Cerebral Cortex Advance Access originally published online on May 11, 2005
Cerebral Cortex 2006 16(2):254-267; doi:10.1093/cercor/bhi105
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The Human Parietal Operculum. I. Cytoarchitectonic Mapping of Subdivisions
1 Institute of Medicine, Research Center Jülich, 52425 Jülich, Germany, 2 C. & O. Vogt-Institute for Brain Research, University of Düsseldorf, 40001 Düsseldorf, Germany and 3 Department of Pyschiatry and Psychotherapy, RWTH Aachen University, 52074 Aachen, Germany
Address correspondence to Professor Karl Zilles, Institut für Medizin, Forschungszentrum Jülich GmbH, D-52425 Jülich, Germany. Email: K.Zilles{at}fz-juelich.de.
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Abstract |
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The human secondary somatosensory cortex (SII) is located on the parietal operculum, as shown by intraoperative stimulation and functional imaging studies. The position and extent of the anatomical correlates of this functionally defined region, however, are still unknown. We have therefore histologically mapped the putative anatomical correlates of the SII cortex in cell-body-stained histological sections of 10 human postmortem brains using quantitative cytoarchitectonic analysis. The gray level index (GLI), which is an indicator of the volume fraction of nerve cell bodies, was measured in the parietal operculum. GLI profiles as measures of the laminar pattern of the cortex were extracted perpendicular to cortical layers. Cytoarchitectonic borders were detected observer-independently by multivariate statistical analysis of the laminar profiles. Four cytoarchitectonic areas (termed OP 1–4) were identified. This cytoarchitectonic heterogeneity of the parietal operculum corresponds to results of functional imaging studies on the human SII cortex and data from non-human primates where multiple subregions within SII have been demonstrated by electrophysiological and connectivity studies.
Key Words: brain mapping • cytoarchitecture • human cerebral cortex • SII • somatosensory cortex
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Introduction |
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The concept of a secondary somatosensory cortex (SII) was introduced for the first time to describe a second cortical representation of the cat's feet next to the previously defined ‘first’ somatosensory area (Adrian, 1940
). Homologous regions were also found in other mammals, including non-human primates (Burton, 1986). The first evidence for a human SII homologue was based on somatosensory sensations following electrical stimulation during neurosurgery in the region of the Sylvian fissure (Penfield and Jasper, 1954). Woolsey et al. (1979) confirmed these results using electrical stimulation and evoked potentials. In functional imaging studies, activations of SII have been reported for many experimental conditions, such as light touch (Ledberg et al., 1995; Disbrow et al., 2000), pain perception (Coghill et al., 1994; Peyron et al., 1999), visceral sensations (Lotze et al., 2001; Aziz et al., 2000) and tactile attention (Burton and Sinclair, 2000; Lam et al., 2001). These activations, however, were distributed widely over the parietal operculum, ranging from a region at the level of the anterior commisure (Peyron et al., 1999) to the retroinsular region (Xu et al., 1997).
Evidence has been provided that the SII region of the macaque monkey can be subdivided into at least two parts (Fig. 1). Both subareas contain a separate complete body representation and can be distinguished from each other by their architecture and connectivity (Burton et al., 1995; Krubitzer et al., 1995). An analogous subdivision of the human SII cortex was subsequently proposed by Disbrow et al. (2000) based on functional magnetic resonance imaging (fMRI) data.
