Cognitive Brain Research 12 (2001) 383–395www.elsevier.com/ locate /bres

Research report

Attentional set modulates visual areas: an event-related potential studyof attentional capture

a,b , a b,c a,b*Stephen R. Arnott , Jay Pratt , David I. Shore , Claude AlainaDepartment of Psychology, University of Toronto, Toronto, Ontario, Canada

bRotman Research Institute, Baycrest Center for Geriatric Care, Toronto, Ontario, CanadacDepartment of Psychology, McMaster University, Toronto, Canada

Accepted 4 June 2001

Abstract

The present experiment offers event-related potential evidence suggesting that modulation of neural activity in the visual cortexunderlies top-down attentional capture by irrelevant cues. Participants performed a covert visual search task where they identified theunique stimulus in a brief, four-location display. Targets defined uniquely by color or onset were run in separate blocks, encouragingobservers to adopt different attentional sets in each block. In Experiment 1, a brief, white, abrupt-onset cue highlighted one of thelocations 100 or 200 ms prior to the target display. In Experiment 2, the cue display consisted of three white and one red cuessimultaneously presented at the four locations. In both experiments, participants were informed that there was no predictive relationbetween the location of the cue and that of the target. Reaction times were dependent on the location of the preceding cue (i.e. attentionwas captured), but only in those blocks where the cue shared the uniquely relevant target feature. Evoked potentials over the righthemisphere were modulated during the attention-capturing blocks just prior to the cue’s appearance. Additionally, the N1 wave elicited bythe cue was enhanced over occipital regions during the attention-capturing blocks. These findings support the notion that attentionalcapture with peripheral cues is not simply reflexive but is modulated by top-down processes. 2001 Elsevier Science B.V. All rightsreserved.

Theme: Neural basis of behavior

Topic: Cognition

Keywords: Visual cortex; Attentional capture; Attentional set; ERP; N1; Top-down

1. Introduction for targets at uncued (i.e. novel) locations, provided thestimulus onset asynchrony (SOA) is shorter than 300 ms

We have all experienced situations where our attention [43].is momentarily drawn to an object that is irrelevant to our Initially it was believed that any peripheral cue pre-current goal. This phenomenon has been termed ‘attention- sented just before the appearance of a target could serve toal capture’ and may be defined as the occasion where a capture attention [53]. However, several experiments havesalient and irrelevant stimulus affects performance on since shown that this is not always the caseanother task irrespective of the observer’s awareness [43]. [3,13,14,18,38]. In particular, Folk and colleagues haveAttentional capture is usually indexed by reaction time argued that attentional capture is contingent on whether or(RT) differences to targets that are preceded by cues such not the cue shares the relevant feature that defines theas the abrupt onset of an object in the periphery. Typically, target (e.g. [11–15] but see also [52]). Their contingentRTs are faster for targets that occur at cued locations than involuntary orienting hypothesis posits that optimum per-

formance on any attentional task requires an observer toadopt a cognitive ‘set’ that controls the exogenous atten-

*Corresponding author. Rotman Research Institute, Baycrest Center fortional system. In other words, only stimulus properties thatGeriatric Care, 3560 Bathurst Street, Toronto, Ontario, M6A 2E1 Canada.are relevant to optimal task performance capture attention.Tel.: 11-416-785-2500, ext. 2737; fax: 11-416-785-2862.

E-mail address: sarnott@rotman-baycrest.on.ca (S.R. Arnott). For example, the abrupt appearance of an object in the

0926-6410/01/$ – see front matter 2001 Elsevier Science B.V. All rights reserved.PI I : S0926-6410( 01 )00066-0

384 S.R. Arnott et al. / Cognitive Brain Research 12 (2001) 383 –395

periphery will only capture attention if the observer is 2.1. Methodsearching for a target that is uniquely defined by an abruptonset. The contingency hypothesis has also been shown to 2.1.1. Participantshold true when targets are uniquely defined by color, or Twelve right-handed young adults (18–30 years old;apparent motion [13,15]. mean age, 22.6; five males) participated in this experiment.

One implication of a ‘set’ theory like the contingency All had normal or corrected-to-normal vision. Volunteershypothesis is that the processing of irrelevant cues can be were remunerated for their participation and all providedmodulated by task instruction. Behavioral measures how- their informed consent according to University of Torontoever, only provide indirect evidence. A more direct way of and the Baycrest Center for Geriatric Care guidelines.measuring the influence of a cognitive set on the process-ing of irrelevant stimuli is to record event-related po- 2.1.2. Stimuli and tasktentials (ERPs). By comparing ERP amplitudes elicited by The stimuli and task were similar to those used inirrelevant cues as a function of task instruction, inferences Experiment 3 of Folk et al. [13]. The displays consisted ofcan be made about the way in which behavioral goals five light grey (IBM color 8) squares on a monitor; one ininfluence neural activity. Visual evoked potentials are the center of the screen, and the remaining four located atcharacterized by a series of positive and negative waves the 12, 3, 6 and 9 o’clock positions (see upper panel ofthat are labeled according to their occurrence. For exam- Fig. 1). Each square subtended a visual angle of 1.18.ple, P1 refers to the first large positive wave following Peripheral boxes were centered 58 from screen center.stimulus onset, whereas N1 refers to the first occurring Participants were asked to focus on the center box through-negative deflection. Though both components are affected out the experiment. Eye movement was monitored usingby attention, the N1 has proven to be especially sensitive the EEG from the lateral eye electrodes. A trial began withto non-spatially directed attentional manipulations, being a fixation display of the five boxes. After 500 ms, thelarger when stimuli are predictable versus nonpredictable, center box flashed off for 100 ms warning the participantas well as being larger over contralateral occipital hemi- of the upcoming trial. A 50-ms cue stimulus then high-spheres when subjects attend to targets based on visual lighted one of the four peripheral boxes following afeatures such as location, luminance or color [26,28,29]. A random duration of 1000, 1100, 1200, 1300 or 1400 ms.recent study provided strong support for the notion that the This cue consisted of four small circles, each subtending aN1 reflects stimulus discrimination rather than arousal or visual angle of 0.368 around the periphery of each of themotor preparation processes [50]. Importantly, the ob- box’s four sides. Each circle was centered approximatelyserved enhancement was the same for color and form 0.38 from its respective box side. Circles were white (IBMdiscriminations, supporting the claim that the N1 reflects color 15) against a black (IBM color 0) background.discrimination in general as opposed to mere pattern The 50-ms target display was presented after a randomrecognition. inter-stimulus interval (ISI) of either 100 or 200 ms. In the

