Unbiased construction of a temporally consistent morphological atlas of neonatal brain development

Premature birth increases the risk of developing neurocognitive and neurobehavioural disorders. The mechanisms of altered brain development causing these disorders are yet unknown. Studying the morphology and function of the brain during maturation provides us not only with a better understanding of normal development, but may help us to identify causes of abnormal development and their consequences. A particular difficulty is to distinguish abnormal patterns of neurodevelopment from normal variation. The Developing Human Connectome Project (dHCP) seeks to create a detailed four-dimensional (4D) connectome of early life. This connectome may provide insights into normal as well as abnormal patterns of brain development. As part of this project, more than a thousand healthy fetal and neonatal brains will be scanned in vivo. This requires computational methods which scale well to larger data sets. We propose a novel groupwise method for the construction of a spatio-temporal model of mean morphology from cross-sectional brain scans at different gestational ages. This model scales linearly with the number of images and thus improves upon methods used to build existing public neonatal atlases, which derive correspondence between all pairs of images. By jointly estimating mean shape and longitudinal change, the atlas created with our method overcomes temporal inconsistencies, which are encountered when mean shape and intensity images are constructed separately for each time point. Using this approach, we have constructed a spatio-temporal atlas from 275 healthy neonates between 35 and 44 weeks post-menstrual age (PMA). The resulting atlas qualitatively preserves cortical details significantly better than publicly available atlases. This is moreover confirmed by a number of quantitative measures of the quality of the spatial normalisation and sharpness of the resulting template brain images.

[1]  Thomas W. Sederberg,et al.  Free-form deformation of solid geometric models , 1986, SIGGRAPH.

[2]  Jean Meunier,et al.  Automatic Computation of Average Brain Models , 1998, MICCAI.

[3]  Ali R. Khan,et al.  Symmetric Data Attachment Terms for Large Deformation Image Registration , 2007, IEEE Transactions on Medical Imaging.

[4]  Paul Suetens,et al.  Construction of a Brain Template from MR Images Using State-of-the-Art Registration and Segmentation Techniques , 2004, MICCAI.

[5]  Alain Trouvé,et al.  Computing Large Deformation Metric Mappings via Geodesic Flows of Diffeomorphisms , 2005, International Journal of Computer Vision.

[6]  Ann-Beth Moller,et al.  National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications , 2012, The Lancet.

[7]  V. Arsigny,et al.  Exponential Barycenters of the Canonical Cartan Connection and Invariant Means on Lie Groups , 2013 .

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

[9]  Daniel Rueckert,et al.  Magnetic resonance imaging of the newborn brain: Manual segmentation of labelled atlases in term-born and preterm infants , 2012, NeuroImage.

[10]  Sébastien Ourselin,et al.  Parametric non-rigid registration using a stationary velocity field , 2012, 2012 IEEE Workshop on Mathematical Methods in Biomedical Image Analysis.

[11]  Karl J. Friston,et al.  Identifying Global Anatomical Differences: Deformation-Based Morphometry , 1998, NeuroImage.

[12]  Alejandro F. Frangi,et al.  Temporal diffeomorphic free-form deformation: Application to motion and strain estimation from 3D echocardiography , 2012, Medical Image Anal..

[13]  Seungyong Lee,et al.  Injectivity Conditions of 2D and 3D Uniform Cubic B-Spline Functions , 2000, Graph. Model..

[14]  Oscar Camara,et al.  Toward the automatic quantification of in utero brain development in 3D structural MRI: A review , 2017, Human brain mapping.

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

[16]  L. R. Dice Measures of the Amount of Ecologic Association Between Species , 1945 .

[17]  Mary Rutherford,et al.  Brain Maturation After Preterm Birth , 2013, Science Translational Medicine.

[18]  Chris Adamson,et al.  A new neonatal cortical and subcortical brain atlas: the Melbourne Children's Regional Infant Brain (M-CRIB) atlas , 2017, NeuroImage.

[19]  Lana Vasung,et al.  The role of neuroimaging in predicting neurodevelopmental outcomes of preterm neonates. , 2014, Clinics in perinatology.

[20]  Peter Lorenzen,et al.  Multi-modal image set registration and atlas formation , 2006, Medical Image Anal..

[21]  Lilla Zöllei,et al.  A unified information theoretic framework for pair- and group-wise registration of medical images , 2006 .

