Mapping Individual Brain Networks Using Statistical Similarity in Regional Morphology from MRI

Representing brain morphology as a network has the advantage that the regional morphology of ‘isolated’ structures can be described statistically based on graph theory. However, very few studies have investigated brain morphology from the holistic perspective of complex networks, particularly in individual brains. We proposed a new network framework for individual brain morphology. Technically, in the new network, nodes are defined as regions based on a brain atlas, and edges are estimated using our newly-developed inter-regional relation measure based on regional morphological distributions. This implementation allows nodes in the brain network to be functionally/anatomically homogeneous but different with respect to shape and size. We first demonstrated the new network framework in a healthy sample. Thereafter, we studied the graph-theoretical properties of the networks obtained and compared the results with previous morphological, anatomical, and functional networks. The robustness of the method was assessed via measurement of the reliability of the network metrics using a test-retest dataset. Finally, to illustrate potential applications, the networks were used to measure age-related changes in commonly used network metrics. Results suggest that the proposed method could provide a concise description of brain organization at a network level and be used to investigate interindividual variability in brain morphology from the perspective of complex networks. Furthermore, the method could open a new window into modeling the complexly distributed brain and facilitate the emerging field of human connectomics.

[1]  Alex R. Smith,et al.  Sex differences in the structural connectome of the human brain , 2013, Proceedings of the National Academy of Sciences.

[2]  V Latora,et al.  Efficient behavior of small-world networks. , 2001, Physical review letters.

[3]  Richard S. J. Frackowiak,et al.  Neurolinguistics: Structural plasticity in the bilingual brain , 2004, Nature.

[4]  Alan C. Evans,et al.  Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. , 2007, Cerebral cortex.

[5]  Karl J. Friston,et al.  Voxel-based morphometry of the human brain: Methods and applications , 2005 .

[6]  Alan C. Evans,et al.  Mapping anatomical correlations across cerebral cortex (MACACC) using cortical thickness from MRI , 2006, NeuroImage.

[7]  K. Worsley,et al.  Impaired small-world efficiency in structural cortical networks in multiple sclerosis associated with white matter lesion load. , 2009, Brain : a journal of neurology.

[8]  Peter Savadjiev,et al.  Fusion of white and gray matter geometry: A framework for investigating brain development , 2014, Medical Image Anal..

[9]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[10]  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.

[11]  Alan C. Evans,et al.  Revealing modular architecture of human brain structural networks by using cortical thickness from MRI. , 2008, Cerebral cortex.

[12]  B. Biswal,et al.  The resting brain: unconstrained yet reliable. , 2009, Cerebral cortex.

[13]  Allan R. Jones,et al.  An anatomically comprehensive atlas of the adult human brain transcriptome , 2012, Nature.

[14]  Jia Liu,et al.  Measuring individual morphological relationship of cortical regions , 2014, Journal of Neuroscience Methods.

[15]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[16]  Bogdan Draganski,et al.  Neuroplasticity: Changes in grey matter induced by training , 2004, Nature.

[17]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[18]  Lester Melie-García,et al.  Studying the human brain anatomical network via diffusion-weighted MRI and Graph Theory , 2008, NeuroImage.

[19]  R. Kahn,et al.  Aberrant Frontal and Temporal Complex Network Structure in Schizophrenia: A Graph Theoretical Analysis , 2010, The Journal of Neuroscience.

[20]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[21]  K. Gurney,et al.  Network ‘Small-World-Ness’: A Quantitative Method for Determining Canonical Network Equivalence , 2008, PloS one.

[22]  Edward T. Bullmore,et al.  Whole-brain anatomical networks: Does the choice of nodes matter? , 2010, NeuroImage.

[23]  Jianhui Zhong,et al.  Disrupted small world networks in patients without overt hepatic encephalopathy: a resting state fMRI study. , 2014, European journal of radiology.

[24]  Emma Muñoz-Moreno,et al.  Normalization of similarity-based individual brain networks from gray matter MRI and its association with neurodevelopment in infants with intrauterine growth restriction , 2013, NeuroImage.

[25]  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.

