Advances in computational and statistical diffusion MRI

Computational methods are crucial for the analysis of diffusion magnetic resonance imaging (MRI) of the brain. Computational diffusion MRI can provide rich information at many size scales, including local microstructure measures such as diffusion anisotropies or apparent axon diameters, whole‐brain connectivity information that describes the brain's wiring diagram and population‐based studies in health and disease. Many of the diffusion MRI analyses performed today were not possible five, ten or twenty years ago, due to the requirements for large amounts of computer memory or processor time. In addition, mathematical frameworks had to be developed or adapted from other fields to create new ways to analyze diffusion MRI data. The purpose of this review is to highlight recent computational and statistical advances in diffusion MRI and to put these advances into context by comparison with the more traditional computational methods that are in popular clinical and scientific use. We aim to provide a high‐level overview of interest to diffusion MRI researchers, with a more in‐depth treatment to illustrate selected computational advances.

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[36]  Juan Ruiz-Alzola,et al.  Nonrigid registration of 3D tensor medical data , 2002, Medical Image Anal..

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[38]  Carl-Fredrik Westin,et al.  Spatial normalization of diffusion tensor MRI using multiple channels , 2003, NeuroImage.

[39]  P. Mitra,et al.  Conventions and nomenclature for double diffusion encoding NMR and MRI , 2016, Magnetic resonance in medicine.

[40]  Hui Zhang,et al.  Imaging brain microstructure with diffusion MRI: practicality and applications , 2019, NMR in biomedicine.

[41]  Yogesh Rathi,et al.  On Approximation of Orientation Distributions by Means of Spherical Ridgelets , 2008, IEEE Transactions on Image Processing.

[42]  Zhizhou Wang,et al.  A constrained variational principle for direct estimation and smoothing of the diffusion tensor field from complex DWI , 2004, IEEE Transactions on Medical Imaging.

[43]  Maxime Descoteaux,et al.  Quantitative evaluation of 10 tractography algorithms on a realistic diffusion MR phantom , 2011, NeuroImage.

[44]  Hanno Scharr,et al.  A Riemannian Bayesian Framework for Estimating Diffusion Tensor Images , 2016, International Journal of Computer Vision.

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[47]  Jean-Philippe Thiran,et al.  COMMIT: Convex Optimization Modeling for Microstructure Informed Tractography , 2015, IEEE Transactions on Medical Imaging.

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[52]  Paul M. Thompson,et al.  Segmentation of High Angular Resolution Diffusion MRI Using Sparse Riemannian Manifold Clustering , 2014, IEEE Transactions on Medical Imaging.

[53]  Maxime Descoteaux,et al.  Dipy, a library for the analysis of diffusion MRI data , 2014, Front. Neuroinform..

[54]  D. Leopold,et al.  Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited , 2014, Proceedings of the National Academy of Sciences.

[55]  Ben Jeurissen,et al.  Diffusion MRI fiber tractography of the brain , 2019, NMR in biomedicine.

[56]  Leif Ellingson,et al.  Nonparametric two-sample tests on homogeneous Riemannian manifolds, Cholesky decompositions and Diffusion Tensor Image analysis , 2013, J. Multivar. Anal..

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[59]  James C. Gee,et al.  Spatial transformations of diffusion tensor magnetic resonance images , 2001, IEEE Transactions on Medical Imaging.

[60]  Christophe Lenglet,et al.  A nonparametric Riemannian framework for processing high angular resolution diffusion images and its applications to ODF-based morphometry , 2011, NeuroImage.

[61]  R. Vidal,et al.  A nonparametric Riemannian framework for processing high angular resolution diffusion images (HARDI) , 2009, 2009 IEEE Conference on Computer Vision and Pattern Recognition.

[62]  Olivier Clatz,et al.  Detection of DTI White Matter Abnormalities in Multiple Sclerosis Patients , 2008, MICCAI.

[63]  Maher Moakher,et al.  A rigorous framework for diffusion tensor calculus , 2005, Magnetic resonance in medicine.

[64]  F. Tomasello,et al.  MRI Tractography of Corticospinal Tract and Arcuate Fasciculus in High-Grade Gliomas Performed by Constrained Spherical Deconvolution: Qualitative and Quantitative Analysis , 2015, American Journal of Neuroradiology.

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[66]  Brandon Whitcher,et al.  Statistical group comparison of diffusion tensors via multivariate hypothesis testing , 2007, Magnetic resonance in medicine.

