Finding imaging patterns of structural covariance via Non-Negative Matrix Factorization

In this paper, we investigate the use of Non-Negative Matrix Factorization (NNMF) for the analysis of structural neuroimaging data. The goal is to identify the brain regions that co-vary across individuals in a consistent way, hence potentially being part of underlying brain networks or otherwise influenced by underlying common mechanisms such as genetics and pathologies. NNMF offers a directly data-driven way of extracting relatively localized co-varying structural regions, thereby transcending limitations of Principal Component Analysis (PCA), Independent Component Analysis (ICA) and other related methods that tend to produce dispersed components of positive and negative loadings. In particular, leveraging upon the well known ability of NNMF to produce parts-based representations of image data, we derive decompositions that partition the brain into regions that vary in consistent ways across individuals. Importantly, these decompositions achieve dimensionality reduction via highly interpretable ways and generalize well to new data as shown via split-sample experiments. We empirically validate NNMF in two data sets: i) a Diffusion Tensor (DT) mouse brain development study, and ii) a structural Magnetic Resonance (sMR) study of human brain aging. We demonstrate the ability of NNMF to produce sparse parts-based representations of the data at various resolutions. These representations seem to follow what we know about the underlying functional organization of the brain and also capture some pathological processes. Moreover, we show that these low dimensional representations favorably compare to descriptions obtained with more commonly used matrix factorization methods like PCA and ICA.

[1]  Sarah E. MacPherson,et al.  Age, executive function, and social decision making: a dorsolateral prefrontal theory of cognitive aging. , 2002, Psychology and aging.

[2]  Stefan Klöppel,et al.  Multivariate models of inter-subject anatomical variability , 2011, NeuroImage.

[3]  D. Louis Collins,et al.  MRI-Based Automated Computer Classification of Probable AD Versus Normal Controls , 2008, IEEE Transactions on Medical Imaging.

[4]  A. Dale,et al.  Thinning of the cerebral cortex in aging. , 2004, Cerebral cortex.

[5]  Hangyi Jiang,et al.  DtiStudio: Resource program for diffusion tensor computation and fiber bundle tracking , 2006, Comput. Methods Programs Biomed..

[6]  Christos Davatzikos,et al.  Quantification of brain maturation and growth patterns in C57BL/6J mice via computational neuroanatomy of diffusion tensor images. , 2008, Cerebral cortex.

[7]  Jens C. Pruessner,et al.  Regional Frontal Cortical Volumes Decrease Differentially in Aging: An MRI Study to Compare Volumetric Approaches and Voxel-Based Morphometry , 2002, NeuroImage.

[8]  Karl J. Friston,et al.  Identifying global anatomical differences: Deformation‐based morphometry , 1998 .

[9]  Mattias Höglund,et al.  Non-Negative Matrix Factorization for the Analysis of Complex Gene Expression Data: Identification of Clinically Relevant Tumor Subtypes , 2008, Cancer informatics.

[10]  S. Resnick,et al.  Longitudinal Magnetic Resonance Imaging Studies of Older Adults: A Shrinking Brain , 2003, The Journal of Neuroscience.

[11]  D. Louis Collins,et al.  Whole-brain voxel-based statistical analysis of gray matter and white matter in temporal lobe epilepsy , 2004, NeuroImage.

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

[13]  J. Cardoso,et al.  Blind beamforming for non-gaussian signals , 1993 .

[14]  Sotirios A. Tsaftaris,et al.  Medical Image Computing and Computer Assisted Intervention , 2017 .

[15]  A. Caprihan,et al.  Application of principal component analysis to distinguish patients with schizophrenia from healthy controls based on fractional anisotropy measurements , 2008, NeuroImage.

[16]  Karthik Devarajan,et al.  Nonnegative Matrix Factorization: An Analytical and Interpretive Tool in Computational Biology , 2008, PLoS Comput. Biol..

[17]  F. Gonzalez-Lima,et al.  Structural equation modeling and its application to network analysis in functional brain imaging , 1994 .

[18]  Dinggang Shen,et al.  Very High-Resolution Morphometry Using Mass-Preserving Deformations and HAMMER Elastic Registration , 2003, NeuroImage.

[19]  Christos Davatzikos,et al.  Imaging patterns of brain development and their relationship to cognition. , 2015, Cerebral cortex.

[20]  O. Sporns,et al.  The economy of brain network organization , 2012, Nature Reviews Neuroscience.

[21]  Philip M. Kim,et al.  Subsystem identification through dimensionality reduction of large-scale gene expression data. , 2003, Genome research.

[22]  J. V. Haxby,et al.  Spatial Pattern Analysis of Functional Brain Images Using Partial Least Squares , 1996, NeuroImage.

[23]  A. Toga,et al.  Mapping brain asymmetry , 2003, Nature Reviews Neuroscience.

[24]  P. Paatero,et al.  Positive matrix factorization: A non-negative factor model with optimal utilization of error estimates of data values† , 1994 .

