Multi-Feature Based Network Revealing the Structural Abnormalities in Autism Spectrum Disorder

Autism spectrum disorder (ASD) is accompanied with impaired social-emotional functioning, such as emotional regulation and recognition, communication, and related behavior. Study of the alternations of the brain networks in ASD may not only help us in understanding this disorder but also inform us the mechanisms of affective computing in the brain. Although morphological features have been used in the diagnosis of a variety of neurological and psychiatric disorders, these features did not show significant discriminative value in identifying patients with ASD, possibly due to the omission of the information related to the changes in structural similarities among cortical regions. In this study, structural images from 66 high-functioning adults with ASD and 66 matched typically-developing controls (TDC) were used to test the hypothesis of cortico-cortical relationships are abnormal in ASD. Seven morphological features of each of the 360 brain regions were extracted and elastic network was used to quantify the similarities between each target region and all other regions. The similarities were then used to construct multi-feature-based networks (MFN), which were then submitted to a support vector machine classifier to classify the individuals of the two groups. Results showed that the classifier with features of MFN significantly improved the accuracy of discriminating patients with ASD from TDCs (78.63 percent) compared to using morphological features only (< 65 percent). The combination of MFN features with morphological features and other high-level MFN properties did not further enhance the classification performance. Our findings demonstrate that the variations in cortico-cortical similarities are important in the etiology of ASD and can be used as biomarkers in the diagnostic process.

[1]  Meritxell Bach Cuadra,et al.  A Surface-Based Approach to Quantify Local Cortical Gyrification , 2008, IEEE Transactions on Medical Imaging.

[2]  A. Simmons,et al.  Disrupted Network Topology in Patients with Stable and Progressive Mild Cognitive Impairment and Alzheimer's Disease , 2016, Cerebral cortex.

[3]  Robin M. Murray,et al.  Structural brain abnormalities in male schizophrenics reflect fronto-temporal dissociation , 1997, Psychological Medicine.

[4]  Daniel Mestre,et al.  Rapid visual-motion integration deficit in autism , 2002, Trends in Cognitive Sciences.

[5]  Lauren E. Libero,et al.  Disrupted cortical connectivity theory as an explanatory model for autism spectrum disorders. , 2011, Physics of life reviews.

[6]  Meritxell Bach Cuadra,et al.  How to measure cortical folding from MR images: a step-by-step tutorial to compute local gyrification index. , 2012, Journal of visualized experiments : JoVE.

[7]  Karl J. Friston,et al.  Automatic Differentiation of Anatomical Patterns in the Human Brain: Validation with Studies of Degenerative Dementias , 2002, NeuroImage.

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

[9]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[10]  Chih-Jen Lin,et al.  LIBSVM: A library for support vector machines , 2011, TIST.

[11]  Richard S. Frackowiak,et al.  Superior temporal sulcus anatomical abnormalities in childhood autism: a voxel-based morphometry MRI study , 2004, NeuroImage.

[12]  Katiuscia Sacco,et al.  Grey matter abnormality in autism spectrum disorder: an activation likelihood estimation meta-analysis study , 2011, Journal of Neurology, Neurosurgery & Psychiatry.

[13]  Alan C. Evans Networks of anatomical covariance , 2013, NeuroImage.

[14]  M. Bellani,et al.  Brain anatomy of autism spectrum disorders II. Focus on amygdala , 2013, Epidemiology and Psychiatric Sciences.

[15]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[16]  E. Courchesne,et al.  When Is the Brain Enlarged in Autism? A Meta-Analysis of All Brain Size Reports , 2005, Biological Psychiatry.

[17]  Anders M. Dale,et al.  A hybrid approach to the Skull Stripping problem in MRI , 2001, NeuroImage.

[18]  Karl J. Friston,et al.  Anterior insular cortex and emotional awareness , 2013, The Journal of comparative neurology.

[19]  Jin Fan,et al.  Hick–Hyman Law is Mediated by the Cognitive Control Network in the Brain , 2018, Cerebral cortex.

