An ERP study of the temporal course of the Stroop color-wordinterference e�ect

p

Mario Liotti*, Marty G. Woldor�, Ricardo Perez III, Helen S. Mayberg1

University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Drive, San Antonio, TX 78284-6240, USA

Received 12 November 1998; received in revised form 23 June 1999; accepted 22 July 1999

Abstract

The electrophysiological correlates of the Stroop color-word interference e�ect were studied in eight healthy subjects using

high-density Event-Related Potentials (ERPs). Three response modalities were compared: Overt Verbal, Covert Verbal, andManual. Both Overt Verbal and Manual versions of the Stroop yielded robust Stroop color-word interference as indexed bylonger RT for incongruent than congruent color words. The Incongruent vs Congruent ERP di�erence wave presented twoe�ects. A ®rst e�ect was a medial dorsal negativity between 350±500 ms post-stimulus (peak at 410 ms). This e�ect had a

signi®cantly di�erent scalp distribution in the Verbal and Manual Stroop versions, with an anterior±medial focus for overt orcovert speech, and a broader medial±dorsal distribution for the manual task. Dipole source analysis suggested two independentgenerators in anterior cingulate cortex. Later on in time, a prolonged positivity developed between 500±800 ms post-stimulus

over left superior temporo-parietal scalp. This e�ect was present for all the three response modalities. A possible interpretationof these results is that Stroop color-word interference ®rst activates anterior cingulate cortex (350±500 ms post-stimulus),followed by activation of the left temporo-parietal cortex, possibly related to the need of additional processing of word

meaning. # 2000 Elsevier Science Ltd. All rights reserved.

1. Introduction

The Stroop color interference task is among themost extensively studied paradigms in cognitive psy-chology. The classical behavioral e�ect consists of alengthening in reaction time to color naming when theword meaning and the presentation do not match (i.e.,they are ``incongruent'') relative to when they corre-spond (i.e., they are ``congruent'') [31]. At a psycho-logical level, the Stroop e�ect has been best explainedin terms of response competition. Longer reaction time

and greater interference is present when the irrelevantattribute of the stimulus (the word meaning) is ana-lyzed faster (i.e. is more automatic) than the relevantattribute (color), and the unwanted response is there-fore available ®rst (``race'' model) [21].

Lesion correlation data in stroke patients [28,35],and neuroimaging studies in healthy volunteers[6,8,11,13,20,22,33] have greatly improved our under-standing of regions in the brain mediating the atten-tional demands involved in the Stroop color wordinterference. More speci®cally, the anterior cingulatecortex appears to be heavily involved, although otherareas have been less consistently reported, such as in-ferior frontal cortex, parietal cortex, posterior cingu-late and motor and premotor regions. The originalPositron Emission Tomography (PET) ®ndings gener-ally supported the construct of an anterior attentionalsystem involved in target detection and response selec-tion, especially when confronted with con¯icting stimu-lus or response biases [24,25].

Neuropsychologia 38 (2000) 701±711

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

PII: S0028-3932(99 )00106 -2

www.elsevier.com/locate/neuropsychologia

pPresented as poster at the 1999 Meeting of the Cognitive Neuro-

science Society. Supported by a NARSAD Young Investigator

Award to ML

* Corresponding author. Tel.: +1-210-567-8186; fax: +1-210-567-

8152.

E-mail address: liotti@uthscsa.edu (M. Liotti).

Current address: Rotman Center, Baycrest Center for Geriatric

Care, Toronto, Canada.

Considerable interest in the Stroop Task derivesfrom its growing utility as a diagnostic and researchtool to probe executive function in frontal lobe injury[28,35] and psychiatric disease. In depression andschizophrenia, Stroop performance is generallyimpaired. PET abnormalities in the anterior cingulatehave been described both at rest and during attentionalperformance [5,9,12,14,17,18]. In depression, abnormalresting state hypometabolism and hypoperfusion havebeen reported in all portions of the anterior cingulate,including the ventral subgenual [12,18], the rostral [17],and the dorsal [5,18] partitions. The dorsal anteriorcingulate abnormality in both depression and schizo-phrenia corresponds to the region implicated in selec-tive attention by previous PET studies in normals[24,25].

In spite of the well-replicated ®nding of anterior cin-gulate involvement in the Stroop color interferencetask delineated by cognitive neuroimaging studiesusing PET [6,8,11,13,22,33] and recently functionalMagnetic Resonance Imaging (fMRI) [20], several keyaspects of the neuropsychology of the Stroop e�ect arestill unknown. The ®rst concerns the temporal courseof the activations in the network of brain regionsinvolved in the execution of the Stroop task. PET islimited by long integration time (40±120 s), and fMRIis limited by the long duration of the hemodynamic re-sponse (several seconds), although Event-RelatedfMRI appear as a promising technique to improve itstemporal resolution [7,27]. Event-Related Potentials(ERPs) possess exquisite temporal resolution (mslevel), but only coarse spatial resolution Ð improvedby the use of high-density electrode arrays [34]. ERPshave the potential to identify the timing, order of acti-vation, and dynamic orchestration of brain regionsduring the unfolding of the Stroop task. Secondly,because of the limited temporal resolution, PET andconventional fMRI only allow block paradigm design.This has been the case for all the available neuroima-ging studies of the Stroop e�ect, whereas most typi-cally blocks of ``incongruent'' color words have beencontrasted to blocks of ``congruent'' color words[6,8,11,13,20,22,33]. It can be argued that under theseconditions the Stroop Task sums up to a rather di�er-ent task. First, the elements of switching and unpre-dictability are absent. Second, the ``incongruent''blocks appear intuitively to require a di�erent atten-tional set, a higher level of sustained attention andarousal, and possibly a di�erent processing strategyaltogether (e�ortful rather than automatic). In ad-dition, in ``congruent'' blocks the word color maybecome irrelevant to the task, since the more auto-matic processing of the word meaning alone is su�-cient to correctly perform the task. In contrast to PETand MRI, ERPs capitalize on selective averaging ofdi�erent stimulus types within the same experimental

