Working memory processes show different degrees of lateralization: Evidence from event-related...

Working memory processes show different degrees oflateralization: Evidence from event-related potentials

DURK TALSMA,a ALBERTUS A. WIJERS,b PETER KLAVER,c and GIJSBERTUS MULDERb

aPsychonomics Department, University of Amsterdam, The NetherlandsbExperimental and Occupational Psychology, University of Groningen, The NetherlandscKlinik und Poliklinik Für Epileptologie, Bonn, Germany

Abstract

This study aimed to identify different processes in working memory, using event-related potentials~ERPs! and responsetimes. Abstract polygons were presented for memorization and subsequent recall in a delayed matching-to-sampleparadigm. Two polygons were presented bilaterally for memorization and a cue indicated whether one~and if so, whichone of the two! or both polygons had to be memorized. A subsequent test figure was presented unilaterally to the leftor right visual field and had to be compared with the memorized figure~s!. ERP results suggested that memorizationtakes place in a visual buffer in contralateral posterior brain areas, whereas identification of the test stimulus as a targetappears to be mainly a left hemispheric process. Increased response times were found for nontarget test stimuli ascompared to targets, and for target test stimuli that were presented contralaterally with respect to the location of thememorized stimulus. In addition, response times were slower when two figures were memorized than when only onewas memorized.

Descriptors: Visual working memory, ERPs, N2pc, Lateralization

Working memory~Baddeley, 1986, 1992; Baddeley & Hitch, 1974!refers to a short-term memory system capable of storing, manip-ulating, and actively maintaining visual and auditory information.In Baddeley’s model, working memory consists of two modality-specific slave systems, the phonological loop and the visuospatialsketchpad, and a central executive. The phonological loop is aspeech-based store coupled with an articulatory~subvocal! re-hearsal process. This process is capable of maintaining the materialin the phonological store by using a recycling process. The visuo-spatial sketchpad is used for temporary storage of visuospatialinformation. The central executive system controls processes suchas the information transfer to and from the slave systems and theinteraction between working memory and long-term memory. Inaddition, it is also involved in controlling attention-demandingmemory processes. The remainder of this article will focus onvisual working memory.

Recently, a growing number of studies have investigated thefunctional, physiological, and neuroanatomical aspects of visualworking memory, using behavioral measures and neuroimagingtechniques~Gratton, 1998; Gratton, Fabiani, Goodman-Wood, &

Desoto, 1998; Mecklinger & Pfeiffer, 1996; Smith et al., 1995!. Onthe basis of this work, Smith and Jonides~1997! have extendedBaddeley’s working memory model in two important respects.First, they suggested that there are two distinctive memory storesfor visual information, one for object~shape! information, and onefor visuospatial~location! information. Secondly, they proposedthat in order to retain information in visual memory, this informa-tion should be continuously mentally rehearsed, just as phonolog-ical information should be in Baddeley’s original model~i.e.,articulatory rehearsal!.

Importantly, recent neuroimaging research on humans, andanatomical, physiological, and behavioral findings in monkeys,have led to converging evidence regarding the organization ofworking memory in the brain. The general consensus appears to bethat visual working memory involves the concerted activity of adistributed neural system, including posterior areas in visual cortexand anterior areas in prefrontal cortex~Ungerleider, Courtney, &Haxby, 1998!. However, several views have been proposed thatvary in subtle ways with respect to the exact neural circuitryinvolved, and the functional significance of the different brainareas.

Smith and Jonides~1997! have argued for hemispheric lateral-ization differences for different types of working memory. Theyproposed that spatial working memory involves the superior pari-etal and prefrontal areas of the right hemisphere, whereas objectworking memory involves superior parietal, inferior temporal, andprefrontal areas in the left hemisphere. Others have more stronglyemphasized domain-specific specializations of different corticalregions, and the similarities with regional specializations found in

This research has been made possible by a fellowship from the RoyalNetherlands Academy of Arts and Sciences. We thank Joop Clots, EdwinKiers, Jan Smit, Eise Hoekstra, Ben Mulder, and Mark Span for technicalsupport. We also thank Gabriele Gratton and an anonymous reviewer fortheir valuable comments on an earlier version of the manuscript.

Address reprint requests to: Durk Talsma, Psychonomics Department,University of Amsterdam, Roetersstraat 15, 1018 WB Amsterdam, TheNetherlands. E-mail [email protected]

Psychophysiology, 38~2001!, 425–439. Cambridge University Press. Printed in the USA.Copyright © 2001 Society for Psychophysiological Research

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the visual perceptual system. For instance, Haxby et al.~1994!have measured changes in regional cerebral blood flow~rCBF! byusing positron emission tomography~PET! while subjects per-formed object~face! identity and spatial location match-to-sampletasks. Ungerleider et al.~1998! noted with respect to this experi-ment that the locations of the activated occipitotemporal and occi-pitoparietal regions in the face matching and spatial locationmatching conditions, respectively, are in good agreement withother PET studies of face perception and visuospatial processing.Thus, the brain organization of working memory would resemblethe organization of the visual system, with a ventral, occipitotem-poral “what” system specialized for the perception and memori-zation of objects, and a dorsal, occipitoparietal “where” systemspecialized for the perception and memorization of spatial infor-mation~Farah, Hammond, Levine, & Calvanio, 1988; Haxby et al.,1991; Ungerleider & Miskin, 1982!.

Recently, a number of neuroimaging studies that require pro-cessing the contents of working memory have found an increasedactivation in the dorsolateral prefrontal cortex~Cohen et al., 1994;Petrides, Alivisatos, Evans, & Meyer, 1993; Petrides, Alivisatos,Meyer, & Evans, 1993; see also Fuster, 1997, for an extensivediscussion!, which is assumed to be a brain area closely associatedwith central executive functions~D’Esposito et al., 1995!.

Ungerleider et al.~1998! have considered the hemispheric lat-eralization of different forms of visual working memory to berather variable. These authors reviewed literature that suggests thatleft lateralization for object working occurs under conditions thatare relatively favorable for a verbal or symbolic encoding strategy.In general, they have concluded that laterality effects in visualmemory may be influenced by a variety of factors, such as memoryset size, retention interval length, and item familiarity, all of whichmay affect the extent to which subjects engage in symbolic orverbal encoding and rehearsal.

It is also conceivable that variations in hemispheric lateraliza-tion reflect other processing differences as well. In this context, therelatively low temporal resolution of neuroimaging techniquessuch as PET and fMRI may have important consequences. In atypical PET study, for instance, a single subtraction image revealsall the brain areas that were more active in a working memorycondition as compared to a control condition. Therefore, it is verydifficult ~at least on the basis of PET data alone! to relate thefunction of these different brain areas to the different processingstages within a working memory task, such as encoding, storage,maintenance, matching, and retrieval. In principle, it could well bethat different processing stages show different hemispheric later-alizations~as has been proposed for long-term memory encodingand retrieval processes; Nyberg et al., 1996!. In that case, varia-tions in hemispheric lateralizations in different working memoryexperiments could reflect differences in the relative contribution ofparticular processing stages.