[67]  Andrew Zalesky,et al.  Building connectomes using diffusion MRI: why, how and but , 2017, NMR in biomedicine.

[68]  Carl-Fredrik Westin,et al.  SlicerDMRI: Open Source Diffusion MRI Software for Brain Cancer Research. , 2017, Cancer research.

[69]  P. Basser,et al.  Parametric and non-parametric statistical analysis of DT-MRI data. , 2003, Journal of magnetic resonance.

[70]  Nicholas Ayache,et al.  Three-dimensional multimodal brain warping using the Demons algorithm and adaptive intensity corrections , 2001, IEEE Transactions on Medical Imaging.

[71]  Carl-Fredrik Westin,et al.  Diffusion Tensor and Functional MRI Fusion with Anatomical MRI for Image-Guided Neurosurgery , 2003, MICCAI.

[72]  David K. Yu,et al.  Superficial white matter fiber systems impede detection of long-range cortical connections in diffusion MR tractography , 2015, Proceedings of the National Academy of Sciences.

[73]  Peter J. Basser,et al.  A normal distribution for tensor-valued random variables: applications to diffusion tensor MRI , 2003, IEEE Transactions on Medical Imaging.

[74]  Paul A. Yushkevich,et al.  Deformable registration of diffusion tensor MR images with explicit orientation optimization , 2006, Medical Image Anal..

[75]  L. O'Donnell,et al.  Reconstruction of the arcuate fasciculus for surgical planning in the setting of peritumoral edema using two-tensor unscented Kalman filter tractography , 2015, NeuroImage: Clinical.

[76]  I. Dryden,et al.  Non-Euclidean statistics for covariance matrices, with applications to diffusion tensor imaging , 2009, 0910.1656.

[77]  Flavio Dell'Acqua,et al.  Comment on “The Geometric Structure of the Brain Fiber Pathways” , 2012, Science.

[78]  C. Lebel,et al.  A review of diffusion MRI of typical white matter development from early childhood to young adulthood , 2019, NMR in biomedicine.

[79]  Brian A. Wandell,et al.  Think Global, Act Local; Projectome Estimation with BlueMatter , 2009, MICCAI.

[80]  Jeremy D. Schmahmann,et al.  Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers , 2008, NeuroImage.

[81]  Nico Papinutto,et al.  Identifying preoperative language tracts and predicting postoperative functional recovery using HARDI q-ball fiber tractography in patients with gliomas. , 2016, Journal of neurosurgery.

[82]  Leif Ellingson,et al.  Nonparametric bootstrap of sample means of positive-definite matrices with an application to diffusion-tensor-imaging data analysis , 2017, Commun. Stat. Simul. Comput..

[83]  N. Ayache,et al.  Log‐Euclidean metrics for fast and simple calculus on diffusion tensors , 2006, Magnetic resonance in medicine.

[84]  Daniel C. Alexander,et al.  MicroTrack: An Algorithm for Concurrent Projectome and Microstructure Estimation , 2010, MICCAI.

[85]  Susanne Schnell,et al.  Global fiber reconstruction becomes practical , 2011, NeuroImage.

[86]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[87]  Dinggang Shen,et al.  F-TIMER: Fast Tensor Image Morphing for Elastic Registration , 2010, IEEE Transactions on Medical Imaging.

[88]  P. Elliott,et al.  UK Biobank: An Open Access Resource for Identifying the Causes of a Wide Range of Complex Diseases of Middle and Old Age , 2015, PLoS medicine.

[89]  Chun-Hung Yeh,et al.  Correction for diffusion MRI fibre tracking biases: The consequences for structural connectomic metrics , 2016, NeuroImage.

[90]  Timothy E. J. Behrens,et al.  Measuring macroscopic brain connections in vivo , 2015, Nature Neuroscience.

[91]  Peter Savadjiev,et al.  Harmonizing Diffusion MRI Data Across Multiple Sites and Scanners , 2015, MICCAI.

[92]  N. Makris,et al.  High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity , 2002, Magnetic resonance in medicine.

[93]  A. Connelly,et al.  White matter fiber tractography: why we need to move beyond DTI. , 2013, Journal of neurosurgery.

[94]  Martha Elizabeth Shenton,et al.  Filtered Multitensor Tractography , 2010, IEEE Transactions on Medical Imaging.

[95]  Milan Sonka,et al.  3D Slicer as an image computing platform for the Quantitative Imaging Network. , 2012, Magnetic resonance imaging.

