Neuropsychologia 44 (2006) 1575–1583

Sex differences in visuo-spatial processing:An fMRI study of mental rotation

Kenneth Hugdahl a,∗, Tormod Thomsen b, Lars Ersland c

a Department of Biological and Medical Psychology, University of Bergen, and National Competence Center for Functional MR,Haukeland University Hospital, Bergen, Norway

b NordicNeuroLab Inc., Bergen, Norwayc Department of Clinical Engineering, Haukeland University Hospital, Bergen, Norway

Available online 6 May 2006

Abstract

Following the theoretical framework of coordinate and categorical principals for visuo-spatial processing, originally formulated by [Kosslyn,S. M. (1987). Seeing and imagining in the cerebral hemispheres: AQ computational approach. Psychological Review, 94, 148–175], we presentdata from an fMRI study on mental rotation, using the classic [Shepard, R. N., & Metzler, J. (1971). Mental rotation of three-dimensional objects.Science, 171, 701–703] task, comparing males and females. Subjects were presented with black-and-white drawings of 3-D shapes taken fromt1atHaic©

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he set of 3-D perspective drawings developed by [Shepard, R. N., & Metzler, J. (1971). Mental rotation of three-dimensional objects. Science,71, 701–703], alternated with 2-D white bars as control stimuli. The drawings were presented pairwise, as black and white drawings againstblack circular background. On half of the trials, the two 3-D shapes were congruent but portrayed with different orientation, in the other half

he two shapes were incongruent. Analysis of response accuracy and reaction times did not reveal any significant differences between the sexes.owever, clusters of significant neuronal activation were found in the superior parietal lobule (BA 7), more intensely over the right hemisphere,

nd bilaterally in the inferior frontal gyrus (BA 44/45). Males showed predominantly parietal activation, while the females, in addition, showednferior frontal activation. We suggest that males may be biased towards a coordinate processing approach, and females biased towards a serial,ategorical processing approach.

2006 Elsevier Ltd. All rights reserved.

eywords: fMRI; Mental rotation; Sex differences; Hemispheric asymmetry

. Introduction

1In the Shepard and Metzler mental rotation task, subjectsre shown pairs of perspective drawing of 3-D regular shapes.he task of the subject on each trial is to decide whether the twohapes are identical, or if one is a mirror-image of the other (seelso Cooper, 1976; Kosslyn, 1980). The typical finding is thatesponse times increase as the angle of disparity between the twohapes increases, with requirements for cognitive processing inrder to determine if they are the same shape or not. A com-on explanation of these findings is that an image of the shape

as to be mentally “rotated” to be superimposed on the refer-nce shape in order for the subject to decide whether the shapes

∗ Corresponding author. Tel.: +47 55 586277; fax: +47 55 589874.E-mail address: hugdahl@psych.uib.no (K. Hugdahl).

1 Parts of the data have previously been published in Thomsen et al. (2000). Weave however re-analyzed and re-interpreted the findings in light of the theoryf Kosslyn (1987).

are identical or not (Shepard & Cooper, 1982; Tagaris et al.,1997).

Based on behavioral responses (response accuracy) severalstudies have found males to perform better than females (e.g.Astur, Tropp, Sava, Constable, & Marcus, 2004; Crucian &Berenbaum, 1998; Fisher & Pellegrino, 1988; Parsons et al.,2004; Peters et al., 1995). This has been explained with refer-ence to differences between the sexes in hemisphere functioning,with males performing better than females on typical right hemi-sphere processing tasks (e.g. Levy & Reid, 1978). However,not all studies have found sex differences in mental rotation.Cohen and Polich (1989) found no differences between malesand females for mental rotations involving letter and polygons,i.e. different tasks than the Shepard and Metzler 3-D task.

