Resting state network estimation in individual subjects

Resting state functional magnetic resonance imaging (fMRI) has been used to study brain networks associated with both normal and pathological cognitive functions. The objective of this work is to reliably compute resting state network (RSN) topography in single participants. We trained a supervised classifier (multi-layer perceptron; MLP) to associate blood oxygen level dependent (BOLD) correlation maps corresponding to pre-defined seeds with specific RSN identities. Hard classification of maps obtained from a priori seeds was highly reliable across new participants. Interestingly, continuous estimates of RSN membership retained substantial residual error. This result is consistent with the view that RSNs are hierarchically organized, and therefore not fully separable into spatially independent components. After training on a priori seed-based maps, we propagated voxel-wise correlation maps through the MLP to produce estimates of RSN membership throughout the brain. The MLP generated RSN topography estimates in individuals consistent with previous studies, even in brain regions not represented in the training data. This method could be used in future studies to relate RSN topography to other measures of functional brain organization (e.g., task-evoked responses, stimulation mapping, and deficits associated with lesions) in individuals. The multi-layer perceptron was directly compared to two alternative voxel classification procedures, specifically, dual regression and linear discriminant analysis; the perceptron generated more spatially specific RSN maps than either alternative.

[1]  David J. Kriegman,et al.  Eigenfaces vs. Fisherfaces: Recognition Using Class Specific Linear Projection , 1996, ECCV.

[2]  Justin L. Vincent,et al.  Distinct cortical anatomy linked to subregions of the medial temporal lobe revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[3]  Habib Benali,et al.  Regions, systems, and the brain: Hierarchical measures of functional integration in fMRI , 2008, Medical Image Anal..

[4]  Biyu J. He,et al.  Electrophysiological correlates of the brain's intrinsic large-scale functional architecture , 2008, Proceedings of the National Academy of Sciences.

[5]  N. Volkow,et al.  Language network: segregation, laterality and connectivity , 2012, Molecular Psychiatry.

[6]  Vesa Kiviniemi,et al.  A Sliding Time-Window ICA Reveals Spatial Variability of the Default Mode Network in Time , 2011, Brain Connect..

[7]  Stefan Golaszewski,et al.  Variability of clinical functional MR imaging results: a multicenter study. , 2013, Radiology.

[8]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[9]  David J. Kriegman,et al.  Recognition using class specific linear projection , 1997 .

[10]  C. D. Gelatt,et al.  Optimization by Simulated Annealing , 1983, Science.

[11]  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.

[12]  M. Fox,et al.  Individual Variability in Functional Connectivity Architecture of the Human Brain , 2013, Neuron.

[13]  Ravi S. Menon,et al.  Resting‐state networks show dynamic functional connectivity in awake humans and anesthetized macaques , 2013, Human brain mapping.

[14]  Xi-Nian Zuo,et al.  Resting-State Functional Connectivity Indexes Reading Competence in Children and Adults , 2011, The Journal of Neuroscience.

[15]  Xi-Nian Zuo,et al.  Reliable intrinsic connectivity networks: Test–retest evaluation using ICA and dual regression approach , 2010, NeuroImage.

[16]  Maurizio Corbetta,et al.  Distinct representations for shifts of spatial attention and changes of reward contingencies in the human brain , 2013, Cortex.

[17]  Biyu J. He,et al.  Breakdown of Functional Connectivity in Frontoparietal Networks Underlies Behavioral Deficits in Spatial Neglect , 2007, Neuron.

[18]  Eswar Damaraju,et al.  Tracking whole-brain connectivity dynamics in the resting state. , 2014, Cerebral cortex.

[19]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[20]  Christian Windischberger,et al.  Toward discovery science of human brain function , 2010, Proceedings of the National Academy of Sciences.

[21]  R. Fisher THE USE OF MULTIPLE MEASUREMENTS IN TAXONOMIC PROBLEMS , 1936 .

[22]  Ali-Mohammad Golestani,et al.  Longitudinal Evaluation of Resting-State fMRI After Acute Stroke With Hemiparesis , 2013, Neurorehabilitation and neural repair.

[23]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[24]  Maurizio Corbetta,et al.  Asymmetry of Anticipatory Activity in Visual Cortex Predicts the Locus of Attention and Perception , 2007, The Journal of Neuroscience.

[25]  Tülay Yildirim,et al.  Improving classification performance of sonar targets by applying general regression neural network with PCA , 2008, Expert Syst. Appl..

