The dynamics of shifting visuospatial attention revealed by event-related potentials

Anna C. Nobre*, Gillian N. Sebestyen, Carlo Miniussi

University of Oxford, Department of Experimental Psychology, South Parks Road, Oxford OX1 3UD, UK

Received 30 September 1999; received in revised form 17 November 1999; received in revised form 23 November 1999

Abstract

We developed a behavioral task for spatial orienting of attention in which the same physical stimulus cued covert peripheral

shifts of attention to either the left or the right visual ®elds in di�erent conditions. The design enabled us to record the brainactivity engaged during spatial shifts of covert attention that was independent from the physical characteristics of the cueingstimulus using event-related potentials (ERPs). ERPs elicited by foveal cues di�ered according to the predicted target locationstarting ca. 160 ms, and di�erences persisted until the occurrence of the target stimuli. Multiple processes were linked to shifting

spatial attention during the cue-target interval. The earliest e�ects consisted of enhanced negative potentials over the posteriorscalp contralateral to the cued location. Later e�ects were concentrated over the right anterior scalp sites, where activityassociated with shifts to the right visual ®eld elicited larger positive potentials. The results extend our understanding of the

neural system that orients spatial attention by providing valuable information about the temporal dynamics and hemisphericasymmetries of activity within its posterior and anterior regions. 7 2000 Published by Elsevier Science Ltd. All rights reserved.

1. Introduction

The neural system that orients attention selectivelytoward spatial locations in the human brain has beende®ned by extensive neuropsychological (for reviewssee Refs. [27, 38]) and brain-imaging [6, 7, 14, 21, 22,31, 40] investigations. Posterior parietal and frontalpremotor areas form a core axis for visuospatialorienting. The aim of the present experiment was tosupplement the functional anatomical knowledge withinformation about the temporal dynamics of neural ac-tivity in the system for visuospatial orienting, by usingevent-related potentials.

ERPs have been extremely informative in the studyof visuospatial attention, but they have been primarilyused to investigate the modulatory e�ects that selectivevisuospatial attention exerts upon ongoing stimulus

processing. The rich ERP literature has demonstratedthat selective visuospatial attention can in¯uence earlyperceptual aspects of stimulus analysis during tasksinvolving sustained or cued attention [13, 18, 21, 24,39]. In tasks where attention is cued on a trial-by-trialbasis, the modulation of visual processing is optional,and is in¯uenced by whether stimuli at the uncued lo-cations remain relevant for behavioral responses [9, 10,12]. The establishment of modulatory e�ects in visualareas by focusing attention voluntarily upon the pres-entation of an instructive symbolic cue takes a fewhundred milliseconds [29]. Re¯exive orienting of atten-tion toward peripheral stimuli may involve additionalor alternative mechanisms capable of modulatingvisual processing with a fast timecourse [21]. Whetherattention is directed voluntarily or re¯exively, the ear-liest stages of visual processing a�ected seem to be inextrastriate visual areas [5, 17, 21, 24], but later proces-sing in primary visual cortex may also be modulated[25]. Spatial information can determine stimulus selec-tion in parallel with other available discriminable fea-tures such as color or motion, though spatial selection

Neuropsychologia 38 (2000) 964±974

0028-3932/00/$ - see front matter 7 2000 Published by Elsevier Science Ltd. All rights reserved.

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* Corresponding author. Tel.: +44-1865-271388; fax: +44-1865-

310447.

E-mail address: anna.nobre@psy.ox.ac.uk (A.C. Nobre).

may take precedence and have a special role inenabling selection of non-spatial features (e.g. Refs. [2,3, 11, 19, 20]).

Only a few studies have reported the ERPs regis-tered prior to target appearance, triggered by the stim-uli that cue a shift of attention across space (e.g., Refs.[13, 15, 42]). In all cases, the experiments have notcontrolled for the visual appearance of the cueingstimulus. In these (and nearly all other) spatial cueingtasks, the physical appearance of the cueing stimuliwas directly coupled to their cueing properties. Thoughthis is unlikely to have any e�ect on results of beha-vioral studies, it may pose a di�culty for interpretingERPs elicited by cueing stimuli. For instance, in theexperiment by Yamaguchi et al. [42], ERPs elicited byarrows pointing to the left (or the brightening of per-ipheral location markers on the left) were comparedwith ERPs elicited by arrows pointing to the right (orthe brightening of peripheral location markers on theright). Therefore, it is possible that the physical di�er-ences between stimuli have contributed to the di�er-ences obtained in the ERPs linked to covert shifts ofattention. In the present experiment we remedied thispotential confound by using foveal symbolic cueswhose physical appearance could be de-coupled fromtheir cueing properties. Across experimental conditionswithin subjects, the identical stimulus cued shifts ofvisuospatial attention to either the left or to the rightvisual ®eld. In this way, it was possible to isolate theERP e�ects that were purely linked to shifting visuos-patial attention, and independent from physical fea-tures of the cueing stimuli. In addition, more extensivesampling of the ERPs was obtained relative to pre-vious studies, which enabled the characterization ofthe topographic distribution of the e�ects. The topo-graphic information helps constrain hypotheses regard-ing the brain areas that may contribute to the e�ects.The increased spatial resolution helps frame the ERPresults within the existing knowledge of the neuroanat-omy of the system for visuospatial orienting.