[20]  L. Schieve,et al.  Brief Report: Estimated Prevalence of a Community Diagnosis of Autism Spectrum Disorder by Age 4 Years in Children from Selected Areas in the United States in 2010: Evaluation of Birth Cohort Effects , 2017, Journal of autism and developmental disorders.

[21]  E. Courchesne,et al.  Brain growth across the life span in autism: Age-specific changes in anatomical pathology , 2011, Brain Research.

[22]  Daniel P. Kennedy,et al.  Mapping Early Brain Development in Autism , 2007, Neuron.

[23]  Nathalie Boddaert,et al.  Autism, the superior temporal sulcus and social perception , 2006, Trends in Neurosciences.

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

[25]  J B Poline,et al.  Direct voxel-based comparison between grey matter hypometabolism and atrophy in Alzheimer's disease. , 2007, Brain : a journal of neurology.

[26]  D. Shen,et al.  Prediction of Alzheimer's Disease and Mild Cognitive Impairment Using Cortical Morphological Patterns Chong-yaw Wee, Pew-thian Yap, and Dinggang Shen; for the Alzheimer's Disease Neuroimaging Initiative , 2022 .

[27]  Eric Courchesne,et al.  A failure of left temporal cortex to specialize for language is an early emerging and fundamental property of autism. , 2012, Brain : a journal of neurology.

[28]  Hua,et al.  Identification of , 2000, Journal of insect physiology.

[29]  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.

[30]  Sam Wass,et al.  Distortions and disconnections: Disrupted brain connectivity in autism , 2011, Brain and Cognition.

[31]  C. Haselgrove,et al.  Connectivity in Autism: A Review of MRI Connectivity Studies , 2015, Harvard review of psychiatry.

[32]  Susan E. Bryson,et al.  Visual orienting deficits in high-functioning people with autism , 1993, Journal of autism and developmental disorders.

[33]  J. Piven,et al.  Visual Scanning of Faces in Autism , 2002, Journal of autism and developmental disorders.

[34]  M. Erb,et al.  Activation of human language processing brain regions after the presentation of random letter strings demonstrated with event-related functional magnetic resonance imaging , 1999, Neuroscience Letters.

[35]  David I. Perrett,et al.  A voxel-based investigation of brain structure in male adolescents with autistic spectrum disorder , 2004, NeuroImage.

[36]  R Jacobson,et al.  Selective subcortical abnormalities in autism , 1988, Psychological Medicine.

[37]  G. Fagiolo Clustering in complex directed networks. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[38]  Jin Fan,et al.  Neuroanatomical Alterations in High-Functioning Adults with Autism Spectrum Disorder , 2016, Front. Neurosci..

[39]  Robert T. Schultz,et al.  Globally weaker and topologically different: resting-state connectivity in youth with autism , 2017, Molecular Autism.

[40]  Jin Fan,et al.  Quantitative Characterization of Functional Anatomical Contributions to Cognitive Control under Uncertainty , 2014, Journal of Cognitive Neuroscience.

[41]  Benjamin D. Singer,et al.  Retinotopic Organization of Human Ventral Visual Cortex , 2009, The Journal of Neuroscience.

[42]  C. Galletti,et al.  Human V6: The Medial Motion Area , 2009, Cerebral cortex.

[43]  Marlies E. Vissers,et al.  Brain connectivity and high functioning autism: A promising path of research that needs refined models, methodological convergence, and stronger behavioral links , 2012, Neuroscience & Biobehavioral Reviews.

[44]  Z. Yao,et al.  Identification of Alzheimer's Disease and Mild Cognitive Impairment Using Networks Constructed Based on Multiple Morphological Brain Features. , 2018, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[45]  John Suckling,et al.  Brain surface anatomy in adults with autism: the relationship between surface area, cortical thickness, and autistic symptoms. , 2013, JAMA psychiatry.

[46]  Lucina Q. Uddin,et al.  Multivariate Searchlight Classification of Structural Magnetic Resonance Imaging in Children and Adolescents with Autism , 2011, Biological Psychiatry.

[47]  J. Baron,et al.  In Vivo Mapping of Gray Matter Loss with Voxel-Based Morphometry in Mild Alzheimer's Disease , 2001, NeuroImage.

