Neural correlates of implicit object identification

Neuropsychologia 42 (2004) 1247–1259

Neural correlates of implicit object identification

D. Pinsa,∗, M. E. Meyerb, J. Foucherc, G. Humphreysd, M. Boucartaa Laboratoire de Neurosciences Fonctionnelles et Pathologies, FRE 2726-CNRS, Université Lille 2,Explorations Fonctionnelles de la Vision, CHRU Lille, Hopital Roger Salengro, 59037 Lille, France

b Service de Biophysique et Traitement de l’Image Médicale, CHU Amiens Nord, 80054 Amiens, Francec Université Louis Pasteur, IPB, UPRES-A 7004 du CNRS, 4 rue Kirschleger, 67085 Strasbourg, France

d University of Birmingham, Behavioural Brain Sciences Centre, Birmingham B15 2TT, UK

Received 7 February 2003; received in revised form 29 January 2004; accepted 30 January 2004

Abstract

The present study sought to assess neural correlates of implicit identification of objects by means of fMRI, using tasks that requirematching of the physical properties of objects. Behavioural data suggests that there is automatic access to object identity when observersattend to a physical property of the form of an object (e.g. the object’s orientation) and no evidence for semantic processing when subjectsattend to colour. We evaluated whether, in addition to neural areas associated with decisions to specific perceptual properties, areasassociated with access to semantic information were activated when tasks demanded processing of the global configuration of pictures. Weused two perceptual matching tasks based on the global orientation or on the colour of line drawings. Our results confirmed behaviouraldata. Activations in the inferior occipital cortex, fusiform and inferior temporal gyri in both tasks (orientation and colour) account forperceptual and structural processing involved in each task. In contrast, activations in the posterior and medial parts of the fusiform gyrus,shown to be involved in explicit semantic judgements, were more pronounced in the orientation-matching task, suggesting that semanticinformation from the pictures is processed in an implicit way even when not required by the task. Thus, this study suggests that corticalregions usually involved in explicit semantic processing are also activated when implicit processing of objects occurs.© 2004 Elsevier Ltd. All rights reserved.

Keywords: Visual areas; Object processing; Semantic processing; Implicit processing

1. Introduction

1.1. Automatic access to semantic knowledge:Behavioural data

Several pieces of evidence suggest that stored knowledgeabout objects is accessed automatically, in the sense thatit occurs even when subjects are engaged in another taskwhile trying to avoid recognising objects or faces (Sergent,1985). In particular, automatic access to object identity canbe inferred from evidence of interference effects based onsemantic information about objects that should be ignored,as shown by picture-word interference effects (Glaser &Dungelhoff, 1984; Shen, Hu, Yacoub, & Ugurbil, 1999),“negative priming” (Tipper, 1985; Tipper & Driver, 1988),and visual scene perception (Biederman, 1981; Biederman,Mazzanotte, & Rabinowitz, 1982; seeBoucart & Humphreys,1992 for a review). These interference effects, based on

∗ Corresponding author. Tel.:+33-3-20-44-62-81;fax: +33-3-20-44-62-81.

E-mail address: [email protected] (D. Pins).

semantic information activated by objects, have also beenreported when stimuli do not enter awareness. For instance,although contralesional stimuli are missed during bilateralstimulation in patients with visual extinction, properties ofthat extinguished stimuli, such as their identity and seman-tic information, can affect performance on the ipsilesionalstimuli in an implicit manner (for reviews, seeDriver, 1996;Driver & Vuilleumier, 2001). Thus, in these studies, the ac-cess to semantic information occur in an irrepressible way,whilst not required by the task and without any attentionalcontrol. It is why some authors (Boucart & Humphreys,1992, 1994, 1997; Boucart, Humphreys, & Lorenceau, 1995;Humphreys & Boucart, 1997), as in Stroop effect studies(MacLeod, 1991), described this process as automatic.

Such an interference was shown by Boucart and col-leagues (Boucart & Humphreys, 1992, 1994, 1997; Boucartet al., 1995; Humphreys & Boucart, 1997), using a paradigminvolving a sequential matching task. A reference picturewas first centrally displayed, and then two pictures were pre-sented (one defined as target and one as distractor), left andright of the fixation point. Observers were asked to matchthe reference picture to one of the two lateral pictures on

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1248 D. Pins et al. / Neuropsychologia 42 (2004) 1247–1259

the basis of a prespecified physical property (e.g. the ori-entation of the main axis of the picture). The target wasthe picture with the same physical property as the reference(e.g. the same orientation), whereas the distractor was thepicture with a different physical property as the reference(e.g. another orientation). To assess the impact of seman-tic information on this physical matching task, relationshipsbetween the reference, the target and the distractor weremanipulated. The reference and the target were either phys-ically identical, semantically related (e.g. two animals) orunrelated (e.g. an animal and a vehicle). For each of theseconditions, the distractor could also be semantically relatedor unrelated to the reference. Observers were never informedabout the semantic relations between stimuli. Although se-mantic information was irrelevant to the task, response times(RTs) were faster when reference and target objects weresemantically related compared to when they were unrelated.On the contrary, RTs were slower when reference and dis-tractor objects were semantically related compared to whenthey belonged to different semantic categories (Boucart &Humphreys, 1992, 1994). These results indicate that atten-tion to a physical property of the pictures failed to preventsemantic processing.