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The microstructural anatomical correlates of the human SII region, however, have not yet been identified. The classical brain maps of Brodmann (1909)
, Vogt and Vogt (1919) and von Economo and Koskinas (1925), for example, differ greatly between each other in their nomenclature as well as in the number and location of candidate areas (Fig. 2, cf. Zilles, 2004). Brodmann's areas 40 and 43 both extend onto the parietal operculum and are therefore by their topography candidates for SII (Fig. 2). The opercular part of von Economo's and Koskinas' (1925) inferior parietal area PF (termed PFop) corresponds to parts of BA 40. The location of their subcentral area PFD corresponds roughly to the location of Brodmann's area (BA) 43. Thus PFop and PFD may be anatomical substrates for SII in the map of von Economo and Koskinas. On the basis of their myeloarchitectonic studies, Vogt and Vogt (1919) defined a subcentral area 72. In contrast to BA 43 or PFD, this area barely reaches the anterior part of the subcentral cortex rostral to the central sulcus. Their area 88 (located on the inferior supramarginal gyrus) may correspond to parts of area PFop. Additionally, Vogt and Vogt (1919) defined two areas in the depth of the Sylvian fissure, areas 73 (rostrally) and 74 (caudally), which have no homologues in the maps of Brodmann (1909) and von Economo and Koskinas (1925). It must be emphasized that the classical architectonic maps relied purely on visual inspection of histological sections. The criteria for the definition of cytoarchitectonic borders thus depended considerably on the observers experience. Differences between the criteria used by the authors and the biological variability between the examined brains, in particular given the small sample sizes of these classical brain mapping studies, presumably influenced the results of former architectonic approaches. This may have led to the differences in the available maps above described. In addition, all these maps represent schematic two-dimensional drawings without information about stereotaxic location and intersubject variability. They also rarely provide information about the cortical areas within the sulci, but show schematic projections onto the cortical surface. The larger portion of cortical areas is thus not shown, since the proportion of cortical surface hidden in sulci reaches two-thirds of the total surface (Zilles et al., 1988). The functionally defined human SII region is hidden almost entirely in the Sylvian fissure, which makes its interpretation with respect to the classical maps almost impossible.
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The aim of the present study was therefore, to analyze the cytoarchitecture of the parietal operculum (i.e. the region of SII) in serial histological sections of 10 human post-mortem brains using a quantitative statistically testable approach for the observer-independent detection of borders between cortical areas (Schleicher et al., 2000
). The results of this mapping study will then be described in standard stereotaxic space and compared with the location of the human SII cortex as described in functional imaging (Eickhoff et al., 2005). |
Material and Methods |
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Ten post-mortem human brains (five male; Table 1) were obtained from the body donor program of the Anatomical Institute of the University of Düsseldorf. Subjects had no clinical history of neurological or psychiatric diseases. Handedness of the subjects was unknown. Considering a general incidence of 90% for right-handedness (Annett, 1973
), it can be assumed that most cases were right handed. The brains were removed from the skull <24 h post mortem and fixed for 
6 months. The whole brains were embedded in paraffin and serially sectioned in a coronal plane (thickness = 20 µm). Each 15th section was stained for cell-bodies using a silver staining method (Merker, 1983). This method yields a higher contrast between black cell bodies and unstained neuropil as compared with traditional Nissl-staining. This contrast is an important prerequisite for automated cytoarchitectonic analysis. Every 4th stained section, i.e. every 60th of the whole series, was analyzed, resulting in a distance of 1.2 mm between examined sections.