[48]  Dinggang Shen,et al.  Diagnosis of autism spectrum disorders using regional and interregional morphological features , 2014, Human brain mapping.

[49]  Rajesh K. Kana,et al.  Surface-based morphometry of the cortical architecture of autism spectrum disorders: volume, thickness, area, and gyrification , 2014, Neuropsychologia.

[50]  M. Sigman,et al.  A big-world network in ASD: Dynamical connectivity analysis reflects a deficit in long-range connections and an excess of short-range connections , 2010, Neuropsychologia.

[51]  A. Gulsrud,et al.  Social Networks and Friendships at School: Comparing Children With and Without ASD , 2010, Journal of autism and developmental disorders.

[52]  Toshiyuki Someya,et al.  Reduced thalamic volume observed across different subgroups of autism spectrum disorders , 2010, Psychiatry Research: Neuroimaging.

[53]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[54]  P. Fonlupt,et al.  Abnormal cerebral effective connectivity during explicit emotional processing in adults with autism spectrum disorder. , 2008, Social cognitive and affective neuroscience.

[55]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

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

[57]  S. Baron-Cohen Theory of mind and autism: A fifteen year review. , 2000 .

[58]  Corinna Cortes,et al.  Support-Vector Networks , 1995, Machine Learning.

[59]  Stewart H Mostofsky,et al.  Developmental dyspraxia is not limited to imitation in children with autism spectrum disorders , 2006, Journal of the International Neuropsychological Society.

[60]  A. Couteur,et al.  Autism Diagnostic Interview-Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders , 1994, Journal of autism and developmental disorders.

[61]  A. Minassian,et al.  Sensorimotor Gating Deficits in Adults with Autism , 2007, Biological Psychiatry.

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

[63]  C. Lord,et al.  Language and Communication in Autism , 2014 .

[64]  G. Frisoni,et al.  Detection of grey matter loss in mild Alzheimer's disease with voxel based morphometry , 2002, Journal of neurology, neurosurgery, and psychiatry.

[65]  L. Faust,et al.  Understanding Other Minds Perspectives From Developmental Cognitive Neuroscience , 2016 .

[66]  Yun Jiao,et al.  Predictive models of autism spectrum disorder based on brain regional cortical thickness , 2010, NeuroImage.

[67]  C. Frith,et al.  Interacting minds--a biological basis. , 1999, Science.

[68]  G. Fink,et al.  Changes in grey matter development in autism spectrum disorder , 2012, Brain Structure and Function.

[69]  L. Soorya,et al.  Impaired Structural Connectivity of Socio-Emotional Circuits in Autism Spectrum Disorders: A Diffusion Tensor Imaging Study , 2011, PloS one.

[70]  Nicholas Lange,et al.  Longitudinal Volumetric Brain Changes in Autism Spectrum Disorder Ages 6–35 Years , 2015, Autism research : official journal of the International Society for Autism Research.

[71]  J. Rabe-Jabłońska,et al.  [Affective disorders in the fourth edition of the classification of mental disorders prepared by the American Psychiatric Association -- diagnostic and statistical manual of mental disorders]. , 1993, Psychiatria polska.

[72]  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.

[73]  Maureen S. Durkin,et al.  Prevalence and Characteristics of Autism Spectrum Disorder Among 4-Year-Old Children in the Autism and Developmental Disabilities Monitoring Network , 2016, Journal of developmental and behavioral pediatrics : JDBP.

[74]  M. Bellani,et al.  Brain anatomy of autism spectrum disorders I , 2013 .

[75]  R. Tibshirani Regression Shrinkage and Selection via the Lasso , 1996 .

[76]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[77]  Dwight J. Kravitz,et al.  Global motion perception deficits in autism are reflected as early as primary visual cortex. , 2014, Brain : a journal of neurology.

[78]  Z. Yao,et al.  Novel Cortical Thickness Pattern for Accurate Detection of Alzheimer's Disease. , 2015, Journal of Alzheimer's disease : JAD.

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

[80]  B. Leventhal,et al.  The Autism Diagnostic Observation Schedule—Generic: A Standard Measure of Social and Communication Deficits Associated with the Spectrum of Autism , 2000, Journal of autism and developmental disorders.