These experiments were run with different physical prop-erties. Based on a large set of data (Boucart & Humphreys,1992, 1994, 1997; Boucart et al., 1995; Humphreys &Boucart, 1997), it was found that there is a semantic inter-ference when tasks required processing of the object globalconfiguration (for instance, orientation, size or shape ofthe picture). However, any effects of the semantic relationsbetween the stimuli were eliminated when pictures werematched on the basis of object surface property (for instance,luminance, colour or texture). Boucart and colleagues(Boucart et al., 1995; Humphreys & Boucart, 1997) went onto argue that the processing of the global configuration of thepicture was critical to the activation of stored object repre-sentations. Effects of semantic relations between the stimulidid not occur in matching tasks based on colour, luminanceor motion where processing of the global configuration wasnot necessary. The most convincing demonstration of thisargument was provided by a colour-matching task in whichobservers were constrained to analyse the global configura-tion to perform the task (Humphreys & Boucart, 1997). Inthis study, the outline contour was composed of two ran-domly distributed colours. One colour was present in twothirds of the pixels making up the reference picture and ob-servers were asked to decide which of the two lateral pictureshad the same “dominant” colour as the reference picture. Incontrast to a previous study with homogeneously colouredpictures where no effect of semantic relations betweenstimuli was observed (Boucart & Humphreys, 1994), this“dominant” colour matching task required integration acrossthe spatial area covered by the whole picture. An effectof the semantic relations between the reference, target anddistractor stimuli was then obtained. In contrast, when ori-entation matching was required on a local part of the stimuli

(the orientation of a line segment drawn inside the picture),semantic interference was reduced (Humphreys & Boucart,1997). This result was recently replicated byMurray andJones (2002).

What is the mechanism responsible for semantic inter-ference in the matching paradigm? Though processing ofphysical information must begin before semantic informa-tion is activated (Riddoch & Humphreys, 1987), it still maynot be completed before semantic representations are con-tacted. Then, semantic interferences would depend on therelative speed of processing of physical and semantic in-formation for decision. It may be that processing of theglobal configuration of pictures is slowed down by conflict-ing information from local parts (e.g. the orientation axisof the parts composing the picture) thus providing a tem-poral advantage for semantic information in decision mak-ing. Once attention is focused on the global configuration,the magnitude of semantic effects depends on the relativespeed of processing of physical and semantic information fordecision.

1.2. The present study

The present study sought to assess this implicit identifi-cation by means of fMRI. The aim was to evaluate whether,in addition to cortical areas associated with the process-ing of physical properties of the object, areas associatedwith explicit processing of semantic information were acti-vated when tasks required processing of the global configu-ration of pictures. The procedure developed byBoucart andHumphreys (1992)was used, with two perceptual match-ing tasks based on the global orientation or on the colour ofline drawings. The evidence of semantic processing showed(Boucart & Humphreys, 1992, 1994; Boucart et al., 1995)in a matching task based on orientation, but not on colour,will allow us to reveal cortical activations related to the im-plicit processing of semantic information which could occurin such a task.

A convergence of studies in animals and humans basedon electrophysiological recordings, lesions and more re-cently on neuro-imaging and TMS, have reported theoccipito-temporal pathway as critical for object processing.In tasks requiring explicit object identification (such as pic-ture naming or picture categorisation), the areas activatedhave been found to extend mainly from the fusiform gyrusin the occipital lobe to the adjacent fusiform gyrus in thetemporal lobe.

In this study, global configuration processing in theorientation-matching task should provide an activation of ar-eas involved in structural processing. Moreover, if attentionto the global configuration of an object triggers semanticprocessing in an implicit way, then we expected activationof areas classically involved in identification or semanticcategorisation decisions. Consequently, regions in the ven-tral occipito-temporal cortex, associated with structural andsemantic processing should be activated in this task. Such

D. Pins et al. / Neuropsychologia 42 (2004) 1247–1259 1249

activations should at least be weaker in the colour decisiontask, where attention to a local part is sufficient to reach adecision.

2. Method

2.1. Subjects

Ten healthy volunteers (eight males and two females,mean age 19.4 years old, S.D. 0.8), who gave written in-formed consent, took part in the fMRI experiment. The studywas approved by the ethics committee of Alsace. Partici-pants were scanned with a whole body MRI system (2 T)using multi-slice echo planar imaging (EPI) and a head coil.They were paid for their participation.

Ten new volunteers (10 females, mean age 33.8 yearsold, S.D. 9.4), with normal or corrected to the nor-mal vision, took part in the RT experiment (outside thescanner).

2.2. Stimuli

The stimuli were 20 outline drawings of common objects(animals, vehicles, clothes, pieces of furniture). Thicknessof the line drawings was of one pixel. The main axis ofthe objects was either vertical or horizontal. Two rectangles,one vertical and one horizontal, were used in the controlcondition. In the orientation-matching task, the pictures werepresented in black on a white background. In the colourmatching task, the outline contour of the pictures was eitherblue or green1 on a white background. The mean size of thestimuli was 8 cm high× 4 cm wide for vertical pictures andthe opposite for horizontal pictures. Stimuli were presentedusing PowerPoint software.

2.3. Apparatus

Visual stimulation was generated on the colour screen of aPC computer (Pentium Pro 266 MHz). Images were directlypresented to the viewer’s eyes with the Fibre Optic VideoGlasses (Avotec, Inc.). The global region subtended by theglasses was of 20◦ of visual angle, covering the whole PCscreen. Then, stimulus size was about 5.5× 2.75◦ of visualangle. The glasses were linked by a flexible cable (optic fi-bre) to a colour LCD projector located just outside the MRIbore. This projector was connected by a shielded cable to avideo interface and to the monitor located in the MRI con-trol room. This was combined with an Avotec Audio sys-tem. Images were acquired with a 2.0 T MR scanner (BrukerAG, Karlsruhe, Germany) using a shielded quadrate headcoil (internal diameter 252 mm), designed to fit inside the

1 The two colors blue and green were chosen because Boucart andHumphreys (Boucart & Humphreys, 1994) found that equivalent responsetimes were obtained in the orientation and in the color-matching taskwhen these two colors were used.

echo-planar imaging (EPI) gradient coil (internal diameter332 mm).

2.4. Procedure

Two experimental tasks were run. In the orientation-matching task, participants were instructed to match areference and target stimuli on the basis of their globalorientation (vertical versus horizontal main axis). In thecolour-matching task, participants were asked to match thereference and target stimuli on the basis of their outlinecolour (green versus blue). These two experimental tasks,with pictures, were compared with control tasks in whichpictures were replaced by outline rectangles, to which simi-lar orientation and colour matching was required (seeFig. 1).