In the present study, brain activity was recorded from Onset target display trials, the display consisted of oneparticipants while they performed a task replicating that of white character (target) randomly appearing in the centerFolk et al. [13]. If the contingent orienting hypothesis is of one of the four peripheral boxes. This character wasinstantiated in early visual processes, then the ERP wave- either an 3 or an 5 symbol, subtending a visual angle ofform evoked by the cue should be modulated by the 0.578. In the Color target display trials, the displaycognitive set that is adopted. Because the task was one of consisted of one bright red (IBM color 12) characterdiscrimination, we were particularly interested in the (target) and three white characters appearing in the fouroccipital N1 component. It was expected that this wave- peripheral boxes. Two of these characters were 3 symbolsform would be enhanced during the block where the cue and two were 5 symbols. The observer’s task was toand target were of the same type compared to the block identify the one unique (i.e. red) item. After the target waswhere their relevant attributes differed (i.e. a comparison identified, there was a 500-ms delay before the start of theof the attentional capturing block versus those blocks next trial.where attention was not captured). Behaviorally, weexpected to replicate the contingent orienting findings of 2.1.3. ProcedureFolk et al. [13]. Participants were seated in front of a computer monitor

in a dimly lit room. A chin rest stabilized the head 40 cmfrom the screen. Participants were instructed to, as quickly

2. Experiment 1: attentional set for abrupt onsets and as accurately as possible, press the z key on thekeyboard with their left index finger if the target was an 3

Experiment 1 examined the effect of an attentional set symbol and to press the / key with their right index fingerfor onset or color on the processing of an irrelevant onset if the target was an 5. Participants were also told that thecue. In this experiment, attentional capture of the onset cue cue that highlighted one of the boxes prior to the targetshould only occur in the context of the onset target. display provided no information as to the upcoming

S.R. Arnott et al. / Cognitive Brain Research 12 (2001) 383 –395 385

Fig. 1. Experimental design for Experiments 1 (upper panel) and 2 (lower panel). The stimuli were white against a black background. The gray items inthe cue and target displays were presented as red.

location of the target symbol, and that they should (ipsilateral or contralateral brain hemisphere to the visualtherefore ignore it. After receiving instructions on either stimulus) and Electrode site. Behavioural data were ana-the Onset or the Color target display (order of target lyzed for mean correct RT and Accuracy. Event-relateddisplay was blocked and counterbalanced across particip- potential data were analyzed according to (1) transientants), ten practice trials were given. Participants then effects on the cue (baselining 2200 to 0 ms prior to cuecompleted 256 experimental trials (a brief break was onset) and (2) baseline shifts (baselining 21000 to 2800provided after 128 trials) for one of the two conditions. ms prior to cue onset). Greenhouse–Geisser corrections forWhen finished, participants were given new instructions multiple comparisons and violations of sphericity werefor the other type of target display and, after a brief break, employed when appropriate using epsilon (e). Significantcompleted 256 trials of the other target type. Participants values were based on P values of 0.05 or less.then rested before repeating the entire 512 trials. Incorrect,anticipatory (,100 ms post-onset), or delayed (.1500 ms 2.1.5. EEG recordingpost-onset) responses were signaled by a 100 ms, 1000 Hz Electrophysiological signals were recorded continuouslyfeedback tone played over speakers at a sound pressure (NEUROSCAN software) with a sampling rate of 250 Hz fromlevel of approximately 60 dB SPL. an Electro-Cap with 58 tin electrodes including those

corresponding to the ten–twenty system [54]. Vertical and2.1.4. Data analysis horizontal eye movements were monitored with electrodes

Variables used in the analyses included Target type placed at the outer canthi and superior and inferior orbits.(color or onset targets), Cue-Target Position (Same or Six additional off-cap electrodes were placed at the leftDifferent), cue Location (upper 12 o’clock, right 3 o’clock, and right mastoids, at the left and right temporal-mandibu-bottom 6 o’clock and left 9 o’clock positions), ISI between lar joint and over the left and right zygomatic arch.cue and target displays (100 or 200 ms), Hemisphere Electrophysiological signals were amplified (gain of 2500)

386 S.R. Arnott et al. / Cognitive Brain Research 12 (2001) 383 –395

and filtered (bandpass 0.05–50 Hz) via Syn Amps. Duringacquisition, all electrodes were referenced to Cz. Afteracquisition, all data were re-referenced to a commonaverage reference and the Cz electrode was then reinstated.

The ERPs to the cues were averaged offline andseparated according to block, stimulus location, ISI andelectrode. The epoch extended over 2200 ms (pre-stimulus) to 250 ms (poststimulus) in one analysis and21000 to 150 ms in a second analysis. ERPs were digitallylowpass filtered to attenuated frequencies above 15 Hz.Trials contaminated by excessive peak-to-peak deflection(i.e. .100 mV or ,2100 mV) at non-eye electrode siteswere excluded from the ERP average. The overall propor-tion of rejected trials was 2.5%.

