Estimation of individual axon bundle properties by a Multi‐Resolution Discrete‐Search method

HighlightsWe present a method for the estimation of the intra‐voxel bundle‐wise diffusion properties for DW‐MRI.Our method overcomes some limitations of most multi‐fiber algorithms and extends them to estimate the diffusion profiles.Our method constraints the sparsity of the axon bundles and uses their spatial redundancy to achieve robustness against noise.We propose a new evaluation metric and a novel methodology for the quantitative evaluation of the methods on in‐vivo data.We present an extensive evaluation on state‐of‐the‐art biophysical synthetic data and on the in‐vivo MASSIVE dataset. Graphical abstract Figure. No caption available. ABSTRACT A stable, accurate and robust‐to‐noise method for the estimation of the intra‐voxel bundle‐wise diffusion properties for diffusion‐weighted magnetic resonance imaging is presented. The proposed method overcomes some of the limitations of most of the multi‐fiber algorithms in the literature and extends them to estimate the diffusion profiles, improving the estimation of the intra‐voxel geometry at challenging microstructure configurations, that is to say: relatively small crossing angles, different voxel‐wise anisotropic diffusion profiles and low SNR. The proposed methodology is based on four key novel ideas: (i) A Multi‐Resolution Discrete‐Search determines the orientation of the fiber bundles accurately and naturally constrains the sparsity on the recovered solutions; (ii) the determination of the number of fiber bundles using the F‐test combined with a Rician bias correction; (iii) a Simultaneous Denoising and Fitting procedure that exploits the spatial redundancy of the axon bundles to achieve robustness with respect to noise; and (iv) a general framework for the estimation of the axial and radial diffusivity parameters independently for each voxel. A new useful evaluation metric is also proposed, which combines the information of the success rate in the estimated number of bundles and the angular error, avoiding in this way, some of the limitations these metrics have individually. A novel methodology for the evaluation of the methods on in‐vivo data is also proposed. This work presents an extensive evaluation: the proposed methodology has been tested on state‐of‐the‐art biophysical synthetic data for a variety of conditions, on the challenging spatially coherent phantom used on the HARDI reconstruction Challenge 2012, and on the recently released in‐vivo MASSIVE data‐set. Our results present significant improvements on the estimation of the number and orientation of the fiber bundles over the Spherical Deconvolution algorithm for multi‐shell data, which is one of the most widely used multi‐fiber algorithm. The results also show that, by the voxel‐wise estimation of the diffusion profiles, the axial and radial diffusivity parameters are robustly estimated, being this essential for a better understanding of the individual bundle diffusion properties at challenging structural configurations.

[1]  P. Hagmann,et al.  Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging , 2005, Magnetic resonance in medicine.

[2]  Baba C. Vemuri,et al.  A Unified Computational Framework for Deconvolution to Reconstruct Multiple Fibers From Diffusion Weighted MRI , 2007, IEEE Transactions on Medical Imaging.

[3]  G. Winston The physical and biological basis of quantitative parameters derived from diffusion MRI. , 2012, Quantitative imaging in medicine and surgery.

[4]  P. Basser,et al.  New modeling and experimental framework to characterize hindered and restricted water diffusion in brain white matter , 2004, Magnetic resonance in medicine.

[5]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[6]  Jürgen Hennig,et al.  Disentangling micro from mesostructure by diffusion MRI: A Bayesian approach , 2017, NeuroImage.

[7]  Timothy Edward John Behrens,et al.  Characterization and propagation of uncertainty in diffusion‐weighted MR imaging , 2003, Magnetic resonance in medicine.

[8]  Dmitry S. Novikov,et al.  Mesoscopic structure of neuronal tracts from time-dependent diffusion , 2015, NeuroImage.

[9]  Jean-Philippe Thiran,et al.  Sparse regularization for fiber ODF reconstruction: from the suboptimality of $\ell_2$ and $\ell_1$ priors to $\ell_0$ , 2012, 1208.2247.

[10]  Alan Connelly,et al.  Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution , 2004, NeuroImage.

[11]  P. Lauterbur,et al.  Apparent diffusion tensor measurements in myelin‐deficient rat spinal cords , 2001, Magnetic resonance in medicine.

[12]  D. Tuch Q‐ball imaging , 2004, Magnetic resonance in medicine.

[13]  Chun-Hung Yeh,et al.  Resolving crossing fibres using constrained spherical deconvolution: Validation using diffusion-weighted imaging phantom data , 2008, NeuroImage.