On each trial, the reference stimulus was centrally dis-played for 440 ms. After a delay of 440 ms, a pair of pictureswas displayed left and right of the screen for 440 ms (thecentre of the picture located at 7 cm from fixation). Partic-ipants had to decide whether the left or the right stimulushad the same orientation (in the orientation-matching task)or the same colour (in the colour-matching task) as the ref-erence stimulus. They answered in pressing the left or theright key according to the spatial location of the target (thestimulus having the same orientation or colour as the ref-erence stimulus). Target and distractor appeared either onthe left side or on the right side according to the trial. Theinter-trial interval was fixed at 880 ms.

Boucart and colleagues (Boucart & Humphreys, 1992,1994, 1997; Boucart et al., 1995; Humphreys & Boucart,1997) used six matching conditions determined by the re-lationships between the reference stimulus and the target(same orientation or same colour) and between the refer-ence stimulus and the distractor (different orientations orcolours). We only used one of them: reference stimulus, tar-get and distractor were always semantically related, whichwas an intermediate condition where (in behavioural stud-ies) there was a facilitation induced by the relationship be-tween stimulus reference and target and an inhibition due tothe relationship between stimulus reference and distractor.

Prior to the MRI recording, participants were shown ex-amples of the two-orientations or two-colours to be discrim-inated on a sheet of paper and they were given a 10 minpractice session on the computer. The practice session wasfollowed by the two experimental tasks (orientation andcolour-matching). Both tasks were run during the same ex-perimental session. Half of the participants started with theorientation-matching task before the colour-matching task;the half others started with the colour-matching task. RTswere not recorded. An experimental session was composedof 48 blocks of 15 trials each (33 s per block). For each task(orientation or colour), 12 experimental blocks with pic-tures (experimental condition) as stimuli alternated (boxcarparadigm) with 12 control blocks with rectangles as stim-uli (control condition). Participants were told that blocks ofpictures would alternate with blocks of rectangles but that


Fig. 1. Illustration of the paradigm and stimuli used in the present study. The experimental condition (pictures of objects) is presented on the top andthe control condition (rectangles) on the bottom. The matching task based on global orientation (the main axis of the object) is presented on the leftand the matching task based on colour (outline colour) is presented on the right of the figure. A reference outline drawing of an object was centrallydisplayed for 440 ms; 440 ms later, two objects (a target and a distractor) were presented 7 cm from the fixation. Subjects were required to decide if theleft or the right lateral picture had the same global orientation (vertical or horizontal) or the same colour (green or blue) as the central reference picturepreviously presented.

they had to attend only to the orientation (or to the colour)of the stimuli regardless of their identity.

In order to record RT data, both tasks (orientation andcolour) were run on ten new subjects outside the scanner.The same stimuli and procedure were used, except that stim-uli were now presented on the colour screen of the PC com-puter. Subjects were placed at a viewing distance of 70 cm.Stimulus size was the same as the one used in the scanner(5.5 × 2.75◦ of visual angle). RTs and performances wererecorded at each trial.

2.5. fMRI imaging protocol

For each participant and each task, a series of echo pla-nar functional images was first collected to provide func-tional images sensitive to BOLD contrast. Single-shot fMRIacquisitions were performed with high performance gradi-ents (30 mT/m, 147.5�s rise time) using a typical gradientecho (EPI fMRI sequence). A total of 5400 gradient echoechoplanar images were then obtained for each experimen-tal task, using 180 volumes of 30 contiguous 3.43 mm slices(repetition time: 4420 m, echo time: 43 m) at a resolution

of 64× 64 pixels (tip angle: 90◦) in a 22 cm field of view(with no gap, and with selective fat suppression), allowingan isotropic 3.43 mm voxel resolution. Images were axialslices aligned to the plane intersecting the anterior and pos-terior commissures.

At the end of the experimental session a series of con-ventional structural images was collected to provide detailedanatomic information. Conventional imaging consisted ofturbo-RARE sequence (resolution: 128×128, flip angle: 90◦,echo time: 73.8 ms, repetition time 15,000 ms, RARE factor:8, field of view: 25.6 cm, 60 slices—2 mm thick—with nogap, isotropic voxel resolution: 2 mm). The head of partici-pants was immobilised with pillows and cushions to reducemotion artefacts. The entire session, including both func-tional and structural sequences, lasted about 1 h.

2.6. Statistical analysis

Data were analysed by statistical parametric mapping withSPM99b (methodology group—Welcome Department ofCognitive Neurology, London, UK:http://www.fil.ion.ucl.ac.uk/spm—Friston et al., 1995) implemented in Matlab

http://www.fil.ion.ucl.ac.uk/spm

http://www.fil.ion.ucl.ac.uk/spm


(Mathworks Inc., Sherborn, MA), with False DiscoveryRate included (http://www.sph.umich.edu/∼nichols/FDR;Genovese, Lazar, & Nichols, 2002). Functional scanswere first realigned, spatially normalised into a stereo-taxic space (giving a new resolution with a pixel size of2 mm× 2 mm× 2 mm) and then smoothed with a 8 mm fullwidth at half maximum isotropic Gaussian kernel.

The aim of the statistical analysis was to identify andcompare regional activation for each experimental task(orientation- and colour-matching tasks on objects) relativeto meaningless visual controls which nevertheless inducedsimilar task demands (in the rectangle baselines). First, im-ages for the experimental condition (pictures of objects) andthe control condition (rectangles) were averaged, to gener-ate a single scan volume per condition, for each participantand each task (orientation and colour). The condition effectswere estimated using a general linear model for each andevery voxel. The resulting set of voxel values constituted astatistical parametric map of the t-statistic, statistical para-metric mapping (SPM) (t), which was then transformed tothe unit normal distribution, SPM (Z).

