Cortical Folding Patterns and Predicting Cytoarchitecture

The human cerebral cortex is made up of a mosaic of structural areas, frequently referred to as Brodmann areas (BAs). Despite the widespread use of cortical folding patterns to perform ad hoc estimations of the locations of the BAs, little is understood regarding 1) how variable the position of a given BA is with respect to the folds, 2) whether the location of some BAs is more variable than others, and 3) whether the variability is related to the level of a BA in a putative cortical hierarchy. We use whole-brain histology of 10 postmortem human brains and surface-based analysis to test how well the folds predict the locations of the BAs. We show that higher order cortical areas exhibit more variability than primary and secondary areas and that the folds are much better predictors of the BAs than had been previously thought. These results further highlight the significance of cortical folding patterns and suggest a common mechanism for the development of the folds and the cytoarchitectonic fields.

[1]  N. Geschwind.  Disconnexion syndromes in animals and man. II. , 1965, Brain : a journal of neurology.

[2]  D. Salat,et al.  Detection of entorhinal layer II using Tesla magnetic resonance imaging , 2005 .

[3]  P. Morosan,et al.  Human Primary Auditory Cortex: Cytoarchitectonic Subdivisions and Mapping into a Spatial Reference System , 2001, NeuroImage.

[4]  A. Schleicher,et al.  Two different areas within the primary motor cortex of man , 1996, Nature.

[5]  A. Schleicher,et al.  Mapping of human and macaque sensorimotor areas by integrating architectonic, transmitter receptor, MRI and PET data. , 1995, Journal of anatomy.

[6]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[7]  K. Amunts,et al.  Towards multimodal atlases of the human brain , 2006, Nature Reviews Neuroscience.

[8]  Shen-Ju Chou,et al.  COUP-TFI regulates the balance of cortical patterning between frontal/motor and sensory areas , 2007, Nature Neuroscience.

[9]  A. Leventhal.  The neural basis of visual function , 1991 .

[10]  A. Galaburda,et al.  Human Cerebral Cortex: Localization, Parcellation, and Morphometry with Magnetic Resonance Imaging , 1992, Journal of Cognitive Neuroscience.

[11]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[12]  Lawrence C. Sincich,et al.  The circuitry of V1 and V2: integration of color, form, and motion. , 2005, Annual review of neuroscience.

[13]  P. Morosan,et al.  Observer-Independent Method for Microstructural Parcellation of Cerebral Cortex: A Quantitative Approach to Cytoarchitectonics , 1999, NeuroImage.

[14]  T. Powell,et al.  An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. , 1970, Brain : a journal of neurology.

[15]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[16]  P S Goldman-Rakic,et al.  Morphological consequences of prenatal injury to the primate brain. , 1980, Progress in brain research.

[17]  E Courchesne,et al.  In vivo myeloarchitectonic analysis of human striate and extrastriate cortex using magnetic resonance imaging. , 1992, Cerebral cortex.

[18]  H. Kinney,et al.  Sequence of Central Nervous System Myelination in Human Infancy. II. Patterns of Myelination in Autopsied Infants , 1988, Journal of neuropathology and experimental neurology.

[19]  Edgar M. Housepian.  Atlas d'anatomie stereotaxique du telencephale. , 1968 .

[20]  P S Goldman-Rakic,et al.  Cytoarchitectonic definition of prefrontal areas in the normal human cortex: I. Remapping of areas 9 and 46 using quantitative criteria. , 1995, Cerebral cortex.

[21]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[22]  B. Brody,et al.  Sequence of Central Nervous System Myelination in Human Infancy. I. An Autopsy Study of Myelination , 1987, Journal of neuropathology and experimental neurology.

[23]  K. Amunts,et al.  Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps , 2005, Anatomy and Embryology.

[24]  N. Geschwind.  Disconnexion syndromes in animals and man. I. , 1965, Brain : a journal of neurology.

[25]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[26]  Hans Liebig,et al.  Input/Output Organization , 1985 .

[27]  J. Grafman,et al.  Imaging cortical anatomy by high‐resolution MR at 3.0T: Detection of the stripe of Gennari in visual area 17 , 2002, Magnetic resonance in medicine.

