention mechanism. A prediction of this hypothesis isthat spatial but not verbal WM should be disrupted in conditions of threat anxiety.Participants performed verbal and spatial n-back WM tasks in the presence or absenceof threat of shock (shocks were not delivered). The presence of anxiety was assessedvia heart rate recordings and self-report. Both measures clearly distinguished betweenWM blocks associated with threat of shock (Threat) and blocks, in which threat wasabsent (Safety). Performance on the spatial WM task was impaired in Threat relativeto Safety. Furthermore, the more anxiety participants reported and the higher theirheart rate in Threat compared to Safety, the more impaired was their spatial WMperformance. This effect was not observed for verbal WM. The results indicate selectivedisruption of spatial WM performance by threat-evoked anxiety, interpreted in terms ofmore overlap in visuospatial attention between anxiety and spatial WM vs. anxiety andverbal WM.

KEY WORDS: threat; anxiety; verbal and spatial working memory; visuospatial attention.

The modulation of cognition by affect is of considerable interest, both clinicallyand theoretically. Although some models of the effects of emotion on cognitive pro-cessing have been cast at a global level, for example, in terms of depletion of cognitiveresources (Ellis & Ashbrook, 1987), more specific accounts have also been advanced.Eysenck and colleagues (Eysenck, 1979, 1982; Eysenck & Calvo, 1992) suggested thateffects of anxiety on performance may be mediated by effects on Working Memory(WM), and reviewed considerable evidence supporting this hypothesis. The origi-nal model of WM (Baddeley & Hitch, 1974) distinguished between the visuospatial,

1School of Psychology, University of Exeter, Exeter, United Kingdom.2Neurosciences Research Institute, Aston University, Birmingham, United Kingdom.3Department of Psychology, Washington University, Saint Louis, Missouri.4Correspondence should be directed to Aureliu Lavric, School of Psychology, Washington SingerLaboratories, University of Exeter, Perry Road, Exeter EX4 4QC, United Kingdom; e-mail:a.lavric@exeter.ac.uk.

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phonological, and Central Executive components. Eysenck and Calvo’s processingefficiency theory (Eysenck & Calvo, 1992) proposed that anxiety impacts primar-ily on the Central Executive, which, in conjunction with the modality-independentcharacter of the latter, would suggest similar levels of disruption of verbal and spatialWM in conditions of anxiety. However, in addition to the general effect of anxietyon the Central Executive, verbal ruminations (i.e., worry) were claimed to depletethe phonological component of WM (Eysenck & Calvo, 1992), thus explaining thedifficulties that highly anxious individuals encounter in verbal tasks (Derakshan &Eysenck, 1998). Furthermore, there is some evidence of more marked disruption ofverbal WM, as compared to spatial WM, in conditions of anxiety (Ikeda, Iwanaga,& Seiwa, 1996; Markham & Darke, 1991).

While the above-mentioned account relies mainly on studies of trait anxiety,a growing corpus of evidence obtained from healthy participants (Bartolic, Basso,Schefft, Glauser, & Titanic-Schefft, 1999; Gray, 2001; Gray, Braver, & Raichle, 2002;Lavric, Shackman, Sarinopoulos, Pederson, & Davidson, 2000) is also consistent withthe possibility that the effects of negative mood on verbal–phonological WM may notbe the same as on visuospatial WM. In particular, one of these studies (Lavric et al.,2000) examined the effects of threat-of-shock anxiety on verbal and spatial WM. Itemployed psychometrically matched verbal and spatial n-back WM tasks and foundthat induced anxiety impaired spatial, but not verbal, n-back performance. However,some methodological limitations have to be acknowledged. In a paradigm employingthreat-of-shock followed by shock delivery (Lavric et al., 2000) it may be difficult toisolate the effects of anxiety from those of shock per se upon cognitive processing. Onthe other hand, certain affect evocation procedures employed in other studies, suchas Velten statements (Bartolic et al., 1999) or affectively laden film clips (Gray, 2001),involve complex cognitive processes whose impact on subsequent WM performanceis difficult to control (Buchwald, Stark, & Coyne, 1981; Philippot, 1993). In addi-tion, many of the investigations mentioned above relied exclusively on self-reportmeasures for verifying the emotion induction, which leaves unanswered questionsconcerning the extent to which emotional states were in fact experienced during thecognitive tasks (Scherer, 1993). Finally, few studies employing affect induction haveunequivocally demonstrated the relationship between the strength of induced affectand the change in WM performance.

