Neuropsychologia 46 (2008) 2524–2531

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Neuropsychologia

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Gender-specific strategy use and neural correlates in a spatialperspective taking task

Stefan Kaisera,∗, Stephan Walthera,b,c, Ernst Nennigc, Klaus Kronmullera,Christoph Mundta, Matthias Weisbroda,d, Christoph Stippichc, Kai Vogeleye

a Department of General Adult Psychiatry, Centre for Psychosocial Medicine, University of Heidelberg, Germanyb Department of General Internal and Psychosomatic Medicine, Centre for Psychosocial Medicine, University of Heidelberg, Germanyc Department of Neuroradiology, University of Heidelberg, Germanyd Department of Psychiatry, SRH Hospital Karlsbad-Langensteinbach, Germany

e Department of Psychiatry, University of Cologne, Germany

a r t i c l e i n f o a b s t r a c t

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ake th, 3PPto beeasedmorbjec

Article history:Received 26 September 2007Received in revised form 7 April 2008Accepted 8 April 2008Available online 25 April 2008

Keywords:Perspective takingSpatial cognitionGenderfMRI

In the context of the preown egocentric viewpointaking paradigm and perferences of neural activityto systematically either t(third-person-perspectiveballs around him that hadrectness scores were decrshowed a trend towards afemale subjects. Female su

jects this performance decline won angle of rotation and error rain contrast to a consistently emgroup, neural activity was incrmotor areas, confirming previovation in the precuneus and thapproach. In a subgroup of madifferences seem to be more prolikely reflects different strategi

1. Introduction

The ability to adopt the viewpoint of someone else is a con-stitutive part of both spatial and social cognition (Vogeley & Fink,2003). However, in the literature the term perspective taking hasbeen used in different ways. First, in the social cognition litera-ture perspective taking has been referred to as process involvedin reasoning about other people’s mental states, also referred toas “theory of mind (ToM)” (Samson, Apperly, Kathirgamanathan,

∗ Corresponding author at: Section of Experimental Psychopathology, Depart-ment of General Adult Psychiatry, Centre for Psychosocial Medicine, University ofHeidelberg, Voss-Strasse 4, 69115 Heidelberg, Germany. Tel.: +49 6221 565412;fax: +49 6221 565477.

E-mail address: stefan kaiser@med.uni-heidelberg.de (S. Kaiser).

0028-3932/$ – see front matter © 2008 Elsevier Ltd. All rights reserved.doi:10.1016/j.neuropsychologia.2008.04.013

tudy spatial perspective taking refers to the ability to translocate one’ssomebody else’s viewpoint in space. We adopted a spatial perspectived a functional magnetic resonance imaging study to assess gender dif-g perspective taking. 24 healthy subjects (12 male/12 female) were askedeir own (first-person-perspective, 1PP) or another person’s perspective

). Presented stimuli consisted of a virtual scenery with an avatar and redcounted, if visible, from 1PP or 3PP. Reaction time was increased and cor-during the cognitively more effortful 3PP condition. Correctness scores

e pronounced decline of performance during 3PP as compared to 1PP ints correctness scores declined by 6.7% from 1PP to 3PP, while in male sub-

as only 2.7%. Debriefings after the experiment, reaction times dependingtes suggest that males are more likely to employ an object-based strategyployed egocentric perspective transformation in females. In the whole

eased in the parieto-occipital, right inferior frontal and supplementaryus studies. With respect to gender, male subjects showed stronger acti-e right inferior frontal gyrus than female subjects in a region-of-interestle subjects whose strategy reports suggest object-based strategies these

nounced. In conclusion, the differential recruitment of brain regions most

es in solving this spatial perspective taking task.© 2008 Elsevier Ltd. All rights reserved.

& Humphreys, 2005). Second, in the literature on spatial cognitionperspective taking defines the translocation of ones own viewpoint,i.e. the imagined translocation of the origin of the egocentric coor-dinate system (Zacks & Michelon, 2005). The overlap in terminologymay be traced back to classical developmental psychology, whichhas shown that spatial perspective transformations and ToM tasksshow interdependent developmental trajectories (Flavell, 1999).The present study focuses on perspective taking in space.

For this approach two levels of description have to be taken intoaccount (Vogeley & Fink, 2003). The first level of description is thephenomenal level, on which the scene is either perceived from athird person perspective (3PP) or first person perspective (1PP). Thesecond level can be referred to as a representational level, on whichdifferent references frames can be separated. In an egocentric refer-ence frame locations are represented in relation to an agent or, morespecifically, certain body parts of the agent. In contrast, allocentric

S. Kaiser et al. / Neuropsycholog

spatial tasks (Voyer et al., 1995). In addition, Kozhevnikov and

Fig. 1. Typical stimuli used in the experiment. Subjects had to count the number ofred balls as visible either from their own perspective (1PP) or the avatar’s perspective(3PP). The two stimuli were selected to represent an easier (upper part) and a moredifficult trial (lower part) in the 3PP condition.

reference frames code object-to-object relationships independentof the observer’s position. Both, perceiving a scene from one’s ownand somebody else’s viewpoint, have in common that the referenceframe is centered on the body axis of the agent (self or other). 3PPrequires the translocation of the origin of the egocentric coordinatesystem from oneself to the other person.

