Investigation of spectrally coherent resting‐state networks using non‐negative matrix factorization for functional MRI data

Spontaneous fluctuations of the functional magnetic resonance imaging (fMRI) signal during the resting state have been characterized by the dominant spectral components in the low‐frequency (<0.1 Hz) range. Although previous studies have reported the spatial patterns of activity of the resting‐state network (RSN), the frequency‐dependent characteristics (i.e., spectral coherence) of the resting state activity have not been fully investigated. This article describes the novel application of a non‐negative matrix factorization (NMF) algorithm to the decomposition of the magnitude spectra of fMRI time‐series into distinct spectral components. From the fMRI data of healthy volunteers during the resting state, the frequency‐specific components were decomposed into five basis functions. Group analysis revealed five different spatial patterns associated with these basis functions, in which each of the spatial patterns may correspond to a distinct spectrally coherent RSN. The RSN with the lowest center frequency showed a similar spatial pattern to the “default‐mode” network, which involves the medial superior and middle frontal cortex along with the posterior cingulate cortex. On the other hand, RSNs with higher frequencies were observed mainly in several posterior regions of the brain including the precuneus and lingual gyrus. Subsequent Granger causality analysis demonstrated that these posterior regions may function as the “hubs” of the RSNs, whereas the anterior regions, including the medial superior and middle frontal cortex, may be characterized as “peripheries” of the network. Our proposed analysis scheme provides supplemental information on both spectral and temporal characteristics of the RSNs, which might be used in a range of applications, including those involving clinical populations. © 2011 Wiley Periodicals, Inc. Int J Imaging Syst Technol, 21, 2117–222, 2011

[1]  Rainer Goebel,et al.  Investigating directed cortical interactions in time-resolved fMRI data using vector autoregressive modeling and Granger causality mapping. , 2003, Magnetic resonance imaging.

[2]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Catie Chang,et al.  Influence of heart rate on the BOLD signal: The cardiac response function , 2009, NeuroImage.

[4]  M. D’Esposito,et al.  The variability of human BOLD hemodynamic responses , 1998, NeuroImage.

[5]  Wang Zhan,et al.  Group independent component analysis reveals consistent resting-state networks across multiple sessions , 2008, Brain Research.

[6]  Karl J. Friston,et al.  Variability in fMRI: An Examination of Intersession Differences , 2000, NeuroImage.

[7]  T. Kohonen Self-organized formation of topographically correct feature maps , 1982 .

[8]  Kevin Murphy,et al.  The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced? , 2009, NeuroImage.

[9]  M. Greicius,et al.  Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI , 2004, Proc. Natl. Acad. Sci. USA.

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

[11]  Laura Astolfi,et al.  The Effect of Connectivity on EEG Rhythms, Power Spectral Density and Coherence Among Coupled Neural Populations: Analysis With a Neural Mass Model , 2008, IEEE Transactions on Biomedical Engineering.

[12]  Rainer Goebel,et al.  Mapping directed influence over the brain using Granger causality and fMRI , 2005, NeuroImage.

[13]  Andrzej Cichocki,et al.  Multilayer Nonnegative Matrix Factorization Using Projected Gradient Approaches , 2007, Int. J. Neural Syst..

[14]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[15]  M. Greicius Resting-state functional connectivity in neuropsychiatric disorders , 2008, Current opinion in neurology.

[16]  G. Izmirlian,et al.  Overview of Commonly Used Bioinformatics Methods and Their Applications , 2004, Annals of the New York Academy of Sciences.

[17]  Gilles Pagès,et al.  Theoretical aspects of the SOM algorithm , 1998, Neurocomputing.

[18]  V. Calhoun,et al.  Temporal lobe and “default” hemodynamic brain modes discriminate between schizophrenia and bipolar disorder , 2008, Human brain mapping.

[19]  Lars Kai Hansen,et al.  Mining the posterior cingulate: Segregation between memory and pain components , 2005, NeuroImage.

[20]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[21]  M. Fox,et al.  Resting-state spontaneous fluctuations in brain activity: a new paradigm for presurgical planning using fMRI. , 2009, Academic radiology.

[22]  A. Seth Causal connectivity of evolved neural networks during behavior. , 2005, Network.

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

[24]  Yihong Yang,et al.  Frequency specificity of functional connectivity in brain networks , 2008, NeuroImage.

[25]  Randy L. Buckner,et al.  Unrest at rest: Default activity and spontaneous network correlations , 2007, NeuroImage.

[26]  Alan C. Evans,et al.  Uncovering Intrinsic Modular Organization of Spontaneous Brain Activity in Humans , 2009, PloS one.

[27]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[28]  S. Amari,et al.  Nonnegative Matrix and Tensor Factorization [Lecture Notes] , 2008, IEEE Signal Processing Magazine.

[29]  V. Calhoun,et al.  Changes in the interaction of resting‐state neural networks from adolescence to adulthood , 2009, Human brain mapping.