Hooven, Chabris, Ellison, and Kosslyn (2004) measured sali-vary testosterone in 27 young males on a 2-day testing schedule.The results showed that increased testosterone levels had a neg-ative effect on reaction time and error rate on the mental rotationtask. The importance of the Hooven et al. (2004) study is that it

028-3932/$ – see front matter © 2006 Elsevier Ltd. All rights reserved.oi:10.1016/j.neuropsychologia.2006.01.026

1576 K. Hugdahl et al. / Neuropsychologia 44 (2006) 1575–1583

identifies a biological marker for the typical male superior per-formance on mental rotation tasks. Similarly, Aleman, Bronk,Kessels, Koppeschaar, and van Honk (2004) found that a singleadministration of testosterone improved performance in youngwomen on a mental rotation task.

The objective of the present study was to further investi-gate sex differences in mental rotation by means of mappingthe crucial neuronal mechanisms involved. Few studies of brainactivation during mental rotation thus far have systematicallyevaluated differences between males and females. A clear major-ity of published studies on brain activation to mental rotationtasks have not separated their findings for males and females(e.g. Belin, Moroni, Gelbert, Cordoliani, & Delaporte, 1998;Cohen et al., 1996; Tagaris et al., 1997, 1998; Watson et al.,1998), or only one sex has been included in the study (e.g.Jancke et al., 1998; Richter, Ugurbil, Georgopoulos, & Kim,1997; Taira, Kawashima, Inoue, & Fukuda, 1998). The firststudy that reported separate results for males and females wasthe study by Tagaris et al. (1996). In two more recent studies,Weiss et al. (2003) and Jordan, Wustenberg, Heinze, Peters, andJancke (2003), it was found that males had increased activationin the inferior parietal lobule compared to females, while femalesshowed increased activations in frontal lobe and fusiform areas.Finally, Seurinck, Vingerhoets, de Lange, and Achten (2004),using rotated hands, found that females recruited left ventralpremotor cortex. A left hemisphere effect in females was alsooor

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Fig. 1. Examples of the 3-D experimental stimuli (far left figure), and 2-D controlstimuli (middle and far right figures).

be expected to be mainly accomplished by using coordinate,metric, representations, in a continuum of space where two spa-tial forms can transform into one another through intermediateorders of points. A possible solution to the paradox could bethat mental rotation cannot be seen as a simple (one mechanism)process and it is in fact likely to be carried out by a system ofoperations working together. Particularly, comparing views of amultipart object (like the Shepard and Metzler’s cubes) mightrequire at the outset also a multipart object’s structural descrip-tion (i.e., representing the individual parts and their relations).In other words, although the mechanics of the rotation (the con-tinuous transformation) might well be taking place in the righthemisphere, verbalizations or the use of verbal strategies mayrequire the cooperation of the left hemisphere. Although theShepard and Metzler cubes may not lend themselves too easilyto verbal labels, or descriptions, it cannot be ruled out that a sub-ject may apply some verbal labels to parts when processing thestimuli (e.g., one could label parts of the cubes shown in Fig. 1as ‘the bottom, nearest arm’ and ‘the top, left-pointing arm’).This would explain why neuronal activations (in fMRI and PETstudies) during rotation tasks are typically bilateral and why aleft hemisphere lesion might compromise – in some cases morethan a right hemisphere lesion – the mental rotation task.

Thus, although bilateral activations typically are found inbrain imaging studies (PET and fMRI), almost all studies havealso reported the right parietal lobule as involved in mental rota-tBe1itifac(isdAittasf

bserved by Alexander, Packard, and Peterson (2002) for mem-ry of the locations of objects briefly presented in the left oright visual half-field.

Mental rotation paradigms are particularly suitable for study-ng visuo-spatial processing strategies in the right and left cere-ral hemispheres. Mental rotation of abstract 3D objects areard to verbalize, and would thus present as pure spatial tasks.ental rotation tasks may also be conceptualized in the Kosslyn

1987) theoretical framework of categorical and coordinate met-ic space, pointing towards a right hemisphere processing supe-iority for such tasks. This is also what has been found. Forxample, Ditunno and Mann (1990) reported faster reactionimes when the shapes were presented in the left visual field.