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Observer Independent Detection of Cortical Borders
Cortical borders were identified using the approach of Schleicher et al. (2000). In short, rectangular regions of interest (ROIs) were defined in both hemispheres of the histological sections (Fig. 3B). The ROIs were digitized in a meander-like sequence using a microscope with a motor stage for automated scanning and focusing (Fig. 3C). Images were processed using the KS 400 image analyzing software (Version 3.0, Zeiss/Germany). The gray level index (GLI; Schleicher and Zilles, 1990), estimating the volume fraction of cell bodies (Wree et al., 1982), was measured by adaptive thresholding in continuously adjoining square measuring fields (32 x 32 µm). The resulting GLI image represents in each pixel the local volume fraction of cell bodies in the corresponding measuring field (Fig. 3D). Equidistant intensity profiles (thickness = 125 µm, spacing = 200 µm; Fig. 3E), which quantify the laminar GLI changes from the border between layers I and II to the border between layer VI and the white matter, were automatically obtained from the GLI images perpendicular to the cortical layers using a minimum length algorithm. Profiles were length normalized in order to compensate for local and individual variations in absolute cortical thickness. The shape of each profile was quantified by a vector of 10 features based on central moments (mean GLI, mean x, SD, skewness and kurtosis, as well as the analogous parameters from the absolute values of its first derivative) (Amunts et al., 2000; Dixon et al., 1988; Zilles et al., 2002). Differences between the feature vectors indicate differences in the shape of the profiles, i.e. in cytoarchitecture. They were measured using the Mahalanobis distance (Mahalanobis et al., 1949; Schleicher et al., 2000). The observer-independent definition of cortical areas is based on the hypothesis that profiles sampled from the same area are similar in shape, resulting in small Mahalanobis distances between their feature vectors. Profiles sampled from different areas differ in shape, resulting in high Mahalanobis distances at their border. To increase the signal-to-noise ratio, distances were calculated between feature vectors from blocks of b (10 < b < 40) adjacent profiles, instead of individual profiles. They were analyzed as a function of the profile number of the border between the blocks (Fig. 3F). The resulting distance function revealed maxima at those positions where the regions covered by the two blocks showed the most different laminar patterns. The significance of these maxima was evaluated by a Hotelling's T2-test with Bonferroni-correction for multiple comparisons (Fig. 3G). The position of a significant maximum was interpreted as a cortical border, if no higher maximum was found within one block size at either side and the maximum could be reproduced at comparable positions in adjacent sections. These criteria in combination with the use of the Mahalanobis distance function and the applied test for significance allowed to discharge minor variations in cytoarchitecture, corresponding to cortical microcolumns or more gradual cytoarchitectonic changes associated with within-area somatotopy, thus revealing only borders between different cortical areas. Using this approach, four different cytoarchitectonic areas have been identified on the parietal operculum. These areas were well distinguishable from the adjacent insular and parietal cortices as shown in Figure 3E. The results of the observer-independent approach were subsequently confirmed by a visual comparison of these quantitative results with the histological sections.
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Interhemispheric, Interareal and Interindividual Differences
For each brain and area, 50–60 profiles (25–30 per hemisphere) were sampled for further statistical analysis throughout its whole extent (4–10 consecutive sections). Sampled regions were free of histological artifacts and showed a perpendicular orientation of the sectioning plane to the cortical surface. Interhemispheric differences in the shape of the profiles were analyzed using a Monte-Carlo analysis, which tests the differences between the left and right hemispheric profiles against differences between profiles selected randomly from the whole sample. Since this analysis did not show any significant (P > 0.05) interhemispheric differences (cf. Fig. 4), profiles of both hemispheres were merged.
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Forty mean feature vectors (10 brains, four areas) were calculated, to quantify the individual areal-specific cytoarchitecture. Interareal differences were tested for significance by multivariate one-way repeated measurements analysis of variance (ANOVA; factor: area, blocking factor: subject). The architectonic dissimilarity between the defined areas was visualized by a canonical scatter plot using the first two canonical variables. The degree of dissimilarity between two areas was quantified by the mean Euclidean distance (ED) between their feature vectors (Amunts et al., 2000
; Schleicher et al., 2000), which, in contrast to the Mahalanobis distance, quantifies the ‘true’ distance between the centroids of two multi-dimensional groups without taking into account their variance. The mean ED between corresponding (same) areas of different brains was used to quantify the intersubject variability (high distances indicated a high degree of dissimilarity, i.e. variability). The interindividual differences were subsequently compared with the inter-areal distances using Student's t-test (Bonferroni-corrected for multiple comparisons). |
Results |
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Four cortical areas were defined by observer-independent cytoarchitectonic mapping, each of which shows a distinct cytoarchitecture. In order to avoid premature speculations about putative functions, we propose a neutral nomenclature for the defined areas. It consists of two parts: OP (for operculum) and a number depending on the caudal to rostral sequence, i.e., OP 1 designates the most caudal area and OP 4 the most rostral.