Beyond such methodological considerations, we sought to test a novel, specifichypothesis of why a selective effect of anxiety on spatial WM performance shouldbe found. Our account is on the basis of the possibility of a systematic associationbetween certain types of affect and specific cognitive mechanisms. For example,positive mood may stimulate exploratory behavior, which could explain its facili-tatory effects on creative tasks (Ashby, Isen, & Turken, 1999; Isen, Daubman, &Nowicki, 1987), but disruptive effects on analytical tasks, for example, reasoningtasks (Oaksford, Morris, Grainger, & Williams, 1996). Similarly, increased attentionto threatening stimuli in anxious individuals, that is, attention to threat (Mathews,Mackintoch, & Fulcher, 1997; Williams, Watts, MacLeod, & Mathews, 1988), mostlikely represents an exacerbation of the normal increase in visuospatial attentionin the presence of an exogenous threat. Attention may well represent the point of

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overlap between anxiety and spatial WM, because there appear to be visuospatialattentional demands during spatial WM that are not present during verbal WM. Inparticular, in verbal WM tasks letters are presented on the screen in either upperor lower case, which encourages one not to rely on their visual representation, butto recode the stimulus and store the phonological code. In contrast, spatial trialsimpose no constraints for intermediary recoding of the visuospatial information onthe screen. Therefore, in spatial, but not verbal, WM tasks the (visual) informationon the screen can be manipulated and retained directly, which would increase thedemands on visuospatial attention. Moreover, WM tasks that require continuous ma-nipulation of the information in WM, for example, n-back tasks (Smith & Jonides,1999), may be particularly demanding with regard to such attentional resources.Evidence from electrophysiological studies supports this proposal. Gevins et al.,(1996) monitored brain activity during verbal and spatial n-back tasks using Event-Related Potentials (ERPs). Spatial trials showed a larger ERP deflection around200 ms poststimulus onset (P200), interpreted by the authors in terms of attentionalprocesses.

Further insight into how visuospatial attention contributes to spatial WM is pro-vided by the proposal that the active maintenance of spatial information is mediatedby covert shifts of attention from one item to the next (Awh, Jonides, & Reuter-Lorenz, 1998; Smyth & Pelky, 1992; Smyth & Scholey, 1994). For instance, Awh,Jonides and Reuter-Lorenz (1998) reasoned that if rehearsal in spatial WM is basedon attentional shifts, then stimuli presented during the delay would be processedmore efficiently if they appear in the same locations as the spatial WM locationsbeing rehearsed. Participants performed a spatial WM task, in which a letter (thecue) appeared in a specific location on the computer screen. In one condition partic-ipants had to memorize the location of the letter, in another condition—its identity.After a delay, a probe letter was presented on the screen and participants had todecide whether it was the same location/letter as the cue. During the delay, falsefonts were presented either in the same location as the cue or not, and participantsmade speeded keypresses to indicate their shape. As predicted by the authors, false-fonts presented in the same locations as the cue location were processed faster whenparticipants had to memorize the location of the cue and there was no facilitationwhen the cue’s identity (letter) had to be memorized.

Applied to neuroimaging, the same logic predicts that visual areas of the braincorresponding to the regions of the visual field, in which the rehearsed locations werepreviously presented, should be more active than other visual areas, even if the entirevisual field is equally stimulated during the delay. This prediction was also confirmedin a recent neuroimaging (fMRI) study (Awh et al., 1999).

On the basis of previous results from affect-manipulation designs (Lavric et al.,2000), as well as on evidence of increases in visuospatial attention in response tothreatening stimuli (Mathews et al., 1997; Mogg & Bradley, 1998; Williams, Watts,MacLeod, & Mathews, 1988), we currently hypothesized that attentional process-ing in threat-evoked anxiety might limit visuospatial attentional resources during ademanding WM task. If so, it should impair spatial but not verbal WM rehearsal,because the former and not the latter relies on shifts of visuospatial attention.

