Elsevier

NeuroImage

Volume 33, Issue 2, 1 November 2006, Pages 430-448
NeuroImage

The human inferior parietal cortex: Cytoarchitectonic parcellation and interindividual variability

https://doi.org/10.1016/j.neuroimage.2006.06.054Get rights and content

Abstract

The inferior parietal cortex (IPC) integrates information from different sensory modalities and plays an important role in a variety of higher cognitive functions. Brodmann (Brodmann, K., 1909. Vergleichende Lokalisationslehre der Großhirnrinde. Barth, Leipzig) proposed a cytoarchitectonic subdivision of the IPC into only two cortical areas, a rostral (BA 40) and a caudal (BA 39) area. Although his scheme was repeatedly challenged by other observers, it is still used for the anatomical localization of functional imaging data. The apparent differences between all these cyto- and myeloarchitectonic maps may be caused partly by the observer-dependent procedure of defining cytoarchitectonic borders by pure visual inspection of histological sections and partly by the interindividual variability of cytoarchitecture. The present observations and the resulting cortical map of the IPC are based on quantitative, observer-independent definitions of cytoarchitectonic borders and take into account each area's topographical variability across brains. Ten human postmortem brains were scanned using an MRI 3-D FLASH sequence prior to histological processing. After embedding in paraffin, serial sections through whole brains were prepared, and the sections were stained for cell bodies. Following high-resolution digitization of sections containing the IPC, we defined the cytoarchitecture and borders of each cortical area of this brain region using a multivariate statistical analysis of laminar cell density profiles. In contrast to previous observations, we found seven cytoarchitectonic areas in the IPC: five in the rostral (covering the region of BA 40) and two in the caudal part (covering the region of BA 39). We observed considerable interindividual variability in the topography of each area. A consistent correspondence between macroanatomical landmarks and cytoarchitectonic borders was not found. This new cytoarchitectonic map of the human IPC demonstrates regional differences in the cortical microstructure that is suggestive of functional differentiation. Furthermore, the map is registered in three dimensions and thereby provides a robust anatomical base for interpreting functional imaging studies.

Introduction

The inferior parietal cortex (IPC) integrates various modalities (e.g., somatosensory, visual, and auditory) and plays an important role in various higher cognitive functions. One may wonder whether this functional complexity is reflected at a structural (e.g., cytoarchitectonic) level.

According to Brodmann (1909; Fig. 1A), the IPC consists of two different cytoarchitectonic areas: BA 40 located on the supramarginal gyrus and BA 39 on the angular gyrus. Rostrally, BA 40 borders the somatosensory cortex (BA 2). Ventrally, BA 40 reaches into the depth of the operculum Rolandi and dorsally to the intraparietal sulcus. The ventral part of BA 39 abuts the temporal cortex. The caudal part of BA 39 borders the occipital cortex.

Other cyto- or myeloarchitectonic maps of this cortical region have been published by Campbell (1905), Vogt and Vogt (1919; Fig. 1B), von Economo and Koskinas (1925; Figs. 1C and D), Gerhardt (1940), Bailey and von Bonin (1951), Sarkissov et al. (1955; Fig. 1E), and Batsch (1956). None of these maps, however, takes into account the interindividual variability of the cortical areas, especially with respect to size and their positions relative to macroscopical landmarks. Furthermore, the maps were published as schematic drawings. Thus, a volume or surface based reference system, which provides the opportunity to import and spatially normalize structural or functional data from other brains, is missing. A third problem is the observer-dependent method of classical cytoarchitectonic studies. As a consequence, the maps are strongly influenced by each investigator’s criteria for defining microstructural borders between cortical areas. This led to considerable differences between the maps. For example, in sharp contrast to Brodmann (1909), von Economo and Koskinas (1925) subdivided BA 40 into five areas.

In the present study, the borders of cytoarchitectonic areas were delineated in 10 postmortem brains using an observer-independent technique (Schleicher et al., 1999, Zilles et al., 2002). The brains and areas were then spatially normalized to the Montreal Neurological Institute (MNI) single reference brain, and a probability map was generated for each area by superimposing the data from all ten brains. An area's probability map reflects the interindividual variability of this area with respect to size and location since a single voxel in MNI space represents the frequency of the representation of parts of this particular area found in one up to ten brains. Following normalization, the 3-D cytoarchitectonic probability maps can be co-registered and compared with functional MRI or PET data in the same reference space (Eickhoff et al., 2005).

This probabilistic and observer-independent procedures have already successfully applied in studies of the somatosensory (BA 3a, 3b, 1: Geyer et al., 1999; BA 2: Grefkes et al., 2001), motor (BA 4: Geyer et al., 1996), and premotor cortex (BA 6: Geyer, 2004), Broca’s speech region (BA 44 and 45: Amunts et al., 1999), primary auditory cortex (BA 41: Morosan et al., 2001), visual cortex (BA 17 and 18: Amunts et al., 2000), and, most recently, the parietal operculum (Eickhoff et al., 2006a, Eickhoff et al., 2006b) and areas hIP1 and hIP2 in the intraparietal sulcus (Choi et al., 2006).

In the present study, we used the same methodical approach to study the cytoarchitectonic organization of the IPC. We found a mosaic of seven areas: five are located on the supramarginal gyrus, two lie on the angular gyrus.

Section snippets

Histology and MR scanning of postmortem brains

We analyzed ten postmortem brains (5 males, 5 females, ranging in age from 37 to 86 years, cf. Table 1) obtained through the body donor program of the Department of Anatomy, University of Düsseldorf, Germany. Subjects had no known history of neurological or psychiatric diseases. We removed the brains from the skull and fixed them for approximately 5 months in 4% formaldehyde diluted in water or in Bodian's fixative (90 ml of 80% ethanol, 5 ml of 37% formaldehyde diluted in water, and 5 ml of

The observer-independent mapping procedure

An example of the observer-independent procedure will be given here in some detail to illustrate the cytoarchitectonic mapping method used in the present study. Fig. 2A shows a lateral view of one of the ten brains after fixation. A coronal whole-brain section no. 1231 (cf. vertical line in Fig. 2A) through this brain, stained for cell bodies, is depicted in Fig. 2B. The box in Fig. 2B marks the ROI within which GLI profiles were extracted. The GLI image of this ROI is depicted at higher

Discussion

The IPC was repeatedly parcellated during the last century (Bailey and von Bonin, 1951, Batsch, 1956, Brodmann, 1909, Campbell, 1905, Gerhardt, 1940, Sarkissov et al., 1955, Vogt and Vogt, 1919, von Economo and Koskinas, 1925). Each map, however, is a schematic drawing of the macro- and microanatomical topography of only one brain, and each investigator employed criteria for defining borders between different cortical areas, which are dependent on the experience and pattern recognition

Acknowledgments

The authors thank U. Blohm for excellent histological work. This work was supported by a grant (to K.Z.) funded by the DFG (grant KFO 112), a Human Brain Project/Neuroinformatics Research grant funded by the National Institute of Biomedical Imaging and Bioengineering, the National Institute of Neurological Disorders and Stroke, and the National Institute of Mental Health and by a grant (to K.Z.) of the European Commission (Grant QLG3-CT-2002-00746).

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