Cerebral Cortex August 2007;17:1800--1811
doi:10.1093/cercor/bhl090
Advance Access publication October 10, 2006
The Somatotopic Organization of
Cytoarchitectonic Areas on the Human
Parietal Operculum
The secondary somatosensory cortex (SII) of nonhuman primates is
located on the parietal operculum. In the monkey, electrophysiological and connectivity tracing studies as well as histological
investigations provide converging evidence for 3 distinct cortical
areas (SII, PV, and VS) within this region, each of which contains
a complete somatotopic map. Although the equivalency of the
parietal operculum as the location of SII between humans and
nonhuman primates is undisputed, the internal organization of the
human SII region is still largely unknown. Based on their
topography, we have previously argued that the cytoarchitectonic
areas OP 1, OP 4, and OP 3 may constitute the human homologues
of areas SII, PV, and VS, respectively. To test this hypothesis, we
here examined (using functional magnetic resonance imaging) the
somatotopic organization of the human parietal operculum by
applying tactile stimulation to the skin at 4 different locations on
either side of the body (face, hands, trunk, and legs). The locations
of the resulting activation foci were then compared with the
cytoarchitectonic maps of this region. Data analysis revealed 2
somatotopic body representations on the lateral operculum in areas
OP 1 and OP 4. The functional border between these 2 body maps
was defined by a mirror reversal in the somatotopic arrangement
and coincided with the cytoarchitectonically defined border between these 2 areas. This somatotopic arrangement closely
matches that described for SII and PV in nonhuman primates. The
data also suggested a third somatotopic map located deeper inside
the Sylvian fissure in area OP 3. Based on the observed topographic
arrangement and their functional response characteristics, we
conclude that cytoarchitectonic areas OP1, OP 4, and OP 3 on the
human parietal operculum constitute the human homologues of
primate areas SII, PV, and VS, respectively.
Keywords: brain, fMRI, homology, mapping, SII, somatosensory cortex
Introduction
The concept of a secondary somatosensory cortex (SII) located
ventrally to the primary somatosensory cortex (SI) has been
introduced more than 60 years ago based on electrophysiological studies in cats (Adrian 1940). Over the following decades,
corresponding areas were described in virtually all examined
mammals including nonhuman primates (Burton 1986). In
anthropoid primates, SII is located on the upper bank of the
Sylvian fissure, that is, the parietal operculum. A correspondingly located human SII region was first described by direct
electrical stimulation (Penfield and Jasper 1954). Subsequently,
studies using evoked potentials (Woolsey et al. 1979) and
positron emission tomography (PET) (Fox et al. 1987; Burton
et al. 1993) confirmed these findings. Since then SII activations
have been reported consistently for a wide range of experimental conditions, for example, light touch and pain (cf., review
Ó The Author 2006. Published by Oxford University Press. All rights reserved.
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Simon B. Eickhoff1,2,3, Christian Grefkes1,3,4, Karl Zilles1,2,3
and Gereon R. Fink1,3,4,5
1
Institut für Medizin, Forschungszentrum Jülich, Jülich,
Germany, 2C. and O. Vogt Institut für Hirnforschung,
Universität Düsseldorf, Germany, 3Brain Imaging Centre West,
Jülich, Germany, 4Neurologische Klinik—Kognitive
Neurologie, Universitätsklinikum RWTH Aachen, Germany
and 5Klinik und Poliklinik für Neurologie, Klinikum der
Universität zu Köln, Köln, Germany
and meta-analysis by Eickhoff, Amunts, et al. 2006), but also for
more complex tasks such as tactile attention (Burton and
Sinclair 2000; Lam et al. 2001) and sensory-motor integration
(Inoue et al. 2002; Wasaka et al. 2005). In contrast to SI, the
human parietal operculum commonly shows bilateral activation
even with unilateral peripheral stimulation (Ruben et al. 2001;
Del Gratta et al. 2002; Bingel et al. 2003; Young et al. 2004). This
observation is in good accordance with SII response characteristics in nonhuman primates (Robinson and Burton 1980a;
Burton et al. 1995; Kaas and Collins 2003).
Nevertheless, the concept of ‘‘SII’’ has changed considerably
over the last 15 years. Electrophysiological and tracing studies as
well as histological investigations in a variety of species have
provided converging evidence that the SII region can be
subdivided into several distinct areas (Cusick et al. 1989;
Krubitzer and Kaas 1990, 1993; Burton et al. 1995; Krubitzer,
Clarey, et al. 1995; Huffman et al. 1999; Slutsky et al. 2000). In
this context, one important feature of a cortical area is the
presence of a separate, complete somatotopic map (Fink et al.
1997). The idea behind this approach is the assumption that
each part of the body is represented only once in each area,
a claim that is strongly supported by the role these topographic
maps seem to play in the development of sensory cortices (Kaas
1997, 2000). To date, the most commonly used nomenclature
(Kaas and Collins 2003) for SII subareas in nonhuman primates
is as follows (Fig. 1): The area immediately ventral to SI is the
‘‘parietal ventral area’’ (PV). PV is caudally followed by ‘‘area SII,’’
which must be differentiated from the earlier defined ‘‘SII
region’’ as the term SII is used for the whole region as well as
for an individual area within it. SII and PV each contain a full
somatotopic map. These maps constitute mirror images of each
other, bordering at the representations of the most distal parts
of the body: face (lateral), hands (intermediate), and feet
(medial). More proximal parts of the body, for example,
shoulder, trunk, and legs (which are considered a proximal
body part because they are distally followed by the feet) are
represented further apart from this border in the anterior part
of PV and the posterior aspect of SII (Burton et al. 1995;
Krubitzer, Clarey, et al. 1995). A third SII subregion, the ‘‘ventral
somatosensory area’’ (VS), has been described in the depth of
the Sylvian fissure medial to SII and PV. VS contains a crude
rostrocaudal somatotopic map in which the head is represented
most anteriorly (Cusick et al. 1989; Krubitzer and Calford 1992;
Qi et al. 2002).
