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93:1020-1034, 2005. First published Sep 22, 2004; doi:10.1152/jn.00637.2004 J NeurophysiolGeyer, Karl Zilles and H. Henrik Ehrsson Eiichi Naito, Per E. Roland, Christian Grefkes, H. J. Choi, Simon Eickhoff, Stefan2 in Human Kinesthesia Dominance of the Right Hemisphere and Role of Area

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Dominance of the Right Hemisphere and Role of Area 2in Human Kinesthesia

Eiichi Naito,1,2 Per E. Roland,1 Christian Grefkes,3 H. J. Choi,3 Simon Eickhoff,3 Stefan Geyer,3 Karl Zilles,3

and H. Henrik Ehrsson1,4

1Division of Human Brain Research, Department of Neuroscience, Karolinska Institute, Stockholm, Sweden; 2Graduate School of Humanand Environmental Studies, Kyoto University, Kyoto, Japan; 3C. and O. Vogt Institute for Brain Research, University of Dusseldorf,Germany; and 4Wellcome Department of Imaging Neuroscience, Institute of Neurology, London, United Kingdom

Submitted 23 June 2004; accepted in final form 11 September 2004

Naito, Eiichi, Per E. Roland, Christian Grefkes, H. J. Choi, SimonEickhoff, Stefan Geyer, Karl Zilles, and H. Henrik Ehrsson.Dominance of the right hemisphere and role of area 2 in humankinesthesia. J Neurophysiol 93: 1020–1034, 2005. First publishedSeptember 22, 2004; doi:10.1152/jn.00637.2004. We have previouslyshown that motor areas are engaged when subjects experience illusorylimb movements elicited by tendon vibration. However, traditionallycytoarchitectonic area 2 is held responsible for kinesthesia. Here weuse functional magnetic resonance imaging and cytoarchitecturalmapping to examine whether area 2 is engaged in kinesthesia, whetherit is engaged bilaterally because area 2 in non-human primates hasstrong callosal connections, which other areas are active members ofthe network for kinesthesia, and if there is a dominance for the righthemisphere in kinesthesia as has been suggested. Ten right-handedblindfolded healthy subjects participated. The tendon of the extensorcarpi ulnaris muscles of the right or left hand was vibrated at 80 Hz,which elicited illusory palmar flexion in an immobile hand (illusion).As control we applied identical stimuli to the skin over the processusstyloideus ulnae, which did not elicit any illusions (vibration). Wefound robust activations in cortical motor areas [areas 4a, 4p, 6; dorsalpremotor cortex (PMD) and bilateral supplementary motor area(SMA)] and ipsilateral cerebellum during kinesthetic illusions (illu-sion-vibration). The illusions also activated contralateral area 2 andright area 2 was active in common irrespective of illusions of right orleft hand. Right areas 44, 45, anterior part of intraparietal region (IP1)and caudo-lateral part of parietal opercular region (OP1), cortexrostral to PMD, anterior insula and superior temporal gyrus were alsoactivated in common during illusions of right or left hand. Theseright-sided areas were significantly more activated than the corre-sponding areas in the left hemisphere. The present data, together withour previous results, suggest that human kinesthesia is associated witha network of active brain areas that consists of motor areas, cerebel-lum, and the right fronto-parietal areas including high-order somato-sensory areas. Furthermore, our results provide evidence for a righthemisphere dominance for perception of limb movement.

I N T R O D U C T I O N

Somatic perception of limb position or limb movementdepends to a large extent on the central processing of kines-thetic information originating from the receptors in muscles.With eyes closed, vibration stimuli at �80 Hz on the tendon ofa limb can elicit a kinesthetic illusory movement of the limb inthe absence of actual movements (Goodwin et al. 1972a,b;Naito and Ehrsson 2001; Naito et al. 1999, 2002a,b). The

vibration stimuli mainly excite the muscle spindle afferentssignaling that the vibrated muscles are stretched although thelimb remains immobile (Burke et al. 1976; Collins andProchazka 1996; Gandevia 1985; Roll and Vedel 1982; Roll etal. 1989). We have consistently demonstrated by positronemission tomography (PET) and functional magnetic reso-nance imaging (fMRI) that the contralateral motor cortex (M1;cytoarchitectonic areas 4a and 4p), primary somatosensorycortex (SI), dorsal premotor cortex (PMD), supplementarymotor area (SMA), cingulate motor area (CMA) (Naito andEhrsson 2001; Naito et al. 1999, 2002a,b), and the ipsilateralcerebellum (Naito et al. 2002a,b) are active during illusorymovements of arm or hand. In particular, M1 appears to beprimarily responsible for the kinesthetic processing of musclespindle input, and its activity is associated with the perceptionof limb movements (Naito 2004; Naito et al. 2002b). Thegeneral aim of the present study was to investigate the brainregions, in addition to the motor areas described in the preced-ing text, which may be active during kinesthetic illusions. Weexamine three specific hypotheses.

First, we examine the hypothesis that area 2 is involved inkinesthetic illusions. A large number of studies in non-humanprimates suggest that neurons in cytoarchitectonic area 2 re-spond to sensory input during passive or active limb move-ments (Burchfiel and Duffy 1972; Costanzo and Gardner 1981;Gardner 1988; Gardner and Costanzo 1981; Iwamura 2000;Iwamura and Tanaka 1996; Iwamura et al. 1993, 1994; Jen-nings et al. 1983; Mountcastle and Powell 1959; Pons et al.1992; Salimi et al. 1999; Schwarz et al. 1973; Taoka et al.1998, 2000; Wolpaw 1980). As there seem to be no obviousanatomical differences between area 2 in monkeys and humans(Zilles and Palomero-Gallagher 2001), one may expect that thehuman area 2 would be involved in the processing of kines-thetic information. One possible reason for the apparent dis-crepancy between our imaging results and the non-humanprimate literature is the differences in afferent input duringkinesthetic illusions and passive limb movement. During ten-don vibration illusions, the muscle spindle afferent is the onlysensory source signaling limb movements (see references inthe preceding text), whereas during passive limb movements,the brain receives multiple somatosensory inputs from musclereceptors, joint receptors, and skin receptors (Burke et al. 1988;Collins and Prochazka 1996; Hulliger et al. 1979). As neurons

Address for reprint requests and other correspondence: E. Naito, GraduateSchool of Human and Environmental Studies, Kyoto University, Sakyo-ku,Kyoto 606 8501 Japan (E-mail: [email protected]).

The costs of publication of this article were defrayed in part by the paymentof page charges. The article must therefore be hereby marked “advertisement”in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

J Neurophysiol 93: 1020–1034, 2005.First published September 22, 2004; doi:10.1152/jn.00637.2004.

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in area 2 respond to input from cutaneous receptors (Costanzoand Gardner 1980; Gardner 1988; Hyvarinen and Poranen1978; Iwamura and Tanaka 1978; Iwamura et al. 1993, 1994;Warren et al. 1986), area 2 may receive a greater amount ofsomatosensory input during passive limb movement than dur-ing tendon vibration. Nevertheless, if human area 2 is genu-inely involved in kinesthetic processing, we would expect todetect area 2 activity during the kinesthetic illusions if we useda sensitive imaging method.

If this is the case, it is important to know the functionaldifferences between M1 and area 2 during kinesthetic illusion.This brings us to our second hypothesis that area 2 should beactive not only during illusion of the contralateral limb but alsoduring illusion of the ipsilateral limb, whereas M1 should beactive only during illusion of the contralateral limb (Naito andEhrsson 2001). Neurons in monkey’s area 2 are known torespond to the afferent input not only from the contralaterallimbs but also from the ipsilateral limbs (Iwamura 2000;Iwamura et al. 1994; Taoka et al. 1998, 2000). Thus wepredicted that area 2 would be active no matter whethersubjects experience illusions of the right or the left limb.

Our third hypothesis was that the right hemisphere wouldhave a dominant role in kinesthetic processing. It is a commonview in clinical neurology that the right hemisphere is special-ized for bodily perception (Berlucchi and Aglioti 1997; Critch-ley 1953; Devinsky and D’Esposito 2004). This notion is basedon human lesion studies (e.g., Halligan et al. 1993; McGonigleet al. 2002; Sellal et al. 1996). However, few imaging studiesof intact brains have been conducted to support this view.Therefore we tested the hypothesis that the right hemisphere isstatistically more active than the left hemisphere when subjectsexperience the illusory movements of the right or the left hand.

We utilized fMRI to measure the brain activity when sub-jects experienced an illusory palmar flexion of the wrist thatwas elicited by the tendon vibration of the wrist extensormuscles. We used fMRI rather than PET because fMRI al-lowed us to collect a significantly greater number of brainscans per subject and hence provides a better statistical powerthan PET to detect relatively weak but significant brain activ-ities. Furthermore, we vibrated the tendon of the right or lefthand respectively in the same group of subjects. This allowedus to directly investigate a possible lateralization of the acti-vations during kinesthetic illusions. Finally, we used cytoar-chitecturally defined areas from 10 postmortem human brainsto describe the topography of each area in a probabilisticfashion.

M E T H O D S

Subjects

Ten right-handed (Oldfield 1971) male subjects (21–33 yr) with nohistory of neurological or other disease participated in the study. Allsubjects had given their informed consent and the Ethical Committeeof the Karolinska Hospital had approved the study. The fMRI exper-iment was carried out following the principles and guidelines of theDeclaration of Helsinki (1975).

fMRI measurement and tasks

A 1.5 T General Electric scanner with head-coil provided T1-weighted anatomical images (3D-SPGR) and functional T2*-weighted echoplanar images (64 � 64 matrix, 3.4 � 3.4 mm, TE �

60 ms). A functional image volume comprised 30 slices of 5-mmthickness (with 0.4-mm interslice gap); this ensured that the wholebrain was within the field of view.

The subjects were blindfolded and their ears were plugged. Theyrested comfortably in a supine position in the MR scanner. Theextended arms were oriented in a relaxed supine position parallel tothe trunk. The arms were supported proximal to the wrist. The handswere completely relaxed in this position. During the experimentalconditions, the subjects were instructed to completely relax (and makeno movements) and to be aware of the sensation from the wrist.

