posterior parietal cortex activity predicts individual ...posterior parietal/superior occipital...

Copyright 2005 Psychonomic Society Inc 144

Cognitive Affective amp Behavioral Neuroscience2005 5 (2) 144-155

Our ability to grab onto and hold in mind the informa-tion presented in a visual scene is extremely limited Forinstance subjects have great difficulty in detecting a grosschange between two similar scenes if these scenes areseparated in time or by another visual stimulus (Rensink2002 Rensink OrsquoRegan amp Clark 1997 Simons 1996)Although the earliest stages of visual information pro-cessing are endowed with virtually unlimited processingcapacities (Pashler 1988 Phillips 1974 Sperling 1960)severe limits occur when the visual information is storedinto visual working memory which can at best accom-modate four visual items (Cowan 2001 Luck amp Vogel1997 Pashler 1988 Vogel Woodman amp Luck 2001)This bottleneck of information processing has signifi-cant real-life consequences since it is considered to limitwhat information can be explicitly perceived and actedupon (Becker Pashler amp Anstis 2000 Chun amp Potter1995 Jolicœur DellrsquoAcqua amp Crebolder 2001 Rensink2002 Shapiro Arnell amp Raymond 1997)

Due to the ubiquitous role of working memory in vi-sual cognition it is not too surprising that it has been as-sociated with a large network of brain regions in both hu-mans (J D Cohen et al 1997 Courtney UngerleiderKeil amp Haxby 1997 Jonides et al 1993 Linden et al2003 Munk et al 2002 Pessoa Gutierrez Bandettiniamp Ungerleider 2002 Sala Raumlmauml amp Courtney 2003)and nonhuman primates (Chafee amp Goldman-Rakic 1998

Constantinidis amp Steinmetz 1996 Funahashi Bruce ampGoldman-Rakic 1989 Fuster 1990 Goldman-Rakic1996 Miller amp Desimone 1994 Quintana amp Fuster1999) Encompassing all the cortical lobes this networkcan be loosely divided into regions that contribute pri-marily to Baddeleyrsquos (1986) central executive system andthose regions involved in maintaining and storing the vi-sual information that is manipulated by the executivesystem the so-called visuospatial sketch pad (Baddeleyamp Logie 1999) or visual short-term memory (VSTM)

Executive processes such as attentional selectioncontrol and manipulation of information have been as-sociated primarily with the frontalprefrontal cortex (BorDuncan Wiseman amp Owen 2003 Curtis amp DrsquoEsposito2003 Sakai Rowe amp Passingham 2002 Smith amp Jonides1999) By contrast the simple storage of sensory infor-mation in VSTM or in auditory short-term memory isthought to involve more posterior regions (Paulesu Frithamp Frackowiak 1993 Postle Berger amp DrsquoEsposito 1999Rowe amp Passingham 2001 Smith amp Jonides 1998) Inparticular substantial evidence indicates that the poste-rior parietal and inferior temporal regions are involvedin the retention of visual information (Munk et al 2002Pessoa et al 2002 Todd amp Marois 2004) However thisanteriorndashposterior dissociation is likely not absolutesince the frontalprefrontal cortex has also been involvedin the simple maintenance of information (eg J DCohen et al 1997 Courtney Petit Maisog Ungerleideramp Haxby 1998 Courtney et al 1997 Curtis amp DrsquoEs-posito 2003 Linden et al 2003)

Thus although there is considerable evidence thateven the simple maintenance of information in VSTMrecruits a vast network of brain regions (Linden et al

This work was supported by grants from the National Science Founda-tion and the National Institute of Mental Health to RM Correspondenceshould be addressed to R Marois Vanderbilt Vision Research CenterDepartment of Psychology Vanderbilt University 530 Wilson Hall 11121st Ave S Nashville TN 37203 (e-mail renemaroisvanderbiltedu)

Posterior parietal cortex activity predictsindividual differences in visual short-term memory capacity

J JAY TODD and RENEacute MAROISVanderbilt University Nashville Tennessee

Humans show a severe capacity limit in the number of objects they can store in visual short-termmemory (VSTM) We recently demonstrated with functional magnetic resonance imaging that VSTMstorage capacity estimated in averaged group data correlated strongly with posterior parietalsuperioroccipital cortex activity (Todd amp Marois 2004) However individuals varied widely in their VSTM ca-pacity Here we examined the neural basis of these individual differences A voxelwise individual-differences analysis revealed a significant correlation between posterior parietal cortex (PPC) activityand individualsrsquo VSTM storage capacity In addition a region-of-interest analysis indicated that other brainregions particularly visual occipital cortex may contribute to individual differences in VSTM capac-ity Thus although not ruling out contributions from other brain regions the individual-differences ap-proach supports a key role for the PPC in VSTM by demonstrating that its activity level predicts indi-vidual differences in VSTM storage capacity

INDIVIDUAL DIFFERENCES IN VSTM CAPACITY 145

2003 Munk et al 2002 Pessoa et al 2002 Sala et al2003) the extent to which different nodes of this net-work process distinct components of VSTM is still notresolved (Pessoa et al 2002) Furthermore the neuralbasis of arguably the most distinctive characteristic ofVSTM its severely limited storage capacity is poorlyunderstood Although a parametric load manipulationhas been used in several studies to isolate brain regionsassociated with visual working memory (eg Braveret al 1997 J D Cohen et al 1997 Druzgal amp DrsquoEs-posito 2003 Jha amp McCarthy 2000 Leung Gore ampGoldman-Rakic 2002 Linden et al 2003) few have ex-plored the neural substrates underlying the capacity con-straints of working memory (eg Callicott et al 1999Duncan et al 1999 Linden et al 2003 Olesen West-erberg amp Klingberg 2004 Vogel amp Machizawa 2004)

In a recent study we sought to identify the neural sub-strates associated with the capacity limit in storing a vi-sual scene in VSTM (both object identities and loca-tions Todd amp Marois 2004) In that study even thoughsubjects were shown from one to eight color objects (Fig-ure 1) they were successful in storing only up to three orfour of them in VSTM More important this VSTM stor-age capacity did not appear to be equally distributedacross the neural network subserving visual workingmemory Rather activity in a particular brain region theposterior parietalsuperior occipital cortex (intraparietalsulcus and intraoccipital sulcus) was found to be tightly

correlated with the limited number of objects stored inVSTM (Todd amp Marois 2004) A much weaker VSTM-capacityndashrelated signal was observed in the ventral oc-cipital and frontal cortex These results suggest that akey function of the posterior parietal cortex (PPC) in theneural network of visual working memory is the storageof visuospatial information

The results of this study (Todd amp Marois 2004) werebased on a group average of VSTM load That is wesought to isolate brain regions that correlated with theaverage number of objects stored in VSTM at each loadHowever an examination of individual storage capacityfunctions reveals a wide range of individual VSTM capac-ities (Figure 2) Using a formula modified from Pashler(1988) by Cowan (2001) to estimate VSTM capacity themaximum number of objects maintained in VSTM wasfound to vary considerably between individuals from174 to 637 This variation in capacity could arise froma wide spectrum of factors ranging from differences inbiology (eg genetics age and possibly gender) to taskexperience (eg Olesen et al 2004 Raichle et al 1994)and to differences in task strategies (Cornoldi amp Vecchi2003 Rypma Berger amp DrsquoEsposito 2002) But irre-spective of what may be the underlying cause(s) for theseindividual differences in VSTM capacity of most sig-nificance here is that a group average analysis does notcapture the neural basis of individual differences sinceit treats intersubject variability as error If the activity of

Figure 1 Trial design Each trial began with the presentation of two digits whichwere rehearsed subvocally throughout the trial Next a varying memory load of coloreddisks (one to eight) was presented Following a brief retention interval (1200 msec inExperiment 1 9200 msec in Experiment 2) the subjects determined whether a probedisk matched in color the disk presented at the same position in the sample displayFinally a judgment was made regarding the two rehearsed digits

Fixation(1000 msec)

Auditory probe(1500 msec)

Probe display(1750 msec)

Retention interval(1200 9200 msec)

Sample display(150 msec)

Fixation(1400 msec)

Auditory stimuli presentation(1000 msec)