A random effect design allowed us to extrapolate theresults to the population. Consequently, a group analysiswas performed to identify anatomical areas of consistentactivation across subjects. To detect the neural substratesspecific for the experimental condition in each experimentaltask (orientation- and colour-matching tasks on pictures ofobjects), we computed contrast images between experimen-tal (pictures of objects) and control conditions (rectangles)for each task. We then obtained one scan volume per task,corresponding to the subtraction between the object andrectangle conditions. We only reported regions made upof a cluster size of at least 20 voxels and activated abovethreshold ofP < 0.001 (uncorrected). One subject had tobe discarded from this analysis since the scanned regionsdid not include the infero-temporal region. Then, the differ-ential activations (difference in signal amplitude) betweentasks (orientation and colour) were tested in a second levelanalysis (two-samplet-test). In this analysis, a region ofinterest has been delimited in the occipito-temporal region(centre:{0, −64,−16}, size:{140, 70, 30}, search volume:297,000 mm3), allowing mainly to reveal activations in ar-eas extending from the fusiform gyrus in the occipital lobeto the fusiform gyrus in the temporal lobe. We only reportedregions made up of a cluster size of at least 100 (800 mm3)and activated above threshold ofP < 0.01 (uncorrected),and both family wise error and false discovery rate (P <

0.05) corrections for multiple comparisons were applied.

3. Results

3.1. Behavioural results

Mean percentage of correct responses was about 97%. Inprevious studies (Boucart & Humphreys, 1992, 1994, 1997;

Fig. 2. Mean reaction times (RTs) and mean error rates obtained in tensubjects outside the scanner in both conditions (rectangles and objects)for both tasks (orientation and colour). Main results show that: (1) RTswere not significantly different between both tasks; (2) the only significanteffect was found between both conditions in the orientation-matchingtask. These results confirm previous behavioural data, showing a semanticinterference in the orientation- but not in the colour-matching task.

Boucart et al., 1995; Humphreys & Boucart, 1997), seman-tic interference was shown through RTs data. Our results(seeFig. 2) show that, in the control condition with rect-angles as stimuli, RTs were not significantly different be-tween orientation- (373 ms) and colour-matching (368 ms)tasks, supporting that both tasks were of equal difficulty[t(9) < 1; ns]. Although RTs did not differ significantly inthe colour-matching task when rectangles (368 ms) or ob-jects (348 ms) were presented ([t(9) = 2.10; ns]; with RTslonger for rectangles than for objects), RTs were signifi-cantly slower in the orientation-matching task when objects(426 ms) rather than rectangles (373 ms) were presented [t(9)= 3.50; P < 0.007]. So, as shown by Boucart and Col-leagues (Boucart & Humphreys, 1992, 1994, 1997; Boucartet al., 1995; Humphreys & Boucart, 1997), a semantic in-terference effect appeared in the orientation-matching taskbut not in the colour-matching task.

3.2. fMRI imaging results

Table 1and Fig. 3 present the locations for significantclusters of activation for each experimental task (orientation-and colour-matching tasks on objects).

3.2.1. Orientation-matching taskCompared to the control condition (rectangles), sig-

nificant regions activated by the orientation experimentalcondition (pictures) first included areas classically involvedin visual and object processing. These differentially acti-vated structures ran from the occipital cortex (BA 18/19)through the inferior temporal lobes and the fusiform gyrus(BA 37/20) bilaterally. The other regions differentiallyactivated were the intra-parietal sulcus (BA 7/40) bilater-ally, the right precuneus (BA 7), the right superior frontalgyrus (BA 6) and the right inferior and middle frontal gyri(BA 44/9/46). Statistical parametric maps are presented inFig. 3.

http://www.sph.umich.edu/~nichols/FDR


Table 1Differential activations associated with orientation or colour-matching tasks on objects as compared with rectangles (P < 0.001, uncorrected for multiplecomparisons; cluster sizes of at least 20 voxels), and associated with the orientation versus colour-matching tasks (P < 0.01, uncorrected for multiplecomparisons; cluster sizes of at least 100 voxels), expressed in terms of usual name and Brodmann’s classification of cortical area, peakZ score withina particular activated region, size of the activated cluster and stereotactic coordinates of the activation peak

Task Region Side Brodmannareas

Z score Cluster size(voxels)

Talairach coordinates(x, y, z)

Orientation Fusiform gyrus Left 37/20 5.11 1648 −26, −50, −22Fusiform gyrus/inferior temporal gyrus Left 19/37 4.75 – −48, −66, −20Inferior occipital gyrus Left 18 4.64 – −28, −100, −2Fusiform gyrus/inferior temporal gyrus Right 37 4.68 1984 46,−52, −20Fusiform gyrus Right 37/20 4.60 – 28,−40, −22Inferior occipital gyrus/fusiform gyrus Right 18/19 4.20 – 52,−78, −4Intra-parietal sulcus Left 7/40 3.47 20 −32, −64, 48Intra-parietal sulcus Right 7/40 5.04 33 50,−50, 54Precuneus Right 7 4.14 40 4,−72, 56Superior frontal gyrus Right 6 3.87 30 34, 16, 62Middle frontal gyrus/inferior frontal gyrus Right 44/9/46 3.47 59 42, 36, 12

Colour Inferior occipital gyrus/fusiform gyrus Right 18/19 5.45 1384 32,−86, −16Fusiform gyrus Right 37/20 4.49 – 28,−40, −24Inferior occipital gyrus/fusiform gyrus Left 18/19 4.76 1481 −32, −86, −18Fusiform gyrus Left 37/20 4.69 – −28, −46, −24Middle occipital gyrus Right 18 4.14 150 30,−94, 12

Orientation vs. colour Lateral posterior fusiform gyrus Right 19/37 4.34 202 56,−58, −14Medial fusiform gyrus Left 37 3.68 301 −28, −56, −8Lateral posterior fusiform gyrus Left 19/37 3.44 221 −50, −68, −16

Fig. 3. The left of the figure shows differential activations observed in the orientation-matching task (green) and in the colour-matching task (red)in therandom effect model (group analysis). Brain views from all sides are displayed. Contrast images are computed between experimental (object pictures)and control (rectangles) conditions. The images have been thresholded atP < 0.001 uncorrected for multiple comparisons at the voxel level. Clustersize made up of at least 20 voxels were considered. Consistent responses are shown for both tasks. The right of the figure shows the same differentialactivations in coronal and horizontal slices.