2. Materials and methods

2.1. Subjects

Seventeen healthy volunteers participated in thestudy. One subject was discarded from the analysisdue to excessive eye movement during the ERP record-ings. The remaining 16 subjects (eight females) had amean age of 24 years. All were right handed (meanscore on the Edinburgh handedness inventory [32]:+93) and had normal or corrected to normal visualacuity. The experimental methods were non-invasiveand had ethical approval from the Department of Ex-perimental Psychology, University of Oxford.

2.2. Behavioral task and procedures

The behavioral task is displayed schematically inFig. 1. Stimuli were presented on a black background.The display consisted of two peripheral white boxes(centered at 78 eccentricity, 18 width) and a small cen-trally located white diamond (0.58 width). During anygiven trial, a colored pattern brie¯y overlaid the cen-tral diamond stimulus (100 ms duration) predicting(80% accuracy) the location of the peripheral box (leftor right) in which the target would appear (100 msduration) after a randomized cue-target interval (CTI).Short (100 ms), medium (300 ms) and long (700 ms)intervals between cue o�set and target appearance(CTI) were presented in an unpredictable fashion. Theshort CTI trials ensured that subjects attempted to ori-ent attention as rapidly as possible, and the use ofthree intervals reduced the temporal predictability ofthe targets (see Ref. [28]). The target was either a verti-cal or a horizontal black-and-white grating that wasfollowed by checkered mask (800 ms duration). Sub-jects discriminated the target and responded to onlyone of the grating orientations (go/no-go response),present in 50% of all trials. The grating orientationrequiring a response alternated across the experimentalblocks performed by each subject, with the order coun-terbalanced across subjects. Subjects responded bymaking a speeded key-press with their index ®nger.The requirement for making a stimulus discriminationand making a conditional response was introduced inorder to maximize attentional demands in the task andto ensure the use of covert focused spatial attention.The hand of response was balanced across subjects.Subjects were asked to respond as quickly as possible,while avoiding mistakes.

The informative cue was a bi-colored green-and-reddiamond. Each constituent colored side formed anarrowhead pointing toward one of the peripheral lo-cations. The side of the constituent colors varied in arandomized and unpredictable fashion over trials, withan equal probability that a given color-side con®gur-ation would appear. There were two cueing conditions,and each subject performed both, in a balanced order.In one condition, the green side of the cue predictedthe likely location of the subsequent target. In theother condition, the red side was predictive.

Subjects performed the task, after the preparationsfor the ERP recordings, in a darkened experimentalroom. The entire experimental session lasted ca. 2.5 h.Subjects reclined on an armchair, at 100-cm distancefrom a computer monitor that was tilted perpendicularto their gaze. Each subject performed four task con-ditions consisting of combinations of which color ofthe cue was informative (red, green) and which gratingorientation required a response (horizontal, vertical).Subjects were informed prior to each task condition

A.C. Nobre et al. / Neuropsychologia 38 (2000) 964±974 965

about the cue-target contingencies and the relevantgrating orientation. Subjects were also requested tomaintain visual ®xation in the center of the foveal dia-mond stimulus and to avoid moving or blinking theeyes during task performance. Each task conditioncontained 240 trials, and subjects completed all fourconditions in one experimental session. The order ofconditions was counterbalanced within and across sub-jects. In one condition, the green-side of the cue wasinformative and subjects responded to the horizontalgratings only. Likewise, the other conditions were:green-vertical; red-horizontal; and red-vertical. A pausewas introduced every 60 trials to allow subjects to rest,and subjects re-initiated the task when they felt ready.

2.3. Behavioral analysis

The reaction times of accurate responses were ana-lyzed using a mixed-design analysis of variance(ANOVA). There were ®ve experimental factorsmanipulated within subjects: the color of the cue-sidethat was predictive (green-side, red-side), trial validity(valid, invalid), target grating orientation (horizontal,vertical), visual ®eld (VF ) of the target (left, right),and CTI (100, 300, 700). The only factor manipulatedbetween subjects was the response hand (left, right).