This particular type of spatial perspective taking requiring toadopt a 3PP has been studied by Vogeley et al. (2004). For thispurpose, simple virtual scenes were presented with a virtual char-acter (avatar) and a number of red balls that were only in partvisible for the avatar (see Fig. 1). Balls had to be counted eitherfrom one’s own (1PP) or the avatars viewpoint (3PP) providinga behavioural measure for the perspective taken. During translo-cation to 3PP increased neural activity was found in a network

including predominantly right-sided medial and superior parietaland frontal areas. To our knowledge, there are no other studiesdirectly addressing this type of egocentric perspective transforma-tion, where the origin of the egocentric coordinate system has tobe translocated from oneself to another agent. However, there isan expanding literature on perspective transformations, where thesubject has to imagine one’s personal point of view moving rela-tive to the environment (Creem-Regehr, Neil, & Yeh, 2007; Wraga,Shephard, Church, Inati, & Kosslyn, 2005; Zacks & Michelon, 2005).These studies have demonstrated involvement of dorsal visuospa-tial processing stream and frontal areas, although there was arelatively high variability between studies regarding the specificregions involved as well as lateralisation.

This variability is also reflected in the behavioural literature,which has shown that performance depends crucially on thetask characteristics including the stimulus material, the type ofpresentation and the memory demands (Easton & Sholl, 1995;Huttenlocher & Presson, 1973; Kozhevnikov & Hegarty, 2001; May,2004; Wraga, Thompson, Alpert, & Kosslyn, 2003). Nevertheless,these studies provide an adequate framework to delineate the cog-

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nitive processes that might underly 3PP and 1PP. For clarity wepresent a putative task analysis of our 3PP condition in sequen-tial order, although the exact order can be considered a matter ofdebate. First, in the 3PP condition the avatar has to be representedin an egocentric reference frame. Second, the actual perspectivetransformation has to be performed, which is considered to bethe step limiting task performance in transformation accounts ofperspective taking (Easton & Sholl, 1995). This step involves thecomputation of the difference between one’s own and the avatar’segocentric reference frames and the subsequent updating of theegocentric reference frame. This update results in a shift of onesown imagined position and orientation to the avatar’s position andorientation. Third, one has to make a positional judgment from thisnew perspective. A fourth process has been postulated in interfer-ence accounts of perspective taking, which consider interferencebetween real and imagined perspectives but not the transforma-tions mentioned above to be crucial for task performance (May,2004). The process of resolving interference would require inhibi-tion of 1PP in order to correctly solve the task from 3PP.

It has been a matter of debate, whether this type of task is reallysolved by using a perspective transformation or an alternative strat-egy based on an object-centered reference frame (Aichhorn, Perner,Kronbichler, Staffen, & Ladurner, 2006; Easton & Sholl, 1995). In anattempt to minimize variation in strategy, we explicitly instructedour subjects to imagine viewing the objects from the avatar’s per-spective and debriefed them accordingly.

The main focus of the present paper was to study a potentialeffect of gender on the neural correlates of spatial perspective tak-ing. Performance differences on spatial cognition tasks dependingon gender are a well-known finding (Coluccia & Louse, 2004; Voyer,Voyer, & Bryden, 1995). However, there is no consensus whethergender differences in performance reflect a different biologicalorganization of neural structures subserving spatial cognition, theinfluence of sex hormones on these structures and/or use of differ-ent strategies to solve spatial tasks. Functional brain imaging hasbegun to delineate the underlying neural correlates of these gen-der differences (Gizewski, Krause, Wanke, Forsting, & Senf, 2006;Halari et al., 2006; Hugdahl, Thomsen, & Ersland, 2006; Levin,Mohamed, & Platek, 2005; Weiss et al., 2003). However, all thesefunctional imaging studies have focused on mental rotation as thekey paradigm to study spatial cognition. This is an important lim-itation, because it has clearly been shown that gender differencesin performance depend on the type of spatial task studied andresults from mental rotation tasks cannot be generalized to other

Hegarty (2001) have provided psychometric evidence for the factthat object-based and perspective transformations rely on separa-ble spatial abilities (Kozhevnikov & Hegarty, 2001). This approachfocusing on inter-individual differences has to our knowledge notbeen applied to the study of gender differences in spatial cognition.

The focus on mental rotation can be explained by the obser-vation that gender differences on a behavioural level tend to bemost prominent during this type of task. Some functional imagingstudies on mental rotation have found stronger parietal activationin men and stronger frontal activation in women (Hugdahl et al.,2006; Weiss et al., 2003). These results have been tentatively inter-preted to reflect a more “gestalt”-like perceptual strategy in menand a more “serial” reasoning strategy in women. However, thesefindings are not consistent and the differential use of strategies isstill a matter of debate (Gizewski et al., 2006; Levin et al., 2005).One study has addressed gender differences in ‘egocentric men-tal rotation’ defined as using an imagined movement of a bodypart to solve the task (Seurinck, Vingerhoets, de Lange, & Achten,2004). However, it has been shown that the processes underlyingimagined movement of body parts are different from those in per-

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spective transformations that involve an imagined movement ofthe observer’s viewpoint as it is required in our task (Creem-Regehret al., 2007). To our knowledge, no study has addressed neural cor-relates of spatial perspective transformations in male and femalesubjects in a comparative manner. Therefore, the goal of the presentstudy was to investigate gender-specific differences in a spatialperspective taking paradigm.