We vibrated the tendon of wrist extensor muscles (the extensorcarpi ulnaris; ECU) to elicit an illusory palmar flexion of the wrist(illusion). To control for the effect of the skin vibration, we appliedthe identical stimuli to the skin over the processus styloideus ulnae,which does not elicit any illusion (vibration). A rest condition wherethe subjects relaxed completely was also included. We used a non-magnetic vibrator that was driven by constant air pressure provided byan air-compressor (Biltema Art. 17–635, Linkoping, Sweden). Thefrequency was �80 Hz. The vibration site was �1 cm2. For eachsubject, we performed six fMRI sessions: in three of these the rightwrist was vibrated alternating with three sessions in which the leftwrist was vibrated (e.g., left session, right session, left session, and soforth). A total of 6 � 128 functional image volumes were collected foreach subject. In each session, there were six conditions. The subjectswere tested on illusion, vibration, and rest when right and left handswere separated and also when right and left hands were in contactpalm to palm. The results from the latter three conditions have beenreported elsewhere (Naito et al. 2002b). Thus in the present paper, weonly describe the results from the conditions where right and lefthands were separated, i.e., illusion, vibration, and rest. Each conditionlasted for 32 s (8 functional images, TR � 4 s) and was repeated twiceduring each session. The order of conditions was randomized accord-ing to a balanced schedule.

In the training session before fMRI, we selected 10 of 16 subjects,who experienced vivid illusory palmar flexion (�20° wrist flexion)(see METHODS sections in Naito and Ehrsson 2001; Naito et al.2002a,b). An electromyogram (EMG) from the skin surface of thevibrated ECU muscle showed slight increase of the activity. From theflexor muscle (the flexor carpi ulnaris; FCU), we found that no EMGactivity was present during illusion. These EMG results confirmedthose in the previous study (Naito et al. 2002a). During the fMRIscanning, we observed no overt hand movements in any of theconditions. After the fMRI, all subjects reported that they vividlyexperienced the sensation of a palmar flexion of the vibrated hand.

fMRI data analysis

The fMRI data were analyzed with the Statistical Parametric Map-ping software [SPM99; http//:www.fil.ion.ucl.ac.uk/spm; WellcomeDepartment of Cognitive Neurology, London, U.K. (Friston et al.1995a,b)]. The functional images were realigned to correct for headmovements (Ashburner and Friston 1997), co-registered with eachsubject’s anatomical MRI, and transformed (linear and nonlineartransformations) into the reference system of Talaraich and Tournoux(Ashburner and Friston 1997; Talaraich and Tournoux 1988), usingthe Montreal Neurological Institute (MNI) reference brain (Naito et al.2002b). The functional images were scaled to 100 to correct for globalchanges in the MR signal to eliminate the effects of global changes inthe signal and were spatially smoothed with a 8-mm full width athalf-maximum (FWHM) isotropic Gaussian kernel and smoothed intime by a 4-s FWHM Gaussian kernel. We fitted a linear regressionmodel (general linear model) to the pooled data from all subjects toincrease the sensitivity of the analysis (fixed effects model) (Naito etal. 2002b). The validity of this approach, in terms of consistency ofeffects across all subjects in the group, was confirmed by conductingsingle-subject volume-of-interest (VOI) analyses (see further in thefollowing text). Each condition was modeled with a boxcar function

1021AREAS ACTIVE DURING ILLUSORY MOVEMENT OF RIGHT OR LEFT HAND

J Neurophysiol • VOL 93 • FEBRUARY 2005 • www.jn.org

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delayed by 4 s and convoluted with the standard SPM99 hemody-namic response function.

To identify the brain areas that are active during the kinestheticillusion we performed pair-wise contrasts of the conditions i.e.,(illusion–vibration). To identify the areas that were active duringillusion of the right hand, we used the contrast of (right illusion–rightvibration). We used the contrast of (right illusion–right rest) as aninclusive mask to exclude voxels that were not at all active during theillusions as compared with the rest condition. This masking procedurewas done to remove voxels that only showed deactivation duringvibration. The threshold for the mask was set at the very liberalthreshold of P � 0.05, uncorrected so that no relevant areas wereexcluded. For the left hand, we used the contrast of (left illusion–leftvibration). We also used the contrast of (left illusion–left rest) as aninclusive mask (P � 0.05, uncorrected). We used a significantthreshold of P � 0.05 (t � 4.58) corrected for multiple comparisonsin the whole brain space.

To depict the areas that are commonly active during illusions ofright and left hand, we used the SPM99 conjunction analysis of [(rightillusion–right vibration) � (left illusion–left vibration)]. Similarly toidentify the areas that are commonly active during skin vibration overthe bone, the conjunction analysis of [(right vibration–right rest) �(left vibration–left rest)] was performed. This latter conjunction wasdone so that we could determine whether the illusion conditionsactivated quantitatively different areas from the vibration conditions.For the conjunction analysis (Price and Friston 1997; Worsley andFriston 2000), we used the same t threshold (4.58) for each of the twocontrasts because we only wanted to depict those voxels that weresignificantly active during right illusions as well as left illusions. Thismeans that the threshold of the conjunction analysis corresponds toP � 0.00000025 for two contrasts after a correction of the number ofmultiple comparisons in the whole brain space. Because of thisconservative threshold in the conjunction analysis, one should bear inmind that we do not report areas that showed a statistical trend foractivation during illusion of one hand and a significant activationduring the illusion of the other hand. Finally, we only report theclusters whose sizes were �10 voxels in this analysis.

Testing of dominance of the right-sided regions that arecommonly active during illusions of right and left hands

The conjunction analysis showed that right-sided areas were activein common during right illusions and left illusions (see RESULTS). Thiscould indicate lateralization of the right hemisphere for kinestheticprocessing during tendon vibration. However, to directly test if thisreflects a genuine dominance of the right hemisphere, one has tocompare the activities in the right areas with those in the correspond-ing areas in the left hemisphere. In other words, one has to test if theright-sided areas are significantly more activated than the correspond-ing areas in the left hemisphere. We did this by flipping (a right-to-lefttransformation in the x axis) the functional images from all scans of allsubjects (the smoothed and normalized images). The right and the lefthemispheres were reversed (flipped images). As just pointed out, thismethod allowed us to directly compare an activity in a voxel in theright hemisphere with the corresponding voxel in the left hemisphere.We defined a new general linear model that included both the flippedand the unflipped data. To test whether the blood oxygenation level-dependent (BOLD) signals of the right hemisphere during illusion ofthe right hand were significantly greater than those registered in theleft hemisphere, we defined the contrast of [(right illusion–rightvibration) – (right flipped illusion–right flipped vibration)]. The con-trast (right illusion–right vibration) was used as an inclusive mask toexclude the areas that were not active during illusion of right hand(P � 0.05, uncorrected). The corresponding contrasts were defined totest the right-sided dominance during illusion of the left hand. Forthese tests, we chose a threshold of P � 0.05 after a correction formultiple comparisons in the right regions.

Single-subject VOI analyses

FUNCTIONAL DIFFERENCES BETWEEN M1 AND AREA 2 DURING ILLU-

SIONS OF THE RIGHT AND LEFT HAND. To investigate functionaldifferences between M1 and area 2 during illusions of the right andleft hand, a post hoc single-subject analysis was done (see METHODS inNaito et al. 2002b). When the right illusion was contrasted with theright vibration, we found peak activities in the left M1 (�36, �24, 51)and in the left area 2 (�30, �36, 60). When the left illusion wascontrasted with the left vibration, we found peak activities in the rightM1 (36, �18, 51) and in the right area 2 (48, �27, 51). Two peaks of(�30, �36, 60) and (48, �27, 51) were located in the caudal part ofthe postcentral gyrus in all subjects (of the anatomically standardizedT1-weighted MR image of each subject). Similarly, peaks of (�36,�24, 51) and (36, �18, 51) were located in the precentral gyrus in allsubjects.

We extracted the fMRI data from the four peaks of activities. Wethen calculated the mean percent increase of BOLD signal for eachepoch of illusion compared with vibration conditions. The meanactivity was calculated from six functional images: we excluded thefirst two functional images. This was done for all epochs on eitherhand in each subject. The percent increase was calculated for eachepoch by using the following formula: (Mean in illusion –Mean in thecorresponding vibration) � 100 Mean in the corresponding vibration.

Finally, the mean value for each individual subject was calculatedfrom the six values from six epochs. The right- and left-hand condi-tions were separately treated. We performed a two-factorial ANOVA[vibrated side (right or left) (2) � MI, area 2 (2) repeated measure-ment design] for the mean of individual subject (see Fig. 3). TheANOVA was done separately for the right and the left hemisphere.

Dominance of right-sided areas during illusions of right andleft hand

To investigate activities in the regions that are commonly activeduring illusions of the right and the left hand, another post hocsingle-subject analysis was done. We extracted the fMRI data fromeight peaks of clusters that were commonly active during illusions ofthe right and the left hand (see Table 3 and Fig. 5). We calculated themean percent increase for each epoch of the illusion compared withthe rest condition. We also calculated the mean for each epoch of thevibration compared with the rest condition.

The mean activity was calculated from six functional images: weexcluded the first two functional images. This was done for all epochson either hand in each subject. The percent increase was calculated foreach epoch by using the following formula: (Mean in illusion orvibration –Mean in the corresponding rest) � 100 divided by Mean inthe corresponding rest.

Finally, the mean value for each individual subject was calculatedfrom the six values from six epochs. The right- and left-hand condi-tions were separately treated. We performed a two-factorial ANOVA[vibrated side (right or left) (2) � illusion, vibration (2); repeatedmeasurement design] for the mean of each individual subject for eachpeak (Fig. 5).

