the role of attentional anterior network on threat-related attentional biases in anxiety

The role of attentional anterior network on threat-relatedattentional biases in anxiety

Cesar Avila *, Maria Antonia Parcet

Apartado de Correos 224, Department de Psicologia Basica, Clınica i Psicobiologia,

Campus de la Carretera de Borriol, Universitat Jaume I, 12080 Castello, Spain

Received 24 October 2000; received in revised form 1 March 2001; accepted 15 March 2001

Abstract

A Posner covert orienting task was developed to investigate the role of the anterior and posterior atten-tional networks described by Posner and Petersen (1990) (Posner, M. I., & Petersen, S. E. (1990). Theattention system of the human brain. Annual Review of Neuroscience, 13, 25–42.) in attentional biasestoward threat-related stimuli observed in non-clinical trait-anxious subjects. This task was administered intwo different conditions depending on the informative value of the cue. Subjects had to detect an asterisktarget that appeared 100 or 500 ms after the cue. As expected, the anxiety group (measured by the Sensi-tivity to Punishment scale) was related to a greater tendency to focus on locations where aversive and non-informative cues had appeared. This effect was observed at the 100 ms, but not at the 500 ms SOA, anddisappears when cues were informative of target location. We have proposed that non-informative threat-related stimuli would activate the anterior network in anxious but not in non-anxious subjects. # 2002Elsevier Science Ltd. All rights reserved.

Keywords: Anxiety; Anterior network; Posterior network; Attention

1. Attentional biases in anxiety

Different cognitive theories of anxiety describe an attentional bias toward detecting and pro-cessing threatening stimuli (Eysenck, 1992; Mathews & McLeod, 1994; Williams, Watts,MacLeod, & Mathews, 1998). The paradigms most frequently used to test this bias are the emo-tional Stroop task and the spatial attention task (Mathews & MacLeod, 1994). The emotionalStroop task required subjects to name the colours of two lists of words as quickly as possible, onelist containing neutral words, and the other threatening words. While with non-anxious subjectsnaming performance was similar for the two lists, anxious subjects typically obtained higher

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E-mail address: [email protected] (C. Avila).

naming times for the threat-related than for the neutral words. The spatial attention task pre-sented vertically two different words for 500 ms: one had a neutral significance and the other hada threatening significance. The subjects’ task was to read aloud the top word and ignore thebottom word. Distribution of attention is measured by a secondary task involving detection of adot which could appear in the spatial location of either upper or lower word after display is ter-minated. Results showed that anxious subjects were faster in detecting probes when they occurredin the area where a threat word had just occurred. Non-anxious subjects showed the oppositepattern, suggesting that they orient away from the location at which threat had occurred. Boththe emotional Stroop and the spatial attention tasks have shown that anxious subjects have aprocessing bias toward supraliminal threat-related stimuli (Mathews & MacLeod, 1994).Pre-attentive selection of threat-related material has also been studied in anxious and non-

anxious subjects. A hypervigilant (Eysenck, 1992) or an orienting (Beck & Clark, 1997) mode thatpermits an early detection of threatening stimuli has been described in anxious subjects. Theirattentional system seems to have evolved for the search and early detection of aversive, personallyrelevant and threat-related stimuli. Although this functioning will have evolutionary value, theproblem in anxiety comes from an excessive detection and further elaboration of this negativematerial (Beck & Clark, 1997). This functioning has been supported through different importantfindings. If compared with non-anxious subjects, anxious subjects: (1) process subliminal threat-related stimuli more deeply (Fox, 1996; Mogg, Bradley, Williams, & Mathews, 1993); (2) givethreat-related significance to homophones with an alternative neutral significance (Mathews,Richards, & Eysenck, 1989; Richards & French, 1992); and (3) are more distracted by neutral andaversive peripheral stimuli (Broadbent, Broadbent, & Jones, 1986; Fox, 1994; Mathews, May,Mogg, & Eysenck, 1990). However, a critical point is to explain why this processing bias does notnormally facilitate a better recall of negative material (Mathews & MacLeod, 1994).Although all this research has clearly shown that anxious subjects have an attentional bias

toward threat-related stimuli, the nature of this bias is far from being clearly known, and theneuropsychological bases for this functioning have not been precisely delimited. Posner and Petersen(1990) described three different and relatively independent attentional networks: the posterior, theanterior, and vigilance. The present paper will study the relevance of the first two in anxiety.