2. Methods

2.1. Subjects

Twelve male (age 28.7 ± 6.6 years) and 12 female subjects (age 27.6 ± 4.9 years)were recruited from local university graduate students and employees. Regard-ing their background male and female subjects were working on or had obtaineda degree in similar faculties. These were psychology (three male, four female),medicine (four male, three female), computer science/mathematics (three male,three female) and law (two male, two female). All subjects were right-handed, hadnormal or corrected vision and were free from neurologic and psychiatric disor-ders. The study was conducted in accordance with the Declaration of Helsinki. Thestudy protocol was approved by the local ethics committee of the Medical Faculty ofthe University of Heidelberg and subjects gave written informed consent after theprocedure had been fully explained.

2.2. Task and procedure

The task was an adapted version of the perspective taking task introduced byVogeley et al. (2004). In a 3D visuospatial task a virtual scene with an avatar in aquadrangular room and red objects were positioned around the avatar’s head atconstant distances using the software package 3-DMax (Autodesk, Montreal) (seeFig. 1). Subjects viewed a projection of these stimuli via a head-coil mounted mirrorsystem. In a blocked design participants were either required to count the objectsas seen from their own (1PP) or from the avatar’s perspective (3PP). The appropriatenumber of objects had to be indicated by a button press using right-hand fingers oneto four. The following features of the scenery were varied systematically: the numberof red balls ranged from one to three, the balls were posted randomly around theavatar’s head in steps of 30◦ , the avatar’s position was varied in 45◦ and the positionof the camera was rotated around the avatar in 60◦ steps.

Overall a sequence of 192 unique stimuli was presented to the subject. Each of thestimuli was presented for 3 s. Each experimental block lasted 36 s and contained 12stimuli. Between blocks a fixation cross was presented for 16 s as a baseline conditionand instructions were presented for 8 s thereafter. Instructions were “How manyballs do you see?” for 1PP condition and “How many balls does he see?” for the3PP condition. Four blocks, two for each condition, were presented in four differentruns in randomized order. The whole experiment took approximately 20 min tocomplete. The present paradigm was considerably shortened as compared to theprevious study (Vogeley et al., 2004) by skipping the second factor of “view”. In the

original study the view on the scene was varied in two different steps, namely anaerial view and a ground view. As this factor of camera position did not have anysignificant influence on the distribution of increased neural activity, this factor wasomitted in the present study.

Before the experiment, subjects were instructed by a slide show followed by atraining session consisting of 12 stimuli for each condition that were not includedin the main experiment. During the training session, subjects received feedback ontheir performance and stimuli were repeated after incorrect responses. After thescanning session, subjects were asked whether they had perceived the avatar asrepresenting a human being and whether it was relevant to their approach to thetask that they had to translocate their viewpoint to an avatar and not to some otherlocation in space.

2.3. Behavioural data analysis

Dependent variables were correctness scores (percentage of correct trials) andreaction time. These were entered into a mixed two-way ANOVA with genderas between-subjects factor and condition (3PP vs. 1PP) as within-subjects fac-tor.

In order to further explore the strategies employed for task performance, wecalculated reaction times for each angle of rotation of the avatar in relation to theobserver, separately for male and female groups. In order to assess a possible linearrelationship of reaction time and rotation angle, we calculated nonparametric corre-lations using Spearman’s rho coefficients for each group. In addition, we calculatedthe percentage of egocentric errors in 3PP, i.e. trials where subjects chose the num-ber of balls they could see from their own instead of the avatar’s perspective. Thispercentage of egocentric errors in relation to overall errors was compared betweengroups via nonparametric Mann–Whitney U-test.

ia 46 (2008) 2524–2531

2.4. fMRI acquisition

Images were acquired on a Siemens Trio 3 T scanner at the Department of Neu-roradiology, University of Heidelberg. Functional images covering the whole brainincluding the cerebellum with isotropic voxels were acquired with the followingparameters: 48 slices of 3.1 mm thickness, matrix size 64 × 64 with 3.1 × 3.1 mm in-plane resolution, TR 4000 ms, TE 60 ms, 90◦ flip angle. In addition a high-resolutionsagittal T1-weighted image was acquired with the following parameters: 176 slices,voxel size 1 × 1 × 1 mm, TR 11 ms, TE 4.92 ms, 15◦ flip angle.