2.4. ERP recordings

The electroencephalographic (EEG) activity wasrecorded continuously from 56 sites using tin electro-des mounted on an elastic cap (Electro-cap Inc.) andpositioned according to the 10±20 International system[1]. The montage included 8 midline sites (FPZ, FZ,FCZ, CZ, CPZ, PZ, POZ, OZ) and 24 sites over eachhemisphere (FP1/FP2, AF3/AF4, AF7/AF8, F3/F4,F5/F6, F7/F8, FC1/FC2, FC3/FC4, FC5/FC6, FT7/FT8, C3/C4, C5/C6, T7/T8, CP1/CP2, CP3/CP4, CP5/CP6, TP7/TP8, P3/P4, P5/P6, P7/P8, PO3/PO4, PO7/PO8, O1/O2 and mastoids). Additional electrodes wereused as ground and reference sites, and to monitor theelectrooculogram (EOG). The ground electrode wasplaced along the midline between FPZ and FZ. Thenose was used as the reference for all electrodes. Datawere recorded with a band-pass ®lter of 0.1±100 Hz,ampli®ed 20,000 times, and digitized at a samplingrate of 250 Hz. The EOG signal was recorded bipo-larly. Electrodes placed on the left and right of theexternal canthi measured horizontal eye movements.Electrodes placed above and below the left eyemeasured vertical eye movements and blinks.

Event-related potentials were constructed o�ine,according to stimulus type. Data were re-®ltered digi-tally with a band-pass of 0.1±60 Hz. Epochs were

Fig. 1. Task schematic. Subjects ®xated on the central diamond stimulus (0.58 width). A bi-colored central cue (100 ms duration) composed of a

green side and a red side (here depicted as gray and black respectively) indicated the likely location of the target (80% probability) to appear in

one of the peripheral boxes (centered at 78 eccentricity, 18 width). Target appeared after one of three CTIs (100, 300, 700 ms). Targets were either

horizontal or vertical gratings presented brie¯y (100 ms) and masked by a checkered pattern (800 ms duration). Only one type of target grating

required a response, according to the task instructions. Subjects responded as soon as possible upon detecting the relevant target stimulus. Trials

were presented every 2.3 s. The blank inter-trial interval (ITI) and the blank inter-stimulus interval (ISI) were complementary and always added

to 1.3 s. Stimuli appeared on a black background. The two panels shown provide examples of valid cueing trials requiring a response in the

green-side condition or invalid cueing trials for the red-side condition.

A.C. Nobre et al. / Neuropsychologia 38 (2000) 964±974966

made starting 200 ms before and ending 1848 ms aftereach stimulus of interest. ERPs were not constructedfor stimuli in trials containing the shortest CTI (CTI,100 ms) because of the sizeable overlap between thevisual responses to the cues and targets. Two types ofERPs were constructed for the cue stimuli, accordingto the two types of spatial predictions (left, right VF).Both trial types containing medium (300-ms) and long(700-ms) CTIs were included. Four types of ERPswere constructed for the target stimuli, according totrial validity and VF (valid-left, invalid-left, valid-right,invalid-right ). Only trials with the long CTIs wereincluded, to avoid contamination of cue-related brainactivity in measures of target processing.

Epochs with excessive drift, or containing eye move-ments or blinks were rejected. Trials were automati-cally eliminated if the voltage exceeded 250 mV at CZor at either the vertical or horizontal EOG channelbetween ÿ200 and 800 ms. In addition, the HEOGwas inspected visually and trials containing saccadeswere also eliminated. The average HEOG for eachsubject was compared as a function of cue prediction,and no systematic eye-movement bias occurred for anysubject.

2.5. ERP analysis

In order to sample evenly any possible localizeddi�erences in ERPs due to the shifting of attentionduring the CTI, we adopted an analysis strategy usingseparate symmetrical regions over the scalp. Successivemean voltage values every 40 ms (10 data points)between 0 and 600 ms post-stimulus were used asdependent variables in four separate regional analyses.The last 200 ms of these analysis represents a timeperiod during which processing of the targets in themedium CTI condition may contribute to the resultsobtained. The four regions were: midline; frontal; cen-tral; and posterior. The electrodes included in eachcase are stated in the relevant sections of the results.In the midline analyses, two factors were tested withinsubjects using ANOVAs: cue prediction (left, right VF)and electrode location (FPZ, FZ, CZ, PZ, OZ). In theother regional analyses, the additional factor of scalphemisphere (left, right) was tested. There were ®ve orsix symmetrical electrode positions in these lateral re-gional analyses. The Greenhouse-Geisser epsilon cor-rection factor was applied where appropriate, tocompensate for possible e�ects of non-sphericity in themeasurements compared. Only the corrected prob-ability values (and degrees of freedom) are reported.

The ERPs elicited by target stimuli in spatial atten-tion tasks have been extensively investigated, and werenot an important focus of the present report. Theidenti®able visual components (P1 and N1) weremeasured over symmetrical posterior sites where they

were largest. The mean amplitude of P1 was measuredat PO7/8 and O1/2 between 120 and 160 ms. N1mean-amplitude was measured at P7/8 and PO7/8between 180 and 220 ms. In addition, the P300 poten-tial was measured at the midline sites where it was lar-gest, CZ and PZ, between 400 and 600 ms. Allamplitude values were calculated with reference to the200 ms pre-stimulus baseline. ANOVAs, using theGreenhouse-Geisser epsilon correction factor tested forthe e�ects of target validity (valid, invalid), target VF(LVF, RVF), electrode site (PO7/8, O1/2 for P1, P7/8,P07/8 for N1; CZ, PZ for P300), and electrode hemi-sphere (left, right) where appropriate.