block (i.e., ``congruent'' words and ``incongruent''words), allowing mixed-trials analysis of the Strooptask in its unadulterated and classical form. Finally,alternative response modalities during the Stroop taskthat are less problematic in terms of motion artifactsin fMRI, such as manual and covert vocal, have notbeen much explored before in any imaging modality[2,15,26].

Three published ERP studies have addressed theStroop e�ect. The ®rst used only two color words,employed manual responses, and reported exclusivelyearly color selection e�ects [26]. The second is a recentstudy using a covert version of the original Strooptask [2]. The third used three color words andemployed only manual responses [15]. All of these stu-dies only employed several electrodes, in the midlineonly. The paucity of studies employing the Stroopparadigm may be partly explained by the concern withcontamination of the cognitive e�ects with overtspeech artifacts and other motion artifacts frequentlyobserved during speech [30,36].

The aim of the present study was to investigate thetemporal course of known brain activations during theconventional, mixed-trial Stroop color-word paradigmusing high-density (64 channel) ERP recordings. Anadditional goal of the study was to directly contrastwithin the same subjects and sessions the conventionalversion of the Stroop task (Overt Speech) with twoalternative response modalities: a covert color namingcondition, and a four-choice manual version of thetask. This approach allowed us to examine the depen-dence of the Stroop e�ect brain activations on the par-ticular response modality employed, as well as being ofgeneral interest for future studies of the Stroop e�ectusing brain activity measures that are highly vulner-able to motion artifacts, such as ERPs and fMRI.

2. Methods

2.1. Subjects

Eight healthy volunteers (right-handed, age 27.6 26.8 years, three men, ®ve women) participated in thestudy. Subjects had no history of current or pastneurological or psychiatric illness, vision was normalor corrected-to-normal. Informed consent wasobtained from all subjects according to the norms ofthe University of Texas Health Science Center Insti-tutional Review Board.

2.2. Stimuli and task

Subjects were seated in a reclining chair facing amonitor placed at 40 cm from their eyes. They werepresented with the words ``red'', ``green'', ``blue'' or

M. Liotti et al. / Neuropsychologia 38 (2000) 701±711702

``yellow'' just above central ®xation presented on adark grey screen. Stimulus duration was 150 ms,stimulus size was 1.8±3.68 (horizontal)� 0.78 (vertical),and interstimulus interval varied randomly between1700±2200 ms. In the Stroop conditions, half of thewords were randomly presented in the congruent color(e.g., the word ``red'' in red ink), and half in any ofthe other three (incongruent) colors. In the Non-colorconditions, all words were in light grey ink. There wasa total of eight conditions. In the Stroop-Verbal Overtcondition, subjects said aloud the presentation color ofthe word, and vocal onset time was recorded througha microphone placed in front of the subject. In theStroop-Verbal Covert condition, subjects wereinstructed to say the color of the word silently in theirmind, without moving their lips, tongue and jaw at all.In the Stroop-Manual4 condition, subjects respondedto the color of the word by pressing one of four but-tons of a corresponding color on a gamepad, two but-tons in each hand. Reaction time and errors wereconcomitantly recorded. There were ®ve additionalcontrol tasks. In the Stroop-Passive blocks, colorwords were passively ¯ashed on the screen. In theStroop-Manual1 condition color words appeared onthe screen, and subjects responded to the appearanceof any word by pressing the same (blue) key with theright hand (manual simple reaction time). In theStroop-Vocal1 CONDITION color words appeared onthe screen, and subjects responded by saying aloud``baagaa'' (vocal simple reaction time). In the NonCo-lor conditions, the same words were presented in whiteink. In the NonColor-Manual4 blocks, subjectsresponded to each word meaning (red, green, blue, yel-low) with one of four buttons as in the Stroop-Man-ual4 condition. In the NonColor-Verbal Covertcondition subjects had to covertly read the word.

There was a total of 36 runs, of which eight eachwere Stroop-Covert and Stroop-Manual4; two wereStroop-Overt, and four each of the remaining tasks.Each run had a total of 72 stimuli (36 congruent and36 incongruent color words for the Stroop blocks) andlasted about 2.5 min. There were 144 stimuli in theStroop-Overt blocks (72 each were congruent vs incon-gruent color-words), and 576 stimuli in all other tasks.The Stroop-Covert and Stroop-Manual4 had 288 stim-uli each for congruent and incongruent color-words.

