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Structural and Functional Analyses of Human Cerebral Cortex Using a Surface-Based Atlas

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Structural and Functional Analyses of Human Cerebral Cortex Using a Surface-Based Atlas The Journal of Neuroscience, September 15, 1997, 17(18):7079–7102 Structural and Functional Analyses of Human Cerebral Cortex Using a Surface-Based Atlas D. C. Van Essen and H. A. Drury Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110 We have analyzed the geometry, geography, and functional distinction between an anterior region in ventral occipito- organization of human cerebral cortex using surface recon- temporal cortex that is selectively involved in form processing structions and cortical flat maps of the left and right hemi- and a more posterior region (in or near areas VP and V4v) spheres generated from a digital atlas (the Visible Man). The involved in both form and color processing. Foci associated total surface area of the reconstructed Visible Man neocortex is with motion processing are mainly concentrated in a region 1570 cm 2 (both hemispheres), ;70% of which is buried in sulci. along the occipito-temporal junction, the ventral portion of By linking the Visible Man cerebrum to the Talairach stereotaxic which overlaps with foci also implicated in form processing. coordinate space, the locations of activation foci reported in Comparisons between flat maps of human and macaque mon- neuroimaging studies can be readily visualized in relation to the key cerebral cortex indicate significant differences as well as cortical surface. The associated spatial uncertainty was empir- many similarities in the relative sizes and positions of cortical ically shown to have a radius in three dimensions of ;10 mm. regions known or suspected to be homologous in the two Application of this approach to studies of visual cortex reveals species. the overall patterns of activation associated with different as- pects of visual function and the relationship of these patterns to Key words: atlas; human; macaque monkey; cerebral cortex; topographically organized visual areas. Our analysis supports a Visible Man; visual areas; computerized neuroanatomy Human cerebral cortex is a thin sheet of tissue that is extensively et al., 1996a). Here, we generate surface reconstructions and convoluted in order for a large surface area to fit within a cortical flat maps for both hemispheres of the Visible Man, a restricted cranial volume. Convolutions occur to varying degrees digital atlas of a human body (Spitzer et al., 1996). This surface- in the cortices of many species and have long been a source of based atlas allows complex patterns of experimental data to be both fascination and frustration for neuroscientists. The fascina- visualized in relation to identified gyral and sulcal landmarks and tion arises because of curiosity about how the convolutions de- in relation to a coordinate system that respects the topology of the velop and what they signify functionally (Welker, 1990; Van cortical surface. Essen, 1997). The frustrations arise because cortical sulci are A surface-based atlas is particularly useful for comparing re- irregular in shape and vary in configuration and location from one sults across the burgeoning number of neuroimaging studies that individual to the next, making it difficult to analyze experimental use positron emission tomography (PET) or functional magnetic data accurately and systematically across cases. resonance imaging (fMRI). Typically, the centers of activation These difficulties can be alleviated to a considerable extent by foci are localized by reporting their stereotaxic coordinates in analyzing cortical organization and function in relation to explicit Talairach space (Fox et al., 1985; Talairach and Tournoux, 1988; representations of the cortical surface. A particularly useful dis- Fox, 1995). To analyze the distribution of foci in relation to the play format involves cortical flat maps, which allow the entire cortical surface, we introduce a method that includes objective surface of the hemisphere to be visualized in a single view (Van estimates of the associated uncertainty in spatial localization. We Essen and Maunsell, 1980). Recent advances in computerized also demonstrate how the accuracy of localization can be im- neuroanatomy allow large expanses of highly convoluted cortex to proved using measurements based on distances along the cortical be digitally reconstructed and flattened (Dale and Sereno, 1993; surface. Carman et al., 1995; Sereno et al., 1995; DeYoe et al., 1996; Drury Human visual cortex is a suitable domain for exploring the utility of this approach. Recent neuroimaging studies of human Received April 25, 1997; revised June 30, 1997; accepted July 2, 1997. visual cortex have revealed six topographically organized visual This project