CerebroMatic: A Versatile Toolbox for Spline-Based MRI Template Creation

Brain image spatial normalization and tissue segmentation rely on prior tissue probability maps. Appropriately selecting these tissue maps becomes particularly important when investigating “unusual” populations, such as young children or elderly subjects. When creating such priors, the disadvantage of applying more deformation must be weighed against the benefit of achieving a crisper image. We have previously suggested that statistically modeling demographic variables, instead of simply averaging images, is advantageous. Both aspects (more vs. less deformation and modeling vs. averaging) were explored here. We used imaging data from 1914 subjects, aged 13 months to 75 years, and employed multivariate adaptive regression splines to model the effects of age, field strength, gender, and data quality. Within the spm/cat12 framework, we compared an affine-only with a low- and a high-dimensional warping approach. As expected, more deformation on the individual level results in lower group dissimilarity. Consequently, effects of age in particular are less apparent in the resulting tissue maps when using a more extensive deformation scheme. Using statistically-described parameters, high-quality tissue probability maps could be generated for the whole age range; they are consistently closer to a gold standard than conventionally-generated priors based on 25, 50, or 100 subjects. Distinct effects of field strength, gender, and data quality were seen. We conclude that an extensive matching for generating tissue priors may model much of the variability inherent in the dataset which is then not contained in the resulting priors. Further, the statistical description of relevant parameters (using regression splines) allows for the generation of high-quality tissue probability maps while controlling for known confounds. The resulting CerebroMatic toolbox is available for download at http://irc.cchmc.org/software/cerebromatic.php.

[1]  Michael Unser,et al.  Splines: a perfect fit for signal and image processing , 1999, IEEE Signal Process. Mag..

[2]  Nick C. Fox,et al.  Simulation of Acquisition Artefacts in MR Scans: Effects on Automatic Measures of Brain Atrophy , 2006, MICCAI.

[3]  Satrajit S. Ghosh,et al.  Evaluating the validity of volume-based and surface-based brain image registration for developmental cognitive neuroscience studies in children 4 to 11years of age , 2010, NeuroImage.

[4]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[5]  D. Hill,et al.  Non-rigid image registration: theory and practice. , 2004, The British journal of radiology.

[6]  Jagath C. Rajapakse,et al.  Statistical approach to segmentation of single-channel cerebral MR images , 1997, IEEE Transactions on Medical Imaging.

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

[8]  P. Huttenlocher,et al.  Synaptic density in human frontal cortex — Developmental changes and effects of aging , 1979, Brain Research.

[9]  Kathrine Skak Madsen,et al.  Postnatal brain development: structural imaging of dynamic neurodevelopmental processes. , 2011, Progress in brain research.

[10]  Christian Gaser,et al.  Models of the Aging Brain Structure and Individual Decline , 2012, Front. Neuroinform..

[11]  S Warfield,et al.  Early assessment of brain maturation by MR imaging segmentation in neonates and premature infants. , 2006, AJNR. American journal of neuroradiology.

[12]  Yaozong Gao,et al.  Segmentation of neonatal brain MR images using patch-driven level sets , 2014, NeuroImage.

[13]  John G. Csernansky,et al.  Open Access Series of Imaging Studies: Longitudinal MRI Data in Nondemented and Demented Older Adults , 2010, Journal of Cognitive Neuroscience.

[14]  C. Davatzikos Spatial normalization of 3D brain images using deformable models. , 1996, Journal of computer assisted tomography.

[15]  Anna Varentsova,et al.  Development of a high angular resolution diffusion imaging human brain template , 2014, NeuroImage.

[16]  Lin Shi,et al.  Intensity and sulci landmark combined brain atlas construction for Chinese pediatric population , 2014, Human brain mapping.

[17]  Thomas E. Nichols,et al.  Rank-order versus mean based statistics for neuroimaging , 2007, NeuroImage.

[18]  Karl J. Friston,et al.  Diffeomorphic registration using geodesic shooting and Gauss–Newton optimisation , 2011, NeuroImage.

[19]  Gints Jekabsons,et al.  Adaptive Regression Splines toolbox for Matlab/Octave , 2015 .

[20]  J Mazziotta,et al.  A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[21]  Terry M. Peters,et al.  3D statistical neuroanatomical models from 305 MRI volumes , 1993, 1993 IEEE Conference Record Nuclear Science Symposium and Medical Imaging Conference.

[22]  J. Gilmore,et al.  More insights into early brain development through statistical analyses of eigen-structural elements of diffusion tensor imaging using multivariate adaptive regression splines , 2013, Brain Structure and Function.