3. Results

3.1. Behavioral data

The main purpose of this experiment was to investi-gate the ERPs associated with shifting attention tospatial locations. Therefore, it was of main interest todetermine whether the foveal cues we employed weresuccessful at driving spatial attention.

The initial ANOVA showed no main e�ect of thebetween-factor of response hand [F(1,14)=0.020, p =0.89] or any interaction between response hand andany other factor. The data for both response handswere therefore collapsed, and a four-factor repeated-measures ANOVA was evaluated. The results con-®rmed the e�cacy of the validity of the cues. Subjectswere signi®cantly faster at identifying targets in validtrials (mean: 445 ms, standard deviation:297 ms) thanin invalid trials (486 2 100 ms) [F(1,15)=36.24, p <0.001]. In addition, the VF location of the target andthe interval at which it appeared also exerted maine�ects on reaction times. Targets in the RVF wereidenti®ed faster (4572101 ms) than those in the LVF(474299 ms) [F(1,15)=10.32, p < 0.05]. Trial VF didnot interact signi®cantly with other factors. Targetsappearing at the shortest CTI were identi®ed moreslowly (477295 ms) than those appearing at the med-ium (458 2 99 ms) or long (463 2 107 ms) intervals[F(2,30)=4.92, p < 0.05]. The CTI interacted with thetrial validity, indicating that the attention e�ects werelarger at the long CTI (55 ms) than at the medium (37ms) or short CTIs (32 ms) [F(2,30)=3.51, p < 0.05].Linear contrasts performed post-hoc showed that allthe attention e�ects were signi®cant at all three inter-vals tested. There was no signi®cant discrepancy in theability of the two color cues to guide spatial shifts ofattention [F(1,15)=0.12, p = 0.73]. The reaction timesto the two types of orientation gratings did not di�ersigni®cantly [F(1,15)=2.08, p=0.17].

A.C. Nobre et al. / Neuropsychologia 38 (2000) 964±974 967

3.2. ERP data

3.2.1. TargetsThe task was not designed to investigate ERPs eli-

cited by targets. Target gratings appeared brie¯y (100ms) and were immediately followed by a checkeredmask. The neural responses to the target and maskstimuli were con¯ated in the ERPs recorded. For sim-plicity, the analysis of ERPs elicited by the target col-lapsed over the two types of orientation gratings andresponse requirements (go, no-go). In order to avoidoverlap from components elicited by the precedingcues, the analysis was restricted to targets in trials withlong CTIs. Consistent with prior reports, the ampli-tudes of early visual components (P1, N1) and of theP300 were larger during valid trials than during invalidtrials. The main e�ect of validity was not signi®cantfor the P1 enhancement. There was only a signi®canttrend for the interaction between validity and electrodesite [F(1.0,15.0)=3.51, p = 0.08], indicating that thedi�erences due to validity were larger over PO7/8 thanO1/2. Trial validity did exert a signi®cant main e�ecton N1 [F(1.0,15.0)=10.57, p E 0.05]. An interactionbetween validity and electrode site showed the e�ect tobe larger over P7/8 than PO7/8. The contralateral N1distribution was indicated by the signi®cant interactionbetween target VF and electrode hemisphere[F(1.0,15.0)=7.27, p E 0.05]. Finally, target validity

also exerted a main e�ect on the P300[F(1.0,15.0)=12.666, p = 0.003]. Valid targets elicitedlarger P300s.

3.2.2. CuesThe brain activity engaged by physically equated

foveal cues was the main focus of the present exper-iment. ERPs were collapsed over the factors that werenot of experimental interest: hand of response andcolor of the cue-side that directed attention. Both ofthese factors were counterbalanced, and neither exertedsigni®cant e�ects on the behavioral results. The mainexperimental factor of interest was the side of the VFpredicted by the cue.

Fig. 2 shows representative waveforms elicited bycues predicting the appearance of the target in the left(solid line) or right (dashed line) VF. Lateral sym-metric electrode sites covering the anterior-posteriorextent of the recordings are shown. ERPs to cues werecharacterized by early visual responses (P1, N1) overlateral posterior sites, followed by a positive peakaround 240 maximal over parietal sites, a negativetrough around 280 ms maximal over parietal and occi-pital sites (N2), and a wide late positive peak around400 ms broadly distributed over central and parietalsites. After the late broad positivity, a slow negativecomponent with a broad distribution over frontal andcentral sites developed and remained until the appear-

Fig. 2. Grand-averaged waveforms (N = 16 subjects) elicited by cues predicting the appearance of targets in the left visual ®eld (Ð) and in the

right visual ®eld (- - -). ERPs elicited by cues in trials containing medium and long CTIs have been averaged together. The electrode montage

used for the experiment is shown at the top. The locations of the electrode sites for the sample waveforms are shaded black. Waveforms are

shown from symmetrical lateral sites covering the posterior-anterior extent of the recordings. Midline sites are not shown, since they contained

no signi®cant e�ects of spatial shifting. Polarity of the waveforms is plotted with positive values upward.

