Network-based statistic: Identifying differences in brain networks

Large-scale functional or structural brain connectivity can be modeled as a network, or graph. This paper presents a statistical approach to identify connections in such a graph that may be associated with a diagnostic status in case-control studies, changing psychological contexts in task-based studies, or correlations with various cognitive and behavioral measures. The new approach, called the network-based statistic (NBS), is a method to control the family-wise error rate (in the weak sense) when mass-univariate testing is performed at every connection comprising the graph. To potentially offer a substantial gain in power, the NBS exploits the extent to which the connections comprising the contrast or effect of interest are interconnected. The NBS is based on the principles underpinning traditional cluster-based thresholding of statistical parametric maps. The purpose of this paper is to: (i) introduce the NBS for the first time; (ii) evaluate its power with the use of receiver operating characteristic (ROC) curves; and, (iii) demonstrate its utility with application to a real case-control study involving a group of people with schizophrenia for which resting-state functional MRI data were acquired. The NBS identified a expansive dysconnected subnetwork in the group with schizophrenia, primarily comprising fronto-temporal and occipito-temporal dysconnections, whereas a mass-univariate analysis controlled with the false discovery rate failed to identify a subnetwork.

[1]  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.

[2]  Edward T. Bullmore,et al.  Reproducibility of graph metrics of human brain functional networks , 2009, NeuroImage.

[3]  John Suckling,et al.  Variable precision registration via wavelets: Optimal spatial scales for inter-subject registration of functional MRI , 2006, NeuroImage.

[4]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[5]  M. Raichle,et al.  Tracking neuronal fiber pathways in the living human brain. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Albert-László Barabási,et al.  Statistical mechanics of complex networks , 2001, ArXiv.

[7]  E. Bullmore,et al.  Permutation tests for factorially designed neuroimaging experiments , 2004, Human brain mapping.

[8]  Jonathan D. Power,et al.  Functional Brain Networks Develop from a “Local to Distributed” Organization , 2009, PLoS Comput. Biol..

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

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

[11]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

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

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

[14]  Danielle S Bassett,et al.  Cognitive fitness of cost-efficient brain functional networks , 2009, Proceedings of the National Academy of Sciences.

[15]  John Suckling,et al.  Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain , 1999, IEEE Transactions on Medical Imaging.

[16]  P. Thiran,et al.  Mapping Human Whole-Brain Structural Networks with Diffusion MRI , 2007, PloS one.

[17]  Karl J. Friston,et al.  Abnormal Cingulate Modulation of Fronto-Temporal Connectivity in Schizophrenia , 1999, NeuroImage.

[18]  E. Bullmore,et al.  The anatomy of first-episode and chronic schizophrenia: an anatomical likelihood estimation meta-analysis. , 2008, The American journal of psychiatry.

[19]  Alex Fornito,et al.  What can spontaneous fluctuations of the blood oxygenation-level-dependent signal tell us about psychiatric disorders? , 2010, Current opinion in psychiatry.

[20]  Paul J. Laurienti,et al.  Comparison of characteristics between region-and voxel-based network analyses in resting-state fMRI data , 2010, NeuroImage.

[21]  David K. Smith Network Flows: Theory, Algorithms, and Applications , 1994 .

[22]  Andrew Zalesky,et al.  A DTI-Derived Measure of Cortico-Cortical Connectivity , 2009, IEEE Transactions on Medical Imaging.

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

[24]  C. Stam,et al.  Small‐world properties of nonlinear brain activity in schizophrenia , 2009, Human brain mapping.

[25]  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.

[26]  P. Basser,et al.  In vivo fiber tractography using DT‐MRI data , 2000, Magnetic resonance in medicine.

[27]  J. Hopcroft,et al.  Algorithm 447: efficient algorithms for graph manipulation , 1973, CACM.

[28]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[29]  Vince D. Calhoun,et al.  Measuring brain connectivity: Diffusion tensor imaging validates resting state temporal correlations , 2008, NeuroImage.

[30]  J. Hopcroft,et al.  Efficient algorithms for graph manipulation , 1971 .

[31]  G Tononi,et al.  Theoretical neuroanatomy: relating anatomical and functional connectivity in graphs and cortical connection matrices. , 2000, Cerebral cortex.

[32]  Olaf Sporns,et al.  Can structure predict function in the human brain? , 2010, NeuroImage.

[33]  M. Yücel,et al.  Mapping grey matter reductions in schizophrenia: An anatomical likelihood estimation analysis of voxel-based morphometry studies , 2009, Schizophrenia Research.

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

[35]  Thomas E. Nichols,et al.  Combining voxel intensity and cluster extent with permutation test framework , 2004, NeuroImage.

[36]  E. Bullmore,et al.  Meta-analysis of diffusion tensor imaging studies in schizophrenia , 2009, Schizophrenia Research.

[37]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[38]  G. Cecchi,et al.  Scale-free brain functional networks. , 2003, Physical review letters.

[39]  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.

[40]  S. Cichon,et al.  Neural Mechanisms of a Genome-Wide Supported Psychosis Variant , 2009, Science.

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

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

[43]  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.

[44]  Daniel Rueckert,et al.  Identifying population differences in whole-brain structural networks: A machine learning approach , 2010, NeuroImage.

[45]  Timothy Edward John Behrens,et al.  New approaches for exploring anatomical and functional connectivity in the human brain , 2004, Biological Psychiatry.

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

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

[48]  Cornelis J. Stam,et al.  Small-world and scale-free organization of voxel-based resting-state functional connectivity in the human brain , 2008, NeuroImage.

[49]  John Suckling,et al.  Generic aspects of complexity in brain imaging data and other biological systems , 2009, NeuroImage.

[50]  R. Kahn,et al.  Efficiency of Functional Brain Networks and Intellectual Performance , 2009, The Journal of Neuroscience.

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

[52]  C. J. Honeya,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009 .

[53]  Yong He,et al.  Age-related changes in topological patterns of large-scale brain functional networks during memory encoding and recognition , 2010, NeuroImage.

[54]  Thomas E. Nichols,et al.  Controlling the familywise error rate in functional neuroimaging: a comparative review , 2003, Statistical methods in medical research.