Anatomical definitions

We used cytoarchitecturally defined areas from 10 postmortembrains to describe in a probabilistic way the topography of cytoarchi-tectonic areas 4a, 4p (Geyer et al. 1996; Schleicher et al. 1999), 2(Grefkes et al. 2001), 6 [dorsal premotor cortex (PMD), and supple-mentary motor area (SMA)] (Geyer 2004; Geyer et al. 2002), 44 and45 (Amunts et al. 1999), areas in the intraparietal sulcus region (IP1and IP2) (Choi et al. 2002), and areas in the parietal opercular region(OP1, OP2, OP3 and OP4) (Eickhoff et al. 2002) in the standardanatomical space (Roland et al. 2001). The brains were corrected fordeformations attributable to histological processing and the images

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were warped to the same standard anatomical format (Roland et al.2001) by using the full-multigrid (FMG) method (Schormann andZilles 1998).

A population map was generated for each area (Roland and Zilles1998). The population maps describe, for each voxel, how manybrains have a representation of one particular cytoarchitectonic area.In the case of anatomically adjacent areas, the individual variation inthe location and extent of each cytoarchitectural area led to populationmaps overlapping each other and thus to voxels representing morethan one area. In these cases, the voxel was allocated to the cytoar-chitectural area with the highest number of postmortem brains asso-ciated with it (Roland and Zilles 1996a, 1998). For example, onevoxel can correspond to area 4a in 5 of the 10 brains and simulta-neously to area 4p in 1 of 10 brains. This voxel was then assigned toarea 4a. The result was a probability map of the cytoarchitectural areas(Roland et al. 2001).

At the “outer” border of a cytoarchitectural area (i.e., where the areaabutted on a cortical region for which microstructural data and thus apopulation map was not available, e.g., anterior border of area 6toward the prefrontal cortex), a threshold of 3 of 10 (30%) brains wasapplied. This means that voxels with a representation of a given areain n � 3 brains were assigned to this area, whereas voxels with arepresentation of this area in n � 3 brains were discarded. Thiscriterion has been used before (see e.g., Bodegard et al. 2001; Naitoet al. 2002b). The result of this procedure is a probability map thatprovides a working definition of each area’s most probable location inthe standard anatomical space (Roland et al. 2001). The probabilitymap was finally transformed into the MNI reference brain space(Ashburner and Friston 1997). This procedure allowed us to relate thelocations of fMRI activation peaks to the cytoarchitectural probabilitymaps (Mohlberg et al. 2003: www.bic.mni.mcgill.ca/cytoarchitecton-ics/). This technique provided us with an observer-independent pos-sibility to localize activations in the cytoarchitectonic areas. However,some cautions are required when interpreting results. Because thecytoarchitectural areas are probability maps, a voxel in the standardspace can correspond to more than one area, i.e., individual postmor-tem brains can have different areas located at this particular location.Thus the anatomical localizations of activations in the cytoarchitec-tural areas should be considered as “probabilistic indicators.” Forfurther discussion of the technique of combining functional imagingand cytoarchitectural mapping, see Bodegard et al. (2001), Ehrsson etal. (2003), Mohlberg et al. (2003), Naito et al. (2002b); Roland et al.(2001), Roland and Zilles (1998), and Young et al. (2004).

We adopted the definition of the functional areas of rostral cingu-late motor area (CMAr) and caudal cingulate motor area (CMAc) inthe cortical motor system as defined by Roland and Zilles (1996b).

R E S U L T S

All subjects verbally reported that they experienced vividillusions of wrist flexion in the illusion condition and noillusion in the vibration condition during fMRI scanning. Whenthe tendon on the right wrist extensor muscles (the ECU) wasvibrated, all subjects felt the illusory flexion of the right wrist.Similarly when the tendon on the left muscle was vibrated, allsubjects felt the illusion of the left wrist. They also reportedthat there was no difference in vividness of illusory experiencebetween the right and left hand. No overt wrist movement wasobserved in any of the experimental sessions.

Brain activation during kinesthetic illusion of righthand movement

When right illusion was contrasted with right vibration, wefound significant activations in cortical motor areas, right

parietal cortex, bilateral inferior frontal cortices, bilateral pre-frontal cortices and right cerebellum (Fig. 1 and Table 1).

In the cortical motor areas, one cluster was located in the leftcytoarchitectonic areas 4a, 4p (M1), and 6 (PMD). This clusterfurther extended rostrally into cortex rostal to area 6 (PMD)and caudally into areas 3a, 3b, and 2. In this cluster, we foundthree peaks of activation in areas 4p, 6 (PMD), and 2. Thesecond cluster was located in the bilateral medial walls of thefrontal lobes. We found three peaks in the left area 6 (SMA/CMAc) and in the right CMAr and CMAc. The third clusterwas located in the right area 6 (PMD). The peak was located inthe border between area 6 (PMD) and cortex rostral to PMD.

In the right parietal cluster, we found three peaks of activa-tion in areas 2, IP1, and OP1. The bilateral inferior frontalclusters extended ventrally into the tip of superior temporalgyrus (STG). In the right cluster, we found four peaks ofactivation in areas 44, 45, STG, and anterior insula. In the leftcluster, we found a peak in STG.

Brain activation during kinesthetic illusion of left-hand movement

When left illusion was contrasted with left vibration, wefound significant activations in cortical motor areas, rightparietal cortices, right inferior frontal cortices, right putamen,and left cerebellum (Fig. 2 and Table 2).

In the cortical motor areas, one cluster was located in theright areas 4a, 4p, 6 (PMD). This cluster further extendedrostrally into cortex rostal to area 6 (PMD) and caudally intoareas 3a, 3b, 2, IP1, and OP1. In this cluster, we found peaksof activation in areas 4a, 6 (PMD), 2, IP1, and OP1, respec-tively. The second cluster was located in the bilateral medialwalls of the frontal lobes. We found three peaks in the left area6 (SMA/CMAc) and in the right area 6 (SMA/CMAc andpre-SMA).

In the right inferior frontal cluster, we found peaks in areas44 and 45 and in the STG. Right superior parietal cortex wasalso activated.

Differences between right- and left-hand illusions

To identify areas that are specifically active during theillusions of right hand movements we contrasted [(right illu-sion–right vibration) - (left illusion–left vibration)]. The leftM1 was significantly activated (�36, �21, 51; area 4p; P �0.05 corrected for whole brain space). Similarly, the right M1(36, �18, 51; area 4a) was specifically activated during theillusion of left hand movement [(left illusion–left vibration) -(left illusion–left vibration)].

Activities in M1 and area 2 during illusions of right- or left-hand movement

Figure 3 shows the mean percent increase of the BOLDsignal in M1 and area 2 when illusion was compared withvibration. The signal in M1 only increased when the subjectsexperienced illusory movements of the contralateral hand,whereas the signal in area 2 also increased when they experi-enced illusions of the ipsilateral hand as well (Fig. 3). Atwo-factorial ANOVA [vibrated side (right or left) (2) � areas(MI, area 2) (2); repeated measurement design] of the percentincrease in each area and hemisphere showed significant inter-



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action between these two factors [F(1,9) � 17.7, P � 0.005 forthe left hemisphere; F(1,9) � 6.8, P � 0.05 for the righthemisphere]. This suggests that M1 participates only in the

processing of kinesthetic illusions of the contralateral hand,whereas area 2 is involved in the illusions of both right and lefthands.

FIG. 1. Active regions during kinestheticillusion of right-hand movement. Right illu-sion was contrasted with right vibration(P � 0.05 corrected). All clusters are dis-played on an anatomical T1-weighted MRIfrom a representative single subject. A: hor-izontal section z � �58; B: z � �51; C: z ��34; D: z � �18; E: z � �4; F: z � �24.Right hemisphere is shown to the right.

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Brain regions commonly active during illusions of right- andleft-hand movement

The results from the simple pair-wise contrasts presented inthe preceding text revealed that some areas appeared to beactivated in common during kinesthetic illusions of both right-and left-hand movement. Most notably, frontal and parietalareas in the right hemisphere seem to be more strongly activeno matter when the subjects experienced illusions of right orleft hand. To verify these observations, we performed twoadditional tests (see METHODS). First we used a conjunctionanalysis to directly show, in the same statistical image, that thesame voxels were active during both right and left illusions.

Using the contrast (right illusion–right vibration) � (leftillusion–left vibration), we found four clusters of active voxelsin the bilateral medial walls of the frontal lobes (SMA/CMAc),the right area 6 (PMD), the right parietal cortex, and the rightinferior frontal cortex (Fig. 4 and Table 3). In the medial wallcluster, we found peaks in bilateral area 6 (SMA/CMAc). Inthe right PMD cluster, the peak was located in the borderbetween area 6 (PMD) and cortex rostal to PMD. In the rightparietal cortex, we found peaks in areas 2, IP1, and OP1.

Finally, in the right inferior frontal cluster, we found peaks inareas 44, 45, and STG. From these findings, it is evident thatthe commonly active areas were predominantly located in theright hemisphere.

In contrast, when we identified the brain areas that wereactive in common during skin vibration over the right- andleft-sided bone (right vibration–right rest) � (left vibration–leftrest), we only found activations in the bilateral parietal oper-cular regions (areas OP1 and OP4). It is noteworthy that noneof the regions that were active in common during illusions ofright- and left-hand movement was commonly activated duringvibration stimuli over the skin (minimum t value of 4.58 in theconjunction analysis). This suggests that there are qualitativedifferences in the activation patterns during kinesthetic illu-sions and during skin vibration with no illusions.

Dominance of the right-sided regions that are commonlyactive during illusions of right- and left-hand movement

As described in the preceding text, we found activations inthe frontal and parietal areas that were active in commonduring illusions of the right and left hand. This finding appearsto suggest a right-hemisphere dominance in the processing ofkinesthetic illusions. However, to statistically test this hypoth-esis, one has to directly compare the activities in the right-sidedareas with those in the corresponding areas in the left hemi-sphere. Therefore we compared the activities of the clusters inthe right hemisphere as detected by the conjunction analysiswith those of the corresponding regions in the left hemisphere(see METHODS).