Fig. 4. Mean amplitude of the fMRI signal (with confidence interval of 90%) in the lateral posterior fusiform gyrus (56,−58, −14) in the righthemisphere and in the medial (−28, −56, −8) and lateral part (−50, −68, −16) of the left fusiform gyrus, respectively. These regions are those wherethe amplitude of the fMRI signal was significantly greater in the orientation-matching task than in the colour-matching tasks on objects (when contrastsbetween object and rectangle conditions where first done), as revealed by a second level analysis run in the occipito-temporal region (region of interest).Data are averaged across all subjects.

3.2.2. Colour-matching taskCompared to the control condition (rectangles), signifi-

cant regions activated by the colour experimental condition(pictures) were areas involved in visual and object process-ing (seeFig. 3). These differentially activated structures werethe right middle occipital cortex (BA 18), and from the infe-rior occipital cortex (BA 18/19) through the fusiform gyrus(BA 19/37/20) bilaterally.

3.2.3. Differential activation between orientation- andcolour-matching tasks

Differential activation between tasks (orientation ver-sus colour) were then revealed in a second analysis. Welooked for cortical areas for which the fMRI signal changewas significantly greater in the orientation- than in thecolour-matching task.Table 1 and Fig. 4 present the lo-cations for significant differential clusters of activationobserved in the occipito-temporal region (region of in-terest). In the orientation-matching task, compared to thecolour-matching task, significant differential activationswere observed in the lateral posterior part of the fusiformgyrus in the right hemisphere (BA 19/37) and in both thelateral posterior (BA 19/37) and the medial parts of thefusiform gyrus (BA 37) in the left hemisphere.

4. Discussion

4.1. Object and semantic processing

The main objective of this study was to assess the cor-tical regions involved in implicit access to semantic infor-mation. Given that semantic interference occurred in ourmatching-task when processing of the global configura-

tion was required (matching on the basis of global orien-tation), we expected that areas involved in global shapeprocessing and in semantic processing of objects wouldbe activated in the orientation-matching task with objectpictures. In contrast, activations in these areas should beweaker in the colour-matching task, where local part pro-cessing was enough and no semantic interference appearedin behavioural performances. Two distinct regions in theoccipito-temporal cortex showed an increased activity inthe orientation compared to the colour-matching task: themedial part of the fusiform gyrus in the left hemisphere andthe lateral posterior part of the fusiform gyrus bilaterally.

4.1.1. Regions involved in semantic processingThe occipito-temporal pathway, or ventral stream, is

consistently reported as critical for object processing. Us-ing different stimuli and tasks, studies have determinedcortical areas involved in different stages of object pro-cessing, including feature or global form extraction andhigher-level processing giving access to semantic knowl-edge. PET, fMRI and more recently TMS studies havedemonstrated a pathway of brain areas which is activatedin tasks requiring explicit object identification such as pic-ture naming (Kiyosawa et al., 1996; Malach et al., 1995;Martin, Wiggs, Ungerleider, & Haxby, 1996; Moore &Price, 1999a; Okada et al., 2000; Stewart, Meyer, Frith,& Rothwell, 2001in a TMS study), same/different namejudgements (Kosslyn, Alpert, & Thompson, 1995; Peraniet al., 1999), delayed matching (Ishai, Ungerleider, Martin,Schouten, & Haxby, 1999), picture categorisation (Gauthier,Anderson, Tarr, Skudlarski, & Gore, 1997; Sergent, Ohta,& MacDonald, 1992; Vandenberghe, Price, Wise, Josephs,& Frackowiak, 1996) and object decision (Gerlach, Law,Gade, & Paulson, 1999, 2000; Schacter et al., 1995). The


areas activated have been found to extend mainly fromthe fusiform gyrus in the occipital lobe (BA 19/37) to theadjacent fusiform gyrus in the temporal lobe (BA 20/37).In addition, objects have also been shown to produce abilateral focus of activation in the lateral occipital region(LO) of the hemispheres (Grill-Spector, Kushnir, Hendler,& Malach, 2000; Grill-Spector, Kushnir, Edelman, Itzchak,& Malach, 1998a; Grill-Spector et al., 1998b; Kanwisher,Chun, McDermott, & Ledden, 1996; Malach et al., 1995),with a correlation found between recognition performanceand fMRI signal in this region (Grill-Spector et al., 2000).LO is located posteriorly on the lateral part of the fusiformgyrus, branching more anteriorly into ventral and dorsalbranches reaching to the anterior border of BA 19 and 37,respectively. The present study show activity in these re-gions in both tasks (orientation and colour), suggesting thatsome process on objects were done in both tasks. Never-theless, the amplitude of the fMRI signal was significantlygreater in most of these regions in the orientation- comparedto the colour-matching task, where an access to semanticinformation was suggested by behavioural data.

Studies, mainly interested in object category-relatedactivations, suggested a distributed representation of infor-mation about objects in the ventral pathway (Ishai et al.,1994), with the same regions including not only the visualfeatures but also semantic knowledge (Chao, Haxby, &Martin, 1999). This conclusion agree with results of studieson mental imagery showing that subsets of these regionsare also activated during the generation of mental imagesfrom long-term memory (Ishai, Haxby, & Ungerleider,2002a; Ishai, Ungerleider, & Haxby, 2000b; O’Craven &Kanwisher, 2000). Moreover, differential responses foundfor non-preferred objects in a category-related region (Ishaiet al., 1994) increase with cognitive demands to thesenon-preferred categories (Ishai, Ungerleider, Martin, &Haxby, 2000c), suggesting that the response to non-preferredobjects in a category-related region carry information aboutthe identity of those objects (Chao, Weisberg, & Martin,2002). The access to semantic information which seems tooccur in our orientation-matching task involve an increasein cognitive demand in this task, that could then explain theincrease in fMRI signal we observed in different regionsof the ventral pathway in the orientationcompared to thecolour-matching task.