[28]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[29]  Mnh,et al.  Histologie du Système Nerveux de Lʼhomme et des Vertébrés , 1998 .

[30]  K. Amunts,et al.  Brodmann's Areas 17 and 18 Brought into Stereotaxic Space—Where and How Variable? , 2000, NeuroImage.

[31]  A. Schleicher,et al.  Transmitter receptors and functional anatomy of the cerebral cortex , 2004, Journal of anatomy.

[32]  A. Galaburda,et al.  Topographical variation of the human primary cortices: implications for neuroimaging, brain mapping, and neurobiology. , 1993, Cerebral cortex.

[33]  J. Rubenstein,et al.  Patterning of frontal cortex subdivisions by Fgf17 , 2007, Proceedings of the National Academy of Sciences.

[34]  A. Schleicher,et al.  The Somatosensory Cortex of Human: Cytoarchitecture and Regional Distributions of Receptor-Binding Sites , 1997, NeuroImage.

[35]  D. V. van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. , 2005, NeuroImage.

[36]  M. Silverman,et al.  Functional organization of the second cortical visual area in primates. , 1983, Science.

[37]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[38]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[39]  K. Zilles,et al.  Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex 2. Spatial Normalization to Standard Anatomical Space , 2000, NeuroImage.

[40]  Anders M. Dale,et al.  Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex , 2001, IEEE Transactions on Medical Imaging.

[41]  K Zilles,et al.  A quantitative approach to cytoarchitectonics: Analysis of structural inhomogeneities in nervous tissue using an image analyser , 1990, Journal of microscopy.

[42]  A. Schleicher,et al.  21 – Quantitative Analysis of Cyto- and Receptor Architecture of the Human Brain , 2002 .

[43]  D. V. van Essen,et al.  A tension-based theory of morphogenesis and compact wiring in the central nervous system. , 1997, Nature.

[44]  M. Jenkinson,et al.  In vivo identification of human cortical areas using high-resolution MRI: An approach to cerebral structure–function correlation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[45]  P. Goldman-Rakic,et al.  Cytoarchitectonic definition of prefrontal areas in the normal human cortex: II. Variability in locations of areas 9 and 46 and relationship to the Talairach Coordinate System. , 1995, Cerebral cortex.

[46]  D. V. Essen,et al.  A tension-based theory of morphogenesis and compact wiring in the central nervous system , 1997, Nature.

[47]  D. Pandya,et al.  Comparison of prefrontal architecture and connections. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[48]  G W Van Hoesen.  The modern concept of association cortex. , 1993, Current opinion in neurobiology.

[49]  T. Deacon,et al.  Monkey homologues of language areas: computing the ambiguities , 2004, Trends in Cognitive Sciences.

[50]  Lawrence L. Wald,et al.  Accurate prediction of V1 location from cortical folds in a surface coordinate system , 2008, NeuroImage.

[51]  Martin I. Sereno,et al.  Cortical visual areas in mammals , 1991 .

[52]  J C Mazziotta,et al.  Automated labeling of the human brain: A preliminary report on the development and evaluation of a forward‐transform method , 1997, Human brain mapping.

[53]  T Schormann,et al.  Three‐Dimensional linear and nonlinear transformations: An integration of light microscopical and MRI data , 1998, Human brain mapping.

[54]  K. Brodmann.  Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[55]  J. Rademacher,et al.  Stereotaxic Localization, Intersubject Variability, and Interhemispheric Differences of the Human Auditory Thalamocortical System , 2002, NeuroImage.

[56]  P. Morosan,et al.  Probabilistic Mapping and Volume Measurement of Human Primary Auditory Cortex , 2001, NeuroImage.

[57]  National Alliance for Medical Image Computing , 2007 .

[58]  A. Schleicher,et al.  Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex 1. Microstructural Organization and Interindividual Variability , 1999, NeuroImage.

[59]  J. Kaas,et al.  A representation of the visual field in the caudal third of the middle tempral gyrus of the owl monkey (Aotus trivirgatus). , 1971, Brain research.

[60]  P. Rakic.  Specification of cerebral cortical areas. , 1988, Science.

[61]  Robert O. Duncan,et al.  Cortical Magnification within Human Primary Visual Cortex Correlates with Acuity Thresholds , 2003, Neuron.