Before starting the experimental session, subjectshad a short practice on the Stroop-Overt task, and ablock of practice on the NonColor-Manual4 task inorder to learn the 4-way response con®guration. Reac-tion time from stimulus onset to a button press or theonset of a vocal response were recorded to the nearestms.

Repeated-measures Analyses of Variance (ANOVAs)were employed for the following behavioral par-ameters: Mean reaction time (RT) to all conditions for

which response latency was recorded (Hits, 200±1500ms), and rate of Errors for the congruent vs incongru-ent color words in the manual version. Within factorswere Type of Task (Manual4 vs Verbal4) and Type ofStimulus (Congruent vs Incongruent).

2.3. EEG recording

Brain electrical activity was continuously recordedusing a customized 64 channel cap (Electrocap Inc

1

,Eaton, OH) including four eye movement electrodes(two at the external canthi and two infraorbital) and aleft mastoid electrode, all referenced to the right mas-toid (bandpass=0.01±100 Hz, gain=104, samplingrate=400 Hz, impedences <5 kO). Eye movementartifacts (blinks and eye movements) were rejected o�-line. Blink artifacts were rejected in all tasks based onthe voltage amplitude at frontal supraorbital sites,since speech-related activity in the overt speech taskswas accompanied by high amplitude potentials at theinferior orbital sites which did not invert over the fron-tal scalp.

ERPs to the onset of the color words (500 ms pre-stimulus baseline and 2000 ms post-stimulus) wereselectively averaged for each subject and for each ofthe following conditions: for the Stroop tasks (Overt-Verbal, Covert-Verbal and Manual4), independentaverages were obtained for congruent and incongruentcolor-words (correct hits only were included in theOvert-Verbal and Manual4 task); for all other con-ditions (Stroop-Passive, Stroop-Manual1, Stroop-Ver-bal1, NonColor-Manual4, NonColor-Covert), allstimuli were averaged together. ERP processingincluded algebraic re-referencing to average reference[34], and smoothing by application of a seven-pointrunning average. ERP subject averages for each con-dition were then grand-averaged across the eight sub-jects. ERP amplitudes were aligned to a 200 ms pre-stimulus baseline period. The main ERP e�ects ofinterest concerned the contrasts between color-congru-ent and color-incongruent words in the Stroop-VerbalOvert, Stroop-Verbal Covert, and Stroop-Manual4conditions. Inspection of the grand-average waveformsfor these contrasts (Fig. 1), as well as inspection ofsequential topographical maps of the Incongruentminus Congruent ERP di�erence waves (Fig. 2) indi-cated that there were two major e�ects of color-wordinterference: an early e�ect (350±500 ms), and a latee�ect (500±800 ms) (see Figs. 1 and 2).

The early e�ect was explored in 50 ms time windowsfrom 350 to 500 ms (see Table 2). We tested theapriori hypothesis that medial dorsal scalp regionsabove the cingulate gyrus would show Stroop-relatedchanges. Four midline sites along the anterior±pos-terior axis (Fcz, Cz, Pzs, Pzi) and four adjacent para-sagittal lateral sites were selected. For each time

M. Liotti et al. / Neuropsychologia 38 (2000) 701±711 703

window (350±400, 400±450, 450±500 ms) and each re-sponse modality (Covert, Overt and Manual),repeated-measures ANOVAs were conducted, with fac-tor being Trial Type (Congruent vs Incongruent), An-terior±Posterior location, and Laterality (left, midline,right). A further analysis was conducted to statisticallyexplore di�erences in scalp distribution between re-sponse modalities at the peak of the e�ect (400±450ms). This analysis was carried out on the Incongruentminus Congruent di�erence waves, after the voltagedata were normalized using the square root of the sumof squares method [19]. Response type was included asa factor.

The late e�ect was explored in 100 ms time windowsfrom 500 to 800 ms (Table 2). In order to explore thetiming of such e�ect over frontal and left posteriorareas, a repeated-measures ANOVA was conducted ineach time window (500±600, 600±700, 700±800 ms)within each response modality, using three electrodesites on each hemisphere: an anterior frontal site (F3a-F4a; F3 and F4, anterior), a central site (C5a-C6a; C5and C6, anterior), and a parietal site (P3i-P4i; P3 andP4, inferior). For all analyses, P-value was set at 0.05,corrected for deviations from sphericity (Greenhouse±Geisser epsilon method).

ERP source analysis was also performed on theInconguent vs Congruent di�erence wave for the Cov-ert and Manual Stroop tasks, using the BESA software(brain electrical source analysis) program [29]. Thisprogram places simulated dipoles in a three-shellspherical head model, and iteratively adjusts their lo-cations and orientations to try to achieve the best ®tbetween observed scalp potentials and the distributionsthat the model dipoles would produce.