A.C. Nobre et al. / Neuropsychologia 38 (2000) 964±974968

ance of the visual responses elicited by the ensuing tar-get stimuli.

A set of regional ANOVAs assessed when ERPs eli-cited by cues diverged as a function of the predictedVF location. Because of the multiple interrelated com-parisons, and hence the likelihood of false-positivespurious signi®cant e�ects, results were only con-sidered reliable if they persisted for at least two succes-sive time bins (40-ms each) in the same regionalanalysis. The results showed localized signi®cant e�ectsof shifting spatial attention starting as early as 160 msand persisting nearly through the last time bin ana-lyzed (until 520±560 ms). Fig. 3 shows the scalp distri-bution of the di�erence between ERPs elicited byshifts to the right and shifts to the left VF during allsigni®cant time bins. The e�ects were lateralized overthe scalp, starting over posterior regions and movinganteriorly toward frontal regions of the scalp. Thedetails of the distribution of the e�ects were revealedby the regional analyses.

The midline analyses involved electrode sites FPZ,FZ, CZ, PZ, and OZ. Cue prediction did not exert anymain e�ect on the data recorded from the midline, nordid it interact with electrode site. The lack of signi®-cant results along the midline of the scalp is consistent

with the highly lateralized appearance of the exper-imental e�ects.

The posterior analyses (electrode sites: P3/4, P5/6,P7/8, PO7/8, O1/2) revealed the earliest signi®cante�ects involving cue prediction. At 160±200 ms, an in-teraction between prediction and electrode site occurred[F(1.7, 25.7)=4.53, p < 0.05]. This e�ect was highlyfocused over electrode site PO7 in the left hemisphere.During the next three time bins (200±320 ms), therewere signi®cant two-way interactions between predic-tion and site and between prediction and hemisphere aswell as a three way interaction among the three factors(all F > 4.5, p < 0.05). The last time bin in the pos-terior analysis to show an e�ect related to predictionoccurred at 320±360 ms, where a three way interactionbetween the three factors predictionxsitexhemispherewas obtained [F(2.5, 38.1)=3.95, p < 0.05]. The earlytermination of the posterior e�ects suggested thatvisual processing of the targets in the medium CTIcondition did not contribute to the results. The pos-terior e�ects indicated that predictive cues toward theright VF elicited a larger negative response over thecontralateral left posterior scalp starting at 160 ms.Predictive cues toward the left VF elicited a largernegative response over the contralateral right hemi-

Fig. 3. Scalp topographies showing the di�erence in grand-averaged ERPs elicited by cues predicting right VF targets and cues predicting left VF

targets (RVF minus LVF predictions). The topographies are plotted from an areal perspective. The anterior scalp is shown on the top and the

right scalp is shown on the right side. Topographies are shown at the midpoint of the ten consecutive time bins showing signi®cant e�ects of

spatial shifting (160±560 ms). The color scale (colored bar on the right) shows the range of possible voltage values in the topographies. The vol-

tage range for the all the topographies is the same (ÿ1.0, +0.7) thus a�ording a visual comparison of changes in the amplitudes as well as the

distributions of the ERP e�ects.

A.C. Nobre et al. / Neuropsychologia 38 (2000) 964±974 969

sphere starting shortly after (180 ms)1. The e�ects weremore accentuated over the left hemisphere, and weremaximal over electrode sites PO7/8.

The frontal analyses (electrode sites: FP1/2, AF7/8, F3/4, F5/6, F7/8) contained signi®cant e�ectsinvolving cue prediction starting later (200±240 ms)and continuing until 520 ms. The ®rst e�ect was athree way interaction between prediction � site �hemisphere [F(2.9, 43.7)=4.33, p < 0.05]. During thesuccessive time bins (240±520 ms) the two-way inter-action between prediction and hemisphere, and thethree way interaction including electrode site remainedsigni®cant (all F > 3.30, p < 0.05). The frontal e�ectsindicated that spatial shifts to the right elicited largerpositive voltage over the ipsilateral right anterior scalp.These right-hemisphere e�ects were not evenly distrib-uted over the frontal scalp, being largest mainly overF5/6 and F7/8.