Some attempts have been made to distinguish the corticalregions associated with different stages of object process-ing. These studies were more interested in cerebral activityshared by different type of stimuli or category of objects. Inparticular, distinct regions in the ventral occipito-temporalcortex were identify byMoore and Price (1999a)investi-gating word and object (relative to meaningless visual con-trols) processing orBar et al. (2001)using different levelsof recognition success for different objects.

The medial surface of the anterior fusiform gyrus wasshown to be activated in the left hemisphere for both wordsand objects, irrespective of the task (naming or viewing:

Moore & Price, 1999a) and its activity was shown to increasebilaterally as a function of subjective rating of recognitionsuccess (Bar et al., 2001). Authors (Bar et al., 2001; Moore& Price, 1999a) associated this region with processing of ob-ject identity and access to semantic objects representations.This agree with previous studies showing a similar region tobe more active when the level of semantic details at whichwords and objects (visual and auditory) were compared (ina matching task) increased (Adams & Janata, 2002), forsemantic relative to perceptual decisions on visually pre-sented words and objects (Vandenberghe et al., 1996), forsemantic relative to phonological decisions on orally pre-sented words (Démonet, Price, Wise, & Frackowiak, 1994;Démonet et al., 1992), for naming words and objects rel-ative to naming letters and colours (Moore, Price, Friston,& Frackowiak, 1996), for retrieving perceptual knowledgefrom long-term memory (Martin, Haxby, Lalonde, Wiggs,& Ungerleider, 1995), and for generating visual mental im-ages of heard object’s names relative to passive listeningof abstract words (D’Esposito et al., 1997). In our study,we found activation in the left medial fusiform gyrus sig-nificantly more pronounced in the orientation- than in thecolour-matching task. Then this activation could be directlyrelated to the implicit semantic processing of object picturesthat occur in this task.

Another site was particularly highlighted in the lateralposterior occipito-temporal region. This region was usuallyassociated with structural processing. Activation in this lat-eral posterior occipito-temporal region does not differentiatefamiliar from unfamiliar objects (Shen et al., 1999), suggest-ing that this region is involved primary in the extraction ofvisual shape information, or in the bottom-up constructionof shape descriptions from simple visual features (lowerlevel feature extraction, segmentation, grouping, surface ex-traction and shape analysis). Consequently, this region waspreviously more associated with sensory processing thanwith explicit recognition (Kanwisher et al., 1996; Malachet al., 1995; Rosier et al., 1997). Nevertheless, some studiesshowed that activity there was also modulated by recogni-tion success (object processing contrasted to word process-ing (Kohler, Kapur, Moscovitch, Winocur, & Houle, 1995),as a direct function of recognition success (Bar et al., 2001),although to a smaller extent as in the medial part of the ante-rior fusiform region. This increased activity was also foundby Vandenberghe et al. (1996)in both associative (matchingtask on picture meaning) and visual (matching on real lifesize) semantic tasks. Therefore, they suggested that, com-pared with visual-perceptual tasks, semantic tasks may leadto enhanced activation of picture-specific structural descrip-tions, which would produce an increased activity in thisregion. Consequently, the increased activity we found in ourstudy in the posterior occipito-temporal region bilaterallyin the orientationcompared to the colour-matching taskcould then be related with semantic processing. The accessto semantic information which seems to occur in this taskwould then lead to enhanced activation of picture-specific


structural descriptions in the posterior occipito-temporalregion.

Thus, differential activations observed in the orientationcompared to the colour-matching task in the medial partof the fusiform gyrus in the left hemisphere and the lateralposterior part of the fusiform gyrus bilaterally suggest anaccess to semantic information in this task. Such a resultagrees with behavioural data showing that semantic inter-ference appears when task required processing of the globalconfiguration of the object (e.g. orientation of the main axis)and is eliminated when pictures were matched on the basisof object surface property (e.g. colour). Nevertheless, wefound activation, although to a smaller extend, in these sameregions in the colour-matching task. Such an activity sug-gests that some object processing occurred in this task. Inparticular, it could reflect local part processing of objects. Inthe orientation-matching task, object processing would in-volve access to semantic information whereas in the colourmatching task this object processing would only consist inpre-recognition analysis. Finally, this activity in the colour-matching task could be strengthened by the fact that half ofparticipants started with the orientation-matching task.

4.1.2. Laterality of occipito-temporal areas in objectperception

Although some studies report bilateral changes inoccipito-temporal areas when comparing object identifica-tion with a fixation condition (Grill-Spector et al., 1998a,b;Kanwisher et al., 1996; Kohler et al., 1995; Koustaal et al.,2001; Okada et al., 2000), others find strongly lateralized(left hemisphere) activations (Damasio, Grabowski, Tranel,Hichwa, & Damasio, 1996; Kosslyn et al., 1994; Moore &Price, 1999a; Perani et al., 1995, 1999; Sergent et al., 1992).These findings have suggested that different cortical sitesare involved in different aspects of object recognition. In ourstudy, we found greater activation in the orientation- com-pared to the colour-matching task bilaterally in the lateralpart of the fusiform gyrus but only in the left hemispherein the medial part of the fusiform gyrus.