[22]  M. Helfroush,et al.  A Tool to Investigate Symmetry Properties of Newborns Brain: The Newborns' Symmetric Brain Atlas , 2013, ISRN neuroscience.

[23]  Reinhard Grebe,et al.  Symmetric brain atlas template for newborns brain asymmetry studies , 2013, 2013 21st Iranian Conference on Electrical Engineering (ICEE).

[24]  Christos Davatzikos,et al.  Comparative Evaluation of Registration Algorithms in Different Brain Databases With Varying Difficulty: Results and Insights , 2014, IEEE Transactions on Medical Imaging.

[25]  Michael I. Miller,et al.  Multi-contrast human neonatal brain atlas: Application to normal neonate development analysis , 2011, NeuroImage.

[26]  Brian B. Avants,et al.  Explicit B-spline regularization in diffeomorphic image registration , 2013, Front. Neuroinform..

[27]  Ali R. Khan,et al.  Symmetric Data Attachment Terms for Large , 2007 .

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

[29]  U. Grenander,et al.  Computational anatomy: an emerging discipline , 1998 .

[30]  Guido Gerig,et al.  Unbiased diffeomorphic atlas construction for computational anatomy , 2004, NeuroImage.

[31]  Daniel Rueckert,et al.  Groupwise Combined Segmentation and Registration for Atlas Construction , 2007, MICCAI.

[32]  J. Ashburner,et al.  Nonlinear spatial normalization using basis functions , 1999, Human brain mapping.

[33]  D. Louis Collins,et al.  Tuning and Comparing Spatial Normalization Methods , 2003, MICCAI.

[34]  Daniel Rueckert,et al.  The developing human connectome project: A minimal processing pipeline for neonatal cortical surface reconstruction , 2017, NeuroImage.

[35]  Reinhard Grebe,et al.  A Neonatal Bimodal MR-CT Head Template , 2017, PloS one.

[36]  J. Hajnal,et al.  Abnormal Cortical Development after Premature Birth Shown by Altered Allometric Scaling of Brain Growth , 2006, PLoS medicine.

[37]  Daniel Rueckert,et al.  Regional growth and atlasing of the developing human brain , 2016, NeuroImage.

[38]  Marc Alexa,et al.  Linear combination of transformations , 2002, ACM Trans. Graph..

[39]  Mads Nielsen,et al.  Kernel Bundle Diffeomorphic Image Registration Using Stationary Velocity Fields and Wendland Basis Functions , 2016, IEEE Transactions on Medical Imaging.

[40]  Hamid Abrishami Moghaddam,et al.  A neonatal atlas template for spatial normalization of whole-brain magnetic resonance images of newborns: Preliminary results , 2007, NeuroImage.

[41]  Jana Hutter,et al.  Three‐dimensional motion corrected sensitivity encoding reconstruction for multi‐shot multi‐slice MRI: Application to neonatal brain imaging , 2017, Magnetic resonance in medicine.

[42]  Peter Lorenzen,et al.  Unbiased Atlas Formation Via Large Deformations Metric Mapping , 2005, MICCAI.

[43]  Sébastien Ourselin,et al.  A parallel-friendly normalized mutual information gradient for free-form registration , 2009, Medical Imaging.

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

[45]  Colin Studholme,et al.  A template free approach to volumetric spatial normalization of brain anatomy , 2004, Pattern Recognit. Lett..

[46]  J. Gilmore,et al.  Infant Brain Atlases from Neonates to 1- and 2-Year-Olds , 2011, PloS one.

[47]  Nicholas Ayache,et al.  Geometric Means in a Novel Vector Space Structure on Symmetric Positive-Definite Matrices , 2007, SIAM J. Matrix Anal. Appl..

[48]  Daniel Rueckert,et al.  Automatic Whole Brain MRI Segmentation of the Developing Neonatal Brain , 2014, IEEE Transactions on Medical Imaging.

[49]  Colin Studholme Simultaneous Population Based Image Alignment for Template Free Spatial Normalisation of Brain Anatomy , 2003, WBIR.

[50]  Brian B. Avants,et al.  The optimal template effect in hippocampus studies of diseased populations , 2010, NeuroImage.

[51]  P. Thomas Fletcher,et al.  Population Shape Regression from Random Design Data , 2007, 2007 IEEE 11th International Conference on Computer Vision.

[52]  John G. Sled,et al.  Quantitative MRI for studying neonatal brain development , 2013, Neuroradiology.