[23]  Bruce Fischl,et al.  FreeSurfer , 2012, NeuroImage.

[24]  D. Sackett Bias in analytic research. , 1979, Journal of chronic diseases.

[25]  D. Shen,et al.  Multi‐atlas based representations for Alzheimer's disease diagnosis , 2014, Human brain mapping.

[26]  Max A. Viergever,et al.  Automatic Segmentation of Eight Tissue Classes in Neonatal Brain MRI , 2013, PloS one.

[27]  Peter Lundberg,et al.  Application of Quantitative MRI for Brain Tissue Segmentation at 1.5 T and 3.0 T Field Strengths , 2013, PloS one.

[28]  John E. Richards,et al.  A database of age-appropriate average MRI templates , 2016, NeuroImage.

[29]  Marko Wilke,et al.  Assessment of spatial normalization of whole‐brain magnetic resonance images in children , 2002, Human brain mapping.

[30]  Clifford R Jack,et al.  Common MRI acquisition non-idealities significantly impact the output of the boundary shift integral method of measuring brain atrophy on serial MRI , 2006, NeuroImage.

[31]  Fred L. Bookstein,et al.  “Voxel-Based Morphometry” Should Not Be Used with Imperfectly Registered Images , 2001, NeuroImage.

[32]  Scott Holland,et al.  Template-O-Matic: A toolbox for creating customized pediatric templates , 2008, NeuroImage.

[33]  Jean-Baptiste Poline,et al.  Dealing with the shortcomings of spatial normalization: Multi‐subject parcellation of fMRI datasets , 2006, Human brain mapping.

[34]  K Kazemi,et al.  Quantitative Comparison of SPM, FSL, and Brainsuite for Brain MR Image Segmentation , 2014, Journal of biomedical physics & engineering.

[35]  M Wilke,et al.  Normative pediatric brain data for spatial normalization and segmentation differs from standard adult data , 2003, Magnetic resonance in medicine.

[36]  N. Makris,et al.  Regional infant brain development: an MRI-based morphometric analysis in 3 to 13 month olds. , 2013, Cerebral cortex.

[37]  Rainer Goebel,et al.  Measuring structural–functional correspondence: Spatial variability of specialised brain regions after macro-anatomical alignment , 2012, NeuroImage.

[38]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[39]  Dwarikanath Mahapatra,et al.  Skull Stripping of Neonatal Brain MRI: Using Prior Shape Information with Graph Cuts , 2012, Journal of Digital Imaging.

[40]  Scott Holland,et al.  Infant brain probability templates for MRI segmentation and normalization , 2008, NeuroImage.

[41]  P. Roland,et al.  Comparison of spatial normalization procedures and their impact on functional maps , 2002, Human brain mapping.

[42]  Richard N. Henson,et al.  CHAPTER 15 – Efficient Experimental Design for fMRI , 2007 .

[43]  P. Huttenlocher Synaptic density in human frontal cortex - developmental changes and effects of aging. , 1979, Brain research.

[44]  Thomas E. Nichols,et al.  Statistical limitations in functional neuroimaging. I. Non-inferential methods and statistical models. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[45]  Brian B. Avants,et al.  Evaluation of automatic neonatal brain segmentation algorithms: The NeoBrainS12 challenge , 2015, Medical Image Anal..

[46]  João Manuel R S Tavares,et al.  Medical image registration: a review , 2014, Computer methods in biomechanics and biomedical engineering.

[47]  Paul M. Thompson,et al.  Mean Template for Tensor-Based Morphometry Using Deformation Tensors , 2007, MICCAI.

[48]  Tobias Kober,et al.  MP2RAGE, a self bias-field corrected sequence for improved segmentation and T1-mapping at high field , 2010, NeuroImage.

[49]  Lewis D. Griffin,et al.  Zen and the art of medical image registration: correspondence, homology, and quality , 2003, NeuroImage.

[50]  S. Holland,et al.  Multidimensional morphometric 3D MRI analyses for detecting brain abnormalities in children: Impact of control population , 2014, Human brain mapping.

[51]  John Ashburner,et al.  SPM: A history , 2012, NeuroImage.

[52]  Arthur W. Toga,et al.  The construction of a Chinese MRI brain atlas: A morphometric comparison study between Chinese and Caucasian cohorts , 2010, NeuroImage.

[53]  P. Fox,et al.  Global spatial normalization of human brain using convex hulls. , 1999, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

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

[55]  D. Louis Collins,et al.  Brain templates and atlases , 2012, NeuroImage.

[56]  Y. Selen,et al.  Model-order selection: a review of information criterion rules , 2004, IEEE Signal Processing Magazine.