To analyze different stages of working memory processes moreexplicitly, we used a matching-to-sample task~Desimone, 1996;Ruchkin, Johnson, Grafman, Canoune, & Ritter, 1996! in which amemory set that was presented at the beginning of each trial had tobe compared with a test stimulus that was presented after a delay.Using event related potentials~ERPs!, this paradigm made it pos-sible to study the effects of different processing stages in workingmemory. First, upon presentation of the memory set, the stimuli hadto be perceived, encoded in working memory, stored, and main-tained. After the test stimulus was presented, another set of oper-ations had to take place. The memorized information had to beretrieved from working memory, and matched with the test stimulus.

Most notably, the general goals of the present study are thefollowing: ~a! to answer the question to what degree retrieval andmatching processes are lateralized,~b! to examine whether or notworking memory for objects stores information regarding the spa-tial position of the memorized objects, and~c! to determine whetherspatial information, if present in object working memory, influ-ences the lateralization of retrieval and matching processes.

To reach these goals, we designed a task in which two polygonswere presented for 1,000 ms bilaterally on a computer screen.During the presentation of these two stimuli, a cue was presentedthat instructed the subjects to memorize for subsequent recognitionthe stimulus presented to the left, the stimulus to the right, or bothstimuli. Thus, the cue served to indicate the memory set, a set ofone figure, originally presented to the left or right of fixation, or aset of two figures~note that always two figures were presented, butthat either one or two of them had to be retained for subsequenttesting!. After a 1,500 ms delay in which only a fixation point wasvisible, a probe stimulus was presented to either the left or rightvisual half-field. Subjects had to decide whether or not the probebelonged to the memory set. Abstract polygons were used in orderto minimize the chances of subjects adopting a verbal strategy.Using this paradigm, both ERPs and response times were mea-sured. ERPs were measured during two successive intervals. Thefirst started with the presentation of the memory set, and lasteduntil the presentation of the test stimulus~the “retention interval”!.The second interval started after presentation of the test stimulusand lasted until 1,000 ms after onset of the test stimulus~the “testinterval”!. Although ERPs were recorded during both the retentionand the test interval, the current article focuses on the ERPs foundduring the test interval, as the results found during the retentioninterval are reported elsewhere~Klaver, Talsma, Wijers, Heinze, &Mulder, 1999!.

It should be noted that the paradigm used in the present studybears resemblance to the object memory condition of the paradigmused by Smith et al.~1995! to distinguish object working memoryfrom spatial working memory. However, a number of differencesexist between our experiment and the one of Smith et al. First, weused ERPs, whereas Smith et al. used PET, allowing us to deter-mine the time course of various working memory processes moreprecisely during the retrieval of visual stimuli from working mem-ory. Secondly, we instructed subjects to memorize the shape of thepolygons, regardless of their location. Comparing the ERP re-sponses to probe stimuli presented at the same location as thememory stimulus with the ERP responses to probe stimuli thatwere presented opposite to the memorized figure allowed us toinvestigate whether spatial information is retained in object mem-ory, even when this is not required for task performance.

As mentioned earlier, the present study addresses the questionof whether the spatiotemporal aspects of several object workingmemory processes can be addressed using ERPs. The currentresearch questions that will be addressed in this article are, there-fore: ~a! Which processes are involved in retrieving stimuli fromworking memory?~b! Are the brain areas involved in these pro-cesses lateralized, as found by Smith and Jonides~1997!, or arethese processes localized bilaterally~cf. Ungerleider et al., 1998!?and ~c! Does location have an influence on the retrieval process?

With regard to the present article, a number of ERP compo-nents are of particular interest. Most notably, these components arethe P1, N1, N2pc, and the P300 components. Research has con-sistently demonstrated that a lateralized stimulus presented at aspatially attended position elicits ERPs with enhanced P1 and N1components as compared to an identical stimulus when attention is

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directed elsewhere in the visual field~for a review, see Wijers,Mulder, Gunter, & Smid, 1996!. The enhancements of the P1 andN1 components can be interpreted as the result of an early atten-tional “sensory gain” mechanism that selectively enhances thesensitivity of the neural pathways processing the attended location~Mangun & Hillyard, 1995!. The N2pc~Luck & Hillyard, 1994! isan N2-like component, a negativity elicited by target stimuli rel-ative to nontargets~Eimer, 1996; Wijers, Lange, Mulder, & Mul-der, 1997!, with a maximum over the posterior scalp contralateralto the visual field of the target. Eimer has suggested that the N2pcreflects a top-down target identification mechanism.

The last component of interest is the P300. The latency of theP300 is generally considered as an index of the duration of stim-ulus evaluation processes, and to be insensitive to processes relatedto the selection, preparation and execution of a motor response~e.g., Magliero, Bashore, Coles, & Donchin, 1984; McCarthy &Donchin, 1981!.

It is expected that ERPs will reveal at least a number ofprocesses associated with retrieval from working memory. Asmentioned, retrieving information from working memory is one ofthe processes that is considered to be performed by the centralexecutive. Because central executive processes are closely relatedto attention-demanding processes, it is plausible that a number ofERP results from attention studies will also be found in the presentstudy.

A major question is whether spatial information is representedin object working memory. If an object was memorized at theposition at which it was originally presented~even though positionwas irrelevant for task performance!, it is expected that spatialattention will remain directed at the location of the memorizedstimulus~Awh, Smith, & Jonides, 1995!. It is expected that duringretention of the memorized stimulus, attention remains focused atthe location of the memorized stimulus. In that case, the ERPselicited by test stimuli presented at the same position as thememorized figure are expected to show enhanced P1 and N1components as compared to ERPs elicited by test stimuli presentedat the opposite position.

Second, the test stimulus had to be matched against the mem-orized stimulus or stimuli. Based on the work of Eimer~1996! andWijers et al.~1997!, it is expected that a working memory targetidentification process will be reflected in an effect similar to theN2pc, which is expected to be most pronounced over the posteriorhemisphere, contralateral to the presentation side of the test stimulus.

Third, after the test stimulus has been identified, a response hadto be made. It can be expected that it will take longer to respondto test stimuli that are presented contralaterally with respect to thememorized stimulus. Although it is not required to memorize thelocation of the memorized stimulus, it can be expected that adifference in location between the memorized stimulus and the teststimulus will act as a distractor, and therefore slow down responsetimes. Moreover, it is expected that test stimuli presented contra-laterally to the memorized stimuli will take longer to evaluate,which will be reflected in an increased latency of the contralateralP300.