Similar results were reported by Corballis and Sergent (1988)hen testing a patient with a surgical split of the corpus callo-

um, thus separating the right and left hemispheres. A moreecent study by Harris, Harris, and Caine (2002) reported thatatients with damage to the right basal ganglia showed signifi-ant performance deficits on a mental rotation task. Howeverther studies on patients with unilateral, left or right hemi-phere lesions (e.g. Kosslyn, Holtzman, Farah, & Gazzaniga,985) have found impaired performance particularly for left-emisphere damaged patients, indicating a left hemisphere basisor mental rotation (cfr. Kosslyn & Brown, 1995). Thus, thereeem to be some contradictory points in the literature that begor explanation. On one hand, Kosslyn’s original theory positshat categorical representations are abstract and qualitatively dis-oint; therefore they cannot be used to describe the continuousigid transformations of parts and spatial rotations. In con-rast, continuous rigid transformations can easily be describedithin a coordinate framework. Hence, mental rotation would

ion, suggesting a right hemisphere processing dominance (e.g.elin et al., 1998; Cohen et al., 1996). Other studies have, how-ver, reported bilateral parietal lobule activation (Tagaris et al.,996, 1997, although these authors used a different task), ornconsistent laterality across subjects (Cohen et al., 1996). Thus,he issue of hemispheric asymmetry in brain activation stud-es of mental rotation is unresolved yet. Part of the explanationor the variability across studies and subjects in hemisphericsymmetry for mental rotation may be the kind of baseline orontrol stimulus used. Both Cohen et al. (1996) and Richter et al.1997) used the same Shepard and Metzler (1971) shapes dur-ng the experimental (mental rotation) and control conditions,ubtracting fMRI images between the two conditions. Howeveruring the control condition, only non-rotated shapes were used.lthough this controls for the effect of visual perception, it may

nduce “carry-over” processing effects from the experimental tohe control stimulus condition, with the subject trying to men-ally rotate also the control stimuli, since they are similar in shapend outline as the experimental stimuli. Therefore, in the presenttudy we used different control shapes in order to optimize dif-erences in mental rotation demands between the experimental

K. Hugdahl et al. / Neuropsychologia 44 (2006) 1575–1583 1577

and control conditions, while controlling for overall visual per-ception and for motor responses. The study of sex differencesin neuronal activation in a mental rotation task is relevant alsofrom the point of view that this has not been the topic in studieson categorical/coordinate processing.

2. Methods

Eleven right-handed healthy adults participated in an fMRI study, six malesand five females (mean age 30 years, range ±10 years). Right-handedness waschecked with the help of the questionnaire developed by Raczkowski, Kalat, andNebes (1974) which consist of 14 questions related to the use of the hands andone question related to the use of the feet. All subjects participated voluntarilyand gave their consent for participation before entering the MR scanner.

The subjects were presented with black-and-white drawings of 3-D shapestaken from the set of 3-D perspective drawings developed by Shepard andMetzler (1971) (see Fig. 1).

In the experimental condition, the subjects were shown 36 pairs of 3-Ddrawings, presented in three blocks of 12 pairs of drawings. The drawings werealways presented pairwise, with one shape rotated along its vertical axis relativeto the other shape. On half of the trials, the two drawings were of the same shape,in the other half of the trials the drawings were of two different “isomeric”shapes. The set of 36 stimulus pairs were selected from the larger set of fivedifferent shapes in seven different rotations (from 0◦ to short of 360◦) taken fromthe Shepard and Metzler (1971) set. The present set of 36 pairs was randomlyselected from the larger set, with the restriction that all five shapes and all sevenrotations should be represented.

During the control conditions, which alternated between the experimentalconditions, the subject saw two 2-D white bars against the same black back-ghpIttteHl

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trial. This was done to have about the same number of right- and left-hand buttonpresses in both the experimental and control conditions.

Before the experiment, the stimulus presentation goggles were adjusted sothat the subject could easily view the stimuli. An audio headset (ResonanceTechnology Inc.) was also fit to the head of the subject, inside the MR headcoil. The headset attenuated some of the background noise and provided forthe MR-machine operator to communicate with the subject. The onset of MR-image acquisition and stimulus presentations were manually synchronized bythe radiographer who operated the MR scanner.