Time

3 1

+

146 TODD AND MAROIS

a brain region isolated with a group average analysisdoes not correlate with individual differences in perfor-mance this would suggest that this brain region maycontribute only a generic component to the cognitiveprocess under investigation and that other brain regionsaccount for the diversity of performance across subjectsOn the other hand a stronger case can be made about abrain region being involved in a specific cognitive pro-cess if that brain region not only is activated in a signif-icant proportion of subjects but also can account for thedifferences in performance between subjects For exam-ple in addition to demonstrating a role for the dorsal pre-frontal cortex (DPFC) in the retrieval of informationfrom auditory-verbal working memory (AVWM) in agroup average analysis Rypma and DrsquoEsposito (1999)showed that individual differences in speed of informa-tion retrieval from AVWM was correlated with the levelof DPFC activity Thus using both group and individual-differences approaches one can isolate a brain regionthat is activated across individuals in a task and subse-quently identify its contribution to individual differencesin performance

The goal of the present study was to determine howan individual-differences approach can inform us aboutthe neural basis of VSTM storage capacity In particularwould an individual-differences approach provide con-verging evidence with the group average analysis for theimportance of the PPC in VSTM storage capacity Orwould such individual-differences analysis instead pointto other brain regions to account for intersubject vari-ability There is electrophysiological evidence in favorof the former possibility Vogel and Machizawa (2004)showed that event-related potentials (ERPs) over poste-rior parietal and lateral occipital sites can predict indi-vidual subjectsrsquo VSTM capacity Importantly the sourceof this ERP signal is largely compatible with the poste-

rior parietalsuperior occipital locus of VSTM storagecapacity isolated in the group average fMRI study (Toddamp Marois 2004)

To determine which neural substrates might captureindividual differences in VSTM capacity we adopted thelogic of Vogel and Machizawa (2004) That is if a brainregion plays an important role in determining the amountof information held in VSTM it is reasonable to expecta strong correlation between individual VSTM capacityestimates and the respective magnitude of activation inthat brain region In other words individuals with largeVSTM capacities would be expected to activate this brainregion more than would individuals with smaller capac-ities Thus in the present study we correlated each sub-jectrsquos brain activity at the set size at which they reachedVSTM capacity with the number of objects they storedin VSTM at that same set size We used this methodolog-ical approach in a voxelwise analysis in order to isolate anybrain regions whose activity correlated with individualdifferences in VSTM capacity We also applied this tech-nique to a more sensitive region-of-interest (ROI) analysisin order to determine whether regions previously impli-cated in VSTM storage capacity on the basis of a groupaverage analysis (Todd amp Marois 2004) track individualdifferences in VSTM capacity

METHOD

In the present study the same data sets as those used in two extantfunctional magnetic resonance imaging (fMRI) experiments of VSTMload (Experiment 1 Todd amp Marois 2004 Experiment 2 ToddFougnie amp Marois in press) were reanalyzed using an individual-differences approach

SubjectsThe subjects were paid volunteers from the Vanderbilt commu-

nity Seventeen young adults (9 females all right-handed) partici-pated in Experiment 1 and 14 (8 females 12 right-handed) volun-teered for Experiment 2 All had normal or corrected-to-normalvisual acuity and normal hearing and color vision The experimen-tal protocol was approved by and consent was received in accor-dance with the Institutional Review Board at the Vanderbilt Uni-versity Medical Center

Task DesignExperiment 1 Fast event-related fMRI study A detailed de-

scription of the experimental method has been published elsewhere(Todd amp Marois 2004) The subjects performed a parametric loadmanipulation of a delayed recognition task (Figure 1) A static dis-play containing a varying number (one two three four six oreight) of colored disks (038ordm of visual angle) each of a differentcolor (red green dark green blue light blue black white brownor yellow) was presented for 150 msec The stimuli were presentedat nine possible locations within an invisible 3 3 matrix (138ordmsquare) After a 1200-msec retention period a single colored diskwas presented in a position previously occupied by a disk in thesample array The subjects indicated by buttonpress whether thecolor of the probe disk was identical to the color of the sample diskat that position (right index finger same right middle finger dif-ferent) Half the trials were matched To control for possible con-tamination of AVWM the subjects performed a concurrent artic-ulatory suppression task (Baddeley 1986) At trial onset twosingle-digit numbers were presented serially through headphones

Figure 2 Individual visual short-term memory K functionsThe K function for each individual (thin lines) is plotted by setsize The group mean K function (n 16) is represented by thethick line


for 250 msec each followed by a 250-msec blank interval and thenby a 250-msec auditory mask composed of superimposed forwardand reversed versions of the individual sound files Following themask there was a 1400-msec period of fixation before the onset of the visual sample array The subjects were instructed to rehearsethe two digits throughout the trial Following the visual probe re-sponse the subjects indicated by buttonpress whether two visuallypresented digits were the same as those rehearsed throughout thetrial

Experiment 2 Slow event-related fMRI study Fourteenyoung adults (8 females 12 right-handed) volunteered for this ex-periment The details of the experimental design have been pub-lished elsewhere (Todd et al in press Todd amp Marois 2004) Theexperimental design was similar to that for the fast event-relatedfMRI experiment described above with the following exceptionsThe retention interval was extended from 1200 to 9200 msec (trialduration 18 sec 7 trialsfMRI run) only two set sizes were em-ployed in order to compensate for the lower number of trials ac-quired with a slow event-related paradigm and there were no non-event trials

fMRI methods fMRI methods have been described elsewhere(Todd amp Marois 2004) Low- and three-dimensional (3-D) high-resolution T1-weighted images were acquired using conventionaltechniques with a 3-T GE MRI scanner (GE Medical Systems Mil-waukee WI) In each functional run 220 T2-weighted echoplanarimages were acquired in 19 axial slices (7 mm thick 375 375 mmin-plane 0-mm skip repetition time (TR) 2000 msec echo time 25 msec FOV 24 cm matrix 64 64) covering the wholebrain and prescribed parallel to the ACndashPC line Trial presentationwas synchronized to TR onset by scanner trigger pulses The stim-uli were presented on an Apple G4 Macintosh using PsychToolBoxfor Matlab The stimuli were back-projected onto a screen viewedby the supine subject in the MR scanner through a prism mirrorThe fMRI methods for Experiment 2 were the same as those forExperiment 1

Data AnalysisBehavioral analysis The estimated number of objects stored in

VSTM (K) was calculated using a formula developed by Pashler(1988) and modified by Cowan (2001) Here K (hit rate cor-rect rejection rate 1)N where N is the number of objects pre-sented in the sample array

fMRI analysis The fMRI data analysis was carried out withBrain Voyager 491 (Brain Innovation Maastricht The Nether-lands) Preprocessing included intrasession image realignment 3-Dmotion correction and correction for slice scan acquisition orderusing sinc interpolation and linear trend removal

Group statistical parametric map analysis VSTM load-modulated regions in Experiment 1 and for the right posterior middlefrontal gyrus (see the Results section) were identified in statisticalparametric maps (SPMs) of blood oxygen level dependent (BOLD)activation using multiple regression analysis with impulse regres-sors for each trial type (six set sizes and a no-event condition) con-volved with a canonical hemodynamic response function (BoyntonEngel Glover amp Heeger 1996) Regression coefficients wereweighted for each set size by their respective group average K valueThe resulting maps from all the subjects were standardized into Ta-lairach space (Talairach amp Tournoux 1988) and were overlaid tocreate composite activation maps The overall model fit was assessedwith an F statistic using a random effects model and voxels wereconsidered significant if p 05 corrected for multiple compar-isons using a cluster threshold of 6 voxels and spatial smoothingGaussian kernel of 80 mm (FWHM Ward 2000) ROIs were iso-lated from the SPMs and time courses for each memory load wereextracted from these ROIs Percentage of signal change of eachtime course was calculated using the nonevent time series as thebaseline condition (Kourtzi amp Kanwisher 2001)

Individual-differences analysis Individual-differences analysiswas carried out using both a voxel-based and an ROI-based ap-proach The voxelwise approach was used to identify regions thattrack individual differences in VSTM storage capacity To isolatesuch regions we first determined for each subject the maximumnumber of objects they could store (Kmax) and the percentage ofBOLD signal change (relative to no-event signal) obtained at theKmax set size Since at set size 1 all the subjects had virtually thesame K value (mean K 095) but very different BOLD signal lev-els we standardized brain activity across subjects by first subtract-ing the percentage of BOLD signal at set size 1 from the percent-age of BOLD signal at set size Kmax By using set size 1 activity asa baseline response for each individual this transformation in-creased our sensitivity for detecting brain regions whose activitycorrelated with individual differences in VSTM capacity (Vogel ampMachizawa 2004) For each individual regressors were defined forset size Kmax and set size 1 and were weighted by the individualrsquosmaximum K value We then probed for voxels whose activity co-varied with the magnitude of the difference between set size Kmaxand set size 1 across individuals