[30]  E. Formisano,et al.  Functional connectivity as revealed by spatial independent component analysis of fMRI measurements during rest , 2004, Human brain mapping.

[31]  Jean-Marie Dufour,et al.  Testing Causality between Two Vectors in Multivariate Autoregressive Moving Average Models , 1992 .

[32]  A. Laird,et al.  An analysis of functional neuroimaging studies of dorsolateral prefrontal cortical activity in depression , 2006, Psychiatry Research: Neuroimaging.

[33]  M. Greicius,et al.  Resting-state functional connectivity reflects structural connectivity in the default mode network. , 2009, Cerebral cortex.

[34]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[35]  Chih-Jen Lin,et al.  Projected Gradient Methods for Nonnegative Matrix Factorization , 2007, Neural Computation.

[36]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[37]  David A. Snyder,et al.  Non-negative matrix factorization of two-dimensional NMR spectra: application to complex mixture analysis. , 2008, The Journal of chemical physics.

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

[39]  D. Auer Spontaneous low-frequency blood oxygenation level-dependent fluctuations and functional connectivity analysis of the 'resting' brain. , 2008, Magnetic resonance imaging.

[40]  J. Gabrieli,et al.  Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia , 2009, Proceedings of the National Academy of Sciences.

[41]  Vince D. Calhoun,et al.  Hybrid ICA–Bayesian network approach reveals distinct effective connectivity differences in schizophrenia , 2008, NeuroImage.

[42]  V. Menon,et al.  A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks , 2008, Proceedings of the National Academy of Sciences.

[43]  Tuomas Virtanen,et al.  Monaural Sound Source Separation by Nonnegative Matrix Factorization With Temporal Continuity and Sparseness Criteria , 2007, IEEE Transactions on Audio, Speech, and Language Processing.

[44]  Mark W. Woolrich,et al.  Network modelling methods for FMRI , 2011, NeuroImage.

[45]  Jeff H. Duyn,et al.  An adaptive filter for suppression of cardiac and respiratory noise in MRI time series data , 2006, NeuroImage.

[46]  Dardo Tomasi,et al.  Magnetic field shift due to mechanical vibration in functional magnetic resonance imaging , 2005, Magnetic resonance in medicine.

[47]  S. Debener,et al.  Default-mode brain dysfunction in mental disorders: A systematic review , 2009, Neuroscience & Biobehavioral Reviews.

[48]  Daniel S. Margulies,et al.  Recent advances in structural and functional brain imaging studies of attention-deficit/hyperactivity disorder , 2007, Current psychiatry reports.

[49]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[50]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Andrzej Cichocki,et al.  Nonnegative Matrix and Tensor Factorization T , 2007 .

[52]  Teuvo Kohonen,et al.  Self-organized formation of topologically correct feature maps , 2004, Biological Cybernetics.

[53]  Lucas C. Parra,et al.  Nonnegative matrix factorization for rapid recovery of constituent spectra in magnetic resonance chemical shift imaging of the brain , 2004, IEEE Transactions on Medical Imaging.

[54]  Yuzhuo Su,et al.  Spectrum separation resolves partial‐volume effect of MRSI as demonstrated on brain tumor scans , 2008, NMR in biomedicine.

[55]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

[56]  Yoshihiko Koga,et al.  Regional Cerebral Blood Flow Changes after Low-Frequency Transcranial Magnetic Stimulation of the Right Dorsolateral Prefrontal Cortex in Treatment-Resistant Depression , 2008, Neuropsychobiology.

[57]  Satoru Kawai,et al.  An Algorithm for Drawing General Undirected Graphs , 1989, Inf. Process. Lett..

[58]  Vince D. Calhoun,et al.  Investigation of relationships between fMRI brain networks in the spectral domain using ICA and Granger causality reveals distinct differences between schizophrenia patients and healthy controls , 2009, NeuroImage.

[59]  Yijun Liu,et al.  Detecting Functional Connectivity in fMRI Using PCA and Regression Analysis , 2009, Brain Topography.

[60]  Thomas Dierks,et al.  BOLD correlates of EEG alpha phase-locking and the fMRI default mode network , 2009, NeuroImage.

[61]  Gustavo Deco,et al.  The Brain Connectivity Workshops: Moving the frontiers of computational systems neuroscience , 2008, NeuroImage.

[62]  Paul Sajda,et al.  Automated tissue segmentation and blind recovery of 1H MRS imaging spectral patterns of normal and diseased human brain , 2008, NMR in biomedicine.

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

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

[65]  Vince D. Calhoun,et al.  A method for functional network connectivity among spatially independent resting-state components in schizophrenia , 2008, NeuroImage.

[66]  F. Castellanos,et al.  Spontaneous attentional fluctuations in impaired states and pathological conditions: A neurobiological hypothesis , 2007, Neuroscience & Biobehavioral Reviews.

[67]  Gabriele Lohmann,et al.  Using non-negative matrix factorization for single-trial analysis of fMRI data , 2007, NeuroImage.