Low-rank network signatures in the triple network separate schizophrenia and major depressive disorder

Brain imaging studies have revealed that functional and structural brain connectivity in the so-called triple network (i.e., default mode network (DMN), salience network (SN) and central executive network (CEN)) are consistently altered in schizophrenia. However, similar changes have also been found in patients with major depressive disorder, prompting the question of specific triple network signatures for the two disorders. In this study, we proposed Supervised Convex Nonnegative Matrix Factorization (SCNMF) to extract distributed multi-modal brain patterns. These patterns distinguish schizophrenia and major depressive disorder in a latent low-dimensional space of the triple brain network. Specifically, 21 patients of schizophrenia and 25 patients of major depressive disorder were assessed by T1-weighted, diffusion-weighted, and resting-state functional MRIs. Individual structural and functional connectivity networks, based on pre-defined regions of the triple network were constructed, respectively. Afterwards, SCNMF was employed to extract the discriminative patterns. Experiments indicate that SCNMF allows extracting the low-rank discriminative patterns between the two disorders, achieving a classification accuracy of 82.6% based on the extracted functional and structural abnormalities with support vector machine. Experimental results show the specific brain patterns for schizophrenia and major depressive disorder that are multi-modal, complex, and distributed in the triple network. Parts of the prefrontal cortex including superior frontal gyri showed variation between patients with schizophrenia and major depression due to structural properties. In terms of functional properties, the middle cingulate cortex, inferior parietal lobule, and cingulate cortex were the most discriminative regions.

[1]  Martin Wiesmann,et al.  Functional Connectivity Bias of the Orbitofrontal Cortex in Drug-Free Patients with Major Depression , 2010, Biological Psychiatry.

[2]  Babak A. Ardekani,et al.  A DTI study of white matter microstructure in individuals at high genetic risk for schizophrenia , 2008, Schizophrenia Research.

[3]  Carles Falcón,et al.  Decreased cerebral activation during CPT performance structural and functional deficits in schizophrenic patients , 2004, NeuroImage.

[4]  J. Ross Quinlan,et al.  C4.5: Programs for Machine Learning , 1992 .

[5]  Yuan Zhou,et al.  Functional disintegration in paranoid schizophrenia using resting-state fMRI , 2007, Schizophrenia Research.

[6]  Janet B W Williams,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[7]  Roman Filipovych,et al.  Identifying Sparse Connectivity Patterns in the brain using resting-state fMRI , 2015, NeuroImage.

[8]  Jianfeng Feng,et al.  Aberrant functional connectivity for diagnosis of major depressive disorder: A discriminant analysis , 2014, Psychiatry and clinical neurosciences.

[9]  Andrea Mechelli,et al.  Voxelwise meta-analysis of gray matter reduction in major depressive disorder , 2012, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[10]  M. Alda,et al.  Reduced subgenual cingulate volumes in mood disorders: a meta-analysis. , 2008, Journal of psychiatry & neuroscience : JPN.

[11]  M. Hamilton A RATING SCALE FOR DEPRESSION , 1960, Journal of neurology, neurosurgery, and psychiatry.

[12]  Vladimir Vapnik,et al.  Support-vector networks , 2004, Machine Learning.

[13]  P. Golland,et al.  Whole brain resting state functional connectivity abnormalities in schizophrenia , 2012, Schizophrenia Research.

[14]  R. Dolan,et al.  The interaction between mood and cognitive function studied with PET , 1997, Psychological Medicine.

[15]  J. Lieberman,et al.  Schizophrenia: new pathological insights and therapies. , 2007, Annual review of medicine.

[16]  G. Busatto,et al.  Brain Anatomical Abnormalities in Schizophrenia: Neurodevelopmental Origins and Patterns of Progression over Time , 2010 .

[17]  Zhigang Luo,et al.  Manifold Regularized Discriminative Nonnegative Matrix Factorization With Fast Gradient Descent , 2011, IEEE Transactions on Image Processing.

[18]  F. Binkofski,et al.  Limbic and Frontal Cortical Degeneration Is Associated with Psychiatric Symptoms in PINK1 Mutation Carriers , 2008, Biological Psychiatry.