The ROI approach was used to determine whether brain regionspreviously implicated in VSTM storage capacity on the basis of agroup average analysis (Todd amp Marois 2004) contributed to indi-vidual differences in VSTM capacity For each ROI we correlatedthe individual differences in Kmax with the individual differences inpercentage of peak activation between set size Kmax and set size 1Specifically the volume corresponding to the peak of the hemody-namic response collapsed across all set sizes was first definedThen for each individual the activation difference between set sizeKmax and set size 1 of the peak volume was computed and these ac-tivation differences were subsequently correlated with each indi-vidualrsquos Kmax Significance for correlation analysis of the intrapari-etal sulcusintraoccipital sulcus (IPSIOS) ROI was set to p 05one-tail on the basis of the a priori expectation of a positive linearrelationship between VSTM capacity and brain activity For con-sistency the same statistical criteria were employed for all the ROIsFor Experiment 2 ROI analysis of individual differences in VSTMcapacity1 was performed by first computing for each individualthe difference in activation between set sizes 1 and 3 and regress-ing this activation difference with their corresponding K value ob-tained at set size 3 across individuals This analysis was performedseparately for the encoding maintenance and retrieval phases ofVSTM using the peak volumes acquired 55ndash75 95ndash115 and155ndash175 sec after stimulus presentation respectively Given the92-sec-long retention interval these peak time windows shouldprovide largely uncontaminated estimates of activity for each of thethree VSTM phases particularly for the maintenance phase (Pessoaet al 2002 Zarahn Aguirre amp DrsquoEsposito 1997)

Outliers were isolated and removed in ROIs using DFFITSi witha cutoff threshold equal to 1 (J Cohen P Cohen West amp Aiken2003) At most two outliers were removed from any given ROI

RESULTS

Voxel-Based AnalysesThe aim of the voxelwise analysis was to isolate brain

regions whose activity correlated with individual differ-ences in VSTM capacity This SPM revealed a single re-gion within the left IPSIOS [t(15) 442 p 05 cor-rected Figure 3A] The activated region largely overlappedthe IPSIOS region isolated in the group analysis (Todd ampMarois 2004) group-based ROI Talairach coordinatesx 14 to 30 y 81 to 58 z 17 to 49 individual-based ROI coordinates x 17 to 29 y 81 to 61z 21 to 45 The contralateral IPSIOS was also acti-

148 TODD AND MAROIS

vated when the threshold was reduced tenfold ROI analy-sis of this IPSIOS region confirmed that individualsrsquoKmax correlated with the activation difference between

set size Kmax and set size 1 [r(12) 56 p 05 Fig-ure 3B] This load-modulated response was not simply dueto high-K individuals demonstrating greater overall acti-vation than low-K individuals did (Vogel amp Machizawa2004) since each subjectrsquos BOLD signal was standardizedat set size 1 The response was also not due to scalingdifferences in activation across individuals with subjectswith greater memory capacity simply having greateroverall activation range since overall activation differ-ences across set sizes did not correlate with individualsrsquoKmax [r(14) 36 ns] Importantly the correlation be-tween individualsrsquo Kmax and activity difference betweenset sizes Kmax and 1 did not extend to supracapacity setsizes That is there was no correlation between individ-ualsrsquo Kmax and the activation difference between set size 8and Kmax for the individuals whose Kmax occurred at setsizes lower than 8 [r(7) 19 ns] Analysis of thesame ROI in Experiment 2 with extended retention in-terval revealed that the activity difference between setsizes 3 and 1 was correlated with individual VSTM ca-pacities at set size 3 during maintenance [r(12) 54 p 05] and retrieval [r(11) 63 p 05] and marginallyso during encoding [r(11) 50 p 08 Figure 3C]

Taken together these analyses indicate that a regionof the IPSIOS that largely overlaps with the PPC regionisolated with a group-based approach to VSTM capacity(Todd amp Marois 2004) tracks individual differences inVSTM capacity

ROI-Based AnalysesIn addition to the IPSIOS our group average study of

VSTM load had revealed weak correlation between VSTMcapacity and ventral occipital (VO) and anterior cingulate(AC) cortex activity (Todd amp Marois 2004) Here weexamined the latter two ROIs to determine whether theiractivity reflects individual differences in VSTM capacity

Ventral occipital ROI Individual-differences analysisapplied to Experiment 1 using the methods described forthe IPSIOS above revealed that VO activity differencebetween set size Kmax and set size 1 did not correlate withindividualsrsquo VSTM capacity [r(14) 32 ns Figure 4A]However individual-differences analysis for Experi-ment 2 indicated that VO activity difference between setsizes 3 and 1 correlated with individualsrsquo VSTM capac-ity at set size 3 during maintenance [r(12) 63 p 05 Figure 4B] but not during encoding [r(12) 02ns] or retrieval [r(12) 14 ns] Thus a correlationbetween individualsrsquo VSTM storage capacity and brainactivity in VO is observed in the VSTM task with thelong retention interval but not with the short retentioninterval (Experiment 1)

Anterior cingulate ROI In the AC activation differ-ences between set size Kmax and set size 1 did not corre-late significantly with individual capacity limit estimates[r(13) 35 ns Figure 5A] Correspondingly Exper-iment 2 revealed no significant correlation between ACactivity and individual VSTM capacities during all threephases of VSTM [encoding r(11) 17 ns maintenance

Figure 3 Intraparietalintraoccipital regions of interest(A) Statistical parametric map of individual differences in visualshort-term memory (VSTM) storage capacity revealed activityalong the left intraparietal sulcusintraoccipital sulcus (IPSIOSp 05 corrected) The peak voxel Talairach coordinates of thisregion are x y z 25 77 33 The contralateral IPSIOS isalso activated when the threshold is reduced tenfold (B) Corre-lation of individual Kmax (VSTM storage capacity estimates) withthe activation difference between set size Kmax and set size 1 forExperiment 1 (C) Correlation of individual Ksetsize3 with the ac-tivation difference between set sizes 3 and 1 for the encoding(red) maintenance (green) and retrieval (blue) phases of VSTMin Experiment 2

A

B

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L R

(t)621442

04

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ivat

ion

diffe

renc

e (

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renc

e (

)

0 1 2 3Ksetsize3


r(12) 42 ns retrieval r(12) 14 ns Figure 5B]Thus AC activity shows nonsignificant correlation trendswith individual differences in VSTM capacity

Right posterior middle frontal gyrus ROI Ourgroup average approach to VSTM capacity failed to re-veal any regions of the frontal or prefrontal cortex thatcorrelated with the number of objects stored in VSTM(Todd amp Marois 2004) However the role of these re-gions in visual working memory has been clearly estab-lished (Curtis amp DrsquoEsposito 2003 Druzgal amp DrsquoEspos-ito 2003 Leung et al 2002 Linden et al 2003 PostleStern Rosen amp Corkin 2000 Sala et al 2003) To de-termine whether an individual-differences analysis maybetter reveal a frontalprefrontal contribution to VSTM

storage capacity we examined a region in the right pos-terior middle frontal gyrus (rpMFG Figure 6A) that canbe observed in the group average SPM of VSTM storagecapacity (Todd amp Marois 2004) when the statisticalthreshold p was reduced 100-fold prior to correction formultiple comparisons A plot of the group average peakBOLD response at each VSTM set size (Figure 6B) re-vealed that the rpMFG response function was differentfrom the group behavioral K function (Figure 6B Toddamp Marois 2004) Instead of leveling off around set size 3or 4 rpMFG response reached asymptote at set size 2 asubcapacity VSTM set size In addition individual-differences analysis revealed that the rpMFG activity dif-ference between set size Kmax and set size 1 did not cor-

Figure 4 Bilateral ventral occipital region of interest (A) Correlation of individual Kmax with the acti-vation difference between set size Kmax and set size 1 in Experiment 1 (B) Correlation of individual Ksetsize3with the activation difference between set sizes 3 and 1 for the encoding (red) maintenance (green) andretrieval (blue) phases of visual short-term memory in Experiment 2

A B04

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0 1 2 3Ksetsize3

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renc

e (

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ivat

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e (

)

Figure 5 Anterior cingulate region of interest (A) Correlation of individual Kmax with the activation dif-ference between set size Kmax and set size 1 in Experiment 1 (B) Correlation of individual Ksetsize3 with theactivation difference between set sizes 3 and 1 for the encoding (red) maintenance (green) and retrieval(blue) phases of visual short-term memory in Experiment 2

