Neural Correlates of Topographic Mental Exploration: The ... · mental exploration task in an environment learned from actual navigation (mental navigation task). An-other group of

NeuroImage 12, 588–600 (2000)doi:10.1006/nimg.2000.0648, available online at http://www.idealibrary.com on

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Neural Correlates of Topographic Mental Exploration: The Impactof Route versus Survey Perspective Learning

E. Mellet, S. Bricogne, N. Tzourio-Mazoyer, O. Ghaem, L. Petit, L. Zago,O. Etard, A. Berthoz,* B. Mazoyer, and M. Denis†

*LPPA-College de France and †LIMSI CNRS Orsay, Universite de Caen, CNRS FRE 2233, CEA LRC 13V, 14074 Caen Cedex, France

Received February 28, 2000

There are two major sources of information to builda topographic representation of an environment,namely actual navigation within the environment(route perspective) and map learning (survey perspec-tive). The aim of the present work was to use positronemission tomography (PET) to compare the neuralsubstrate of the topographic representation built fromthese two modes. One group of subjects performed amental exploration task in an environment learnedfrom actual navigation (mental navigation task). An-other group of subjects performed exploration in thesame environment learned from a map (mental maptask). A right hippocampal activation common to bothmental navigation and mental map tasks was evi-denced and may correspond the neural substrateof a “dual-perspective” representation. The parahip-pocampal gyrus was additionally activated bilaterallyduring mental navigation only. These results suggestthat the right hippocampus involvement would be suf-ficient when the representation incorporates essen-tially survey information while the bilateral parahip-pocampal gyrus would be involved when theenvironment incorporates route information and in-cludes “object” landmarks. The activation of a pariet-ofrontal network composed of the intraparietal sul-cus, the superior frontal sulcus, the middle frontalgyrus, and the pre-SMA was observed in common forboth mental navigation and mental map and is likelyto reflect the spatial mental imagery components ofthe tasks. © 2000 Academic Press

Key Words: spatial mental imagery; route perspec-tive; survey perspective; parieto-frontal network; hip-pocampus; parahippocampus; positron emission to-mography.

INTRODUCTION

Mental exploration constitutes a type of spatialmental imagery, which allows one to activate the

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representation of a previously perceived environ-ment and to move mentally from a point to anotherwhile no visual input is present. To build such aspatial representation, people acquire informationfrom different ways, e.g., by actually navigating inthe environment (information is then acquired in anegocentric or “route” perspective) or by learningmaps (information is acquired in an exocentric or“survey” perspective). The issue whether the topo-graphic representation built from either route per-spective or survey learning exhibited distinct or sim-ilar properties has been addressed by several studies(Thorndyke and Hayes-Roth, 1982; Taylor and Tver-sky, 1992; Ferguson and Hegarty, 1994; Schneiderand Taylor, 1999; Taylor et al., 1999). These behav-ioral data provide discrepant results and it remainsunclear whether perspective is maintained in mem-ory. Some studies have compared the representationof environments built from text descriptions in sur-vey perspective, text descriptions in route perspec-tive, or memorization of maps and found no effect ofthe perspective learning on subject’s performance ina task testing their memory of the spatial organiza-tion of the environment (Taylor and Tversky, 1992).This supports that survey or route description mayresult in topographic representations that shareproperties.

On the other hand, other studies found an effect ofthe perspective learning on the properties of the topo-graphic representation built from either text descrip-tions (Schneider and Taylor, 1999) or visual experience(Thorndyke and Hayes-Roth, 1982; Taylor et al., 1999).For example, route distance estimations are more ac-curate than Euclidean distance estimations when in-formation has been initially acquired by actual naviga-tion, while the reverse pattern is observed when thespatial information has been encoded through surveylearning (Thorndyke and Hayes-Roth, 1982). In thesame vein, survey-learning subjects make more errors

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when judging orientation than when estimating of lo-cation landmarks belonging to the environmentlearned. On the opposite, route-learning subjects judgeorientation more accurately than they judge landmarklocation. The structure of the topographic representa-tion seems therefore in part constrained by the route orsurvey perspective in which spatial information is ac-quired.

Previous neuroimaging studies have investigatedthe neural substrate of navigation and studies exploredeither encoding (Maguire et al., 1996, 1998a; Aguirre et

l., 1996) or retrieval (Maguire et al., 1997, 1998b;haem et al., 1997; Aguirre and D’Esposito, 1997) of

opographical knowledge. In most of these studies, thenvironment was learned in route perspective, but theuilt representation was assumed to use both surveynd route information (for example, see Maguire et al.1997, 1998a). It thus appears that while the neuralubstrate of both encoding and retrieval of topographicnformation has been studied, the effect of the learningerspective on the neural structures involved in theetrieval and utilization of the topographic representa-ion has, to our knowledge, never been considered.