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

[27]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[28]  Christian F. Beckmann,et al.  Modelling with independent components , 2012, NeuroImage.

[29]  A. P. Dunmur,et al.  Learning and generalization in a linear perceptron stochastically trained with noisy data , 1993 .

[30]  Peter J. Ramadge,et al.  Inter-subject alignment of human cortical anatomy using functional connectivity , 2013, NeuroImage.

[31]  Justin L. Vincent,et al.  Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[32]  M. Greicius,et al.  Greater than the sum of its parts: a review of studies combining structural connectivity and resting-state functional connectivity , 2009, Brain Structure and Function.

[33]  John W. Harwell,et al.  Similar patterns of cortical expansion during human development and evolution , 2010, Proceedings of the National Academy of Sciences.

[34]  M. Corbetta,et al.  Extrastriate body area in human occipital cortex responds to the performance of motor actions , 2004, Nature Neuroscience.

[35]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[36]  Catie Chang,et al.  Time–frequency dynamics of resting-state brain connectivity measured with fMRI , 2010, NeuroImage.

[37]  Michael W. Cole,et al.  Global Connectivity of Prefrontal Cortex Predicts Cognitive Control and Intelligence , 2012, The Journal of Neuroscience.

[38]  G L Romani,et al.  Functional Connectivity MR Imaging of the Language Network in Patients with Drug-Resistant Epilepsy , 2011, American Journal of Neuroradiology.

[39]  G. Frisoni,et al.  Functional network disruption in the degenerative dementias , 2011, The Lancet Neurology.

[40]  M. Raichle,et al.  Disease and the brain's dark energy , 2010, Nature Reviews Neurology.

[41]  Dietmar Cordes,et al.  Hierarchical clustering to measure connectivity in fMRI resting-state data. , 2002, Magnetic resonance imaging.

[42]  Roger Guimerà,et al.  Cartography of complex networks: modules and universal roles , 2005, Journal of statistical mechanics.

[43]  M. Fox,et al.  Intrinsic functional relations between human cerebral cortex and thalamus. , 2008, Journal of neurophysiology.

[44]  Lawrence D. Jackel,et al.  Backpropagation Applied to Handwritten Zip Code Recognition , 1989, Neural Computation.

[45]  M. Fox,et al.  PREOPERATIVE SENSORIMOTOR MAPPING IN BRAIN TUMOR PATIENTS USING SPONTANEOUS FLUCTUATIONS IN NEURONAL ACTIVITY IMAGED WITH FUNCTIONAL MAGNETIC RESONANCE IMAGING: INITIAL EXPERIENCE , 2009, Neurosurgery.

[46]  Michelle Hampson,et al.  Connectivity–behavior analysis reveals that functional connectivity between left BA39 and Broca's area varies with reading ability , 2006, NeuroImage.

[47]  A. Snyder,et al.  Longitudinal analysis of neural network development in preterm infants. , 2010, Cerebral cortex.

[48]  Marc Joliot,et al.  Brain activity at rest: a multiscale hierarchical functional organization. , 2011, Journal of neurophysiology.

[49]  Geoffrey E. Hinton,et al.  Learning representations by back-propagating errors , 1986, Nature.

[50]  R. Nathan Spreng,et al.  The Fallacy of a “Task-Negative” Network , 2012, Front. Psychology.

[51]  Maurizio Corbetta,et al.  Anticipatory and Stimulus-Evoked Blood Oxygenation Level-Dependent Modulations Related to Spatial Attention Reflect a Common Additive Signal , 2009, The Journal of Neuroscience.

[52]  M. Fox,et al.  The global signal and observed anticorrelated resting state brain networks. , 2009, Journal of neurophysiology.

[53]  M. Corbetta,et al.  Episodic Memory Retrieval, Parietal Cortex, and the Default Mode Network: Functional and Topographic Analyses , 2011, The Journal of Neuroscience.

[54]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[55]  R. Buckner,et al.  The organization of the human striatum estimated by intrinsic functional connectivity. , 2012, Journal of neurophysiology.

[56]  Kurt E. Weaver,et al.  Mapping anterior temporal lobe language areas with fMRI: A multicenter normative study , 2011, NeuroImage.

[57]  M. Corbetta,et al.  Resting interhemispheric functional magnetic resonance imaging connectivity predicts performance after stroke , 2009, Annals of neurology.