An homologous subdivision of the human SII was then
proposed (Disbrow et al. 2000) using functional magnetic
resonance imaging (fMRI). Disbrow et al. provided data which
suggested that the human SII region may contain several
somatotopically organized areas by demonstrating multiple
as on the existing evidence for their functional homology
(Young et al. 2004; Naito et al. 2005; Eickhoff, Lotze, et al.
2006; Eickhoff, Weiss, et al. 2006).
The aim of the present study was to examine whether the
somatotopic organization of OP 1, 3, and 4 corresponds to that
of SII, PV, and VS in nonhuman primates. We accordingly
analyzed the functional responses elicited on the parietal
operculum by tactile stimulation of 4 body parts: face, hand,
trunk, and leg. These locations were chosen based on the
somatotopic organization of the SII region in nonhuman
primates: In macaques, head and hands are represented at the
border between there areas. They may therefore be used to
define the functional border between the human homologues
of these areas. The opercular representation of the trunk and
the legs (instead of the feet, which are also represented at the
functional border between SII and PV) was analyzed because
these more proximal sites are represented at the anterior
border of PV and the posterior border of area SII, respectively.
They should thus have 2 clearly separable representations in
their human homologues. Furthermore, if the human parietal
operculum is organized similar to that of nonhuman primates,
the head should be represented lateral to the hand, whereas the
trunk should be represented lateral to the leg.
Materials and Methods
Figure 1. The somatotopic organization of the cortical areas in the lateral sulcus of
nonhuman primates (adopted and summarized from Krubitzer and Kaas 1990;
Krubitzer and Calford 1992; Burton et al. 1995; Krubitzer, Clarey, et al. 1995; Qi et al.
2002). Three distinct anatomical areas (SII, PV, and VS) have consistently been defined
in the ‘‘SII region’’ in a wide variety of species. Each of these areas has a separate and
complete representation of the whole skin.
activation foci within the SII region for various body parts.
Further evidence for multiple areas in the human SII region was
provided by fMRI and PET studies showing multiple opercular
activation foci (Burton et al. 1993; Ledberg et al. 1995; Ferretti
et al. 2003).
A recent cytoarchitectonic study of our own group (Eickhoff,
Amunts, et al. 2006; Eickhoff, Schleicher, et al. 2006), based
on histological examination in a series of postmortem brains,
identified 4 distinct cytoarchitectonic areas (OP 1--4) on the
human parietal operculum. Topographically OP 4 corresponds
to primate PV as both are located near to the superficially
exposed cortical surface within the Sylvian fissure bordering SI.
OP 1 is located caudally to OP 4 and thus seems to constitute
the human homologue of area SII. Like macaque areas SII and
PV, OP 4 and OP 1 share a common border running in a medial
to lateral direction. In contrast, OP 3 is located deeper in the
Sylvian fissure than both aforementioned areas. It is thus the
most likely candidate for a human homologue of area VS. Finally,
OP 2 is not part of the SII but rather comparable with the
parietal-insular vestibular cortex (PIVC) of nonhuman primates
(Eickhoff, Weiss, et al. 2006).
Please note that in order to allow the reader a better
orientation and avoid unnecessary confusion due to differences
in nomenclature, we will use the terms OP 1 (SII), OP 2 (PIVC),
OP 3 (VS), and OP 4 (PV) throughout the text. This denotation is
based on the established topological correspondence between
these 4 cytoarchitectonic fields on the human parietal operculum (Eickhoff, Amunts, et al. 2006; Eickhoff, Schleicher, et al.
2006) and the respective areas in nonhuman mammals, as well
Subjects and Stimulation
14 healthy subjects (7 males, mean age 25.6 ± 3.4 years) with no history
of neurological or psychiatric illness gave informed consent. All subjects
were strongly right handed as assessed by the Edinburgh handedness
inventory (Oldfield 1971). The study was approved by the ethics
committee of the Medical Faculty, RWTH Aachen, Germany.
Somatosensory stimulation was applied to the face, hands, trunk, and
legs. The extent of the stimulated skin areas is illustrated in Figure 2.
Each location was separately stimulated on either the left or the right
side of the body resulting in 8 separate conditions. Stimulation was
performed manually by brushing the subject’s skin with a sponge in
a back-and-forth manner with a frequency of approximately 2 Hz
because this method was previously shown to be highly effective in
evoking SII activations in both humans (Disbrow et al. 2000) and
nonhuman primates (Robinson and Burton 1980b; Krubitzer and Kaas
1990; Krubitzer, Clarey, et al. 1995). Upon debriefing after the
experiment, all subjects reported that the stimuli were easy to perceive
but had not caused any pain. The fMRI paradigm consisted of 8 sessions
of 11 stimulation cycles. Each cycle consisted of approximately 18-s
stimulation followed by 18 s rest. In each of the 8 sessions, a different
anatomical site was stimulated. The order of the experimental sessions
was pseudorandomized across subjects.