In the present work, we compared the neural basis ofpatial knowledge derived from two typical sources ofpatial information, namely actual navigation and mapearning. Since, the topographic representations builtrom either route or map visual learning have beenhown to exhibit some distinctive behavioral features,e hypothesized that the neural network engaged in

he activation of the representation would differ ac-ording to the perspective in which the topographicnformation has been acquired. We also expected neu-al structures common to both perspectives reflectingeatures shared by the two types of representation. Inrder to test this hypothesis, we used positron emissionomography (PET) to compare the pattern of activationn two groups of subjects during the mental explorationf the same environment that was learned in two dif-erent ways: either from actual navigation or from aap. Unlike most of the neuroimaging studies, our

xploration tasks were performed in absence of anyisual input and thus included a strong component ofpatial mental imagery. This make our tasks very closeo the natural activity of way finding. Actually, findingne’s way requires most of the time to mentally simu-ate a route or to inspect a mental map of the environ-

ent, and thus strongly calls for spatial mental imag-ry.In the following, “mental navigation” will refer to theental exploration of a representation learned from an

ctual walk in the environment (Study 1), and “mentalap” will refer to the mental exploration of a repre-

entation learned from a map (Study 2). The two tasksill be jointly named “mental exploration tasks.”

MATERIALS AND METHODS

Because it was important to use exactly the samenvironment for both route and survey learning, wehose a multistudy design. The constitution of twoistinct groups of subjects for the two types of learningas crucial to ascertain that the subjects learned thenvironment in one perspective only.

Study 1: Mental Navigation

The mental navigation task is part of a previousork published elsewhere (Ghaem et al., 1997). Data

have been fully reanalyzed in order to be included in amultistudy design (See data analysis section).

Subjects

Five healthy right-handed male volunteers (20–22years old) participated in this study. All were free fromnervous disease or injury and had no abnormalities ontheir T1-weighted magnetic resonance images (MRI).In order to ensure optimal homogeneity of the sampleof the subjects with respect to their imagery abilities,subjects were selected as high visuospatial imagers onthe basis of their scores on the Minnesota Paper FormBoard (MPFB) and on the Mental Rotations Test(MRT); all subjects scored beyond the 75th percentile ofa population of 100 male subjects.

PET Methodology and Task Design

(a) Learning and training phase: Learning. Theay before the PET scanning, the subjects walkedithin an environment (a park) they had never seenefore. The learning phase included three repetitionsf the same walk within the park. The first walk wasuided by the experimenter. The subjects were in-tructed to memorize the route they covered includinghe direction changes (Fig. 1, left). Furthermore, dur-ng this first walk, seven landmarks were pointed outnd named by the experimenter (see Fig. 1A, left).uring the second and third walks, the subjects had to

ollow the first route they learned and name the land-arks they met, under the experimenter’s control.Training. The day after learning, three to four

ours before the PET scanning, subjects were trainedo the mental navigation task proper. The names of twoandmarks (e.g., “gas station,” “phone box”) belongingo the environment were presented through earphoneso indicate the route segment that the subject had toentally simulate. The subject was instructed to recall

he visual and sensory-motor mental images of hisalk in a route perspective along the path segment.hree sessions of training including five segments de-

ivered in different orders were performed. The lengthf the path segments varied from 48 to 172 m.

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(b) PET procedure. Six sequential measurementsof the normalized regional cerebral blood flow (NrCBF)were obtained from each subject on an ECAT 953B/31PET camera (time acquisition: 80 s), replicating a se-ries of three experimental conditions presented in ran-domized order. All conditions were performed eyesclosed in total darkness, a black and opaque cloth cov-ering the whole camera. For the purpose of the presentstudy, two conditions only were included: A rest condi-tion and a mental navigation task. In the rest conditionsubjects were eyes closed in total darkness. The secondtask was the mental navigation task described above inthe training section, namely mentally follow the pathbetween two landmarks verbally delivered and press akey when the second landmark was reached. Five dif-ferent segments, randomly delivered, were used duringeach replication of the mental navigation condition.

The duration of the mental navigation along eachsegment was recorded. In order to monitor the sponta-neous eye movements executed during the two condi-tions, horizontal electroculograms (EOG) were re-corded for each subject using surface electrodes placedat the outer canthi and at the right ear as a reference.

Study 2: Mental Map

Subjects

Six healthy right-handed male volunteers (age:19–25 years) selected for their high spatial imageryability participated in this study. All were free fromnervous disease or injury and had no abnormalities ontheir T1-weighted magnetic resonance images (MRI).

PET Methodology and Task Design

(a) Learning and training phase: Learning. Theday before PET scanning, the subjects were taught themap thanks to eight slides projected on a blank screen.The map to learn represented the park described aboveand included seven colored dots that were linked bypaths (Fig. 1, left). The dots were located at the sameplace than the landmarks belonging to the actual en-vironment. The final size of the map was length:1.64 m, width: 1 m and viewing angle: 25° 3 15°. Thefirst slide represented the whole map, including theseven colored dots. The subjects were told to examinethe map during 3 min in order to memorize it. The nextseven slides represented the whole map with a singledot, each slide showing one of the seven dots. Eachslide was presented during 5 s and the name of theorresponding dot was said by the experimenter. Theearning phase was completed by a last presentation ofhe whole map including the seven dots during 3 min,s in the initial phase. Note that there was no explicitnstruction to scan along the paths during the learninghase.To ensure that the subjects had accurately memo-

rized the map, they were required to pin point each dotlocation on a slide of a blank map at the end of thelearning phase.

Training. The day after the learning, three to fourhours before the PET scanning, subjects were trainedin the mental map task proper. Eyes closed, they had tovisualize the map as accurately as possible includingthe seven dots, they were then given through ear-phones the name of two colored dots (e.g., “red,” “blue”)and had then to imagine a laser dot following the pathsegment drawn on the original map between the twodots. Once the second dot was reached, the subjectshad to press a button with their right index, this actionreleasing the auditory delivery of a second pair of dots.Two sessions of training including segments deliveredin a different order were performed. The length of thepath segments varied from 15 to 198 cm on the mapcorresponding in the actual environment to a lengthvarying from 48 to 574 m.