[19]  Peter F. Liddle,et al.  Clinical Utility of Machine-Learning Approaches in Schizophrenia: Improving Diagnostic Confidence for Translational Neuroimaging , 2013, Front. Psychiatry.

[20]  E. Bullmore,et al.  Meta-Analysis of Gray Matter Anomalies in Schizophrenia: Application of Anatomic Likelihood Estimation and Network Analysis , 2008, Biological Psychiatry.

[21]  Michael Mitzenmacher,et al.  Detecting Novel Associations in Large Data Sets , 2011, Science.

[22]  G. Arbanas Diagnostic and Statistical Manual of Mental Disorders (DSM-5) , 2015 .

[23]  J. McGrath,et al.  Schizophrenia: a concise overview of incidence, prevalence, and mortality. , 2008, Epidemiologic reviews.

[24]  H. Mayberg,et al.  Frontal lobe dysfunction in secondary depression. , 1994, The Journal of neuropsychiatry and clinical neurosciences.

[25]  Christos Davatzikos,et al.  Finding imaging patterns of structural covariance via Non-Negative Matrix Factorization , 2015, NeuroImage.

[26]  M. Buchsbaum,et al.  Thalamic and prefrontal FDG uptake in never medicated patients with schizophrenia. , 2005, The American journal of psychiatry.

[27]  Mark Mühlau,et al.  Aberrant dependence of default mode/central executive network interactions on anterior insular salience network activity in schizophrenia. , 2014, Schizophrenia bulletin.

[28]  Jean Ponce,et al.  Task-Driven Dictionary Learning , 2010, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[29]  Vince D. Calhoun,et al.  Single subject prediction of brain disorders in neuroimaging: Promises and pitfalls , 2017, NeuroImage.

[30]  Seungjin Choi,et al.  Semi-Supervised Nonnegative Matrix Factorization , 2010, IEEE Signal Processing Letters.

[31]  M. Owen,et al.  Schizophrenia , 2016, The Lancet.

[32]  Leo Breiman,et al.  Random Forests , 2001, Machine Learning.

[33]  Junming Shao,et al.  Aberrant topology of striatum's connectivity is associated with the number of episodes in depression. , 2014, Brain : a journal of neurology.

[34]  J. Andrews-Hanna,et al.  Large-Scale Network Dysfunction in Major Depressive Disorder: A Meta-analysis of Resting-State Functional Connectivity. , 2015, JAMA psychiatry.

[35]  H. Möller,et al.  Individualized differential diagnosis of schizophrenia and mood disorders using neuroanatomical biomarkers. , 2015, Brain : a journal of neurology.

[36]  J R Moeller,et al.  Regional cerebral blood flow in mood disorders. I. Comparison of major depressives and normal controls at rest. , 1990, Archives of general psychiatry.

[37]  B. Ravnkilde,et al.  Hippocampal volume and depression: a meta-analysis of MRI studies. , 2004, The American journal of psychiatry.

[38]  Chris H. Q. Ding,et al.  Convex and Semi-Nonnegative Matrix Factorizations , 2010, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[39]  Pedro M. Domingos,et al.  On the Optimality of the Simple Bayesian Classifier under Zero-One Loss , 1997, Machine Learning.

[40]  G. Rajkowska,et al.  Reduced Density of Calbindin Immunoreactive GABAergic Neurons in the Occipital Cortex in Major Depression: Relevance to Neuroimaging Studies , 2010, Biological Psychiatry.

[41]  Lianli Gao,et al.  Common and distinct changes of default mode and salience network in schizophrenia and major depression , 2018, Brain Imaging and Behavior.

[42]  M. First,et al.  The Structured Clinical Interview for DSM-III-R (SCID). I: History, rationale, and description. , 1992, Archives of general psychiatry.

[43]  K. Pearson VII. Note on regression and inheritance in the case of two parents , 1895, Proceedings of the Royal Society of London.

[44]  Gerty J. L. M. Lensvelt-Mulders,et al.  Brain volume abnormalities in major depressive disorder: A meta‐analysis of magnetic resonance imaging studies , 2009, Human brain mapping.

[45]  Cheng Luo,et al.  Dysfunction of Large-Scale Brain Networks in Schizophrenia: A Meta-analysis of Resting-State Functional Connectivity , 2018, Schizophrenia bulletin.