3. Results

3.1. Task performance

In the mean Reaction Time analysis (Table 1), avery robust Stroop color-word interference e�ect wasobtained both in the Vocal version of the task,F(1,7)=104.8, P < 0.0001, mean e�ect size=85 ms;and in the manual version of the task (Manual4),F(1,7)=47.8, P < 0.0001, mean e�ect size=110 ms.For both choice and simple RT versions of the task,vocal and manual RTs were not statistically di�erent.Similarly, RTs to the congruent color-words (Man-ual4) were the same as RTs to the words in the Non-Color4 condition, F(1,7)=0.05, n.s. For the accuracydata, restricted to the manual version of the Strooptask, percent errors for incongruent color-words, con-gruent color words, and non-color words were enteredin a one-way ANOVA. Stimulus type was signi®cant,F(2,14)=5.1, P = 0.02. Simple mean e�ects revealed

signi®cantly more errors for incongruent than congru-ent and control color words, F= 8.6, P= 0.01, and F= 6.6, P = 0.022, respectively, and no di�erence forcongruent color words vs control non-color words, F=0.13, P=0.73, ns.

3.2. Event-related potentials

Fig. 1 shows the grand average ERP waveforms forFCz, Cz, Pzs (Pz, superior), and Pzi (Pz, inferior) forthe Stroop color words for the congruent and theincongruent words for the Overt Verbal version of theTask (left), the Covert Verbal task (center), and theManual version of the task (right). Note that theERPs for Inconguent and Congruent color wordsdiverge between 350±500 ms over scalp, with theIncongruent color word presenting a negative wave(peak at 410 ms) that is reduced in the ERP to thecongruent color word. Second, in the Covert andOvert versions of the task the e�ect is centered overmedial anterior scalp, while in the Manual Stroop taskthere is a more posterior and broader scalp distri-bution including anterior as well as central and pos-terior dorsal scalp (Fig. 1, right), and appearingslightly left-sided.

Fig. 3 shows the later Incongruent vs Congruentdi�erence between 500 and 800 ms (peaking with amaximum 600±700 ms), which center was on the leftposterior superior (temporo-parietal) scalp region andinverting over the anterior frontal region, that appearsto be due to a more protracted late positive complex(LPC) for Incongruent than Congruent and Controlcolor words for all response modalities (Fig. 2).

3.3. Early medial color interference (Stroop) e�ect(350±500 ms)

Table 2, top shows the results of the ANOVAs foreach of the time windows examined and each responsemodality. The strongest e�ects were in the 400±450 mswindow. For the Covert and Overt versions of thetask, there were signi®cant Trial Type � Site inter-actions. Speci®c comparisons analyzing the source ofthese interactions revealed that in the Overt task, therewere signi®cant Trial Type di�erences at frontocentral(F= 33.8, P= 0.002) and central sites (F= 23.7, P=0.005) but not at posterior sites (simple mean e�ects).There was also a signi®cant interaction with laterality,due to a signi®cant e�ect on the left at FC sites, butnot on the right (see Fig. 1). Similarly, for the Coverttask Stroop e�ects were present over frontocentral (F= 47.7, P = 0.0004) and central scalp (F = 20.6, P =0.005), but not over posterior scalp, with no lateralitye�ects. In contrast, in the Manual task, there werestrongly signi®cant main e�ects of Trial type, but nohint of a signi®cant interaction with site, due to a

M. Liotti et al. / Neuropsychologia 38 (2000) 701±711704

broader distribution of the Incongruent vs Congruentnegative di�erence extending over central and parietalsites as well (Table 2, top right).

The hypothesis of a scalp distribution di�erence ofthe early Stroop e�ects between response modalitieswas con®rmed by the results of the analysis on theIncongruent minus Congruent di�erence waves, after

amplitude normalization [19]. As predicted, there wasa signi®cant Response Modality � Site interaction,F(6,42)=6.0, P < 0.008. As expected, this interactionwas due to a signi®cant di�erence between Covert/Overt Tasks and the Manual Task at the two posteriorscalp locations (P < 0.01), and no di�erence over an-terior and central sites (Fig. 2, left).

Fig. 1. Top: Grand-average ERPs at FCz, Cz, Pzs and Pzi for Congruent color words (purple line) and Incongruent color words (blue line) Left:

Overt verbal task. Center: Covert verbal task. Right: Manual task. Vertical dashed line indicates peak of early frontal e�ect across the three ver-

sions of the task.

Bottom: Topographical maps of the voltage amplitudes for the Incongruent vs Congruent color word di�erence wave in the 400±450 ms win-

dow. Left: Overt verbal task. Center: Covert verbal task. Right: Manual task. Note the change in scalp topography between verbal versions of

the task (anterior medial) and the manual version of the task (broad dorsal).

M. Liotti et al. / Neuropsychologia 38 (2000) 701±711 705

To gain further insight into topographic di�erencesbetween the Stroop e�ects for the di�erent responsemodalities, as well as into possible sources for thesee�ects, we applied dipole source modelling to the earlymedial e�ect using the BESA program [29]. Our ®rstapproach to this modelling was to seed BESA with thestereotactic coordinates [32] of the anterior cingulatee�ect in Pardo et al.'s PET Stroop study (x = 8, y =15, z = 32 mm) [22], with the orientation only left tovary. At the peak of the activity (410 ms), this yieldeda solution with a residual variance (RV) of 20.3% forthe Covert Task, and 14.7% for the Manual Task (not

shown). We then proceeded with the following logic:Since we were interested in localizing possible genera-tors within dorsal cingulate cortex, we let x, y, andorientation of the dipole vary, while keeping the samez. This yielded improved single dipole solutions, to anRV=17% for the Covert task and an RV=12.5% forthe Manual task (see Fig. 2, right). The stereotacticcoordinates [32] were x=ÿ11, y = 6, z = 32 mm forCovert, with the Manual e�ect dipole estimate beingmore posterior (x=7, y=ÿ2, z=32). Thus, assumingour hypothesis that a major source of this activity wasarising from anterior cingulate cortex, these modelling