The central analyses (electrode sites: FC3/4, FC5/6,C3/4, C5/6, CP3/4, CP5/6) yielded results that were in-termediate between the posterior and frontal analyses.Cue prediction interacted signi®cantly with hemisphereover two groups of consecutive time bins 200±320 and400±480 ms (all F>11.7, p<0.05). A three-way inter-action also occurred during this later time period butwas more persistent (440±560 ms, all F > 2.8, p <0.05). Overall, the e�ects registered over the centralscalp region re¯ect a relative positivity over the hemi-sphere ipsilateral to the predicted target location. Theearlier e�ects over central scalp regions re¯ect theextension of the e�ects that are maximal over posteriorsites. The relative positivity ipsilateral to the predictedVF extends more anteriorly than the more pronouncedrelative contralateral negativity, and is registered atelectrode sites in the central analyses. The early e�ectsalso capture the transition between posterior and fron-tal e�ects, during which the central electrode sites ipsi-lateral to the predicted shift are relatively morepositive. The later e�ects re¯ect the extensive anteriore�ects, which spread over frontal and central regionsof the scalp over the right-hemisphere.

4. Discussion

The main contribution of the experiment was to reg-ister on-line the brain activity associated with shiftingattention toward peripheral spatial locations usingERPs. Electrophysiological measures still provide the

only non-invasive means to track neural activity inreal-time. ERPs have been invaluable in revealing themodulatory e�ects that spatial attention exerts overvisual stimuli [12, 19]. In contrast, they have been usedonly scarcely to study brain activity during the actualshifting of spatial attention that occurs prior to thepresentation of the target stimuli (cf., Refs. [13, 15,42]). One of the reasons why ERPs elicited by cuesmay have been investigated and/or reported minimally,is that the physical appearance of cueing stimuli inspatial orienting tasks go hand-in-hand with their pre-dictive qualities. Arrows pointing to the left predictstimuli on the left, whereas arrows pointing to theright predict stimuli on the right, etc. ERPs are verysensitive to the physical attributes of stimuli. Withoutusing identical stimuli it is di�cult to tease apart thee�ects that result from physical di�erences in the stim-uli and the e�ects that result from purely mental oper-ations engaged by the stimuli independently from theirappearance. To resolve this methodological shortcom-ing, we designed a variant of the cued covert spatialattention task [37], in which the same foveal stimuluscould direct covert shifts of attention either toward theleft or right VF, according to the instruction in a giventask condition. This task design enabled us to recordERPs from physically identical cueing stimuli (e.g.,green-side on the left) when it predicted either a shifttoward the left (green-side predictive) or toward theright (red-side predictive). By using these compositearrow-head cues, we maintained, as much as possible,the cueing characteristics of the task similar to pre-vious reports of spatial cueing using central arrows. Itwould also be possible to use other more abstract cuesthat predicted di�erent VF locations, and to balancetheir cueing assignment within or between subjects(e.g., see Ref. [28]).

The behavioral e�ects obtained using these compo-site arrow-head cues were in agreement with prior ®nd-ings of cued covert visual spatial attention. Thecomposite cues were e�ective at driving shifts of atten-tion. Subjects were signi®cantly faster to identify tar-gets appearing in the predicted VF location. Thefacilitatory e�ects were present at all intervals, thoughthey were larger at the longest CTI suggesting anincreasing ability to direct attention over a few hun-dred milliseconds [34, 35]. We also found a behavioralbene®t to identify targets located in the right VF thatwas independent of the hand used for response. Aright VF advantage is not consistently reported insimilar tasks. The reason for this RVF advantage isnot completely clear, but may be related to the hemi-spheric asymmetry in the control of spatial attentionshown by neuropsychology [16, 26] and supported bybrain-imaging studies [6, 14, 31]. For instance, the®ndings could be explained under the notion that boththe right and left hemispheres of the brain direct atten-

1 The ERP di�erences are relative measures, and the polarity of

the di�erences do not carry special signi®cance. Therefore, this

description is equivalent to stating that there was a focal area

with relatively more positive voltage over the scalp ipsilateral to

the VF predicted by the cue. The same logic holds for other

di�erences described.

A.C. Nobre et al. / Neuropsychologia 38 (2000) 964±974970

tion to the right VF while only the right hemispheredirects attention to the left VF [26]. The right visual®eld might thus receive more attentional resourcesthan the left VF. The presence of the RVF advantagemay depend on speci®c task parameters and di�culty,which may have been fortuitously optimized in thepresent experiment. However, it was not within thescope of the present experiment to address this inter-esting issue.

The ERP e�ects elicited by the target stimuli werealso in agreement with previous reports (see Refs. [39,24, 8, 10, 13, 18, 25]). Visual processing of target stim-uli was relatively enhanced by focused spatial attentiondirected by the foveal cues on a trial-by-trial basis.The e�ects were not very pronounced or signi®cant onthe ®rst measured visual potential (P1). This is in linewith the notion that attentional modulation is attenu-ated in cases where targets cued on a trial-by-trialbasis remain relevant for behavioral performanceregardless of whether they appear at the cued oruncued location [10, 12, 13]. In addition, the long-latency P300 potential was also augmented by directedattention (see also Refs. [13, 23]). The present exper-iment did not provide any new information regardingthe modulatory e�ects exerted by covert visual spatialattention. However, the replication of standard target-related ERP e�ects facilitates the interpretation of thecue-related ERP e�ects.