[25]  Erkki Oja,et al.  Independent component analysis: algorithms and applications , 2000, Neural Networks.

[26]  Keith A. Young,et al.  The functional connectivity of the human caudate: An application of meta-analytic connectivity modeling with behavioral filtering , 2012, NeuroImage.

[27]  A. Dale,et al.  High consistency of regional cortical thinning in aging across multiple samples. , 2009, Cerebral cortex.

[28]  Alan C. Evans,et al.  A nonparametric method for automatic correction of intensity nonuniformity in MRI data , 1998, IEEE Transactions on Medical Imaging.

[29]  Christos Boutsidis,et al.  SVD based initialization: A head start for nonnegative matrix factorization , 2008, Pattern Recognit..

[30]  E. Bullmore,et al.  Imaging structural co-variance between human brain regions , 2013, Nature Reviews Neuroscience.

[31]  R. Tibshirani,et al.  A penalized matrix decomposition, with applications to sparse principal components and canonical correlation analysis. , 2009, Biostatistics.

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

[33]  G. Paxinos,et al.  Atlas of the Human Brain , 2000 .

[34]  I Daubechies,et al.  Independent component analysis for brain fMRI does not select for independence , 2009 .

[35]  Alexander J. Smola,et al.  Support Vector Regression Machines , 1996, NIPS.

[36]  Karl J. Friston,et al.  Cerebral Asymmetry and the Effects of Sex and Handedness on Brain Structure: A Voxel-Based Morphometric Analysis of 465 Normal Adult Human Brains , 2001, NeuroImage.

[37]  Bruce Fischl,et al.  Genetic topography of brain morphology , 2013, Proceedings of the National Academy of Sciences.

[38]  Chih-Jen Lin,et al.  LIBSVM: A library for support vector machines , 2011, TIST.

[39]  Brian B. Avants,et al.  Sparse canonical correlation analysis relates network-level atrophy to multivariate cognitive measures in a neurodegenerative population , 2014, NeuroImage.

[40]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[41]  P. Smaragdis,et al.  Non-negative matrix factorization for polyphonic music transcription , 2003, 2003 IEEE Workshop on Applications of Signal Processing to Audio and Acoustics (IEEE Cat. No.03TH8684).

[42]  D. Marcus,et al.  White matter lesions are prevalent but differentially related with cognition in aging and early Alzheimer disease. , 2005, Archives of neurology.

[43]  Alan C. Evans,et al.  Structural asymmetries in the human brain: a voxel-based statistical analysis of 142 MRI scans. , 2001, Cerebral cortex.

[44]  Anthony Randal McIntosh,et al.  Partial least squares analysis of neuroimaging data: applications and advances , 2004, NeuroImage.

[45]  Christos Davatzikos,et al.  DTI-DROID: Diffusion tensor imaging-deformable registration using orientation and intensity descriptors , 2010 .

[46]  Christos Davatzikos,et al.  Spatiotemporal maturation patterns of murine brain quantified by diffusion tensor MRI and deformation-based morphometry , 2005, Proc. Natl. Acad. Sci. USA.

[47]  Janaina Mourão Miranda,et al.  Classifying brain states and determining the discriminating activation patterns: Support Vector Machine on functional MRI data , 2005, NeuroImage.

[48]  Eileen Luders,et al.  Brain maturation: Predicting individual BrainAGE in children and adolescents using structural MRI , 2012, NeuroImage.

[49]  Patrik O. Hoyer,et al.  Non-negative Matrix Factorization with Sparseness Constraints , 2004, J. Mach. Learn. Res..

[50]  Norbert Schuff,et al.  Deformation tensor morphometry of semantic dementia with quantitative validation , 2004, NeuroImage.

[51]  S Makeig,et al.  Analysis of fMRI data by blind separation into independent spatial components , 1998, Human brain mapping.

[52]  Erkki Oja,et al.  Linear and Nonlinear Projective Nonnegative Matrix Factorization , 2010, IEEE Transactions on Neural Networks.

[53]  Ben Taskar,et al.  Generative-Discriminative Basis Learning for Medical Imaging , 2012, IEEE Transactions on Medical Imaging.

[54]  Ben Taskar,et al.  A General and Unifying Framework for Feature Construction, in Image-Based Pattern Classification , 2009, IPMI.

[55]  R. Woods,et al.  Principal Component Analysis and the Scaled Subprofile Model Compared to Intersubject Averaging and Statistical Parametric Mapping: I. “Functional Connectivity” of the Human Motor System Studied with [15O]Water PET , 1995, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[56]  Yasser Ghanbari,et al.  Dominant Component Analysis of Electrophysiological Connectivity Networks , 2012, MICCAI.

[57]  Thomas S. Huang,et al.  Graph Regularized Nonnegative Matrix Factorization for Data Representation. , 2011, IEEE transactions on pattern analysis and machine intelligence.

[58]  Xin Liu,et al.  Document clustering based on non-negative matrix factorization , 2003, SIGIR.