A B 03

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150 TODD AND MAROIS

relate with individualsrsquo VSTM capacity [r(14) 25ns Figure 6C] Finally there was no correlation be-tween rpMFG activity and individualsrsquo VSTM capacityat set size 3 for the encoding [r(10) 49 ns] and re-trieval [r(11) 42 ns] phases of VSTM in Experi-ment 2 but there was a marginal correlation duringmaintenance [r(11) 53 p 06 Figure 6D] Thusboth the group average and the individual-differencesapproaches suggest that rpMFG activity does not tightlycorrelate with VSTM storage capacity

DISCUSSION

Using a voxelwise individual-differences approachwe showed that posterior parietalsuperior occipital cor-tex activity predicts individual differences in VSTM ca-pacity Importantly this area largely overlapped with the

PPC region that was isolated with a group-based ap-proach (Todd amp Marois 2004) This key result suggeststhat the IPSIOS does not simply contribute a genericcomponent to VSTM storage capacity since it may alsobe involved in setting individual differences in VSTMstorage capacity Thus just as an individual-differencesapproach has consolidated the importance and clarifiedthe role of the lateral prefrontal cortex in working mem-ory (Rypma et al 2002 Rypma amp DrsquoEsposito 19992000) the present individual-differences analysis pro-vides converging evidence with the group average ap-proach (Todd amp Marois 2004) that the PPC is a keyneural locus of our limited capacity for storing a mentalrepresentation of the visual world (Todd amp Marois 2004)

By virtue of its central role in goal-driven attention andspatial working memory (Corbetta Kincade amp Shulman2002 Corbetta amp Shulman 2002 LaBar Gitelman Par-

Figure 6 Right posterior middle frontal gyrus (rpMFG) region of interest (A) The statistical paramet-ric map of group-averaged K-weighted visual short-term memory (VSTM) load function in Experiment 1reveals activation in the rpMFG (threshold t 212) The peak voxel Talairach coordinates are x yz 26 5 45 (B) Behavioral K function (empty circles dashed line) and rpMFG peak response func-tion (solid circles and line) for the group average analysis in Experiment 1 Percentage of signal change ison the left ordinate K values are on the right ordinate Peak percentage of signal change corresponded tothe volume acquired 56 sec after stimulus presentation (C) Correlation of individual Kmax with the acti-vation difference between set size Kmax and set size 1 in Experiment 1 (D) Correlation of individual Ksetsize3with the activation difference between set sizes 3 and 1 for the encoding (red) maintenance (green) andretrieval (blue) phases of VSTM in Experiment 2

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(t)506212

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e (

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ber of objects encoded (K)

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rish amp Mesulam 1999 Wojciulik amp Kanwisher 1999) andin visual feature integration (Friedman-Hill Robertsonamp Treisman 1995 Shafritz Gore amp Marois 2002) thePPC is well positioned to build an integrated mental rep-resentation of the visual scene However it is importantto note that the present experimental paradigm focusedon capacity limits in storing all of the information pres-ent in the visual scenemdashthat is both the identity (color)and the location of objects Although object and spatialworking memory activate overlapping networks (HaxbyPetit Ungerleider amp Courtney 2000 Mecklinger BoschGruenewald Bentin amp von Cramon 2000 Postle Sternet al 2000 Sala et al 2003) the processing of object iden-tity and location information preferentially activates sepa-rate ventral inferior temporal and dorsal parietal processingstreams respectively (Courtney Ungerleider Keil ampHaxby 1996 Haxby et al 1991 Postle amp DrsquoEsposito1999 Postle Stern et al 2000 Ungerleider amp Mishkin1982) Furthermore there is psychophysical and neuro-psychological evidence that VSTM stores for spatial in-formation and object information are at least partly distinct(Della Sala Gray Baddeley Allamano amp Wilson 1999Klauer amp Zhao 2004 Logie 1995 Logie amp Marchetti1991 Mottaghy Gangitano Sparing Krause amp Pascual-Leone 2002 Oliveri et al 2001 Tresch Sinnamon ampSeamon 1993 Woodman Vogel amp Luck 2004) Thusalthough the present study highlights the importance of theposterior parietalsuperior occipital cortex in the capac-ity limit of storing the entire visual scene it is certainlypossible that different brain regions could contribute pre-dominantly to purely object-based forms of VSTM stor-age capacity

Although the correlation analyses support the hypothe-sis that the IPSIOS is involved in VSTM storage capacitythey also suggest that it is unlikely to be the only brainregion contributing to individual differences in VSTMstorage capacity Indeed IPSIOS activity accounts forabout 40 of the intersubject variance in VSTM storagecapacity Correspondingly the ROI-based analyses sug-gested that individual differences in VSTM capacity mayalso be reflected in the activity of additional brain re-gions albeit not as consistently and robustly as in theIPSIOS AC activity was found to be poorly sensitive toindividual differences in VSTM capacity with either theshort (Experiment 1) or the long (Experiment 2) retentioninterval paradigms These results are generally consistentwith the group average results (Todd amp Marois 2004)Time course analysis of the AC suggests that it is activatedlater than the IPSIOS and the VO cortex primarily atretrieval (Todd amp Marois 2004) Similarly other workhas shown that AC activity in visual working memorytasks climaxes at retrieval (Petit Courtney Ungerleider ampHaxby 1998) Together these results are in line with theidea that the AC cortex is involved primarily in response-related processes (Carter et al 1998 Paus 2001 Smith ampJonides 1999 Swick amp Turken 2002 van Veen J DCohen Botvinick Stenger amp Carter 2001 ZhangLeung amp Johnson 2003) and may exert little function instoring the mental representation of the visual scene

By contrast to the AC VO cortex activity showed anintriguing relationship with individual differences inVSTM capacity On the one hand both the group average(Todd amp Marois 2004) and the individual-differences(present study) analyses of Experiment 1 suggest that theVO cortex activity does not robustly track the number ofobjects that can be stored in VSTM Indeed there is evi-dence that the VO cortex may be more sensitive to sensoryperceptual load than to VSTM load since its activity ismodulated by the number of objects present in a scene evenwhen the objects need not be stored in VSTM (Todd ampMarois 2004) Correspondingly we observed no signifi-cant maintenance-related VO cortex activity at the grouplevel in a VSTM task with a long retention interval (Toddamp Marois 2004) On the other hand the individual-differences analysis in Experiment 2 (extended retentioninterval) revealed that VO cortex activity is correlatedwith individual differences in VSTM capacity during themaintenance phase of VSTM Previous studies of ventralstream contributions to VSTM (in either the VO or theinferior temporal cortex) have yielded conflicting results(Druzgal amp DrsquoEsposito 2003 Jha amp McCarthy 2000Leung et al 2002 Linden et al 2003 Munk et al2002 Pessoa et al 2002 Sala et al 2003) with severalof these studies showing no evidence of sustained activ-ity across extended retention intervals (Jha amp McCarthy2000 Munk et al 2002 Pessoa et al 2002) The resultsof the latter studies including our own (Todd amp Marois2004) suggest that information is not maintained in theventral stream during VSTM However the individual-differences analysis in Experiment 2 indicates that evenwhen a group approach reveals neither a load effect noreven a sustained response throughout the retention in-terval of a VSTM task activation levels in the VO cor-tex can still contain information about individual differ-ences in VSTM capacity These results may serve as acautionary note that simply performing group averageanalyses of visual working memory load as is currentlyperformed in most studies may conceal more subtleneural contributions to VSTM that are revealed with anindividual-differences approach

Our group analysis of VSTM capacity did not revealany load-sensitive regions in the lateral frontal or theprefrontal cortex even when the statistical threshold wasrelaxed tenfold (Todd amp Marois 2004) This is despitethe fact that numerous studies in human and nonhumanprimates have shown the importance of the frontal andprefrontal cortex in visual working memory (J D Cohenet al 1997 Courtney et al 1997 Funahashi et al 1989Jha amp McCarthy 2000 Leung et al 2002 Miller Erick-son amp Desimone 1996 Munk et al 2002 Postle BergerTaich amp DrsquoEsposito 2000 Quintana amp Fuster 1992Rao Rainer amp Miller 1997) For this reason we furtherexplored possible contributions of frontalprefrontal re-gions to VSTM capacity by analyzing a region of therpMFG that surfaced in the SPM when the threshold inthe group average analysis of VSTM storage capacity(Todd amp Marois 2004) was relaxed 100-fold (Figure 6A)The location of this rpMFG activation is consistent with