Method

ParticipantsFourteen participants volunteered for the experiment. Two of themwere excluded from the experiment due to excessive EOG activity.Of the remaining 12 participants, five were women. The mean agewas 22, ranging from 20 to 27. All subjects were students at the

University of Groningen, right-handed, and had normal or corrected-to-normal vision. They were ignorant with respect to the purposeof the present study and received a verbose debriefing and insightin their behavioral results after finishing the experiment. Partici-pants were paid 10 Dutch guilders per hour for participating in theexperiment.

Stimulus PresentationStimulus presentation is depicted in Figure1. Each trial startedwith the presentation of two vertical lines, to the left and right ofa centrally presented fixation dot. These lines served as a cue andwere presented for 1,250 ms. Subsequently, on each trial twopolygon figures were presented for 1,000 ms, at an angle of about5 degrees in the horizontal line of sight, to the outside of the cuelines, which remained visible during this second interval. Whenthe cue line was colored red, the figure on the corresponding sideof the display had to be memorized; if the other line was green, thefigure on the opposite side could be ignored; if both were red, bothfigures should be retained. Thus, in all trials two figures werepresented in the retention interval, and the cue randomly indicatedone of the three memory conditions~low memory load: memorizethe left or the right figure, or high memory load: memorize bothfigures!. In the third frame, only a fixation dot was presented, for1,500 ms; in this interval subjects had to retain the cued stimuliwithout external information. In the fourth frame, a single teststimulus was presented randomly with equal chance to the left orthe right of the fixation dot. The test figure was presented at anangle of about 5 degrees from the fixation point in the horizontalline of sight. Subjects had to respond to the test stimulus bydeciding whether or not it was identical to~one of! the cuedmemory set figure~s!. The test stimulus was presented for 500 ms.A fifth frame was presented for 1,750 ms and contained only afixation dot. During this time, subjects were still allowed to re-spond. Responses were made by raising the left and right indexfinger from a button marked either “YES” or “NO.” The assign-ment of the YES and NO button was balanced across subjects.

There were 12 different trial types~stimulus categories!, de-fined by the combination of memory cueing~left, right, or both!,visual field of test stimulus presentation~left or right!, and targettype ~memorized: target, or not memorized: nontarget!. When anontarget test figure was presented, and subjects had been cued tomemorize only one figure, the nontarget figure was also differentfrom the ignored figure presented in the retention interval. Foreach stimulus category a total of 100 trials was presented. Acomputer assigned each trial randomly to one of 25 blocks, eachconsisting of 48 trials.

Polygon ConstructionThe stimuli used in this experiment consisted of a set of 200polygons. The basic shape of each figure was a 10-sided polygon.The x and y coordinates of each vertex were computed as follows.First, ten radials were defined, each starting at the origin of thecoordinate system and separated from the previous by an angle of36 degrees. On each radial, a random distance was calculated. Thethus created vertices were connected and finally the created figurewas filled with the color white. To control for illuminance, eachfigure was resized to match a standard size between 2,250 and2,500 pixels, subtending a visual angle of about 1.4 degrees. Usingthis procedure, 4,000 prototype figures were generated. Because itwas found in pilot studies that subjects had trouble discriminatingthe figures from each other, an index for each figure’s shape wascalculated. By comparing the shape index of each figure to each

Lateralization in working memory processes 427

other prototype, an index of uniqueness was obtained for eachfigure.1 The 200 figures with the highest uniqueness score wereselected and saved as an image file.

ProcedurePreceding each measurement, all trials were randomly distributed;therefore, each subject received a unique series of stimuli. Afterattachment of the electrodes, participants were given several blocksof practice trials. These practice trials were the same as the trialsused in the experiment, except that during practice only 24 trialswere presented in a block and no EEGs were measured. Partici-pants were required to continue practicing until the followingcriteria were met. Their mean error percentage had to be less then20% and their average overall response times should be stable andlie in an interval that ranged approximately from 600 to 700 ms.During this session, the participants were also trained in fixating atthe center of the screen and the experimenters provided feedbackon their performance. During the experiment, participants werepermitted a small break between two task blocks and were re-quested to take one when the experimenters, monitoring the re-sults, noticed that the behavioral results in a given task blockdropped below the performance criteria met during the trainingsession.

Instrumentation and RecordingParticipants were seated in a comfortable chair, in a sound-attenuated room. Stimuli were presented on a 14-in. VGA com-puter display. The experiment was monitored from an adjacentroom. The presentation of the stimulus material and the datacollection was controlled by a personal computer. EEG measure-ments were made using 31 Ag-AgCl electrodes, at the standard10020 locations plus PO7, PO8, PO3, PO4, Oz, P9, P10, PO9, Oz,P9, P10, PO9, PO10, O9, O10, and Iz. Horizontal eye movementswere measured by deriving an electro-oculogram~EOG! from twoelectrodes, located to the outer canthi of the eyes. Vertical EOGwas derived from the FP1 electrode. All EEG electrodes weremeasured relative to a reference electrode attached to the left earlobe. The impedance of each electrode was kept below 5 kV. EEGand EOG were amplified with a 10-s time constant and a 200-Hzlow pass filter, sampled at 1000 Hz, digitally low pass filtered witha cut-off frequency of 30 Hz, and on-line reduced to a samplefrequency of 100 Hz. The data were digitally stored for off-lineanalysis.

Data AnalysisBehavioral data.Average response times were calculated for thecorrect responses for each stimulus category. In addition, a meanpercentage of error was calculated per stimulus type. The resultingaverage response times and error percentages were used as input ina SPSS-MANOVA within-subjects analysis. In these analyses thefollowing factors were tested: Memory~three levels: memorizeleft, right, and both figures!, Visual Field to which the test stimuluswas presented~two levels: left and right visual field! and Tartype~two levels: targets versus nontargets!. After this overall analysis,planned comparisons were performed to elucidate the interpreta-tion of the interactions~memory left versus memory right, andmemory left and memory right versus memory both!. Greenhouse–Geisser correction was applied to tests involving the factor Memory.

1The following procedure was used to select the figures. First, for eachfigure, the point of gravity was calculated, which was defined as the meanof the mathematical points of gravity, of the 10 triangles each polygon wascomposed of. Second, the sum of the distances from the center of gravityof each of the 10 vertices of the polygon was calculated. The thus obtainedsum distance was used to calculate a differentiation score. This was doneby comparing the current figure to each other and calculating the differencebetween the current figure’s sum distance and the other figure’s sumdistance. For each comparison, the absolute value of this difference wasadded to the current figure’s differentiation score.

Figure 1. Outline of the present paradigm.~a! Schematic representation of the duration of each frame and interval.~b! Example ofstimuli presented during one trial.


Physiological data.ERPs were averaged off-line. Using anautomatic artifact detection program, trials containing horizontalEOG ~criterion 20mV !, vertical EOG~criterion 50mV !, and outof range artifacts were rejected.2 ERP trials associated with incor-rect responses were also excluded. Trial length was 1,100 ms, andstarted 100 ms before the onset on the test stimulus~a differenttrial interval was chosen for the analyses of the ERP data in theretention interval; see Klaver et al., 1999!. The 100-ms prestimulusinterval was taken as the baseline voltage. Averages were calcu-lated separately for the different subjects and for the differentstimulus categories.