Fig. 2. Left: Mean Amplitudes of the Incongruent minus Congruent di�erence wave (400±450 ms) for each combination of scalp topography and

type of task. The early negativity is similar over frontocentral (FrCe) and Central (Ce) scalp, but signi®cantly di�erent over superior and inferior

parietal scalp (Par s, Par I) for the speech and manual versions of the task.

Right: BESA source dipole solutions for the early Stroop interference e�ect in the covert task (top) and manual task (bottom). RV=Residual

Variance. For both tasks, a dipole was placed in R anterior Cingulate [22]. z was kept ®xed (to constrain a solution in Anterior Cingulate), while

x, y and the orientation were free to vary.

Table 1

Summary of performance data. Top row: Group mean reaction time and standard deviation for the di�erent conditions of the study. Bottom

row: Group mean percent errors and standard deviation for the di�erent conditions of the study

Task Non-color Stroop Stroop Stroop Stroop Stroop Stroop

Man4 (Contr) Man4 (Cong) Man4 (Inc) Vocal4 (Cong) Vocal4 (Inc) Man1 Vocal1

Mean RT 601 (81) 598 (88) 708 (117) 627 (110) 712 (103) 284 (39) 332 (82)

Errors 3.1 (2.0) 2.2 (1.2) 9.2 (9.2)

M. Liotti et al. / Neuropsychologia 38 (2000) 701±711706

results suggested somewhat di�erent but nearby gen-erators in this region for the Stroop e�ect in theSpeech and the Manual versions of this task. Thisresult is consistent with the signi®cant di�erential scalpdistribution of these e�ects reported above (Fig. 2).

3.4. Late color interference (Stroop) e�ect (500±800ms)

Table 2, bottom, shows the results of the ANOVAsfor each of the time windows examined and each re-

sponse modality. The strongest e�ects were in the 600±700 ms window. For all response modalities, there wasno main e�ect of Trial Type, but signi®cant Trial Type� Site interactions. For all tasks, e�ects were signi®-cant over frontal scalp (Overt: P=0.001, Covert: P=0.01, Manual: P = 0.007) and parietal scalp (Overt: P=0.004; Covert: P=0.03; Manual: P=0.02). For allresponse modalities, there was a signi®cant Trial Type� Hemisphere interaction, due to Incongruent wordsbeing more positive over the left hemisphere, and nodi�erence for Congruent words (Fig. 3). The e�ects

Fig. 3. Grand-average ERPs at P3i and P4i for Congruent color words (purple line) and Incongruent color words (blue line). Top: Overt vocal

task. Center: Covert vocal task. Bottom: Manual task. On the right are topographical maps of the voltage amplitudes for the Incongruent vs

Congruent color word di�erence wave at in the 600±700 ms window. Note the similar left-sided scalp distribution in the three versions of the

task.

M. Liotti et al. / Neuropsychologia 38 (2000) 701±711 707

over frontal and left parietal scalp had identical timingfeatures in all modalities. Modelling of the dipolesources of the late Stroop e�ect was not carried out,because it was unlikely to have been produced by an-terior cingulate activation, and because we had noapriori hypothesis on the location of the generator,since this late posterior left-sided e�ect does notappear to have a clear counterpart in previous PETstudies of the Stroop e�ect.

4. Discussion

In the present study, robust behavioral and electro-physiological e�ects of color-word interference wereobtained across various versions (overt, covert, man-ual) of a mixed-trial Stroop task. Strong behaviorale�ects were obtained both in the standard vocal ver-sion of the task and in a manual choice-RT version ofthe task. Electrophysiological e�ects were obtained inall three Stroop conditions, including the covert vocalconditions for which no behavior was available. Acrossthe three tasks, processing of each attention-demand-ing incongruent color word relative to the more auto-matic processing of the congruent color word resultedin a biphasic activation involving ®rst medial dorsalscalp, and then left temporo-parietal and anterior fron-tal scalp.

These data provide new information on the time

course of the Stroop e�ect. In line with previous PET®ndings in the Stroop paradigm, we interpret the earlynegativity as originating in dorsal anterior cingulatecortex and relating to the need of suppressing or over-riding the processing of the incongruent word mean-ing. We interpret the late e�ect as later re-activation ofleft-sided regions involved in retrieval of the meaningof the incongruent color word.

