A parcellation scheme based on von Mises-Fisher distributions and Markov random fields for segmenting brain regions using resting-state fMRI

Understanding the organization of the human brain requires identification of its functional subdivisions. Clustering schemes based on resting-state functional magnetic resonance imaging (fMRI) data are rapidly emerging as non-invasive alternatives to cytoarchitectonic mapping in postmortem brains. Here, we propose a novel spatio-temporal probabilistic parcellation scheme that overcomes major weaknesses of existing approaches by (i) modeling the fMRI time series of a voxel as a von Mises-Fisher distribution, which is widely used for clustering high dimensional data; (ii) modeling the latent cluster labels as a Markov random field, which provides spatial regularization on the cluster labels by penalizing neighboring voxels having different cluster labels; and (iii) introducing a prior on the number of labels, which helps in uncovering the number of clusters automatically from the data. Cluster labels and model parameters are estimated by an iterative expectation maximization procedure wherein, given the data and current estimates of model parameters, the latent cluster labels, are computed using α-expansion, a state of the art graph cut, method. In turn, given the current estimates of cluster labels, model parameters are estimated by maximizing the pseudo log-likelihood. The performance of the proposed method is validated using extensive computer simulations. Using novel stability analysis we examine the sensitivity of our methods to parameter initialization and demonstrate that the method is robust to a wide range of initial parameter values. We demonstrate the application of our methods by parcellating spatially contiguous as well as non-contiguous brain regions at both the individual participant and group levels. Notably, our analyses yield new data on the posterior boundaries of the supplementary motor area and provide new insights into functional organization of the insular cortex. Taken together, our findings suggest that our method is a powerful tool for investigating functional subdivisions in the human brain.

[1]  Polina Golland,et al.  Discovering structure in the space of fMRI selectivity profiles , 2010, NeuroImage.

[2]  Kaustubh Supekar,et al.  Developmental Maturation of Dynamic Causal Control Signals in Higher-Order Cognition: A Neurocognitive Network Model , 2012, PLoS Comput. Biol..

[3]  Radford M. Neal Pattern Recognition and Machine Learning , 2007, Technometrics.

[4]  K. Amunts,et al.  Centenary of Brodmann's Map — Conception and Fate , 2022 .

[5]  K Zilles,et al.  Anatomy and transmitter receptors of the supplementary motor areas in the human and nonhuman primate brain. , 1996, Advances in neurology.

[6]  Naomi B. Pitskel,et al.  Three Systems of Insular Functional Connectivity Identified with Cluster Analysis , 2010, Cerebral cortex.

[7]  Jill P. Mesirov,et al.  A resampling-based method for class discovery and visualization of gene expression microarray data , 2003 .

[8]  Jonathan D. Power,et al.  A Parcellation Scheme for Human Left Lateral Parietal Cortex , 2010, Neuron.

[9]  Timothy Edward John Behrens,et al.  Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Jonathan D. Power,et al.  Parcellation in left lateral parietal cortex is similar in adults and children. , 2012, Cerebral cortex.

[11]  G. Glover,et al.  Spiral‐in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts , 2001, Magnetic resonance in medicine.

[12]  Anton Osokin,et al.  Fast Approximate Energy Minimization with Label Costs , 2010, 2010 IEEE Computer Society Conference on Computer Vision and Pattern Recognition.

[13]  Timothy Edward John Behrens,et al.  Triangulating a Cognitive Control Network Using Diffusion-Weighted Magnetic Resonance Imaging (MRI) and Functional MRI , 2007, The Journal of Neuroscience.

[14]  R. Malach,et al.  Data-driven clustering reveals a fundamental subdivision of the human cortex into two global systems , 2008, Neuropsychologia.

[15]  Michael P. Milham,et al.  A convergent functional architecture of the insula emerges across imaging modalities , 2012, NeuroImage.