1.1. Attentional networks

The posterior network involves portions of the parietal cortex, the pulvinar and parts of themidbrain’s superior colliculus. These areas co-operate in orienting to sensory stimuli. The modaltask employed for the study of its functioning is the covert orienting task developed by Posner(1980, 1988). This task requires a manual response to a target which may appear in one of twodifferent peripheral locations. A cue is always presented 100 or 500 ms before the target at thesame or on the opposite side of the target. At 100-ms SOA, results show that responses to thetarget appearing at the cued location were more rapid than at the uncued location. The posteriornetwork made three simple cognitive operations to move covert attention within the space: theparietal lobe disengages attention from its current focus, the superior colliculus moves attentionto the cued location, and the pulvinar engages attention in that location (Posner, 1988; Posner,Inhoff, Friedich, & Cohen, 1987). A further consequence of the action of the posterior network isinhibition of return. This phenomenon is observed at 500-ms SOA, and serves to prevent attention

716 C. Avila, M.A. Parcet / Personality and Individual Differences 32 (2002) 715–728

from returning to the previously disengaged location. Thus, at SOAs greater than 300 ms,response times in the uncued trials were faster than in the cued trials. In the absence of expecta-tions about target location, these two automatic phenomena carried out by the posterior networkserve to search and respond to target stimuli efficiently.The anterior network, implicated in tasks requiring the detection of events, involves specific

areas of the mid-prefrontal cortex, including the anterior cingulate gyrus and the supplementarymotor area. This network is responsible for regulating the posterior attentional network (Posneret al., 1987) and for controlling attention to semantic information (Fuentes, Carmona, Agis, &Catena, 1994; Petersen, Fox, Posner, Mintun, & Raichle, 1988), maintaining expectations in tasksrequiring attentional priming (i.e. when SOAs between primes and targets were long). Vogt,Finch, and Olson (1992) have proposed that this network may provide a site for interactionbetween motivational (expectations) and cognitive processes, executing functions of volitionalcontrol and awareness, particularly awareness of target stimuli. It has been suggested that theanterior cingulate is active in tasks in which automatic processes might fail including situationsjudged to be dangerous (Norman & Shallice, 1986). Recent theoretical approaches to the func-tions of the anterior cingulate have attributed two different functions to this structure. Posner andDiGirolamo (1998) proposed that the anterior cingulate triggers a set of processes that guide theselection of stimuli for action. However, recently some researchers have proposed that the func-tion of this structure serves to exert executive control to detect the existence of conflicts ininformation processing (Carter et al., 2000).Although the anterior and posterior networks can be thought of as working with a relative

autonomy, both are linked via important reciprocal connections (Goldman-Rakic, 1988). Thispermits the anterior network to execute a hierarchical control over the posterior network (Posner,1990). Posner et al. (1987) administered the covert orienting task to a group of parietal-damagedpatients in single and dual-task conditions. In the two different dual-task situations, two languagetasks that activated the anterior network were used: counting backwards, and searching for thephoneme p in a list of auditory words. They found that in the dual-task conditions, the languagetask reduced the advantage of detecting targets at cued location when compared with uncuedlocation; i.e. the language task interfered with the orienting task. Following additive factors logic(Sternberg, 1969), and taking into consideration that the posterior network was damaged in thesepatients, the authors were able to conclude that the anterior network was involved in both tasks.Posner and Petersen (1990) proposed that ‘‘the anterior system can pass control to the posteriorsystem when it is not occupied with processing other material’’ (p. 35).Another situation in which the anterior network takes control over the posterior network is

obtained when cues in the Posner covert orienting task are linked to expectations about targetlocation (Jackson & Houghton, 1992). Subjects could be informed that the cue signals the mostprobable target location (normally in 80% of trials) generating a strong expectation about targetlocation. Jonides (1981) found that exogenous, non-informative cues produced more rapid, moreeffective, and more difficult to suppress changes in orienting than informative cues. Recentresearch of the neural basis of endogenous and exogenous spatial orienting has shown two rele-vant differences (Rosen et al., 1999): (1) endogenous, but not exogenous cues, selectively activatedthe right dorsolateral prefrontal cortex; and (2) both endogenous and exogenous cues activatedthe right anterior cingulate more than neutral cues, but the difference was more pronounced forendogenous cues. These results were consistent with the proposal that informative cues would

C. Avila, M.A. Parcet / Personality and Individual Differences 32 (2002) 715–728 717

produce a greater activation of the anterior network than non-informative cues. Thus, the pre-sence of informative cues results in a stronger activation of the anterior network which takescontrol over the posterior network, maintaining attention on most probable target locations andpreventing disengagement.

1.2. A model for explaining attentional biases in anxiety

This framework sketched in Fig. 1 may serve to explain the attentional biases described inanxious subjects. Fig. 1 shows that exogenous, non-informative cues directly activate the poster-ior network and endogenous, informative cues would activate the anterior network which wouldtake control over the posterior network. We propose that peripheral aversive word cues, as rele-vant semantic cues, would be able in some cases to activate the anterior system which would also

Fig. 1. Proposed model for explaining attentional biases in anxiety.