[46]  Heng Tao Shen,et al.  Principal Component Analysis , 2009, Encyclopedia of Biometrics.

[47]  L. Parsons,et al.  Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. , 1999, The American journal of psychiatry.

[48]  A L Brody,et al.  Prefrontal-subcortical and limbic circuit mediation of major depressive disorder. , 2001, Seminars in clinical neuropsychiatry.

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

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

[51]  T. Higuchi,et al.  Regional cerebral blood flow in mood disorders , 1997 .

[52]  Karl J. Friston,et al.  Structural and Functional Brain Networks: From Connections to Cognition , 2013, Science.

[53]  B. Biswal,et al.  Music Intervention Leads to Increased Insular Connectivity and Improved Clinical Symptoms in Schizophrenia , 2018, Front. Neurosci..

[54]  Xiaoming Wang,et al.  Altered Structural and Functional Feature of Striato-Cortical Circuit in Benign Epilepsy with Centrotemporal Spikes , 2015, Int. J. Neural Syst..

[55]  Katherine E Henson,et al.  Risk of Suicide After Cancer Diagnosis in England , 2018, JAMA psychiatry.

[56]  K. Pearson Contributions to the Mathematical Theory of Evolution , 1894 .

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

[58]  Mervi Eerola,et al.  Major depressive disorder and white matter abnormalities: a diffusion tensor imaging study with tract-based spatial statistics. , 2010, Journal of affective disorders.

[59]  Renaud Jardri,et al.  Cortical activations during auditory verbal hallucinations in schizophrenia: a coordinate-based meta-analysis. , 2011, The American journal of psychiatry.

[60]  R. Passingham,et al.  Is Gray Matter Volume an Intermediate Phenotype for Schizophrenia? A Voxel-Based Morphometry Study of Patients with Schizophrenia and Their Healthy Siblings , 2008, Biological Psychiatry.

[61]  C. Sorg,et al.  Prediction of Alzheimer's disease using individual structural connectivity networks , 2012, Neurobiology of Aging.

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

[63]  Edith Pomarol-Clotet,et al.  Overall brain connectivity maps show cortico‐subcortical abnormalities in schizophrenia , 2010, Human brain mapping.

[64]  A. Alexander,et al.  White matter tractography using diffusion tensor deflection , 2003, Human brain mapping.

[65]  R. Kahn,et al.  The neurobiology and treatment of first-episode schizophrenia , 2014, Molecular Psychiatry.

[66]  H. Möller,et al.  Depression-related variation in brain morphology over 3 years: effects of stress? , 2008, Archives of general psychiatry.

[67]  Stefan Haufe,et al.  On the interpretation of weight vectors of linear models in multivariate neuroimaging , 2014, NeuroImage.

[68]  E. Bora,et al.  Neuroanatomical abnormalities in schizophrenia: A multimodal voxelwise meta-analysis and meta-regression analysis , 2011, Schizophrenia Research.

[69]  B. Horwitz,et al.  Brain activity during transient sadness and happiness in healthy women. , 1995, The American journal of psychiatry.

[70]  Sabine Van Huffel,et al.  Multiparametric Non-Negative Matrix Factorization for Longitudinal Variations Detection in White-Matter Fiber Bundles , 2017, IEEE Journal of Biomedical and Health Informatics.

[71]  Jason Weston,et al.  Gene Selection for Cancer Classification using Support Vector Machines , 2002, Machine Learning.

[72]  Yunde Jia,et al.  FISHER NON-NEGATIVE MATRIX FACTORIZATION FOR LEARNING LOCAL FEATURES , 2004 .

[73]  J. Mazziotta,et al.  Reduction of prefrontal cortex glucose metabolism common to three types of depression. , 1989, Archives of general psychiatry.

[74]  M. Minzenberg,et al.  Meta-analysis of 41 functional neuroimaging studies of executive function in schizophrenia. , 2009, Archives of general psychiatry.

[75]  Valentin Riedl,et al.  Insular dysfunction within the salience network is associated with severity of symptoms and aberrant inter-network connectivity in major depressive disorder , 2014, Front. Hum. Neurosci..

[76]  Jen-Chuen Hsieh,et al.  Regional cortical thinning in patients with major depressive disorder: A surface-based morphometry study , 2012, Psychiatry Research: Neuroimaging.