The Cytoarchitecture of OP 1–OP 4
Area OP 1 (Fig. 5A; cf. Fig. 6)
Layer II of OP 1 was poorly separated from layer III, since its granular cells intermingled with the small pyramidal cells of upper layer III. Layer III showed a subdivision into three sublayers defined by an increasing size of pyramidal cells. The inner granular layer IV was well separated from the adjacent pyramidal layers (III and V). Layer V contained loosely scattered, medium-sized pyramidal cells. Layer VI contained large cells and appeared slightly more cell-dense than layer V. The cells of layers III–VI were frequently arranged in widely spaced columns reaching into the underlying white matter, which renders the cortex–white matter border less distinct.
The laminar pattern was quantified by the corresponding GLI profile: the GLI peak at the layer II/III border was broad, reflecting the smooth transition between these layers. The numerous large pyramidal cells in deep layer III caused an increase in the GLI curve and separated it from the more cell-sparse middle parts of layer III. The absolute GLI maximum was found in the cell-dense layer IV. The GLI decreased throughout layer V without any detectable sublamination and increased again in layer VI, reflecting its numerous large cells. Finally, a gradual decrease towards the white matter was observed.
Area OP 2 (Fig. 5B; cf. Figs 6A and 8A)
The granular cells of layer II intermingled to such a degree with the small pyramidal cells of layer III, that both layers could not be separated from each other. A pronounced increase in size and density of pyramidal cells throughout layer III as noted in OP 1 was not observed, although a few larger pyramidal cells have been found in deep layer III. The horizontal lamination was more distinct than in OP 1 due to the high cell density in layer IV. Layer V contented mainly small pyramidal cells. Compared with OP 1, OP 2 had thinner infragranular layers and a more sharply defined white matter border.
Since only small pyramidal cells were found in lower layer III, the GLI did not increase at this cortical depth as seen in OP 1. A distinct peak of the GLI profile in layer IV reflected its higher volume fractions of cell bodies as compared with layers III and V. The rapid decrease of the GLI towards the white matter corresponded to the sharp cortex–white matter border.
Area OP 3 (Fig. 7A; cf. Fig. 8)
The border of layer II to the cell-sparse layer III was blurred. Layer III showed a low cell packing density and contained only very few large cells. Layer IV and the infragranular layers, which showed a low overall cell packing density, were thin. Layer VI was only slightly more cell-dense than layer V, which contained only very few small pyramidal cells. The white matter border was sharp.
The average GLI was lower than in OP 2 (Fig. 8A). The GLI peaks in layer II, IV and VI did not reach such values as in the other opercular areas. In particular, the difference in the GLI between layers V and VI was less pronounced than in OP 4. The distinct border to the white matter was reflected by the sharp decrease in GLI the end of the profile.
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Area OP 4 (Fig. 7B; cf. Figs 6B and 8B)
The border between layers II and upper layer III, which contained numerous small pyramidal cells, was inconspicuous. The middle part of layer III was sparse of cells, whereas deep layer III contained many medium-sized pyramidal cells. Layer IV had a moderate cell packing density and was poorly separated from the adjacent pyramidal cell layers. The upper part of layer V contained medium-sized pyramidal cells defining a cell-dense sublayer, which has not been found in any other parietal opercular area. In contrast, the lower sublayer of layer V was rather sparse of cells. The transition between layer VI and the white matter was blurred.
The GLI decreased at the border between layer II and III, which reflected the low packing density of cell bodies in the latter layer. The GLI showed a local minimum in the cell-sparse layer IIIb whereas the numerous large pyramidal cells in IIIc caused an increase in the GLI. The absolute maximum of the GLI profile coincided with the cell-dense layer IV. The subdivision of layer V was reflected by a higher GLI in the cell-dense upper sublayer Va as compared with the more cell-sparse lower sublayer Vb.