take control over the posterior network. Our hypothesis was that the presence of threat-relatedstimuli would produce a greater activation of the anterior attentional network in anxious than innon-anxious subjects. If this activation is produced while subjects are engaging in parallel atten-tional tasks (i.e. emotional Stroop or spatial attention task), then the anterior network wouldcarry out, in anxious subjects, two different functions which interfered between them: (1) theconscious processing of threat-related material; and (2) the visuo-spatial orienting task. Themutual inhibition between both cognitive and emotional tasks (Drevets & Raichle, 1998) wouldimpair or slow attentional performance. Contrarily, the lower activation of the anterior networkby aversive cues in non-anxious subjects would increase the probability of a more efficient controlof the visuo-spatial functions from the posterior network.A previous study by Derryberry and Reed (1994) would support these hypotheses. They asso-

ciated one of the two peripheral locations used in the Posner task with reward (gaining points),and the other with punishment (losing points). Subjects were instructed that if a detection targetappeared in one location and their response was rapid they would gain points, but if the targetappeared in the other location and their response was too slow they would lose points. Non-informative pre-target cues could signal one of the peripheral locations. Neutral trials wereincluded using central cues, and were used to calculate costs and benefits. Results showed that, at100-ms SOA, neurotic introverts were slow to disengage attention from a cue signalling thelocation associated with punishment. In contrast, neurotic extraverts were slow to shift theirattention away from a cue signalling the location associated with reward. Although the authorsprovided relevant explanations for their results, we could also explain them following the modeldepicted in Fig. 1. An aversive cue could activate the anterior network in anxious subjects (i.e.neurotic introverts), and this network could take control and interfere with the visuo-spatialfunctions. In contrast, non-anxious subjects (i.e. stable extraverts) would control attentionalfunctions directly through the posterior system.

1.3. The present study

In the present paper, we have developed a procedure which is a combination of that designedto study spatial attentional bias in anxiety, and that employed by Derryberry and Reed (1994).Our main objective is give support to the model of the Fig. 1. A Posner covert orienting task wasdesigned to study the efficacy of aversive and neutral cues to orient attention while searching for asimple target. Our adaptation of the Posner task used neutral and threat-related words as cues,followed by an asterisk target. As usually employed in these tasks, there were two different cue–target intervals of 100 and 500 ms. This task would permit us to investigate the attentional effectsof emotional cues on responses to neutral targets. This procedure would eliminate the possibilityof a response bias toward emotional stimuli when there was a competition between emotionaland neutral stimuli. Two types of trials were considered in this task. In valid trials, cues and tar-gets appeared on the same hemifield. In invalid trials, targets appeared on the opposite hemifieldthan cues. The present task had 80% of valid trials and 20% of invalid trials. The task wasadministered under two different conditions. In the non-informed condition, subjects were notinformed of the cue–target relationship. As previously found in this task when using non-infor-mative cues (Posner & Cohen, 1984), we expected that cued locations would produce fasterresponse times than uncued at the 100-ms interval. However, at the 500-ms interval, we also


expected to obtain inhibition of return (i.e. response times in uncued locations should be fasterthan in cued locations). In the informed condition, subjects were initially informed of the cue–target relationship. Previous results with this procedure have shown that informative cues serve tofocus attention on most probable target locations at both 100-ms and 500-ms SOAs (Posner &Cohen, 1984).Subjects were classified as anxious and non-anxious subjects according to their scores on the

Sensitivity to Punishment scale of the Sensitivity to Punishment and Sensitivity to RewardQuestionnaire (Torrubia, Avila, Molto, & Caseras, 2001). This scale was designed to measure thefunctioning of the reactivity and responsivity of the Behavioural Inhibition System (Gray, 1982)and has been used in a number of experimental studies (Avila, 2001; Brebner & Martin, 1995;Torrubia et al., 1995; Zuckerman, 1999).According to the model of Fig. 1, our main hypothesis was that these general attentional effects

would be modulated by the emotional significance of the cue, the informative value of the cue andthe trait-anxiety group. The following hypotheses guided this investigation:

1. For the non-informed condition, we expected that trait-anxious subjects would display adifferent functioning of covert orienting as a result of the presence of threat-related cues.Specifically, we expected to find a predisposition of anxious subjects to show strongervalidity effects (i.e. difference in reaction time between valid and invalid trials) with threat-related rather than neutral cues. Threat-related cues, which are relevant for anxious subjects,would activate the anterior network more than neutral cues (Fig. 1), initiating a consciouscontrol over the posterior system, and slowing performance speed of visuo-spatial functions.

2. The non-anxious group, however, were not expected to show any difference between neutraland threat-related cues in the magnitude of the validity effect in the non-informed condition.The difference is that threat-related cues, similarly to neutral cues, are not relevant semanticcues for the non-anxious group. Then, no activation of the anterior network was expected,and the posterior network would directly control visuospatial attentional functions.

3. Because biases in anxiety are preattentional, these effects were expected to be automatic inthe sense of being involuntary and closely time-locked to the appearance of the cue. Thus, itis hypothesized that differences should be obtained at the 100-ms SOA, which is more likelyto reflect the influence of automatic initial shifts in orientation. No hypothesis was madeabout the effects of cue type on inhibition of return.