Only few studies to date have examined the brainactivity linked to the setting up of spatial expectationsprior to target presentation in spatial orienting tasksusing event-related potentials [13, 15, 42]. Harter et al.[15] were the ®rst to describe the ERP e�ects linked toshifts of spatial attention, based on a study conductedon a large group of children (6±9 years old) using atask where central arrows indicated the likely (75%)location of targets that appeared 600 ms later. (It ispossible that developmental factors may have a bear-ing on their results.) They reported di�erences due todirecting attention starting around 180 ms. The earlieste�ects (180±400 ms post-cue) were negative potentialsover parietal and occipital electrodes contralateral tothe direction of attention. Later e�ects (400±700 mspost-cue) consisted of a relative positivity contralateralto the direction of attention at occipital and centralelectrodes. Late negative potentials linked to motorpreparation and anticipation (contingent negative vari-ation, CNV) were also identi®ed in the waveforms, butwere not modulated by the direction of attention.Yamaguchi et al. [42] used central arrows that pre-dicted (80%) the location of a target appearing after avariable interval. The earliest e�ects (240±380 ms post-cue) were also an enhanced negativity contralateral tothe direction of the attentional shift over lateral pos-terior scalp sites. In their case, the later e�ects (380±440 ms) re¯ected enhancement of negative potentials

contralateral to the shift direction. These e�ects havebeen replicated in subsequent studies by the samegroup, in which they have tested attentional shifting indi�erent experimental populations such as the elderly,and neurological patients [41, 43, 44]. Yamaguchi etal. [42] also conducted experiments using predictive(80%) peripheral cues. Waveforms elicited by cues inthis case are likely to re¯ect a combination of thephysical attributes of the lateralized stimuli, automaticpriming of attention by the peripheral transients, aswell as endogenous attentional shifts caused by thepredictive probabilities of the stimuli. The complexityof the factors contributing to the peripheral-cueingresults makes the results di�cult to interpret or com-pare to the other studies. Eimer [13] also used a spatialorienting task. Arrows predicted (73%) the location ofa target that followed after a ®xed interval and whoselocation or shape required discrimination. Hemeasured the potentials linked to anticipation and re-sponse preparation preceding the targets. His resultsshowed that spatial cues triggered processes linked toresponse preparation, as re¯ected by the contingentnegative variation (CNV) and in lateralized responsepotentials (LRPs). These potentials were larger in thelocation-discrimination condition, since the cue carriedrelevant predictive information about the response tobe delivered. Waveforms elicited by the cues per sewere not reported, so the results are di�cult to com-pare to the other studies.

In the present experiment, brain activity speci®callylinked to the shifting of visual spatial attention todi�erent VF locations was identi®ed starting 160 msafter the presentation of the cueing stimuli. These ERPdi�erences therefore started hundreds of millisecondsprior to the appearance of the target stimuli (at either300 or 700 ms post cue), and they persisted throughoutall or most of the CTI (until 560 ms). The changes inthe scalp distribution of the e�ects (see Fig. 3) shownby the results of the statistical analyses over separatescalp regions suggest that there are multiple neuralprocesses involved in shifting spatial attention covertly.The e�ects were highly lateralized and concentratedover the posterior and the central-anterior portions ofthe scalp. The results indicated that brain activity sen-sitive to the direction of shifts of attention occurs ear-lier over posterior regions (160±360 ms) and proceedsto central (200±320 and 400±560 ms) and frontal (200±520 ms) regions. There is also extensive temporal over-lap between the focal e�ects, consistent with a largedegree of concurrent activity in multiple brain areas.Both the posterior and the central-frontal e�ects wereasymmetrical over the two hemispheres.

These results complement and help clarify the pre-vious reports of ERP e�ects linked to shifting visualattention in space. In all cases, shifting spatial atten-tion seems to a�ect at least two general stages of pro-

A.C. Nobre et al. / Neuropsychologia 38 (2000) 964±974 971

cessing. Earlier e�ects occur over posterior scalpregions, followed by later e�ects over central and an-terior scalp locations. The earlier e�ects, involving aposterior contralateral negative potential, are stableacross the di�erent experiments. The replication of thise�ect in the present study, indicates that it is notbound to the physical attributes of the cueing stimulus.Instead, it re¯ects some aspect of the mental andneural operations involved in anticipating or preparingfor a relevant stimulus at a predicted spatial location.The latency of this e�ect may be found to vary accord-ing to the time required for translating the meaning ofthe cueing stimulus into a spatial expectation. The den-ser electrode sampling in the present experiment alsode®nes more accurately the distribution and the latera-lization of this e�ect. The later e�ects involving morecentral and anterior scalp regions are much more vari-able across the di�erent experiments, including in itspolarity and lateralization. This would suggest that thelater e�ects may be more sensitive to response-relatedvariables in the di�erent tasks.