[14]  Giuseppe Scotti,et al.  A Model-Based Deconvolution Approach to Solve Fiber Crossing in Diffusion-Weighted MR Imaging , 2007, IEEE Transactions on Biomedical Engineering.

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

[16]  Simon K. Warfield,et al.  Parametric Representation of Multiple White Matter Fascicles from Cube and Sphere Diffusion MRI , 2012, PloS one.

[17]  G. Sapiro,et al.  Reconstruction of the orientation distribution function in single‐ and multiple‐shell q‐ball imaging within constant solid angle , 2010, Magnetic resonance in medicine.

[18]  C. Beaulieu,et al.  The basis of anisotropic water diffusion in the nervous system – a technical review , 2002, NMR in biomedicine.

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

[20]  Daniel C. Alexander,et al.  Bingham–NODDI: Mapping anisotropic orientation dispersion of neurites using diffusion MRI , 2016, NeuroImage.

[21]  P. Basser,et al.  Axcaliber: A method for measuring axon diameter distribution from diffusion MRI , 2008, Magnetic resonance in medicine.

[22]  J. Tropp Algorithms for simultaneous sparse approximation. Part II: Convex relaxation , 2006, Signal Process..

[23]  Jan Sijbers,et al.  Multi-tissue constrained spherical deconvolution for improved analysis of multi-shell diffusion MRI data , 2014, NeuroImage.

[24]  Pierrick Coupé,et al.  Rician Noise Removal by Non-Local Means Filtering for Low Signal-to-Noise Ratio MRI: Applications to DT-MRI , 2008, MICCAI.

[25]  Mariano Rivera,et al.  Diffusion Basis Functions Decomposition for Estimating White Matter Intravoxel Fiber Geometry , 2007, IEEE Transactions on Medical Imaging.

[26]  Joel A. Tropp,et al.  Algorithms for simultaneous sparse approximation. Part I: Greedy pursuit , 2006, Signal Process..

[27]  P. Callaghan,et al.  Diffraction-like effects in NMR diffusion studies of fluids in porous solids , 1991, Nature.

[28]  Jelle Veraart,et al.  In vivo observation and biophysical interpretation of time-dependent diffusion in human white matter , 2016, NeuroImage.

[29]  T. Nakada,et al.  Absolute eigenvalue diffusion tensor analysis for human brain maturation , 2003, NMR in biomedicine.

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

[31]  John Russell,et al.  Dysmyelination Revealed through MRI as Increased Radial (but Unchanged Axial) Diffusion of Water , 2002, NeuroImage.

[32]  Paul Suetens,et al.  Convex Non-negative Spherical Factorization of Multi-Shell Diffusion-Weighted Images , 2015, MICCAI.

[33]  Chun-Hung Yeh,et al.  Diffusion orientation transform revisited , 2010, NeuroImage.

[34]  F. Kruggel,et al.  Quantitative mapping of the per‐axon diffusion coefficients in brain white matter , 2015, Magnetic resonance in medicine.

[35]  W. Tseng,et al.  Sparse Solution of Fiber Orientation Distribution Function by Diffusion Decomposition , 2013, PloS one.

[36]  David L Donoho,et al.  Compressed sensing , 2006, IEEE Transactions on Information Theory.

[37]  Giovanna Rizzo,et al.  Noise Correction on Rician Distributed Data for Fibre Orientation Estimators , 2008, IEEE Transactions on Medical Imaging.

[38]  Derek K. Jones,et al.  Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging , 2013, Human brain mapping.

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

[40]  Carl-Fredrik Westin,et al.  Multi-Diffusion-Tensor Fitting via Spherical Deconvolution: A Unifying Framework , 2010, MICCAI.

[41]  Giuseppe Scotti,et al.  A modified damped Richardson–Lucy algorithm to reduce isotropic background effects in spherical deconvolution , 2010, NeuroImage.

[42]  M. Catani,et al.  Diffusion-based tractography in neurological disorders: concepts, applications, and future developments , 2008, The Lancet Neurology.

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

[44]  Baba C. Vemuri,et al.  Regularized positive-definite fourth order tensor field estimation from DW-MRI , 2009, NeuroImage.

[45]  D. Louis Collins,et al.  Diffusion Weighted Image Denoising Using Overcomplete Local PCA , 2013, PloS one.

[46]  Matt Hall,et al.  Resolving axon fiber crossings at clinical b-values: an evaluation study. , 2011, Medical physics.

[47]  Baba C. Vemuri,et al.  Resolution of complex tissue microarchitecture using the diffusion orientation transform (DOT) , 2006, NeuroImage.