4. In the informed condition, we hypothesized that performance would not be related to trait-anxiety, because cues that informed about possible target location would activate stronglyand equally the anterior network in anxious and non-anxious groups. Then, the anteriornetwork would take a similar control in both groups over the posterior network.

2. Method

2.1. Subjects

Seventy-six female undergraduates from an introductory psychology course participated in theexperiment in a partial fulfilment of a course requirement. Mean age was 19.61 (S.D.=2.09) with


range between 18 and 27 years. Subjects were classified in two groups according to their scores onthe Sensitivity to Punishment (SP) scale of the Sensitivity to Punishment and Sensitivity toReward Questionnaire. Cut-off scores were calculated from a large undergraduate sample(Torrubia et al., 2001). Subjects scoring 12 or higher on the SP scale were designated high anxious(SP+), and subjects scoring below 12 were classified as low anxious (SP�).

2.2. Task

Participants were located at approximately 60 cm from the screen. At the beginning of a trial,the screen was black, followed by ‘+’ at a central fixation point that remained on the screen tothe end of the trial. This fixation point was followed 500 ms later by a peripheral cue. Subjectswere instructed to fixate the central point, to avoid moving their eyes, and to press the ‘‘zero’’ keyon the keyboard number pad with whichever index finger they wanted to whenever an asterisktarget appeared. This target could appear on either the left or the right side of the central fixationpoint (approximately 5.6� from it), just 0.8� below the cue or in the equivalent position in theother visual field (Fig. 2).This cue consisted of a word written in white capital letters that remained on the screen to the

end of each trial. Eight threat-related and eight neutral words served as cues (Table 1). Threatwords were obtained from previous research on attentional biases in anxiety. Threat and neutralwords were matched for length. The average frequency of occurrence using the Alameda andCuetos (1995) norms was not significantly different for threat and neutral words [t (14)=0.66,P=0.52]. Each word cue occurred with equal frequency on the left and right sides. The word cuewas followed by the target presented in 91% of the trials. The remaining 9% of the trials werecatch trials (a cue followed by no target). The stimulus onset asynchrony (SOA) between theonset of the cue and the target was randomly either 100 or 500 ms.Validity of the cue was obtained from the relationship between location of the cue and the

target. Valid trials were those in which cues and targets were presented in the same location. Ininvalid trials, cues appeared in the opposite location of targets. There were 128 valid trials, 32

Fig. 2. Sequence of events and exposure durations of stimuli in the task.


invalid trials, and 16 catch-trials. Hence, cues predicted target location in 80% of the trials.Intertrial interval varied randomly between 2000 and 2500 ms.The task could be administered on two different conditions depending on instructions. In the

Informed Condition, subjects were informed that cues were followed by targets in the samelocation on 80% of trials, so they should expect targets in the same location of cues. In the non-informed Condition, participants were not initially informed of this relationship, so they nor-mally will disengage from cues at long SOAs.1

2.3. Procedure

Subjects first completed the SPSRQ questionnaire in the classroom situation. Subjects of SP+and SP� groups were then ascribed to the two conditions presenting instructions on the screen.They were tested in small groups of 3–7. Subjects completed a block of practice 20 trials beforebeginning a set of four blocks of 48 trials. The experimenter remained in the room during all theexperiment.

3. Results

Performance in the orienting tasks was analyzed from median reaction times using a2�2�2�2�2 analysis of variance. The within-subject factors were Cue Validity (valid or invalid),Cue Valence (aversive or neutral), and SOA (100 or 500), whereas the between-subjects factorswere Sensitivity to Punishment (high vs. low) and Condition (informed vs. non-informed). Meansof median reaction times for each condition appear in Table 2. Mean errors on catch trials were0.72(S.D.=0.9) and there were no differences between groups.

Table 1Threat and neutral words cues in English and Spanish

Threat words Neutral words

English Spanish English Spanish

Failure FRACASO Wardrobe ARMARIODeath MUERTE Music MUSICACancer CANCER Shepherd PASTOR

Idiot IDIOTA Garden JARDINWar GUERRA Drum TAMBORError ERROR Tree ARBOL

Fear MIEDO Paper PAPELHate ODIO Rock ROCA

1 Normally, validity with exogenous cues in the Posner task used to be 50%. In this study, we preferred to choose

the 80% validity to make both conditions comparable. A pilot work conducted to test this possibility showed that bothfacilitation and inhibition of return effects were obtained when using this percentage of validity.