FMRI Procedure and Image Preprocessing
Functional magnetic resonance (MR) images were acquired on a Siemens
Sonata 1.5-T whole-body scanner (Erlangen, Germany) using blood
oxygen level--dependent (BOLD) contrast (gradient-echo echo planar
imaging [EPI] pulse sequence, time repetition = 3 s, resolution = 3.1 3
3.1 3 3.1 mm, 30 axial slices for whole-brain coverage). Each session
consisted of 132 EPI images. The fMRI scanning was preceded by the
acquisition of 4 dummy images allowing the MR scanner to reach
a steady state which were discarded prior to further analysis. Additional
high-resolution anatomical images (voxel size 1 3 1 3 1 mm) were
acquired using a standard T1-weighted 3-dimensional magnetizationprepared rapid gradient-echo sequence. Images were analyzed on
a Pentium 4 Windows XP system using SPM5 (http://www.fil.ion.ucl.ac.
uk/spm). The EPI images were corrected for head movement between
scans by an affine registration (Ashburner and Friston 2003b). One
subject was removed from further analysis due to excessive head
motion (more than 1.5 mm movement between scans). The T1 scan was
coregistered to the mean of the realigned EPIs and subsequently
Cerebral Cortex August 2007, V 17 N 8 1801
voxels as Bayesian prior (Friston 2002; Friston, Glaser, et al. 2002;
Friston, Penny, et al. 2002; Friston and Penny 2003a, 2003b). The
resulting posterior probability maps were thresholded at a probability
of 99.99% for an effect size greater than 2 prior standard deviations
(c threshold). That is, only those voxels were considered as significantly
activated that had parameter estimates larger than c with at least 99.99%
confidence. The rationale for using the prior standard deviation as the
effect size threshold c is that it equates to a ‘‘background noise level,’’
that is, to a level of activation that is generic to the brain as a whole. The
chosen threshold thus allows directing Bayesian inference to only show
those voxels that are almost certainly more active than this generic
response (Friston, Glaser, et al. 2002; Friston and Penny 2003a, 2003b).
For the considerably weaker activations resulting from stimulation of
trunk and legs, the threshold was lowered to 99% confidence for
activation greater than background noise.
In order to delineate those parts of the opercular cortex that were
tuned most specifically to input from the examined body parts, we
subsequently identified those clusters of voxels where stimulation of
a particular body part (irrespectively of the stimulated side) was more
likely to evoke activation than stimulation of any of the 3 other examined
body parts. First, the joint probability for activation following either leftor right-sided stimulation of a particular body parts was computed for
each voxel to quantify its responsiveness to stimulation of each body
parts. To delineate the core of the SII representation of the head, hands,
trunk, and legs, these joint probabilities were then compared across
stimulation sites, resulting in a maximum likelihood representation.
Each voxel was hereby assigned to that body part whose stimulation
resulted in the highest probability for activation at this particular voxel,
given that the joint posterior probability for activation following left- or
right-sided stimulation was at least 99%. The resulting clusters of
maximum likelihood representation thus define those parts of the SII
region, which were most responsive to stimulation of the respective
body part. It has to be noted that the respective clusters are mutually
exclusive because in a particular voxel, only a single body part can be
represented most likely, although there will be some apparent overlap
in the surface projection used to illustrate the location of these regions.
Figure 2. Overview on the skin surface stimulated for each of the different body part
conditions. The areas shaded in darker gray represent the portions of the body that
were stimulated. The arrows mark the direction of stimulation. Face and trunk were
stimulated with a sponge rubbed in a back-and-forth motion in a rostrocaudal direction.
For stimulation of the regions on the limbs (hands and leg), the sponge was rubbed in
a back-and-forth motion from proximal to distal.
normalized to the Montreal Neurological Institute (MNI) single-subject
template (Evans et al. 1992; Collins et al. 1994; Holmes et al. 1998) using
linear proportions and a nonlinear sampling algorithm (Ashburner and
Friston 2003a, 2003c). The resulting normalization parameters were
then also applied to the EPI volumes. These were hereby transformed
into standard stereotaxic space and resampled at 1.5 3 1.5 3 1.5 mm
voxel size. The normalized images were spatially smoothed using a 6mm full width half maximum Gaussian kernel to meet the statistical
requirements of the general linear model and to compensate for residual
anatomical variations across subjects.
Statistical Analysis
The data were analyzed in the context of the general linear model
employed by SPM5 (Kiebel and Holmes 2003). Each experimental
condition was modeled using a boxcar reference vector convolved with
a canonical hemodynamic response function. Low-frequency signal
drifts were filtered using a set of discrete cosine functions with a cutoff
period of 72 s. No global scaling was applied. The main effects for the 8
stimulation conditions were computed by applying appropriate baseline
contrasts.
The corresponding contrasts from different subjects were then
analyzed in a second-level Bayesian mixed-effects model to allow
inference to the general population (Penny and Holmes 2003) using
the probabilistic empirical Bayes algorithm implemented in SPM5. This
algorithm calculates the conditional distribution for the parameter
estimates (across subjects) at each voxel using the variance across
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Comparison with Cytoarchitectonic Data
The localization of significant activations with respect to cytoarchitectonic areas was analyzed on the basis of a summary map (maximum
probability map) that identifies the most likely anatomical area at each
voxel of the MNI single-subject template (Eickhoff et al. 2005; Eickhoff,
Heim, et al. 2006). The definition of this map is based on probabilistic
cytoarchitectonic maps derived from the analysis of cortical areas in
a sample of 10 human postmortem brains (Schleicher et al. 2005), which
were subsequently normalized to the MNI reference space (Amunts
et al. 2004; Eickhoff, Schleicher, et al. 2006). To quantify the correspondence between anatomical and the functional data, the maximum
likelihood clusters defined above were then compared with the
probabilistic maps of the parietal operculum (Eickhoff et al. 2005;
Eickhoff, Amunts, et al. 2006) using the SPM Anatomy toolbox (www.
fz-juelich.de/ime/spm_anatomy_toolbox).