4.1. Early anterior color interference e�ect(350±500 ms)

This consisted in a greater negativity of the Incon-gruent minus Congruent color word di�erence peakingat 410 ms. The e�ect in the present study had a dis-tinct scalp topography for the speech and manual ver-sions of the task (see Fig. 1), with a more focalanterior medial distribution in the ®rst, and a signi®-cantly di�erent, and more di�used, mid-dorsal distri-bution for the second. Dipole source modellingsuggested two independent sources in anterior cingu-late cortex for speech and manual modalities (see Fig.2, right). The anteromedial region activated in thespeech version of the task is reasonably close to thedorsal anterior cingulate activations reported in PETstudies of the Stroop e�ect [i.e., 6,22]. Our data indi-cate that a Covert Stroop task involves the same acti-vations in anterior frontal cortex as the classicalversion of the task, for which a behavioral e�ect can

Table 2

Top: Summary of results for the ANOVAs on the early Stroop e�ect (top) for the 350±400, 400±450, and 450±500 ms time windows. Bottom:

Summary of results for the ANOVAs on the late Stroop e�ect for the 500±600, 600±700, and 700±800 ms time windowsa

Task Overt Covert Manual

Trial Trial� Site Trial Trial� Site Trial Trial� Site

Time (ms) F P F P F P F P F P F P

Early e�ect

350±400 1.6 ns 4.9 0.060 1.7 ns 5.8 0.04� 5.8 0.05� 1.6 ns

400±450 4.4 0.080 8.7 0.02� 2.4 ns 15.6 0.002��� 28.6 0.001���� 0.1 ns

450±500 2.3 ns 11.8 0.008�� 0.1 ns 8.1 0.02� 3.1 ns 1.2 ns

Task Overt Covert Manual

Trial Trial� Site Trial�Hem Trial Trial� Site Trial�Hem Trial Trial� Site Trial�Hem

Time (ms) F P F P F P F P F P F P F P F P F P

Late e�ect

500±600 1.3 ns 21.6 0.002��� 2.3 ns 0.0 ns 6.2 0.04� 6.4 0.04� 0.1 ns 2 ns 8.7 0.02�

600±700 0.5 ns 29.6 0.001���� 4.6 0.070 1.0 ns 12.0 0.009�� 9.2 0.02� 1.3 ns 15.7 0.004��� 5.1 0.060700±800 0.0 ns 7.0 0.03� 4.9 0.060 1.0 ns 10.4 0.002��� 3.6 ns 1.2 ns 9.7 0.02� 7.7 0.03�

a �=< .05; ��=< .01; ���=< .005; ����=< .001;0=< .10.

M. Liotti et al. / Neuropsychologia 38 (2000) 701±711708

be concomitantly demonstrated. Therefore, the Covertversion can be employed in fMRI studies providedperhaps that behavior is recorded in the same subjectsand sessions shortly before or after to insure monitor-ing of cognitive performance in an overt version of thetask.

In the present manual 4-choice version of the Strooptask, robust RT interference e�ects were obtained, buta signi®cantly di�erent scalp distribution was observed,with a more di�used dorsal negative di�erence span-ning from anterior to posterior sites. Dipole modellingsuggested a more posterior source in anterior cingulatecortex. (Figs. 1 and 3). Our data indicate that manualStroop implicates di�erent subregion(s) of the anteriorcingulate than the classical vocal version of the Task.It has been hypothesized that a crucial role of the ACregion is response selection [24,25]. It is possible thatdi�erent AC subregions may be involved in the selec-tion of competing responses using di�erent e�ectors.This interpretation is supported by PET evidence ofnon-overlap of AC activations using hand, speech andsaccadic responses [23] and by recent evidence that AClesion (ACA aneurysm rapture) produces impairedmanual Stroop but not Verbal Stroop [35]. In addition,a recent high density ERP study suggested independentsources in the anterior cingulate associated with errordetection and target monitoring [3].

Our results have important implications for futureneuroimaging studies of the Stroop task. An Overt ver-sion of the Stroop task is considered to be di�cult toemploy with either ERPs or fMRI, due to motion arti-facts associated with overt speech. In this study, wefound that Stroop-related responses in the Overt taskwere mostly spatially and temporally separable fromspeech artifacts (most likely of muscular origin: ton-gue, lips and jaw movements and contraction of themasticatory muscles) which tended to produce largeamplitude potentials with negative polarity over the in-ferior orbital region, and positive polarity over inferioroccipital scalp areas bilaterally (at or below the Inion).The anterior Stroop incongruency e�ect was presentwith the same spatio-temporal features in the Covertversion of the task, in which no overt speech was pro-duced and the speech artifacts were absent (see in Fig.1). These results indicate that ERPs can be recordedfor cognitive tasks involving overt speech, when thecognitive e�ects of interest do not overlap in time orspace with such speech artifacts and special care istaken to selectively remove eye-movement activity[30,36].

Finally, it is important to compare the early interfer-ence e�ect with other published ERP ®ndings withsimilar latency and scalp distribution. The Stroopinterference e�ect is in the time range of the N400, anERP di�erence wave observed when a semantic con-text built by a sentence or a previous word is violated

(e.g., I eat my toast with ``butter'' vs I eat my toastwith ``socks''). The only published ERP study usingthe original Stroop task (covert version) reported anincongruent color interference e�ect peaking at 400ms, as in the present study [26]. That e�ect had a simi-lar broad dorsal distribution, with centro-parietalmaximum as the traditional N400 [10,16], and was infact interpreted as an N400 [26]. However that studyemployed a few electrodes, only in the midline. Amore anterior scalp distribution (midline frontal) of aN4-like e�ect has been observed in studies in whichnameable object meaning violated a previously estab-lished semantic context [4]. Importantly, an N400 in-terpretation appears unlikely in view of the di�erentscalp distribution of the interference e�ect for speechand manual responses.

