Disparity between dorsal and ventral networks in patients with obsessive-compulsive disorder: evidence revealed by graph theoretical analysis based on cortical thickness from MRI

As one of the most widely accepted neuroanatomical models on obsessive-compulsive disorder (OCD), it has been hypothesized that imbalance between an excitatory direct (ventral) pathway and an inhibitory indirect (dorsal) pathway in cortico-striato-thalamic circuit underlies the emergence of OCD. Here we examine the structural network in drug-free patients with OCD in terms of graph theoretical measures for the first time. We used a measure called efficiency which quantifies how a node transfers information efficiently. To construct brain networks, cortical thickness was automatically estimated using T1-weighted magnetic resonance imaging. We found that the network of the OCD patients was as efficient as that of healthy controls so that the both networks were in the small-world regime. More importantly, however, disparity between the dorsal and the ventral networks in the OCD patients was found in terms of graph theoretical measures, suggesting a positive evidence to the imbalance theory on the underlying pathophysiology of OCD.

[1]  R. Ghrist Barcodes: The persistent topology of data , 2007 .

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

[3]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[4]  A L Brody,et al.  Neuroimaging and frontal-subcortical circuitry in obsessive-compulsive disorder , 1998, British Journal of Psychiatry.

[5]  O. A. van den Heuvel,et al.  Common and distinct neural correlates of obsessive-compulsive and related disorders. , 2006, The Psychiatric clinics of North America.

[6]  Edward T. Bullmore,et al.  Efficiency and Cost of Economical Brain Functional Networks , 2007, PLoS Comput. Biol..

[7]  P. Basser Inferring microstructural features and the physiological state of tissues from diffusion‐weighted images , 1995, NMR in biomedicine.

[8]  Marcus Kaiser,et al.  Brain architecture: a design for natural computation , 2007, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

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

[10]  Daniel Güllmar,et al.  White matter structure and symptom dimensions in obsessive-compulsive disorder. , 2012, Journal of psychiatric research.

[11]  Marcus Kaiser,et al.  A tutorial in connectome analysis: Topological and spatial features of brain networks , 2011, NeuroImage.

[12]  Chi-Hua Chen,et al.  Neurocognitive endophenotypes of obsessive-compulsive disorder. , 2007, Brain : a journal of neurology.

[13]  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.

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

[15]  J. Raduà,et al.  Voxel-wise meta-analysis of grey matter changes in obsessive-compulsive disorder. , 2009, The British journal of psychiatry : the journal of mental science.

[16]  Kenji Fukui,et al.  Diffusion tensor imaging and tract-based spatial statistics in obsessive-compulsive disorder. , 2011, Journal of psychiatric research.

[17]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[18]  Ann M Graybiel,et al.  Toward a Neurobiology of Obsessive-Compulsive Disorder , 2000, Neuron.

[19]  James L. Abelson,et al.  Hyperactive Error Responses and Altered Connectivity in Ventromedial and Frontoinsular Cortices in Obsessive-Compulsive Disorder , 2011, Biological Psychiatry.

[20]  A. Gorini,et al.  Disorganization of anatomical connectivity in obsessive compulsive disorder: A multi-parameter diffusion tensor imaging study in a subpopulation of patients , 2010, Neurobiology of Disease.

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

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

[23]  Mark E. J. Newman,et al.  The Structure and Function of Complex Networks , 2003, SIAM Rev..

[24]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.

[25]  K. Worsley,et al.  Unified univariate and multivariate random field theory , 2004, NeuroImage.

[26]  H. Groenewegen,et al.  The major symptom dimensions of obsessive-compulsive disorder are mediated by partially distinct neural systems. , 2008, Brain : a journal of neurology.

[27]  Jungsu S. Oh,et al.  Reduced fronto‐callosal fiber integrity in unmedicated OCD patients: A diffusion tractography study , 2012, Human brain mapping.

[28]  M. Desrocher,et al.  Neuroimaging studies of obsessive-compulsive disorder in adults and children. , 2006, Clinical psychology review.

[29]  Massimo Marchiori,et al.  Economic small-world behavior in weighted networks , 2003 .

[30]  J. Kwon,et al.  Neural correlates of clinical symptoms and cognitive dysfunctions in obsessive–compulsive disorder , 2003, Psychiatry Research: Neuroimaging.

[31]  Manzar Ashtari,et al.  White matter abnormalities in obsessive-compulsive disorder: a diffusion tensor imaging study. , 2005, Archives of general psychiatry.