Upon entering the MR-section of the Radiology Department, the purpose ofthe study and the general procedure was explained to the subject. After position-ing the subject in the MR machine, a test stimulus was displayed in the goggles sothat they could be individually adjusted for each subject. The head coil was thenclosed and the subject’s head was positioned in the center of the magnetic field.Before entering the magnet, all subjects were interviewed by an experiencedneuroradiologist for health status, and they also filled out and signed a ques-tionnaire regarding any metallic implants or any other medical/psychologicalcondition that would jeopardize participation in the study.

After acquiring MR anatomic images (about 6–10 min), the seven blockswith experimental and control stimuli were presented, alternating between theexperimental and control stimuli. The entire sequence of stimuli was automati-cally controlled from the MEL2 computer program. After the session, the subjectwas debriefed. It could be argued that a blocked-design would enhance process-ing differences between the control and experimental conditions, again, thiswould however be equivalent for males and females.

Image acquisition was performed with a 1.5 T Siemens Vision MR scannerequipped with 25 mT/m gradients. Scanning of anatomy, using a T1-weighted3D FLASH pulse sequence, was done initially. Thereafter, serial imaging with 70BOLD sensitive echo planar (EPI) whole brain measurements was done duringstimuli presentations, divided into 7 blocks of 10 EPI multi-slice measurementseach. The first 10 measurements were not used in the analysis. Each wholebFw1m

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round as for the 3-D drawings (see Fig. 1). The 2-D bars were oriented eitherorizontally or vertically. The 2-D white bars were chosen to control for visualerception and motor responding, while having no mental rotation requirements.n contrast to the study by Cohen et al. (1996), we chose not to divide the con-rol stimuli into segments, like for the 3-D drawings. This was done to minimizehe risk that the subject would be “tempted” to mentally rotate also the con-rol stimuli. There could still be processing differences between the control andxperimental conditions (e.g. no decision was required in the control condition).owever, any such processing differences between the stimuli would be equiva-

ent across gender, thus not affecting the main hypothesis about sex differences.The 3-D experimental drawings were presented for 3 s on each trial, with

n inter trial interval of 2 s when the screen was black. Thus, each block of MRcans was 60 s [12 stimuli × (3 + 2 s)] during the experimental condition. Thereere six blocks, three blocks with the 3-D experimental stimulus drawings and

hree blocks with the 2-D control stimuli.The control stimuli were presented in four blocks of 20 presentations each.

owever, the first block of 20 presentations was not used in the data analysis,eaving three blocks a 20 presentations as the basis for collection of the MRata. The control stimuli were presented for 3 s, after which the next stimulusair appeared. There were an equal number of horizontal and vertical controltimuli.

The stimulus presentation sequence was controlled from a PC via a computerrogram written in the MEL2 (Schneider, Rodgers, Maciejcyk, Zuccolotto, &t. James, 1995) programming platform. The PC was connected to Resonanceechnology Inc. stimulus presentation equipment, and the subject viewed therawings through a pair of specially designed goggles that were fastened to theR head coil.

In the experimental condition, the task of the subject was to decide on eachresentation whether the two 3-D drawings were of the same shape, or if theyere from two different shapes. The subject made a response by pressing onef two buttons on a response-box placed on his/her chest. The subject pressedhe right hand button if the two drawings were of the same shape, and the leftand button if they were of two different shapes. The MEL2 computer programecorded response accuracy (“correct”, “incorrect”) and reaction time (ms) onach trial. A valid response could span the presentation interval plus the interrial interval periods (=3 + 2 s). During the control condition, the task of theubject was to press the right- and left-hand buttons in an alternating (self-paced)equence, without giving special thoughts to which button was pressed on each

rain EPI acquisition consisted of 16 contiguous axial slices, each 7 mm thick.lip angle/TR/TE/FOV/matrix = 50◦/1.76 ms/84 ms/7 mm/230 mm/128 × 128as used, giving a measurement time of 4 s and an in-plane resolution of.8 mm × 1.8 mm. The delay period between the end of one volume measure-ent to the beginning of the next was 2 s.