Target0nontarget difference waves.Difference waves were com-puted by subtracting the ERPs to nontarget figures from theERPs to target figures, for the electrode pair P70P8 ~visualinspection revealed that the target-nontarget difference wavesshowed a maximal N2pc at these electrodes!. Mean amplitudesfor these difference waves, in latency bands of 20 ms~coveringthe 160–500 ms latency range! were submitted to an SPSS-MANOVA using a repeated measurement design. The effects ofthe following factors on the difference waves were tested: Hemi-sphere~P7 versus P8!, Memory Load ~memorizing one versustwo figures!, Visual Field ~the test figure being presented to theright versus left visual field!, and IpsiCon~the test stimulusbeing presented to the same versus opposite visual field as~oneof ! the memorized figure~s!!. It should be noted that maineffects of the difference waves are reflected in a significance ofthe factor Constant, that indicates whether the difference wavesdiffer significantly from zero. To reduce the chances of a type Ierror, due to the relative high number of tests, effects were con-

sidered significant only when two or more consecutive 20-ms in-tervals showed an effect.3

P1 and N1 components.P1 and N1 amplitudes were computedat the electrode pair PO70PO8 as the mean amplitudes of the threeERP samples centered at the peaks of the P1 and N1 componentsin the grand-average ERP. P1 latency was somewhat earlier at theelectrode contralateral to the visual field of the test stimulus.Therefore, P1 amplitude was computed as the mean amplitude inthe 100–120-ms interval contralaterally, and in the 130–150-msinterval ipsilaterally. N1 latency was identical for the ipsilateraland contralateral electrodes. N1 amplitude was computed as themean amplitude in the 170–190-ms latency range.

P1 and N1 amplitudes values were submitted to SPSS-MANOVA’s. The tested factors were Memory~memorize left fig-ure, memorize right figure, memorize both figures!, Visual Field~the test figure being presented to the right versus left visualhalf-field!, and Hemi-Lat~electrodes over the hemisphere ipsilat-eral versus contralateral to the visual field of the test figure!.Greenhouse–Geisser correction was applied for tests involvingMemory.

The P300.The P300 was determined as the maximum ampli-tude in the 300–1,000 ms interval at Pz. P300 amplitudes andlatencies were submitted to an SPSS-MANOVA analysis. The firstanalysis tested the factors Tartype~targets versus nontargets!, Mem-ory ~memorize left, memorize right, and memorize both!, andVisual Field ~test figure presented in the right versus left visualhalf-field!. The second analysis was confined to the target ERPsand tested for the factors Memory Load~memorize one versus twofigures!, Visual Field ~right versus left!, and IpsiCon~the testfigure presented to the same side as~one of! the memorizedfigure~s!, or to the opposite side.4

Results

Behavioral DataThe average response times are shown graphically in Figure 2.Visual inspection of Figure 2 suggests the following effects. First,responses to stimuli in the high memory load condition~Figure 2,bottom row! were slower than responses to stimuli in the lowmemory load condition~Figure 2, top row!. Second, when targettest stimuli were presented in the same visual field as the memo-rized stimuli, responses were faster, as compared to test stimuli

2EOG detection for the present data was done only in the period of teststimulus presentation. Therefore, in principle, the participants could havemoved their eyes to the memory items in the retention interval, and thiswould remain undetected in the present analysis.~For the data in theretention interval, as reported by Klaver et al.~1999!, a different intervalfor averaging and EOG detection was chosen.! For the following reasons,we consider it unlikely that the data are much influenced by eye movementbehavior.~a! In the training phase participants were strongly discouragedfrom moving their eyes from fixation. During training, and also during thesubsequent experimental measurements, the EOG signal was continuouslymonitored by the experimenter. If the experimenter saw systematic hori-zontal EOG activity, in the subsequent break the participant was againstressed not to move the eyes. Two of the participants who failed to complywith these instructions were excluded from the experiment.~b! Althoughnot shown in the present article, the averaged interval included also theretention interval~although no EOG detection was done for this interval!.Inspection of the averaged horizontal EOG showed that there was indeedsome EOG activity in the retention interval, systematically related to theside of the cued memory figure. However, the amplitude of this activitywas small~about 4mV ! relative to the size of the horizontal EOG signalsin the trials that were rejected in the analysis of the retention interval~about30 mV; Klaver et al.!. Therefore, this residual EOG activity probablymostly reflects small, involuntary eye movements, much smaller than afull-blown fixation of the memory figure.~c! The main conclusions in thepresent article pertain to lateralization effects as a function of the relativepresentation sides of the memory and test figures. If participants hadfixated the memory figure on each trial, so that each figure was memorizedat the fovea, there would be no difference between memory figures in theleft versus right visual field, and no difference between the test figuressubsequently being presented to the right or left. Nevertheless, clear per-formance and ERP results were obtained as a function of the relationbetween the visual fields of the memory and test figures~see Resultssection!. The important general point is that eye movement behavior couldnot have contributed to the kinds of effects we report here, but rather wouldhave tended to diminish such effects.

3When testing this many intervals~17 mean amplitude variables!, therisk of capitalizing on chance has to be dealt with. The significancecriterion for one interval was set at 0.05. As 17 intervals were tested, foreach factor there is a chance of 173 0.055 0.85 that one of the intervalswould show an effect. If the criterion of two consecutive intervals is used,this chance is reduced to 0.04~16 3 0.053 0.05!, a value lower than thesignificance criterion of 0.05.

4It should be noted that the first and the second analyses for the P300latencies and amplitudes are somewhat different. In the high memory loadcondition, whenever a target was presented, one of the two stimuli from thememory set was randomly chosen. So for the high memory load condition,the location of the stimulus that was actually chosen was used in definingthe factor IpsiCon. For nontargets, presented in the high memory loadcondition, no such location could be defined, however, because the stimuliat both locations were cued for memorization and an entirely new figurewas presented as a test stimulus. Hence, no factor IpsiCon could be definedfor the latter category. For this reason, the second analysis was confined totarget stimuli only.


presented contralaterally relative to the memorized stimulus~Fig-ure 2, left column!. For nontarget stimuli, on the contrary, it did notmatter whether the test stimulus was presented at the same side asthe memorized figure or at the opposite side~Figure 2, upperright!.

These observations were confirmed by statistical analyses. Asignificant effect of Memory,F~2,26! 5 57.52;p , .0001; GG5.61, was found. A planned comparison analysis confirmed that thiseffect resulted from the difference between the low memory loadconditions and the high memory load condition,F~1,13! 5 64.03;p , .0001, and not from the difference between the two lowmemory load conditions~i.e., between the memorize left andmemorize right conditions;F~1,13! 5 1.27;p . .200!. The inter-action between Memory and Visual Field was highly significant,F~2,26! 5 19.74;p , .0001; GG5 .99. This reflected that teststimuli presented in the ipsilateral visual field relative to thepresentation side of the memorized stimulus yielded faster re-sponses that test stimuli presented in the contralateral visual field.Furthermore, the analyses confirmed that this interaction was stron-ger for target stimuli than for nontargets~Interaction Memory3Visual Field3 Tartype,F~2,26! 5 9.03;p , .005; GG5 .91!.