[32]  J. Kwon,et al.  Functional connectivity in fronto-subcortical circuitry during the resting state in obsessive-compulsive disorder , 2010, Neuroscience Letters.

[33]  Yong He,et al.  Diffusion Tensor Tractography Reveals Abnormal Topological Organization in Structural Cortical Networks in Alzheimer's Disease , 2010, The Journal of Neuroscience.

[34]  Brian B. Avants,et al.  Structural connectivity via the tensor-based morphometry , 2011, 2011 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[35]  S. Rauch,et al.  Obsessive-compulsive disorder: beyond segregated cortico-striatal pathways , 2012, Trends in Cognitive Sciences.

[36]  Ali R. Khan,et al.  FreeSurfer-initiated fully-automated subcortical brain segmentation in MRI using Large Deformation Diffeomorphic Metric Mapping , 2008, NeuroImage.

[37]  E. Bullmore,et al.  Integrating evidence from neuroimaging and neuropsychological studies of obsessive-compulsive disorder: The orbitofronto-striatal model revisited , 2008, Neuroscience & Biobehavioral Reviews.

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

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

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

[41]  B. Harrison,et al.  Altered Cortico-Striatal Functional Connectivity in Obsessive-Compulsive Disorder , 2009, NeuroImage.

[42]  Alan C. Evans,et al.  Cortical thickness analysis examined through power analysis and a population simulation , 2005, NeuroImage.

[43]  Moo K. Chung,et al.  Heat Kernel Smoothing Using Laplace-Beltrami Eigenfunctions , 2010, MICCAI.

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

[45]  Dan J Stein,et al.  Hoarding disorder: a new diagnosis for DSM‐V? , 2010, Depression and anxiety.

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

[47]  A. Brody,et al.  Brain-behavior relationships in obsessive-compulsive disorder. , 2001, Seminars in clinical neuropsychiatry.

[48]  J. V. Haxby,et al.  Spatial Pattern Analysis of Functional Brain Images Using Partial Least Squares , 1996, NeuroImage.

[49]  Geraldo F. Busatto,et al.  Regional Gray Matter Abnormalities in Obsessive-Compulsive Disorder: A Voxel-Based Morphometry Study , 2005, Biological Psychiatry.

[50]  V. Latora,et al.  A measure of centrality based on network efficiency , 2004, cond-mat/0402050.

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

[52]  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 .

[53]  Yufeng Zang,et al.  Abnormal small-world architecture of top-down control networks in obsessive-compulsive disorder. , 2011, Journal of psychiatry & neuroscience : JPN.

[54]  M. First,et al.  Structured clinical interview for DSM-IV axis I disorders : SCID-I : clinical version : scoresheet , 1997 .

[55]  J. Lerch,et al.  Patterns of Coordinated Anatomical Change in Human Cortical Development: A Longitudinal Neuroimaging Study of Maturational Coupling , 2011, Neuron.

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

[57]  Suck-Won Kim,et al.  The Yale-Brown Obsessive-Compulsive Scale: Measures of internal consistency , 1994, Psychiatry Research.

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

[59]  Fritz Hohagen,et al.  Neuropsychological performance in obsessive-compulsive disorder: a critical review , 2004, Biological Psychology.

[60]  J. Kwon,et al.  Altered Brain Activation in Ventral Frontal-Striatal Regions Following a 16-week Pharmacotherapy in Unmedicated Obsessive-Compulsive Disorder , 2011, Journal of Korean medical science.

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

[62]  K. Yamashita,et al.  Regional gray and white matter volume abnormalities in obsessive–compulsive disorder: A voxel-based morphometry study , 2010, Psychiatry Research: Neuroimaging.

[63]  Nikos Makris,et al.  Automatically parcellating the human cerebral cortex. , 2004, Cerebral cortex.

[64]  J. Pujol,et al.  Mapping structural brain alterations in obsessive-compulsive disorder. , 2004, Archives of general psychiatry.

[65]  A. Beck,et al.  An inventory for measuring clinical anxiety: psychometric properties. , 1988, Journal of consulting and clinical psychology.

[66]  S. Whiteside,et al.  A meta–analysis of functional neuroimaging in obsessive–compulsive disorder , 2004, Psychiatry Research: Neuroimaging.

[67]  J. Kwon,et al.  Neuroimaging in obsessive–compulsive disorder , 2009, Expert review of neurotherapeutics.

[68]  J. Cummings,et al.  Frontal-subcortical circuits and human behavior. , 1993, Journal of psychosomatic research.