(b) PET Procedure

Four to six sequential measurements (time acquisi-tion: 90 s) of NrCBF were obtained from each subjecton an ECAT Exact HR1 PET camera, replicating twoor three times a series of two experimental conditionspresented in randomized order (Due to technical prob-lems, the PET camera did not start during some of theacquisition resulting in missing replications in somesubjects). All conditions were performed eyes closed intotal darkness, a black and opaque cloth covering thewhole camera.

In the rest condition, subjects were eyes closed intotal darkness. The second task was the mental maptask described above in the training section, namelymentally follow the path between two dots auditorilydelivered and press a key when the second dot wasreached. Fourteen different segments, randomly deliv-ered, were used during each mental map conditions.The duration of the mental scan along each segmentwas recorded.

In order to monitor the spontaneous eye movementsexecuted during both conditions, horizontal electrocu-lograms (EOG) were recorded for each subject usingsurface electrodes placed at the outer canthi and at theright ear as a reference. The EOG system can detectsaccades superior to a one degree of visual angle andwas calibrated before each condition. All EOG recordswere analyzed by computer using a dedicated software(SAMO), which detects saccadic components and quan-tifies the amplitude and frequency of spontaneous sac-cadic eye movements.

Data Analysis

In order to be included in the analysis, all the scansfrom the two studies were processed using the same

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procedure which induced a reanalysis of the CBF datafor the mental navigation study (Study 1). After auto-matic realignment (AIR) (Woods et al., 1997), the orig-inal brain images were transformed into the standardstereotactic Talairach space using the MNI template(Friston et al., 1995a). The camera used in the mental

avigation group have a smaller field of view than thene used in the mental map group. This results in anal volume common to both groups extending in zirection from 163 mm to 227 mm from AC/PC line inhe most anterior part of the brain to 167 mm to 214m in its most posterior part. It thus included hip-

ocampal and parahippocampal regions. The imagesere smoothed using a Gaussian filter of 12 mmWHM leading to a final smoothness of 15 mm FWHM.he rCBF was normalized within and between subjectssing a proportional model. The comparisons acrossonditions were made by way of t statistics. Statisticalarametric maps corresponding to comparisons be-ween conditions and between studies were generatedith the 1999 version of SPM (Friston et al., 1995b).imple comparisons within each study concerned men-al navigation versus rest for Study 1 (Table 1) andental map versus rest for Study 2 (Table 1). For each

omparison, the voxel amplitude t map was trans-ormed in a Z volume that was thresholded at P ,.001 (uncorrected for multiple comparisons).Between-study comparisons included (mental navi-

ation 2 rest) versus (mental map 2 rest) and theeverse comparison, i.e. (mental map 2 rest) versusmental navigation 2 rest) (Table 2, thresholded at P ,.001, uncorrected for multiple comparisons). In ordero avoid “false” activation due to deactivation in theecond contrast, each interaction was masked by theain effect thresholded at 0.05 (for example (mentalavigation 2 rest) versus (mental map 2 rest) wasasked by mental navigation 2 rest).Activations common to different contrasts were iden-

ified by conjunction analysis (Price and Friston, 1997).his analysis was performed to uncover the voxels thatere activated in both mental map and mental navi-ation as compared to rest (Table 2). The threshold waset to P , 0.001 (uncorrected for multiple comparisons)or this conjunction analysis.

RESULTS

Behavioral Results

ye Movements Analysis

Mental navigation. The amplitude of horizontalaccadic eye movements was significantly highermean difference 1.1° 6 0.4°, P 5 0.003, n 5 5, post hoctest) during the mental navigation task than during

he rest condition. Note that although significant, the

ifference in amplitude was only of 1° (which is theinimum angle detected by our EOG system) and no

ignificant difference was observed for the frequency ofaccades between the two conditions.Mental map. The mean amplitude of spontaneous

orizontal saccadic eye movements during both theest and the mental map conditions were 4.7 6 0.4°mean 6 SD) and 6.2 6 3.5°, respectively. No signifi-ant difference between these two conditions was ob-erved in terms of either amplitude or frequency (postoc paired t test, P 5 0.84 and P 5 0.82, respectively).

TABLE 1

Mental Navigation versus Rest and Mental Mapversus Rest (P , 0.001)

Anatomical location ofmaximum voxel

CoordinatesZ

scorex y z

Mental navigation versus restL. intraparietal sulcus/precuneus 216 266 54 5.4L. occipito-parietal sulcus 214 256 20 3.9L. occipito-parietal sulcus 230 264 6 3.5R. occipito-parietal sulcus 24 268 24 4.9R. posterior cingulate gyrus 16 256 12 4.0Median superior frontal gyrus 10 10 48 4.1L. precentral/superior frontal

sulcus 226 22 56 3.5R. precentral/superior frontal

sulcus 36 28 52 3.4R. middle frontal gyrus 30 46 24 3.2R. parahippocampal gyrus 28 224 222 3.2L. parahippocampal gyrus 234 238 28 3.2