The basic design for the fMRI analyses was a factorial 2 × 2 design, withex (males and females) and stimulus (experimental and control) as factors.ctivation differences were analyzed for the main effects of sex and stimulus

nd for the interaction of sex by stimulus.For the behavioral data (response accuracy and RT), the design was reduced

o a one-factor design with sex as the only factor. The reason for this was thato valid behavioral data were obtained during the control condition due to theature of the control stimuli and the nature of the task. The fMRI neuroimagingata were analyzed according to the general linear model implemented in thePM96 Software (Friston, 1994, 1997). The fMRI images were motion cor-ected, and smoothed with a 8 mm kernel, and then subjected to a fixed-effectstatistical analysis (which reduces the generalizability fo the findings to theeneral population). Areas with statistically significant changes in signal inten-ity were determined using the t-statistic for each voxel. The resulting set of-values constituted the statistical parametric map (SPM), and coordinates origi-ally obtained in the MNI reference system were transformed into the Talairachnd Tournoux (1988) system. Voxels were considered significant if their corre-ponding Z-score exceeded a height threshold of p < 0.001, Z > 3.09, with thextent threshold set to p = 0.05. Z-values for the peak-activated voxels in sig-ificant clusters are presented in tables along with corresponding p-values, andalairach and Tournoux (1988) coordinates for anatomical localization. Subtrac-

ion images were analyzed for the main effect of sex, for stimulus content (3-Dbjects versus 2-D objects), and for the interaction of sex by stimulus content.

. Results

An analysis of variance for response accuracy and reactionime showed no significant differences between the males andemales, neither for response accuracy (males 26% correct, S.D.6%, females, 17% correct, S.D. 21%), nor for reaction time

1578 K. Hugdahl et al. / Neuropsychologia 44 (2006) 1575–1583

Fig. 2. Clusters of significant MR signal increases in the 3-D experimental stimulus condition after subtraction of the 2-D control stimulus condition, for the wholegroup. Data were transformed to Z-scores in the SPM-96 analysis software and plotted onto lateral views of the MR anatomy template in the SPM-96 software. Theimages were height thresholded at a significance level of p < 0.001 (Z > 3.09). See text and corresponding table for further details.

(males 3100 ms, S.D. 275 ms, females 2700 ms, S.D. 310 ms),although there was a tendency for the males to be more accurate,and the females to be faster.

For the BOLD fMRI data, there was a significant main effectof stimulus (3-D experimental versus 2-D control), as seen inFig. 2. The 3-D mental rotation tasks produced significant clus-ters of activation in the right and left superior parietal lobule(Brodmann area 7; x: 22, y: −73, z: 38 and x: −20, y: −51, z:52), and in the right and left inferior frontal lobe (Brodmannarea 44; x: 36, y: 8, z: 28 and x: −41, y: 20, z: 18). The inferiorfrontal gyrus activations also extended into the middle frontalgyrus, particularly on the left side, as seen in Fig. 2. Similarly,the inferior prietal lobule activations extended into the dorsaloccipital lobe, and the superior parietal activation also extendedinto the vicinity of the intraparietal sulcus. Although not for-mally tested, the corresponding t-values for the peak voxel inthe significant clusters were larger in the right compared to theleft hemispheres (t = 7.82 and 6.71 for the parietal activations,and t = 4.82 and 4.65 for the corresponding frontal activations.

There were no significant activations at the threshold levelfor the reversed subtraction (2-D minus 3-D stimuli), neither atthe cluster nor at the voxel level.

Subtracting activation for the females from activation for themales, for the 3-D stimulus condition, there were significant acti-vations in the right parietal lobule in Brodmann area 7 (t = 5.48,x: 25, y: −62, z: 42). The reversed subtraction, subtracting acti-vs

mann area 45 (t = 4.86, x: 36, y: 20, z: 22). When subtracting the2-D stimulus condition from the 3-D stimulus condition for themales, a significant cluster of activation was obtained in the rightsuperior parietal lobule (Fig. 3 upper panel), peak voxel t = 7.70,x: 22, y: −69, z: 42. Significant activations were also observedin the left superior parietal lobule, peak voxel t = 5.13; x: −27,y: −50, z: 43. The reversed comparison (2-D stimuli minus 3-Dstimuli) did not result in any significant activations.