Error rates showed a similar pattern of results as the responsetimes. The most important findings concerning error rates werethat subjects responded somewhat conservatively as shown by thefact that they missed more target stimuli than they falsely identi-

fied nontargets~main effect of Tartype,F~1,13! 5 24.75; p ,.0001!. Furthermore, in high memory load conditions, more errorswere made then in the memory load 1 conditions,F~1,13! 5232.25;p , .0001.

Similar to the response times data, for error rates, an interactionbetween the factors Memory and Visual Field was found,F~2,26! 517.92;p , .0001; GG5 .75, as well as a three-way interactionbetween Memory, Visual Field, and Tartype,F~2,26! 5 17.85;p ,.0001; GG5 .91. These findings indicate that the memory traceswere weaker when stimuli were maintained contralaterally withrespect to the side the of the test stimulus.

Physiological DataERP waveforms.As illustrated in Figures 3–6, the ERP wave-forms show posterior P1 and N1 components that are followed bythe P2, N2, and P300 components. Over the anterior areas, N1, P2,and N2 components can be observed that merge into a positivegoing waveform preceding the P300.

P1 and N1 amplitudes.As can be seen in Figures 3–6, theamplitude of the P1 component is similar for all conditions. The P1amplitude was not different for stimuli presented at the same oropposite position as the memory item~Memory 3 Visual Field,F~1,11! 5 0.2, p . .8!. However, the three-way interaction be-

Figure 2. Averages and standard deviations of the response times. Upper left: low memory load, target stimuli. Upper right: lowmemory load, nontarget stimuli. Lower left: high memory load, target stimuli. Lower right: high memory load, nontarget stimuli. LVF:left visual field; RVF: right visual field.


Figure 3. Grand average ERP waveforms for the target0nontarget differences in the low memory load conditions for test stimulipresented to the left visual field. The main components in this figure comprise right hemisphere P1 and N1 components over posteriorelectrodes, a left hemisphere posterior N2, and a paritietal P300. Anterior leads contain N1, P2, and N2 components, which merge intoa positive wave preceding the P300.~a! Stimuli memorized in the left visual field.~b! Stimuli memorized in the right visual field.


Figure 4. Grand average ERP waveforms for the target0nontarget differences in the low memory load conditions for test stimulipresented to the right visual field. The main components in this figure comprise left hemisphere P1 and N1 components over posteriorelectrodes, a left hemisphere posterior N2, and a paritietal P300. Anterior leads contain N1, P2, and N2 components, which merge intoa positive wave preceding the P300.~a! Stimuli memorized in the left visual field.~b! Stimuli memorized in the right visual field.


tween Memory3 Visual Field 3 Hemi-Lat approached signifi-cance,F~2,22! 5 2.86,p 5 .087, GG5 .89.

The N1 was larger at the electrodes contralateral to the teststimuli ~Hemi-Lat,F~1,11! 5 31.7,p , .001!. In contrast to whatwas expected, however, the N1 amplitudes were larger whenthe test stimuli were presented to the visual field opposite to thememorized stimuli, as compared to the N1 amplitudes in theconditions in which the memorized stimuli and the test stimuliwere presented to the same visual fields. This was clearly the caseat the electrodes contralateral to the visual field of the test stimu-lus. For the N1 at the ipsilateral electrodes, these effects weremuch smaller, and in the opposite direction. This pattern of resultswas reflected in a significant Memory3 Visual Field3 Hemi-Latinteraction,F~2,22! 5 5.2, p , .05, GG5 .87. The Memory3Visual Field 3 Hemi-Lat interaction was also significant whentested over the two low memory load conditions only,F~1,11! 57.9, p , .05.

Target-nontarget differences.Starting at about 250 ms, theERPs elicited by target figures showed a negativity as compared tonontarget figures~see Figures 3–6!. This negativity showed astrongly localized topography over the inferior lateral occipitotem-poral region of the scalp~see Figure 7!. Figure 8 shows thedifference potentials. The onset of the target versus nontargetdifference waves was at about the same latency, independent ofmemory and independent of whether the test figures were pre-

sented ipsilaterally or contralaterally to the memorized figures.This was evidenced by the fact that the difference wave wasstatistically significant in the latency range 260–320 ms~and in the400–440 ms range!, without effects of Memory Load or IpsiCon~see Table 1!.

However, when the test figures were presented in the oppositevisual field as the memorized stimuli, the negativity persistedmuch longer than when the memorized and test figures werepresented in the same visual field; in the latter case, target ERPsshowed a relatively early increase in positivity as compared tonontargets. This was reflected by an effect of IpsiCon in the320–480-ms latency range.

Interestingly, the negativity was most strongly lateralized to theleft hemisphere; Hemisphere became significant in the ranges260–320 ms and 340–380 ms~and also the IpsiCon3 Hemisphereinteraction: 320–480 ms!. When figures were memorized in theright visual field, targets elicited a negativity only over the lefthemisphere~independent of the visual field of target presentation!.When figures were memorized in the left visual field, targets~again, independent of the visual field in which they were pre-sented! also elicited a right hemisphere negativity, which wasgenerally smaller, though, than the negativity over the left hemi-sphere. This was reflected by significant Visual Field3 IpsiCon3Hemisphere interactions in the 260–320-ms range.

To determine more precisely the onset latencies of the target0nontarget difference, tests involving factors Visual Field and Ipsi-

Figure 5. Grand average ERP waveforms for the target0nontarget differences in the high memory load conditions for test stimulipresented to the right visual field. The main components in this figure comprise right hemisphere P1 and N1 components over posteriorelectrodes, a left hemisphere posterior N2, and a paritietal P300. Anterior leads contain N1, P2, and N2 components, which merge intoa positive wave preceding the P300.


Con were performed for the left hemisphere data, separately forthe low memory load and high memory load conditions. Thesetests confirmed our conclusion above, that memory load and pre-sentation of the target test figure ipsilateral versus contralateral tothe memorized figure hardly affected the onset latencies of thedifference waves. For the conditions in which only one figure wasmemorized, the difference wave was significant in the ranges240–340 ms and 400–440 ms, and there was a later effect ofIpsiCon~300–460 ms!. In the conditions in which both figures hadto be memorized, the difference wave was significant in the range260–320 and there was also a later effect of IpsiCon~320–380 msand 400–500 ms!.