Mental map versus restL. intraparietal sulcus/precuneus 28 272 54 4.6L. intraparietal sulcus 222 268 54 3.3R. intraparietal sulcus/precuneus 16 272 52 3.3Median superior frontal gyrus 26 2 54 4.0Median superior frontal gyrus 0 10 46 3.6L. precentral/superior frontal

sulcus 220 24 64 3.2R. precentral/superior frontal

sulcus 38 24 54 3.2R. middle frontal gyrus 34 38 30 4.5R. superior frontal sulcus 32 54 16 3.3L. superior temporal gyrus 264 224 8 4.2R. superior temporal gyrus 62 220 6 4.1R. middle temporal sulcus 56 242 12 3.5R. hippocampus 30 212 218 2.9*R. supramarginal gyrus 48 244 24 3.4L. lenticular nucleus 218 16 0 3.4L. anterior insula 224 28 8 3.3R. lenticular nucleus 26 24 8 3.2

Note. Foci of significant normalized regional cerebral blood flow(NrCBF) increases when mental navigation (upper part) and mentalmap task (lower part) were compared to the rest conditions. Thedata, based, respectively, on five and six subjects are local maximadetected with SPM software. Within these regions, the anatomicallocalization of the maximum Z scores of the voxel is given on thebasis of the MNI template, using the stereotactic coordinates of theTalairach space in mm (R., right; L., left).


Debriefing of the Subjects

Within the five subjects of the navigation group fourreported that they did not use a mental map strategy tomentally navigate but instead used a route perspec-tive.

Within the six subjects of the map group, all ratedthe map mental image as accurate and reported thatthey actually follow the instructions they were givenbefore the experiment (imagine a laser dot followingthe path segment drawn on the original map betweenthe two dots).

Chronometric Data Analysis

The much longer reaction times we reported in themental navigation group compared to the mental map

TABLE 2

Conjunction and Comparison of Mental Mapand Mental Navigation

Anatomical location of max. voxel

CoordinatesZ

scorex y z

Conjunction of mental navigation andmental map

L. intraparietal sulcus/precuneus 210 270 54 6.6L. intraparietal sulcus 222 268 54 5.1R. intraparietal sulcus 22 270 48 4.3R. superior occipital gyrus 40 278 28 3.5Median superior frontal gyrus 2 12 46 5.3L. precentral/superior frontal

sulcus 222 24 54 4.9L. precentral sulcus 234 24 54 3.9R. precentral/superior frontal

sulcus 38 24 52 4.7R. middle frontal gyrus 32 46 24 4.9R. medial frontal gyrus 20 48 210 4.0L. lenticular nucleus/anterior

insula 230 14 4 4.4R. lenticular nucleus 26 16 2 3.2R. hippocampus 26 220 218 3.4L. superior temporal gyrus 266 220 2 4.0R. middle temporal gyrus 64 236 214 3.4

Mental navigation vs mental mapR. occipito-parietal sulcus/cuneus 24 270 24 4.8L. intraparietal sulcus/precuneus 218 260 54 3.2L. posterior cingulate gyrus 212 246 28 3.4L. inferior frontal sulcus 252 16 30 3.2R. parahippocampal gyrus 32 220 226 2.7*L. parahippocampal gyrus 228 236 218 3.1

Mental map vs mental navigationR. precentral gyrus 64 8 16 4.4R. superior temporal gyrus 52 212 10 4.3R. superior temporal gyrus 62 218 6 4.0R. Heschl gyrus 44 24 8 3.7

Note. Upper part: Conjunction analysis revealing foci of significantNrCBF increases common to mental navigation and mental maptasks as compared to rest. Middle part: Foci of significant differencebetween mental navigation and mental map tasks. *P 5 0.002 un-corrected. Lower part: Foci of significant difference between mentalnavigation and mental map tasks. (See Table 1 legend for details.)

group (respectively, 43.9 6 14.0 and 7.4 6 1.4 s) rein-force the assumption that the two tasks were actuallydifferent and that the subjects used a different perspec-tive in the two tasks.

In each study, a correlation was computed betweenthe time (averaged across subjects) spent to cover thedifferent route segments. This correlation took intoaccount only the route segments for which all subjectsprovided responses (respectively, n 5 5 for the mentalnavigation group, and n 5 9 for the mental map group).

Mental navigation. A positive correlation was evi-denced between time and distance: the longer the dis-tance between two landmarks was, the longer the sub-jects took to mentally cover the route between thelandmarks (Fig. 1A, right; r 5 0.92, P 5 0.025, n 5 5).

Mental map. A positive correlation was also foundbetween time and distance in the mental map group(Fig. 1B, right; r 5 0.91, P 5 0.006, n 5 9).

Note that because the average time spent to coverthe route segments was longer in the mental naviga-tion than in the mental map group, more pairs oflandmarks were delivered to the survey than to theroute group (about 11 for the survey subjects versusthree for mental navigation subjects).

Pet Results

Mental Navigation versus Rest (Table 1; Fig. 2A)

The reanalysis of the present contrast using the MNItemplate revealed activation of the same set of corticalregions previously reported (Ghaem et al., 1997). Note,however, that the coordinates of activation may differfrom this earlier report because the template used forthe spatial normalization was different and the proce-dures used to compute the present normalization weremore accurate. This can result in a different anatomi-cal localization for some foci. Some other foci are nomore present in the results because they just failed toreach the significance level in the new analysis (L.dorsolateral prefrontal cortex, Z score 5 2.9, and L.middle occipital gyrus, Z score 5 3.0).