2.5. fMRI analysis

Data analysis was performed with SPM2 (FIL, London) implemented in MATLAB7 (Mathworks, Sherborn). Functional images were realigned and coregistered withthe high-resolution T1-weighted image. Both functional and structural images werethen normalized to the MNI template. Functional images were spatially smoothedwith a kernel of 10 mm FWHM. A general linear model with regressors 3PP, 1PP andinstruction represented by boxcar functions convolved with the canonical hemo-dynamic response function (hrf) was fitted to the data. T-contrasts for 3PP vs. 1PPwere computed for each subject. First, a group analysis was performed for the wholegroup of 24 subjects. For this purpose, single subject contrast images were enteredinto a hierarchical model equivalent to a random-effects model allowing for pop-ulation inference (Holmes & Friston, 1998). Statistical threshold was set to p < 0.05familywise error (FWE) corrected.

For comparison between male and female subjects we selected a region ofinterest (ROI) approach to focus on those brain regions that had been identified asresponsible for performance on our task in the current and the previous study usingthe same paradigm (Vogeley et al., 2004). All ROI analyses were performed usingMarsbar software (www.marsbar.sourceforge.net). ROIs were defined as sphereswith 10 mm radius around the following peak voxels. Two ROIs were selected basedindependently on the highest peak activations in the previous study (Vogeley et al.,2004), located in the precuneus (x = 2, y = −60, z = 56), closely corresponding to anactivation site in the group analysis of the actual study (x = 9, y = −61, z = 53), andthe right inferior frontal gyrus (x = 48, y = 12, z = 24) that borders on the right frontalactivation observed in the present study (x = 42, y = 15, z = 19). These ROI definitionsdrawn from the previous study are based on data from male participants only. There-fore, we decided to include the two highest peak activation foci from the presentstudy that were less prominent or absent in the previous study and could be a resultof the inclusion of female participants. These were located in the middle occipitalgyrus (x = 32, y = −76, z = 34) and the supplementary motor area (x = 3, y = 22, z = 40).These ROIs were based on the analysis of the whole sample in the present studyand should therefore not be biased towards greater activation in male subjects. Thesingle subject ROI contrast estimates for the 3PP contrast (3PP > 1PP) were enteredinto a two-sample t-test. Mean percent local signal change was calculated based onthe parameter weights for the respective regressors 3PP and 1PP.

Since it is possible that the there are gender differences in brain areas not coveredby these ROIs, we additionally performed an exploratory whole-brain comparisonbetween groups with a statistical threshold of p < 0.001 (uncorrected) and an extentthreshold of 10 voxels.

3. Results

3.1. Behavioural data

Dependent variables were correctness scores (in %) and meanreaction time (see Table 1). We found a main effect of condi-tion (F(1, 22) = 23.00, p < 0.001) indicating that subjects performedworse in the 3PP than in the 1PP condition, replicating the find-ings of Vogeley et al. (2004). There was no main effect of gender,indicating no significant differences in performance when col-lapsing both conditions. However, there was a trend towards agender × condition interaction (F(1, 22) = 3.36, p < 0.1) with a morepronounced difference between 3PP and 1PP in female than in malesubjects. Numerically, female subjects correctness scores declinedby 6.1% from 1PP to 3PP, while in male subjects the performancedecline was only 2.7%.

For reaction times there was only a main effect of condition (F(1,22) = 34.4, p < 0.001) indicating that subjects reacted faster in the1PP condition than in the 3PP condition. There was no main effectof gender or gender × condition interaction.

Regarding post-scan questions, all subjects stated that theyperceived the avatar as a human being. Furthermore, all femaleparticipants stated that it was relevant to their approach to the

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PP

79.895.9

were detected in the ROIs of right middle occipital gyrus (t = 1.11,p = 0.14) and supplementary motor area (t = 0.9, p = 0.19). Fig. 3shows mean percent local signal change for male and femalesubjects in both conditions. This shows a relative signal increasefor 3PP as opposed to 1PP in both groups. This increase in neuralactivity is significantly more pronounced in male subjects in theprecuneus and right inferior frontal gyrus.

In an exploratory post hoc analysis we split the male group intwo groups based on the subjective strategy reports. This yieldedtwo groups with six subjects each. One group who reported consis-

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Table 1Behavorial data

Male

3PP 1

Reaction time (ms) 1027.8 ± 242.3 8Correctness score (%) 93.2 ± 3.7

task that they had to translocate their viewpoint to an avatar (andnot to some otherwise marked point in space) and that they didnot use any alternative strategy to solve the task. In the male groupsix subjects considered the avatar to be important, while six statedthat they had not paid attention to the fact that the relevant pointin space was an avatar and that they did not imagine themselves inthe avatar’s position.

In order to explore the strategies used during 3PP we calculatedreaction times for each angle of rotation between the avatar in rela-tion to the observer’s viewpoint (see Fig. 2). Inspection of reactiontimes suggest a nearly monotonic increase with increasing angle ofdisparity between head and gaze direction of participants as com-pared to virtual characters in female subjects as confirmed by ahighly significant correlation (Spearman’s R = 0.43, p < 0.01). In malesubjects the pattern was more heterogeneous regarding the vari-ation with angle and larger variation between individuals, whichresulted in a correlation that reached statistically only trend level(Spearman’s R = 0.19, p = 0.07).