In each individual average, the ocular (electro-oculo-gram (EOG)) artefacts (e.g. blinks and lateral eye move-ments) not removed by the artefact rejection criteria werecorrected using ocular source components [35]. Thisprocess required a separate EOG calibration recording,which used the same electrode montage and was com-pleted during the same experimental session. During thiscalibration, participants made saccades to a fixation point Fig. 2. Mean correct reaction time for onset cue-target location (same or

different). Error bars represent the standard error of the mean.that alternated between the center and the edge of thescreen, separately in the up, down, right and left directions.As well, intermittent blinking was recorded. This allowed Critically, there was an interaction between Target typefor the creation of an ocular data set by concatenating and Cue-Target Position [F(1,11)513.22, P,0.005] (seeaverage recordings of each of the saccades and the blinks. Fig. 2). In the color condition, RTs did not differ accordingA principal component analysis of this data set provided a to where the cue had been located (different location5483set of components that represented the variance related to ms, same location5482 ms; P50.99), whereas in the onsetthe eye movements. Those components that explained block, same locations resulted in faster RTs than didmore than 1% of the variance and were specifically related different locations (423 and 452 ms, respectively, P,

to the EOG waveforms were used as source components to 0.05). The only other interaction was between Targetsubtract EOG contamination from the average ERPs. Location and Cue-Target Position [F(3,33)54.95, P,0.05,

e50.698].2.2. Results and discussion

2.2.2. Accuracy2.2.1. Reaction time Accuracy was high overall, with a mean hit rate of

A four-way within-observer analysis of variance (96.9%). Early (,100 ms) and late (.1500 ms) errors(ANOVA) was performed on the mean correct RT data comprised 0.02% of the total trials. Again, a within-using the factors of ISI (100 or 200 ms), Target type (color observer ANOVA was used with the same factors as above.or onset target display), Target Location (top, right, Accuracy was higher for the onset condition (mean hit ratebottom, or left) and Cue-Target Position (same or differ- 97.7%) than for the color condition (mean hit rate 96.1%)ent). Overall, participants had faster RTs for onset target [F(1,11)59.84, P,0.01]. As expected, accuracy wasdisplays (mean 438 ms) than for color target displays higher for targets preceded by cues in the same location(mean 483 ms) [F(1,11)5100.92, P,0.001]. Other main (97.3%) than for those in different locations (96.5%)effects included ISI, with 200 ms ISI trials being re- [F(1,11)55.59, P,0.05]. There were no other significantsponded to faster (mean 466 ms) than 100 ms ISI trials accuracy effects, although there was a trend for an(mean 455 ms) [F(1,11)551.87, P,0.001] and Cue-Target interaction between target Location and Cue-Target Posi-Position with targets occurring in the same location as the tion [F(3,33)52.19, P50.066, e50.760].cues being responded to faster (mean 453 ms) than targetspreceded by cues at a different location (mean 468 ms) 2.2.3. Transient ERP effects[F(1,11)516.59, P,0.01]. There was also a main effect of Due to the unique anatomical mapping of upper, lowerTarget Location [F(3,33)53.85, P,0.05, e50.745] with and lateral visual fields in striate cortex [1,22], analysis ofthe target located in the right box being responded to faster the transient cue ERPs was carried out separately for eachthan those located in the bottom and top locations (8.8 and cue location. As well, only the 200 ms ISI trials were13.1 ms, respectively, P,0.01). analyzed as these enabled us to isolate cue N1 components

S.R. Arnott et al. / Cognitive Brain Research 12 (2001) 383 –395 387

without interference from the target display. Evoked than ipsilateral occipital lobe. This was quantified bypotentials to cue stimuli were characterized by a positive– taking the mean amplitude voltage over a 20 ms windownegative complex occurring over posterior regions (Fig. 3). of 165–185 ms at electrode sites to the left and right of the

occipital midline (O1 and O2). A three-way ANOVA with2.2.3.1. N1 for lateral cues. For right and left cues, the Target type (onset and color), Cue Location (right or left)prominent N1 deflection peaked approximately 175 ms and Hemisphere (contralateral and ipsilateral brain hemi-after stimulus onset and was larger over the contralateral sphere to the hemifield location of the cue) yielded a main

Fig. 3. Posterior topographic view of group (n512) mean ERPs to abrupt onset cues located at left and right (transposed to appear at left) (upper panel),bottom (middle panel), and top (lower panel) cue locations during color (solid) and onset (dashed) blocks. Corresponding cue schematics are shown to theleft of each ERP display. The arrow on the upper panel highlights the N1 component. Significant N1 differences are indicated by circles (P,0.05). 200-msinter-stimulus interval trials only.

388 S.R. Arnott et al. / Cognitive Brain Research 12 (2001) 383 –395

effect of Hemisphere [F(1,11)530.86, P,0.001], with the that by promoting an attentional set to abrupt onsets,N1 being more negative over the hemisphere contralateral attentional capture to onset cues would occur during the(mean 21.20 mV) rather than ipsilateral (mean 20.90 mV) onset but not the color block. Furthermore, even thoughto the stimulus. The interaction between Hemisphere and the irrelevant cue was identical in both blocks, the transientTarget type was also significant [F(1,11)512.00, P,0.01]. ERPs demonstrated an N1 enhancement over sensory areas