[59]  E. Oja,et al.  Independent Component Analysis , 2013 .

[60]  Karl J. Friston,et al.  Dynamic discrimination analysis: A spatial–temporal SVM , 2007, NeuroImage.

[61]  L. Pantoni Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges , 2010, The Lancet Neurology.

[62]  Alan C. Evans,et al.  3D Anatomical Atlas of the Human Brain , 1998, NeuroImage.

[63]  Stephen M. Smith,et al.  Probabilistic independent component analysis for functional magnetic resonance imaging , 2004, IEEE Transactions on Medical Imaging.

[64]  Jonathan D. Power,et al.  Prediction of Individual Brain Maturity Using fMRI , 2010, Science.

[65]  C. Olson,et al.  Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. , 1992, Cerebral cortex.

[66]  Anthony Randal McIntosh,et al.  Partial Least Squares (PLS) methods for neuroimaging: A tutorial and review , 2011, NeuroImage.

[67]  Jorma Laaksonen,et al.  Projective Non-Negative Matrix Factorization with Applications to Facial Image Processing , 2007, Int. J. Pattern Recognit. Artif. Intell..

[68]  Christos Davatzikos,et al.  Voxel-Based Morphometry Using the RAVENS Maps: Methods and Validation Using Simulated Longitudinal Atrophy , 2001, NeuroImage.

[69]  Jean-Franois Cardoso High-Order Contrasts for Independent Component Analysis , 1999, Neural Computation.

[70]  Christos Davatzikos,et al.  Unsupervised Learning of Functional Network Dynamics in Resting State fMRI , 2013, IPMI.

[71]  S. Resnick,et al.  An image-processing system for qualitative and quantitative volumetric analysis of brain images. , 1998, Journal of computer assisted tomography.

[72]  Anastasios Tefas,et al.  Exploiting discriminant information in nonnegative matrix factorization with application to frontal face verification , 2006, IEEE Transactions on Neural Networks.

[73]  Karl J. Friston,et al.  Functional Connectivity: The Principal-Component Analysis of Large (PET) Data Sets , 1993, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[74]  Pablo Tamayo,et al.  Metagenes and molecular pattern discovery using matrix factorization , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[75]  H. Sebastian Seung,et al.  Learning the parts of objects by non-negative matrix factorization , 1999, Nature.

[76]  J. Pekar,et al.  A method for making group inferences from functional MRI data using independent component analysis , 2001, Human brain mapping.

[77]  Jérôme Idier,et al.  Algorithms for Nonnegative Matrix Factorization with the β-Divergence , 2010, Neural Computation.

[78]  Erkki Oja,et al.  Independent Component Analysis , 2001 .

[79]  Efstathios D. Gennatas,et al.  Network-level structural covariance in the developing brain , 2010, Proceedings of the National Academy of Sciences.

[80]  Jerry L. Prince,et al.  Adaptive fuzzy segmentation of magnetic resonance images , 1999, IEEE Transactions on Medical Imaging.

[81]  A. McIntosh,et al.  Multivariate statistical analyses for neuroimaging data. , 2013, Annual review of psychology.

[82]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[83]  Tamir Hazan,et al.  Non-negative tensor factorization with applications to statistics and computer vision , 2005, ICML.

[84]  Lucie N. Hutchins,et al.  Position-dependent motif characterization using non-negative matrix factorization , 2008, Bioinform..

[85]  Alan C. Evans,et al.  Growth patterns in the developing brain detected by using continuum mechanical tensor maps , 2000, Nature.

[86]  L. K. Hansen,et al.  Generalizable Patterns in Neuroimaging: How Many Principal Components? , 1999, NeuroImage.

[87]  Michael W. L. Chee,et al.  Improvement of brain segmentation accuracy by optimizing non-uniformity correction using N3 , 2009, NeuroImage.

[88]  Nick C Fox,et al.  Imaging of onset and progression of Alzheimer's disease with voxel-compression mapping of serial magnetic resonance images , 2001, The Lancet.

[89]  Stefan Klöppel,et al.  Estimating the age of healthy subjects from T1-weighted MRI scans using kernel methods: Exploring the influence of various parameters , 2010, NeuroImage.

[90]  B. Miller,et al.  Neurodegenerative Diseases Target Large-Scale Human Brain Networks , 2009, Neuron.

[91]  John Ashburner,et al.  Computational anatomy with the SPM software. , 2009, Magnetic resonance imaging.

[92]  R. Malach,et al.  When the Brain Loses Its Self: Prefrontal Inactivation during Sensorimotor Processing , 2006, Neuron.

[93]  A. Owen,et al.  Anterior prefrontal cortex: insights into function from anatomy and neuroimaging , 2004, Nature Reviews Neuroscience.

[94]  H. Hotelling Relations Between Two Sets of Variates , 1936 .

[95]  H. Knutsson,et al.  Detection of neural activity in functional MRI using canonical correlation analysis , 2001, Magnetic resonance in medicine.