We found that when the subjects experienced illusory move-ments of the right hand, right area 6 (PMD)/cortex rostral toPMD, area 45, IP1/OP1, and STG were significantly moreactivated than the corresponding left regions (Table 4). Incontrast, right SMA and area 2 did not show significantlystronger activity than the corresponding left regions duringillusions of right-hand movement. During illusions of the lefthand, right area 6 (PMD)/cortex rostral to PMD, 44, 4p, 2, IP1,and STG were significantly more activated than the corre-sponding left regions. These results demonstrate a right-hemi-sphere dominance in the processing of kinesthetic illusionselicited by the tendon vibration.

Single-subject analysis for a dominance of right-sided areasduring illusions of right- and left-hand movement

To investigate activities in those regions that are active incommon during illusions of right- and left-hand movement,another post hoc single-subject analysis was done (see METH-ODS). One purpose of this analysis was to confirm that theactivities in the right-sided regions that were commonly activeduring illusions of right- and left-hand movement were notbiased by the data from a few subjects. We tested if the meanpercent increase of the BOLD signal across subjects in theillusion condition is greater than that in the vibration condition(see METHODS). Another purpose was to test whether the levelsof activities in the right-sided areas differ between right andleft illusions.

Figure 5 shows that the mean percent increase of the BOLDsignal was greater in the illusion condition than in the vibrationcondition in all commonly activated areas [main effect of

TABLE 1. Significant activations when right illusion wascontrasted with right vibration

Areas

Coordinates ofPeak

t-Value

ClusterSize

Voxelsx y z

Left areas 4a-4p-6-3a-3b-2 cluster 185Area 4p �36 �24 51 8.35Area 2 �30 �36 60 5.89Area 6 (PMD) extending cortex

rostral to PMD �27 �9 57 5.72Bilateral medial wall cluster 458

L area 6 (SMA/CMAc) �3 �3 48 9.39R CMAr 3 15 42 7.58R CMAc 6 �21 36 5.78

Right area 6 cluster 56R PMD/cortex rostral to PMD 33 0 54 7.04

Right areas 2-IP1-OP1 cluster 324Area 2 42 �36 54 8.66Areas IP1/OP1 66 �27 33 8.63Area OP1 69 �24 21 7.75

Right areas 44–45-STG-insularcluster 525

STG 51 18 �12 10.02Area 44 57 15 �3 9.87Area 45 57 21 24 6.17Anterior insular 36 24 �3 7.23

Left areas 44–45-STG cluster 109STG �57 12 �6 8.64

Right PFC 45 51 6 9.27 118Left PFC �36 48 18 6.19 22Right cerebellum lobe V 15 �54 �24 5.49 13Left anterior insular �36 21 �3 5.55 11

Area IP1 is caudally located to area 2, lining the rostral part of theintraparietal sulcus and also ventrally extending into supramarginal gyrus(SMG). Area OP1 is located laterally in the parietal operculum (PO) and alsodorsally extending into SMG (see Fig. 4) and see also (Young et al. 2004).Coordinates in Talairach and Tournoux (1988) as defined by the MontrealNeurological Instiutute. The atlas of the human cerebellum is based on that ofSchmahmann et al. (2000). Anatomical naming of the activated areas is basedon coordinates of activation peaks. PMD, dorsal premotor cortex; SMA:supplemenatry motor area, CMA: cingulate motor area, CMAr: rostral CMA,CMAc: caudal CMA, STG: superior temporal gyrus, PFC: prefrontal cortex.x/y indicates border between area x and area y.



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tendon vibration in the ANOVA, see METHODS; left SMA/CMAc: F(1,9) � 14.5, P � 0.005; right SMA/CMAc: P �0.025; right area 2: P � 0.11; right PMD/cortex rostral to

PMD: P � 0.025; right IP1: P � 0.05; right area 45: P � 0.1;right area 44: P � 0.025; right STG: P � 0.025]. In addition,the left-hand stimulation activated right SMA/CMAc, area 2

FIG. 2. Active regions during kinestheticillusion of left hand movement. Left illusionwas contrasted with left vibration (P � 0.05corrected). A: horizontal section z � �63; B:z � �55; C: z � �34; D: z � �18; E: z ��4; F: z � �27. For other conventions, seelegend of Fig. 1.

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and PMD/cortex rostral to PMD significantly more than theright-hand stimulation [main effect of the vibrated side in theANOVA; SMA/CMAc: F(1,9) � 5.5, P � 0.05; area 2: P �0.025; PMD/cortex rostral to PMD: P � 0.005]. In contrast,there were no significant differences between right- and left-hand stimulation in right IP1, areas 44 and 45, and STG (P �0.33 for all regions).

D I S C U S S I O N

We measured brain activities by fMRI when healthy humansubjects experienced kinesthetic illusory flexions of the right orleft wrist elicited by tendon vibration. There were three mainfindings.

First, in the absence of actual limb movements, we foundrobust activations in the contralateral cortical motor areas[areas 4a and 4p (M1) and 6 (PMD)]. We also found strongactivity in bilateral medial area 6 (SMA/CMAc) and in theipsilateral anterior cerebellum. These results corroborate thosefrom our earlier studies that the motor system participates inthe processing of kinesthetic illusions (Naito 2004; Naito andEhrsson 2001; Naito et al. 1999, 2002a,b).

Second, as suggested by electrophysiological studies inmonkeys, cytoarchitectonic area 2, especially right area 2, wasalso involved in the processing of kinesthetic signals in humansubjects. However, the engagement of area 2 in kinestheticillusions was different from that of M1 in a sense that M1 wasstrictly active during illusions of the contralateral limb,whereas area 2 was also active during illusions of the ipsilateral

limb (Fig. 3). This suggests functional differences in theprocessing of kinesthetic signals between M1 and area 2.

Third, we found a dominance of the right hemisphere inbrain activation during kinesthetic illusions. Right area 6(PMD)/cortex rostral to PMD, areas 44, 45, IP1, OP1, anteriorinsula, and STG were all activated in common during illusionsof right and left hand (Fig. 4). These right-sided areas weresignificantly more activated than the corresponding areas in theleft hemisphere (Table 4). This provides the first neurophysi-ological evidence for a dominant role of the right hemispherein human kinesthetic processing.

Methodological considerations

In the illusion and vibration conditions, we vibrated the skinsurface at two sites of the wrist. Because the size of skin areathat was contacted by the vibrator was identical (�1 cm2) andwe used the same frequency (80 Hz) of vibration stimuli,similar sets of skin receptors would probably be recruited inthese two conditions (Naito and Ehrsson 2001). It is veryunlikely that the conspicuous differences in brain activationsobserved during the illusion and vibration conditions were dueto the fact that we vibrated the different skin areas around thewrist. The distance between the two stimulation areas wassmall [3.6 � 0.5 (SD) cm], and therefore the cutaneous afferentinput should be very similar. The difference in activationbetween these two conditions arose from the fact that thetendon of the wrist extensor muscle was only vibrated in theillusion condition. This tendon vibration is an optimal stimulusto excite muscle spindle afferents and elicit kinesthetic illu-sions (Naito and Ehrsson 2001; Naito et al. 1999, 2002a,b; Rolland Vedel 1982; Roll et al. 1989). In contrast, when wevibrated the skin surface over the nearby bone, the subjects didnot experience any reliable illusions because the tendon wasnot directly stimulated. Although muscle spindles are highly

FIG. 3. Mean percent increase of the blood oxygenation level-dependent(BOLD) signal in M1 and area 2 when illusion was compared with vibration(single-subject analysis). The signal in M1 only increased when the subjectsexperienced illusory movements of the contralateral hand, whereas the signalin area 2 also increased when they experienced illusions of the ipsilateral handas well. Bars indicate SE.

TABLE 2. Significant activations when left illusion was contrastedwith left vibration

Structures

Coordinates ofPeak

t-Value

ClusterSize

Voxelsx y z

Right areas 4a-4p-6-3a-3b-2-IP1-OP1cluster 558

Area 4a 36 �18 51 9.78Area 6 (PMD) extending cortex

rostral to PMD 27 �18 63 6.39Area IP1/OP1 57 �33 33 6.32Areas 2/IP1 63 �27 42 5.94Area 2 48 �27 51 5.67Area OP1 69 �33 24 5.15

Bilateral medial wall cluster 295R area 6 (SMA/CMAc) 6 �3 51 9.18L area 6 (SMA/CMAc) �6 �3 48 6.65R area 6 (Pre-SMA) 9 15 60 5.87


Areas 44/45 60 18 18 7.62STG 51 24 �15 7.36Area 44 60 15 6 6.42

Left cerebellum cluster 150Lobe V �18 �51 �27 7.92Lobe V �27 �42 �39 5.74Crus I �27 �66 �33 5.21

Right putamen-insular cluster 107Rostral 30 �9 0 7.22Caudal 27 9 �3 6.22Anterior insular 36 18 0 4.99

Right superior parietal 15 �48 63 5.72 17

See Table 1.



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FIG. 4. Active regions shared by illusionsof right- and left-hand movement. All clus-ters and cytoarchitectonic maps are dis-played on an anatomical T1-weighted MRIfrom a single subject. Right hemisphere isshown to the right. Blue voxels indicatecytoarchitectonic probability map of area 6.Yellow voxels: area 2; orange voxels: areaIP1; dark blue voxels: IP2; green voxels:area 45; white voxels: area 44; light yellowvoxels: area OP1; light blue voxels: areaOP4; light green voxels: area OP2; pinkvoxels: area OP3. Superimposed clusters en-circled by red voxels are the results of theconjunction analysis (right illusion–right vi-bration) � (left illusion–left vibration). Weemployed the same t threshold of 4.58 asused in the contrast of (illusion–vibration).The bilateral medial area 6 (SMA/CMAc),right cortex rostral to PMD (area 6), areas 2,44 and 45, IP1, and OP1, anterior insula andtip of STG were commonly activated. Theright hemisphere was predominantly acti-vated no matter whether the subjects experi-enced illusions of the right or left hand.