´Scheffe’s tests revealed that the contralateral electrode was during the onset block. Also as anticipated, the N1 effectmore negative during the onset condition (22.78 mV) was small. Before accepting the explanation that theversus the color condition (22.10 mV) (P,0.01) but that observed capture was the result of top-down modulation ofthe ipsilateral electrodes did not differ between conditions. sensory areas by an attentional set, we attempted to

replicate the findings under somewhat different conditions.2.2.3.2. N1 for bottom cues. The N1 component for the Specifically, we repeated the experiment using a cuebottom cue occurred slightly later over occipital sites and display that shared a feature uniquely relevant to targets inwas quantified by a mean voltage measurement over a the color block rather than the onset block. We expected torange of 180–200 ms post cue onset. The Target type by observe both attentional capture in the behavioral data andElectrode ANOVA on this interval over posterior elec- an N1 enhancement during the color as oppose to the onsettrodes (TP9, TP10, CB1, CB2, O1, O2, Oz and Iz) block. As an additional test of the modulation hypothesis,indicated a main effect of Target type [F(1,11)55.12, we expected that the N1 voltage topography might differP,0.05], with the N1 being larger for cues presented slightly from Experiment 1, targeting unique visual areasduring the onset (22.28 mV) than in the color (21.31 mV) that process color as oppose to abrupt onset [2,8,19].condition. There was no interaction between Target typeand Electrode [F(7,77)50.94, e50.33].

3. Experiment 2: attentional set for color2.2.3.3. N1 for top cues. The N1 component for the topcues reversed in polarity over posterior sites as expected.

Experiment 2 examined the effect of an attentional setReversals for upper and lower visual field stimuli have

for onset or color targets on the processing of an irrelevantbeen noted before and are most likely a consequence of

color cue. In this experiment, attentional capture of theretinopic mapping and the inversion of neuronal popula-

color cue should only occur in the context of the colortions below and above the calcarine fissure [22,30,44].

target.There was however, no significant difference in N1amplitude elicited by the cue during the onset versus colortarget blocks. 3.1. Method

2.2.4. Top-down processing and baseline shifts3.1.1. Participants

The role of top-down contributions to the capture effectTwelve young adults participated (21–30 years old;

was evaluated by examining the one-second epoch leadingmean age 26.3 years; seven males). Eight had participated

up to the cue onset. This analysis allowed us to examinein the first experiment. All had normal or corrected-to-

whether the observed N1 modulations over occipital areasnormal vision. Volunteers were remunerated for their

reflected transient changes in neural activity or slowerparticipation and all provided their informed consent

changes that would have affected the prestimulus baseline.according to University of Toronto and the Baycrest

Because participants had no way of knowing the upcomingCenter for Geriatric Care guidelines.

location of the cue or how long the ISI between cue andtarget would be, all trials were collapsed into two averages:one for the Onset block and one for the Color block (Fig. 3.1.2. Stimuli and procedure4). Apart from the cue display, the stimuli, task and

Occipital electrode sites (O1, Oz and O2) were mea- recording of ERPs were the same as in Experiment 1. Insured at 200–150, 150–100, 100–50 and 50–0 ms inter- the cue display, four 50-ms cue stimuli simultaneouslyvals prior to cue onset. The Target type by Electrode highlighted each of the four peripheral boxes (see lowerANOVAs did not reveal any differences in Target type, panel of Fig. 1). These cues each consisted of four smallsupporting the idea that the N1 amplitude differences were circles, each subtending a visual angle of 0.368 around thestimulus related. However, there was an effect of Target periphery of each of the box’s four sides. Each circle wastype at right fronto–central sites. Specifically, 50 ms prior centered approximately 0.38 from its respective box side.to the cue there was an increased negativity in the onset The circles were white around three of the peripheralrelative to the color block over the right central sites of boxes and red around the remaining peripheral box. TheFCz, FC2, Cz, C2, C6, CPz and Pz [F(1,11)56.82, P, location of this red cue was random from trial to trial.0.05]. Participants were again instructed that the cues provided

The results of Experiment 1 confirmed initial predictions no information as to the upcoming target location.

S.R. Arnott et al. / Cognitive Brain Research 12 (2001) 383 –395 389

Fig. 4. Top view of brain activity during the 1000-ms interval preceding cue onset during color (solid) and onset (dashed) blocks. Circles indicatesignificant differences between the Target Types (P,0.05).

3.2. Results and discussion faster, respectively, P values ,0.001, 0.01 and 0.05,respectively).

3.2.1. Reaction time As expected, there was an interaction between TargetA four-way ANOVA was performed on the mean correct type and Cue-Target Position [F(1,11)556.70, P,0.001]

RT data using ISI (100 ms or 200 ms), Target type (color (Fig. 5). In the onset condition, RTs did not differor onset target display), Target Location (top, right, according to where the cue had been located (differentbottom, or left) and Cue-Target Position (same or differ- location5446 ms, same location5445 ms; P50.99),ent) as factors. Overall, participants again had faster RTs whereas in the color block same locations resulted in fasterfor onset target displays (mean 446 ms) than for color RTs than did different locations (P,0.001, 464 and 513target displays (mean 488 ms) [F(1,11)525.18, P,0.001]. ms, respectively). Other interactions included ISI andOther main effects included ISI, with 200 ms ISI trials Target type [F(1,11)54.71, P,0.05] and ISI and Positionagain being responded to faster (mean 474 ms) than 100 [F(3,33)57.25, P,0.01 e50.755].ms ISI trials (mean 460 ms) [F(1,11)519.24, P,0.01] andCue-Target Position with targets occurring in the samelocation as the cues being responded to faster (mean 454 3.2.2. Accuracyms) than targets preceded by cues at a different location Accuracy was again high overall, (mean Hit rate5

(mean 480 ms) [F(1,11)541.81, P,0.001]. There was also 94.3%). Early (,100 ms) and late (.1500 ms) errorsa main effect of Target Location [F(3,33)510.12, P, comprised less than 0.01% of the total trials. A four-way0.001, e50.863] with targets located in the right position ANOVA using ISI (100 or 200 ms), Target type (color orbeing responded to faster than targets located in the onset target display), Location of target (top, right, bottom,bottom, top and left locations (19.5, 19.6 and 10.1 ms or left) and Cue-Target Position (different or same) as

390 S.R. Arnott et al. / Cognitive Brain Research 12 (2001) 383 –395

Experiment 1) who demonstrated Target type effectsopposite to those predicted. Running this same ANOVAwithout those participants revealed a Target type effect[F(1,8)59.11, P,0.05], with the N1 to the color cue beinggreater in the color (25.86 mV) than in the onset (24.43mV) conditions.