Probability of Activation within OP 1--4
This analysis represented a complementary approach to the justdescribed identification of the significant activation foci and was carried
out in order to characterize the responsiveness of OP 1--4 to tactile
stimulation. First, the mean posterior probabilities for activation greater
than background noise following the 8 experimental conditions (4 body
parts 3 2 sides) were calculated within each area. The probabilities for
activation of this area following stimulation of a specific body part
regardless of the stimulated side were subsequently derived by the
union of the probabilities for left- and right-sided stimulations. These
probabilities were then statistically compared by means of a 2-way
analysis of variance (ANOVA). The 2 factors of this ANOVA were ‘‘area’’
and ‘‘body part.’’ The level of significance was P < 0.05. If the effect of
a factor was significant, we used a subsequent pairwise multiple
comparison procedure (Tukey test) to isolate the conditions in which
the levels of this factor differed significantly (P < 0.05, corrected for
multiple comparisons).
Results
We will first describe the significant activations on the parietal
operculum separately for each body part. To assess the
effectiveness and specificity of applied stimulation, we also
examined the evoked activation in the SI, that is, areas 3a, 3b, 1,
and 2 (Geyer et al. 1999, 2000; Grefkes et al. 2001). We will then
combine these individual results into a somatotopic map of the
human parietal operculum and analyze the mean probabilities
for activations following somatosensory stimulation in areas
OP 1--4.
Face
As expected (Boling et al. 2002; Iannetti et al. 2003), the face
representation within SI was located bilaterally on the inferior
lateral aspect of the postcentral gyrus, close to but clearly
separated from the Sylvian fissure (Fig. 3A,C).
The contralateral SII activation to left- and right-sided face
stimulations consisted of 2 clusters on the lateral parietal
operculum (Fig. 3B,D). One of them was found at the lateral
aspect of the border between OP 1 (SII) and OP 4 (PV), the
other was located more posteriorily and medially, that is, within
OP 1 (SII). In the left face condition, the anterior lateral cluster
showed a second maximum located in OP 3 (VS) (Fig. 3D).
Stimulation of the left face also resulted in a significant cluster of
activation on the left lateral operculum at the border between
OP 1 (SII) and OP 4 (PV) (Fig. 3B). Stimulation of the right face,
on the other hand, caused more scattered activation on the
ipsilateral operculum (Fig. 3B). Four of these clusters were
located in the superficial parts of OP 1 (SII) and OP 4 (PV) while
the fifth cluster was observed more medially within OP 4 (PV)
extending into OP 3 (VS) (24% of its volume were allocated to
OP 3 [VS]).
Hands
The location of the anterior parietal activations (Fig. 4A,C) was
in good accordance with the well-established location of the
‘‘SI hand area’’ between the middle and superior third of the
postcentral gyrus (Bingel et al. 2003; Blankenburg et al. 2003;
Young et al. 2004).
Stimulation of both hands resulted in a single yet extended
cluster of activation in contralateral SII. These clusters were
located medially to the activation observed for face stimulation.
On both hemispheres, the opercular hand activations were
located at the border between OP 1 (SII) and OP 4 (PV) (Fig.
4B,D). Moreover, both activations also extended into OP 3 (VS)
(25% of cluster volume in the left hand condition, 20% in the
right hand condition). Ipsilateral activation, on the other hand,
was much smaller and only significant at a more lenient
threshold (99% confidence) where it appeared at the same
location as the contralateral activations.
Figure 3. (A) Main effect of right face stimulation on the SI (cytoarchitectonic areas: Brodmann areas 3a, 3b, 1, and 2) displayed on the MNI single-subject template. Areas shown
had conditional estimates that could be declared as active greater than background noise with at least 99% confidence. (B) Main effect of right face stimulation on the parietal
operculum, that is, the region of SII. The statistically significant clusters of activations are shown superimposed on the cytoarchitectonic maximum probability map (MPM) of areas
OP 1--4 rendered onto the MNI single-subject template. The temporal lobes were removed for display purposes. Activation clusters shown on this rendering had conditional
estimates that could be declared as active greater than background noise with at least 99.99% confidence. (C) and (D) same as (A) and (B) showing the main effects of left face
stimulation on the SI and the parietal operculum.
Cerebral Cortex August 2007, V 17 N 8 1803
Figure 4. (A) Main effect of right hand stimulation on the SI rendered onto the MNI single-subject template (99% confidence for activation greater than background noise).
(B) Main effect of right hand stimulation on the parietal operculum. The statistically significant activations in the SII region as well as the cytoarchitectonic maximum probability map
of OP 1--4 are shown on a surface rendering of the MNI single-subject template (shown without temporal lobes for displaying purposes). The confidence threshold of activation
greater than background noise was 99.99%. (C) and (D) same as (A) and (B) showing the main effects of left hand stimulation on the SI and the parietal operculum.
Trunk
As in previous studies (Itomi et al. 2000; Fabri et al. 2005), tactile
trunk stimulation evoked bilateral activation in SI, which was
located medially and superior to the SI hand area (Fig. 5A,C).