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sensitive and some spindles in the hand would be activated bythe spread of the vibration from the bone to the surroundingtissue, this spread was not strong enough to elicit any clearillusions. In a previous study, we found that when we vibratedthe skin surface over the tendon, we never elicited any illusionsnor found any motor activations (10 and 220 Hz) unless weused optimal vibration frequency (70 and 80 Hz) (Naito et al.1999). Thus the present brain activations detected when illu-sion was contrasted with vibration is most likely to be associ-ated with kinesthetic illusions elicited by afferent informationfrom muscle spindles excited by tendon vibration at an optimalfrequency (80 Hz). We did not measure the attention to thestimuli in the different conditions. However, we think it isunlikely that differences in attention could explain our results.First, the subjects did not perform any active task, they werejust instructed to relax and be aware of the sensation form theirwrists. Second, the subjects were instructed to be aware of theirwrists both in the illusion and in the vibration conditions. Thissuggests that the participants were attending slightly to thestimulated hand in both conditions.

Cytoarchitectonic area 2 and parietal cortex

Area 2 was more strongly activated when the tendon wasvibrated over the skin (illusion) than when only the skin wasvibrated without directly involving the tendon (vibration; Fig.5C). Hence, the activity in this area probably reflects theprocessing of kinesthetic afferent input from muscle spindles.This result fits well with results from earlier single-unit studiesin non-human primates that neurons in area 2 react to kines-thetic afferent input during passive limb movements (see ref-erences in the INTRODUCTION).

Area 2 was active during illusions of not only the contralat-eral but also the ipsilateral hand (Fig. 1, A and B) even thoughthe activity in area 2 was larger when the contralateral handwas stimulated (Fig. 3). This finding is in good agreement withfindings in non-human primates that neurons in area 2 respondto somatosensory afferent input from not only the contralateralbut also the ipsilateral limb (Iwamura 2000; Iwamura et al.

1994; Taoka et al. 1998, 2000). The bilateral involvement ofarea 2 in the central processing of kinesthetic illusions isdifferent from the strictly contralateral engagement of M1 (Fig.3). This difference implies that M1 and area 2 might participatein different stages of neuronal processing of kinesthetic infor-mation and suggests that human area 2 is a high-order somato-sensory area (Bodegard et al. 2001; Roland et al. 1998).

In addition, we found peaks of activation in areas IP1 andOP1 in the right hemisphere when the subjects experiencedillusory wrist movements. Area IP1 is caudally located to area2, lining the rostral part of the intraparietal sulcus and alsoextending into supramarginal gyrus (SMG; Fig. 4B). Area OP1is located laterally in the parietal operculum (PO; Fig. 4D) andalso extending into SMG (Fig. 4C) (see also Young et al.2004). These areas are considered to be high-order somatosen-sory areas in humans in a sense that they are engaged insomatosensory tasks but less somatotopically organized(Young et al. 2004). Indeed, identical section in the right areasIP1 and OP1 was commonly engaged in illusions of right- orleft-hand movements.

The precise homology between the cytoarchitectural areas ofthe human and monkey inferior parietal lobe is still unknown(Eidelberg and Galaburda 1984). In the present study, theactivation (areas IP1 and OP1) associated with kinestheticillusion was located in the lateralmost part of the inferiorparietal cortex (Fig. 4, Table 1). Similarly, the lateral andposterior part of the monkey inferior parietal cortex (area7b/PF) contains neurons that predominantly respond to som-esthetic input (Hyvarinen 1981; Hyvarinen and Shelepin1979). In fact, it has been suggested that the inferior parietalcortex in monkeys (area 7b/PF) corresponds to the SMG in thehuman brain (Passingham 1998). In the monkey brain, thissomaesthetic section of the inferior parietal cortex has ipsilat-eral cortical connections with areas 2, 4, 5, 45, PO (Hyvarinen1982a,b; Neal et al. 1987, 1990b), ventral premotor cortex(Ghosh and Gattera 1995; Godschalk et al. 1984; Neal et al.1990a), SMA (Cavada and Goldman-Rakic 1989), and insularcortex (Neal et al. 1987, 1990b 1990b). In our present study,we observed activations in all these areas in conjunction with

TABLE 4. Comparing activation in the right hemisphere and theleft hemisphere (flip analysis)

Structures

Coordinates ofPeak

t-Value

ClusterSize

Voxelsx y z

Right illusion: unflipped vsflipped

R STG 48 27 �15 6.87 91R cortex rostral to PMD/area 6

(PMD) 36 3 51 5.17 24R area 45 57 24 18 4.6 41R area IP1/OP1 63 �24 33 3.9 17

Left illusion: unflipped vs flippedR STG 51 27 �12 3.86 12R cortex rostral to PMD/area 6

(PMD) 33 3 54 3.95 12R area 44 57 15 21 5.99 71R area 4p 36 �30 57 6.02 119R area 2 48 �24 48 5.18R IP1 60 �24 39 4.8

See Table 1.

TABLE 3. Common active areas during right illusion andleft illusion

Structures

Coordinates ofPeak

t-Value

ClusterSize

Voxelsx y z

Bilateral medial wall cluster 176R area 6 (SMA/CMAc) 3 0 51 7.93L area 6 (SMA/CMAc) �6 �3 48 6.65

Right areas 2-IP1-OP1 cluster 134Area 2 39 �36 57 7.46Area IP1 63 �27 42 5.94Areas IP1/OP1 57 �27 33 5.85


STG 51 24 �15 7.36Area 45 57 21 24 6.17Area 44 60 15 6 6.42STG/areas 44/45 57 18 �6 6.32

Right area 6 (PMD)/cortex rostalto PMD 33 �3 54 6.57 42

See Table 1.



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activation in SMG (areas IP1 and OP1); this indicates that thehuman SMG could be an important node in the network offronto-parietal sensorimotor-related areas that represent limbmovements.

The involvement of the right PO (area OP1) in kinestheticillusions is consistent with the early observation that the rightPO was activated during passive movements of the right arm(Weiller et al. 1996). Although PO seems to be activated by awide range of somatosensory stimuli (Bodegard et al. 2000;Ledberg et al. 1995; Naito et al. 1999; Roland et al. 1998), ourresults indicate that the right PO is active when we sense limbmovements. Although the role of the right inferior parietalareas in kinesthetic processing is still unclear, the presentresults fit well with human brain lesion studies demonstratingthat damage to the right inferior parietal cortex impairs per-ception of one’s own body (Berlucchi and Aglioti 1997;Damasio 1999; Hyvarinen 1982b; Sellal et al. 1996).

Frontal areas

Kinesthetic illusions activated the contralateral areas 4a, 4p,and 6 (PMD), bilateral SMA (area 6), CMA, and pre-SMA(area 6), and the ipsilateral cerebellum. The contralateral clus-ter extended into areas 3a and 3b, but we could not find anysignificant peaks in these areas. The activity in M1 (areas 4aand 4p) was strictly related to the illusions of the contralateralhand (Fig. 3), whereas SMA and CMA were bilaterally en-gaged in illusions. The evidence that SMA and CMA partici-pates in the kinesthetic processing of muscle spindle afferentinput fits with the finding that many neurons in the SMA andCMA respond to proprioceptive input during joint rotation andmuscle stretch (Cadoret and Smith 1995). The bilateral activa-tion pattern in these areas irrespective of illusions of right- orleft-hand movement (Fig. 4) is most probably due to intercon-nection between right and left SMA as has been well estab-lished by non-human primates studies showing that neurons intwo SMAs are strongly interconnected (Rouiller et al. 1994;Tanji 1994).

One of the new observations in the present study was thatkinesthetic illusions activated the border between area 6(PMD) and cortex rostral to PMD in the right hemisphere nomatter if the participants experienced illusions of right or lefthand (Fig. 4). In the present study, the blindfolded subjectswere instructed to be aware of the hand movements with nointention of executing movement. When we sense limb move-ment, we are not only aware of the changes in joint angle, butwe also sense the changes of limb location in extrapersonalspace. We speculate that the activity in this area is related tothe somatic monitoring of positional changes of the limb inextrapersonal space because this area is associated with spatial-cognitive processes in primates (Boussaoud 2001; Picard andStrick 2001).

In addition, we found a large active cluster that was locatedin the inferior frontal cortex and that extended into the anteriorinsula and superior temporal cortex. We know that lesions thatdamage this region impair the normal perception of one’s ownbody (Berlucchi and Aglioti 1997; Sellal et al. 1996), and thus

FIG. 5. Mean percent increase of the BOLD signal in the areas that wereactive in common when illusion was compared with rest and vibrationcompared with rest, respectively. Bars indicate SE.

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it is possible that the activity in these areas is related tokinethetic perception. The inferior frontal peak was located inthe right-sided equivalent of Broca’s area (areas 44 and 45)(Amunts et al. 1999). Previously, right areas 44 and 45 wereactivated during motor imagery of the right hand (Binkofski etal. 2000; Ehrsson et al. 2003) and when visually observinghand actions (Buccino et al. 2001). Right area 44, together withright PMv (ventral part of area 6), is also active during theperformance of skilled finger movements of the right hand(Ehrsson et al. 2001). Thus right areas 44 and 45 appear to berelated both to kinesthetic and motor representations of handactions.

Activation in the anterior insular cortex is commonly ob-served during painful and unpleasant stimulation, and it hasbeen suggested that these regions contain a representation ofthe physical condition of one’s body (Craig 2002). Finally, adistinct peak of activity was found in the right tip of the STGduring illusions. The superior temporal gyrus is a multimodalsensory area that receives somatosensory input (Jones andPowell 1970; Seltzer and Pandya 1978), and human lesionstudies suggest that this region may be involved in functionsrelated to spatial awareness (Karnath et al. 2001).