3.2.3.3. N1 for top cues. The N1 for cue displays with thetop cue colored appeared slightly greater over posteriorsites (TP9/10, CB1/2, O1/2, Oz and Iz) during the colorblock, however an ANOVA did not reveal a significantdifference between Target types [F(1,11)50.50]. Omittingthe three participants discussed above improved this, butthe effect did not reach significance [F(1,8)53.89]. Otherstudies have also reported smaller occipital activation inresponse to upper relative to lower visual field [36,41].Possible reasons include stronger synchronicity in neuronalfiring in response to lower visual field stimuli [36].

3.2.4. Top-down processing and baseline shiftsTo test whether the N1 effects were stimulus related as

Fig. 5. Mean correct reaction time for color cue-target location (same or in Experiment 1 or the result of a baseline shift, occipitaldifferent). Error bars represent the standard error of the mean. electrode sites (O1, Oz and O2) were measured at 200–

150, 150–100, 100–50 and 50–0 ms intervals prior to cuefactors was performed on the Hit accuracy data. There onset. Again, there were no differences between the targetwere no significant effects or interactions. types, thus favoring the former explanation.

In addition, we again observed an enhanced negativity3.2.3. Transient ERP effects during the attentional capturing blocks just prior to the cue

Although the cue stimulus in Experiment 2 occurred in onset. However, the modulation appeared to be moreall quadrants of the visual field, it was the unique red color lateral than in Experiment 1. An ANOVA confirmed this asthat was predicted to have captured attention, thus evoked a mean amplitude measurement did not demonstrate apotentials were analyzed according to which quadrant the Target type effect when the same electrode sites used inred cue occurred: lateral, lower and upper visual fields. As Experiment 1 were measured. An ANOVA over morein Experiment 1, only the 200 ms ISI cues were analyzed. lateral parietal / temporal areas of the right hemisphereThese transients are displayed in Fig. 6. (TP8/10, CB2, P6/8 and CP6) did demonstrate enhanced

negativity during the attentional capturing (color) block3.2.3.1. N1 for lateral cues. The N1 peak to the cue [F(1,11)55.82, P,0.05] (Fig. 7).displays with a uniquely colored lateral box occurred at180 ms. A four-way ANOVA for the 170–190 ms intervalusing Target type, Cue Location, Hemisphere and Elec- 4. General discussiontrode (O1/2 and PO3/4) yielded a significant interactionbetween Target type and Hemisphere [F(1,11)55.02, P, The present ERP results suggest that when an attentional

´0.05]. A Scheffe’s test revealed that the N1 to the cue was set is adopted, attentional capture is the result of sensorygreater in the color (25.56 mV) than the onset (25.11 mV) brain areas being gated to respond preferentially to target-condition over the hemisphere contralateral to the cue relevant features. More precisely, even though the irrele-position (P,0.05). vant cue was identical in both blocks, we recorded a small

but reliable N1 enhancement over occipital sites to an3.2.3.2. N1 for bottom cues. A mean voltage measure- onset cue (Experiment 1) during an attention-capturingment over a range of 180–200 ms post cue onset for cue onset target block rather than during a non-attentiondisplays containing a uniquely colored cue at the bottom capturing color target block. In contrast, when irrelevantlocation was carried out. The Target type by Electrode color cues were used (Experiment 2), the N1 cue enhance-ANOVA on this interval over posterior electrodes (TP9/ ment reversed, being greatest during the color (attention-10, CB1/2, O1/2, Oz and Iz) did not indicate a main effect capturing) rather than the onset (non-capturing) targetof Target type [F(1,11)50.50]. However, further data blocks. Importantly, these occipital N1 enhancements wereexploration revealed that this was in large part due to data shown not to be due to a prestimulus baseline shift infrom three subjects (none of which had participated in neural activity (e.g. arousal). These N1 changes must

S.R. Arnott et al. / Cognitive Brain Research 12 (2001) 383 –395 391

Fig. 6. Posterior topographic view of group (n59) mean ERPs to colored cues located at left and right (transposed to appear at left) (upper panel), bottom(middle panel), and top (lower panel) cue locations during color (solid) and onset (dashed) blocks. Corresponding cue schematics are shown to the left ofeach ERP display. The arrow on the upper panel highlights the N1 component. Significant N1 topographic differences are indicated by circles (P,0.05)200-ms inter-stimulus interval trials only.

therefore reflect the influence of top-down processes. share a target-relevant feature. Although we do not proposeConsistent with this, the visual N1 component has been that attentional capture is a purely top-down process as the

1recently implicated as an index of a discrimination process contingency hypothesis implies , the present results sug-within the focus of attention [50]. gest that when a situation demands a top-down, attentional

The results are compatible with the contingent involun-1tary orienting hypothesis, which posits that stimuli only There do seem to be instances of purely bottom-up, stimulus-driven

capture attention when they occur in situations where they attentional capture (see [47,48]).