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METHOD

General Considerations

We sought to test our hypothesis by employing a methodologically improvedparadigm, relative to our earlier studies (Gray, 2001; Lavric et al., 2000). Similarlyto these studies, the paradigm uses verbal and spatial n-back WM tasks that con-tain identical stimuli and are matched for difficulty. Threat of shock (Chua, Krams,Toni, Passingham, & Dolan, 1999; Grillon, Ameli, Woods, Merikangas, & Davis,1991; Lavric et al., 2000; Reiman, Fusselman, Fox, & Raichle, 1989) is employedfor anxiety evocation. This procedure requires no explicit cooperation from partici-pants, limits the amount of cognitive processing to the basic attention to threat, min-imizes individual differences in learning history, and allows for concurrent cognitivetask performance and affect induction and assessment. Furthermore, neuroimagingstudies have provided evidence regarding the neuroanatomical correlates of anxietyevoked by threat-of-shock (Chua et al., 1999). Importantly, threat-of-shock does notimply the delivery of shocks. Because electric shocks can be a powerful confoundingvariable, the current design is limited to threat-of-shock and does not at any pointcontain shock delivery. To obtain an on-line physiological measure of affective state,we employed heart rate recordings. The presence of threat has unequivocally beenassociated with increased sympathetic activity, resulting in increased heart rate (Ax,1953; Palomba, Sarlo, Angrilli, Mini, & Stegagno, 2000). Furthermore, it was decidedto directly test the relationship between the strength of evoked anxiety (as measuredby heart rate and self-report) and changes in WM performance using appropriateanalytical techniques. It has been recently shown (Gray, 2001) that differences in par-ticipants’ responsiveness to emotion induction can provide additional insight whenlinked to WM performance.

Participants

Thirty-nine right-handed students with no history of neurological or psychiatricdisorder were paid 10 pounds sterling for participating in the study after providinginformed written consent. Two participants withdrew from the session after practice.Data from one participant were discarded because of near-chance accuracy (chance–50%), leaving 36 participants (18 females and 18 males, mean age = 20; SD = 1.76,range = 18–25).

n-Back WM Tasks

The present verbal and spatial n-back WM tasks have identical stimuli, and aredistinguished only by their instructions. As illustrated in Fig. 1, stimuli are presentedin blocks of trials. Each trial consists of the 500-ms presentation of a square boxwith several instances of the same letter inside, in upper- or lowercase font. The boxwith letters is superimposed upon a background configuration of randomly arrayedletters. The box contains one of six possible letters and appears in one of six possiblelocations. During the 2500-ms intertrial interval the background is displayed alone.

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Threat-Evoked Anxiety, Attention, and Spatial Versus Verbal WM 493

Fig. 1. Verbal and spatial 3-back n-back tasks.

In both verbal and spatial versions of the task, participants have to decide whetherthe stimulus is the same (“target”) or different (“nontarget”) from that displayedthree trials ago (hence, 3-back). They are instructed to respond with their right handas quickly and accurately as possible by pressing “s” (same) for targets and “d”(different) for nontargets. In the verbal version, participants are instructed to payattention to the identity of the letter contained in the box and ignore its location andthe letter’s case. In the spatial version, the location of the box is to be remembered.

To increase the reliance on spatial WM during the spatial version of the task,we used nonsymmetric, partially overlapping spatial locations (intended to makeverbalization more difficult). We employed an even (50%/50%) target/nontargetratio, because noneven ratios can encourage low-effort strategies if the participantsbecome aware of the distribution.

Because each of the four conditions (WM verbal-Safety, WM spatial-Safety,WM verbal-Threat, WM-spatial-Threat) had the same number of n-back trials (34),accuracy was quantified as the absolute number of correct responses for every partic-ipant. Response times for trials to which correct responses were made were averagedwithin the four experimental conditions for each participant.

Procedure

Before starting the experiment, participants were told that the experiment con-sists of two parts: in the first part they would practice two memory tasks and in thesecond part stress would be induced whereas they would perform the memory tasks.Subsequently, participants performed Part 1. This part included three practice n-back

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494 Lavric, Rippon, and Gray

blocks: one verbal n-back block (5 min), one spatial n-back block (5 min) and onen-back block, half of which was verbal and half spatial (4 min in total). A 3-min restwas given to participants after Part 1.