[16]  Stan Z. Li Markov Random Field Modeling in Image Analysis , 2009, Advances in Pattern Recognition.

[17]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[18]  Alan C. Evans,et al.  Multi-level bootstrap analysis of stable clusters in resting-state fMRI , 2009, NeuroImage.

[19]  Luke J. Chang,et al.  Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. , 2013, Cerebral cortex.

[20]  Stan Z. Li,et al.  Markov Random Field Modeling in Image Analysis , 2001, Computer Science Workbench.

[21]  Jill P. Mesirov,et al.  Consensus Clustering: A Resampling-Based Method for Class Discovery and Visualization of Gene Expression Microarray Data , 2003, Machine Learning.

[22]  Remco J. Renken,et al.  Group analyses of connectivity-based cortical parcellation using repeated k-means clustering , 2009, NeuroImage.

[23]  M. Fox,et al.  Noninvasive functional and structural connectivity mapping of the human thalamocortical system. , 2010, Cerebral cortex.

[24]  Olga Veksler,et al.  Fast Approximate Energy Minimization via Graph Cuts , 2001, IEEE Trans. Pattern Anal. Mach. Intell..

[25]  Sang Won Seo,et al.  Defining functional SMA and pre-SMA subregions in human MFC using resting state fMRI: Functional connectivity-based parcellation method , 2010, NeuroImage.

[26]  M. Petrides,et al.  Broca’s region: linking human brain functional connectivity data and non‐human primate tracing anatomy studies , 2010, The European journal of neuroscience.

[27]  Inderjit S. Dhillon,et al.  Clustering on the Unit Hypersphere using von Mises-Fisher Distributions , 2005, J. Mach. Learn. Res..

[28]  Donald Geman,et al.  Stochastic Relaxation, Gibbs Distributions, and the Bayesian Restoration of Images , 1984, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[29]  E. Bullmore,et al.  Neurophysiological architecture of functional magnetic resonance images of human brain. , 2005, Cerebral cortex.

[30]  K. Brodmann Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[31]  Katiuscia Sacco,et al.  Functional connectivity of the insula in the resting brain , 2011, NeuroImage.

[32]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[33]  Xenophon Papademetris,et al.  Graph-theory based parcellation of functional subunits in the brain from resting-state fMRI data , 2010, NeuroImage.

[34]  Mark Jenkinson,et al.  A consistent relationship between local white matter architecture and functional specialisation in medial frontal cortex , 2006, NeuroImage.

[35]  Kaustubh Supekar,et al.  Dynamic Reconfiguration of Structural and Functional Connectivity Across Core Neurocognitive Brain Networks with Development , 2011, The Journal of Neuroscience.

[36]  Damien A. Fair,et al.  Defining functional areas in individual human brains using resting functional connectivity MRI , 2008, NeuroImage.

[37]  Donald Geman,et al.  Stochastic relaxation, Gibbs distributions, and the Bayesian restoration of images , 1984 .

[38]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[39]  Ana L. N. Fred,et al.  Combining multiple clusterings using evidence accumulation , 2005, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[40]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[41]  Kristen A. Lindquist,et al.  The brain basis of emotion: A meta-analytic review , 2012, Behavioral and Brain Sciences.

[42]  E. Bullmore,et al.  A Resilient, Low-Frequency, Small-World Human Brain Functional Network with Highly Connected Association Cortical Hubs , 2006, The Journal of Neuroscience.

[43]  R Cameron Craddock,et al.  A whole brain fMRI atlas generated via spatially constrained spectral clustering , 2012, Human brain mapping.

[44]  Jonathan D. Power,et al.  Identifying Basal Ganglia Divisions in Individuals Using Resting-State Functional Connectivity MRI , 2010, Front. Syst. Neurosci..

[45]  Kaustubh Supekar,et al.  Dissociable connectivity within human angular gyrus and intraparietal sulcus: evidence from functional and structural connectivity. , 2010, Cerebral cortex.