How does the muscle spindle information reach the nonpri-mary frontal and parietal areas? In non-human primates neu-rons in M1 (Asanuma et al. 1980; Brinkman et al. 1985;Colebatch et al. 1990; Fetz et al. 1980; Hore et al. 1976; Huertaand Pons 1990; Lemon 1981; Lemon et al. 1976; Lemon andPorter 1976; Lemon and Van Der Burg 1979; Porter andLemon 1993; Rosen and Asanuma 1972; Strick and Preston1982; Wong et al. 1978), area 3a (Hore et al. 1976; Huerta andPons 1990; Iwamura et al. 1983; Philips et al. 1971; Schwarzet al. 1973), and area 2 (Burchfiel and Duffy 1972; Costanzoand Gardner 1981; Gardner and Costanzo 1981; Iwamura et al.1993, 1994; Jennings et al. 1983; Mountcastle and Powell1959; Schwarz et al. 1973) respond to muscle spindle afferentinput. It is well established that M1 is connected with cytoar-chitectonic area 2 (Darian-Smith et al., 1993; Ghosh et al.1987; Jones et al. 1978; Leichnetz 1986; Pons and Kaas 1986)and with SMA and PMD (Darian-Smith et al. 1993; Godschalket al. 1984; Ghosh et al. 1987; Jones et al. 1978; Leichnetz1986; Stepniewska et al. 1993). Area 2 is also connected withSMA and PMD (Pons and Kaas 1986). The inferior parietalcortex has ipsilateral connections with areas 2, 4, 45, PO(Hyvarinen 1982a,b; Neal et al. 1987, 1990b), ventral premotorcortex (Ghosh and Gattera 1995; Godschalk et al. 1984; Nealet al. 1990a), SMA (Cavada and Goldman-Rakic 1989), andthe insular cortex (Neal et al. 1987, 1990b). In addition,fronto-parietal opercular regions and insular cortex are con-nected with sensory-motor areas (Cipolloni and Pandya 1999;Darian-Smith et al. 1993; Guldin et al. 1992; Preuss andGoldman-Rakic 1989). This evidence suggests that also inhumans the kinesthetic information from muscle spindles isspread from “primary” motor and sensory areas to “nonpri-mary” fronto-parietal association areas. However, it should bestressed that future studies are needed to elucidate the exactroles of these nonprimary areas in kinesthetic perception. Sofar we only have conclusive evidence that activity in theprimary motor cortex reflect the perception of limb movementper se (Naito 2004; Naito et al. 2002b).

Right hemispheric dominance for kinesthetic processing

An important observation was that right area 6 (PMD)/cortex rostral to PMD, areas 44, 45, IP1, OP1, anterior insula,and STG were statistically more activated than the correspond-ing regions in the left hemisphere no matter whether thesubjects experienced illusions of the right or left hand. Impor-tantly, none of these right-sided areas was activated in commonwhen the skin surface over the nearby bone of right or left handwas vibrated. Thus it is unlikely that the activity in theseright-sided areas reflects the somatosensory processing of skinvibration or attention to somatosensory stimuli. Rather, theactivities in these right-sided areas seem to be related to theprocessing of kinesthetic information, which is consistent withthe results from human brain lesion studies (Halligan et al.1993; McGonigle et al. 2002; Sellal et al. 1996).

Claims of hemispheric dominance of brain functions haverarely been statistically supported with the exception of lan-guage dominance in the left hemisphere (Binder et al. 1997;Springer et al. 1999; Vikingstad et al. 2000; Wada and Ras-mussen 1960). Here a hemispheric dominance for humankinesthesia has been statistically demonstrated for the first timein a neuroimaging experiment of intact brains, though a dom-inance of the right hemisphere for somatosensory functions hasbeen suggested (thermal pain: Coghill et al. 2001; tactile andproprioception: Kawashima et al. 2002). The reason for thisright-sided dominance in right-handed subjects is unknown.However, one may conjecturally suggest a developmentalarrangement of the functional organization of language andbody functions, permitting simultaneous use of language andmotoring of somatic functions (e.g., Chiron et al. 1997; Cor-ballis et al. 2000; Geschwind and Galaburda 1985; Karnath2001). This would give the brain a benefit of avoiding inter-ference between language and somatic functions (Roland 2002;Roland and Zilles 1998).

As stated, our results suggest that the right hemisphere isspecialized for the perception of one’s own body. Interestingly,this conclusion fits well with the observation that patients thatundergo preoperative evaluation lose awareness and memoryof arm weakness during amytal inactivation of their righthemisphere (Carpenter et al. 1995; Meador et al. 2000). Duringsuch inactivation testing, these patients no longer feel theweakness of their arm, they lose the ability to visually recog-nize the weak arm as their own, and they become poor inpointing to different parts of their arm. Thus our results that, inhealthy subjects, perception of an illusory limb movementengages a right-sided network of frontal and parietal areas,provides a neurophysiological basis for these perceptual defi-cits in patients after inactivation of the right hemisphere.

G R A N T S

This study was supported by the Axel and Margaret Ax:sson Johnsson’sFoundation and the Swedish Medial Research Council (Project 9456-11A and5925). E. Naito was supported by the grant-aids for the exchange of foreignresearch for young scientists from the Ministry of Education, Culture, Sports,Science, and Technology (MEXT) Japan. H. H. Ehrsson was supported by apostdoctoral grant from the Human Frontier Science Programme.

R E F E R E N C E S

Amunts K, Schleicher A, Burgel U, Mohlberg H, Uylings HBM, and ZillesK. Broca’s region revisited: cytoarchitecture and intersubject variability.J Comp Neurol 412: 319–341, 1999.



on February 9, 2007

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Asanuma H, Larsen K, and Yumiya H. Peripheral input pathways to themonkey motor cortex. Exp Brain Res 38: 349–355, 1980.

Ashburner J and Friston KJ. Spatial transformation of images. In: HumanBrain Function, edited by Frackowiak RSJ, Friston KJ, Frith CD, Dolan RJ,and Mazziotta JC. San Diego: Academic, 1997, p. 43–58.

Berlucchi G and Aglioti S. The body in the brain: neural bases of corporealawareness. Trends Neurosci 20: 560–564, 1997.

Binkofski F, Amunts K, Stephan KM, Posse S, Schormann T, Freund HJ,Zilles K, and Seitz RJ. Broca’s region subserves imagery of motion: acombined cytoarchitectonic and fMRI study. Hum Brain Mapp 11: 273–285,2000.

Binder JR, Frost JA, Hammeke TA, Cox RW, Rao SM, and Prieto T.Human brain language areas identified by functional magnetic resonanceimaging. J Neurosci 17: 353–362, 1997.

Bodegard A, Geyer S, Naito E, Zilles K, and Roland PE. Somatosensoryareas in man activarted by moving stimuli: cytoarchitectonic mapping andPET. Neuroreport 11: 187–191, 2000.

Bodegard A, Geyer S, Grefkes C, Zilles K, and Roland PE. Hierarchicalprocessing of tactile shape in the human brain. Neuron 31: 317–328, 2001.

Boussaoud D. Attention versus intention in the primate premotor cortex.Neuroimage 14: S40–45, 2001.

Brinkman J, Colebatch JG, Porter R, and York DH. Responses of precen-tral cells during cooling of postcentral cortex in conscious monkeys.J Physiol 368: 611–625, 1985.

Buccino G, Binkofski F, Fink GR, Fadiga L, Fogassi L, Gallese V, SeitzRJ, Zilles K, Rizzolatti G, and Freund HJ. Action observation activatespremotor and parietal areas in a somatotopic manner: an fMRI study. EurJ Neurosci 13: 400–404, 2001.

Burchfiel JL and Duffy FH. Muscle afferent input to single cells in primatesomatosensory cortex. Brain Res 45: 241–246, 1972.

Burke D, Hagbarth K, Lofstedt L, and Wallin G. The responses of humanmuscle spindle endings to vibration of non-contracting muscles. J Physiol261: 673–693, 1976.

Burke D, Gandevia SC, and Macefield G. Responses to passive movementof receptors in joint, skin, and muscle of the human hand. J Physiol 402:347–361, 1988.

Cadoret G and Smith AM. Input-output properties of hand-related cells in theventral cingulate cortex in the monkey. J Neurophysiol 73: 2584–2590,1995.

Carpenter K, Berti A, Oxbury S, Molyneux AJ, Bisiach E, and OxburyJM. Awareness of and memory for arm weakness during intracarotidsodium amytal testing. Brain 118: 243–251, 1995.

Cavada C and Goldman-Rakic P. Posterior parietal cortex in rhesus monkey.II. Evidence for segregated corticocortical networks linking sensory andlimbic areas with the frontal lobe. J Comp Neurol 287: 422–445, 1989.

Chiron C, Jambaque I, Nabbout R, Lounes R, Syrota A, and Dulac O. Theright brain hemisphere is dominant in human infants. Brain 120: 1057–1065,1997.

Choi HJ, Amunts K, Mohlberg H, Fink GR, Schleicher A, and Zilles K.Cytoarchitectonic mapping of the anterior ventral bank of the intraparietalsulcus in humans. Neuroimage E40: 401, 2002.

Cipolloni PB and Pandya DN. Cortical connections of the frontoparietalopercular areas in the rhesus monkey. J Comp Neurol 403: 431–458, 1999.

Coghill RC, Gilron I, and Iadarola MJ. Hemispheric lateralization ofsomatosensory processing. J Neurophysiol 85: 2602–2612, 2001.

Colebatch JG, Sayer RJ, Porter R, and White OB. Responses of monkeyprecentral neurons to passive movements and phasic muscle stretch: rele-vance to man. Electroencephalogr Clin Neurophysiol 75: 44–55, 1990.

Collins DF and Prochazka A. Movement illusions evoked by ensemblecutaneous input from the dorsum of the human hand. J Physiol 496:857–871, 1996.

Corballis PM, Funnell MG, and Gazzaniga MS. An evolutionary perspec-tive on hemispheric asymmetries. Brain Cogn 43: 112–117, 2000.

Costanzo RM and Gardner EP. A quantitative analysis of responses ofdirection-sensitive neurons in somatosensory cortex of awake monkeys.J Neurophysiol 43: 1319–1341, 1980.

Costanzo RM and Gardner EP. Multiple-joint neurons in somatosensorycortex of awake monkeys. Brain Res 214: 321–333, 1981.

Craig AD. How do you feel? Interoception: the sense of the physiologicalcondition of the body. Nat Rev Neurosci 3: 655–666, 2002.