4.2. Late left posterior color interference e�ect (500±800 ms)

A secondary ®nding of this study was the identi®-cation of a more extended late positive complex (LPC)in the incongruent relative to the congruent colorword peaking 600±700 ms post-stimulus onset and cen-tered over left posterior superior scalp, inverting po-larity over anterior frontal scalp. Such e�ect replicatedquite well in the three versions of the task (see Fig. 2,right). This di�erence is highly suggestive of a recur-sive process in which re-entrant activation of posteriorword processing regions takes place upon signalling ofcolor incongruence by anterior regions, possibly theanterior cingulate area. We were not able to tem-porally separate the left posterior positivity from anequally strong anterior frontal negativity (Fig. 3, Table2), since they appeared to wax and wane together.Although we cannot rule out the independent contri-bution of anterior frontal generators shown to play arole in ERP studies of semantic processing of words[1,3,30,36], the combined frontal and posterior distri-bution is more suggestive of a major contributionfrom a left posterior generator. Similar topographyinversions from dorsal scalp to ventral scalp regionshave been reported for both the P300 and the N400using the average reference (as used here) rather thana mastoid reference [1,34,]. A number of high-densityERP studies support the idea that the left-lateralizedLPC e�ects may re¯ect semantic processing of theword meaning. In particular, a left-lateralized LPCe�ect with similar scalp distribution and timing wasobserved when the ERP covertly or overtly repeating aword was subtracted by the ERP covertly or overtlygenerating a verb related to a presented word [1,30,37].Dipole modelling provided solutions interpreted assources in the Wernicke's region [1,30].

M. Liotti et al. / Neuropsychologia 38 (2000) 701±711 709

5. Conclusion

The results reported here would not have been poss-ible without the selective averaging capabilities pro-vided by the ERP technique, allowing the extraction ofthe speci®c contribution of congruent and incongruentwords within the same blocks of trials, and withoutthe high temporal resolution provided by ERPs, indi-cating the exact temporal course and the highlydynamic nature of these e�ects.

This study clari®es the timing of activations duringthe Stroop color-word interference e�ect. An earlynegative interference e�ect peaks at 410 ms, withdi�erent scalp topography for speech and manual ver-sions of the task, and distinct anterior source genera-tors, possibly in the Anterior Cingulate region. Thise�ect is followed by a protracted late positive complexfor incongruent relative to congruent words between500±800 ms, centered over left posterior superior (tem-poroparietal) cortex and anterior frontal areas, poss-ibly re¯ecting activation of word meaning regions.

Acknowledgements

The authors wish to thank Dr. Christie Thomas forhelpful comments in earlier versions in of the manu-script.

References

[1] Abdullev YG, Posner MI. Event-related brain imaging of

semantic encoding during processing of single words.

Neuroimage 1997;7:1±13.

[2] Aine CJ, Harter MR. Event-related potentials to Stroop stimuli:

color and word processing. Annals of the New York Academy

of Sciences 1984;425:152±3.

[3] Badgaiyan RD, Posner MI. Mapping the cingulate cortex in re-

sponse selection and monitoring. Neroimage 1998;7:255±60.

[4] Barrett SE, Rugg MD. Event-Related Potentials and the seman-

tic matching of pictures. Brain and Cognition 1991;14:201±12.

[5] Bench CJ, Friston KJ, Brown RG, Scott LC, Frackowiak RS,

Dolan RJ. The anatomy of melancholia Ð focal abnormalities

of cerebral blood ¯ow in major depression. Psychological

Medicine 1992;22:607±15.

[6] Bench C, Frith CD, Grasby PM, Friston KJ, Paulesu E, et al.

Functional anatomy of attention using the Stroop test.

Neuropsychologia 1993;31:907±22.

[7] Burock MA, Buckner RL, Woldor� MG, Dale AM.

Randomized event-related experimental designs allow for extre-

mely rapid presentation rates using functional MRI.

Neuroreport 1998;9(16):3735±9.

[8] Carter CS, Mintun M, Cohen JD. Interference and facilitation

e�ects during selective attention: an H2O-15O PET study of

Stroop task performance. Neuroimage 1995;2:264±72.

[9] Carter CS, Mintun M, Nichols T, Cohen JD. Anterior cingulate

gyrus dysfunction and selective attention de®cits in schizo-

phrenia: a [15O]H2O PET study during single-trial Stroop task

performance. American Journal of Psychiatry 1997;154:1670±5.

[10] Curran T, Tucker DM, Kutas M, Posner MI. Topography of

the N400: brain electrical activity re¯ecting semantic expectancy.

Electroencephalography and Clinical Neurophysiology

1993;88:188±209.

[11] Derbyshire SW, Vogt BA, Jones AK. Pain and Stroop interfer-

ence tasks activate separate processing modules in anterior cin-

gulate cortex. Experimental Brain Research 1998;118:52±60.

[12] Drevets WC, Price JL, Simpson Jr JR, Todd RD, Reich T, et

al. Subgenual prefrontal cortex abnormalities in mood dis-

orders. Nature 1997;386:824±7.