152 TODD AND MAROIS

the findings of several visual working memory studies(Courtney et al 1998 Jha amp McCarthy 2000 Leunget al 2002 Linden et al 2003 Pessoa et al 2002)However the peak response function across set sizes forthis brain region revealed a step function that differedmarkedly from the quadratic behavioral function de-scribing the number of objects stored in VSTM (Fig-ure 6B Todd amp Marois 2004) These results stronglysuggest that the rpMFG does not store individual repre-sentations of visual objects and hence is unlikely to rep-resent the site of VSTM storage capacity This conclu-sion is further supported by the finding that the rpMFGdoes not appear to robustly track individual differencesin VSTM capacity

If the rpMFG does not closely track the number of ob-jects stored in VSTM what might account for its step-function with VSTM load The Talairach coordinates ofthe rpMFG place it near the human homologue of thefrontal eye field (FEF Paus 1996) an area involved incontrolling eye movements and covert shifts of attention(Corbetta 1998) Thus rpMFG activity could reflect ei-ther microsaccades attention shifts or more generallyspeaking attentional deployment during the VSTM taskInterestingly a similar step-function in the human FEFhas also been found in a visual objectndashtracking experi-ment in which a parametric manipulation of attentionalload was used (Culham Cavanagh amp Kanwisher 2001)lending further credence to the idea that the rpMFG rolein VSTM may be attention related Specifically the MFGcould help maintain attentional focus toward the objectrepresentations that are stored in the PPC and the occipitalcortex The involvement of the MFG in VSTM tasks maybe particularly important for long retention intervals thatrequire maintenance of attentional focus which may ac-count for the moderate correlation between this brain re-gionrsquos activity and individual differences in VSTM capac-ity Such an attentional function of the frontalprefrontalcortex in working memory has been proposed by Curtisand DrsquoEsposito (2003)

Thus although the present MFG results are consistentwith the notion that the frontalprefrontal cortex is in-volved in VSTM (eg J D Cohen et al 1997 Courtneyet al 1998 Courtney et al 1997 Jha amp McCarthy2000 Leung et al 2002 Linden et al 2003) they sup-port recent models suggesting that the role of these brainregions in visual working memory does not include stor-age of visuospatial information per se (Curtis amp DrsquoEs-posito 2003 DrsquoEsposito amp Postle 1999 Passingham ampSakai 2004 Postle Berger Goldstein Curtis amp DrsquoEs-posito 2001 Rowe Toni Josephs Frackowiak amp Pass-ingham 2000) Indeed these studies are generally con-sistent with brain lesion work indicating that althoughthe prefrontal cortex may be required for active mainte-nance of visual information over long delays it likelydoes not dictate storage capacity (DrsquoEsposito amp Postle1999)

The results of both the group average (Todd amp Marois2004) and the individual-differences (present study) analy-

ses are highly consistent with a recent electrophysiologicalstudy of VSTM storage capacity (Vogel amp Machizawa2004) That study demonstrated a strong correlation be-tween amplitude differences of ERPs across memoryarray sizes and individual differences in VSTM capacityFurthermore the ERP signal was strongest at parietaland occipital electrode sites a position that is consistentwith the posterior parietaloccipital foci of activation ob-served in the present imaging study

As with the ERP findings our fMRI study revealed apositive correlation between an individualrsquos behavioralmeasure of VSTM capacity and the set size at which theneural response reached asymptote Other working mem-ory studies have shown a positive relationship betweenperformance and neural activity (eg Olesen et al 2004Pessoa et al 2002) However the relationship betweenbrain activity and performance levels is not always pos-itive since increased task performance has also been as-sociated with decreased brain activity (eg BeauchampDagher Aston amp Doyon 2003 Jansma Ramsey Slagteramp Kahn 2001 Jenkins Brooks Nixon Frackowiak ampPassingham 1994 Raichle et al 1994) Such inverse re-lationships are typically assumed to reflect more effi-cient neural processing (eg Jansma et al 2001 Rypmaet al 2002) If so the positive correlation between PPCactivity and individualsrsquo VSTM capacity suggests thatincreased capacity may not be associated with more ef-ficient neural processing per se Instead the storage ofadditional objects in VSTM is likely to result from ei-ther an enhancement of activity of the nerve cells withina given neural tissue or the recruitment of additionalcells within the same tissue In either case our resultssuggest that subjects who can store a larger representa-tion of the visual scene may do so because they have agreater neural cache for this representation in the PPC

REFERENCES

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Baddeley A [D] (1986) Working memory New York Oxford Uni-versity Press

Baddeley A D amp Logie R (1999) Working memory The multiplecomponent model In A Miyake amp P Shah (Eds) Models of work-ing memory Mechanisms of active maintenance and executive con-trol (pp 28-61) New York Cambridge University Press

Beauchamp M H Dagher A Aston J A amp Doyon J (2003)Dynamic functional changes associated with cognitive skill learningof an adapted version of the Tower of London task NeuroImage 201649-1660

Becker M W Pashler H amp Anstis S (2000) The role of iconicmemory in change-detection tasks Perception 29 273-286

Bor D Duncan J Wiseman R J amp Owen A M (2003) Encod-ing strategies dissociate prefrontal activity from working memory de-mand Neuron 37 361-367

Boynton G M Engel S A Glover G H amp Heeger D J (1996)Linear systems analysis of functional magnetic resonance imaging inhuman V1 Journal of Neuroscience 16 4207-4221

Braver T S Cohen J D Nystrom L E Jonides J Smith E Eamp Noll D C (1997) A parametric study of prefrontal cortex in-volvement in human working memory NeuroImage 5 49-62

Callicott J H Mattay V S Bertolino A Finn K Coppola R


Frank J A Goldberg T E amp Weinberger D R (1999) Phys-iological characteristics of capacity constraints in working memoryas revealed by functional MRI Cerebral Cortex 9 20-26

Carter C S Braver T S Barch D M Botvinick M M Noll Damp Cohen J D (1998) Anterior cingulate cortex error detectionand the online monitoring of performance Science 280 747-749

Chafee M V amp Goldman-Rakic P S (1998) Matching patterns ofactivity in primate prefrontal area 8a and parietal area 7ip neuronsduring a spatial working memory task Journal of Neurophysiology79 2919-2940

Chun M M amp Potter M C (1995) A two-stage model for multi-ple target detection in rapid serial visual presentation Journal of Ex-perimental Psychology Human Perception amp Performance 21 109-127

Cohen J Cohen P West S G amp Aiken L S (2003) Applied mul-tiple regressioncorrelation analysis for the behavioral sciences (3rded) Mahwah NJ Erlbaum

Cohen J D Perlstein W M Braver T S Nystrom L E NollD C Jonides J amp Smith E E (1997) Temporal dynamics of brainactivation during a working memory task Nature 386 604-608

Constantinidis C amp Steinmetz M A (1996) Neuronal activity inposterior parietal area 7a during the delay periods of a spatial mem-ory task Journal of Neurophysiology 76 1352-1355

Corbetta M (1998) Frontoparietal cortical networks for directing at-tention and the eye to visual locations Identical independent oroverlapping neural systems Proceedings of the National Academy ofSciences 95 831-838

Corbetta M Kincade J M amp Shulman G L (2002) Neural sys-tems for visual orienting and their relationships to spatial workingmemory Journal of Cognitive Neuroscience 14 508-523

Corbetta M amp Shulman G L (2002) Control of goal-directed andstimulus-driven attention in the brain Nature Reviews Neuroscience3 201-215

Cornoldi C amp Vecchi T (2003) Visuo-spatial working memory andindividual differences New York Psychology Press

Courtney S M Petit L Maisog J M Ungerleider L G ampHaxby J V (1998) An area specialized for spatial working memoryin human frontal cortex Science 279 1347-1351

Courtney S M Ungerleider L G Keil K amp Haxby J V(1996) Object and spatial visual working memory activate separateneural systems in human cortex Cerebral Cortex 6 39-49

Courtney S M Ungerleider L G Keil K amp Haxby J V(1997) Transient and sustained activity in a distributed neural systemfor human working memory Nature 386 608-611

Cowan N (2001) The magical number 4 in short-term memory A re-consideration of mental storage capacity Behavioral amp Brain Sci-ences 24 87-185

Culham J C Cavanagh P amp Kanwisher N G (2001) Attentionresponse functions Characterizing brain areas using fMRI activationduring parametric variations of attentional load Neuron 32 737-745