Critchley M. The Parietal Lobes. London: Edward Arnold, 1953.Damasio AR. The Feeling of What Happens: Body and Emotion in the Making

of Consciousness. New York: Harcourt Brace, 1999.

Darian-Smith C, Darian-Smith I, Burman K, and Ratcliffe N. Ipsilateralcortical projections to areas 3a, 3b, and 4 in the macaque monkey. J CompNeurol 335: 200–213, 1993.

Devinsky O and D’Esposito M. Neurology of Cognitive and BehavioralDisorders. Oxford: Oxford 2004, p. 68–102.

Ehrsson HH, Fagergren E, and Forssberg H. Differential fronto-parietalactivation depending on force used in a precision grip task: an fMRI study.J Neurophysiol 85: 2613–2623, 2001.

Ehrsson HH, Geyer S, and Naito E. Imagery of voluntary movement offingers, toes, and tongue activates corresponding body-part-specific motorrepresentations. J Neurophysiol 90: 3304–3316, 2003.

Eickhoff S, Geyer S, Amunts K, Mohlberg H, and Zilles K. Cytoarchitec-tonic analysis and stereotaxic map of the human secondary somatosensorycortex. Neuroimage 20278, 2002.

Eidelberg D and Galaburda AM. Inferior parietal lobule. Divergent archi-tectonic asymmetries in the human brain. Arch Neurol 41: 843–852, 1984.

Fetz EE, Finocchio DV, Baker MA, and Soso MJ. Sensory and motorresponses of precentral cortex cells during comparable passive and activejoint movements. J Neurophysiol 43: 1070–1089, 1980.

Friston KJ, Ashburner J, Frith CD, Heather JD, and Frackowiak RSJ.Spatial registration and normalization of images. Hum Brain Mapp 2:165–188, 1995a.

Friston KJ, Holmes AP, Worsley KJ, Poline JB, Frith CD, and Frackow-iak RSJ. Statistical parametric maps in functional imaging: a general linearapproach. Hum Brain Mapp 2: 189–210, 1995b.

Gandevia SC. Illusory movements produced by electrical stimulation oflow-threshold muscle afferents from the hand. Brain 108: 965–981, 1985.

Gardner EP. Somatosensory cortical mechanisms of feature detection intactile and kinesthetic discrimination. Can J Physiol Pharmacol 66: 439–454, 1988.

Gardner EP and Costanzo RM. Properties of kinesthetic neurons in somato-sensory cortex of awake monkeys. Brain Res 214: 301–319, 1981.

Geschwind N and Galaburda AM. Cerebral lateralization. Biological mech-anisms, associations, and pathology. I. A hypothesis and a program forresearch. Arch Neurol. 42: 428–459, 1985.

Geyer S. The microstructural border between the motor and the cognitivedomain in the human cerebral cortex. Adv Anat Embryol Cell Biol 174:I–VIII, 1–89, 2004.

Geyer S, Grefkes C, Mohlberg H, and Zilles K. A 3D population map ofBrodmann’s area 6 (supplementary motor and premotor cortex) in humans.Abstr Soc Neurosci 262.2, 2002.

Geyer S, Ledberg A, Schleicher A, Kinomura S, Schomann T, Burgel U,Klingberg T, Larsson J, Zilles K, and Roland PE. Two different areaswithin the primary motor cortex of man. Nature 382: 805–807, 1996.

Ghosh S, Brinkman C, and Porter R. A quantitative study of the distributionof neurons projecting to the precentral motor cortex in the monkey (M.fascicularis). J Comp Neurol 259: 424–444, 1987.

Ghosh S and Gattera R. A comparison of the ipsilateral cortical projection todorsal and ventral subdivisions of the macaque premotor cortex. SomatosensMot Res 12: 359–378, 1995.

Godschalk M, Lemon RN, Kuypers HGJM, and Ronday HK. Corticalafferents and efferents of monkey postarcuate area: an anatomical andelectrophysiological study. Exp Brain Res 56: 410–424, 1984.

Goodwin GM, McCloskey DI, and Matthews PBC. The contribution ofmuscle afferents to kinesthesia shown by vibration induced illusions ofmovement and by the effects of paralysing joint afferents. Brain 95:705–748, 1972a.

Goodwin GM, McCloskey DI, and Matthews PBC. Proprioceptive illusionsinduced by muscle vibration: contribution by muscle spindles to perception?Science 175: 1382–1384, 1972b.

Grefkes C, Geyer S, Schormann T, Roland PE, and Zilles K. Humansomatosensory area 2: observer-independent cytoarchitectonic mapping,interindividual variability, and population map. Neuroimage 14: 617–631,2001.

Guldin WO, Akbarian S, and Grusser OJ. Cortico-cortical connections andcytoarchitectonics of the primate vestibular cortex: a study in squirrelmonkeys (Saimiri sciureus). J Comp Neurol 326: 375–401, 1992.

Halligan PW, Marshall JC, and Wade DT. Three arms: a case study ofsupernumerary phantom limb after right hemisphere stroke. J Neurol Neu-rosurg Psych 56: 159–166, 1993.

Hore J, Preston JB, Durkovic RG, and Cheney PD. Responses of corticalneurons (area 3a and 4) to ramp stretch of hindlimb muscles in the baboon.J Neurophysiol 39: 484–500, 1976.

1032 NAITO ET AL.


on February 9, 2007

jn.physiology.orgD

ownloaded from


Huerta MF and Pons TP. Primary motor cortex receives input from area 3ain macaque. Brain Res 537: 367–371, 1990.

Hulliger M, Nordh E, Thelin AE, and Vallbo AB. The responses of afferentfibers from the glabrous skin of the hand during voluntary finger movementsin man. J Physiol 291: 233–249, 1979.

Hyvarinen J. Regional distribution of functions in parietal association area 7of the monkey. Brain Res 206: 287–303, 1981.

Hyvarinen J. The posterior parietal lobe of the primate brain. Physiol Rev 62:1060–1129, 1982a.

Hyvarinen J. Studies of Brain Function. The Parietal Cortex of Monkey andMan. Berlin: Springer-Verlag, 1982b, p. 48–139.

Hyvarinen J and Poranen A. Movement-sensitive and direction and orien-tation-selective cutaneous receptive fields in the hand area of the post-central gyrus in monkeys. J Physiol 283: 523–537, 1978.

Hyvarinen J and Shelepin Y. Distribution of visual and somatic functions inthe parietal associative area 7 of the monkey. Brain Res 169: 561–564, 1979.

Iwamura Y. Bilateral receptive field neurons and callosal connections in thesomatosensory cortex. Philos Trans R Soc Lond B Biol Sci 355: 267–273,2000.

Iwamura Y, Iriki A, and Tanaka M. Bilateral hand representation in thepostcentral somatosensory cortex. Nature 369: 554–556, 1994.

Iwamura Y and Tanaka M. Postcentral neurons in hand region of area 2:their possible role in the form discrimination of tactile objects. Brain Res150: 662–666, 1978.

Iwamura Y and Tanaka M. Representation of reaching and grasping in themonkey postcentral gyrus. Neurosci Lett 214: 147–150, 1996.

Iwamura Y, Tanaka M, Sakamoto M, and Hikosaka O. Functional subdi-visions representing different finger regions in area 3 of the first somato-sensory cortex of the conscious monkey. Exp Brain Res 51: 315–326, 1983.

Iwamura Y, Tanaka M, Sakamoto M, and Hikosaka O. Rostrocaudalgradients in the neuronal receptive field complexity in the finger region ofthe alert monkey’s postcentral gyrus. Exp Brain Res 92: 360–368, 1993.

Jennings VA, Lamour Y, Solis H, and Fromm C. Somatosensory cortexactivity related to position and force. J Neurophysiol 49: 1216–1229, 1983.

Jones EG, Coulter JD, and Hendry SHC. Intracortical connectivity ofarchitectonic fields in the somatic sensory, motor and parietal cortex ofmonkeys. J Comp Neurol 181: 291–348, 1978.

Jones EG and Powell TPS. An anatomical study of converging sensorypathways within the cerebral cortex of the monkey. Brain 93: 793–820,1970.

Karnath HO. New insights into the functions of the superior temporal cortex.Nat Neurosci 2: 568–576, 2001.

Karnath HO, Ferber S, and Himmelbach M. Spatial awareness is a functionof the temporal not the posterior parietal lobe. Nature 411: 950–953, 2001.

Kawashima R, Watanabe J, Kato T, Nakamura A, Hatano K, SchormannT, Sato K, Fukuda H, Ito K, and Zilles K. Direction of cross-modalinformation transfer affects human brain activation: a PET study. EurJ Neurosci 16: 137–144, 2002.

Ledberg A, O’Sullivan BT, Kinomura S, and Roland PE. Somatosensoryactivations of the parietal operculum of man. A PET study. Eur J Neurosci7: 1934–1941, 1995.

Leichnetz GR. Afferent and efferent connections of the dorsolateral precentralgyrus (area 4, hand/arm region) in the macaque monkey, with comparisonsto area 8. J Comp Neurol 254: 460–492, 1986.

Lemon RN. Functional properties of monkey motor cortex neurones receivingafferent input from the hand and fingers. J Physiol 311: 497–519, 1981.

Lemon RN, Hanby JA, and Porter R. Relationship between the activity ofprecentral neurones during active and passive movements in consciousmonkeys. Proc R Soc Lond B Biol Sci 194: 341–373, 1976.

Lemon RN and Porter R. Afferent input to movement-related precentralneurones in conscious monkeys. Proc R Soc Lond B Biol Sci 194: 313–339,1976.

Lemon RN and Van Der Burg J. Short-latency peripheral inputs to thalamicneurons projecting the motor cortex in the monkey. Exp Brain Res 36:445–462, 1979.

McGonigle DJ, Hanninen R, Salenius S, Hari R, Frackowiak RSJ, andFrith CD. Whose arm is it anyway? An fMRI case study of supernumeraryphantom limb. Brain 125: 1265–1274, 2002.

Meador KJ, Loring DW, Feinberg TE, Lee GP, and Nichols ME. Anosog-nosia and asomatognosia during intracarotid amobarbital inactivation. Neu-rology 55: 816–820, 2000.