Location of OP 1–4 with Respect to Macroanatomical Landmarks
Areas OP 1 (caudally) and OP 4 (rostrally) were located more superficially on the parietal operculum than OP 2 (caudally) and OP 3 (rostrally) (Fig. 9). The border between the superficial and the deep areas was located more medial on the posterior parietal operculum (between OP 1 and OP 2) than on its anterior part (between OP 3 and OP 4). As a consequence, OP 3 had a common border with OP 1 in all hemispheres (section 7 in Fig. 9A). OP 1 reached the free surface of the supramarginal gyrus in 16 of the 20 hemispheres, although in five of these hemispheres the dorsal border of OP 1 was located close to the Sylvian fissure. OP 4 was found on the free surface (posterior subcentral gyrus) in all hemispheres. Its most dorsal extent was usually (18 of 20 hemispheres) several millimeters apart from the Sylvian fissure. The border between OP 1 and OP 4 was located close to the posterior subcentral sulcus, although both areas could be found on either side of this sulcus. OP 2 and OP 3 were located completely within the Sylvian fissure. Whereas OP 3 sometimes occupied up to three-quarter of the parietal operculum, OP 2 was exclusively located in the depth of the Sylvian fissure. Both OP 2 and OP 3 reached the insular lobe in all 20 hemispheres and cover at maximum its upper third.
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OP 4 was the most rostral area in 19 hemispheres. It usually extended approximately to the level of the lateral end of the central sulcus but never reached the precentral part of the subcentral gyrus. This makes the central sulcus a good landmark for the anterior extent of OP 4. OP 1 was the most caudal area in 17 of the 20 hemispheres. OP 1 and OP 2 always extended into the retroinsular region but never reached the caudal end of the Sylvian fissure. Although there was no precise macroscopical landmark for the posterior end these areas, a small gyrus located in the deeper half of the parietal operculum provided a good estimate: In 15 out of the 16 hemispheres where this gyrus was present it was at least partially occupied by OP 1 and/or OP 2 (cf. section 10 in Fig. 9A).
Location of OP 1–4 with Respect to Surrounding Cortical Areas
The cytoarchitectonic areas surrounding OP 1–4 are described in clockwise manner (cf. Fig. 9C): The cortex located on the precentral (frontal) part of the subcentral gyrus showed clear cytoarchitectonic differences to OP 4. In the anterior subcentral cortex a sublamination of layer V was not found but large pyramidal cells were distributed evenly throughout the whole layer V. The cell density within layer III was considerably lower than in OP 4 (Fig. 10A). The extent and possible subparcellations of this region were not examined in this study, since the focus of this examination was on the parietal operculum, whose anterior end is macroscopically defined by level of the central sulcus.
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A common border between OP 4 and the primary somatosensory cortex was observed in 17/20 hemispheres. In detail, area 3a bordered OP 4 in two hemispheres, 3b in 10 hemispheres and BA 2 in seven hemispheres. The most consistent border, which was observed in all 17 hemispheres where OP 4 did neighbor the anterior parietal areas, was the border between OP 4 and area 1. This border was also the most extensive one, whereas the borders between OP 4 and areas 3a, 3b and 2 were usually only observed in very few consecutive sections. Area 1 can be differentiated from OP 4 by its large elongated pyramidal cells in layer lower layer III, its higher cell density and the very pronounced columnar arrangement of its nerve cells (Fig. 10B; cf. figures and descriptions in Geyer et al., 1999
). The relative thickness of the infragranular layers was smaller in BA 1 than in OP 4. Further caudally OP 1 bordered area 1 in just a single case. A common border between OP 1 and area 2 was only found in the hemisphere where we also observed a border between OP 1 and area 1 and in two additional hemispheres. In all of those hemispheres, OP 4 did also border area 1. Thus most of the dorsal border of OP 1 was formed by the inferior parietal cortex (IPC), which showed smaller, less prominent pyramidal cells in sublamina IIIc and thinner infragranular layers than OP 1 (Fig. 11A).