The P300.The first analysis tested for target0nontarget differ-ences, memory condition~left versus right versus both! and visualfield. There was a significant Memory effect for both the P300latency, F~2,22! 5 14.1; p , .005, GG5 .59, and amplitude,F~2,22! 5 8.5;p , .005, GG5 .92. A planned comparison showedthat this reflected the increased latency~by about 100 ms! anddecreased amplitude in the high memory load condition as com-pared to the two low memory load conditions, as there was nosignificant difference between the memorize left and right condi-tions. The P300 latency tended to be increased for nontargets ascompared to targets~by about 50 ms,F~1,11! 5 4.0;p5 .069!. Forthe P300 latency, there was no significant interaction betweenMemory and Visual Field,F~2,22! 5 0.74, p . .4, nor a Mem-ory 3 Visual Field3 Tartype interaction,F~2,22! 5 2.3,p . .14.

The second analysis, restricted to the target P300s, showed thatthe P300 latency was increased~by about 100 ms! when twofigures were memorized as compared to the conditions where onlyone figure was memorized~Memory Load,F~1,11! 5 5.6, p ,.05!. The P300 latency also tended to be increased~by about50 ms! when the test figure was presented contralaterally to thememorized figure, as compared to the ipsilateral presentation~Ip-siCon, F~1,11! 5 3.9, p 5 .074!. Similarly, the P300 amplitudewas smaller in the high memory load condition,F~1,11! 5 6.9;p , .05, and with contralateral presentation, relative to the mem-orized figure~IpsiCon,F~1,11! 5 3.9;p , .05!. P300 latencies aresummarized in Table 2 and P300 amplitudes can be found inTable 3.

Discussion

The present study tried to find evidence for the involvement ofvisual brain areas in the storage and retention processes of workingmemory processing, and tried to examine the hemispheric lateral-ization of these processes. The next section discusses the mainresults found during the memorization and recognition phase ofworking memory processes.

Behavioral DataA striking difference was found in the pattern of response times fortarget stimuli on the one hand and nontarget stimuli on the other

Figure 6. Grand average ERP waveforms for the target0nontarget differences in the high memory load conditions for test stimulipresented to the right visual field. The main components in this figure comprise left hemisphere P1 and N1 components over posteriorelectrodes, a left hemisphere posterior N2, and a paritietal P300. Anterior leads contain N1, P2, and N2 components, which merge intoa positive wave preceding the P300.


hand, as was reflected in a significant Memory3 Visual Field3Tartype interaction. This result indicates that target stimuli pre-sented in the same visual field as the memory stimulus yieldedfaster responses than those presented contralaterally. However, thisinteraction did not exist for nontarget stimuli. It is therefore plau-sible that the location where the memorized stimuli were presented

is also being retained in working memory for visual objects.Although it is currently unclear why location is being processedeven under task conditions that do not require processing location,a number of studies have reported similar effects. For example,Dill and Fahle ~1998! have demonstrated a position invarianceeffect for visual object recognition. It was found that an increasingmismatch in location between two stimuli with an identical iden-tity yields increasingly longer response times, whereas the re-sponse times for stimuli that were not identical were all about aslong as the response times to identical stimuli at the most differ-entiating locations. Currently, there exists no satisfactory explana-tion for this effect. It has been suggested~e.g., Foster & Kahn,1985! that two patterns have to be aligned before a comparison canbe made. It is, however, unlikely that this is the case, because theeffect is only apparent for target stimuli, and not for nontargets. Aswill be discussed in more detail later, the present ERP results alsoshowed an early difference between target and nontarget ERPs thatdid not differ for targets presented ipsilaterally, relative to thememorized figure, and the targets presented contralaterally. This

Figure 7. Scalp topography of the target0nontarget difference waves at300 ms after stimulus onset, pooled over the low and high memory loadconditions. Contour spacing is 0.3mV. Upper left: the test stimulus pre-sented in the left visual field~LVF ! matched the figure memorized in theLVF. Upper right: the test stimulus presented in the LVF matched the figurememorized in the right visual field~RVF!. Lower left: test stimulus pre-sented in the RVF, memorized in the LVF. Lower right: test stimuluspresented in the RVF, memorized in the RVF.

Figure 8. Difference waves for the target0nontarget differences, obtained at the P7 and P8 electrodes by subtracting ERP responsesto nontarget stimuli from those of target stimuli. The upper half shows the effects for the low memory load condition and the lowerhalf of the figure the effects in the high memory load condition.

Table 1. Latency Ranges in Which Interval Analyses ShowedSignificant Effects for the Target–Nontarget DifferenceWaves at P70P8

Effect Time

Constant 260–320 400–440Memory ~A!Visual Field ~B!IpsiCon ~C! 320–480Hemi ~D! 260–320 340–380A 3 C 360–400A 3 D 320–360C 3 D 320–480B 3 C 3 D 260–320


suggests that targets can be identified at a relatively early stage,independent of location.

A possible explanation might be that whenever both locationand identity of the memorized stimulus and the target stimulusagree, target identification processing is terminated relatively early.However, in the conditions when either location or shape of thememory and test stimuli do not match, the brain automaticallyinitiates a verification process that has a negative effect on re-sponse times. If such a hypothetical verification processes forspatial and object properties were to be performed in parallel bythe dorsal and ventral pathways, respectively, it becomes plausiblethat response times for mismatch trials are prolonged by an ap-proximately constant factor, regardless of the type of mismatch.

An alternative explanation for this effect could be that subjectsperceive the scene as a whole, including computer screen and cuelines, assuming that a changing location changes the appearance ofthe scene, which causes the extra costs in response times. We donot believe that this is very likely, however. During memorization,we always presented two stimuli, along with a cue indicating therelevance of each stimulus. During the test interval, however, onlyone stimulus and no cue lines were presented, leading to differ-ences between the display during the retention interval and the testinterval. Therefore, if the change of the scene as such would yieldextra response time costs, it would be expected that these costswould be present on all trials, which is not the case.

Slow Waves in the Retention IntervalTo relate the present data to the results obtained during the reten-tion interval, we briefly review the main findings of the datareported by Klaver et al.~1999!. In this study, a negative goingslow wave was found over the posterior hemisphere, contralateralto the presentation side of the stimulus, which could be related toboth encoding of the stimulus and the subsequent retention phase.As suggested by Klaver et al., the observed slow wave reflects a

process that enhances the visual information that has to memo-rized. When the figure in the left visual field had to be memorized,this led to additional processing in the right hemisphere. Similarly,when the figure in the right visual field had to be memorized, thisled to an increased processing in the left hemisphere. Moreover,when both figures were relevant, both hemispheres were involvedin processing the information they received from the contralateralvisual field.

This result is in support of the hypothesis that working memoryprocesses are performed bilaterally. In accordance with the inter-pretation of Klaver et al.~1999!, Gratton, Corballis, and Jain~1997! took similar results as an indication of the formation of amemory representation in the hemisphere in which the informationwas initially presented. It should be noted, though, that the studyof Gratton et al.~1997! was different from the study of Klaveret al. in several respects. Most notably, Gratton~1998! studied theresponse to test stimuli that were memorized beforehand, whereasthe Klaver et al. data were obtained directly while stimuli wereencoded in working memory.