Overall analysis yielded significant main effects for SOA [F (1,72)=153.37, P<0.001], CueValidity [F (1,72)=72.95, P<0.001] and Condition [F (1,72)=7.98, P<0.01]. Inspection of themain effects revealed that, averaged across the levels of the other conditions, the 500-ms SOAresulted in faster reaction times than the 100-ms SOA (by about 37 ms.), the valid conditionresulted in faster reaction times than the invalid condition (by about 24 ms.) and that the non-informed condition resulted in faster reaction times than the informed condition (by about 37ms.). These main effects were modulated by the Cue Validity � SOA � Condition significantinteraction, [F (1, 72)=38.92, P<0.001], reflecting that the Cue Validity main effect was yieldedat the 100-ms SOA in both conditions (Fig. 3), but the non-informed condition reversed the CueValidity main effect at the 500-ms SOA showing the typical inhibition of return effect (Fig. 4).These results show that cues in the non-informed group were exogenous and yielded the typicalbiphasic effect of initial facilitation and later inhibition of return, whereas cues in the informedgroup were endogenous because they only yielded facilitation that was maintained at the long SOA.The SP and Cue Valence factors only entered in one interaction. The Cue Validity � Cue

Valence � SOA � SP � Condition interaction was significant, [F (1,72)=6.24, P<0.02]. Thisinteraction was interpreted by planned comparisons using the subtracted measures of validity(reaction times in invalid trials minus reaction times in valid trials). As predicted, anxiety differ-ences were observed for the non-informed condition. This indicated that the validity effect at the100-ms SOA in anxious subjects was greater for aversive than neutral cues, whereas non-anxioussubjects showed the reversed effect (Fig. 3). No personality differences were found at the 500-msSOA or in the informative-condition (Fig. 4).

Table 2Mean reaction times as a function of SOA, Cue Valence, and Cue Validity

Aversive cue Neutral cue

100 ms SOA 500 ms SOA 100 ms SOA 500 ms SOA

Valid Invalid Valid Invalid Valid Invalid Valid Invalid

Non-informed conditionSP� 352 376 341 321 348 391 342 317SP+ 340 388 362 320 342 379 356 323

Informed conditionSP� 368 435 335 374 371 428 331 379SP+ 400 452 361 402 393 442 361 401

Fig. 3. Validity effects obtained at 100-ms SOA by anxious (SP+) and non-anxious (SP�) groups.


4. Discussion

Our adaptation of the Posner task has confirmed some expected results. At the short SOA, theexpected difference in reaction times between valid and invalid trials was found in both condi-tions, which would indicate that detection was faster at cued than uncued locations. At the longSOA, results depend on condition. In the informed condition, the difference observed betweenvalid and invalid trials was maintained as in the short SOA. However, in the non-informed con-dition, this effect was reversed at the 500-ms SOA showing the well-described phenomenon ofinhibition of return. As typically obtained (Jonides, 1981), the magnitude of the validity effect atthe 100-ms SOA was stronger in the informed than in the non-informed condition. That is,endogenous cues caused a slowness in the disengage, move, and engage functions necessary todetect an invalidly cued target. This difference is relevant because it reflects that these orientingfunctions are performed more slowly when controlled endogenously from the anterior network.Personality correlates of these global effects failed to replicate previous findings which showed

a greater inhibition of return in subjects with high neuroticism or sensitivity to punishment(Avila, 1995). Differences in the procedure used in this study as the SOA (500 ms instead of 1000ms), the inclusion of a central cue or the type of cue (words instead of physical changes) couldpossibly explain these differences. Furthermore, we could consider that the use of aversive cuescould modify global attentional functioning in anxious and neurotic subjects (Mathews et al.,1990).Our main area of interest was to study the interaction between sensitivity to punishment, con-

dition and emotional content of the cue on attentional performance. Results have confirmed ourhypotheses within this undergraduate non-clinical sample. First, in the non-informed condition,the anxious group (measured with Sensitivity to Punishment scale) showed a greater validityeffect for threat-related than for neutral cues. Second, this difference between aversive and neutralcues was not found for the non-anxious group. Third, these effects were found only at the shortSOA and not at the long SOA, indicating that the effect was a rather automatic effect closelytime-locked to the appearance of the cue. Finally, as expected the informed condition did notyield any anxiety differences in attentional focusing on aversive cues.These results are consistent with the model proposed in Fig. 1 designed to integrate the atten-

tional biases obtained in anxious subjects in the attentional networks describe by Posner andcolleagues. We have hypothesized that the anterior or executive network may be the key structureto the understanding of attentional biases toward threat-related material in anxious subjects. Inthe absence of relevant stimuli, orienting functions are basically performed by the posterior

Fig. 4. Validity effects obtained at 500-ms SOA by anxious (SP+) and non-anxious (SP�) groups.