[26]  Yong He,et al.  Graph Theoretical Analysis of Functional Brain Networks: Test-Retest Evaluation on Short- and Long-Term Resting-State Functional MRI Data , 2011, PloS one.

[27]  Liang Wang,et al.  Parcellation‐dependent small‐world brain functional networks: A resting‐state fMRI study , 2009, Human brain mapping.

[28]  Hiroshi Fukuda,et al.  Age‐related changes in topological organization of structural brain networks in healthy individuals , 2012, Human brain mapping.

[29]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[30]  Yong He,et al.  GRETNA: a graph theoretical network analysis toolbox for imaging connectomics , 2015, Front. Hum. Neurosci..

[31]  E. Bullmore,et al.  Hierarchical Organization of Human Cortical Networks in Health and Schizophrenia , 2008, The Journal of Neuroscience.

[32]  Alan C. Evans,et al.  Age- and Gender-Related Differences in the Cortical Anatomical Network , 2009, The Journal of Neuroscience.

[33]  Michael Weiner,et al.  Network-level analysis of cortical thickness of the epileptic brain , 2010, NeuroImage.

[34]  D. Cicchetti,et al.  Developing criteria for establishing interrater reliability of specific items: applications to assessment of adaptive behavior. , 1981, American journal of mental deficiency.

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

[36]  J. Fleiss,et al.  Intraclass correlations: uses in assessing rater reliability. , 1979, Psychological bulletin.

[37]  M. Mesulam Principles of Behavioral and Cognitive Neurology , 2000 .

[38]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[39]  A. Vespignani,et al.  The architecture of complex weighted networks. , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Neda Bernasconi,et al.  Graph-theoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. , 2011, Cerebral cortex.

[41]  Tianzi Jiang,et al.  Regional coherence changes in the early stages of Alzheimer’s disease: A combined structural and resting-state functional MRI study , 2007, NeuroImage.

[42]  David W. Scott,et al.  Multivariate Density Estimation: Theory, Practice, and Visualization , 1992, Wiley Series in Probability and Statistics.

[43]  E. Bullmore,et al.  Disrupted Axonal Fiber Connectivity in Schizophrenia , 2011, Biological Psychiatry.

[44]  Alan C. Evans,et al.  BigBrain: An Ultrahigh-Resolution 3D Human Brain Model , 2013, Science.

[45]  A. Reiss,et al.  Assessment and prevention of head motion during imaging of patients with attention deficit hyperactivity disorder , 2007, Psychiatry Research: Neuroimaging.

[46]  Michael B. Miller,et al.  How reliable are the results from functional magnetic resonance imaging? , 2010, Annals of the New York Academy of Sciences.

[47]  D. W. Scott,et al.  Multivariate Density Estimation, Theory, Practice and Visualization , 1992 .

[48]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[49]  Alan C. Evans,et al.  Developmental changes in organization of structural brain networks. , 2013, Cerebral cortex.

[50]  G. Rees,et al.  The structural basis of inter-individual differences in human behaviour and cognition , 2011, Nature Reviews Neuroscience.

[51]  Yong He,et al.  Changing topological patterns in normal aging using large-scale structural networks , 2012, Neurobiology of Aging.

[52]  C. Stam,et al.  Small-world networks and functional connectivity in Alzheimer's disease. , 2006, Cerebral cortex.

[53]  Danielle Smith Bassett,et al.  Small-World Brain Networks , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[54]  John Ashburner,et al.  Structural plasticity in the bilingual brain: Proficiency in a second language and age at acquisition affect grey-matter density. , 2004 .

[55]  Denise C. Park,et al.  The adaptive brain: aging and neurocognitive scaffolding. , 2009, Annual review of psychology.

[56]  Olaf Sporns,et al.  The Human Connectome: A Structural Description of the Human Brain , 2005, PLoS Comput. Biol..

[57]  Min Chen,et al.  Multi-parametric neuroimaging reproducibility: A 3-T resource study , 2011, NeuroImage.

[58]  Keith A. Johnson,et al.  Cortical Hubs Revealed by Intrinsic Functional Connectivity: Mapping, Assessment of Stability, and Relation to Alzheimer's Disease , 2009, The Journal of Neuroscience.