In addition, we obtained the percentage of egocentric errors inrelation to overall errors (female 45.5 ± 20.8%, male 29.4 ± 19.0%).Female subjects showed a trend towards a higher proportion ofegocentric errors than male subjects (Mann–Whitney U, z = 1.7,p = 0.08).

3.2. fMRI results for whole group analysis

With respect to the factor condition a whole brain analysiscollapsing both genders was performed to identify the primarilyactivated brain regions during the condition of 3PP. An extendednetwork of brain areas during 3PP (3PP > 1PP) was found compris-ing bilateral middle occipital gyrus, right precuneus, right middleand inferior frontal gyrus, right supplementary motor area andbilateral cerebellum (see Table 2). This network is dominated bya large parieto-occipital cluster and right frontal areas (see Fig. 3).There were no main effects for 1PP at the same statistical threshold(1PP > 3PP).

Fig. 2. Mean 3PP reaction times (in ms) for each angle of rotation between observer’sand avatar’s perspective for female (dark) and male (light) subjects.

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Female

3PP 1PP

± 223.3 1051.6 ± 111.5 978.5 ± 86.9± 2.6 91.2 ± 5.3 97.3 ± 1.7

3.3. fMRI results for comparison between male and femalesubjects

With respect to the factor gender ROI analyses revealed asignificantly increased neural activation as indexed by % signalchange in the precuneus (t = 1.84, p = 0.04) and right inferiorfrontal gyrus (t = 2.14, p = 0.02) for male subjects as comparedto female subjects (see Fig. 4). No significant gender differences

tent translocation to the avatar’s viewpoint (male-egocentric) andone group who did not (male-object). We then compared thesegroups separately with the female group for the right precuneusand right inferior frontal gyrus ROIs. Numerically, both male groupsshowed higher signal change in these ROIs than female subjects.However, only the male-object group showed a significant differ-ence in the right inferior frontal gyrus ROI (t = 2.52, p = 0.01) and atrend-level difference in the right precuneus ROI (t = 1.58, p = 0.06)when compared to female subjects.

In order to assess whether there were gender differences inregions not covered by our ROIs we performed an exploratory

Fig. 3. Whole group SPM {t} map for contrast 3PP vs. 1PP thresholded at p < 0.05familywise error corrected (critical t = 5.93) projected onto a high-resolution T1 dataset of one participant of the study.

cholog

ts, FW

T

14.4713.1613.1012.1710.5010.3010.58.778.568.388.368.027.456.90

2528 S. Kaiser et al. / Neuropsy

Table 2Talaraich coordinates of significant activation foci for contrast 3PP vs. 1PP, all subjec

Region Cluster size

R middle occipital gyrus 5804L middle occipital gyrusR precuneusR middle frontal gyrus 1126R inferior frontal gryrusR precentral gyrusR supplementary motor area 283R cerebellum 40L cerebellum 53L insula 88L superior frontal gyrus 95Cerebellar vermis 104R thalamus 53L precentral gyrus 53

whole brain comparison between male and female subjects, whichrevealed no significant group differences at a threshold of p < 0.001(uncorrected) and 10 voxels extension.

3.4. Correlations between task performance and signal change

In order to elucidate whether the observed results are modu-lated by task performance, we correlated correctness scores andmean percent signal change for each condition and ROI separately.No significant correlations were found.

4. Discussion

The present study focused on the differential neural activationof a simple visuospatial task with respect to the factor gender.In both conditions of 3PP and 1PP an egocentric reference framewas used, but 3PP additionally required the translocation of one’sown perspective to the avatars perspective as reflected in a highererror rate and increased reaction times during the 3PP condition.This result replicates the findings obtained in the previous studyemploying the same paradigm (Vogeley et al., 2004). Regarding

Fig. 4. Mean percent local signal change both groups in both conditions (dark = 3PP, lighfrontal gyrus (x = 4, y = 12, z = 24). (Lower left) Middle occipital gyrus (x = 32, y = −76, z = 34relative activation for the contrast 3PP vs. 1PP was observed in precuneus and right inferi

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E p < 0.05, highest peak in each cluster in bold font

X Y Z

32 −76 34−29 −71 33

9 −61 5336 0 5342 15 1945 4 27

3 22 4026 −31 −31

−12 −49 −38−33 20 −4−21 3 52

3 −25 189 −8 6

−42 4 27

gender differences, female participants showed a trend towardsa more pronounced performance decline in the 3PP condition asopposed to 1PP. This difference in performance is unlikely to bea result of different practice with spatial cognition resulting fromthe subjects’ professional background, because both groups hadbalanced educational backgrounds.

On a neural level, 3PP as opposed to 1PP leads to extensiveactivation in parieto-occipital, frontal and cerebellar areas, pre-dominantly on the right side. The observed activation foci arecomparable to those reported by Vogeley et al. (2004) with anadditional activation focus in the supplementary motor area. Over-all, male and female participants recruited a similar network ofbrain regions for performing the 3PP task. The lack of gender differ-ences in the whole-brain group comparison indicates that male andfemale subjects largely recruit a similar network of brain regionsfor solving this perspective taking task. However, small but signif-icant differences emerged in the ROI analysis based on the peakcoordinates of our previous study (Vogeley et al., 2004). Male sub-jects showed higher signal change in the precuneus and the rightinferior prefrontal cortex. This effect is unlikely to result froma larger activation in all brain regions in male subjects, because

t = 1PP). (Upper left) Precuneus (x = 2, y = −60, z = 56). (Upper right) Right inferior). (Lower right) Supplementary motor area (x = 3, y = 22, z = 40). Significantly higheror frontal gyrus in males.