392 S.R. Arnott et al. / Cognitive Brain Research 12 (2001) 383 –395

Fig. 7. Top view of brain activity during the 1000 ms interval preceding cue onset in Experiment 2 during color (solid) and onset (dashed) blocks. Circlesindicate significant differences between the Target Types (P,0.05).

set (e.g. a search strategy for a specific feature) sensory with their proposed top-down temporal delay. Moreover,areas are modulated to respond preferentially to that the larger and broader N1 waves for the distractors sharingspecific feature. the relevant feature is also in line with a longer disengage-

Recently, an alternative to the contingent orienting ment process. However, this type of N1 effect could alsohypothesis has been put forward by Theeuwes et al. [46]. be explained by positing that higher-order sensory areasThey suggest that salient stimuli in the visual field always are modulated throughout the entire block (i.e. an atten-capture attention regardless of attentional set. Only after tional set) and only exert their influence when visualtop-down processes are brought to bear on the distractor (a processing reaches this level.process that is believed to take at least 150 ms from There is considerable evidence supporting the notionstimulus onset) is one able to disengage from that stimulus. that the present findings are due to early sensory modula-Thus, a distractor that is clearly different from the target tion by attention to features (see [23] for a review). For(e.g. a red cue versus an abruptly onsetting white target in example, single-cell recordings in monkey V1, V2 and V4the present experiment) is easily dismissed using top-down cortices have demonstrated that visual neuronal responsesprocesses, freeing up the attentional system to engage are enhanced for stimuli possessing cued features (e.g.attention elsewhere (i.e. on the target). Conversely, a [27]). Moreover, when the cued feature switches mid-waydistractor that is harder to distinguish from a target (e.g. a through a block of trials, the neuron’s response rapidlyred cue versus a red target) is more difficult to disengage switches, responding to stimuli sharing the now relevantfrom and as a result, demonstrates cue-target position RT feature, with previous ‘target’ stimuli eliciting responseseffects (i.e. attentional capture). Although the present no greater than other non-target stimuli. These results haveexperiment was not designed to specifically test this been demonstrated in extrastriate areas for color [32],hypothesis, the timing of our N1 cue effects is consistent orientation [20] and direction of motion [10]. Corroborat-

S.R. Arnott et al. / Cognitive Brain Research 12 (2001) 383 –395 393

ing evidence is also provided by imaging studies (see ingly, both experiments showed a bilateral phasic negativi-[7,21,33]). ty over frontal areas for both conditions approximately

Whatever the mechanism, it is clear that top-down 900–600 ms before the irrelevant cue’s onset. Whether thisprocessing exerts its influence on visual areas at a very reflects the source of top-down modulation is difficult toearly stage of stimulus analysis. Because the spatial say as the latency also overlapped with electrical responsesresolution of ERPs is relatively poor in comparison to to the blink of the fixation point. Notably though, atten-other imaging techniques, especially at small signal-to- tional capturing blocks in both experiments demonstratednoise ratios and because of the inverse problem in ERPs an enhanced negativity relative to the non-capturing blocks(i.e. there is no unique solution as to the location of during the last 50 ms before the onset of the cue. Thoughunderlying generator(s) based on a given topographic both right sided, the voltage topographies of these differ-map), whether or not the top-down influences targeted ences were localized over different areas of the scalp beingdifferent parts of the visual cortex cannot stated with any situated predominately over fronto–central and posteriordegree of certainty. That said, several ERP studies do temporal sites during the ‘onset’ (Experiment 1) andsuggest that attention to different visual features can ‘color’ (Experiment 2) attentional set experiments, respec-modulate different areas of visual cortex [8,30]. Of par- tively. It is interesting to note that these areas coincideticular relevance are single-cell recordings in the monkey with those reported to be specialized for processing onsetthat have associated abrupt onsets with activity in the and color information. This could suggest that in blockslateral intraparietal area [19] whereas color processing where the irrelevant cue was more similar to the sub-seems to be localized in the inferior temporal cortex and sequent target block, more resources were devoted to thesubsequent fusiform and lingual gyri [2]. appropriate feature processing cortical area (i.e. spatial or

Much of the evidence available suggests that top-down object identification areas). This would be consistent withmodulation signals originate in the anterior frontal cortex, both the hypothesis of Theeuwes et al. [46] that attentionalwith some studies also implicating (predominately right- capture is the result of an automatic, bottom-up capturesided) parietal and temporal cortices [4,9,16,39,40]. For followed shortly by a top-down discrimination process asexample, when observers are given a visual task whose well as the contingent involuntary orienting hypothesis ofstimuli are presented at varying rates, regional cerebral Folk and co-workers [13,15]. More research carefullyblood flow measurements demonstrate activity in dorsola- examining the predictions of these two competing hypoth-teral prefrontal cortex (DLPFC) that is stimulus and eses will be required before definitive conclusions can beresponse independent [40]. As well, observers carrying out reached.Stroop tasks demonstrate increased fMRI activity in thissame region as demand on attention increases (i.e. neutralversus incongruent trials) [4]. Lateral prefrontal neurons in

Acknowledgementsthe monkey have shown enhanced activity during the delayof an object match-to-sample task [39]. It is well docu-

This research was supported by an Ontario Graduatemented that both the superior longitudinal fasiculus andScholarship to S.R.A., Natural Sciences and Engineeringinferior occipital-frontal fasiculus connect DLPFC effer-Research Council of Canada grants to J.P. and C.A. and aently and afferently with occipital cortex [42] therebyTanenbaum postdoctoral fellowship to D.I.S.providing a direct connection for modulating influences.

Such distributed networks have also been shown to beselectively influenced by parietal and temporal cortices[49]. The parietal cortex has been shown to be selectively Referencesactive during spatial attention [6] with perhaps some areasbeing involved in general attention not requiring constant

[1] C.J. Aine, S. Supek, J.S. George, D. Ranken, J. Lewine, J. Sanders,goal-directed updating [51]. In contrast, the temporal E. Best, W. Tiee, E.R. Flynn, C.C. Wood, Retinotopic organizationcortex seems to be important for object identification of human visual cortex: departures from the classical model, Cereb.