[13] George MS, Ketter TA, Parekh PI, Rosinsky N, Ring H, et al.

Regional brain activity when selecting response despite interfer-

ence: An H215O PET study of the Stroop and emotional Stroop.

Human Brain Mapping 1994;1:194±209.

[14] George MS, Ketter TA, Parekh PI, Rosinsky N, et al. Blunted

left cingulate activation in mood disorder subjects during a re-

sponse interference task (the Stroop). Journal of

Neuropsychiatry & Clinical Neurosciences 1997;9:55±63.

[15] Grapperon J, Vidal F, Leni P. The contribution of cognitive

evoked potentials to knowledge of mechanisms on the Stroop

test. Neurophysiologie Clinique 1988;28:207±20.

[16] Kutas M, Hillyard SA. Reading senseless sentences: brain po-

tentials re¯ect semantic incongruity. Science 1980;207:203±5.

[17] Mayberg HS, Brannan SK, Mahurin RK, Jerabek PA,

Brickman J, et al. Cingulate function in depression: a potential

predictor of treatment response. Neuroreport 1997;8:1057±61.

[18] Mayberg HS, Liotti M, Brannan SK, McGinnis S, Mahurin

RK, et al. Reciprocal limbic-cortical function and negative

mood: converging PET ®ndings in depression and normal sad-

ness. American Journal of Psychiatry 1999;156:1675±82.

[19] McCarthy G, Woods CC. Scalp distributions of event-related

potentials: an ambiguity associated with analysis of variance

models. Electroencephalography and Clinical Neurophysiology

1985;62:203±8.

[20] McKeown MJ, Jung TP, Makeig S, Brown G, Kindermann SS,

et al. Spatially independent activity patterns in functional MRI

data during the Stroop color-naming task. Proceedings of the

National Academy of Sciences USA 1998;95:803±10.

[21] Morton J, Chambers SM. Selective attention to words and col-

ors. Quarterly Journal of Experimental Psychology 1973;25:387±

97.

[22] Pardo JV, Pardo PJ, Janer KW, Raichle ME. The anterior cin-

gulate cortex mediates processing selection in the Stroop atten-

tional con¯ict paradigm. Proceedings of the National Academy

of Sciences USA 1990;87:256±9.

[23] Paus T, Petrides M, Evans AC, Meyer E. Role of the human

anterior cingulate cortex in the control of oculomotor, manual

and speech responses: a positron emission tomography study.

Journal of Neurophysiology 1993;70:453±69.

[24] Posner MI, Petersen SE. The attentional sytem of the human

brain. Annual Review of Neuroscience 1990;13:25±42.

[25] Posner MI, Raichle ME. Images of mind: exploring the brain's

activity. New York: W. H. Freeman, 1994 [Scienti®c American

Library].

[26] Rebai M, Bernard C, Lannou J. The Stroop's test evokes a

negative brain potential, the N400. International Journal of

Neuroscience 1997;91:85±94.

[27] Rosen BR, Buckner RL, Dale AM. Event-related functional

MRI: past, present and future. Proceedings of the National

Academy of Sciences USA 1998;95:773±80.

[28] Rousseaux M, Godefroy O, Cabaret M, Benaim C, Pruvo JP.

Analysis and course of cognitive de®cits after rupture of aneur-

ysms of the anterior communicating artery. Revue

Neurologique 1996;152:678±87.

[29] Scherg M, Picton TW. Separation and identi®cation of event-re-

lated potential components by brain-electrical source analysis

M. Liotti et al. / Neuropsychologia 38 (2000) 701±711710

(BESA). Electroencephalography and Clinical Neurophysiology

1984;42:24±37.

[30] Snyder AZ, Abdullaev YG, Posner MI, Raichle ME. Scalp elec-

trical recordings re¯ect cerebral blood ¯ow responses during

processing of written words. Proceedings of the National

Academy of Sciences USA 1995;92:1689±93.

[31] Stroop JR. Studies of interference in serial verbal reactions.

Journal of Experimental Psychology 1935;18:643±62.

[32] Talairach J, Tournoux P. Co-planar stereotaxic atlas of the

human brain. New York: Thieme, 1988.

[33] Taylor SF, Kornblum S, Lauber EJ, Minoshima S, Koeppe

RA. Isolation of speci®c interference processing in the Stroop

task: PET activation studies. Neuroimage 1997;6:81±92.

[34] Tucker DM, Liotti M, Potts GF, Russell GS, Posner MI.

Spatiotemporal analysis of brain electrical ®elds. Human Brain

Mapping 1998;1:134±52.

[35] Turken A, Swick D. Attention and anterior cingulate cortex.

Cognitive Neuroscience Society Abstracts 1998;s14:143.

[36] Van Turennout M, Hagoort P, Brown CM.

Electrophysiological evidence of the time course of semantic

and phonological processes in speech production. Journal of

Experimental Psychology: Learning, Memory & Cognition

1997;23:787±806.

[37] Woldor� MG, Prigden S, Liotti M, Perez III R, Fox PT. The

time course of verb generation. Neuroimage 1998;7:S160.

M. Liotti et al. / Neuropsychologia 38 (2000) 701±711 711