An activation of the left intraparietal sulcus ex-tended medially to the left precuneus. Within the me-dial part of the occipital lobe, an activation of occipi-toparietal sulcus was bilaterally detected extendingforward to the right posterior cingulate cortex. Themedian frontal region corresponding to the pre-SMAwas also activated as well as the bilateral superiorfrontal sulcus near the intersection with the precentralsulcus. An activation located in the right middle frontalgyrus was also detected.

A bilateral activation was detected in the medialpart of the temporal lobe (Fig. 2A). On the right side, itwas located in the depth of the posterior collateralsulcus, at a level that corresponds to the limit betweenentorhinal and parahippocampal cortex (Bohbot et al.,


1998). On the left side, the activation was in a moreposterior location and corresponds to the parahip-pocampal cortex. A slight CBF increase occurred in theright hippocampus that did not reach significance be-cause of a strong interindividual variability.

Mental Map versus Rest (Table 1; Fig. 2B)

The intraparietal sulcus was bilaterally activated,the activation extending medially to the precuneus. Inthe frontal lobe, a median frontal region anterior to theVAC plane was significantly activated and corre-sponded to the anterior part of supplementary motorarea (pre-SMA). The superior frontal sulcus presenteda bilateral activation located at the intersection withthe precentral sulcus. An activation was also detectedin the right middle frontal gyrus.

The superior temporal cortex was activated bilater-ally in the vicinity of Heschl’s gyrus and extended inthe right hemisphere within the superior temporal sul-cus and the right supramarginal gyrus.

At a subcortical level, the lenticular nucleus pre-sented a bilateral CBF increase extending to the ante-rior insula on the left side.

During mental map, the right medial temporal pre-sented an activation that just failed to reach the 0.001

FIG. 1. Left: Environment learned by both mental navigation aperformed from an actual navigation within the environment includiphone box; Ch, chalet; S, statue). In the mental map group learning wNote that the environment to be learned was the same in both groulandmarks. Right: (A) Linear regression analysis between mental nanalysis between mental map exploration duration and route segmenresponse times and segment lengths for the segments to which all s

threshold of significance (P 5 0.002) while the leftmedial temporal lobe was clearly not activated. Thisright sided activation was located in the hippocampus,within the uncal sulcus (Fig. 2B). Note that, as shownon the histograms (Fig. 2B), the CBF slightly increasedin this region during mental navigation.

Conjunction of Mental Navigation and Mental Map(Table 2, Fig. 2C)

This analysis revealed the regions which presented asimilar activation in both mental navigation and men-tal map tasks. At the parietal level, it included bilat-erally the intraparietal sulcus and the precuneus. Inthe frontal lobe, common activations were observed inthe pre-SMA and in the superior frontal sulcus at theintersection with the precentral sulcus.

Additional common activation was detected in theright middle frontal gyrus and bilaterally in the lentic-ular nucleus extending leftward to the anterior insula.

Finally, the temporal cortex presented an activationlocated in the superior temporal gyrus on the left sideand in the middle temporal gyrus on the right side.

In the medial part of the temporal lobe, an activationwas detected that straddled the right hippocampus andthe adjacent enthorhinal cortex.

mental map groups. In the mental navigation group learning wasctual landmarks (T, tower; G, gas station; Po, portal; Cu, cubes; Ph,

performed with a map of this environment and included colored dots.and that the dot locations were the same as locations of the actualigation duration and route segments length. (B) Linear regressionlength. In each group the regression was computed between averageects provided a response.

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Mental Navigation versus Mental Map (Table 2)

This contrast revealed an activation in the occipito-parietal sulcus at the border of the medial part of theoccipital lobe (cuneus) and the medial part of the pari-etal lobe (precuneus). An activation in the middle oc-cipital gyrus was also detected in the direct compari-son.

Left-sided CBF differences were also observed inthe inferior frontal gyrus (pars triangularis) and inhe posterior cingulate cortex. In the medial tempo-al lobe, the left parahippocampal cortex presented aignificant activation while a trend toward signifi-ance was present in the right homologous area (P 5

0.004).

FIG. 2. (A) Middle: Statistical parametric map (SPM) revealingmentally explore the environment previously learned by actual navparahippocampus corresponding to the two contrasts described aboduring the mental navigation task. (B) Left: SPM revealing the activthe map previously learned. The volume was thresholded at P , 0.0iew of the MNI template. Right: Adjusted CBF difference in the hipest; MN, mental navigation versus rest. (C) Left SPM revealing theap tasks (conjunction analysis). Right: Adjusted CBF differences i

bove. H, hippocampus; EC, entorhinal cortex; cs, collateral sulcus;

Mental Map versus Mental Navigation (Table 2)

This comparison showed that mental map inducedgreater right-sided CBF increase in the inferior part ofthe precentral sulcus and the superior temporal gyrusincluding Heschl’s gyrus. This latter activation is likelyto reflect that, as mentioned above, the frequency ofauditory stimulation was more important in the men-tal map group than in the mental navigation group.