[96]  Jean-Francois Mangin,et al.  A Novel Global Tractography Algorithm Based on an Adaptive Spin Glass Model , 2009, MICCAI.

[97]  Carl-Fredrik Westin,et al.  Nonlinear Registration of Diffusion MR Images Based on Fiber Bundles , 2007, MICCAI.

[98]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[99]  Max A. Viergever,et al.  Sheet Probability Index (SPI): Characterizing the geometrical organization of the white matter with diffusion MRI , 2016, NeuroImage.

[100]  Yogesh Rathi,et al.  Joint Multi-Fiber NODDI Parameter Estimation and Tractography Using the Unscented Information Filter , 2016, Front. Neurosci..

[101]  Rachid Deriche,et al.  High Angular Resolution Diffusion MRI Segmentation Using Region-Based Statistical Surface Evolution , 2009, Journal of Mathematical Imaging and Vision.

[102]  Douglas L. Rosene,et al.  The Geometric Structure of the Brain Fiber Pathways , 2012, Science.

[103]  Tim B. Dyrby,et al.  Orientationally invariant indices of axon diameter and density from diffusion MRI , 2010, NeuroImage.

[104]  Alan Connelly,et al.  SIFT2: Enabling dense quantitative assessment of brain white matter connectivity using streamlines tractography , 2015, NeuroImage.

[105]  J Sijbers,et al.  Multiscale white matter fiber tract coregistration: A new feature‐based approach to align diffusion tensor data , 2006, Magnetic resonance in medicine.

[106]  W. Eric L. Grimson,et al.  Consistency Clustering: A Robust Algorithm for Group-wise Registration, Segmentation and Automatic Atlas Construction in Diffusion MRI , 2009, International Journal of Computer Vision.

[107]  Daniel C. Alexander,et al.  NODDI: Practical in vivo neurite orientation dispersion and density imaging of the human brain , 2012, NeuroImage.

[108]  Michael I. Miller,et al.  Diffeomorphic Matching of Diffusion Tensor Images , 2006, 2006 Conference on Computer Vision and Pattern Recognition Workshop (CVPRW'06).

[109]  Ofer Pasternak,et al.  The effect of metric selection on the analysis of diffusion tensor MRI data , 2010, NeuroImage.

[110]  Flavio Dell'Acqua,et al.  Modelling white matter with spherical deconvolution: How and why? , 2018, NMR in biomedicine.

[111]  Christophe Phillips,et al.  Statistical tests for group comparison of manifold-valued data , 2013, 52nd IEEE Conference on Decision and Control.

[112]  Thomas R. Knösche,et al.  White matter integrity, fiber count, and other fallacies: The do's and don'ts of diffusion MRI , 2013, NeuroImage.

[113]  Carl-Fredrik Westin,et al.  Q-space trajectory imaging for multidimensional diffusion MRI of the human brain , 2016, NeuroImage.

[114]  Evan Calabrese,et al.  Diffusion Tractography in Deep Brain Stimulation Surgery: A Review , 2016, Front. Neuroanat..

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[116]  Alan Connelly,et al.  The effects of SIFT on the reproducibility and biological accuracy of the structural connectome , 2015, NeuroImage.

[117]  Rachid Deriche,et al.  DTI segmentation by statistical surface evolution , 2006, IEEE Transactions on Medical Imaging.

[118]  Rachid Deriche,et al.  Sparse Reconstruction Challenge for diffusion MRI: Validation on a physical phantom to determine which acquisition scheme and analysis method to use? , 2015, Medical Image Anal..

[119]  P. Thomas Fletcher,et al.  Principal Geodesic Analysis on Symmetric Spaces: Statistics of Diffusion Tensors , 2004, ECCV Workshops CVAMIA and MMBIA.

[120]  Benjamin Thyreau,et al.  Voxelwise Multivariate Statistics and Brain-Wide Machine Learning Using the Full Diffusion Tensor , 2011, MICCAI.

[121]  Daniel C. Alexander,et al.  Camino: Open-Source Diffusion-MRI Reconstruction and Processing , 2006 .

[122]  Fabrice Heitz,et al.  Longitudinal change detection in diffusion MRI using multivariate statistical testing on tensors , 2012, NeuroImage.

[123]  J. Fernandez-Miranda,et al.  Advanced diffusion MRI fiber tracking in neurosurgical and neurodegenerative disorders and neuroanatomical studies: A review. , 2014, Biochimica et biophysica acta.