On the surface, the present ®ndings of an enhancedpositivity over the scalp sites ipsilateral to the directionof attention shift are consistent with the report of anenhanced negativity contralateral to the direction ofshifts by Yamaguchi et al. [41]. However, direct com-parison of the waveforms across the two studiessuggest that di�erent e�ects may be at play. Theapparent discrepancies remain to be clari®ed. Thedi�erent experiments to date have involved di�erentresponse requirements, and enabled di�erent degreesof motor preparation based upon cue presentation.The tasks by Harter et al. [15] and Yamaguchi et al.[42] required simple target detection, whereas the pre-sent task required target discrimination. In the task byHarter et al. [15], subjects could also predict the tem-poral interval at which the target would appear. E�ectsof temporal expectations may have therefore in¯u-enced their results (see Ref. [28]). The results by Eimer[13] reinforce the notion that response anticipation andpreparation processes are triggered by the spatial cue-ing stimuli. To test the dependence of the later e�ectsto response-related variables, experiments are neededin which the response requirements and predictabilityare manipulated systematically.

The distribution of the early posterior and later cen-tral-anterior e�ects in the present study is consistentwith engagement of posterior parietal and frontal pre-motor brain areas involved in covert visual spatialattention that have been anatomically de®ned usingbrain imaging [6, 14, 31]. However, given the relativelylate latency and complex scalp distributions of thee�ects, we did not consider it fruitful to attempt tomodel the anatomical sources directly.

The posterior e�ects consisted of a focal area withrelatively more negative voltage over the scalp contral-

ateral to the VF predicted by the cue. The e�ect waslarger over the left hemisphere. At ®rst this mayappear to be inconsistent with notions of right-hemi-sphere dominance for attention. Instead, it may re¯ecta larger variability in the engagement of left-hemi-sphere posterior regions based on the direction ofattention and a more consistent involvement of rightposterior regions in both leftward and rightward shifts.The scalp distribution of the posterior e�ects is sugges-tive of involvement of posterior parietal regions. Ifindeed parietal activity is re¯ected in these posteriore�ects, this would support a special role of parietalregions in initiating the computation or implemen-tation of spatial representations to guide visual atten-tion.

The central-frontal e�ects were concentrated overthe right scalp, with little or no di�erentiationobserved over left-hemisphere sites. Sensitivity to thedirection of spatial shifts of attention in more anteriorregions seems to be more restricted to only one hemi-sphere. Posterior and anterior regions may thereforeexhibit a di�erent type of hemispheric asymmetryduring visual spatial orienting. The voltage was rela-tively more positive during rightward than leftwardshifts of attention. The scalp distribution of the cen-tral-frontal e�ects appears to change shape during theduration of the e�ect (see Fig. 3), and likely re¯ectsthe activation of multiple brain areas and processes.Many cortical areas whose activity is consistent withlateral central and/or frontal e�ects are involvedduring visual spatial attention. These areas can be con-sidered candidates for the source of the ERP e�ects,and include lateral and medial premotor areas, linkedto the frontal and supplementary eye ®elds respectively(see Ref. [33]); the anterior cingulate cortex; and pos-terior temporal areas (see Ref. [14] for brain imagingresults in similar spatial cueing tasks using fovealcues).

The results thus reveal a rich succession of neuralprocesses supporting covert shifts of visual spatialattention. The ERP e�ects reported are uncontami-nated by any physical di�erence in the cueing stimuli,isolating the mental act(s) involved. Lateralized pos-terior brain activity (more accentuated over the lefthemisphere) signaling di�erent directions of spatialshifts commences during or just after visual analysis ofthe cueing stimulus (as indicated by P1 and N1 com-ponents). Frontal e�ects sensitive to the direction ofshifts of attention occur later, and are mainly con®nedto the right hemisphere. Though there is a clear pos-terior-to-anterior progression of the ERP e�ects, size-able temporal overlap also exists between the focale�ects. Thus, many brain areas and processes appearto contribute to the act of directing expectationstoward a speci®c peripheral location in space. Forinstance, predictive cues may trigger disengagement

A.C. Nobre et al. / Neuropsychologia 38 (2000) 964±974972

from the present focus of attention [36], build a rep-resentation of the predicted location [27], bias the rel-evant spatial representation in working memory [4],predict the likely interval of the target arrival [7], pre-pare possible responses [13], and stimulate emotionalanticipation [30]. The ERP e�ects observed give a ®rstindication of the dynamics of neural activity in the sys-tem that directs visual spatial attention, and help tobridge between brain imaging methodologies with highanatomical and temporal resolution.

Acknowledgements

The research was supported by a project grant toACN by The Wellcome Trust. The authors wish tothank Dr Leonardo Chelazzi for helpful commentsand discussion.

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