Curtis C E amp DrsquoEsposito M (2003) Persistent activity in the pre-frontal cortex during working memory Trends in Cognitive Sciences7 415-423

Della Sala S Gray C Baddeley A Allamano N amp Wilson L(1999) Pattern span A tool for unwelding visuo-spatial memoryNeuropsychologia 37 1189-1199

DrsquoEsposito M amp Postle B R (1999) The dependence of span anddelayed-response performance on prefrontal cortex Neuropsycho-logia 37 1303-1315

Druzgal T J amp DrsquoEsposito M (2003) Dissecting contributions ofprefrontal cortex and fusiform face area to face working memoryJournal of Cognitive Neuroscience 15 771-784

Duncan J Bundesen C Olson A Humphreys G Chavda Samp Shibuya H (1999) Systematic analysis of deficits in visual at-tention Journal of Experimental Psychology General 128 450-478

Friedman-Hill S R Robertson L C amp Treisman A (1995) Pari-etal contributions to visual feature binding Evidence from a patientwith bilateral lesions Science 269 853-855

Funahashi S Bruce C J amp Goldman-Rakic P S (1989) Mne-

monic coding of visual space in the monkeyrsquos dorsolateral prefrontalcortex Journal of Neurophysiology 61 331-349

Fuster J M (1990) Inferotemporal units in selective visual attentionand short-term memory Journal of Neurophysiology 64 681-697

Goldman-Rakic P S (1996) Regional and cellular fractionation ofworking memory Proceedings of the National Academy of Sciences93 13473-13480

Haxby J V Grady C L Horwitz B Ungerleider L GMishkin M Carson R E Herscovitch P Schapiro M B ampRapoport S I (1991) Dissociation of object and spatial visual pro-cessing pathways in human extrastriate cortex Proceedings of theNational Academy of Sciences 88 1621-1625

Haxby J V Petit L Ungerleider L G amp Courtney S M(2000) Distinguishing the functional roles of multiple regions in dis-tributed neural systems for visual working memory NeuroImage 11145-156

Jansma J M Ramsey N F Slagter H A amp Kahn R S (2001)Functional anatomical correlates of controlled and automatic pro-cessing Journal of Cognitive Neuroscience 13 730-743

Jenkins I H Brooks D J Nixon P D Frackowiak R S J ampPassingham R E (1994) Motor sequence learning A study withpositron emission tomography Journal of Neuroscience 14 3775-3790

Jha A P amp McCarthy G (2000) The influence of memory loadupon delay-interval activity in a working-memory task An event-related functional MRI study Journal of Cognitive Neuroscience 1290-105

Jolicœur P DellrsquoAcqua R amp Crebolder J M (2001) The at-tentional blink bottleneck In K Shapiro (Ed) The limits of atten-tion Temporal constraints in human information processing (pp 82-99) New York Oxford University Press

Jonides J Smith E E Koeppe R A Awh E Minoshima S ampMintun M A (1993) Spatial working memory in humans as re-vealed by PET Nature 363 623-625

Klauer K C amp Zhao Z (2004) Double dissociations in visual andspatial short-term memory Journal of Experimental PsychologyGeneral 133 355-381

Kourtzi Z amp Kanwisher N (2001) Representation of perceivedobject shape by the human lateral occipital complex Science 2931506-1509

LaBar K S Gitelman D R Parrish T B amp Mesulam M (1999)Neuroanatomic overlap of working memory and spatial attention net-works A functional MRI comparison within subjects NeuroImage10 695-704

Leung H C Gore J C amp Goldman-Rakic P S (2002) Sustainedmnemonic response in the human middle frontal gyrus during on-line storage of spatial memoranda Journal of Cognitive Neuro-science 14 659-671

Linden D E Bittner R A Muckli L Waltz J A Krieges-korte N Goebel R Singer W amp Munk M H J (2003) Cor-tical capacity constraints for visual working memory Dissociation offMRI load effects in a fronto-parietal network NeuroImage 201518-1530

Logie R H (1995) Visuo-spatial working memory Hillsdale NJErlbaum

Logie R H amp Marchetti C (1991) Visuo-spatial working mem-ory Visual spatial or central executive In R H Logie amp M Denis(Eds) Mental images in human cognition (pp 105-115) Amster-dam North-Holland

Luck S J amp Vogel E K (1997) The capacity of visual workingmemory for features and conjunctions Nature 390 279-281

Mecklinger A Bosch V Gruenewald C Bentin S amp vonCramon D Y (2000) What have Klingon letters and faces in com-mon An fMRI study on content-specific working memory systemsHuman Brain Mapping 11 146-161

Miller E K amp Desimone R (1994) Parallel neuronal mechanismsfor short-term memory Science 263 520-522

Miller E K Erickson C A amp Desimone R (1996) Neural mecha-nisms of visual working memory in prefrontal cortex of the macaqueJournal of Neuroscience 16 5154-5167

154 TODD AND MAROIS

Mottaghy F M Gangitano M Sparing R Krause B J ampPascual-Leone A (2002) Segregation of areas related to visualworking memory in the prefrontal cortex revealed by rTMS CerebralCortex 12 369-375

Munk M H Linden D E Muckli L Lanfermann H ZanellaF E Singer W amp Goebel R (2002) Distributed cortical systemsin visual short-term memory revealed by event-related functionalmagnetic resonance imaging Cerebral Cortex 12 866-876

Olesen P J Westerberg H amp Klingberg T (2004) Increasedprefrontal and parietal activity after training of working memory Na-ture Neuroscience 7 75-79

Oliveri M Turriziani P Carlesimo G A Koch G Tomaiuolo FPanella M amp Caltagirone C (2001) Parieto-frontal interac-tions in visual-object and visual-spatial working memory Evidencefrom transcranial magnetic stimulation Cerebral Cortex 11 606-618

Pashler H (1988) Familiarity and visual change detection Percep-tion amp Psychophysics 44 369-378

Passingham D amp Sakai K (2004) The prefrontal cortex and work-ing memory Physiology and brain imaging Current Opinion in Neu-robiology 14 163-168

Paulesu E Frith C D amp Frackowiak R S (1993) The neuralcorrelates of the verbal component of working memory Nature 362342-345

Paus T (1996) Location and function of the human frontal eye-fieldA selective review Neuropsychologia 34 475-483

Paus T (2001) Primate anterior cingulate cortex Where motor con-trol drive and cognition interface Nature Reviews Neuroscience 2417-424

Pessoa K Gutierrez E Bandettini P A amp Ungerleider L G(2002) Neural correlates of visual working memory fMRI ampli-tude predicts task performance Neuron 35 975-987

Petit L Courtney S M Ungerleider L G amp Haxby J V(1998) Sustained activity in the medial wall during working memorydelays Journal of Neuroscience 18 9429-9437

Phillips W A (1974) On the distinction between sensory storage andshort-term visual memory Perception amp Psychophysics 16 283-290

Postle B R Berger J S amp DrsquoEsposito M (1999) Functional neu-roanatomical double dissociation of mnemonic and executive controlprocesses contributing to working memory performance Proceed-ings of the National Academy of Sciences 96 12959-12964

Postle B R Berger J S Goldstein J H Curtis C E ampDrsquoEsposito M (2001) Behavioral and neurophysiological correlatesof episodic coding proactive interference and list length effects in arunning span verbal working memory task Cognitive Affective ampBehavioral Neuroscience 1 10-21

Postle B R Berger J S Taich A M amp DrsquoEsposito M (2000)Activity in human frontal cortex associated with spatial workingmemory and saccadic behavior Journal of Cognitive Neuroscience12 2-14

Postle B R amp DrsquoEsposito M (1999) ldquoWhatrdquondashthenndashldquowhererdquo in vi-sual working memory An event-related fMRI study Journal of Cog-nitive Neuroscience 11 585-597

Postle B R Stern C E Rosen B R amp Corkin S (2000) AnfMRI investigation of cortical contributions to spatial and nonspatialvisual working memory NeuroImage 11 409-423

Quintana J amp Fuster J M (1992) Mnemonic and predictive func-tions of cortical neurons in a memory task NeuroReport 3 721-724

Quintana J amp Fuster J M (1999) From perception to action Tem-poral integrative functions of prefrontal and parietal neurons Cere-bral Cortex 9 213-221

Raichle M E Fiez J A Videen T O MacLeod A M PardoJ V Fox P T amp Petersen S E (1994) Practice-related changesin human brain functional anatomy during nonmotor learning Cere-bral Cortex 4 8-26