[48]  Lester Melie-García,et al.  Deconvolution in diffusion spectrum imaging , 2010, NeuroImage.

[49]  Paul L. Rosin,et al.  A pitfall in the reconstruction of fibre ODFs using spherical deconvolution of diffusion MRI data , 2013, NeuroImage.

[50]  R. Henkelman Measurement of signal intensities in the presence of noise in MR images. , 1985, Medical physics.

[51]  P. Basser,et al.  Estimation of the effective self-diffusion tensor from the NMR spin echo. , 1994, Journal of magnetic resonance. Series B.

[52]  B W Kreher,et al.  Multitensor approach for analysis and tracking of complex fiber configurations , 2005, Magnetic resonance in medicine.

[53]  M. Horsfield,et al.  Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging , 1999, Magnetic resonance in medicine.

[54]  Christophe Lenglet,et al.  Estimating Orientation Distribution Functions with Probability Density Constraints and Spatial Regularity , 2009, MICCAI.

[55]  D. Alexander A general framework for experiment design in diffusion MRI and its application in measuring direct tissue‐microstructure features , 2008, Magnetic resonance in medicine.

[56]  T. Mareci,et al.  Generalized diffusion tensor imaging and analytical relationships between diffusion tensor imaging and high angular resolution diffusion imaging , 2003, Magnetic resonance in medicine.

[57]  Martijn Froeling,et al.  “MASSIVE” brain dataset: Multiple acquisitions for standardization of structural imaging validation and evaluation , 2017, Magnetic resonance in medicine.

[58]  Valerij G. Kiselev,et al.  Fiber Continuity: An Anisotropic Prior for ODF Estimation , 2011, IEEE Transactions on Medical Imaging.

[59]  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.

[60]  Alan Connelly,et al.  MRtrix: Diffusion tractography in crossing fiber regions , 2012, Int. J. Imaging Syst. Technol..

[61]  H. Gudbjartsson,et al.  The rician distribution of noisy mri data , 1995, Magnetic resonance in medicine.

[62]  Kalvis M. Jansons,et al.  Persistent angular structure: new insights from diffusion magnetic resonance imaging data , 2003 .

[63]  P. Basser,et al.  In vivo measurement of axon diameter distribution in the corpus callosum of rat brain. , 2009, Brain : a journal of neurology.

[64]  C. Wheeler-Kingshott,et al.  A ranking of diffusion MRI compartment models with in vivo human brain data , 2013, Magnetic resonance in medicine.

[65]  Guillermo Sapiro,et al.  Non-local sparse models for image restoration , 2009, 2009 IEEE 12th International Conference on Computer Vision.

[66]  Mark W. Woolrich,et al.  Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? , 2007, NeuroImage.

[67]  P. Basser,et al.  Diffusion tensor MR imaging of the human brain. , 1996, Radiology.

[68]  Lawrence L. Wald,et al.  White matter compartment models for in vivo diffusion MRI at 300mT/m , 2015, NeuroImage.

[69]  Hui Zhang,et al.  Axon diameter mapping in the presence of orientation dispersion with diffusion MRI , 2011, NeuroImage.

[70]  A. Scheibel,et al.  Fiber composition of the human corpus callosum , 1992, Brain Research.

[71]  Leandro Beltrachini,et al.  Neural Processing of Emotional Facial and Semantic Expressions in Euthymic Bipolar Disorder (BD) and Its Association with Theory of Mind (ToM) , 2012, PloS one.

[72]  Alessandro Foi,et al.  Image Denoising by Sparse 3-D Transform-Domain Collaborative Filtering , 2007, IEEE Transactions on Image Processing.

[73]  M. Smith,et al.  An unbiased signal-to-noise ratio measure for magnetic resonance images. , 1993, Medical physics.

[74]  A. Romano,et al.  Pre-surgical planning and MR-tractography utility in brain tumour resection , 2009, European Radiology.

[75]  Alan Connelly,et al.  Robust determination of the fibre orientation distribution in diffusion MRI: Non-negativity constrained super-resolved spherical deconvolution , 2007, NeuroImage.

[76]  Jean-Philippe Thiran,et al.  Structured sparsity for spatially coherent fibre orientation estimation in diffusion MRI , 2015, NeuroImage.

[77]  Rachid Deriche,et al.  Quantitative Comparison of Reconstruction Methods for Intra-Voxel Fiber Recovery From Diffusion MRI , 2014, IEEE Transactions on Medical Imaging.

[78]  Santiago Aja-Fernández,et al.  DWI filtering using joint information for DTI and HARDI , 2010, Medical Image Anal..