Part 2 was preceded by another set of instructions, which informed participantsthat between one and three unpleasant but not particularly painful shocks wouldbe administered during the next n-back block and that each shock would be in-creasingly stronger. Participants were also told that shocks were not related to taskperformance. Consequently, participants were given the written consent form forPart 2. For participants who did not consent (2 participants), the session was termi-nated. Those who provided their consent for Part 2 were shown the shock equipment(fake) used in the experiment and were affixed shock electrodes (fake). Subsequentlythey performed an n-back block identical to the third practice block (half-verbal andhalf-spatial, order counterbalanced across participants, total duration 4 min), con-taining two instruction screens with the words “Shock Block.” This constituted theThreat condition. Importantly, shocks were not administered at any point during theexperiment. The Safety condition was represented by an equivalent n-back block,distinguished only by instruction screens with the words “Safety Block.” Half of theparticipants had the Safety block at the end of Part 1, after the three practice blocks.To counterbalance for the order of Safety and Threat blocks, the other half of theparticipants had the Safety block after the threat block (i.e., in Part 2).

Participants were debriefed at the end of the experiment, after completing theself-report scales (see below), and the reason for the nondelivery of shock was thenexplained.

Heart Rate

The absolute number of heartbeats per condition was derived on-line from theelectrocardiogram (recorded via a POLAR chest strap and heart rate monitor) andsubsequently reduced to the mean heart rate (beats per minute).

Self-Report

After the experimental session, participants provided a retrospective assess-ment of their affective state during Threat and Safety, by making a vertical mark oneach of five 100-mm-long lines, that is, visual analog scales (Bond & Lader, 1974)corresponding to the adjectives anxious, excited, scared, sad, aroused.

Statistical Analysis

Heart Rate and Self-Report

Participants heart rate was submitted to an ANOVA with Affect (safety/threat)and Task (verbal n-back/spatial n-back) as repeated measure variables and Genderas a between-participants variable. A similar ANOVA was performed for self-report:Adjective (scores on the five visual analog scales) × Affect × Gender.

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Threat-Evoked Anxiety, Attention, and Spatial Versus Verbal WM 495

Accuracy and RT

As an initial step, accuracy and RT were subjected to a generalized ANOVA/regression with Task and Affect as repeated measures, Gender as a between-participants variable and Heart Rate Difference (HRDif) as a continuous indepen-dent variable. HRDif was computed as the difference between heart rates duringThreat and Safety. To further investigate the relationship between n-back perfor-mance and the intensity of threat-evoked affect, similar generalized ANOVAs wereperformed with differences in self-report scores replacing HRDif as continuous inde-pendent variable, e.g. Fear Difference (FearDif) = difference between self-reportedfear (visual analog scale, adjective scared) in Threat as compared to Safety. Only ad-jectives, which showed significant Threat versus Safety differences in the self-reportanalysis, were entered as continuous independent variables.

Post Hoc Analysis and Corrections

t Tests and correlations were employed as post hoc analyses. t Tests were per-formed subject to significant ANOVA interactions involving repeated measure vari-ables (e.g., Task, Affect). If independent continuous variables (e.g., HRDif)showed significant ANOVA interactions, correlations (Pearson’s r) were computedbetween these and Performance Decrement (PDcr = Accuracy-in-Safety minusAccuracy-in-Threat). Such correlations would clarify the relationship between heartrate (or self-report measures), affective state, and WM performance. For example,a significant positive correlation between HRDif and PDcr would mean that thehigher heart rate in Threat as compared to Safety, the lower the performance inThreat relative to Safety.

Greenhouse–Geisser corrections were applied for violations of sphericity inANOVAs. Only corrected p values are reported.

Holm’s procedure was used to control for α-inflation in multiple t tests andcorrelations. For transparency, t and r values are reported as they came out in theanalyses (uncorrected). However, all the associated p values were corrected wherenecessary for multiple comparisons and are reported as such.