Rao S C Rainer G amp Miller E K (1997) Integration of whatand where in the primate prefrontal cortex Science 276 821-824

Rensink R A (2002) Change detection Annual Review of Psychol-ogy 53 245-277

Rensink R A OrsquoRegan J K amp Clark J J (1997) To see or not tosee The need for attention to perceive changes in scenes Psycho-logical Science 8 368-373

Rowe J B amp Passingham R E (2001) Working memory for loca-tion and time Activity in prefrontal area 46 relates to selection ratherthan maintenance in memory NeuroImage 14 77-86

Rowe J B Toni I Josephs O Frackowiak R S J amp Passing-ham R E (2000) The prefrontal cortex Response selection ormaintenance within working memory Science 288 1656-1660

Rypma B Berger J S amp DrsquoEsposito M (2002) The influence ofworking-memory demand and subject performance on prefrontalcortical activity Journal of Cognitive Neuroscience 14 721-731

Rypma B amp DrsquoEsposito M (1999) The roles of prefrontal brain re-gions in components of working memory Effects of memory loadand individual differences Proceedings of the National Academy ofSciences 96 6558-6563

Rypma B amp DrsquoEsposito M (2000) Isolating the neural mechanismsof age-related changes in human working memory Nature Neuro-science 3 509-515

Sakai K Rowe J B amp Passingham R E (2002) Active mainte-nance in prefrontal area 46 creates distractor-resistant memory Na-ture Neuroscience 5 479-484

Sala J B Raumlmauml P amp Courtney S M (2003) Functional topogra-phy of a distributed neural system for spatial and nonspatial informa-tion maintenance in working memory Neuropsychologia 41 341-356

Shafritz K M Gore J C amp Marois R (2002) The role of theparietal cortex in visual feature binding Proceedings of the NationalAcademy of Sciences 99 10917-10922

Shapiro K L Arnell K M amp Raymond J E (1997) The atten-tional blink Trends in Cognitive Sciences 1 291-296

Simons D J (1996) In sight out of mind When object representa-tions fail Psychological Science 7 301-305

Smith E E amp Jonides J (1998) Neuroimaging analyses of humanworking memory Proceedings of the National Academy of Sciences95 12061-12068

Smith E E amp Jonides J (1999) Storage and executive processes inthe frontal lobes Science 283 1657-1661

Sperling G (1960) The information available in brief visual presen-tations Psychological Monographs General amp Applied 74 1-29

Swick D amp Turken A U (2002) Dissociation between conflict de-tection and error monitoring in the human anterior cingulate cortexProceedings of the National Academy of Sciences 99 16354-16359

Talairach J amp Tournoux P (1988) Co-planar stereotaxic atlas ofthe human brain 3-Dimensional proportional system An approachto cerebral imaging (M Rayport Trans) New York Thieme

Todd J J Fougnie D amp Marois R (in press) Visual short-termmemory load suppresses temporo-parietal junction activity and in-duces inattentional blindness Psychological Science

Todd J J amp Marois R (2004) Capacity limit of visual short-termmemory in human posterior parietal cortex Nature 428 751-754

Tresch M C Sinnamon H M amp Seamon J G (1993) Double dis-sociation of spatial and object visual memory Evidence from selec-tive interference in intact human subjects Neuropsychologia 31211-219

Ungerleider L G amp Mishkin M (1982) Two cortical visual systemsIn D J Ingle M A Goodale amp R J W Mansfield (Eds) Analysis ofvisual behavior (pp 549-586) Cambridge MA MIT Press

van Veen V Cohen J D Botvinick M M Stenger V A ampCarter C S (2001) Anterior cingulate cortex conflict monitoringand levels of processing NeuroImage 14 1302-1308

Vogel E K amp Machizawa M G (2004) Neural activity predictsindividual differences in visual working memory capacity Nature428 748-751

Vogel E K Woodman G F amp Luck S J (2001) Storage of featuresconjunctions and objects in visual working memory Journal of Exper-imental Psychology Human Perception amp Performance 27 92-114


Ward B D (2000) Simultaneous inference for fMRI data Availableat httpafninimhnihgovpubdist docmanualsAlphaSimpdf

Wojciulik E amp Kanwisher N (1999) The generality of parietal in-volvement in visual attention Neuron 23 747-764

Woodman G Vogel E amp Luck S J (2004) Independent visualworking memory stores for object identity and location Manuscriptsubmitted for publication

Zarahn E Aguirre G amp DrsquoEsposito M (1997) A trial-based ex-perimental design for fMRI NeuroImage 6 122-138

Zhang J X Leung H-C amp Johnson M K (2003) Frontal activa-tions associated with accessing and evaluating information in work-ing memory An fMRI study NeuroImage 20 1531-1539

NOTE

1 Whereas the term capacity in Experiment 1 could denote the max-imum number of objects the subjects can store this is not the case forExperiment 2 given that only set sizes 1 and 3 were used However agiven individualrsquos capacity is not fixed since it depends on object com-plexity (Alvarez amp Cavanagh 2004) and task specifics (eg durationof retention interval) Thus the term capacity in this article refers eitherto the maximum number of objects one can store (Experiment 1 Kmax)or to the number of objects one can store at the largest set size tested(Experiment 2 Ksetsize3) K refers to the estimated number of objectsstored at a given set size and therefore varies with set size

(Manuscript received October 8 2004revision accepted for publication March 31 2005)


2003 Munk et al 2002 Pessoa et al 2002 Sala et al2003) the extent to which different nodes of this net-work process distinct components of VSTM is still notresolved (Pessoa et al 2002) Furthermore the neuralbasis of arguably the most distinctive characteristic ofVSTM its severely limited storage capacity is poorlyunderstood Although a parametric load manipulationhas been used in several studies to isolate brain regionsassociated with visual working memory (eg Braveret al 1997 J D Cohen et al 1997 Druzgal amp DrsquoEs-posito 2003 Jha amp McCarthy 2000 Leung Gore ampGoldman-Rakic 2002 Linden et al 2003) few have ex-plored the neural substrates underlying the capacity con-straints of working memory (eg Callicott et al 1999Duncan et al 1999 Linden et al 2003 Olesen West-erberg amp Klingberg 2004 Vogel amp Machizawa 2004)

In a recent study we sought to identify the neural sub-strates associated with the capacity limit in storing a vi-sual scene in VSTM (both object identities and loca-tions Todd amp Marois 2004) In that study even thoughsubjects were shown from one to eight color objects (Fig-ure 1) they were successful in storing only up to three orfour of them in VSTM More important this VSTM stor-age capacity did not appear to be equally distributedacross the neural network subserving visual workingmemory Rather activity in a particular brain region theposterior parietalsuperior occipital cortex (intraparietalsulcus and intraoccipital sulcus) was found to be tightly

correlated with the limited number of objects stored inVSTM (Todd amp Marois 2004) A much weaker VSTM-capacityndashrelated signal was observed in the ventral oc-cipital and frontal cortex These results suggest that akey function of the posterior parietal cortex (PPC) in theneural network of visual working memory is the storageof visuospatial information

The results of this study (Todd amp Marois 2004) werebased on a group average of VSTM load That is wesought to isolate brain regions that correlated with theaverage number of objects stored in VSTM at each loadHowever an examination of individual storage capacityfunctions reveals a wide range of individual VSTM capac-ities (Figure 2) Using a formula modified from Pashler(1988) by Cowan (2001) to estimate VSTM capacity themaximum number of objects maintained in VSTM wasfound to vary considerably between individuals from174 to 637 This variation in capacity could arise froma wide spectrum of factors ranging from differences inbiology (eg genetics age and possibly gender) to taskexperience (eg Olesen et al 2004 Raichle et al 1994)and to differences in task strategies (Cornoldi amp Vecchi2003 Rypma Berger amp DrsquoEsposito 2002) But irre-spective of what may be the underlying cause(s) for theseindividual differences in VSTM capacity of most sig-nificance here is that a group average analysis does notcapture the neural basis of individual differences sinceit treats intersubject variability as error If the activity of

Figure 1 Trial design Each trial began with the presentation of two digits whichwere rehearsed subvocally throughout the trial Next a varying memory load of coloreddisks (one to eight) was presented Following a brief retention interval (1200 msec inExperiment 1 9200 msec in Experiment 2) the subjects determined whether a probedisk matched in color the disk presented at the same position in the sample displayFinally a judgment was made regarding the two rehearsed digits

Fixation(1000 msec)