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S. Kaiser et al. / Neuropsy

the other regions did not show larger activation in male subjects.There were no brain regions with higher signal change in femaleparticipants.

4.1. Behavioural data and task strategies

These significant differences between genders in performanceand neural activation can relate either to different strategiesemployed or alternatively to differential allocation of effort andrecruitment of cognitive control processes. As mentioned in theintroduction, the task was designed as an egocentric perspectivetransformation with according instructions. However, it is possibleto use an alternative strategy based on an object-centered refer-ence frame (Aichhorn et al., 2006; Easton & Sholl, 1995). Whilewe explicitly instructed our subjects to imagine themselves in theposition of the avatar, it is still possible that some subjects haveused such an alternative object-based strategy. In an attempt tominimize variation in strategy, we explicitly instructed our sub-jects to imagine viewing the objects from the avatar’s perspectiveand debriefed them accordingly. All female subjects and half of themale subjects in the study reported that they had used an egocen-tric strategy according to the instructions. In contrast, half of ourmale subjects reported that it was irrelevant for their approach tothe task that the avatar represented a human agent and that theydid not imagine themselves in the position of the avatar. This raisesthe question whether male subjects tended to use an object-basedreference frame during 3PP. This would involve a different (but notmutually exclusive) set of cognitive processes. The first cognitiveprocess would involve a coding of object-to-object relationshipsbetween the avatar (and its facing direction) and the balls in anallocentric reference frame. In a second step it would have to bedetermined whether the ball lies within a prespecified angle of theavatar’s facing direction. Here, the encoding and positional judg-ments might be more complex than in the egocentric strategy, butit is important to note that this strategy does not involve a rota-tion operation. Therefore, with this type of strategy one would notexpect an increase in reaction time with increasing angle of gazedirection disparity between subject and avatar.

Indeed, further analyses of the behavioural data provide addi-tional evidence for a differential strategy use between genders. Inour study we observed a nearly monotonic increase of reactiontime with increasing angle of gaze direction disparity betweenparticipants and virtual characters in female subjects. Previousstudies have shown that error rates and reaction times increase

with increasing angle of rotation in perspective transformationtasks (May, 2004). This has been observed to a lesser extent, whenconflict between real and imagined perspective was reduced, aswould be expected in our study without bodily presence and witha numerical response (Wraga et al., 2003). Nevertheless, most stud-ies of egocentric perspective transformations with presentationand response requirements comparable to our study have reportedan increase in reaction time at least up to 180◦ although with arelatively flat curve (Creem-Regehr et al., 2007; Zacks, Vettel, &Michelon, 2003). Therefore, our findings support the hypothesisof a consistent use of an egocentric strategy in female subjects. Incontrast, male subjects showed a more heterogeneous pattern withan initial increase of reaction time up to 60◦ disparity, but no fur-ther monotonic increase. This pattern in conjunction with a highinter-individual variability suggests that male subjects did not con-sistently employ an egocentric strategy or tried to employ differentstrategies.

In our study the analysis of errors was limited by the low overallerror rate. This, however, is a general methodological requirementin blocked fMRI studies to assure that participants have reallyreached their cognitive target state. This precluded analysis of

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errors depending on the degree of gaze disparity. However, femalesubjects showed a general trend towards a higher proportion ofegocentric errors. These were defined as counting the balls fromone’s own, but not the avatar’s perspective summarized over all3PP trials. This is in line with previous findings that children’s andto lesser extent adults’ errors on perspective tasks are not randombut “egocentric” errors (Huttenlocher & Presson, 1973; May, 2004).This would imply that suppression of 1PP is required in order torespond correctly in the 3PP condition. This finding has to be inter-preted with caution, because in our task using a numeric responseit is difficult to reliably differentiate true egocentric errors (withfailure of inhibiting 1PP) from other error types. Nevertheless, inconjunction the analysis of reaction times depending on angle andthe egocentric errors support the use of an egocentric perspec-tive transformation in female subjects and more heterogeneousstrategies including an alternative object-based approach in malesubjects.

4.2. Differential activation in right precuneus

Gender differences in brain activation were observed in the rightprecuneus, which was part of a large parieto-occipital cluster ofincreased neural activity during 3PP vs. 1PP. In our previous studythis region showed the largest signal change in the 3PP vs. 1PP con-trast in a group consisting of male subjects only. In the present studymale subjects showed higher signal change in the right precuneusthan female subjects.