Following right trunk stimulation, 2 distinct activation clusters were identified on the contralateral operculum (Fig. 5B).
The contralateral SII activation following left-sided stimulation
was considerably weaker but in a similar location (Fig. 5D). These
2 clusters on the respective contralateral sides were located in
the superficial part of the parietal operculum similar to those
observed for face stimulation. However, instead of being located
at the border between OP 1 (SII) and OP 4 (PV), the trunk
activations were located at the anterior border of OP 4 (PV) and
the posterior border of OP 1 (SII), that is, to either side of the
head representation. Ipsilateral to the stimulated side, the same
pattern was observed for the stimulation of the right trunk (Fig.
5B). Stimulation of the left trunk, on the other hand, failed to
evoke activation in left OP 4 (PV), that is, the anterior focus was
missing (Fig. 5D).
Stimulation Leg
In SI, the legs were represented even more medially than the
trunk (Fig. 6A,C). Their location close to the midline, extending
into the interhemispheric fissure, was similar to the one
described in previous imaging studies (Del Gratta et al. 2000;
Ruben et al. 2001).
SII activations following leg stimulation were weaker than
those resulting from stimulation of any other body part.
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Nevertheless, 3 distinct activation clusters were observed for
both left- and right-sided stimulations on the contralateral
operculum (Fig. 6B,D). Similar to the activations following
trunk stimulation, 2 of these foci were located at the anterior
border of OP 4 (PV) and the posterior border of OP 1 (SII).
However, activation evoked by leg stimulation was located more
medially than the trunk representations. Stimulation of either leg
also resulted in a third, more medial activation cluster in the
contralateral operculum extending into OP 3 (VS). Ipsilateral
activation was mainly found on the posterior parietal operculum
(OP 1 [SII]). The anterior focus, on the other hand, was missing
following right leg stimulation (Fig. 6B).
Somatotopic Maps on the Human Parietal Operculum
The opercular representation of a specific body part was
delineated by computing its clusters of maximum likelihood
representation, that is, by identifying those voxels where the
probability for activation following stimulation of that body part
was higher than those following stimulation of any of the 3
other parts of the body (Fig. 7 and Table 1). A synopsis of these
clusters clearly outlines the somatotopic organization of OP 1
(SII) and OP 4 (PV). The face and hand areas were mainly
located centrally on the parietal operculum at the border
between OP 1 (SII) and OP 4 (PV) (Fig. 7A,B). In contrast, the
trunk and the legs were represented twice on the parietal
operculum. That is, they were represented anterior (in the
anterior part of OP 4 [PV]) as well as posterior (in the posterior
part of area OP 1 [SII]) to the representations of the distal body
Figure 5. (A) Main effect of right trunk stimulation on the SI (defined by cytoarchitectonic areas: Brodman areas BA 3a, 3b, 1, and 2) displayed on a surface rendering of the MNI
single-subject template. Areas shown had conditional estimates that could be declared as active greater than background noise with at least 99% confidence. (B) Main effect of
right trunk stimulation on the parietal operculum, that is, the region of SII. The statistically significant clusters of activations are shown superimposed on the maximum probability
map (MPM) of OP 1--4 rendered onto the MNI single-subject template (the temporal lobes removed). Activation clusters shown on this rendering had conditional estimates that
could be declared as active greater than background noise with at least 99% confidence. (C) and (D) same as (A) and (B) showing the main effects of left trunk stimulation on the SI
and the parietal operculum.
parts, which were found at the OP 1 (SII)/OP 4 (PV) border (Fig.
7C,D). Moreover, the representations of the different body parts
were also arranged in a rostrocaudal sequence from the
superficial parietal operculum to its deeper aspect. That is,
the head was represented lateral to the hand and the trunk was
represented lateral to the leg.
The somatotopic organization of the deeper parietal operculum was less well defined. A distinct representation of the leg
was observed on the medial operculum at the border between
OP 2 (PIVC) and OP 3 (VS) (Fig. 7D), clearly separated from
activation in OP 1 (SII) and OP 4 (PV). No such distinct
representation in the deep parietal operculum was observed
for any of the other examined body parts. However, the
representations of both hands and both sides of the face
extended into OP 3 (VS) (Fig. 7A,B). All these activations in
OP 3 (VS) were located anterior to its leg representation. However, a clear differentiation between them, corresponding to
a full somatotopic arrangement within OP 3 (VS), was impossible. Whereas the head was represented anterior to the hand
on the right hemisphere, these activations largely overlapped on
the left. In the latter hemisphere, the trunk activation also
extended into OP 3 (VS) at roughly the same anterior--posterior
location as that following leg stimulation.
Probability of Activation within OP 1--4
The mean posterior probabilities for activation greater than
background noise within OP 1--4 following tactile stimulation
were compared by means of a 2-way ANOVA. This analysis
revealed a significant main effect of the factor body part (F = 5.8,
degrees of freedom [df] = 3, P < 0.05). In the subsequent
pairwise comparison, the probabilities for activation following
leg stimulation were significantly lower than those following
stimulation of the face, hand, or trunk (P < 0.05, corrected for
multiple comparisons). No significant difference in the probabilities for SII activation was found between any other body
parts. The main effect for factor area was also significant (F =
11.1, df = 3, P < 0.05). The pairwise comparison between OP 1--4
revealed that the probability for activation following tactile
stimulation was significantly higher in OP 1 (SII) than in any
other area (P < 0.05 corrected, Fig. 8). Similarly, the mean
probability for activation was significantly lower in OP 2 (PIVC)
than in OP 1 (SII), 3, or 4 (P < 0.05 corrected). There was,
however, no significant difference in the posterior probabilities
between OP 3 (VS) and OP 4 (PV) (Fig. 8).