[57]  D. Shen,et al.  DICCCOL: dense individualized and common connectivity-based cortical landmarks. , 2013, Cerebral cortex.

[58]  Gerard R. Ridgway,et al.  Symmetric Diffeomorphic Modeling of Longitudinal Structural MRI , 2013, Front. Neurosci..

[59]  S. Mori,et al.  Quantitative evaluation of brain development using anatomical MRI and diffusion tensor imaging , 2013, International Journal of Developmental Neuroscience.

[60]  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 .

[61]  Arno Klein,et al.  Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration , 2009, NeuroImage.

[62]  Borys Shuter,et al.  Reproducibility of brain tissue volumes in longitudinal studies: Effects of changes in signal-to-noise ratio and scanner software , 2008, NeuroImage.

[63]  Dinggang Shen,et al.  Neonatal atlas construction using sparse representation , 2014, Human brain mapping.

[64]  Ranjan Duara,et al.  Comparing new templates and atlas-based segmentations in the volumetric analysis of brain magnetic resonance images for diagnosing Alzheimer’s disease , 2012, Alzheimer's & Dementia.

[65]  Alan C. Evans,et al.  Total and regional brain volumes in a population-based normative sample from 4 to 18 years: the NIH MRI Study of Normal Brain Development. , 2012, Cerebral cortex.

[66]  L. Jäncke,et al.  Brain structural trajectories over the adult lifespan , 2012, Human brain mapping.

[67]  Marko Wilke,et al.  Variability of gray and white matter during normal development: a voxel-based MRI analysis , 2003, Neuroreport.

[68]  Paul M. Thompson,et al.  Robust Brain Extraction Across Datasets and Comparison With Publicly Available Methods , 2011, IEEE Transactions on Medical Imaging.

[69]  J. Ashburner,et al.  Multimodal Image Coregistration and Partitioning—A Unified Framework , 1997, NeuroImage.

[70]  George Fein,et al.  Automated MRI cerebellar size measurements using active appearance modeling , 2014, NeuroImage.

[71]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[72]  A. Toga,et al.  Detection and mapping of abnormal brain structure with a probabilistic atlas of cortical surfaces. , 1997, Journal of computer assisted tomography.

[73]  R. Beisteiner,et al.  The benefits of skull stripping in the normalization of clinical fMRI data☆ , 2013, NeuroImage: Clinical.

[74]  Pierrick Coupé,et al.  An Optimized Blockwise Nonlocal Means Denoising Filter for 3-D Magnetic Resonance Images , 2008, IEEE Transactions on Medical Imaging.

[75]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[76]  Karl J. Friston,et al.  Incorporating Prior Knowledge into Image Registration , 1997, NeuroImage.

[77]  Paul M. Thompson,et al.  Automated brain tissue assessment in the elderly and demented population: Construction and validation of a sub-volume probabilistic brain atlas , 2005, NeuroImage.

[78]  K. Zilles,et al.  Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty , 2009, Human brain mapping.

[79]  Denis Cousineau,et al.  Outliers detection and treatment: a review , 2010 .

[80]  Jonathan E. Clark,et al.  Fast and Robust , 2002, Int. J. Robotics Res..

[81]  M. Wilke,et al.  Long‐term neurobiological consequences of early postnatal hCMV‐infection in former preterms , 2014, Human brain mapping.

[82]  Eero P. Simoncelli,et al.  Image quality assessment: from error visibility to structural similarity , 2004, IEEE Transactions on Image Processing.

[83]  S. Baron-Cohen,et al.  Neuroscience and Biobehavioral Reviews a Meta-analysis of Sex Differences in Human Brain Structure , 2022 .

[84]  J. Freidman,et al.  Multivariate adaptive regression splines , 1991 .

[85]  Karl J. Friston,et al.  Computing average shaped tissue probability templates , 2009, NeuroImage.

[86]  Damien Garcia,et al.  Robust smoothing of gridded data in one and higher dimensions with missing values , 2010, Comput. Stat. Data Anal..

[87]  Alan C. Evans,et al.  Fast and robust parameter estimation for statistical partial volume models in brain MRI , 2004, NeuroImage.

[88]  Jennifer L. Whitwell,et al.  Accurate automatic estimation of total intracranial volume: A nuisance variable with less nuisance , 2015, NeuroImage.

[89]  Wendy Bogers,et al.  Automated subcortical segmentation using FIRST: Test–retest reliability, interscanner reliability, and comparison to manual segmentation , 2013, Human brain mapping.

[90]  I. Johnsrude,et al.  The problem of functional localization in the human brain , 2002, Nature Reviews Neuroscience.