was supported by National Institutes of Health Grant EY02091 and joint funding from the National Institute of Mental Health, NASA, and the National areas (Sereno et al., 1995; DeYoe et al., 1996) plus many activa- Institute on Drug Abuse under Human Brain Project MH/DA52158. Information tion foci related to specific aspects of visual function, such as about the Visible Man image data set is available at http://www.nlm.nih.gov/ motion, form, and color processing (e.g., Corbetta et al., 1991; research/visible/visible_human.html. Information on acquiring the CARET soft- ware (in executable form) and surface reconstructions (3-D and 2-D) of the Visible Tootell et al., 1996). Many issues remain unresolved, however, Man is available at http://v1.wustl.edu/caret.html. We thank Drs. M. Raichle, S. concerning the degree of functional specialization in different Petersen, J. L. Price, M. Corbetta, and E. A. DeYoe for valuable discussions, S. Kumar for cortical contouring and technical assistance, and S. Danker for manu- areas and regions. We show that existing neuroimaging data are script preparation. consistent with substantial overlap or close interdigitation of Correspondence should be addressed to David C. Van Essen, Department of different functions in many regions; involvement in just a single Anatomy and Neurobiology, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, MO 63110. aspect of visual function has been convincingly demonstrated in Copyright © 1997 Society for Neuroscience 0270-6474/97/177079-24$05.00/0 only a few regions. 7080 J. Neurosci., September 15, 1997, 17(18):7079–7102 Van Essen and Drury • Structural and Functional Analyses of Human Cerebral Cortex segments, because the algorithm used to generate a wire frame recon- struction operates only on closed contours. Surface reconstructions and area estimates. Each image was thresholded to show only the traced contours, which were then converted to a discrete sequence of points using the wand tool of NIH Image. After transfer to a Silicon Graphics (Mountain View, CA) UNIX workstation, contours were subsampled to a spacing of ;1.5 mm between nodes and loaded into custom software [Computerized Anatomical Reconstruction and Editing Tools (CARET)], which is designed for the interactive viewing and editing of surface reconstructions and associated experimental data. A wire frame reconstruction was generated using the Nuages software (Geiger, 1993). Topologically inappropriate links (typically occurring where contours change shape markedly between sections) were corrected by manual editing of the surface. After deleting the artificial links between terminations of neocortex, the resulting surface contained 51,408 nodes (99,920 triangular tiles) in the left hemisphere and 53,833 nodes (104,559 tiles) in the right hemisphere. A smoothing algorithm was used to remove nonbiological surface irregularities in the initial three-dimensional (3-D) reconstruction. The optimal amount of smoothing, judged by visual inspection, involved 100 iterations with a smoothing parameter of 0.05 (cf. Drury et al., 1996a). A visibly under-smoothed reconstruction (smoothed for only 50 iterations and containing numerous artifactual irregularities) was 10% larger in surface area. When viewed in relation to the cortical volume using VoxelView software (Vital Images, Fairfield, IA), the smoothed surface deviates systematically from its starting position in regions where the cortex is sharply creased, lying closer to the white matter along gyral regions and closer to the pial surface along the fundus of sulcal folds. The degree to which this smoothed surface underestimates the surface area of a perfect midthickness representation is difficult to determine pre- cisely but is unlikely to exceed 10%. Surface geometry. A curvature estimation algorithm (Malliot et al., 1993; Drury et al., 1996a) was used to compute the principal curvatures Figure 1. Image of the cut brain surface from the Visible Man cerebrum, along the major and minor axes (kmax and kmin ) for each node in the taken 46 mm from the top of the head (26 mm from the beginning of reconstruction. These values were used to calculate the mean curvature cortex). A contour representing the estimated trajectory of cortical layer (the average of the two principal curvatures), which is a measure of local 4 is drawn for the left hemisphere. In regions where the cortex was cut folding, and the intrinsic (Gaussian) curvature (the product of the two obliquely, close scrutiny of several nearby sections was often needed to principal curvatures), which indicates whether the surface is locally infer the most likely contour for layer 4. Cerebral cortex was contained in curved like a sphere or a saddle. A gray scale or color scale representa- 108 images (1 mm intervals), with an in-plane resolution of 2048 3 1216 tion of these
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