Integrated Construction of Multimodal Atlases with Structural Connectomes in the Space of Riemannian Metrics

The structural network of the brain, or structural connectome, can be represented by fiber bundles generated by a variety of tractography methods. While such methods give qualitative insights into brain structure, there is controversy over whether they can provide quantitative information, especially at the population level. In order to enable populationlevel statistical analysis of the structural connectome, we propose representing a connectome as a Riemannian metric, which is a point on an infinite-dimensional manifold. We equip this manifold with the Ebin metric, a natural metric structure for this space, to get a Riemannian manifold along with its associated geometric properties. We then use this Riemannian framework to apply object-oriented statistical analysis to define an atlas as the Fréchet mean of a population of Riemannian metrics. This formulation ties into the existing framework for diffeomorphic construction of image atlases, allowing us to construct a multimodal atlas by simultaneously integrating complementary white matter structure details from DWMRI and cortical details from T1-weighted MRI. We illustrate our framework with 2D data examples of connectome registration and atlas formation. Finally, we build an example 3D multimodal atlas using T1 images and connectomes derived from diffusion tensors estimated from a subset of subjects from the Human Connectome Project.

[1]  B. Dewitt Quantum Theory of Gravity. I. The Canonical Theory , 1967 .

[2]  David G. Ebin,et al.  The manifold of Riemannian metrics , 1970 .

[3]  D. Freed,et al.  The basic geometry of the manifold of Riemannian metrics and of its quotient by the diffeomorphism group. , 1989 .

[4]  Peter W. Michor,et al.  THE RIEMANNIAN MANIFOLD OF ALL RIEMANNIAN METRICS , 1991 .

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

[6]  P. Basser,et al.  In vivo fiber tractography using DT‐MRI data , 2000, Magnetic resonance in medicine.

[7]  Michael I. Miller,et al.  Landmark matching via large deformation diffeomorphisms , 2000, IEEE Trans. Image Process..

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

[9]  Carl-Fredrik Westin,et al.  New Approaches to Estimation of White Matter Connectivity in Diffusion Tensor MRI: Elliptic PDEs and Geodesics in a Tensor-Warped Space , 2002, MICCAI.

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

[11]  Rachid Deriche,et al.  Inferring White Matter Geometry from Di.usion Tensor MRI: Application to Connectivity Mapping , 2004, ECCV.

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

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

[14]  Joan Alexis Glaunès,et al.  Surface Matching via Currents , 2005, IPMI.

[15]  K. Amunts,et al.  Towards multimodal atlases of the human brain , 2006, Nature Reviews Neuroscience.

[16]  Timothy Edward John Behrens,et al.  A Bayesian framework for global tractography , 2007, NeuroImage.

[17]  Ross T. Whitaker,et al.  Interactive Visualization of Volumetric White Matter Connectivity in DT-MRI Using a Parallel-Hardware Hamilton-Jacobi Solver , 2007, IEEE Transactions on Visualization and Computer Graphics.

[18]  P. Thomas Fletcher,et al.  Riemannian geometry for the statistical analysis of diffusion tensor data , 2007, Signal Process..

[19]  Hans Johnson,et al.  BRAINSFit: Mutual Information Registrations of Whole-Brain 3D Images, Using the Insight Toolkit , 2007, The Insight Journal.

[20]  Ross T. Whitaker,et al.  A Volumetric Approach to Quantifying Region-to-Region White Matter Connectivity in Diffusion Tensor MRI , 2007, IPMI.

[21]  Brian B. Avants,et al.  Multivariate Normalization with Symmetric Diffeomorphisms for Multivariate Studies , 2007, MICCAI.

[22]  Carl-Fredrik Westin,et al.  Automatic Tractography Segmentation Using a High-Dimensional White Matter Atlas , 2007, IEEE Transactions on Medical Imaging.

[23]  Arthur W. Toga,et al.  Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template , 2008, NeuroImage.

[24]  Michael I. Miller,et al.  Large Deformation Diffeomorphic Metric Curve Mapping , 2008, International Journal of Computer Vision.

[25]  B. Clarke The Completion of the Manifold of Riemannian Metrics , 2009, 0904.0177.

[26]  B. Clarke Geodesics, distance, and the CAT(0) property for the manifold of Riemannian metrics , 2010, 1011.1521.

[27]  Carl-Fredrik Westin,et al.  Unbiased Groupwise Registration of White Matter Tractography , 2012, MICCAI.

[28]  Baba C. Vemuri,et al.  Recursive Karcher Expectation Estimators And Geometric Law of Large Numbers , 2013, AISTATS.

[29]  B. Khesin,et al.  Geometry of Diffeomorphism Groups, Complete integrability and Geometric statistics , 2013 .

[30]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

[31]  Ross T. Whitaker,et al.  Improved segmentation of white matter tracts with adaptive Riemannian metrics , 2014, Medical Image Anal..

[32]  Andrea Fuster,et al.  Adjugate Diffusion Tensors for Geodesic Tractography in White Matter , 2015, Journal of Mathematical Imaging and Vision.

[33]  Baba C. Vemuri,et al.  Tractography From HARDI Using an Intrinsic Unscented Kalman Filter , 2015, IEEE Transactions on Medical Imaging.

[34]  Martin Bauer,et al.  Diffeomorphic Density Matching by Optimal Information Transport , 2015, SIAM J. Imaging Sci..

[35]  K. Alexander To the Quantum Theory of Gravity , 2015 .

[36]  Klas Modin,et al.  Generalized Hunter–Saxton Equations, Optimal Information Transport, and Factorization of Diffeomorphisms , 2012, 1203.4463.

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

[38]  Nicholas Ayache,et al.  A Framework for Creating Population Specific Multimodal Brain Atlas Using Clinical T1 and Diffusion Tensor Images , 2016 .

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

[40]  Yogesh Rathi,et al.  An anatomically curated fiber clustering white matter atlas for consistent white matter tract parcellation across the lifespan , 2018, NeuroImage.

[41]  Sandip S. Panesar,et al.  Population-Averaged Atlas of the Macroscale Human Structural Connectome and Its Network Topology , 2018 .

[42]  Timothy D. Verstynen,et al.  Population-averaged atlas of the macroscale human structural connectome and its network topology , 2018, NeuroImage.

[43]  Yonggang Shi,et al.  Topographic Filtering of Tractograms as Vector Field Flows , 2019, MICCAI.

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

[45]  Christian Osendorfer,et al.  Deep Iterative Surface Normal Estimation , 2019, 2020 IEEE/CVF Conference on Computer Vision and Pattern Recognition (CVPR).

[46]  Joseph V. Hajnal,et al.  Multi-channel Registration for Diffusion MRI: Longitudinal Analysis for the Neonatal Brain , 2020, WBIR.

[47]  Carl-Fredrik Westin,et al.  SlicerDMRI: Diffusion MRI and Tractography Research Software for Brain Cancer Surgery Planning and Visualization , 2020, JCO clinical cancer informatics.

[48]  Andrea Fuster,et al.  Geodesic Tubes for Uncertainty Quantification in Diffusion MRI , 2021, IPMI.

[49]  P. Thomas Fletcher,et al.  Structural Connectome Atlas Construction in the Space of Riemannian Metrics , 2021, IPMI.