[58]  Maurizio Corbetta,et al.  Attention to Memory and the Environment: Functional Specialization and Dynamic Competition in Human Posterior Parietal Cortex , 2010, The Journal of Neuroscience.

[59]  Maurizio Corbetta,et al.  Anticipatory Suppression of Nonattended Locations in Visual Cortex Marks Target Location and Predicts Perception , 2008, The Journal of Neuroscience.

[60]  M. Corbetta,et al.  An Event-Related Functional Magnetic Resonance Imaging Study of Voluntary and Stimulus-Driven Orienting of Attention , 2005, The Journal of Neuroscience.

[61]  Archana Venkataraman,et al.  Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. , 2010, Journal of neurophysiology.

[62]  Edward T. Bullmore,et al.  Modular and Hierarchically Modular Organization of Brain Networks , 2010, Front. Neurosci..

[63]  Angela R Laird,et al.  Cerebellum and auditory function: An ALE meta‐analysis of functional neuroimaging studies , 2005, Human brain mapping.

[64]  D. Poeppel,et al.  Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language , 2004, Cognition.

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

[66]  M. Corbetta,et al.  Interaction of Stimulus-Driven Reorienting and Expectation in Ventral and Dorsal Frontoparietal and Basal Ganglia-Cortical Networks , 2009, The Journal of Neuroscience.

[67]  Timothy O. Laumann,et al.  Parcellating an Individual Subject's Cortical and Subcortical Brain Structures Using Snowball Sampling of Resting-State Correlations , 2013, Cerebral cortex.

[68]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[69]  Michael J. Lyons,et al.  Automatic Classification of Single Facial Images , 1999, IEEE Trans. Pattern Anal. Mach. Intell..

[70]  H. Barrett,et al.  Objective assessment of image quality. III. ROC metrics, ideal observers, and likelihood-generating functions. , 1998, Journal of the Optical Society of America. A, Optics, image science, and vision.

[71]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[72]  Eric Clarkson,et al.  Experimental determination of object statistics from noisy images. , 2003, Journal of the Optical Society of America. A, Optics, image science, and vision.

[73]  Christopher L. Asplund,et al.  The organization of the human cerebellum estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

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

[75]  Bruce W. Suter,et al.  The multilayer perceptron as an approximation to a Bayes optimal discriminant function , 1990, IEEE Trans. Neural Networks.

[76]  F ROSENBLATT,et al.  The perceptron: a probabilistic model for information storage and organization in the brain. , 1958, Psychological review.

[77]  Bharat B. Biswal,et al.  Inter-individual differences in resting-state functional connectivity predict task-induced BOLD activity , 2010, NeuroImage.

[78]  Conor Liston,et al.  Motor deficits correlate with resting state motor network connectivity in patients with brain tumours , 2012, Brain : a journal of neurology.

[79]  Yanmei Tie,et al.  Defining language networks from resting‐state fMRI for surgical planning—a feasibility study , 2014, Human brain mapping.

[80]  I ScottKirkpatrick Optimization by Simulated Annealing: Quantitative Studies , 1984 .

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

[82]  Manuel Schabus,et al.  Hierarchical clustering of brain activity during human nonrapid eye movement sleep , 2012, Proceedings of the National Academy of Sciences.

[83]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[84]  Timothy S. Coalson,et al.  Parcellations and hemispheric asymmetries of human cerebral cortex analyzed on surface-based atlases. , 2012, Cerebral cortex.

[85]  Peter Fransson,et al.  Assessing the Influence of Different ROI Selection Strategies on Functional Connectivity Analyses of fMRI Data Acquired During Steady-State Conditions , 2011, PloS one.

[86]  M. Fox,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[87]  Bryan R. Conroy,et al.  Function-based Intersubject Alignment of Human Cortical Anatomy , 2009, Cerebral cortex.

[88]  G L Romani,et al.  Reorganization of Functional Connectivity of the Language Network in Patients with Brain Gliomas , 2012, American Journal of Neuroradiology.

[89]  Timothy O. Laumann,et al.  Functional Network Organization of the Human Brain , 2011, Neuron.

[90]  M. Corbetta,et al.  Right Hemisphere Dominance during Spatial Selective Attention and Target Detection Occurs Outside the Dorsal Frontoparietal Network , 2010, The Journal of Neuroscience.

[91]  Abraham Z. Snyder,et al.  A brief history of the resting state: The Washington University perspective , 2012, NeuroImage.

[92]  Carl D. Hacker,et al.  Clustering of Resting State Networks , 2012, PloS one.