[124]  L. O'Donnell,et al.  Does diffusion MRI tell us anything about the white matter? An overview of methods and pitfalls , 2015, Schizophrenia Research.

[125]  Alexandra J. Golby,et al.  Corticospinal tract modeling for neurosurgical planning by tracking through regions of peritumoral edema and crossing fibers using two-tensor unscented Kalman filter tractography , 2016, International Journal of Computer Assisted Radiology and Surgery.

[126]  Jean-Philippe Thiran,et al.  A convex optimization framework for global tractography , 2013, 2013 IEEE 10th International Symposium on Biomedical Imaging.

[127]  Paul Suetens,et al.  Global tractography of multi-shell diffusion-weighted imaging data using a multi-tissue model , 2015, NeuroImage.

[128]  Olivier Clatz,et al.  DT-REFinD: Diffusion Tensor Registration With Exact Finite-Strain Differential , 2009, IEEE Transactions on Medical Imaging.

[129]  Anuj Srivastava,et al.  Riemannian Analysis of Probability Density Functions with Applications in Vision , 2007, 2007 IEEE Conference on Computer Vision and Pattern Recognition.

[130]  Paul M. Thompson,et al.  Group action induced averaging for HARDI processing , 2012, 2012 9th IEEE International Symposium on Biomedical Imaging (ISBI).

[131]  M. Descoteaux,et al.  Direct native-space fiber bundle alignment for group comparisons , 2014 .

[132]  Alain Trouvé,et al.  Statistical models of sets of curves and surfaces based on currents , 2009, Medical Image Anal..

[133]  R. Deriche,et al.  From Diffusion MRI to Brain Connectomics , 2013 .

[134]  Maher Moakher,et al.  A Differential Geometric Approach to the Geometric Mean of Symmetric Positive-Definite Matrices , 2005, SIAM J. Matrix Anal. Appl..

[135]  Max A. Viergever,et al.  Quantifying the brain's sheet structure with normalized convolution , 2017, Medical Image Anal..

[136]  Jean-Philippe Thiran,et al.  Accelerated Microstructure Imaging via Convex Optimization (AMICO) from diffusion MRI data , 2015, NeuroImage.

[137]  Paul M. Thompson,et al.  Brain Fiber Architecture, Genetics, and Intelligence: A High Angular Resolution Diffusion Imaging (HARDI) Study , 2008, MICCAI.

[138]  Yung-Chin Hsu,et al.  A large deformation diffeomorphic metric mapping solution for diffusion spectrum imaging datasets , 2012, NeuroImage.

[139]  Paul M. Thompson,et al.  Brain Differences Visualized in the Blind Using Tensor Manifold Statistics and Diffusion Tensor Imaging , 2007, 2007 Frontiers in the Convergence of Bioscience and Information Technologies.

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

[141]  Alessandro Daducci,et al.  Microstructure Informed Tractography: Pitfalls and Open Challenges , 2016, Front. Neurosci..

[142]  P. Thomas Fletcher,et al.  Principal geodesic analysis for the study of nonlinear statistics of shape , 2004, IEEE Transactions on Medical Imaging.

[143]  Rachid Deriche,et al.  A Riemannian Framework for Orientation Distribution Function Computing , 2009, MICCAI.

[144]  M. Berger,et al.  Quantifying accuracy and precision of diffusion MR tractography of the corticospinal tract in brain tumors. , 2014, Journal of neurosurgery.

[145]  Mark F. Lythgoe,et al.  Compartment models of the diffusion MR signal in brain white matter: A taxonomy and comparison , 2012, NeuroImage.

[146]  Rachid Deriche,et al.  Statistics on the Manifold of Multivariate Normal Distributions: Theory and Application to Diffusion Tensor MRI Processing , 2006, Journal of Mathematical Imaging and Vision.

[147]  Heidi Johansen-Berg,et al.  Diffusion MRI at 25: Exploring brain tissue structure and function , 2012, NeuroImage.

[148]  Ali R. Khan,et al.  The DTI Challenge: Toward Standardized Evaluation of Diffusion Tensor Imaging Tractography for Neurosurgery , 2015, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[149]  Dinggang Shen,et al.  Large deformation diffeomorphic registration of diffusion-weighted imaging data , 2014, Medical Image Anal..

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

[151]  C. Nimsky Fiber tracking--we should move beyond diffusion tensor imaging. , 2014, World neurosurgery.