When the same comparison was made for the females (Fig. 3lower panel), there were, once again significant activation in theright parietal lobule and right inferior frontal lobe (peak voxels:t = 6.90 and 4.28, x: 22, y: −77, z: 38 and x: −38, y: 20, z:22, respectively). In addition, the females showed significantactivation in the left and right inferior frontal lobes (Brodmannarea 45), t = 5.37 and 4.68, x: 40, y: 24, z: 22 and x: −20, y: −58,z: 46, respectively. The reversed comparison (2-D stimuli minus3-D stimuli) did not result in any significant activations.

Fig. 4 shows remaining significant activations in the malesand females, respectively, when subtracting the activationsobserved in the other sex.

In addition to the significance tests reported above, the num-ber of activated voxels above the height threshold in the rightand left superior parietal lobule (Brodmann 7) were compared,and subjected to a one-way ANOVA. This showed a significantright hemisphere effect, F(1,10) = 9.74, p < 0.05 (means = 98.48and 21.00 activated voxels in the right and left Brodmann area7e

ation for the males from activation for the females, resulted in aignificant activation in the right inferior frontal gyrus, in Brod-

, respectively). A similar analysis for number of activated vox-ls above threshold in the frontal lobe (Brodmann areas 44/45)

K. Hugdahl et al. / Neuropsychologia 44 (2006) 1575–1583 1579

Fig. 3. Upper panel: clusters of significant MR signal increases for the males after subtracting activity during the 2-D stimulus condition from the 3-D stimuluscondition. The images were height thresholded at a significance level of p < 0.001 (Z > 3.09). See text and corresponding table for further details. Lower panel:clusters of significant MR signal increases for the females after subtracting activity during the 2-D stimulus condition from the 3-D stimulus condition. The imageswere height thresholded at a significance level of p < 0.001 (Z > 3.09). See text for further details.

also showed a significant right hemisphere effect, F(1,10) = 9.19,p < 0.05 (means = 88.72 and 30.76 activated voxels in the rightand left hemisphere, respectively).

There was a significant correlation between number of acti-vated voxels in the right parietal lobule and number of cor-rect responses (from the group as a whole), Pearson’s r = 0.81,p < 0.05. Similarly, the correlation between activated voxels inthe right prefrontal cortex and number of correct responses wasalso significant, Pearson’s r = 0.71, p < 0.05. No other corre-lations were significant. For the reaction time data, only thecorrelation with number of activated voxels in the right parietallobule was significant, Pearson’s r = 0.45, p < 0.05, with longerreaction times correlating with increasing number of activatedvoxels.

4. Discussion

A common finding in the present data with regard to visuo-spatial processing and brain function is that the task of mentalrotation pre-supposes a form of coordinate metric processing inthe right parietal lobe, thus supporting Kosslyn’s (1987) orig-inal formulations on the nature of hemispheric asymmetry fordifferent aspects of visuo-spatial processing. The role of theright parietal lobe, furthermore, seems to be the same for malesand females, since the main sex difference was observed forfrontal lobe activations. The fMRI activation data for the whole

group showed significant increases in neuronal activation bilat-erally in the superior parietal lobule, although predominantlyon the right side. This is in agreement with previous studieson mental rotation (e.g. Belin et al., 1998; Cohen et al., 1996;Jordan et al., 2003; Tagaris et al., 1997, 1998). The parietal lob-ule thus seems to be important in mental rotation tasks, whichmay tap into the dorsal pathway of the visual processing sys-tem (cf. Tomasino & Rumiati, 2004; Ungerleider & Mishkin,1982). Other authors have made similar claims, e.g. Cohen etal. (1996) suggested that the superior part of the parietal lob-ule is involved in encoding of visual stimuli, while Belin etal. (1998) suggested that the same area is involved in visualsearch, and Colby, Duhamel, and Goldberg (1995) maintainedthat it is involved in object recognition in space. It is difficultfrom the present data to distinguish between these different func-tions, linked to the superior parietal lobule. A possible commondenominator may, however, be that all studies cited assume aform of visual encoding within a metric-like spatial framework.In contrast, it has been shown with PET and fMRI that theleft superior parietal lobule is involved in categorical spatialrelations processing (Kosslyn, Thompson, Gitelman, & Alpert,1998; Trojano et al., 2002). Thus, generally, both parietal lob-ules seem to be specifically involved in processing of spatialrelations, as also confirmed from animal studies (e.g Morton& Morris, 1995; Steinmetz, 1998), clinical lesion studies (e.g.Tomasino & Rumiati, 2004), and studies on healthy individuals