network (Posner & Petersen, 1990). Our initial proposal was that threat-related stimuli throughconnections from the amygdala, the hippocampus, and the orbito-frontal to the anterior cingu-late would have an increased probability of activating the anterior network in anxious subjectsrather than in non-anxious subjects. Once activated, the anterior network should take executivecontrol over the functions of the posterior network. This control would serve to monitor orient-ing functions due to a relevant stimulus (i.e. a threat) having entered into the consciousness. Thiscontrol, however, would also imply a greater slowness in the performance of these orientingfunctions. Reaction time data were consistent with this interpretation: with the exception of theanxious group in invalid aversive trials, RTs were faster for the non-informed than the informedgroup. A further consideration is that this model does not emphasize a different level of proces-sing of threat-related and neutral words in anxious and non-anxious subjects. Attentional biasesare not necessarily a consequence of a different processing of threat-related material in anxioussubjects. The model is simply based on the fact that these stimuli activate the anterior network,causing a different emotional experience (Lane, Reiman, Axelrod, Yun, Holmes, & Schwartz,1998). This fact could explain a typical failure in finding explicit memory differences associatedwith anxiety (Mathews & McLeod, 1994).The present model is consistent with a recent proposal by Hamner, Lorberbaum, and George

(1999) indicating that the anterior cingulate may serve a critical gating function in modulatingconditioned fear responses, that is, this structure determines which stimuli would or would not beattended to. It was suggested that patients with anxiety disorders (i.e. the model was tested insubjects with post-traumatic stress disorder) would attend easily to exogenous irrelevant stimuli.These authors reviewed different neuroimaging, pharmacological, and cognitive studies thatsupported their model.Our model makes specific hypotheses about when attentional biases toward threatening stimuli

in anxious and non-anxious subjects are likely to be found. The key factor here is to consider thatattentional biases are not a consequence of a deficient functioning in attentional structures, butrather, are the result of a different mode of control due to the parallel activation of the samestructure. The semantic activation by relevant stimuli of the anterior network would imply acontrol of orienting functions from this network (Posner et al., 1987). This different control fromthe anterior network could possibly provide an explanation for the attentional biases observed inanxious subjects in paradigms such as the emotional Stroop and the spatial attention task. Inboth cases, the appearance of a threat-related cue would slow attentional changes toward anotherdimension of the cue (i.e. color in emotional Stroop) or toward a neutral cue (i.e. spatial attentiontask). Other results typically found in anxiety research may be fitted into this model. First, somestudies have shown that peripheral threat distractors interfere more with the main and neutraltask in anxious than in non-anxious subjects (Eysenck & Byrne, 1992; Mathews et al., 1990;Newman et al., 1993; Shapiro & Lim, 1989). According to our proposal, threat-related distractorswould activate the anterior network, and this system would control orienting functions. Second,Derryberry and Tucker (1994) have described experiments which showed that an aversive centralstimulus impaired detection of peripheral neutral stimuli.The present model also predicts when attentional biases toward threat-related stimuli are not

likely to be observed. First, no differences should be found when the task does not involveattentional functions (MacLeod & Mathews, 1991; Mathews & Milroy, 1994). That is, tasks suchas categorizing emotional and neutral words do not involve a dual-task activation in the anterior


network. Second, anxiety differences in performance are not likely to show up when the main taskactivates the anterior network. This could help to explain previous results showing no inter-ference effects in phobic subjects when threatened by a phobic object or situation (Amir,McNally, Riemann, Burns, Lorenz, & Mullen, 1996; Mathews & Sebastian, 1993). We couldassume that, in these studies, the phobic situation would activate the anterior network in allsubjects, suppressing as in the informed condition differences in attentional functioning. Oneunresolved issue in our proposed model is the role of subliminal threat-related stimuli, which alsoyielded similar attentional biases (Mogg, Bradley, & Hallowell, 1994). One possibility is that thesestimuli could also activate the anterior network via the amygdala (Morris, Ohman, & Dolan,1999). A second possibility is that these stimuli cause attentional biases in a different form.In summary, previous research has described attentional biases toward threat-related material

in anxious subjects. However, this research has not integrated recent advances in understandingthe neuropsychological basis of attention. The present approach has used the Posner covert-orienting task to study these biases. Results were integrated in the attentional networks describedby Posner and Petersen (1990), considering the attentional network as the key structure for theunderstanding of attentional biases in anxious subjects. Further studies should assess therelevance of this network.

Acknowledgements

This research was supported by a research grant P1A98-09 from the Fundacio Caixa-Castello.We would like to thank Sybil Eysenck, Luis Fuentes and an anonymous reviewer for their com-ments earlier versions of this paper. We thank Daniel Soltice for his help with English ‘‘flow’’.

References

Alameda, J. R., & Cuetos, F. (1995). Diccionario de frecuencias de las unidades linguısticas del castellano. Oviedo: Ser-

vicio de Publicaciones de la Universidad de Oviedo.Amir, N., McNally, R. J., Riemann, B. C., Burns, J., Lorenz, M., & Mullen, J. T. (1996). Suppression of the emotionalStroop effect by increased anxiety in patients with social phobia. Behavior Research and Therapy, 34, 945–948.

Avila, C. (1995). Facilitation and inhibition of visual orienting as a function of personality. Personality and IndividualDifferences, 18, 503–509.