[53]  Dinggang Shen,et al.  Feature‐based groupwise registration by hierarchical anatomical correspondence detection , 2012, Human brain mapping.

[54]  J C Mazziotta,et al.  Automated image registration: II. Intersubject validation of linear and nonlinear models. , 1998, Journal of computer assisted tomography.

[55]  Daniel Rueckert,et al.  Spatio-temporal Image Analysis for Longitudinal and Time-Series Image Data , 2015, MICCAI 2015.

[56]  Michael I. Miller,et al.  Multi-contrast large deformation diffeomorphic metric mapping for diffusion tensor imaging , 2009, NeuroImage.

[57]  Sébastien Ourselin,et al.  Fast free-form deformation using graphics processing units , 2010, Comput. Methods Programs Biomed..

[58]  Nicholas Ayache,et al.  A Log-Euclidean Framework for Statistics on Diffeomorphisms , 2006, MICCAI.

[59]  Tomoki Arichi,et al.  A dedicated neonatal brain imaging system , 2016, Magnetic resonance in medicine.

[60]  Daniel Rueckert,et al.  Nonrigid registration using free-form deformations: application to breast MR images , 1999, IEEE Transactions on Medical Imaging.

[61]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

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

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

[64]  Brian B. Avants,et al.  Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain , 2008, Medical Image Anal..

[65]  Nicholas Ayache,et al.  Symmetric Log-Domain Diffeomorphic Registration: A Demons-Based Approach , 2008, MICCAI.

[66]  C. Boesch,et al.  Structural and Neurobehavioral Delay in Postnatal Brain Development of Preterm Infants1 , 1996, Pediatric Research.

[67]  Nicholas Ayache,et al.  LCC-Demons: A robust and accurate symmetric diffeomorphic registration algorithm , 2013, NeuroImage.

[68]  Daniel Rueckert,et al.  A Multi-channel 4D Probabilistic Atlas of the Developing Brain: Application to Fetuses and Neonates , 2012 .

[69]  Daniel Rueckert,et al.  Consistent groupwise non-rigid registration for atlas construction , 2004, 2004 2nd IEEE International Symposium on Biomedical Imaging: Nano to Macro (IEEE Cat No. 04EX821).

[70]  Fabrice Heitz,et al.  Symmetric Nonrigid Image Registration: Application to Average Brain Templates Construction , 2008, MICCAI.

[71]  Terry S. Yoo,et al.  Insight into Images: Principles and Practice for Segmentation, Registration, and Image Analysis , 2004 .

[72]  Hong Wang,et al.  Abnormal Cerebral Structure Is Present at Term in Premature Infants , 2005, Pediatrics.

[73]  Simon K. Warfield,et al.  A normative spatiotemporal MRI atlas of the fetal brain for automatic segmentation and analysis of early brain growth , 2017, Scientific Reports.

[74]  Brian B. Avants,et al.  N4ITK: Improved N3 Bias Correction , 2010, IEEE Transactions on Medical Imaging.

[75]  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.

[76]  Daniel Rueckert,et al.  A dynamic 4D probabilistic atlas of the developing brain , 2011, NeuroImage.

[77]  Daniel Rueckert,et al.  Construction of a consistent high-definition spatio-temporal atlas of the developing brain using adaptive kernel regression , 2012, NeuroImage.

[78]  Terrie E. Inder,et al.  MRI of the Neonatal Brain , 2002 .

[79]  Ernesto Zacur,et al.  Algorithms for computing the group exponential of diffeomorphisms: Performance evaluation , 2008, 2008 IEEE Computer Society Conference on Computer Vision and Pattern Recognition Workshops.

[80]  Simon K. Warfield,et al.  Construction of a Deformable Spatiotemporal MRI Atlas of the Fetal Brain: Evaluation of Similarity Metrics and Deformation Models , 2014, MICCAI.

[81]  Dinggang Shen,et al.  HAMMER: hierarchical attribute matching mechanism for elastic registration , 2002, IEEE Transactions on Medical Imaging.

[82]  Monica Hernandez,et al.  Contributions to 3D Diffeomorphic Atlas Estimation: Application to Brain Images , 2007, MICCAI.

[83]  David Rey,et al.  Symmetrization of the Non-rigid Registration Problem Using Inversion-Invariant Energies: Application to Multiple Sclerosis , 2000, MICCAI.

[84]  Daniel Rueckert,et al.  Diffeomorphic Registration Using B-Splines , 2006, MICCAI.