Cortex. 6 (1996) 354–361.[17,40,45]. Although it is not yet exactly clear why, there[2] L. Anllo-Vento, S.J. Luck, S.A. Hillyard, Spatio-temporal dynamicsdoes seem to be a specialized role for the right hemisphere

of attention to color: evidence from human electrophysiology, Hum.in sustained attention [31,34,37].Brain Mapp. 6 (1998) 216–238.

In the current study, there was clear evidence of an [3] W.F. Bacon, H.E. Egeth, Overriding stimulus-driven attentionalincreasing negativity over central scalp sites as the time to capture [see comments], Percept. Psychophys. 55 (1994) 485–496.cue onset approached (Figs. 4 and 7). Undoubtedly this [4] M.T. Banich, M.P. Milham, R.A. Atchley, N.J. Cohen, A. Webb, T.

Wszalek, A.F. Kramer, Z.-P. Liang, V. Barad, D. Gullett, C. Shah, C.reflects, in part, the contribution of attention and motorBrown, Prefrontal regions play a predominate role in imposing anpreparations to the upcoming cue and target (i.e. aattentional ‘set’: evidence from fMRI, Cogn. Brain Res. 10 (2000)

readiness potential; [5,25]) as well as phasic alertness from 1–9.subcortical areas such as the reticular formation of the [5] C.H.M. Brunia, Waiting in readiness: gating in attention and motorthalamus or the intralaminar thalamic nuclei [24]. Interest- preparation, Psychophysiology 30 (1993) 327–339.

394 S.R. Arnott et al. / Cognitive Brain Research 12 (2001) 383 –395

[6] C.L. Colby, M.E. Goldberg, Space and attention in parietal cortex, [28] S.J. Luck, S.A. Hillyard, M. Mouloua, M.G. Woldorff, V.P. Clark,Annu. Rev. Neurosci. 22 (1999) 319–349. H.L. Hawkins, Effects of spatial cuing on luminance detectability:

[7] M. Corbetta, F.M. Miezin, S. Dobmeyer, G.L. Shulman, S.E. psychophysical and electrophysiological evidence for early selec-Petersen, Selective and divided attention during visual discrimina- tion, J. Exp. Psychol. Hum. Percept. Perform. 20 (1994) 887–904.tions of shape, color and speed: functional anatomy by positron [29] G.R. Mangun, S.A. Hillyard, Modulations of sensory-evoked brainemission tomography, J. Neurosci. 11 (1991) 2383–2402. potentials indicate changes in perceptual processing during visual–

[8] F. Cortese, L.J. Bernstein, C. Alain, Binding visual features during spatial priming, J. Exp. Psychol. Hum. Percept. Perform. 17 (1991)high-rate serial presentation, NeuroReport 10 (1999) 1565–1570. 1057–1074.

[9] J.T. Coull, Neural correlates of attention and arousal: insights from [30] G.R. Mangun, S.A. Hillyard, Mechanisms and models of selectiveelectrophysiology, functional neuroimaging and psychopharmacolo- attention, in: G.R. Mangun, S.A. Hillyard (Eds.), Mechanisms andgy, Prog. Neurobiol. 55 (1998) 343–361. Models of Selective Attention, Oxford University Press, Oxford,

[10] V.P. Ferra, K.K. Rudolph, J.H. Maunsell, Response of neurons in the 1996, pp. 40–85.parietal and temporal visual pathways during a motion task, J. [31] M.M. Mesulam, Spatial attention and neglect: parietal, frontal andNeurosci. 14 (1994) 6171–6186. cingulate contributions to the mental representation and attentional

[11] C.L. Folk, S. Annett, Do locally defined feature discontinuities targeting of salient extrapersonal events, Philos. Trans. R. Soc.capture attention?, Percept. Psychophys. 56 (1994) 277–287. Lond. B Biol. Sci. 354 (1999) 1325–1346.

[12] C.L. Folk, R. Remington, Selectivity in distraction by irrelevant [32] B.C. Motter, Neural correlates of feature selective memory andfeatural singletons: evidence for two forms of attentional capture, J. pop-out in extrastriate area V4, J. Neurosci. 14 (1994) 2190–2199.Exp. Psychol. Hum. Percept. Perform. 24 (1998) 847–858.

[33] K.M. O’Craven, B.R. Rosen, K.K. Kwong, A. Treisman, R.L.[13] C.L. Folk, R.W. Remington, J.C. Johnston, Involuntary covert

Savoy, Voluntary attention modulates fMRI activity in human MT-orienting is contingent on attentional control settings, J. Exp.

MST, Neuron 18 (1997) 591–598.Psychol. Hum. Percept. Perform. 18 (1992) 1030–1044.

[34] J.V. Pardo, P.T. Fox, M.E. Raichle, Localization of a human system[14] C.L. Folk, R.W. Remington, J.C. Johnston, Contingent attentional

for sustained attention by positron emission tomography, Nature 349capture: a reply to Yantis (1993), J. Exp. Psychol.: Hum. Percept.

(1991) 61–64.Perform. 19 (1993) 682–685.[35] T.W. Picton, P. van Roon, M.L. Armilio, P. Berg, N. Ille, M. Scherg,[15] C.L. Folk, R.W. Remington, J.H. Wright, The structure of attentional

The correction of ocular artifacts: a topographic perspective, Clin.control: contingent attentional capture by apparent motion, abruptNeurophysiol. 111 (2000) 53–65.onset and color, J. Exp. Psychol. Hum. Percept. Perform. 20 (1994)

[36] K. Portin, S. Vanni, V. Virsu, R. Hari, Stronger occipital cortical317–329.activation to lower than upper visual field stimuli. Neuromagnetic[16] C. Frith, R.J. Dolan, Brain mechanisms associated with top-downrecordings, Exp. Brain Res. 124 (1999) 287–294.processes in perception, Philos. Trans. R. Soc. Lond. B Biol. Sci.