1580 K. Hugdahl et al. / Neuropsychologia 44 (2006) 1575–1583

Fig. 4. Upper panel: clusters of significant MR signal increases for the males after subtracting activity for the females, during the 3-D stimulus condition. Lowerpanel: The reversed subtraction, females minus males. The images were thresholded at a significance level of p < 0.001 (Z > 3.09). See text and corresponding tablefor further details.

(e.g. Michel, Kaufman, & Williamson, 1994). Hence, there arestrong suggestions that areas in the superior parietal lobule areresponsible for the mental act of “rotating” the object in thevisual buffer (cf. Alivisatos & Petrides, 1997), which would cor-respond to a coordinate processing strategy in Kosslyn’s (1987)terminology. We therefore suggest that mental rotation is partof a functional neuronal network that involves both parietal andfrontal cortical areas, with left frontal lobe areas responsible fora categorical identification of the stimulus, and parietal lobuleareas responsible for the actual “rotation” to be executed.

The hemisphere difference was larger over parietal com-pared to frontal areas. This is in accordance with other acti-vation studies showing that the right hemisphere is dominant orspecialized for processing of visuo-spatial tasks, including theclassic mental rotation task (e.g. Crucian & Berenbaum, 1998;Deutsch, Bourbon, Papanicolaou, & Eisenberg, 1988; Fisher &Pellegrino, 1988). Some authors have, however, claimed thatthe classic mental rotation stimuli can be “rotated” serially asparts rather than as a gestalt, which may invoke left hemisphereserial, categorical processing demands (e.g. Francis & Irwin,1997). An important issue with respect to right and left hemi-sphere processing is to what extent different individuals mayuse different processing strategies when solving the mental rota-tion task, which may confound group differences (cf. Wilson,

Swain, & Davis, 1994). Such individual differences in process-ing strategy may also explain some of the variability betweenstudies with respect to hemisphere dominance. The most clearevidence for hemisphere asymmetry was seen over the supe-rior parietal lobule, particularly over Brodmann area 7 withsignificantly more activated voxels, and with more intensivelyactivated peak voxels, over the right hemisphere compared tohomologous areas over the left hemisphere. Brodmann area 7is part of the dorsal pathway of the ventral–dorsal visual pro-cessing system suggested by Ungerleider and Mishkin (1982),and which is crucial for the localization of objects in space. Theparietal lobule also receives input from other sensory modali-ties, which may imply that the coding of spatial locations maybe multimodal. A caveat is that, although our data suggest arobust group right hemisphere effect, there were individual dif-ferences in the present study; however, these may reflect, aspointed out by Cohen et al. (1996), variability in brain activa-tion for hemisphere dominance across subjects. Similar to thepresent findings, Cohen et al. (1996) found largest activity acrossall their eight subjects in Brodmann area 7, with a small degreeof right hemisphere dominance (see also Tagaris et al., 1997).Thus, most studies seem to converge on the superior parietallobule as a crucial cortical area in mental rotation. Perhaps anargument could be made on the basis of the present findings

K. Hugdahl et al. / Neuropsychologia 44 (2006) 1575–1583 1581

of selective activation in Broca’s area in the females reflectsome aspect of categorical spatial processing (cf. Kosslyn et al.,1998).