[81]  Simon B Eickhoff,et al.  Brain structure anomalies in autism spectrum disorder—a meta‐analysis of VBM studies using anatomic likelihood estimation , 2012, Human brain mapping.

[82]  Anders M. Dale,et al.  Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex , 2001, IEEE Transactions on Medical Imaging.

[83]  A. Friederici The brain basis of language processing: from structure to function. , 2011, Physiological reviews.

[84]  Sigal Berman,et al.  Anatomical Abnormalities in Autism? , 2016, Cerebral cortex.

[85]  Peter Kochunov,et al.  Heritability of brain volume, surface area and shape: An MRI study in an extended pedigree of baboons , 2007, Human brain mapping.

[86]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[87]  Jin Fan Attentional Network Deficits in Autism Spectrum Disorders , 2013 .

[88]  Christine Ecker,et al.  Neuroimaging in autism spectrum disorder: brain structure and function across the lifespan , 2015, The Lancet Neurology.

[89]  Lawrence Scahill,et al.  Social Skills Development in Children with Autism Spectrum Disorders: A Review of the Intervention Research , 2007, Journal of autism and developmental disorders.

[90]  Eric Courchesne,et al.  Differential effects of developmental cerebellar abnormality on cognitive and motor functions in the cerebellum: an fMRI study of autism. , 2003, The American journal of psychiatry.

[91]  Allan L. Reiss,et al.  Estimating individual contribution from group-based structural correlation networks , 2015, NeuroImage.

[92]  Karl J. Friston Causal Modelling and Brain Connectivity in Functional Magnetic Resonance Imaging , 2009, PLoS biology.

[93]  Jin Fan,et al.  Abnormal autonomic and associated brain activities during rest in autism spectrum disorder. , 2014, Brain : a journal of neurology.

[94]  Stewart H. Mostofsky,et al.  Motor Signs Distinguish Children with High Functioning Autism and Asperger’s Syndrome from Controls , 2006, Journal of autism and developmental disorders.

[95]  Alexander J. Dufford,et al.  Gray matter volume of the anterior insular cortex and social networking , 2018, The Journal of comparative neurology.

[96]  N. Meinshausen,et al.  High-dimensional graphs and variable selection with the Lasso , 2006, math/0608017.

[97]  J. Decety,et al.  Empathic arousal and social understanding in individuals with autism: evidence from fMRI and ERP measurements. , 2014, Social cognitive and affective neuroscience.

[98]  Alan C. Evans,et al.  Neuroanatomical differences in brain areas implicated in perceptual and other core features of autism revealed by cortical thickness analysis and voxel‐based morphometry , 2009, Human brain mapping.

[99]  Jin Fan,et al.  Chapter 11 – Functional Neuroimaging of Deficits in Cognitive Control , 2017 .

[100]  H. Zou,et al.  Regularization and variable selection via the elastic net , 2005 .

[101]  Kaustubh Supekar,et al.  Estimation of functional connectivity in fMRI data using stability selection-based sparse partial correlation with elastic net penalty , 2012, NeuroImage.

[102]  Jared A. Nielsen,et al.  Multisite functional connectivity MRI classification of autism: ABIDE results , 2013, Front. Hum. Neurosci..

[103]  Steven C. R. Williams,et al.  Describing the Brain in Autism in Five Dimensions—Magnetic Resonance Imaging-Assisted Diagnosis of Autism Spectrum Disorder Using a Multiparameter Classification Approach , 2010, The Journal of Neuroscience.

[104]  Shuiwang Ji,et al.  SLEP: Sparse Learning with Efficient Projections , 2011 .

[105]  Aixia Guo,et al.  Gene Selection for Cancer Classification using Support Vector Machines , 2014 .

[106]  Jesper Andersson,et al.  A multi-modal parcellation of human cerebral cortex , 2016, Nature.

[107]  Nathan D. Cahill,et al.  The predictive power of structural MRI in Autism diagnosis , 2015, 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[108]  Janaina Mourão Miranda,et al.  Investigating the predictive value of whole-brain structural MR scans in autism: A pattern classification approach , 2010, NeuroImage.