No activation of the right hippocampus was evi-denced when contrasting mental navigation and men-tal map. This suggests, together with its activation inthe conjunction analysis, that the right hippocampusplays a role in both mental navigation and mental maptasks.

bilateral activation clusters in the parahippocampus when subjectstion. Left and right: Adjusted CBF differences in the left and right. This illustrates the specificity of the parahippocampal activationn cluster in the right hippocampus when subjects mentally explored(not corrected for multiple comparisons) and projected on a coronalampus corresponding to the two contrasts: MM, mental map versust hippocampal area activated in both mental navigation and mental

he right hippocampus corresponding to the two contrasts describedinferior temporal sulcus.

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DISCUSSION

The main purpose of the present study was to evi-dence the neural structures engaged in the utilizationof a topographic representation that has been builtfrom two different sources, actual navigation and map.It has recently been emphasized that acquiring theenvironment knowledge in a given perspective does notwarrant that the subject will use the subsequent men-tal representation in the same perspective (Aguirreand D’Esposito, 1999). Numerous factors such as inter-individual variability may constrain the “route” or“survey” perspective of their representation (Heft,1979; Thorndyke and Hayes-Roth, 1982). Further-more, it has been suggested that a representation in aroute perspective may integrate spatial information ofnonvisible parts of the environment (Thorndyke andHayes-Roth, 1982). Moreover, the differences evi-denced in the neural structure involved in the mentalnavigation and in the mental map tasks does not nec-essarily imply that the final representation was in adifferent perspective, but may reflect that the compu-tations required to obtain the final representation usedduring the tasks were different. For these reasons, thedifferences in the neural structures engaged in ourmental navigation and mental map tasks could be at-tributed either to the differences of the encoded mate-rial (e.g., 3-D versus 2-D), to the nature of the task(mental navigation in a subject-centered perspectiveversus mental map of a visually reconstructed map) orto both. However, the impossibility to disentanglethese two sources of disparity is not conflicting with thequestion addressed in the present work: Does the waya person has learned an environment have an influenceupon the patterns of activation during the utilization ofthe resulting topographic representation?

In the following sections, we will first discuss boththe behavioral and anatomofunctional similarities ev-idenced between the two tasks, then we will focus onthe anatomofunctional differences existing betweenthese two tasks.

Similarities in Behavioral and Anatomo-FunctionalResults

Both the mental navigation and the mental maptasks required the recall of the spatial positions ofitems (i.e., landmarks, dots), the maintenance of thespatial relationships of the scenes, and the mentaldisplacement from an item to another. The behavioralresults reflected the common features of the two tasks:in both tasks we evidenced a positive correlation be-tween times and distances. Such correlation is gener-ally taken as reflecting the structural isomorphismbetween mental images and the configurations thatthey represent (Kosslyn et al., 1978, see Cocude et al.,1999, and Denis and Kosslyn, 1999, for a review). The

present work shows that this isomorphism is preservedwhether the topographic information has been ac-quired from survey or route perspective. Our findingsstrengthen the assumption that it is a general propertyof spatial mental images.

The similarities observed in the behavioral resultswere also expressed into the detection of a common setof regions similarly activated in both exploration tasks.These regions include the right hippocampus in themedial temporal lobe and a parietofrontal network thatincluded four distinct regions.

1. Right Hippocampus

The right hippocampus was activated whatever themodality of topographic information encoding. The as-sumption that the hippocampus plays a key role inhuman navigation originates from electrophysiologicaland lesions studies in rodents (O’Keefe andDostrovsky, 1971; Morris et al., 1982). It has beenproposed that the hippocampus maintains a cognitivemap, providing a survey representation of the environ-ment (O’Keefe and Nadel, 1978). The situation is lessclear in humans. First, while hippocampal lesions mayresult in topographic disorientation, this trouble is ac-companied by global episodic memory impairment(Vargha-Khadem et al., 1997), which makes the spe-cific role of hippocampus in navigation difficult to as-sess. A recent study has however reported a routelearning impairment in seven subjects with right hip-pocampal lesion and emphasize the role of this regionin spatial memories consolidation (Barrash et al.,2000). On the other hand, parahippocampal lesionsresulted more specifically in topographic disorientationsuggesting that this region also plays a key role inhuman navigation (Habib and Sirigu, 1987; Barrash etal., 2000; Bohbot et al., 1998; Aguirre and D’Esposito,1999). Second, neuroimaging studies have provided di-verging results: some works using either encoding orretrieval navigational tasks reported an activation inthe hippocampus proper (Maguire et al., 1996, 1997,1998b; Gron et al., 2000), while some others did not(Aguirre et al., 1996; Maguire et al., 1998b; Aguirre andD’Esposito, 1997). The hippocampal activation re-ported here indicates that there exists an hippocampalregion which is active during the recall of a topographicrepresentation built from either route or survey infor-mation. If we assume that hippocampus would be theneural substrate of “cognitive maps,” the present hip-pocampal activation could suggest that subjects haveincluded some survey information in the representa-tion initially acquired in a route perspective. This givesa support to the proposition that it may exist an inter-mediate representation between route or surveyknowledge in which people may “look through” obsta-cles (Thorndyke and Hayes-Roth, 1982). This type ofrepresentation emphasizes that once the subjects have

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actually walked in the environment they have acquiredinformation about parts of environment hidden by theobstacles and use a “survey knowledge from a perspec-tive within” (Thorndyke and Hayes-Roth, 1982). Thepresent hippocampal activation could reflect the use ofsuch a “dual” representation.