The present findings also indicate the inferior frontal gyrus inthe prefrontal cortex to be involved in mental rotation. This mayindicate that the subjects in addition to processing the stimulias visual gestalts, also activated speech areas in the prefrontalcortex as part of “silently speaking to oneself” when trying tosolve the task. This may be particularly interesting when thedata for the males and females are analyzed separately. Fig. 3shows that while the males mainly showed remaining activationin the parietal lobule, the females showed remaining activity inthe right inferior frontal gyrus. Although the remaining activa-tion in the inferior frontal gyrus in the females was primarilylocated on the right side, it may nevertheless address the issuethat males and females use different processing strategies whensolving the mental rotation task. Males seem to process the 3-Dstimuli mainly as visual gestalts, using right hemisphere objectrecognition and rotation functions, while females may use morefrontal lobe areas that may be related to the utilization of lan-guage functions when solving the task. Fig. 3 clearly shows thatmales and females activate different areas in the brain when solv-ing a mental rotation task, although there are also overlappingareas, particularly in Brodmann area 7 in the superior parietallobule. If the activation seen in Brodmann area 45 is reflectingspeech, this might suggest the use of verbal labels during the task.IgubAutalpppl

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allocation rather than brain activation to mental rotation. How-ever, there seems to be no easy interpretation of the relationshipbetween task performance and neuronal activation, since lowactivation could mean high effort (when trying to solve a diffi-cult task), and vice versa. In addition, several researchers haveobserved that increased levels of difficulty typically increase theactivation levels, but the qualitative pattern of activation tendsto remain identical (Carpenter, Just, Keller, Eddy, & Thulborn,1999; Honey, Bullmore, & Sharma, 2000). A word of caution,though, seems necessary: the absence of a sex-difference in thebehavioral data could have been a floor effect caused by theshort presentation times of the stimuli (3 s). Another possibilityfor the lack of sex differences in the behavioral data could bethat such differences are usually observed with larger samplesthan the present one (see Voyer et al., 1995). Interestingly, thiscould mean that BOLD activation has more power to capture sexdifferences in mental processing than the behavioral data. Thus,it cannot be completely ruled out that the rather short presen-tation time (3 s) of the stimuli may have prevented subjects toadequately process the stimuli on each trial. This could have ledto aborted trials and low performance. Such a possibility may,however, not necessarily confound the pattern of activation datasince this is more affected by the intended effort by the subjectthan accuracy rates. Similarly, it cannot be ruled out that if therewas a difference in preferred response strategy by males andfemales when solving the task, this could have lead to differ-era

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A

n turn, one could suggest that what is verbalized in this case,iven the present task, is abstract spatial relations that might besed to “check” whether the two views match or not. This coulde thought of as the use of verbal strategies mentioned above.

recent lesion study by Tranel and Kemmerer (2004) on these of spatial prepositions would seem to back up such a view,hat is, the female group may have been using a verbally medi-ted categorical spatial encoding strategy. Subjects with brainesions were compared to healthy controls on tasks that requiredroduction, comprehension and semantic analysis of locativerepositions (e.g. on, in, around, etc.). The results showed thatatients with impaired knowledge of locative prepositions hadesions in the left frontal lobe.

Although the males and females performed about equal onehavioral variables related to mental rotation, it is obvious thatheir brain activation patterns differed. Thus, it seems that theyse different strategies, leading up to the same performanceevel, with males utilizing a parietal lobule “gestalt” percep-ual strategy, while females may utilize a frontal lobe “serial”easoning strategy. Couched in the current theoretical frame-ork, we suggest that males may be biased towards a coordinate

pproach, and females biased towards a categorical approach,howing more left-sided activation. This would argue againstny differences in BOLD activation between the sexes as beingue to differences in performance between males and females.his is an important point (also made by Jordan et al., 2003, seelso Weiss et al., 2003) since otherwise any differences in acti-ation could be due to different levels of performance for malesnd females. Theoretically, activation differences in the presencef significant performance differences when solving the mentalotation tasks could reflect general cognitive effort and resource

nces in brain areas activated. Although a possibility, this seemsather remote in its ability to generate the qualitative patterns ofctivation that were observed.

The significant correlations between number of activatedoxels in the right parietal lobule and overall number of cor-ect identifications reinforces the previous argument of a rightemisphere basis for mental rotation, with improved accuracyn the task when the critical area is activated. We observed noask performance – brain activation relationship that was specifico the left hemisphere.

cknowledgements

The present study was financially supported by a grant fromaukeland University Hospital to Kenneth Hugdahl. The con-

tructive comments by Bruno Laeng on an earlier version of theanuscript are greatly acknowledged.

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