[77]  Simone Kühn,et al.  Resting-state brain activity in schizophrenia and major depression: a quantitative meta-analysis. , 2013, Schizophrenia bulletin.

[78]  Anastasios Tefas,et al.  Exploiting discriminant information in nonnegative matrix factorization with application to frontal face verification , 2006, IEEE Transactions on Neural Networks.

[79]  J. Krystal,et al.  Increased occipital cortex GABA concentrations in depressed patients after therapy with selective serotonin reuptake inhibitors. , 2002, The American journal of psychiatry.

[80]  Alan L. Yuille,et al.  Non-negative matrix factorization of multimodal MRI, fMRI and phenotypic data reveals differential changes in default mode subnetworks in ADHD , 2014, NeuroImage.

[81]  N. Weiskopf,et al.  Tx/Rx Head Coil Induces Less RF Transmit-Related Heating than Body Coil in Conductive Metallic Objects Outside the Active Area of the Head Coil , 2017, Front. Neurosci..

[82]  S. Lui,et al.  Is depression a disconnection syndrome? Meta-analysis of diffusion tensor imaging studies in patients with MDD. , 2013, Journal of psychiatry & neuroscience : JPN.

[83]  Gareth J. Barker,et al.  A Diffusion Tensor Imaging Study of White Matter in Early-Onset Schizophrenia , 2008, Biological Psychiatry.

[84]  Marc Joliot,et al.  Links among resting-state default-mode network, salience network, and symptomatology in schizophrenia , 2013, Schizophrenia Research.

[85]  V. Menon Large-scale brain networks and psychopathology: a unifying triple network model , 2011, Trends in Cognitive Sciences.

[86]  J. Gabrieli,et al.  Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia , 2009, Proceedings of the National Academy of Sciences.

[87]  Jong H. Yoon,et al.  General and Specific Functional Connectivity Disturbances in First-Episode Schizophrenia During Cognitive Control Performance , 2011, Biological Psychiatry.

[88]  Fenna M. Krienen,et al.  Opportunities and limitations of intrinsic functional connectivity MRI , 2013, Nature Neuroscience.

[89]  E. Bora,et al.  Gray matter abnormalities in Major Depressive Disorder: a meta-analysis of voxel based morphometry studies. , 2012, Journal of affective disorders.

[90]  C. Davatzikos,et al.  Neuroanatomical Classification in a Population-Based Sample of Psychotic Major Depression and Bipolar I Disorder with 1 Year of Diagnostic Stability , 2014, BioMed research international.

[91]  R. McCarley,et al.  Abnormal angular gyrus asymmetry in schizophrenia. , 2000, The American journal of psychiatry.

[92]  E. Torrey,et al.  Schizophrenia and the inferior parietal lobule , 2007, Schizophrenia Research.

[93]  Susanne Walitza,et al.  Aberrant coupling within and across the default mode, task-positive, and salience network in subjects at risk for psychosis. , 2014, Schizophrenia bulletin.

[94]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[95]  S. Kay,et al.  The positive and negative syndrome scale (PANSS) for schizophrenia. , 1987, Schizophrenia bulletin.

[96]  D. Kibler,et al.  Instance-based learning algorithms , 2004, Machine Learning.

[97]  Wei Han,et al.  Exploring Common and Distinct Structural Connectivity Patterns Between Schizophrenia and Major Depression via Cluster-Driven Nonnegative Matrix Factorization , 2017, 2017 IEEE International Conference on Data Mining (ICDM).

[98]  H. Sebastian Seung,et al.  Learning the parts of objects by non-negative matrix factorization , 1999, Nature.

[99]  Hiroshi Fukuda,et al.  Male elderly subthreshold depression patients have smaller volume of medial part of prefrontal cortex and precentral gyrus compared with age-matched normal subjects: a voxel-based morphometry. , 2005, Journal of affective disorders.

[100]  Alan C. Evans,et al.  Changes in cortical thickness during the course of illness in schizophrenia. , 2011, Archives of general psychiatry.

[101]  G. F. Hughes,et al.  On the mean accuracy of statistical pattern recognizers , 1968, IEEE Trans. Inf. Theory.