2. ParietoFrontal Network

A parietofrontal network was activated whicheverthe way the spatial representation had been built andwas thus neither dependent on the complexity of thematerial to learn (i.e., 2-D or 3-D), nor on the perspec-tive in which the topographic information was acquired(here route or survey). This network included the bi-lateral intraparietal sulcus, the bilateral superior fron-tal sulcus, the right middle frontal gyrus and the pre-SMA. We postulate that this set of regions belongs to anetwork specialized in the processing of visuospatialinformation whenever the visual input is no longerpresent as it is the case in our two spatial imagerytasks. This network could reflect the spatial workingmemory processes required to maintain the mentalimage of the map or of the actual environment (Melletet al., 1998).

The first component of the network corresponds tothe intraparietal sulcus. This structure is commonlyinvolved during visuospatial attention (Corbetta et al.,1998), spatial working memory (Smith et al., 1996;

etit et al., 1996), and spatial mental imagery (Mellett al., 1995, 1996, 2000). To our knowledge it has notet been possible with functional imaging to dissociateetween these different components in the intrapari-tal sulcus.The second component is constituted by a bilateral

egion located in the depth of the superior frontal sul-us near its intersection with the precentral sulcus andabeled as Brodmann’s area 6 (BA6) in the Talairachtlas (Talairach and Tournoux, 1988). This region haseen reported activated in spatial working memorytudies (Jonides et al., 1993; Petit et al., 1996) and inpatial mental imagery studies (Kawashima et al.,995; Mellet et al., 1996). Its implication in the present

study nicely fits with the fact that this area seemsspecifically involved in the period during which thevisual input is no longer present and the spatial infor-mation has to be held on-line (Courtney et al., 1998a).Although eye movements were not different from restduring mental map and differed by very small ampli-tude during mental navigation, we wanted to ascertainthat the frontal activation described here was distinctfrom the frontal eye field (FEF). For this purpose, wedisplayed the activations reported in the present con-junction analysis together with those corresponding tothe FEF and evidenced during the execution of self-paced saccades previously reported in a distinct groupof six subjects (Petit et al., 1996). Figure 3 shows that

both patterns of activation were indeed different, thesuperior frontal activation being distinct and anteriorto the FEF activation. This result is in agreement withthose of a previous study which showed that the supe-rior frontal activation elicited by a spatial workingmemory task was distinct and anterior from the onerelated to eye movements (Courtney et al., 1998a,998b).The third component is materialized by a frontal

ctivation located in the right middle frontal gyrusabeled BA 9/46 in the Talairach atlas. This regionppears less specifically spatial than the frontal BA 6.s a matter of fact, both object and spatial workingemory studies reported an activation in this region

for a review see Smith and Jonides, 1997; Courtney etl., 1998b). Although in the present study, it was acti-ated in both mental exploration tasks, spatial by na-ure, further studies are required to characterize itsole and its domain specificity in the frame of workingemory processes.The fourth component common to the two mental

xploration tasks corresponds to the pre-SMA. Thisegion has been functionally distinguished from theMA in that it is involved in complex motor tasks aspposed to the SMA proper located posteriorely andnvolved in simpler motor tasks (Picard and Strick,996). In the present study, the subject had to press autton as soon as the dots or landmarks that termi-ated a segment was reached. It has recently beenroposed that pre-SMA would be tightly linked toorking memory, being involved in the preparation for

electing a motor response based on information heldn-line (Petit et al., 1998).We suggest that this parietofrontal network consti-

tutes the smallest set of regions necessary to deal withspatial representation including spatial working mem-ory and spatial mental imagery. Neuroimaging studieshave consistently reported an activation of this parieto-frontal network during spatial imagery task performedin absence of any visual input (Roland et al., 1987;Mellet et al., 1995, 1996; Kawashima et al., 1995). In amore general perspective, the parietofrontal systemconstitutes a large-scale distributed network that in-cluded a posterior “sensory” pole and an anterior “mo-tor” pole. It has been suggested that this bipolar orga-nization reflects a general frame for storage andretrieval of memories and give rise to the so-called“perception-action cycle” (Fuster, 1997, 1998). Thepresent study provides further support to this view indemonstrating that a similar organization prevails forthe neural substrate of spatial representation.

AnatomoFunctional Differences

The spatial representations the subjects reactivatedin the two tasks differed according to the nature oftheir encoding. In the scanning task, the mental image


included a complete description of the map comprisingthe borders, the paths, and the dots in 2-D. In thenavigation task, the mental image included only localviews, excluding the landmarks that were not visiblefrom the subject point of view. The route perspectivethus required an additional computation to derive theshortest path to reach a given landmark.

1. Medial temporal lobe (MTL) activity in mentalmap and mental navigation. Although the right hip-pocampus was activated whatever the perspective inwhich the topographic information was encoded, differ-ences related to the mode of learning were observedwithin the parahippocampal regions. Given that mostof the studies of navigation reported bilateral activa-

FIG. 3. In red: SPM revealing the activations shared by mentala bilateral parietofrontal network including the intraparietal sulcus,elicited in a distinct group of subject by the execution of self-pacedposterior to the superior frontal area activated in both mental expactivation in the conjunction analysis of both mental exploration taskThe norm of the vector distance between FEF an frontal activation ithe smoothness value and the foci can be considered as distinct. Theactivated in the self-paced saccades only (Petit et al., 1996). The histonavigation (MN), mental map (MM), and self-paced saccades (S).

tion of the parahippocampal gyrus (Aguirre et al., 1996;Maguire et al., 1998b; Aguirre and D’Esposito, 1997), ithas been suggested that in humans, parahippocampalgyrus is crucial for navigation and spatial mapping(Aguirre et al., 1998).