A more direct observation of the contralateral organization ofworking memory can be found in Gratton~1998! and Gratton et al.~1998!, who used the event related optical signal~EROS! methodto show that the occipital brain areas in the contralateral hemi-sphere are involved in memorizing visual stimuli. Results of thesestudies indicate that a centrally presented test stimulus caused adecrease in the EROS response over the hemisphere to which thesame stimulus was presented~the contralateral hemisphere!. Whena new, previously not memorized stimulus was presented, no suchdifferences between contralateral and ipsilateral hemisphere werefound. For the ipsilateral hemisphere, responses to old~memo-rized! and new stimuli were similar. These data can be taken asconverging evidence that the contralateral hemispheres play animportant role in memorizing visual stimuli.

Although these data suggest that memorization can be per-formed independently by the left and right hemispheres, the datapresented by Klaver et al.~1999! also showed a positive goingslow wave for the high memory load condition. This finding couldbe interpreted as evidence for a capacity limitation in the visualworking memory system, suggesting that, at least to some degree,the left and right visual areas share a common resource. A similarconclusion has been reached by Luck, Hillyard, Mangun, andGazzaniga~1994!, who have shown that scanning times increasedlinearly with the number of distractor items in a serial search task,regardless of whether these displays were presented unilaterally orbilaterally. It was assumed that if both hemispheres were indepen-dently capable of scanning one visual half-field, search timeswould be smaller for bilaterally presented displays than for thosepresented unilaterally, given a constant number of distractor items.One interesting observation in the Luck et al. study is that, incontrast to control subjects, commissurotomy~“split brain”! pa-tients were significantly faster in scanning bilaterally presenteddisplays. It can therefore be assumed that in normal control sub-jects, the left and right visual areas can, in principle, work inde-pendently, but that a common central executive system coordinatesthe correct operation of the visual areas.

P1 and N1 Components After Test Stimulus PresentationIn the test interval, subjects were presented with a single, lateral-ized test figure. The P1 and N1 components elicited by the testfigure would be indicative of the spatial distribution of attention asa function of the original position and the number of memorizedfigure~s!. Effects were visible only for the N1; most clearly so for

Table 2. P300 Latencies in the Different Memory Conditions forthe Right and Left Visual Field Test Stimulus Presentationsand for Targets and Nontargets

Targets Nontargets

Test LVF Test RVF Test LVF Test RVF

Memorize left 457 502 547 501Memorize right 499 445 560 557Memorize both 583 562 600 601

Table 3. P300 Amplitudes in the Different Memory Conditionsfor the Right and Left Visual Field Test Stimulus Presentationsand for Targets and Nontargets

Targets Nontargets

Test LVF Test RVF Test LVF Test RVF

Memorize left 12.3 9.4 10.9 9.1Memorize right 9.2 11.6 7.7 8.6Memorize both 7.7 8.6 6.6 7.7


the contralateral N1. The contralateral N1, which usually showsmuch larger effects of attention than the ipsilateral N1~for areview see Wijers et al., 1996!, was smaller when the test stimuluswas presented to the visual field from which a memory figure wasretained. We might take this to signify that during the retention ofa lateralized memory figure, spatial attention to the position orig-inally containing the memory figure is actually diminished. TheseERP effects of spatial attention are thought to reflect attentionalmodulation of early visual processing~e.g., Hillyard & Mangun,1986!.

To conclude, during the retention of the figure, the early pro-cessing of information from the same position is suppressed~i.e.,at the presentation of the test figure!. Enhanced perceptual pro-cessing in the retention interval might serve to lead to moreefficient storage in the visual memory buffer. Inhibition of percep-tual processing during the retention interval, on the other hand,might serve to protect the stored memory representation fromirrelevant environmental inputs. Although the test stimulus as suchis not an irrelevant stimulus, it should be noted that the location atwhich the test stimulus is presented is not known beforehand. Forthis reason, it is possible that a suppression of visual input ismaintained until the test stimulus is presented.

The above-mentioned conclusion that visual input to the mem-orized location is suppressed seems to contradict the observationthat responses were faster when test stimuli were presented to thesame hemisphere. It is possible, however, that although initially~inthe time range of the N1 component! visual input is suppressed, theonset of the target identification process itself~presumably duringthe N2 latency range; see below! was the same for both theconditions where the test stimulus was presented to the samehemisphere as the memorized stimulus and for conditions wherethe memorized stimuli were presented to different hemispheres.Hence, it can be concluded that although the reduced N1 amplitudeindicates that visual input is initially suppressed, this effect is notstrong enough to delay processes that start later.

Target IdentificationAlthough it was expected that the difference between target andnontarget stimuli would be reflected in a difference in the N2latency range, it was also expected that this difference would befound over the contralateral hemisphere, with respect to the pre-sentation side of the test stimulus~Eimer, 1996; Luck & Hillyard,1994; Wijers et al., 1997!. Contrary to what was expected, how-ever, a dominantly left hemispheric topography was found for theposterior N2, suggesting that target identification is mainly a lefthemispheric process. If target identification is indeed solely per-formed by the left hemisphere, one would also expect faster re-sponses for stimuli presented to the right visual field, which isclearly not the case in the present study. Even more so, a similardecrease in response times could be observed when memorizedstimuli and target test stimuli were presented to the same left orright hemisphere.

Although the target0nontarget effects are the most pronouncedin the left hemispheric posterior N2, a closer inspection of the data~see Figures 3 and 5! shows that, although the N2 component isstill most clearly present over the left hemisphere, a similar butsmaller effect can be observed over the right hemisphere. Theobservation that a smaller right hemispheric posterior N2 is alsopresent when stimuli were memorized in the left visual field can beinterpreted as evidence for some degree of right hemispheric in-volvement in target identification. The larger left hemispheric

effect, however, suggests that the left hemisphere is more special-ized in target identification than the right hemisphere is.

The current data also provide a possible explanation for thedifferences observed by Smith and Jonides~1997!. These authorshave noted that the degree of hemispheric lateralization dependson variations in task demands. Most notably, they suggested thatstudies with discrete trials, that is, tasks where the memorizationphase precedes the subsequent testing, such as the present para-digm, generally showed more left hemispheric lateralization thanthose using continous presentation, such as the n-back task~Smith& Jonides!. It is likely that continuous working memory tasksplace a relatively high demand on storage and rehearsal processes.The results from Klaver et al.~1999! show that these processeshave a contralateral topography. Tasks using more discrete trials,on the other hand, are more likely to place a relatively highdemand on retrieval and matching processes. Most notably, thepresent data show a left hemispheric lateralization that is related tostimulus identification. In summary, it is plausible that continuousworking memory tasks involve relatively more storage and re-hearsal, which evoke mainly a bilateral pattern of activation duringPET studies, as reported by Smith and Jonides. Discrete workingmemory tasks, on the other hand, yield a more lateralized patternof activation in PET studies, due to the relatively stronger contri-bution of processes involved in target identification.