Because the right hemisphere shows greater sensitivityto alterations of perceptual form, some authors (Gerlachet al., 1999, 2000; Marsolek, Squire, Kosslyn, & Lulenski,1994; Martin et al., 1996; Okada et al., 2000; Sergent et al.,1992; Vuilleumier, Henson, Driver, & Dolan, 2002) sug-gest that it may be dominant in structural processing, withthe inferior temporal lobe as a part of the hierarchicallyorganized object-processing pathway for the extraction ofvisual features. The right hemisphere would be crucialwhen perceptual operations involving corrections, trans-formation or rotation of the incoming stimulus have to beimplemented (Sergent, 1985; Vuilleumier et al., 2002). Incontrast, activation in the left fusiform has been relatedto semantic processing for pictures and words (Sergent,1985; Vandenberghe et al., 1996). This has been confirmedby more recent studies.Gerlach, Law, Gade, and Paulson(2000)reported activation in the left inferior temporal gyrus

(BA 20) in categorisation tasks compared to object decisiontasks, suggesting a role for the left inferior temporal gyrusin semantic processing. Moreover,Stewart et al. (2001)in aTMS study found a significant increase in latency to namepictures when stimulation was given over the left BA 37compared with the Vertex site (which served as a controlsite). In contrast, subjects who also received TMS over rightBA 37 showed no significant difference in picture namingwhen stimulation was given over this site compared to theVertex site. Stimulation applied over the left BA 37 siteproduced significantly longer naming latencies comparedwith stimulation given over the right BA 37.

Such a laterality could explain why the differentialactivation found in the orientationcompared to thecolour-matching task appeared in more areas in the left thanin the right hemisphere. On the one hand, this differentialactivation could reflect the access to semantic informationinvolved by the orientation task. This result agree withprevious imaging results (Boucart et al., 2000) showing anactivation in the left inferior temporal lobe, which occurredmore frequently in an orientation decision task than in acolour decision task. On the other hand, if the right hemi-sphere is more associated with structural processing thanthe left, activations found in the right hemisphere in bothtasks (orientation and colour) confirms structural processinginvolved in both tasks. The fact that no significant differenceappeared in the signal amplitude between both tasks in themedial part of the fusiform gyrus in the right hemisphere,suggests this area more involved in local processing.

4.1.3. Other activated areasOther regions, outside the ventral occipito-temporal

pathway, whereas not involved in the colour-matchingtask, showed a significant activation in the orientationmatching-task. We observed activations in the inferior andmiddle frontal gyrus (BA 9/44/46) in the right hemisphere.A region extending from the inferior frontal gyrus to thefrontal operculum (BA 44) has been shown to be involvedin conditions requiring internal verbalisation (Grafton,Fadiga, Arbib, & Rizzolatti, 1997) and silent naming ofpictures of objects (Martin et al., 1996). Grafton and col-leagues (Grafton et al., 1997) suggested that this region isinvolved in coding words corresponding to the name and/oractions of the presented object.Gerlach et al. (1999, 2000)showed an activation in the right inferior frontal gyrus as-sociated with object decision tasks, even when these tasksare contrasted with categorisation tasks. They suggest thatthis activation could reflect access to stored visual/spatialknowledge (structural descriptions) for manipulable objects.

The middle frontal gyrus (BA 46) has been reported tobe involved in semantic processing (Bottini et al., 1994;Price, Wise, & Frackowiak, 1996). Although usually foundin the left hemisphere (Binder et al., 1997; Démonet et al.,1992), Kang, Constable, Gore, and Avrutin (1999)found aright-lateralized activation of BA 46 in a semantic task onwords. The middle frontal gyrus has also been implicated in


verbal working memory tasks (Petrides, Alivisatos, Meyer,& Evans, 1993). Therefore, some authors (e.g.Clark et al.,1997; Demb et al., 1995; Gabrieli et al., 1996; Gerlach et al.,1999, 2000) have suggested that these regions are involvedin operating on and/or maintaining higher-level verbal rep-resentations (i.e. semantic, lexical or phonological informa-tion). Then, these additional activated areas strengthen thefirst results suggesting that structural and semantic process-ings are involved in the orientation-matching task, whileonly structural processing appeared in the colour-matchingtask.

4.2. Perceptual processing

4.2.1. Colour processingConsistent with lesion studies that have demonstrated

colour deficits associated with damage to ventral cortex(Damasio, Yamada, Damasio, Corbett, & McKee, 1980;Meadows, 1974; Zeki, 1990), PET imaging (Gulyás &Roland, 1994; Zeki, 1990), fMRI mapping (Sakai et al.,1995) and ERP source localisation studies (Andrew & Chen,1997; Plendl et al., 1993) have repeatedly shown the cerebralresponse to be located in the lingual and fusiform gyri ofthe visual extrastriate cortex. In particular,Hadjikhani, Liu,Dale, Cavanagh, and Tootell (1998), who have thoroughlymapped cortical regions responsible to colour processing inhumans, reported prominent colour-selective activation inthe representations of the fovea in the classically retinotopicvisual areas (V1, V2, V3/VP, V3A and V4v). Moreover,they describe a new area, V8, that responds slightly betterthan neighbouring cortical regions to coloured stimuli. Thisarea is located beyond the classically retinotopic visual ar-eas (foveal V8 centred at±33,−65,−14). Then, V8 differsfrom V4v in its global functional properties, including butnot limited to colour sensitivity and would be involved inwavelength-dependent processing and perhaps in the con-scious perception of colour itself (based on the response toillusory colours).

Although our data do not allow such a sharp analyseof the different retinotopic visual areas, we can assumethat part of the activity found in the areas from the in-ferior occipital cortex even to the posterior part of thefusiform gyrus in the colour-matching task (contrast im-ages between experimental- outline drawings of objects-and control-rectangles conditions) were the result of colourperception. However, since the same basic task-relatedprocessing was required for both pictures and rectangles,then, the obtained contrast images should not show thisactivation. The significant contrast images thus suggest thatcolour processing of complex pictures increases activationin the areas usually involved to process these attributes.

4.2.2. Orientation and global shape processingFMRI and PET studies investigating cortical areas in-

volved in the processing of shape information have shownthat the perception of geometrical or meaningless shapes

in passive viewing (Martin et al., 1996), in same/differentmatching (Georgopoulos et al., 2001; Perani et al., 1999), inobject construction (Georgopoulos et al., 2001), in shape cat-egorisation (Gulyás & Roland, 1994) and in shape discrim-ination (Corbetta, Miezin, Dobmeyer, Shulman & Petersen,1991b; Shen et al., 1999) tasks results in ventrally dis-tributed activations including mainly the occipito-temporalgyrus (BA 18/19/37) and lingual gyrus (BA 18/17).