The interpretation of precuneus activation is complicated by thefact that it has a key role in the spatial coding both in egocentric(Galati et al., 2000; Zaehle et al., 2007) and allocentric coordi-nate systems (Frings et al., 2006). Coding of spatial informationin an egocentric coordinate system has led to activation in left orbilateral precuneus (Schmidt et al., 2007; Zaehle et al., 2007). Therecent study by Zaehle et al. nicely demonstrated left precuneusactivation in the egocentric condition of an imagery task basedon verbal descriptions. Their task did not include visual stimula-tion or spatial transformations and thus provided strong evidencefor left precuneus involvement in egocentric coding even withouttransformation requirements. Previous studies addressing spatialtransformations in addition to encoding reported a left-sided domi-nance for perspective transformations and a right-sided dominancefor object-based transformations in superior parietal regions (Zacks& Michelon, 2005). One exception is the study by Creem-Regehr etal. (2007), who have reported right-sided dominance of precuneus

activation in a perspective transformation, when extrinsic codingof objects relative to oneself after an imagined body transforma-tion was required. Similarly our 3PP condition did not require animagined body transformation, but a judgement about the posi-tions of objects after an imagined perspective transformation. Insum, both the studies by Creem-Regehr et al. (2007) and our ownstudy differ from most other perspective transformation tasks inthe neuroimaging literature in that an object-relative decision incontrast to a body-relative decision was required.

Based on the subjects’ strategy reports and the behaviouraldata, we considered the possibility that the larger right precuneusactivation in male subjects was related to a stronger use of object-based strategies in this group. The higher right precuneus signalchange in male subjects reporting not to have consistently takenthe avatar’s perspective might support this interpretation, becausea right-hemispheric dominance has repeatedly been reported forobject-based tasks (Zacks & Michelon, 2005; Zacks et al., 2003).In a direct comparison between perspective and object-based spa-tial transformations, Zacks and coworkers have reported relativelylarger right-sided activation in this brain region during the lattertype of task (Zacks, Rypma, Gabrieli, Tversky, & Glover, 1999). How-

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ever, object-based rotation tasks do not only involve the precuneus,but also more laterally located superior parietal areas.

The comparison with studies on object-based transformationsdoes not allow us to conclusively clarify whether the observeddifferences relate to the object-based encoding or the spatial judge-ments performed upon this information. Allocentric encoding hasbeen reported to lead to bilateral activation in the precuneus (Fringset al., 2006). However, it is likely that the second step of theobject-based strategy has also contributed to the observed gen-der differences. When objects are directly coded in relation to theavatar, a spatial transformation in the sense of translocation or rota-tion is not necessarily needed. Instead, when all objects are codedin an object-based reference frame, the task can at least partiallybe solved as a complex allocentric positional judgment task. Lesscomplex allocentric positional judgment tasks have been shownto recruit primarily right parietal areas including the precuneus,although there is some overlap with brain areas recruited whenperforming egocentric judgments (Galati et al., 2000).

4.3. Differential activation in right inferior frontal gyrus

Another important focus of activation, which showed gen-der differences, was located in the right middle and inferiorfrontal gyrus. This brain region could be related either to the spa-tial operations described in our provisional task analysis or togreater involvement of general cognitive control processes such asresponse inhibition or working memory.

It is interesting to note that this brain region has not been shownto be activated in other studies on egocentric perspective transfor-mation. If any, activation was observed in the left middle frontalgyrus and was more strongly related to the rotation of body parts(Creem-Regehr et al., 2007) or rotation around one’s own bodyaxis (Creem et al., 2001). In contrast, bilateral activation of middleand inferior frontal gyrus has often been reported in mental rota-tion tasks requiring an object-based transformation (Cohen et al.,1996). The finding of higher signal change in men than in womencould support the assumption that men are more likely to use anobject-based strategy in the present task.

The larger right frontal activation in men might seem at oddswith studies on mental rotation tasks reporting the opposite pat-tern of increased activation in female subjects (Hugdahl et al., 2006;Weiss et al., 2003). However, it has to be noted that this finding isnot consistent (Gizewski et al., 2006; Levin et al., 2005). In addition,all the studies showed an increased right frontal activation for the

rotation compared to the control condition for both genders, i.e.frontal activation was related to performance of an object-basedtask. Therefore, in our study a larger proportion of male subjectsusing an object-based strategy might well lead to the observed pat-tern. This interpretation also receives some support by our post hocanalysis, which showed a higher right prefrontal signal change inmale subject’s reporting not to have consistently taken the avatar’sperspective.

However, alternative explanations relating to cognitive controlprocesses should also be considered. Right prefrontal areas haveconsistently been shown to be involved in inhibition of motor andcognitive processes and have been implicated in suppression of1PP in false-belief tasks (Aron, Robbins, & Poldrack, 2004; Samsonet al., 2005). However, if inhibitory control would account forthe differences between genders, one would expect higher pre-frontal activation with a consistent egocentric strategy, i.e. in thefemale group. In our study increased right prefrontal activation wasobserved in the male group suggesting that it is not related to asuppression of the self-perspective. Behavioural studies have sug-gested that the amount of interference depends on the exact taskspecifications, e.g. bodily presence or response mode (May, 2004).