[37] M.I. Posner, S.E. Petersen, The attention system of the human brain,352 (1997) 1221–1230.Annu. Rev. Neurosci. 13 (1990) 25–42.[17] J.M. Fuster, R.H. Bauer, J.P. Jervey, Functional interactions between

[38] J. Pratt, A.B. Sekuker, J. McAuliffe, The role of attentional set oninferotemporal and prefrontal cortex in a cognitive task, Brain Res.attentional cueing and inhibition of return, Visual Cognit. 8 (2001)330 (1985) 299–307.33–46.[18] B.S. Gibson, E.M. Kelsey, Stimulus-driven attentional capture is

[39] G. Rainer, W.F. Asaad, E.K. Miller, Selective representation ofcontingent on attentional set for displaywide visual features, J. Exp.relevant information by neurons in the primate prefrontal cortex,Psychol. Hum. Percept. Perform. 24 (1998) 699–706.Nature 393 (1998) 577–579.[19] J.P. Gottlieb, M. Kusunoki, M.E. Goldberg, The representation of

[40] G. Rees, R. Frackowiak, C. Frith, Two modulatory effects ofvisual salience in monkey parietal cortex, Nature 391 (1998) 481–attention that mediate object categorization in human cortex, Science484.

[20] P.E. Haenny, P.H. Schiller, State dependent activity in monkey 275 (1997) 835–838.visual cortex. I. Single cell activity in V1 and V4 on visual tasks, [41] N. Rubin, K. Nakayama, R. Shapely, Enhanced perception ofExp. Brain. Res. 69 (1988) 225–244. illusory contours in the lower versus upper visual hemifields,

[21] J.V. Haxby, B. Horwitz, L.G. Ungerleider, J.M. Maisog, P. Pietrini, Science 271 (1996) 651–653.C.L. Grady, The functional organization of human extrastriate [42] P.A. Salin, J. Bullier, Corticocortical connections in the visualcortex: a PET-rCBF study of selective attention to faces and system: structure and function, Physiolog. Rev. 75 (1995) 107–154.locations, J. Neurosci. 14 (1994) 6336–6353. [43] D.J. Simons, Attentional capture and inattentional blindness, Trends

[22] D.A. Jeffreys, J.G. Axford, Source locations of pattern-specific Cogn. Sci. 4 (2000) 147–155.components of human visual evoked potentials. II. Component of [44] W. Skrandies, The upper and lower visual field in man: elec-extrastriate cortical origin, Exp. Brain Res. 16 (1972) 22–40. trophysioloical and functional differences, in: W. Skrandies (Ed.),

[23] S. Kastner, L.G. Ungerleider, Mechanisms of visual attention in the The Upper and Lower Visual Field in Man: Electrophysioloical andhuman cortex, Annu. Rev. Neurosci. 23 (2000) 315–341. Functional Differences, Springer-Verlag, New York, 1987, pp. 1–93.

´[24] S. Kinomura, J. Larsson, B. Gulyas, P.E. Roland, Activation by [45] K. Tanaka, Neuronal mechanisms of object recognition, Science 262attention of the human reticular formation and thalamic intralaminar (1993) 685–688.nuclei, Science 271 (1996) 512–515. [46] J. Theeuwes, P. Atchley, A.F. Kramer, On the time course of

[25] H.H. Kornhuber, L. Deecke, Hirnpotentialanderungen bei Willkur- top-down and bottom-up control of visual attention, in: J. Theeuwes,bewegungen und passiven bewegungen des menschen: P. Atchley, A.F. Kramer (Eds.), On the Time Course of Top-down

¨Bereitschaftspotential und reafferente potentiale, Pflugers Arch. 284 and Bottom-up Control of Visual Attention, Cambridge, 2000, pp.(1965) 1–17. 105–124.

[26] J.J. Lange, A.A. Wijers, L.J. Mulder, G. Mulder, Color selection and [47] M. Turatto, G. Galfano, Color, form and luminance capture attentionlocation selection in ERPs: differences, similarities and ‘neural in visual search, Vision Res. 40 (2000) 1639–1643.specificity’, Biol. Psychol. 48 (1998) 153–182. [48] M. Turatto, G. Galfano, Attentional capture by color without any

[27] S.J. Luck, L. Chelazzi, S.A. Hillyard, R. Desimone, Neural mecha- relevant attentional set, Percept Psychophys. 63 (2001) 286–297.nisms of spatial selective attention in areas V1, V2, and V4 of [49] L.G. Ungerleider, Functional brain imaging studies of corticalmacaque visual cortex, J. Neurophysiol. 77 (1997) 24–42. mechanisms for memory, Science 270 (1995) 769–775.

S.R. Arnott et al. / Cognitive Brain Research 12 (2001) 383 –395 395

[50] E.K. Vogel, S.J. Luck, The visual N1 component as an index of a [53] S. Yantis, J. Jonides, Abrupt visual onsets and selective attention:discrimination process, Psychophysiology 37 (2000) 190–203. evidence from visual search, J. Exp. Psychol. Hum. Percept.

[51] E. Wojciulik, N. Kanwisher, The generality of parietal involvement Perform. 10 (1984) 601–621.in visual attention, Neuron 23 (1999) 747–764. [54] American Electroencephalographic Society, Guidelines for standard

[52] S. Yantis, Stimulus-driven attentional capture and attentional control electrode position nomenclature, J. Clin. Neurophysiol. 8 (1991)settings, J. Exp. Psychol. Hum. Percept. Perform. 19 (1993) 676– 200–202.681.