The present orientation-matching task demanded theextraction of the main axis of objects, requiring in turnthat subjects process the global configurations. This globalshape processing should occur in both the object and therectangle conditions, though (as already noted) it maybe more difficult for the objects (due to the presence ofmultiple conflicting orientations). Thus, any activation ofcortical areas involved in global shape processing should belarger in the orientation-matching task on objects than onrectangles. Activation in the occipito-temporal cortex (BA18/19/37) in our orientation-matching task could reflect inpart this global shape processing on complex pictures. Wealso found activation in the occipito-temporal cortex bilat-erally (BA 18/19/37) in the colour-matching task. It is notclear whether this activation can be related to the globalshape processing or can be related to the local part pro-cessing of the picture. Nevertheless, the activations in theseregions have been found to be larger in the orientation thanin the colour-matching task, supporting the idea that theprocessing of the global configuration was more required toperform the orientation-matching task.

4.2.3. Simple to complex stimuliDrawings of multi-component relative to simple shaped

objects has previously been shown to activate three areas inthe right hemisphere: the medial extrastriate cortex (BA 18),the occipito-temporal cortex (BA 19/39) and the fusiformgyrus (BA 20).Moore and Price (1999b)found this patternof activation for pictures of animals relative to fruits andcomplex artefacts (such as vehicles) relative to simple (suchas tools) man-made objects. They suggested that the rightoccipito-temporal and fusiform gyri are affected by the com-plexity of the visual configurations of objects. It could bethat pictures of objects activate the LO more strongly sincethey contain a richer source of complex features, comparedto the more repetitive or less naturalistic texture patterns.

In both tasks (colour and orientation), we found largeractivation for object pictures than for rectangles in the re-gions involved in complex stimulus processing. Indeed,the increased activation found for objects in the rightoccipito-temporal and fusiform cortices in both tasks canbe attributed, at least in part, to the difference in complexitybetween rectangles and object pictures.

4.2.3.1. Selective attention. In each of our tasks, subjectshad to select the target on the basis of a given physical char-acteristic (colour or orientation). Therefore, mechanismsof selective attention were involved in the matching tasks.


Selective attention to a particular stimulus attribute hadbeen shown to increase neural activation in extrastriate ar-eas that preferentially process the selected attribute (Haxbyet al., 1994). Selective attention to either shape, colouror speed leads to response enhancement in regions of theposterior portion of the fusiform gyrus, including area V4(Beauchamp, Haxby, Jennings, & DeYoe, 1999; Clark et al.,1997; Corbetta, Miezin, Dobmeyer, Shulman, & Petersen,1991a; Haxby et al., 1994; O’Craven, Rosen, Kwong,Treisman, & Savoy, 1997). More precisely, for shape, acti-vations have been localised in the collateral sulcus, fusiformand parahippocampal gyri, the calcarine/parieto-occipitalsulcus intersection, and in temporal cortex along the su-perior temporal sulcus. For colour, they were localised incollateral sulcus between lingual and fusiform gyri and indorsolateral occipital cortex (Corbetta et al., 1991a; Engel,Zhang, & Wandell, 1997; Gulyás, Larsson, Amunts, Zilles,& Roland, 1997).

It follows that some of the activations we found in infe-rior occipital, occipito-temporal and fusiform gyri in bothtasks (colour and orientation) may reflect selective attention,rather than perceptual or structural processing of stimuli.However, the rectangle control condition also required se-lective attention mechanisms to shape or colour. Then, if thesignificant contrast images (between object and rectangleconditions) reflect some attentional mechanisms, it wouldmean that attentional factors are more involved when mean-ingful or more complex stimuli have to be processed.

One other contribution of selective attention to the ob-served differential patterns of activity is as follows. The ex-traction of the global orientation from complex line drawingsmay require the suppression of conflicting information fromlocal parts (e.g. the orientation axis of the parts or outlinecontour composing the picture; seeBoucart & Humphreys,1994). This should not be the case for the colour-matchingtask. Hence, there may be greater attention-related activ-ity in the orientation-matching task on objects. Consistentwith this, activations occurred in supplementary motor area(BA 6) in the right hemisphere and in the intraparietal sul-cus (BA 40) bilaterally, for the orientation-matching taskon pictures of objects only. These areas are other foci ofactivation previously related to selective attention mecha-nisms, and in particular, the premotor/prefrontal activation(BA 6) has been associated to the need to maintain an in-ternal (working memory) representation of the task instruc-tions and difficulty (Haxby et al., 1994; Indovina & Sanes,2001). Although task difficulty was equalised between bothtasks (colour and orientation), as confirmed by similar RTsfound in the control condition, it could be useful in a nextstudy to have a better control on this stimulus complexityand its possible effect in the increased activity in areas alsorelated with a perceptual or semantic processing. A newexperiment should be run using stimuli of different com-plexity levels (more complex geometrical forms involvingconflicting information from the different orientations-localparts-composing the picture).

In conclusion, based on previous behavioural data,we expected an implicit access to object identity in aorientation-matching task but not in a colour-matching task.Our imaging data are consistent with this, suggesting a largeractivation of areas associated with the semantic processingof objects in the orientation than in the colour-matchingtask. The cortical regions previously shown to be involvedin explicit semantic processing also seem to be recruitedin a matching task involving implicit access to semanticinformation.

Acknowledgements

This study was supported by a Programme Hospitalier deRecherche Clinique to M. Boucart, D. Pins and M.E. Meyerand by a EEC Biomed grant (No. PL962775) to M. Bou-cart and G. Humphreys. The authors are grateful to CorinneMarrer for her help in recording brain images.

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Neural correlates of implicit object identification