Measuring and comparing brain cortical surface area and other areal quantities

Structural analysis of MRI data on the cortical surface usually focuses on cortical thickness. Cortical surface area, when considered, has been measured only over gross regions or approached indirectly via comparisons with a standard brain. Here we demonstrate that direct measurement and comparison of the surface area of the cerebral cortex at a fine scale is possible using mass conservative interpolation methods. We present a framework for analyses of the cortical surface area, as well as for any other measurement distributed across the cortex that is areal by nature. The method consists of the construction of a mesh representation of the cortex, registration to a common coordinate system and, crucially, interpolation using a pycnophylactic method. Statistical analysis of surface area is done with power-transformed data to address lognormality, and inference is done with permutation methods. We introduce the concept of facewise analysis, discuss its interpretation and potential applications.

[1]  Michael I. Miller,et al.  Deformable templates using large deformation kinematics , 1996, IEEE Trans. Image Process..

[2]  Ivan J. Balaban,et al.  An optimal algorithm for finding segments intersections , 1995, SCG '95.

[3]  Stephan J Sanders,et al.  Whole exome sequencing identifies recessive WDR62 mutations in severe brain malformations , 2010, Nature.

[4]  Thomas E. Nichols,et al.  Controlling the familywise error rate in functional neuroimaging: a comparative review , 2003, Statistical methods in medical research.

[5]  Pasko Rakic,et al.  Renewed focus on the developing human neocortex , 2010, Journal of anatomy.

[6]  J. Morris,et al.  Differential effects of aging and Alzheimer's disease on medial temporal lobe cortical thickness and surface area , 2009, Neurobiology of Aging.

[7]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[8]  Andrew J. Saykin,et al.  Voxelwise genome-wide association study (vGWAS) , 2010, NeuroImage.

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

[10]  S. Heckers,et al.  Abnormal cortical folding patterns within Broca's area in schizophrenia: Evidence from structural MRI , 2007, Schizophrenia Research.

[11]  Paul Yiu,et al.  The uses of homogeneous barycentric coordinates in plane Euclidean geometry , 2000 .

[12]  Hans J. Johnson,et al.  Cerebral cortex structure in prodromal Huntington disease , 2010, Neurobiology of Disease.

[13]  Anders M. Dale,et al.  Improved Localization of Cortical Activity By Combining EEG and MEG with MRI Cortical Surface Reconstruction , 2002 .

[14]  A. Dale,et al.  Improved Localizadon of Cortical Activity by Combining EEG and MEG with MRI Cortical Surface Reconstruction: A Linear Approach , 1993, Journal of Cognitive Neuroscience.

[15]  Thomas Ottmann,et al.  Algorithms for Reporting and Counting Geometric Intersections , 1979, IEEE Transactions on Computers.

[16]  P. Rakic Evolution of the neocortex: Perspective from developmental biology , 2010 .

[17]  H. Bridge,et al.  High-resolution MRI: in vivo histology? , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[18]  Paul M. Thompson,et al.  Anatomically Driven Strategies for High-Dimensional Brain Image Warping and Pathology Detection , 1999 .

[19]  Jeff H. Duyn,et al.  High-field MRI of brain cortical substructure based on signal phase , 2007, Proceedings of the National Academy of Sciences.

[20]  M. Lombardi Interpolation and smoothing. , 2002, astro-ph/0208533.

[21]  M. Rushworth,et al.  Behavioral / Systems / Cognitive Connectivity-Based Parcellation of Human Cingulate Cortex and Its Relation to Functional Specialization , 2008 .

[22]  P. Macdonald,et al.  Interpreting Multivariate Data , 1982 .

[23]  Tom Vercauteren,et al.  Diffeomorphic demons: Efficient non-parametric image registration , 2009, NeuroImage.

[24]  Anderson M. Winkler,et al.  Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies , 2010, NeuroImage.

[25]  John P. Snyder,et al.  Map Projections: A Working Manual , 2012 .