Auditory probe(1500 msec)

Probe display(1750 msec)

Retention interval(1200 9200 msec)

Sample display(150 msec)

Fixation(1400 msec)

Auditory stimuli presentation(1000 msec)

Time

3 1

+

146 TODD AND MAROIS





METHOD


















RESULTS



148 TODD AND MAROIS









A

B

C

L R

(t)621442

04

03

02

01

0

ndash011 2 3 4 5 6 7

Kmax

Act

ivat

ion

diffe

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e (

)

04

03

02

01

0

ndash01

ndash02

Act

ivat

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diffe

renc

e (

)

0 1 2 3Ksetsize3






A B04

03

02

01

0

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ndash 02

03

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01

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ndash 01

ndash 02

ndash031 2 3 4 5 6 7

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0 1 2 3Ksetsize3

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renc

e (

)

Act

ivat

ion

diffe

renc

e (

)


A B 03

02

01

0

ndash 01

ndash 020 1 2 3

Ksetsize3

Act

ivat

ion

diffe

renc

e (

)

02

01

0

ndash 01

ndash 021 2 3 4 5 6 7

Kmax

Act

ivat

ion

diffe

renc

e (

)

150 TODD AND MAROIS


DISCUSSION





A B

03

02

01

0

ndash 01

ndash 020 1 2 3

Ksetsize3

Act

ivat

ion

diffe

renc

e (

)

02

01

0

1 2 3 4 5 6 7Kmax

Act

ivat

ion

diffe

renc

e (

)

C D

L R

y = ndash7 mm

(t)506212

02

01

0

Sig

nal c

hang

e (

)

4

3

2

1

0

Num


1 2 3 4 6 8Set size






152 TODD AND MAROIS







REFERENCES























































154 TODD AND MAROIS




















































NOTE



146 TODD AND MAROIS





METHOD


















RESULTS



148 TODD AND MAROIS









A

B

C

L R

(t)621442

04

03

02

01

0

ndash011 2 3 4 5 6 7

Kmax

Act

ivat

ion

diffe

renc

e (

)

04

03

02

01

0

ndash01

ndash02

Act

ivat

ion

diffe

renc

e (

)

0 1 2 3Ksetsize3






A B04

03

02

01

0

ndash 01

ndash 02

03

02

01

0

ndash 01

ndash 02

ndash031 2 3 4 5 6 7

Kmax

0 1 2 3Ksetsize3

Act

ivat

ion

diffe

renc

e (

)

Act

ivat

ion

diffe

renc

e (

)


A B 03

02

01

0

ndash 01

ndash 020 1 2 3

Ksetsize3

Act

ivat

ion

diffe

renc

e (

)

02

01

0

ndash 01

ndash 021 2 3 4 5 6 7

Kmax

Act

ivat

ion

diffe

renc

e (

)

150 TODD AND MAROIS


DISCUSSION





A B

03

02

01

0

ndash 01

ndash 020 1 2 3

Ksetsize3

Act

ivat

ion

diffe

renc

e (

)

02

01

0

1 2 3 4 5 6 7Kmax

Act

ivat

ion

diffe

renc

e (

)

C D

L R

y = ndash7 mm

(t)506212

02

01

0

Sig

nal c

hang

e (

)

4

3

2

1

0

Num


1 2 3 4 6 8Set size






152 TODD AND MAROIS







REFERENCES























































154 TODD AND MAROIS




















































NOTE














RESULTS



148 TODD AND MAROIS









A

B

C

L R

(t)621442

04

03

02

01

0

ndash011 2 3 4 5 6 7

Kmax

Act

ivat

ion

diffe

renc

e (

)

04

03

02

01

0

ndash01

ndash02

Act

ivat

ion

diffe

renc

e (

)

0 1 2 3Ksetsize3






A B04

03

02

01

0

ndash 01

ndash 02

03

02

01

0

ndash 01

ndash 02

ndash031 2 3 4 5 6 7

Kmax

0 1 2 3Ksetsize3

Act

ivat

ion

diffe

renc

e (

)

Act

ivat

ion

diffe

renc

e (

)


A B 03

02

01

0

ndash 01

ndash 020 1 2 3

Ksetsize3

Act

ivat

ion

diffe

renc

e (

)

02

01

0

ndash 01

ndash 021 2 3 4 5 6 7

Kmax

Act

ivat

ion

diffe

renc

e (

)

150 TODD AND MAROIS


DISCUSSION





A B

03

02

01

0

ndash 01

ndash 020 1 2 3

Ksetsize3

Act

ivat

ion

diffe

renc

e (

)

02

01

0

1 2 3 4 5 6 7Kmax

Act

ivat

ion

diffe

renc

e (

)

C D

L R

y = ndash7 mm

(t)506212

02

01

0

Sig

nal c

hang

e (

)

4

3

2

1

0

Num


1 2 3 4 6 8Set size






152 TODD AND MAROIS







REFERENCES























































154 TODD AND MAROIS




















































NOTE



148 TODD AND MAROIS









A

B

C

L R

(t)621442

04

03

02

01

0

ndash011 2 3 4 5 6 7

Kmax

Act

ivat

ion

diffe

renc

e (

)

04

03

02

01

0

ndash01

ndash02

Act

ivat

ion

diffe

renc

e (

)

0 1 2 3Ksetsize3






A B04

03

02

01

0

ndash 01

ndash 02

03

02

01

0

ndash 01

ndash 02

ndash031 2 3 4 5 6 7

Kmax

0 1 2 3Ksetsize3

Act

ivat

ion

diffe

renc

e (

)

Act

ivat

ion

diffe

renc

e (

)


A B 03

02

01

0

ndash 01

ndash 020 1 2 3

Ksetsize3

Act

ivat

ion

diffe

renc

e (

)

02

01

0

ndash 01

ndash 021 2 3 4 5 6 7

Kmax

Act

ivat

ion

diffe

renc

e (

)

150 TODD AND MAROIS


DISCUSSION





A B

03

02

01

0

ndash 01

ndash 020 1 2 3

Ksetsize3

Act

ivat

ion

diffe

renc

e (

)

02

01

0

1 2 3 4 5 6 7Kmax

Act

ivat

ion

diffe

renc

e (

)

C D

L R

y = ndash7 mm

(t)506212

02

01

0

Sig

nal c

hang

e (

)

4

3

2

1

0

Num


1 2 3 4 6 8Set size






152 TODD AND MAROIS







REFERENCES























































154 TODD AND MAROIS




















































NOTE








A B04

03

02

01

0

ndash 01

ndash 02

03

02

01

0

ndash 01

ndash 02

ndash031 2 3 4 5 6 7

Kmax

0 1 2 3Ksetsize3

Act

ivat

ion

diffe

renc

e (

)

Act

ivat

ion

diffe

renc

e (

)


A B 03

02

01

0

ndash 01

ndash 020 1 2 3

Ksetsize3

Act

ivat

ion

diffe

renc

e (

)

02

01

0

ndash 01

ndash 021 2 3 4 5 6 7

Kmax

Act

ivat

ion

diffe

renc

e (

)

150 TODD AND MAROIS


DISCUSSION





A B

03

02

01

0

ndash 01

ndash 020 1 2 3

Ksetsize3

Act

ivat

ion

diffe

renc

e (

)

02

01

0

1 2 3 4 5 6 7Kmax

Act

ivat

ion

diffe

renc

e (

)

C D

L R

y = ndash7 mm

(t)506212

02

01

0

Sig

nal c

hang

e (

)

4

3

2

1

0

Num


1 2 3 4 6 8Set size






152 TODD AND MAROIS







REFERENCES























































154 TODD AND MAROIS




















































NOTE



150 TODD AND MAROIS


DISCUSSION





A B

03

02

01

0

ndash 01

ndash 020 1 2 3

Ksetsize3

Act

ivat

ion

diffe

renc

e (

)

02

01

0

1 2 3 4 5 6 7Kmax

Act

ivat

ion

diffe

renc

e (

)

C D

L R

y = ndash7 mm

(t)506212

02

01

0

Sig

nal c

hang

e (

)

4

3

2

1

0

Num


1 2 3 4 6 8Set size






152 TODD AND MAROIS







REFERENCES























































154 TODD AND MAROIS




















































NOTE








152 TODD AND MAROIS







REFERENCES























































154 TODD AND MAROIS




















































NOTE
















































154 TODD AND MAROIS




















































NOTE









NOTE



posterior parietal cortex activity predicts individual ...posterior parietal/superior occipital...

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