RESULTS

Heart Rate

The analysis of heart rate (see Fig. 2 and Table I) found significant main effectsof Affect, F(1, 34) = 8.46, p < .01, higher heart rate in Threat than Safety, and Task,F(1, 34) = 9.24, p < .01, higher heart rate in Verbal n-back than in Spatial n-back.However, not all participants showed increases in heart rate in Threat compared toSafety. For this reason, in some analyses of the effect of anxiety on WM performance,we focused only on the 24 participants (about 70%) who did show increases (HRDif >

0), that is, those for whom there was objective evidence of a successful emotioninduction.

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496 Lavric, Rippon, and Gray

Fig. 2. Participants’ heart rate in the four conditions (here, as well as in thesubsequent figures error bars indicate SE of mean).

Self-Report

Scores on several visual analog scales differentiated Threat from Safety. TheANOVA significant main effect of Affect, F(1, 34) = 172.13, p < .0001, and Ad-jective × Affect interaction, F(4, 136) = 32.24, p < .001, were followed by signifi-cant post hoc t tests comparing Threat versus Safety for adjectives scared, t(35) =10.64, p < .001; anxious, t(35) = 10.23, p < .001; excited, t(35) = 5.94, p < .001; andaroused, t(35) = 2.95, p < .05 (see Fig. 3 and Table II). The Threat versus Safety t testfor the adjective sad was not significant, t(35) = −0.417, p > .5.

Accuracy

Our key prediction was an interaction of Affect (threat vs. safety) with Task(verbal vs. spatial) on WM performance. As expected, there were substantial in-dividual differences in participants’ responsiveness to the emotion induction. Wetherefore sought to control for and capitalize on these differences in the strengthof the induction when assessing the key interaction of interest (see Gray, in press).Firstly, across all participants, we statistically controlled for individual differenceson the basis of physiological (HRDif) and self-report (FearDif) measures. Sec-ondly, we focused only on participants with objective evidence for a successfulemotion induction: the increase in their heart rate in Threat as compared to Safety(HRDif).

In the first analysis of WM performance, we included measures of individualdifferences in the strength of the emotion induction as a continuous variable. Thetest of the three-way Affect × Task × Strength-of-Induction interaction affords anatural test of the hypothesis. It imposes the additional constraint that the interactionof interest be strongest for those participants experiencing the strongest emotionalstate. Testing this three-way interaction by ANOVA revealed a significant Task ×Affect × HRDif interaction, F(1, 33) = 4.49, p < .05. Similarly, the Task × Affect ×FearDif interaction approached significance, F(1, 33) = 3.86, p = .058. In addition,

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Threat-Evoked Anxiety, Attention, and Spatial Versus Verbal WM 497

Tabl

eI.

Mea

nsan

dSt

anda

rdD

evia

tion

sfo

rH

eart

Rat

e,A

ccur

acy

and

Rea

ctio

nT

ime

Ver

balW

MSp

atia

lWM

Safe

tyT

hrea

tSa

fety

Thr

eat

MSD

SEM

SDSE

MSD

SEM

SDSE

Hea

rtra

te(b

/min

)83

.80

11.0

61.

8487

.69

13.6

02.

2781

.97

11.8

51.

9785

.33

12.6

42.

11A

ccur

acy

1(%

cor)

78.2

212

.25

2.04

74.0

117

.41

2.90

80.4

69.

191.

5373

.65

13.6

12.

97A

ccur

acy

2(%

cor)

77.8

111

.38

1.90

76.9

015

.71

2.62

81.0

38.

501.

4272

.77

13.5

92.

27R

T(m

s)10

63.5

030

2.10

50.3

510

63.6

431

3.22

52.2

099

0.15

275.

3245

.89

1036

.44

324.

2954

.05

Not

e.A

ccur

acy

1re

pres

ents

allp

arti

cipa

nts,

accu

racy

2re

pres

ents

only

part

icip

ants

(app

roxi

mat

ely

70%

ofpa

rtic

ipan

ts)

who

had

high

erhe

art

rate

inT

hrea

tas

com

pare

dto

Safe

tybl

ocks

(i.e

.HrD

if>

0).