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The cortex caudal to OP 2 was occupied by a retroinsular area (Ri), whose cytoarchitecture was a ‘mixture’ of features from the IPC and OP 2: the border between OP 2 and the retroinsular cortex was marked by a decrease of cell density in layers IV and VI, a blurring of the white matter border in the retroinsular cortex and appearance of medium sized pyramidal cells in lower layer III, which were not present in OP 2 (Fig. 11B). Ventrally OP 2 and OP 3 bordered the granular insular cortex (Ig). This border was characterized by a considerable increase in cortical thickness especially in the subgranular layers and a decrease in the overall cell density. The insular cortex further contained bigger, more prominent pyramidal cells and a less distinct white matter border (Fig. 12).
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Interhemispheric, Interareal and Interindividual Cytoarchitectonic Differences
Representative samples of profiles for OP 1–4 were analyzed. No significant cytoarchitectonic differences between the left and right hemispheric samples were found for any area. Thus samples from both hemispheres were merged and 40 mean feature vectors (10 brains, 4 areas) were calculated. The subsequent MANOVA showed that the feature vectors representing areas OP 1–4 differed significantly from each other (P < 0.05).
In a next step the average interareal distances representing the differences in cytoarchitecture between OP 1–4 were compared with the interindividual variability of these areas, i.e. the average distance between homologous areas in different brains. The cytoarchitectonic dissimilarities between the different areas (interareal distances) were significantly higher than their interindividual differences for all areas (P < 0.05; Fig. 13). Moreover, the interareal distances between OP 1–4 reflected the qualitatively described dissimilarities very well: on visual examination, the most striking cytoarchitectonic differences were found between the superficial areas OP 1 and OP 4 and the more deeply located OP 2 and OP 3. The corresponding interareal distances were correspondingly high (e.g. ED = 1.39 between OP 1 and OP 2; cf. Fig. 6A). The cytoarchitectonic differences were less pronounced between OP 2 and OP 3 or between OP 1 and OP 4 (Fig. 6B and 8A). This is in good accordance to the lower interareal distances differences between these areas (ED OP 2/OP 3 = 0.75, ED OP 1/OP 4 = 0.56; Fig. 13). Importantly, since this analysis was based on the average laminar patterns of each area as calculated from line profiles sampled across its whole extent these results by no means depend on the location of the different borders relative to the plane of sectioning (which can not be ruled out entirely for the observer-independent mapping algorithm per se) but do reflect genuine differences and similarities in cytoarchitecture.
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The obtained results were visualized in a canonical scatter plot, where the distances between the symbols reflect the dissimilarity in the shape of the corresponding GLI profiles (Fig. 14). In spite of a considerable interindividual variability, the differences in the profile shapes between the four cortical areas caused the formation of four distinct clusters (OP 1–4). These clusters were separated without any overlap of the 95% confidence areas of each group's centroid.
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Discussion |
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The present study reports four distinct architectonic areas on the human parietal operculum (OP 1–4), which were identified using classical cytoarchitectonic criteria and quantitative cytoarchitectonic analysis. The application of a statistical approach for the detection of areal borders and the quantification of cytoarchitectonic variability in the present study represent an important difference from the classical cytoarchitectonic examinations (e.g. Brodmann, 1909
; Sarkissov et al., 1949; von Economo and Koskinas, 1925), which relied purely on visual inspection of histological sections and thus the individual experience of the observer.