Our results confirm such a claim, but provide a newinsight: MTL regions involved in the mental explora-tion may differ according to the perspective in whichthe environment was encoded. As a matter of fact, ourresults revealed an activation in the bilateral entorhi-nal/parahippocampal cortex when subject mentally ex-plore an environment built from a route perspective,while these regions were not involved when the envi-ronment had been learned in a survey mode. This

igation and mental map compared to rest. This analysis uncoveredsuperior frontal sulcus, and the pre-SMA. In yellow: The activationscades (S) are shown in yellow. Note that the FEF are distinct andation tasks The maximum voxel in the precentral/superior frontalas 38, 24, 52 for the left frontal and 222, 24, 54 for the right frontal.us 17 mm for the right and 24 mm for the left. This distance exceedplementary eye field (SEF) part of the SMA proper was significantlyms represent the adjusted CBF differences observed during mental

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result is compatible with several propositions thathave been made recently regarding the role of parahip-pocampal gyrus in topographical processes. It has beenshown that the parahippocampal gyrus is active in theencoding of an environment when salient landmarkswere present but not when landmarks were lacking(Maguire et al., 1998a). In the present mental explora-tion tasks, real salient landmarks were used to marklimits in the mental navigation while only colored dotslimited the segment to explore during mental map.This also fits with the bilateral parahippocampal acti-vations reported during the mental evocations of sa-lient landmarks (Maguire et al., 1997). In addition, arecent work showed that the parahippocampal cortexis engaged in the passive viewing of local environmentas compared to the passive viewing of objects (Epsteinand Kanwisher, 1998). In the same vein, these regionshad been involved in the retrieval of spatial relation-ships between objects (Owen et al., 1996; Johnsrude etal., 1999). Our results show that the parahippocampalcortex is also active when the environment is onlymentally imaged and suggest that this region is acommon neural substrate for viewing an environmentand dealing with the mental image of this environ-ment.

In summary, our results are compatible with a dis-sociation between the right hippocampus and the bi-lateral parahippocampal gyrus. Right hippocampus in-volvement would be sufficient when the representationincorporates essentially survey information. On theother hand, the bilateral parahippocampal gyruswould be additionally involved when the environmentto mentally explore is a large-scale space, which incor-porates route information and includes “object” land-marks. Note, however, that this result concerned anall-male sample of subjects. As a matter of fact, it hasrecently been emphasized that during navigationmales take advantage of both landmarks and geomet-ric configuration while female mainly rely on landmark(Maguire et al., 1999). Given that one major differencebetween map and actual navigation learning con-cerned the nature of the landmarks the contrast be-tween the navigation and the map group might havebeen different in a mixed gender or all-female sample(Gron et al., 2000).

2. Differences between mental map and mental nav-igation in other regions. The posterior cingulate cor-tex was activated in the mental navigation conditionand not in the mental map task. Interestingly thisregion has been consistently reported in previous neu-roimaging works involving topographical tasks (Agu-irre et al., 1996; Maguire et al., 1997, 1998a; Aguirreand D’Esposito, 1997). It has been suggested that thisregion contributes to the transformation of a routerepresentation to a survey representation (Vogt et al.,1992). As suggested in the introduction, it is likely that

to reach parts of the environment that are not visiblefrom an initial location, subjects have to derive surveyinformation from the route knowledge they acquired.This is not the case for mental map, in which thetopographic representation used includes by naturesurvey knowledge. In this framework, the specificity ofthe posterior cingulate contribution to the mental nav-igation task may reflect the transformation of route tosurvey knowledge required to perform the task.

The median occipitoparietal regions (cuneus andprecuneus) were activated during the mental naviga-tion task and not during the mental map task. Duringthe mental exploration, the subjects generated visualimages that resulted from actual navigation and thusperceived more detailed and realistic than the sche-matic map visualized during mental map. This occipi-toparietal activation could be related to a richer andmore vivid visual imagery activity during mental nav-igation than during mental map. However, this inter-pretation must be moderated because the occipitopari-etal regions evidenced here appeared more medial andinferior than those reported in visuospatial imagery(Mellet et al., 1995, 1996, 2000). Alternately, the occip-itoparietal region reported in the present study is an-atomically interposed between the parietal cortex andthe posterior cingulate and may also contribute to thetransformation of route coordinates into survey coordi-nates.

Conclusion

The present findings demonstrate the contribution ofboth common and distinct regions in the mental explo-ration of an environment learned in either route orsurvey perspective. A parietofrontal network involvedin the general processing of spatial representationswas activated in both mental exploration tasks to-gether with a right hippocampal area that may sub-serve a cognitive map common to both types learning.The additional processes required to elaborate a cogni-tive map from a route knowledge expressed in theactivation of additional regions including bilaterallyparahippocampal gyrus for “object” landmarks process-ing.

ACKNOWLEDGMENTS

The authors are indebted to V. Beaudoin and P. Lochon for theirinvaluable help in tracer production and data acquisition and to F.Crivello for his help in data analysis.

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Neural Correlates of Topographic Mental Exploration: The ... · mental exploration task in an environment learned from actual navigation (mental navigation task). An-other group of