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498 Lavric, Rippon, and Gray

Fig. 3. Self-report scores.

the ANOVA found a significant main effect of Affect, F(1, 33) = 5.93, p < .025. Themain effects of Task and HRDif were found to be nonsignificant, F(1, 33) = 0.46,p > .5, and F(1, 33) = 0.45, p > .5, respectively.

The pattern of selective spatial n-back disruption was fully confirmed by post hoct tests. Among t tests comparing Threat and Safety blocks for both n-back types as wellas verbal and spatial n-back blocks for both Affect types, only one was significant:Spatial Safety versus Spatial Threat, t(35) = 3.16, p < .05. The t tests comparingVerbal Safety versus Verbal Threat, t(35) = 1.93, p > .1, Verbal Safety versus SpatialSafety, t(35) = −1.42, p > .1, and Verbal Threat versus Spatial Threat, t(35) = .123,p > .9, were all nonsignificant.

Moreover, there was a significant positive correlation of PDcrSpatial withHRDif, r(36) = .44, p < .01. The correlation of PDcrSpatial with FearDif was alsopositive, but it did not reach significance, r(36) = .21, p = .22. The same correlationsof PdcrVerbal were nonsignificant, r(36) = −.09, p > .6, and r(36) = −.1, p > .5respectively. These interactions and correlations suggest that the more anxiety theparticipants reported and the higher their heart rate in the Threat condition, themore impaired was their spatial, but not verbal, n-back performance.

In the second analysis, we focused only on the 24 participants with increasedheart rate during Threat than during Safety (HRDif > 0). Testing the key two-wayinteraction by ANOVA revealed a significant Task × Affect interaction, F(1, 23) =3.95, p = .05 (see Fig. 4 and Table I). The ANOVA also revealed a significantmain effect of Affect, F(1, 23) = 5.62, p < .05. The main effect of Task was non-significant, F(1, 23) = 0.06, p > .75. In post hoc t tests, the effect of Affect was

Table II. Means and Standard Deviations for Scores on Visual-Analog Scales

Safety WM blocks Threat WM blocks

Self-report (mm) M SD SE M SD SE

Anxious 26.03 23.50 3.92 72.11 21.39 3.56Excited 21.36 22.18 3.70 50.75 29.55 4.92Scared 15.69 20.81 3.47 62.83 27.53 4.59Sad 9.30 13.74 2.29 10.13 15.45 2.57Aroused 10.44 19.57 3.26 17.30 23.78 3.96

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Threat-Evoked Anxiety, Attention, and Spatial Versus Verbal WM 499

Fig. 4. Participants’ accuracy (% correct responses). The pattern of selectivedisruption of spatial n-back (WM) performance is particularly striking isparticipants who responded to anxiety induction, as indicated by ANOVAsand correlations. To illustrate this data is presented from the 24 participants(approximately 70% of participants) who had higher heart rate in Threat ascompared to Safety blocks (HRDif > 0).

significant for the spatial task, t(23) = 3.04, p < .01, but not the verbal task, t(23) =0.56, p > .5.

Reaction Time

Participants tended to respond slower in Threat than in Safety in spatial, butnot verbal, n-back tasks (see Fig. 5 and Table I). However, ANOVA interactionsinvolving Task and Affect did not reach significance, F(1, 33) = 1.97, p > .15. Themain effect of Affect was also nonsignificant, F(1, 33) = 0.87, p > .25. The maineffect of Task was significant, F(1, 33) = 4.53, p < .05, with faster responses in thespatial n-back.

Fig. 5. Mean reaction-time in the four conditions. Statistical analysis didnot reveal reliable effects.

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500 Lavric, Rippon, and Gray

DISCUSSION

The results clearly indicate a differential effect of threat-evoked anxiety onspatial versus verbal WM. Performance on spatial, but not verbal, n-back was sig-nificantly impaired when participants had higher heart rate and reported beingmore fearful in Threat than in Safety, which emphasizes the specificity of the ef-fect (see Fig. 4 and Table I). Importantly, similar results were obtained when self-report (adjective scared) or physiological (heart rate) measures of the difference inanxiety were used as independent continuous variables. Note that accuracy anal-yses found no significant main effect of Task type, and post hoc tests revealed nosignificant differences between verbal and spatial n-back tasks in Safety. This in-dicates that the verbal and spatial n-back tasks were well matched on difficulty.The RT findings did not find reliable differences between Threat and Safety (seeFig. 5), but they indicated that there was no speed–accuracy tradeoff in the spatialWM task.