[26]  U. Grenander,et al.  Statistical methods in computational anatomy , 1997, Statistical methods in medical research.

[27]  Isabelle Bloch,et al.  From 3D magnetic resonance images to structural representations of the cortex topography using topology preserving deformations , 1995, Journal of Mathematical Imaging and Vision.

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

[29]  H. Kennedy,et al.  Making bigger brains–the evolution of neural-progenitor-cell division , 2008, Journal of Cell Science.

[30]  Paul M. Thompson,et al.  A framework for computational anatomy , 2002 .

[31]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[32]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[33]  W. Klunk,et al.  Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound‐B , 2004, Annals of neurology.

[34]  J. Gaddum,et al.  Lognormal Distributions , 1945, Nature.

[35]  Dong-Hyun Kim,et al.  Triple-layer appearance of Brodmann area 4 at thin-section double inversion-recovery MR imaging. , 2009, Radiology.

[36]  Mert R. Sabuncu,et al.  Learning Task-Optimal Registration Cost Functions for Localizing Cytoarchitecture and Function in the Cerebral Cortex , 2010, IEEE Transactions on Medical Imaging.

[37]  Bruce Fischl,et al.  Geometrically Accurate Topology-Correction of Cortical Surfaces Using Nonseparating Loops , 2007, IEEE Transactions on Medical Imaging.

[38]  D. Shepard A two-dimensional interpolation function for irregularly-spaced data , 1968, ACM National Conference.

[39]  D. V. van Essen,et al.  Computerized Mappings of the Cerebral Cortex: A Multiresolution Flattening Method and a Surface-Based Coordinate System , 1996, Journal of Cognitive Neuroscience.

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

[41]  Stephen M. Smith,et al.  Evidence for abnormalities of cortical development in adolescent-onset schizophrenia , 2008, NeuroImage.

[42]  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.

[43]  H. Kenner Geodesic Math and How to Use It , 1976 .

[44]  Anders M. Dale,et al.  Genetic Influences on Cortical Regionalization in the Human Brain , 2011, Neuron.

[45]  Satrajit S. Ghosh,et al.  Evaluation of volume-based and surface-based brain image registration methods , 2010, NeuroImage.

[46]  C. T. Butts,et al.  Revisiting the Foundations of Network Analysis , 2009, Science.

[47]  John A. Vince Mathematics for Computer Graphics , 2017, Undergraduate Topics in Computer Science.

[48]  Peter F. Liddle,et al.  Regional contraction of brain surface area involves three large-scale networks in schizophrenia , 2011, Schizophrenia Research.

[49]  Peter H. Lauritzen,et al.  Monotone and Conservative Cascade Remapping between Spherical Grids (CaRS): Regular Latitude–Longitude and Cubed-Sphere Grids , 2008 .

[50]  Katrin Amunts,et al.  Cortical Folding Patterns and Predicting Cytoarchitecture , 2007, Cerebral cortex.

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

[52]  Leonidas J. Guibas,et al.  Computing convolutions by reciprocal search , 1986, SCG '86.

[53]  Richard S. J. Frackowiak,et al.  Human Primary Auditory Cortex Follows the Shape of Heschl's Gyrus , 2011, The Journal of Neuroscience.

[54]  K. Amunts,et al.  Centenary of Brodmann's Map — Conception and Fate , 2022 .

[55]  Ayse Pinar Saygin,et al.  Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data , 2006, NeuroImage.

[56]  Alan C. Evans,et al.  Detecting changes in nonisotropic images , 1999, Human brain mapping.

[57]  Chun-Fu Wu,et al.  Possible metabolic pathways of ethanol responsible for oxidative DNA damage in human peripheral lymphocytes. , 2011, Alcoholism, clinical and experimental research.

[58]  Feng Gao,et al.  Retrospective motion correction protocol for high‐resolution anatomical MRI , 2006, Human brain mapping.