[59]  Huiguang He,et al.  Accurate prediction of AD patients using cortical thickness networks , 2012, Machine Vision and Applications.

[60]  R. Tsien,et al.  Specificity and Stability in Topology of Protein Networks , 2022 .

[61]  Edward T. Bullmore,et al.  Age-related changes in modular organization of human brain functional networks , 2009, NeuroImage.

[62]  C. Stam,et al.  Indications for network regularization during absence seizures: Weighted and unweighted graph theoretical analyses , 2009, Experimental Neurology.

[63]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[64]  S. Rombouts,et al.  Loss of ‘Small-World’ Networks in Alzheimer's Disease: Graph Analysis of fMRI Resting-State Functional Connectivity , 2010, PloS one.

[65]  J. Mugler,et al.  Three‐dimensional magnetization‐prepared rapid gradient‐echo imaging (3D MP RAGE) , 1990, Magnetic resonance in medicine.

[66]  K. Sneppen,et al.  Specificity and Stability in Topology of Protein Networks , 2002, Science.

[67]  Yong He,et al.  Structural brain networks and neuropsychiatric disorders , 2011, Current opinion in psychiatry.

[68]  Tianzi Jiang,et al.  Modulation of functional connectivity during the resting state and the motor task , 2004, Human brain mapping.

[69]  Yong He,et al.  Disrupted small-world networks in schizophrenia. , 2008, Brain : a journal of neurology.

[70]  D. V. Essen,et al.  A tension-based theory of morphogenesis and compact wiring in the central nervous system , 1997, Nature.

[71]  Richard D. Deveaux,et al.  Applied Smoothing Techniques for Data Analysis , 1999, Technometrics.

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

[73]  D. Willshaw,et al.  Cerebral Cortex doi:10.1093/cercor/bhr221 Cerebral Cortex Advance Access published September 21, 2011 Similarity-Based Extraction of Individual Networks from Gray Matter MRI Scans , 2022 .

[74]  O. Sporns,et al.  Organization, development and function of complex brain networks , 2004, Trends in Cognitive Sciences.

[75]  Gretel Sanabria-Diaz,et al.  Surface area and cortical thickness descriptors reveal different attributes of the structural human brain networks , 2010, NeuroImage.

[76]  Jun Li,et al.  Brain Anatomical Network and Intelligence , 2009, NeuroImage.

[77]  Alan C. Evans,et al.  Structural Insights into Aberrant Topological Patterns of Large-Scale Cortical Networks in Alzheimer's Disease , 2008, The Journal of Neuroscience.

[78]  Yong He,et al.  BrainNet Viewer: A Network Visualization Tool for Human Brain Connectomics , 2013, PloS one.

[79]  Leonard M. Freeman,et al.  A set of measures of centrality based upon betweenness , 1977 .

[80]  Yuan Zhou,et al.  Abnormal Cortical Networks in Mild Cognitive Impairment and Alzheimer's Disease , 2010, PLoS Comput. Biol..

[81]  Xiaoqi Huang,et al.  Disrupted Brain Connectivity Networks in Drug-Naive, First-Episode Major Depressive Disorder , 2011, Biological Psychiatry.

[82]  Olaf Sporns,et al.  The small world of the cerebral cortex , 2007, Neuroinformatics.

[83]  D. V. van Essen,et al.  A tension-based theory of morphogenesis and compact wiring in the central nervous system. , 1997, Nature.

[84]  E. Bullmore,et al.  The Convergence of Maturational Change and Structural Covariance in Human Cortical Networks , 2013, The Journal of Neuroscience.

[85]  Liang Wang,et al.  Altered small‐world brain functional networks in children with attention‐deficit/hyperactivity disorder , 2009, Human brain mapping.

[86]  Alan C. Evans,et al.  Quantifying variability in the planum temporale: a probability map. , 1999, Cerebral cortex.

[87]  Chun Kee Chung,et al.  Functional Cortical Hubs in the Eyes-Closed Resting Human Brain from an Electrophysiological Perspective Using Magnetoencephalography , 2013, PloS one.

[88]  Alan C. Evans,et al.  Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. , 2009, Cerebral cortex.