The current results not only confirm our previous findings from studies thatemployed the same tasks (Lavric et al., 2000), but they resolve important method-ological issues. For instance, current outcomes rule out the interpretation of thepreviously observed selective disruption of spatial WM in terms of the effects ofelectric stimulation, because the current paradigm did not employ shock delivery.An important advantage of the current study relative to many of the earlier stud-ies (Bartolic et al., 1999; Gray, 2001) is the use of objective, on-line measurementof the induced affect. Participants’ heart rate was higher during Threat than duringSafety blocks, for both verbal and spatial n-back tasks, as revealed by ANOVA andpost hoc tests (see Fig. 3 and Table I). In conjunction with the self-reported differ-ences on adjectives anxious, scared, excited, and aroused (see Fig. 2 and Table II),it suggests that anxiety was successfully evoked by threat-of-shock for both ver-bal and spatial tasks, which rules out the potential interpretation of the observedspatial n-back accuracy decrement in terms of selective inhibition of anxiety dur-ing the verbal task. Higher heart rate associated with verbal as compared to spa-tial n-back in both Affect conditions, indicated by the significant main effect ofTask, could be explained by more subvocal or vocal articulatory activity duringrehearsal in the verbal task (participants were not discouraged from overtly re-hearsing letters). The systematic relationship between the increase in heart rateand self-reported fear and the decrement in spatial n-back performance in Threat,revealed by ANOVAs and correlations, is an important novel result, because itprovides further validation to the selective character of threat–anxiety effects onspatial WM.

A legitimate question to be asked is whether the spatial n-back is not moresensitive to any disruption than to the verbal n-back. If that would be the case, thespecificity of the effect reported here could be questioned. In Lavric et al.’s study(Lavric et al., 2000) electromyographic (EMG) recordings were performed. In theWM trials following the delivery of shocks, startle probes were found to disrupt bothspatial and verbal n-back performance equally, suggesting that the two tasks are notdisproportionately susceptible to disruption.

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WM, Anxiety, and Visuospatial Attention

The present results are interpreted in terms of the reliance of threat-evokedanxiety and spatial n-back task on a common visuospatial attention mechanism.As suggested by recent behavioral (Awh et al., 1998), electrophysiological (Awh,Lourdes & Hillyard, 2000), and neuroimaging (Awh et al., 1999) studies, rehearsalof locations in WM tasks is likely to be based on covert shifts of attention. In thecurrent experiment, the nature of the task (3-back) requires the maintenance inWM of at least three items at any time during the task. It seems that in one of then-back WM tasks (spatial), the three items (locations) were rehearsed by shiftingattention from location to location. In contrast, the rehearsal of the three letters inthe verbal n-back could be based primarily on articulatory (phonological) processes.We therefore believe that the significant demands on visuospatial attention, imposedby the presence of threat, interfered with the rehearsal of locations but not letters.

Attention to Threat

Two cognitive models of anxiety and attention are of relevance in the currentcontext: the Attention to Threat model by Mathews and coworkers (Mathews et al.,1997; Mathews & Mackintoch, 1998) and the Cognitive–Motivational model of anx-iety by Mogg and colleagues (Mogg & Bradley, 1998). The two models make similarpredictions for moderate to high levels of anxiety: They postulate an attentional biasin processing material with moderate to high negative affective content (attention tothreat). Because of our self-report and physiological data, the current study inducedrelatively high levels of anxiety, it is likely that both models can accommodate thepresent data. Indeed, the proposal that highly threatening cues are preferentiallyattended to, is central to our account of the present results. What the current resultsseem to add is that this attentional bias in threat can have a detrimental, but selective,effect on cognitive function.