Avila, C. (2001). Distinguishing BIS-mediated and BAS-mediated disinhibition mechanisms: a comparison of disin-hibition models of Gray and Patterson and Newman. Journal of Personality and Social Psychology, 80, 311–324.

Beck, A. T., & Clark, D. A. (1997). An information processing model of anxiety: automatic and strategic processes.Behavior Research and Therapy, 35, 49–58.

Brebner, J. M. T., & Martin, M. (1995). Testing for stress and happiness: the role of personality factors.

In C. D. Spielberger, I. G. Sarason, J. Brebner, E. Greenglass, P. Laungani, & A. M. O’Roark (Eds.), Stress andemotion: anxiety, anger, and curiosity (Vol. 15) (pp. 139–172). Washington, DC: Taylor & Francis.

Broadbent, D. E., Broadbent, M. H. E., & Jones, J. L. (1986). Performance correlates of self-reported cognitive failure

and obsessionality. British Journal of Clinical Psychology, 25, 285–289.Carter, C. S., Macdonald, A. M., Botvinick, M., Ross, L. L., Stenger, V. A., Noll, D., & Cohen, J. D. (2000). Parsingexecutive processes: strategic vs. evaluative functions of the anterior cingulate cortex. Proceedings of the National

Academy of Sciences, 97, 1944–1948.


Derryberry, D., & Reed, M. A. (1994). Temperament and attention: orienting toward and away from positive and

negative signals. Journal of Personality and Social Psychology, 66, 1128–1139.Derryberry, D., & Tucker, D. M. (1994). Motivating the focus of attention. In P. Niedenthal, & S. Kitayama (Eds.),The heart’s eye: emotional influences in perception and attention (pp. 167–196). San Diego, CA: Academic Press.

Drevets, W. C., & Raichle, M. E. (1998). Reciprocal suppression of regipnal cerebral blood flow during emotionalversus higher cognitive processes: implications for interactions between cognition and emotion. Cognition and Emo-tion, 12, 353–386.

Eysenck, M. W. (1992). Anxiety: the cognitive perspective. Exeter: LEA.Eysenck, M. W., & Byrne, A. (1992). Anxiety and susceptibility to distraction. Personality and Individual Differences,13, 793–798.

Fox, E. (1994). Attentional bias in anxiety: a defective inhibition hypothesis. Cognition and Emotion, 8, 165–195.

Fox, E. (1996). Selective processing of threatening words in anxiety: the role of awareness. Cognition and Emotion, 10,449–480.

Fuentes, L. J., Carmona, E., Agis, I., & Catena, A. (1994). The role of anterior attention system in semantic processing

of both foveal and parafoveal words. Journal of Cognitive Neuroscience, 6, 17–25.Goldman-Rakic, P. S. (1988). Topography of cognition: parallel distributed networks in primate association cortex.Annual Review of Neuroscience, 11, 137–156.

Gray, J. A. (1982). The neuropsychology of anxiety: an enquiry of the septo-hippocampal system. Oxford: Oxford Uni-versity Press.

Hamner, M. B., Lorberbaum, J. P., & George, M. S. (1999). Potential role of the anterior cingulate cortex in PTSD:

review and hypothesis. Depression and Anxiety, 9, 1–14.Jackson, S., & Houghton, G. (1992). Basal ganglia function in the control of visuospatial attention (Technical ReportNo. 92-6). Universidad de Oregon.

Jonides, J. (1981). Voluntary vs. automatic control over mind’s eye’s movement. In J. B. Long, & A. D. Baddeley

(Eds.), Attention and performance IX (pp. 187–203). Hillsdale: Erlbaum.Lane, R. D., Reiman, E. M., Axelrod, B., Yun, L. S., Holmes, A., & Schwartz, G. E. (1998). Neural correlates of levelsof emotional awareness. Evidence of an interaction between emotion and attention in the anterior cingulate cortex.

Journal of Cognitive Neuroscience, 10, 525–535.MacLeod, C., & Mathews, A. (1991). Biased cognitive operations in anxiety: accessibility of information processingpriorities. Behavior Research and Therapy, 29, 599–610.

Mathews, A., May, J., Mogg, K., & Eysenck, M. W. (1990). Attentional bias in anxiety: selective search or defectivefiltering? Journal of Abnormal Psychology, 99, 166–173.

Mathews, A., & MacLeod, C. (1994). Cognitive approaches to emotion and emotional disorders. Annual Review Psy-

chology, 45, 25–50.Mathews, A., & Milroy, R. (1994). Processing of emotional meaning in anxiety. Cognition and Emotion, 8, 535–553.Mathews, A., Richards, A., & Eysenck, M. (1989). Interpretation of homophones related to threat in anxiety states.Journal of Abnormal Psychology, 98, 31–34.

Mathews, A., & Sebastian, S. (1993). Suppression of emotional Stroop effects by fear arousal. Cognition and Emotion,8, 517–530.