It was also found that the relative onset of the N2 effect was thesame for all conditions, indicating that the target identificationprocess starts relatively early. Furthermore, the onset latency of theN2 target0nontarget difference appeared to be equal for test stimulipresented ipsilaterally and contralaterally relative to location of thememorized stimulus, in the low memory load as well as the highmemory load conditions.

From the given results, it appears that a discrepancy existsbetween the relative onset of the target0nontarget identificationprocess, as reflected by the N2 effect, and the effects found forresponse times. As mentioned, a possible explanation for thisdiscrepancy is the occurrence of additional verification processesthat were executed whenever a mismatch in location or identitybetween memorized stimulus and test stimulus occurs.

The P300A number of studies~e.g., Magliero et al., 1984; McCarthy &Donchin, 1981! on the P300 latency have provided evidence forthe hypothesis that the P3 is related to stimulus evaluation. Ac-cording to this hypothesis, the latency of the P3 component isrelated to the duration of a perceptual analysis that is independentof motor processes. With regard to the present study, it is interest-ing to note that no significant interaction between Memory andVisual Field nor an interaction between Memory, Visual Field, andTartype factors was found. In view of the stimulus evaluationhypothesis, absence of these interactions suggests that the stimulusevaluation process terminates at approximately the same latencyfor both test stimuli presented ipsilaterally and contralaterally,relative to the memorized stimulus, and also for targets and non-targets. However, when the analysis of the P300 latencies wasconfined to target stimuli, as in the second P300 analysis, a ten-dency for increased P300 latencies could be observed when thetargets were presented contralaterally, relative to the memorizedstimuli, as compared to ipsilateral targets. Because the overall test,including both target and nontarget figures, failed to reach signif-icance for the Visual Field3 Memory Load interactions, theinterpretation of the Visual Field3 IpsiCon interactions in thesecond analysis should be interpreted cautiously. Despite these


considerations, however, it is possible that a tendency for increasedP300 latencies for targets presented contralaterally to the memo-rized stimuli can be observed in the present data. Moreover, in-creased P300 latencies were observed for nontargets, compared totargets. Taken together, these effects suggest that although targetidentification is a process that can be performed at a relativelyearly stage, both the processing of nontarget stimuli and stimulipresented under high memory load conditions require an additionalstimulus-evaluating process. Although it is, therefore, not reallyclear from the present data, it is possible that the increased re-sponse times for target test stimuli presented contralaterally to thememorized stimuli are also caused by additional stimulus-evaluationprocesses.

It was also found that the P300 showed an increase in latencyand a decrease in amplitude for the memorize both conditions,compared to the memorize left and right conditions. Research hasshown that the P300 decreases in amplitude and increases inlatency as a function of display load in memory search tasks~e.g., Brookhuis et al., 1981; Brookhuis, Mulder, Mulder, & Gloerig,1983; Hofman, Simons, & Houck, 1983; Mulder, Gloerig,Brookhuis, van Dellen, & Mulder, 1984; van Dellen, Brookhuis,Mulder, Okita, & Mulder, 1985!. In addition, the amplitude of theP300 has been related to the confidence subjects have in theirdecision. The observed increase in P300 latency and decrease ofthe P300 amplitude could, therefore, indicate that subjects are lessconfident in their responses to stimuli in the high memory loadcondition. These results could, therefore, suggest that the repre-sentation of the memorized stimuli is weaker in the high memoryload condition.

General ConclusionsThe present data show that response times are faster for targetstimuli presented at the same location as the location at whichthe memorized stimulus was presented. Although a tendency for thesame pattern of results could be observed for the latencies of theP300 component for target stimuli, this effect should be interpretedcarefully, because the overall effect was not significant. Convergingevidence for the assumption that targets presented contralaterallyto the memorized stimulus yield an additional confirmation-seeking process after target identification can possibly be found inthe longer duration of the N2. As can be seen in Figure 8, thenegativity persisted longer when test stimuli were presented con-tralaterally, relative to the memorized stimulus, as compared to theconditions where test stimuli were presented ipsilaterally. A pos-sible explanation for this effect is that the identification processtakes longer to complete for targets presented contralaterally, rel-ative to the memorized stimulus. The latter part of the N2 couldtherefore reflect a location recheck process. Alternatively, the in-creased negativity for contralateral targets could also indicate that

although the target identification process starts at the same latencyacross conditions, identification is slower when a mismatch inlocation occurs.

These effects could be explained by assuming that stimuli canbe identified relatively easily whenever both location and objectidentity are identical for the memorized stimulus and the teststimulus. It is plausible that additional confirmation seeking pro-cesses are required whenever a mismatch occurs in either thelocation or shape of the test stimulus.

Based on this explanation, it would seem logical that contra-lateral nontargets would also yield increased response times com-pared to nontargets presented ipsilaterally to the memorizedstimulus. According to this reasoning, contralateral nontargetswould require both verification of the location and the shape ofthe stimulus, whereas nontargets presented ipsilaterally to thememorized stimulus would only require confirmation of the shapeof the stimulus.

It has been shown, however~Ungerleider & Miskin, 1982!, thatthe dorsal and ventral pathways process spatial and nonspatialfeatures of a stimulus largely independently. Assuming that thesetwo pathways can operate in parallel, a possible explanation for theobserved differences in response times for ipsilaterally and con-tralaterally presented target and nontarget stimuli might be thefollowing. Although contralaterally presented nontargets requireadditional shape confirmation as well as an extra location verifi-cation process, the two processes operate largely in parallel, and aresponse can be generated as soon as the slowest of the twoprocesses has terminated. For nontargets, additional processing istherefore always required. For targets, on the other hand, addi-tional processing is only required for contralaterally presentedtargets. In accordance with this reasoning, responses to ipsilater-ally presented targets can be faster than responses to contralaterallypresented targets, but response times to nontargets will be approx-imately the same for ipsilaterally and contralaterally presentednontargets.

An interesting difference appears to exist in lateralization be-tween retention and matching processes. Although it was foundthat retention takes place mainly in a visual buffer that is localizedin the contralateral posterior hemisphere~Gratton, 1998; Grattonet al., 1997, 1998; Klaver et al., 1997!, the matching processyielded its largest effect over the left posterior hemisphere. The lasteffect was reflected in the difference in the N2 between targets andnontargets that was the most pronounced over the left posteriorareas. Furthermore, the N2 difference between targets and nontar-gets did not differ significantly for the high and low memorymemory load conditions. This implies that object identification cantake place independently of the number of items stored in memory,suggesting that object matching is a process that can be performedlargely in parallel, mainly in the left posterior brain areas.

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~Received August 2, 1999;Accepted August 1, 2000!


Working memory processes show different degrees of lateralization: Evidence from event-related...

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