Other Models of Anxiety

The results reported here, as well as previous findings showing a similar patternof results (Lavric et al., 2000), may seem divergent from reports of selective effectsof anxiety on verbal WM (Ikeda, Iwanaga, & Seiwa, 1996; Markham & Darke, 1991).However, the model of anxiety proposed by Heller and colleagues (Heller, Etienne,& Miller, 1995; Heller & Nitschke, 1998) can easily reconcile the two patterns of data.The model makes the distinction between anxious apprehension (i.e., worry) and anx-ious arousal (i.e., panic). The two types of anxiety, though not mutually exclusive,are proposed to engage different cognitive processes (e.g., anxious apprehensionis associated with verbal ruminations), different physiological characteristics (e.g.,anxious arousal associated with physiological hyperarousal and somatic tension)and involve distinct patterns of brain activity, that is, greater left-frontal activity inanxious apprehension and greater right-parietal activity in anxious arousal. It seemsthat the type of anxiety investigated by the above-mentioned authors would more

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closely match that of anxious apprehension, while threat-of-shock anxiety elicitedin the current study would be an instance of anxious arousal, as confirmed by ourphysiological recordings. Our additional claim is that on the cognitive side anxiousarousal is also associated with increased visuospatial attention to potentially threat-ening stimuli, and could therefore limit the availability of visuospatial attentionalresources.

Finally, it seems pertinent to consider in the context of the current results thecognitive model of worry proposed by Borkovec and coworkers (Borkovec & Inz,1990; Borkovec, Lyonfields, Wiser, & Diehl, 1993). The model proposes that worry,considered to have a predominantly verbal character, can decrease the potency ofthreatening stimuli that are processed visually. One aspect of our results seems con-sistent with the model: Indeed our data suggest that threat is likely to be representedprimarily visually. It remains to be seen to what extent the findings from the currentparadigm, which used threat-of-shock for anxiety evocation, will generalize to otheranxiety states.

Anxiety, WM, and Interhemispheric Asymmetries

It would be tempting to hypothesize (Bartolic et al., 1999; Gray, 2001; Gray et al.,2002; Lavric et al., 2000) that the functional anatomy underlying our effect is inter-pretable in terms of prefrontal (Davidson, 1992) or parietal (Heller & Nitschke, 1998)interhemispheric asymmetries. Indeed, there is substantial evidence that attention isright lateralized in the prefrontal and parietal areas (see Cabeza & Nyberg, 2000, fora review) and that there is some tendency of right lateralization in spatial WM tasksin roughly the same cortical regions (Awh et al., 1999; Reuter-Lorenz et al., 2000;Smith & Jonides, 1999). Furthermore, evidence from recordings of brain electricalactivity have associated anxious arousal with greater right-parietal activity (Heller &Nitschke, 1998) and some neuroimaging studies found greater right-prefrontal cor-tex (PFC) activity in anxious arousal (Rauch, Savage, Alpert, Fischman, & Jenike,1997).

However, other neuroimaging evidence suggests that caution is needed in draw-ing such conclusions. In particular, an fMRI study investigating the n-back tasksemployed in the study reported here performed comparisons between the left andright dorsolateral PFC regions and found no reliable differences in lateralizationbetween verbal and spatial n-back tasks in this part of the PFC (Shackman et al.,2000). A recent study of threat-of shock anxiety found only left-lateralized activa-tion in the (orbitofrontal) PFC (Chua et al., 1999). Further investigations would haveto elucidate the functional–anatomical correlates of selective modulation of spatialWM by threat-induced anxiety, and, in particular, the role of prefrontal and parietalinterhemispheric asymmetries.

In conclusion, the current results indicate selective impairments in spatial WMperformance in conditions of threat-of-shock anxiety and are interpreted in termsof more overlap in visuospatial attention between anxiety and spatial WM relativeto anxiety and verbal WM. The anxiety induction procedure employed may serve asa useful model of some aspects of clinical anxiety, thus providing insights into theassociated cognitive deficits.

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ACKNOWLEDGMENTS

The authors are grateful to Tim Dalgleish, Richard Davidson, Ray Dolan,Elisabeth Maylor, Jack Nitschke, Mike Oaksford, Diego Pizzagalli, Sid Sarinopoulos,Alex Shackman, and Fred Toates for valuable discussions. Many thanks to GaynorEvans for helpful advice in the preparation of the study. The first author was sup-ported by an ORS award from the British Government.

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