With respect to their topography, OP 4 and possibly OP 3 correspond approximately to Brodmann's BA 43. In Brodmann's map, however, BA 43 covers the whole subcentral gyrus (Brodmann, 1909), whereas we described a clearly different cytoarchitecture on the precentral part of this gyrus. BA 40 extends from the intraparietal sulcus to the insular cortex and covers also the parietal operculum. Its border to BA 43 is located approximately at the posterior subcentral sulcus and coincides thus with the location of the border between OP 4 and OP 1. Therefore areas OP 1 (and OP 2) seem to be included among other inferior parietal regions in Brodmann's definition of BA 40.
Later researchers (von Economo and Koskinas, 1925; Sarkissov et al., 1949) found architectonic differences between the inferior parietal cortex and the adjacent operculum (PF versus PFop; area 40 versus area 40op), which we could confirm by showing significant cytoarchitectonic differences between the IPC and OP 1. Subparcellations within the parietal operculum, however, which may correspond to OP 2 or OP 3, were not described in these maps. Both Sarkissov (1949) and von Economo and Koskinas (1925) defined a separate cytoarchitectonic area on the subcentral gyrus similar in location to OP 4 (areas 43 and PFD respectively). This area was distinguished from the rostrally adjacent agranular motor cortex (due to its well developed layer IV) and the primary somatosensory cortex (e.g., due to smaller cells in deeper layer III). The characterization of PFD provided by von Economo and Koskinas (1925) is close to the description of OP 4: PFD is e.g. described as containing large pyramidal cells in sublayers IIIc and Va. Such cells were also found in OP 4. Like OP 4, PFD has a high cell density, thick infragranular layers and a blurred cortex-white matter border. However, there is one important difference between these maps and our own results. Whereas area OP 4 is followed rostrally by another granular area, PFD and BA 43 border the (agranular) motor cortex. Thus, another cytoarchitectonic entity might be included in the definition of both PFD and BA 43.
Vogt and Vogt (1919) defined several areas on the parietal operculum based on their myeloarchitectonic studies. Two of these areas (areas 73 and 74) are located completely in the depth of the Sylvian fissure. Areas 72 and 88 are located superficially and extend onto the free surface. This myeloarchitectonic parcellation of the parietal operculum is the only ‘classical’ brain map, which shows multiple cortical areas on the parietal operculum and includes areas, which do not extend onto the free surface. This myeloarchitectonic map is thus most similar to our own cytoarchitectonic results, which also shows the existence of several opercular areas, two of which (OP 2 and OP 3) are not found on the free surface of the brain.
SII Maps in Non-human Primates
The human SII region is considered to be homologous to the SII cortex of non-human primates (Burton et al., 1993; Disbrow et al., 2000). Based on converging evidence from microelectrode mapping, histological examination and tracing experiments on cortico-cortical and thalamic connectivity (Krubitzer et al., 1986, 1993, 1995; Krubitzer and Kaas, 1990; Burton et al., 1995; Disbrow et al., 2003), the existence of multiple areas within the SII region is now considered a general feature of the somatosensory cortex of anthropoid primates (Kaas and Collins, 2003). The most commonly used parcellation scheme for the SII region is as follows (Figs 1 and 15): the opercular area located immediately adjacent to the SI cortex is termed the parietal ventral area (PV). Area PV is followed caudally by area SII. It has to be pointed out, that this ‘area SII’ is not equivalent to the ‘SII region’, but denotes an individual area within this region. Area VS (ventral somatosensory) is located deeper in the Sylvian fissure medially adjacent to area SII and PV.