Discussion
In the present study, we examined the location of significant
BOLD signal changes on the parietal operculum (i.e., SII)
following tactile stimulation of the face, hands, trunk, and
legs. Two mirror image somatotopic representations were
observed within cytoarchitectonically defined areas OP 1 (SII)
and OP 4 (PV). The functional border between these 2 body
maps, defined by the mirror reversal in their somatotopic
arrangement, coincided with the architectonic border between
Cerebral Cortex August 2007, V 17 N 8 1805
Figure 6. (A) Main effect of right leg stimulation in the SI rendered onto the MNI single-subject template (99% confidence for activation greater than background noise). (B) Main
effect of leg hand stimulation on the parietal operculum. The statistically significant activations in the SII region as well as the cytoarchitectonic maximum probability maps of OP 1--4
are shown on a surface rendering of the MNI single-subject template (shown without temporal lobes for display purposes). The confidence threshold of activation greater than
background noise was 99.99%. (C) and (D) same as (A) and (B) showing the main effects of left leg stimulation in the SI and the parietal operculum.
Figure 7. Synopsis of the maximum likelihood representation for each body part (cf., Figs 3--6), allowing the identification of somatotopic maps on the human parietal operculum.
Each of the subplots (A--D) shows the cortex that was more responsive to tactile stimulation of a specific body part (cf., Fig. 2) than to stimulation of any of the 3 other body parts,
superimposed on the cytoarchitectonic maximum probability map (MPM) of OP 1--4 (surface rendering of the MNI single-subject template). The numbers of the different clusters of
representation match those in Table 1, which provides details on the size, location, and corresponding cytoarchitectonic probabilities for these clusters. Note that the respective
clusters are mutually exclusive in 3-dimensional space because only a single body part can be represented most likely at a particular voxel.
1806 Somatotopic Organization of Parietal Opercular Areas
d
Eickhoff et al.
Table 1
Probabilistic combination of the somatotopic representations for the 4 examined body parts with
the cytoarchitectonic maps of parietal opercular areas OP 1 (SII), OP 2 (PIVC), OP 3 (VS), and OP
4 (PV)
Center
X
Voxel
% P (OP 1) % P (OP 2) % P (OP 3) % P (OP 4)
(P 5 27%) (P 5 26%) (P 5 24%) (P 5 25%)
Y
Z
16
18
29
29
19 1642
19 848
27 460
26 363
20
29
50
55
14
Hands
1
54 22 21 1291
2
56 21 21 488
51
47
14
8
Trunk
1
2
3
4
65 6 12 434
58 7 12 572
60 32 25 1100
54 32 23 2382
3
4
43
47
Legs
1
2
3
4
5
6
57
48
47
50
38
39
Head
1
2
3
4
60
65
50
53
4
9
35
31
22
22
11
11
26
22
20
21
287
72
357
644
258
255
51
52
14
26
44
44
78
76
65
59
32
30
100
88
52
45
56
50
47
71
8
7
8
9
7
7
35
35
5
59
23
22
33
P
18
42
43
52
59
97
100
Note: The representation for each body part comprised those voxels, which were tuned most
specifically to input from the examined body parts. The center of gravity (in anatomical MNI
space—Evans et al. 1992; Eickhoff et al. 2005) and the extent and the mean probability for
anatomically defined areas OP 1--4 are given for each of these representations. For comparison,
the mean probabilities for each area averaged over its entire probability map are given in the top
row. The numbers in the left hand column correspond to those used to label the respective
clusters in Figure 7.
Figure 8. Mean probability over all body parts for activation within cytoarchitectonically defined areas OP 1--4. The probability for activation following stimulation of
a specific body part within a given area was calculated as the union of the mean
probabilities (across all voxel assigned to this area) for left- and right-sided
stimulations. Asterisks denote significant differences in the mean probability for
activation between different areas (P \ 0.05, corrected for multiple comparisons).
these 2 areas. There was also some evidence for a third
somatotopic map deeper in the Sylvian fissure, corresponding
most likely to cytoarchitectonically defined area OP 3 (VS). This
interpretation was corroborated by the observation that the
mean probability for somatosensory activations in OP 3 (VS) was
not significantly smaller than that for OP 4 (PV).
Previous Maps of the Parietal Operculum in Monkeys
and Humans
The observation of multiple representations for each body part
in the lateral sulcus has challenged the traditional view of the SII
as an uniform region since the late 80s of the last century
(Krubitzer et al. 1986; Cusick et al. 1989). Subsequent data obtained in nonhuman primates by electrophysiology (Krubitzer
et al. 1986; Cusick et al. 1989; Krubitzer and Calford 1992;
Krubitzer, Clarey, et al. 1995; Beck et al. 1996; Huffman et al.
1999; Qi et al. 2002), tracer injection (Krubitzer et al. 1986,
1993; Cusick et al. 1989; Krubitzer and Kaas 1990; Burton et al.
1995; Beck et al. 1996; Qi et al. 2002), and histological studies
(Krubitzer et al. 1986, 1993; Krubitzer and Calford 1992; Burton
et al. 1995; Krubitzer, Manger, et al. 1995; Huffman et al. 1999;
Kaas and Collins 2001; Qi et al. 2002) revealed converging
evidence for the existence of at least 3 distinct cortical areas
(SII, PV, and VS) within the SII region. Therefore, these areas are
now regarded as part of the general organization of somatosensory cortices in primates and possibly also other mammals
(Krubitzer 1995; Kaas and Collins 2001, 2003). An overview on
their topography and somatotopic organization is given in
Figure 9 next to a summary of the somatotopic layout within
the cytoarchitectonic areas of the human parietal operculum as
observed in the present study.