Mohlberg H, Lerch J, Amunts K, Evans A, and Zilles K. Probabilisticcytoarchitectonic maps transformed into MNI space (Abstract). Hum BrainMapp 19: 905, 2003.

Mountcastle VB and Powell TPS. Central nervous mechanisms subservingposition sense and kinesthesia. Bull Johns Hopkins Hosp 105: 173–200,1959.

Naito E. Sensing limb movements in the motor cortex: how humans sense limbmovement. Neuroscientist 9: 73–82, 2004.

Naito E and Ehrsson HH. Kinesthetic illusion of wrist movement activatesmotor-related areas. Neuroreport 12: 3805–3809, 2001.

Naito E, Ehrsson HH, Geyer S, Zilles K, and Roland PE. Illusory armmovements activate cortical motor areas: a PET study. J Neurosci 19:6134–6144, 1999.

Naito E, Kochiyama T, Kitada R, Nakamura S, Matsumura M, YonekuraY, and Sadato N. Internally simulated movement sensations during motorimagery activate the cortical motor areas and the cerebellum. J Neurosci 22:3683–3691, 2002a.

Naito E, Roland PE, and Ehrsson HH. I feel my hand moving: a new roleof the primary motor cortex in somatic perception of limb movement.Neuron 36: 979–988, 2002b.

Neal JW, Pearson RC, and Powell TP. The corticocortical connections ofarea 7b, PF, in the parietal lobe of the monkey. Brain Res 419: 341–346,1987.

Neal JW, Pearson RC, and Powell TP. The ipsilateral corticocortical con-nections of area 7 with the frontal lobe in the monkey. Brain Res 509:31–40, 1990a.

Neal JW, Pearson RC, and Powell TP. The ipsilateral cortico-corticalconnections of area 7b, PF, in the parietal and temporal lobes of the monkey.Brain Res 524: 119–132, 1990b.

Oldfield RC. The assessment and analysis of handedness: the Edinburghinventory. Neuropsychologia 9: 97–113, 1971.

Passingham RE. The specialization of the human cerebral cortex. In: Com-parative Neuropsychology, edited by Milner AD. Oxford: Oxford, 1998, p.271–298.

Phillips CG, Powell TPS, and Wiesendanger M. Projection from lowthreshold muscle afferents of hand and forearm to area 3a of baboon’scortex. J Physiol 217: 419–446, 1971.

Picard N and Strick PL. Imaging the premotor areas. Curr Opin Neurobiol11: 663–672, 2001.

Pons TP, Garraghty PE, and Mishkin M. Serial and parallel processing oftactual information in somatosensory cortex of rhesus monkey. J Neuro-physiol 68: 518–527, 1992.

Pons TP and Kaas JH. Corticocortical connections of area 2 of somatosen-sory cortex in macaque monkeys: a correlative anatomical and electrophys-iological study. J Comp Neurol 248: 313–335, 1986.

Porter R and Lemon RN. Inputs from the peripheral receptors to motor cortexneurones. In: Corticospinal Function and Voluntary Movement. New York:Oxford, 1993, p. 247–272.

Price CJ and Friston KJ. Cognitive conjunction: a new approach to brainactivation experiments. NeuroImage 5: 261–270, 1997.

Preuss TM and Goldman-Rakic PS. Connections of the ventral granularfrontal cortex of macaques with perisylvian premotor and somatosensoryareas: anatomical evidence for somatic representation in primate frontalassociation cortex. J Comp Neurol 282: 293–316, 1989.

Romaiguere P, Anton JL, Roth M, Casini L, and Roll JP. Motor andparietal cortical areas both underlie kinaesthesia. Cogn Brain Res 16:74–82, 2003.

Roland PE. Dynamic depolarization fields in the cerebral cortex. TrendsNeurosci 25: 183–190, 2002.

Roland PE, O’Sullivan B, and Kawashima R. Shape and roughness activatedifferent somatosensory areas in the human bran. Proc Natl Acad Sci USA95: 3295–3300, 1998.

Roland PE and Zilles K. The developing european computerized human braindatabase for all imaging modalities. Neuroimage 4: 39–47, 1996a.

Roland PE and Zilles K. Functions and structures of the motor cortices inhumans. Curr Opin Neurobiol 6: 773–781, 1996b.

Roland PE and Zilles K. Structural divisions and functional fields in thehuman cerebral cortex. Brain Res Rev 26: 87–105, 1998.

Roland PE, Svensson G, Lindeberg T, Risch T, Baumann P, Dehmel A,Frederiksson J, Halldorson H, Forsberg L, Young J, and Zilles K. Adatabase generator for human brain imaging. Trends Neurosci 24: 562–564,2001.

Roll JP and Vedel JP. Kinaesthetic role of muscle afferent in man, studied bytendon vibration and microneurography. Exp Brain Res 47: 177–190, 1982.

Roll JP, Vedel JP, and Ribot E. Alteration of proprioceptive messagesinduced by tendon vibration in man: a microneurograpic study. Exp BrainRes 76: 213–222, 1989.



on February 9, 2007

jn.physiology.orgD

ownloaded from


Rosen I and Asanuma H. Peripheral afferent inputs to the forelimb area of themonkey motor cortex: input-output relations. Exp Brain Res 14: 257–273, 1972.

Rouiller EM, Babalian A, Kazennikov O, Moret V, Yu XH, and Wiesen-danger M. Transcallosal connections of the distal forelimb representationsof the primary and supplementary motor cortical areas in macaque monkeys.Exp Brain Res 102: 227–243, 1994.

Salimi I, Brochier T, and Smith AM. Neuronal activity in somatosensorycortex of monkeys using a precision grip. I. Receptive fields and dischargepatterns. J Neurophysiol 81: 825–834, 1999.

Schleicher A, Amunts K, Geyer S, Morosan P, and Zilles K. Observer-independent method for microstructure parcellation of cerebral cortex: aquantitative approach to cytoarchitectonics. Neuroimage 9: 165–177, 1999.

Schmahmann JD, Doyon J, Toga AW, Petrides M, and Evans AC. MRIAtlas of the Human Cerebellum. San Diego: Academic, 2000.

Schormann T and Zilles K. Three-dimensional linear and nonlinear transfor-mations: an integration of light microscopical and MRI data. Hum BrainMapp 6: 339–347, 1998.

Schwarz DWF, Deecke L, and Fredrickson JM. Cortical projection of groupI muscle afferents to area 2, 3a and the vestibular field in the rhesus monkey.Exp Brain Res 17: 516–526, 1973.

Sellal F, Renaseau-Leclerc C, and Labrecque R. The man who had six arms.Analysis of supernumerary phantom limbs after right hemisphere stroke.Rev Neurol (Paris) 152: 190–195, 1996.

Seltzer B and Pandya DN. Afferent cortical connections and architectonics ofthe superior temporal sulcus and surrounding cortex in the rhesus monkey.Brain Res 149: 1–24, 1978.

Springer JA, Binder JR, Hammeke TA, Swanson SJ, Frost JA, BellgowanPSF, Brewer CC, Perry HM, Morris GL, and Mueller WM. Languagedominance in neurologically normal and epilepsy subjects. Brain 122:2033–2045, 1999.

Stepniewska I, Preuss TM, and Kaas JH. Architectonics, somatotopicorganization, and ipsilateral cortical connections of the primary motor area(M1) of owl monkeys. J Comp Neurol 330: 238–271, 1993.

Strick PL and Preston JB. Two representations of the hand in area 4 of aprimate. II. Somatosensory input organisation. J Neurophysiol 48: 150–159,1982.

Tanji J. The supplementary motor area in the cerebral cortex. Neurosci Res19: 251–268, 1994.

Taoka M, Toda T, and Iwamura Y. Representation of the midline trunk,bilateral arms, and shoulders in the monkey postcentral somatosensorycortex. Exp Brain Res 123: 315–322, 1998.

Taoka M, Toda T, Iriki A, Tanaka M, and Iwamura Y. Bilateral receptivefield neurons in the hindlimb region of the postcentral somatosensory cortexin awake macaque monkeys. Exp Brain Res 134: 139–146, 2000.

Talairach J and Tournoux P. A Co-Planar Stereotaxic Atlas of a HumanBrain. New York: Thieme, 1988.

Vikingstad EM, George KP, Johnson AF, and Cao Y. Cortical languagelateralization in right handed normal subjects using functional magneticresonance imaging. J Neurol Sci 175: 17–27, 2000.

Wada J and Rasmussen T. Intracarotid injection of sodium amytal for thelateralization of cereberal speech dominace: experimental and clinical ob-servations. J Neurosurg 17: 266–282, 1960.

Warren S, Hamalainen HA, and Gardner EP. Objective classification ofmotion- and direction-sensitive neurons in primary somatosensory cortex ofawake monkeys. J Neurophysiol 56: 598–622, 1986.

Weiller C, Juptner M, Fellows S, Rijntjes M, Leonhardt G, Kiebel S,Muller S, Diener HC, and Thilmann AF. Brain representation of activeand passive movements. Neuroimage 4: 105–110, 1996.

Wolpaw JR. Correlation between task-related activity and responses to per-turbation in primate sensorimotor cortex. J Neurophysiol 44: 1122–1138,1980.

Wong YC, Kwan HC, MacKay WA, and Murphy JT. Spatial organizationof precentral cortex in awake primates. I. Somatosensroy inputs. J Neuro-physiol 41: 1107–1119, 1978.

Worsley KJ and Friston KJ. A test for a conjunction. Stat Prob Lett 47:135–140, 2000.

Young JP, Herath P, Eickhoff S, Choi HJ, Grefkes C, Zilles K, and RolandPE. Somatotopy and attentional modulation of the human parietal andopercular regions. J Neurosci 24: 5391–5399, 2004.

Zilles K and Palomero-Gallagher N. Cyto-, myelo-, and recpetor architec-tonics of the human parietal cortex. Neuroimage 14: S8–S20, 2001.

1034 NAITO ET AL.


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ownloaded from


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