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Based on its topography OP 4 may correspond to the primate area PV: like PV, OP 4 is located superficially within the Sylvian fissure close to the central sulcus and borders the primary somatosensory cortex (SI). OP 1 is located caudally to OP 4 next to the inferior parietal cortex, suggesting that it is a human analogue to area SII. However, the human anatomy seems to differ from the topographical relationships observed for non-human primates in the respect that OP 1 (i.e. area SII) borders the anterior parietal areas 1 and 2 in only a very few cases, whereas in non-human primates there is a consistent border between area SII and area 1 (Coq et al., 2004
). Like areas SII and PV, OP 4 and OP 1 share a common border running in a medial to lateral direction. Topologically OP 3 is a good candidate for a human analogue of VS (Fig. 15): OP 3 is located deeper in the Sylvian fissure than OP 1 and OP 4 (which represent the possibly analogue to areas SII and PV) and borders both of these areas. No distinct area has yet been described in SII cortex of non-human primates, which corresponds topographically to OP 2. Most authors examining the cortex posterior to the primate SII region have described the neurons in this region as responding to various and often complex stimuli, including input from other sensory modalities like the auditory and vestibular systems (Robinson and Burton, 1980; Akbarian et al., 1988; Krubitzer et al., 1995; Guldin and Grusser, 1998). In summary, the objectively defined areal boundaries within the human parietal operculum show good agreement with the primate data on that region. This correspondence is be further corroborated by a meta-analysis of human functional imaging studies (Eickhoff et al., 2005), which shows that the functional activations within these areas follow the predictions from primate work: the hand representation within the parietal operculum is found at the border between OP 1 and OP 4, as is the case for their topographical analogues in the primate brain areas SII and PV. Functional Inhomogeneity of the Human SII Region
Functional imaging studies on the human somatosensory system provided ample evidence of a functional inhomogeneity of SII. A positron emission tomography (PET) study by Ledberg et al. (1995), for example, revealed two separate foci within the parietal operculum. The superficial one was activated by roughness and length discrimination, the deeper one by a somatosensory reaction time task. Two activations within the SII region were also demonstrated in a PET study by Burton et al. (1997): an anterior, deep focus was activated as the result of direct touch of the finger, which is mediated mainly by cutaneous receptors. A more caudal, superficial activation was associated with stimulation by a ring like plectrum intended to activate mainly deep receptors. Despite its lower spatial resolution, a magnetoencephalography recording during median nerve stimulation also revealed two consecutive responses located within the SII region. The earlier response was found more anteriorly and medially to the later one (Mima et al., 1997). In an fMRI study, Disbrow et al. (2000) stimulated the hand, foot, face, hip and shoulder by sponge brushing. The authors demonstrated two complete, somatotopically organized body maps on the human parietal operculum, probably analogous to the primate areas SII and PV, as well as two additional cortical fields whose somatotopy could not be consistently resolved.
A functional segregation of the human SII cortex was also suggested with respect to pain perception. In a PET experiment, non-painful and painful stimulation resulted in two distinct activation clusters within the SII region (Coghill et al., 1994). A recent fMRI study on the cortical representation of pain and touch confirmed these results by demonstrating two spatially separate activations within SII (Ferretti et al., 2003): one was located on the subcentral gyrus, the other more posterior within the Sylvian fissure. Only the activation of the posterior focus was modulated by the perceived pain intensity. Further evidence that only the posterior parts of the SII region are involved in pain perception was provided by lesion studies: only patients with lesions involving the posterior parietal operculum showed a raised pain threshold on the contralateral body side, whereas patients with more anterior lesions had no deficits in pain perception (Greenspan and Winfield, 1992; Greenspan et al., 1999).
This functional heterogeneity of SII favors the assumption that the four cytoarchitectonic areas on the parietal operculum represent functionally distinct regions. They likely contribute differentially to somatosensory processing tasks (e.g. pain perception, tactile attention and somatosensory working memory) which have been ascribed to SII. If activities from all four areas have been labeled as located within ‘SII’, this might potentially have caused confusion about the function of the SII region. To answer the question of the functional meaning of the structural differentiation, it is now necessary to correlate the defined cytoarchitectonic areas with functional imaging data as shown in Eickhoff et al. (2005).
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Acknowledgments |
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This Human Brain Project/Neuroinformatics research was funded jointly by the National Institute of Mental Health, of Neurological Disorders and Stroke, of Drug Abuse, the National Cancer Center, the Deutsche Forschungsgemeinschaft (KFO-112) and the Volkswagenstiftung.
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