First evidence for human homologues of these areas was
provided by an fMRI study examining the representation of 5
body parts in SII (Disbrow et al. 2000). This data indicated
a double representation of the shoulder and the hips within SII
and thereby supported the notion of a homology of the SII
region between monkeys and humans. The present study
confirms the findings by Disbrow et al. but extends them in
several important aspects: First, we used a genuine randomeffects model for the analysis of our data, which compares the
observed effect sizes with their variation across subjects and
thus allows inference on the general population from which the
subjects were drawn (Friston, Penny, et al. 2002; Penny and
Holmes 2003). Second, in contrast to Disbrow et al., we
examined the entire brain, not just the perisylvian cortex,
allowing the additional examination of activations in SI. The
importance of this supplementary information lies in the fact
that by comparison of the evoked activations in SI with its wellknown somatotopic organization, we could monitor the efficacy
and specificity of the stimulation. Given the good correspondence between the SI activation observed in our study and
their previously described location, we demonstrated that the
applied stimulation was appropriate for somatotopic mapping.
Finally and most important, due to the recent progress in
cytoarchitectonic mapping of the human cerebral cortex (Zilles
et al. 2002, 2003; Schleicher et al. 2005; Eickhoff, Schleicher,
et al. 2006), we were now able to relate the observed activations
and their somatotopic arrangement to distinct cytoarchitectonically defined cortical areas. This comparison allows for the first
time to examine a crucial aspect of homology: the correspondence of both structure and function. Our results show that SII
and PV do not only contain separate somatotopic organizations
but also can be differentiated on the basis of their cytoarchitectonic features as previously described for nonhuman primates
(Cusick et al. 1989; Krubitzer and Kaas 1990, 1993; Burton et al.
1995; Krubitzer, Clarey, et al. 1995; Qi et al. 2002; Wu and Kaas
2003).
Ruben et al. (2001), on the other hand, examined the
somatotopic organization of the human SII region by stimulating
Cerebral Cortex August 2007, V 17 N 8 1807
Figure 9. Comparison of the somatotopic organization of SII, PV, and VS in nonhuman
primates (Krubitzer and Kaas 1990; Krubitzer and Calford 1992; Burton et al. 1995;
Krubitzer, Clarey, et al. 1995; Qi et al. 2002) with the somatotopic organization within
areas OP 1--4 on the human parietal operculum (B).
the subjects’ hands and feet. The authors demonstrated a lateral
to medial arrangement of these 2 body parts, which is in line
with primate data, the results by Disbrow et al. (2000) and our
results. As acknowledged by the authors, the design of their
study did not, however, allow to demonstrate the double
somatotopy within the parietal operculum because hands and
feet are both represented at the SII/PV border.
The Human Homologues of SII and PV
The hypothesis that OP 1 and OP 4 are the human homologues
of monkey SII and PV was initially based on their location and
topographic relationship to neighboring cortical areas (Eickhoff,
Schleicher, et al. 2006). It received further support from a metaanalysis of functional imaging studies on hand activations in SII.
This analysis showed that the most likely location for SII hand
activations was the border between OP 1 and OP 4, similar to its
position at the border between SII and PV in monkeys (Eickhoff,
Amunts, et al. 2006). The present study confirms these results
by showing significant activation following tactile hand stimulation at the same location, thereby again closely matching the
1808 Somatotopic Organization of Parietal Opercular Areas
d
Eickhoff et al.
location of the SII/PV hand region in monkeys (Fig. 9B). The
head was represented more laterally at the border between OP
1 (SII) and OP 4 (PV). This also follows closely the predictions
from nonhuman primates where the functional border between
SII and PV is defined by a mirror reversal of the somatotopic map
along the representations of the head (lateral), hands (intermediate), and feet (medial) (Cusick et al. 1989; Krubitzer
and Kaas 1990, 1993; Burton et al. 1995; Krubitzer, Clarey, et al.
1995; Qi et al. 2002; Wu and Kaas 2003).
This mirror reversal along distal body parts implies that
proximal body parts are represented to either side of this
functional border, that is, separately in SII and PV (Fig. 9A). In
the present experiment, we stimulated 2 more proximal
locations, the trunk and the leg (which is a proximal body
part because it is followed more distally by the foot). Both were
represented twice on the parietal operculum: One of these 2
representations for either body part was located in the anterior
part of OP 4 (PV) and the other in the posterior part of area OP 1
(SII). Representations of proximal body parts were thus found
to either side of the functional boundary between SII and PV as
expected from animal data (Fig. 9B). Moreover, the topographic
relationship between trunk and leg activations is also identical
to that observed in monkeys where the leg is represented
medial to the trunk (Cusick et al. 1989; Krubitzer and Kaas
1990, 1993; Burton et al. 1995; Krubitzer, Clarey, et al. 1995; Qi
et al. 2002; Wu and Kaas 2003). However, differences between
the human data and the known somatotopic maps from
nonhuman primates were also observed. These differences
were mainly related to the representation of proximal body
parts. In humans, the trunk representation appears to be more
lateral, which is, toward the free surface of the parietal cortex,
than in monkeys. In particular, the trunk representation was
located lateral to the SII/PV hand representation which is
not the case in other species. Also, in humans, the representation of the legs was further separated from the functional and
anatomical border between SII (OP 1) and PV (OP 4) compared
with nonhuman primates. Such variations of a common topological scheme, however, are well recognized in a wide variety
of species (Krubitzer, Clarey, et al. 1995; Kaas and Collins 2003)
and can thus also be expected when comparing human and
nonhuman primate data. The observed differences can therefore be interpreted as an evolutionary modulation of the
‘‘general’’ primate SII map in the human species.