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In our study the setup as a projected presentation and numericinstead of actual pointing response might limit the amount of inter-ference. Taken together, it seems unlikely that the increased rightprefrontal activation in male subjects is due to higher recruitmentof brain regions subserving inhibitory and interference control.

Alternatively, right prefrontal activation has been suggested toreflect the working memory component of spatial tasks (Suchan,Botko, Gizewski, Forsting, & Daum, 2006). Thus, the higher activa-tion of right prefrontal areas in male subjects might reflect a higheramount of effort and a stronger recruitment of brain areas subserv-ing working memory. However, the reaction time and error patternsin conjunction with increased right precuneus and prefrontal acti-vation are most parsimoniously explained by the use of differentstrategies to solve the task. It has to be kept in mind that a differen-tial strategy use and a higher amount of effort by the male subjectsare not mutually exclusive.

4.4. Common activation in middle occipital cortex andsupplementary motor area

The peak activation in the present study was located in the rightmiddle occipital gyrus with concomitant activation in the left hemi-sphere and did not reveal any gender differences. In the literatureon mental rotation tasks it has been an open question whether acti-vation in dorsal extra striate areas reflects perception/encoding ofthe stimulus or the subsequent spatial transformations. The firstalternative has received some support by the observation that theseareas are most consistently activated when a rotation task is com-pared either with a baseline or a rotation task with less complexvisual stimulation (Jordan, Heinze, Lutz, Kanowski, & Jancke, 2001;Vingerhoets, de Lange, Vandemaele, Deblaere, & Achten, 2002). Arecent study employing event-related fMRI has provided evidencefavouring the perception/encoding alternative (Ecker, Brammer,David, & Williams, 2006). In the context of our provisional taskanalysis, the middle occipital cortex is most likely to be involved inthe first required cognitive operation, namely the representation ofthe avatar in an egocentric reference frame. When comparing 3PPand 1PP it has to be kept in mind, that both conditions use the sametype of stimulus material. However, in the 1PP condition the avataris irrelevant for solving the task and therefore does not need to beconsidered.

In the literature on egocentric perspective transformations,activation of middle occipital cortex has not been consistentlydescribed (Zacks & Michelon, 2005). Activity in middle occip-

ital gyrus was observed more laterally in proximity to theparieto-temporo-occipital junction in areas involved in visualmotion perception (Wraga et al., 2005; Zacks et al., 2003). How-ever, in a recent study Creem-Regehr et al. (2007) investigatedtwo different types of egocentric transformations, body-part andbody-perspective transformations. Both types of egocentric trans-formations led to strong activity in middle occipital cortex in closeproximity to the areas observed in our study. These results are inconcordance with the assumption that middle occipital cortex acti-vation mainly reflects the encoding component of our perspectivetransformation task.

Activation of the supplementary motor area (SMA) was observedmore strongly in the recent study as compared to the original studyby Vogeley et al. (2004). This difference between studies couldresult from the inclusion of female participants. However, therewere no significant gender differences in this region. Another pos-sible explanation is the improved signal-to-noise ratio when usinga 3 T scanner as compared to 1.5 T. Activation of SMA has commonlybeen observed in mental rotation tasks, although it was not clearwhether SMA relates to the actual spatial transformation or someother feature required for task performance, such as the mere rep-

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resentation of complex three-dimensional shapes. One study hasprovided evidence that SMA plays a role in object-based transfor-mations (Johnston, Leek, Atherton, Thacker, & Jackson, 2004). It hasto be kept in mind that this does not necessarily imply a motorstrategy, since SMA activation has been observed in a variety ofcomplex cognitive tasks (Picard & Strick, 2001). In a recent studyWraga et al. have compared self and object rotations (Wraga et al.,2005). SMA activity was observed when comparing self vs. objectrotations. However, no SMA activation was found in the comparisonbetween self-rotations and a high-level control condition requiringa visibility judgment without rotation. The authors speculated thatself-rotation and control conditions involved encoding of the stim-ulus with respect to egocentric coordinates. With respect to ourstudy, the SMA activation found in the present study can relate tothe encoding of the stimuli in relation to the observer as well as tothe cognitive processes involved in the actual perspective transfor-mation, i.e. calculating the difference between the two referenceframes and updating of the egocentric reference frames.

5. Conclusion

Male and female participants recruit a similar network of brainregions including parieto-occipital, right frontal and supplemen-tary motor areas when solving a simple spatial perspective takingtask from somebody else’s (3PP) or one’s own viewpoint in space(1PP). Despite these similarities, male subjects show higher acti-vation in the precuneus and right inferior frontal gyrus. Althoughgender differences are relatively small, the present results indicatethat gender differences in spatial cognition are not limited to men-tal rotation tasks studied previously through functional imaging.Based on the subjects’ strategy reports and the behavioural data,the most parsimonious explanation for the observed gender differ-ences is a differential use of strategies. Women seem to perform thetask more consistently as an egocentric perspective transformation,while male subjects also employ object-based strategies that acti-vate right precuneus and right inferior frontal gyrus more strongly.

Further studies on gender differences in perspective transforma-tions should separate the cognitive processes involved in moredetail to delineate gender-specific strategy use.

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