Mogg, K., Bradley, B. P., & Hallowell, N. (1994). Attentional bias to threat: roles of trait anxiety, stressful events, and

awareness. Quarterly Journal of Experimental Psychology, 47, 841–864.Mogg, K., Bradley, B. P., Williams, R., & Mathews, A. (1993). Subliminal processing of emotional information inanxiety and depression. Journal of Abnormal Psychology, 102, 304–311.

Morris, J. S., Ohman, A., & Dolan, R. J. (1999). A subcortical pathway to the right amygdala mediating the ‘‘unseen’’fear. Proceedings of the National Academy of Sciences, 96, 1680–1685.

Newman, J. P., Wallace, J. F., Strauman, T. J., Skolaski, R. L., Oreland, K. M., Mattek, P. W., Elder, K. A., &McNeely, J. (1993). Effects of motivationally significant stimuli on the regulation of dominant responses. Journal of

Personality and Social Psychology, 65, 165–175.Norman, D. A., & Shallice, T. (1986). Attention to action: willed and automatic control of behavior. In R. J. Davidson,G. E. Schwartz, & D. Shapiro (Eds.), Consciousness and self-regulation (pp. 1–18). New York: Plenum.


Petersen, S., Fox, P. T., Posner, M. I., Mintun, M., & Raichle, M. E. (1988). Positron emission tomographic studies of

the cortical anatomy of single-word processing. Nature, 331, 585–589.Posner, M. I. (1980). Orienting of attention. The VIIth Sir Frederic Barlett Lecture. Quaterly Journal of ExperimentalPsychology, 32, 3–25.

Posner, M.I. (1988). Structures and functions of selective attention. In T. Boll, & B. Bryant, Clinical neuropsychology andbrain function: research, measurement, and practice (pp. 169–202). Washington: American Psychological Association.

Posner, M. I. (1990). Hierarchical distributed networks in the neuropsychology of selective attention. In A. Camarazza

(Ed.), Cognitive neuropsychology and neurolinguistics (pp. 187–210). New York: Plenum.Posner, M. I., & Cohen, Y. (1984). Components of visual orienting. In H. Bouman, & D. Bowhuis (Eds.), Attention andperformance X (pp. 55–66). Hillsdale, NJ: Erlbaum.

Posner, M. I., & DiGirolamo, G. J. (1998). Executive attention: conflict, target detection and cognitive control. In R.

Parasuraman (Ed.), The attentive brain (pp. 401–423). Cambridge: MIT Press.Posner, M. I., Inhoff, A.W, Friedich, F. A., & Cohen, A. (1987). Isolating attentional systems: a cognitive-anatomicalanalysis. Psychobiology, 15, 107–121.

Posner, M. I., & Petersen, S. E. (1990). The attention system of the human brain. Annual Review of Neuroscience, 13,25–42.

Richards, A., & French, C. C. (1992). An anxiety-related bias in semantic activation when processing threat/neutral

homographs. Quarterly Journal of Experimental Psychology, 45A, 503–525.Rosen, A. C., Rao, S. M., Caffarra, P., Scaglioni, A., Bobholz, J. A., Woodley, S. J., Hammeke, T. A., Cunningham,J. M., Prieto, T. E., & Binder, J. R. (1999). Neural basis of endogenous and exogenous spatial orienting. A functional

MRI study. Journal of Cognitive Neuroscience, 29, 135–152.Shapiro, K. L., & Lim, A. (1989). The impact of anxiety on visual attention to central and peripheral events. BehaviorResearch and Therapy, 27, 345–351.

Sternberg, S. (1969). The discovery of processing stages: extensions of Donders’ method. In W. G. Koster (Ed.),

Attention and performance II (pp. 276–315). Amsterdam: Elsevier.Torrubia, R., Avila, C., Molto, J., & Caseras, X. (2001). The sensitivity to punishment and sensitivity reward ques-tionnaire (SPSRQ) as a measure of Gray’s anxiety and impulsivity dimensions. Personality and Individual Differences

(in press).Torrubia, R., Avila, C., Molto, J., & Grande, I. (1995). Testing for stress and happiness: the role of the behavioralinhibition system. In C. D. Spielberger, I. G. Sarason, J. Brebner, E. Greenglass, P. Laungani, & A. M. O’Roark

(Eds.), Stress and emotion: anxiety, anger, and curiosity (Vol. 15) (pp. 189–211). Washington, DC: Taylor & Francis.Vogt, B. A., Finch, D. M., & Olson, C. R. (1992). Overview: functional heterogeneity in cingulate cortex: the anteriorexecutive and posterior evaluative regions. Cerebral Cortex, 2, 435–443.

Williams, J. M. G., Watts, F. N., MacLeod, C., & Mathews, A. (1998). Cognitive psychology and emotional disorders.Chichester: Wiley.

Zuckerman, M. (1999). Incentive motivation: just extraversion? Behavioral and Brain Sciences, 22, 539–540.


the role of attentional anterior network on threat-related attentional biases in anxiety

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