[69]  Leonardo Franklin Fontenelle,et al.  White matter microstructure in patients with obsessive-compulsive disorder. , 2011, Journal of psychiatry & neuroscience : JPN.

[70]  W. Goodman,et al.  The Yale-Brown Obsessive Compulsive Scale. I. Development, use, and reliability. , 1989, Archives of general psychiatry.

[71]  Dan J Stein,et al.  Obsessive–compulsive disorder: a review of the diagnostic criteria and possible subtypes and dimensional specifiers for DSM‐V , 2010, Depression and anxiety.

[72]  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.

[73]  Jong-Min Lee,et al.  White matter alterations in male patients with obsessive–compulsive disorder , 2009, Neuroreport.

[74]  Alan C. Evans,et al.  Convergence and divergence of thickness correlations with diffusion connections across the human cerebral cortex , 2012, NeuroImage.

[75]  Lutz Jäncke,et al.  The Problem of Thresholding in Small-World Network Analysis , 2013, PloS one.

[76]  KJ Worsley,et al.  SurfStat: A Matlab toolbox for the statistical analysis of univariate and multivariate surface and volumetric data using linear mixed effects models and random field theory , 2009, NeuroImage.

[77]  Alan C. Evans,et al.  Automated 3-D Extraction of Inner and Outer Surfaces of Cerebral Cortex from MRI , 2000, NeuroImage.

[78]  A. Beck,et al.  An inventory for measuring depression. , 1961, Archives of general psychiatry.

[79]  P. Szeszko,et al.  Gray matter structural alterations in psychotropic drug-naive pediatric obsessive-compulsive disorder: an optimized voxel-based morphometry study. , 2008, The American journal of psychiatry.

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

[81]  Moo K. Chung,et al.  Cortical thickness analysis in autism with heat kernel smoothing , 2005, NeuroImage.

[82]  Alan C. Evans,et al.  Cortical thickness measured from MRI in the YAC128 mouse model of Huntington's disease , 2008, NeuroImage.

[83]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[84]  D. Veltman,et al.  Neuroimaging in Obsessive-Compulsive Disorder , 2005 .

[85]  B. Aouizerate,et al.  Gray Matter Alterations in Obsessive–Compulsive Disorder: An Anatomic Likelihood Estimation Meta-Analysis , 2010, Neuropsychopharmacology.

[86]  Daniel Rueckert,et al.  Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data , 2006, NeuroImage.

[87]  Anders M. Dale,et al.  Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature , 2010, NeuroImage.

[88]  Moo K. Chung,et al.  Computing the Shape of Brain Networks Using Graph Filtration and Gromov-Hausdorff Metric , 2011, MICCAI.

[89]  Jun Soo Kwon,et al.  Grey matter abnormalities in obsessive–compulsive disorder , 2001, British Journal of Psychiatry.

[90]  T. Nakamae,et al.  Reduced cortical thickness in non-medicated patients with obsessive-compulsive disorder , 2012, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[91]  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.

[92]  Olaf Sporns,et al.  Small worlds inside big brains , 2006, Proceedings of the National Academy of Sciences.

[93]  R. Hu Diagnostic and Statistical Manual of Mental Disorders (DSM-IV) , 2003 .

[94]  Steven Taylor,et al.  Early versus late onset obsessive-compulsive disorder: evidence for distinct subtypes. , 2011, Clinical psychology review.

[95]  Peter Willett,et al.  What is a tutorial , 2013 .

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

[97]  Jun Soo Kwon,et al.  Cortical thinning in obsessive compulsive disorder , 2007, Human brain mapping.

[98]  T. Yoshiura,et al.  Brain activation of patients with obsessive-compulsive disorder during neuropsychological and symptom provocation tasks before and after symptom improvement: A functional magnetic resonance imaging study , 2005, Biological Psychiatry.

[99]  Jun Ma,et al.  Atlas Generation for Subcortical and Ventricular Structures With Its Applications in Shape Analysis , 2010, IEEE Transactions on Image Processing.

[100]  Moo K. Chung,et al.  Heat Kernel Smoothing via Laplace-Beltrami Eigenfunctions and Its Application to Subcortical Structure Modeling , 2011, PSIVT.

[101]  Yong He,et al.  Age-related alterations in the modular organization of structural cortical network by using cortical thickness from MRI , 2011, NeuroImage.

[102]  Moo K. Chung,et al.  Laplace-Beltrami eigenfunction expansion of cortical manifolds , 2011, 2011 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.