Thus, in summay, OP 1 (SII) and OP 4 (PV) both appear to
contain a complete somatotopic map. These 2 maps are mirror
images of each other with the reversal occurring at the location
of the anatomical border between these areas. We therefore
have found additional evidence that OP 1 represents the human
homologue of macaque area SII, whereas OP 4 represents the
human homologue of macaque PV.
Functional Differentiation between OP 1 (SII) and
OP 4 (PV)
The interpretation of OP 1 and OP 4 as human SII and PV,
respectively, also provides an explanation for the observation
that area OP 1 (SII) was generally more responsive to tactile
stimuli than OP 4 (PV). Studies in nonhuman primates have
shown that the functional properties and connectivity patterns
of SII (OP 1) and PV (OP 4) are similar albeit not identical. Area
SII is a purely somatosensory area and strongly interconnected
with the parietal somatosensory network. PV, on the other
hand, is more involved in sensory-motor integration and has
dense connections with the frontal motor and premotor
cortices (Qi et al. 2002; Disbrow et al. 2003; Kaas and Collins
2003). The purely somatosensory task used in our study can
therefore be expected to activate the human homologue of area
SII (OP 1) more strongly than the PV homologue OP 4. As shown
by the individual activation maps (Figs 3--6) and most pronounced by the overall probability of activation (Fig. 8), our
results do once more follow closely the predictions from animal
physiology.
Functional Evidence for a Human VS
To date, no functional description of a human VS homologue has
been reported. However, OP 3 has been regarded as its most
likely structural homologue based on its location in the depth
of the Sylvian fissure medially to OP 1 (SII) and OP 4 (PV)
(Eickhoff, Amunts, et al. 2006; Eickhoff, Schleicher, et al. 2006).
The results of the current study support this hypothesis for the
following reasons: First, our fMRI experiment provided evidence for a potential third somatotopic map in the human
parietal operculum. The somatotopic arrangement of this area,
however, could not be defined as conclusively as those in the
more lateral opercular areas OP 1 (SII) and OP 4 (PV). Rather it
was mainly based on an additional activation following leg
stimulation that was clearly distinct from the leg-associated
activations in OP 1 (SII) and OP 4 (PV). For the other body parts,
however, a clear somatotopic order could not be elucidated in
OP3. The second evidence for the hypothesis that OP 3
corresponds to human VS was provided by the mean probabilities for activation within OP 1--4. OP 1 (SII), OP 4 (PV), and OP 3
(VS) all showed significantly higher probabilities for activation
following tactile stimulation than OP 2. These results are well in
line with previous data showing that OP 2 constitutes the
human PIVC and thus is not part of the SII region (Eickhoff,
Weiss, et al. 2006). The likelihood for somatosensory activation
within OP 3 (VS), on the other hand, was not significantly
smaller than within OP 4 (i.e., PV). This suggests that OP 3 is
most likely also part of the SII. Considering this observation, its
topography and the—limited—evidence for a somatotopic
organization of this area, we suggest that OP 3 might represent
the human homologue of VS in nonhuman primates. Although
our data thus provide the first evidence for the existence of
a human VS, it has to be noted that, in spite of a considerable
amount of studies on nunhuman primates (reviewed by Kaas
and Collins 2003), the functional relevance of this region is still
largely elusive and more work is needed to fully understand its
role in the somatosensory network.
Conclusions
The data of the present study imply that cytoarchitectonic areas
OP1, OP 4, and OP 3 in the human parietal operculum are
equivalent to macaque areas SII, PV, and VS, respectively. This
claim is based on the activations elicited by stimulation of
different body parts, their somatotopic organization, and
importantly their relation to cytoarchitectonically defined areas
OP1 (SII), OP4 (PV), and OP3 (VS). These multiple somatotopic
maps strongly suggest that several functionally distinct areas
exist in human parietal operculum as has been described in the
macaque. The functional relevance of the different subregions
of the human SII region with respect to, for example, pain
perception, tactile discrimination, sensory-motor integration,
and tactile attention needs to be investigated in more detail in
future studies. By matching probabilistic cytoarchitectonic
maps with functional imaging data, such analyses is likely to
help establishing a correlation between different stimulation
paradigms and the individual cortical areas in the human
parietal operculum and will thereby advance our understanding
of the integrated functional and cytoarchitectonic organization
of the human SII region.
Notes
This Human Brain Project/Neuroinformatics research was funded
jointly by the National Institute of Mental Health, of Neurological
Disorders and Stroke, and of Drug Abuse and the National Cancer
Centre. We are grateful to our colleagues from the MR, Architectonic
Brain Mapping, and Cognitive Neurology groups for valuable support
and advice. GRF is supported by the Deutsche Forschungsgemeinschaft
(DFG—KFO 112, TP 1). Conflict of Interest: None declared.
Address correspondence to Simon B. Eickhoff, Institut für Medizin,
Forschungszentrum Jülich GmbH, D-52425 Jülich, Germany. Email:
[email protected].
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