[59]  Karen Nuytemans,et al.  Whole Exome Sequencing , 2020, Definitions.

[60]  P. Rakic,et al.  Decision by division: making cortical maps , 2009, Trends in Neurosciences.

[61]  H. Gouraud Continuous Shading of Curved Surfaces , 1971, IEEE Transactions on Computers.

[62]  D. Cox,et al.  An Analysis of Transformations , 1964 .

[63]  Philip W. Jones First- and Second-Order Conservative Remapping Schemes for Grids in Spherical Coordinates , 1999 .

[64]  Christiane Jablonowski,et al.  Geometrically Exact Conservative Remapping (GECoRe): Regular Latitude–Longitude and Cubed-Sphere Grids , 2009 .

[65]  W. Stahel,et al.  Log-normal Distributions across the Sciences: Keys and Clues , 2001 .

[66]  E. G. Jones,et al.  Microcolumns in the cerebral cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[67]  M. Wassef,et al.  Cerebral cortex development: From progenitors patterning to neocortical size during evolution , 2009, Development, growth & differentiation.

[68]  J D Watson,et al.  Nonparametric Analysis of Statistic Images from Functional Mapping Experiments , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[69]  R. Flowerdew,et al.  Using areal interpolation methods in geographic information systems , 1991 .

[70]  David P. Dobkin,et al.  The quickhull algorithm for convex hulls , 1996, TOMS.

[71]  Anders M. Dale,et al.  Candidate Gene Analysis of the Human Natural Killer-1 Carbohydrate Pathway and Perineuronal Nets in Schizophrenia: B3GAT2 Is Associated with Disease Risk and Cortical Surface Area , 2011, Biological Psychiatry.

[72]  A. Dale,et al.  Distinct genetic influences on cortical surface area and cortical thickness. , 2009, Cerebral cortex.

[73]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[74]  Tyrone D. Cannon,et al.  Progressive brain structural changes mapped as psychosis develops in ‘at risk’ individuals , 2009, Schizophrenia Research.

[75]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[76]  Stefan Gazdzinski,et al.  Cortical thickness, surface area, and volume of the brain reward system in alcohol dependence: relationships to relapse and extended abstinence. , 2011, Alcoholism, clinical and experimental research.

[77]  A. L. Koch,et al.  The logarithm in biology. 1. Mechanisms generating the log-normal distribution exactly. , 1966, Journal of theoretical biology.

[78]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[79]  Joseph D. Clinton,et al.  Structural Design Concepts for Future Space Missions , 1968 .

[80]  P. Royston A Toolkit for Testing for Non‐Normality in Complete and Censored Samples , 1993 .

[81]  Leonidas J. Guibas,et al.  Algorithms for bichromatic line-segment problems and polyhedral terrains , 1994, Algorithmica.

[82]  A. M. Dale,et al.  A hybrid approach to the skull stripping problem in MRI , 2004, NeuroImage.

[83]  D. Buxhoeveden,et al.  The minicolumn hypothesis in neuroscience. , 2002, Brain : a journal of neurology.

[84]  A. L. Koch,et al.  The logarithm in biology. II. Distributions simulating the log-normal. , 1969, Journal of theoretical biology.

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

[86]  Bruce Fischl,et al.  Genetic and environmental contributions to regional cortical surface area in humans: a magnetic resonance imaging twin study. , 2011, Cerebral cortex.

[87]  A W Toga,et al.  Brain surface contraction mapped in first-episode schizophrenia: a longitudinal magnetic resonance imaging study , 2009, Molecular Psychiatry.

[88]  Bruce R. Rosen,et al.  Predicting the location of entorhinal cortex from MRI , 2009, NeuroImage.

[89]  John W. Harwell,et al.  Similar patterns of cortical expansion during human development and evolution , 2010, Proceedings of the National Academy of Sciences.

[90]  C. D. Boor,et al.  Bicubic Spline Interpolation , 1962 .

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

[92]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[93]  Alan C. Evans,et al.  Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification , 2005, NeuroImage.

[94]  D. Samuel Schwarzkopf,et al.  The surface area of human V1 predicts the subjective experience of object size , 2010, Nature Neuroscience.

[95]  R. Sibson,et al.  A brief description of natural neighbor interpolation , 1981 .

[96]  Nicholas Ayache,et al.  Spherical Demons: Fast Diffeomorphic Landmark-Free Surface Registration , 2010, IEEE Transactions on Medical Imaging.

[97]  R. Coleman,et al.  Use of florbetapir-PET for imaging beta-amyloid pathology. , 2011, JAMA.

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

[99]  Jonathan D. Power,et al.  A Parcellation Scheme for Human Left Lateral Parietal Cortex , 2010, Neuron.

[100]  Anders M. Dale,et al.  Sex-dependent association of common variants of microcephaly genes with brain structure , 2009, Proceedings of the National Academy of Sciences.

[101]  Bryan R. Conroy,et al.  Function-based Intersubject Alignment of Human Cortical Anatomy , 2009, Cerebral cortex.

[102]  Gretel Sanabria-Diaz,et al.  Surface area and cortical thickness descriptors reveal different attributes of the structural human brain networks , 2010, NeuroImage.

[103]  Anjen Chenn,et al.  Regulation of Cerebral Cortical Size by Control of Cell Cycle Exit in Neural Precursors , 2002, Science.

[104]  R. Turner,et al.  Microstructural Parcellation of the Human Cerebral Cortex – From Brodmann's Post-Mortem Map to in vivo Mapping with High-Field Magnetic Resonance Imaging , 2011, Front. Hum. Neurosci..

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

[106]  Katrin Amunts,et al.  Locating the functional and anatomical boundaries of human primary visual cortex , 2009, NeuroImage.

[107]  Ian N. Gregory,et al.  Modelling long‐term pan‐European population change from 1870 to 2000 by using geographical information systems , 2010 .

[108]  W. Tobler Smooth pycnophylactic interpolation for geographical regions. , 1979, Journal of the American Statistical Association.

[109]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

[110]  R. Christensen Plane Answers to Complex Questions: The Theory of Linear Models. , 1997 .

[111]  C. Jack,et al.  Alzheimer's Disease Neuroimaging Initiative , 2008 .

[112]  C. C. Engberg Skew Frequency Curves in Biology and Statistics , .

[113]  Michael F. Goodchild,et al.  Areal interpolation: A variant of the traditional spatial problem , 1980 .

[114]  V. Mountcastle Perceptual Neuroscience: The Cerebral Cortex , 1998 .

[115]  Jean-Philippe Thirion,et al.  Image matching as a diffusion process: an analogy with Maxwell's demons , 1998, Medical Image Anal..

[116]  Alan C. Evans,et al.  Positional and surface area asymmetry of the human cerebral cortex , 2009, NeuroImage.

[117]  Brenna Argall,et al.  SUMA: an interface for surface-based intra- and inter-subject analysis with AFNI , 2004, 2004 2nd IEEE International Symposium on Biomedical Imaging: Nano to Macro (IEEE Cat No. 04EX821).

[118]  Gilbert Shapiro,et al.  The Linkage of Data Describing Overlapping Geographical Units , 1973 .

[119]  M. Miller,et al.  Landmark Matching via Large Deformation Diffeomorphisms on the Sphere , 2004 .

[120]  S. Shapiro,et al.  An Analysis of Variance Test for Normality (Complete Samples) , 1965 .

[121]  K. Zilles,et al.  Structural divisions and functional fields in the human cerebral cortex 1 Published on the World Wide Web on 20 February 1998. 1 , 1998, Brain Research Reviews.

[122]  Ingrid Agartz,et al.  A common MECP2 haplotype associates with reduced cortical surface area in humans in two independent populations , 2009, Proceedings of the National Academy of Sciences.