Unsupervised Manifold Learning Using High-Order Morphological Brain Networks Derived From T1-w MRI for Autism Diagnosis

Brain disorders, such as Autism Spectrum Disorder (ASD), alter brain functional (from fMRI) and structural (from diffusion MRI) connectivities at multiple levels and in varying degrees. While unraveling such alterations have been the focus of a large number of studies, morphological brain connectivity has been out of the research scope. In particular, shape-to-shape relationships across brain regions of interest (ROIs) were rarely investigated. As such, the use of networks based on morphological brain data in neurological disorder diagnosis, while leveraging the advent of machine learning, could complement our knowledge on brain wiring alterations in unprecedented ways. In this paper, we use conventional T1-weighted MRI to define morphological brain networks (MBNs), each quantifying shape relationship between different cortical regions for a specific cortical attribute at both low-order and high-order levels. While typical brain connectomes investigate the relationship between two ROIs, we propose high-order MBN which better captures brain complex interactions by modeling the morphological relationship between pairs of ROIs. For ASD identification, we present a connectomic manifold learning framework, which learns multiple kernels to estimate a similarity measure between ASD and normal controls (NC) connectional features, to perform dimensionality reduction for clustering ASD and NC subjects. We benchmark our ASD identification method against both supervised and unsupervised state-of-the-art methods, while depicting the most discriminative high- and low-order relationships between morphological regions in the left and right hemispheres.

[1]  Ajay S. Pillai,et al.  Altered task‐related modulation of long‐range connectivity in children with autism , 2018, Autism research : official journal of the International Society for Autism Research.

[2]  Tatiana A. Stroganova,et al.  Arousal and attention re-orienting in autism spectrum disorders: evidence from auditory event-related potentials , 2014, Front. Hum. Neurosci..

[3]  Dinggang Shen,et al.  Ensemble Hierarchical High-Order Functional Connectivity Networks for MCI Classification , 2016, MICCAI.

[4]  Geraldine Dawson,et al.  Neural correlates of face and object recognition in young children with autism spectrum disorder, developmental delay, and typical development. , 2002, Child development.

[5]  Jure Leskovec,et al.  Modeling Information Diffusion in Implicit Networks , 2010, 2010 IEEE International Conference on Data Mining.

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

[7]  Islem Rekik,et al.  Pairing-based Ensemble Classifier Learning using Convolutional Brain Multiplexes and Multi-view Brain Networks for Early Dementia Diagnosis , 2017, CNI@MICCAI.

[8]  Y. Duan,et al.  Detecting corpus callosum abnormalities in autism based on anatomical landmarks , 2010, Psychiatry Research: Neuroimaging.

[9]  Vassilis Tsiaras,et al.  Extracting biomarkers of autism from MEG resting-state functional connectivity networks , 2011, Comput. Biol. Medicine.

[10]  Matcheri S. Keshavan,et al.  An MRI study of increased cortical thickness in autism. , 2006, The American journal of psychiatry.

[11]  R. Lenroot,et al.  Heterogeneity within Autism Spectrum Disorders: What have We Learned from Neuroimaging Studies? , 2013, Front. Hum. Neurosci..

[12]  N. Kanwisher,et al.  The lateral occipital complex and its role in object recognition , 2001, Vision Research.

[13]  Nicholas Lange,et al.  Corpus Callosum Area in Children and Adults with Autism. , 2013, Research in autism spectrum disorders.

[14]  Heidi Johansen-Berg,et al.  Tractography: Where Do We Go from Here? , 2011, Brain Connect..

[15]  Matcheri S. Keshavan,et al.  Volumetric alterations of the orbitofrontal cortex in autism , 2007, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[16]  Islem Rekik,et al.  Joint Pairing and Structured Mapping of Convolutional Brain Morphological Multiplexes for Early Dementia Diagnosis , 2019, Brain Connect..

[17]  Geoffrey E. Hinton,et al.  Visualizing Data using t-SNE , 2008 .

[18]  Sanna Kuusikko-Gauffin,et al.  Face memory and object recognition in children with high-functioning autism or Asperger syndrome and in their parents , 2011 .

[19]  Dinggang Shen,et al.  Multiple-Network Classification of Childhood Autism Using Functional Connectivity Dynamics , 2014, MICCAI.

[20]  Yanbin Liu,et al.  Discriminative multi-view feature selection and fusion , 2015, 2015 IEEE International Conference on Multimedia and Expo (ICME).

[21]  Dinggang Shen,et al.  Reveal Consistent Spatial-Temporal Patterns from Dynamic Functional Connectivity for Autism Spectrum Disorder Identification , 2016, MICCAI.

[22]  Antonio Y Hardan,et al.  An MRI study of increased cortical thickness in autism. , 2006, The American journal of psychiatry.

[23]  Jared A. Nielsen,et al.  Functional connectivity magnetic resonance imaging classification of autism. , 2011, Brain : a journal of neurology.

[24]  Ruth A. Carper,et al.  Unusual brain growth patterns in early life in patients with autistic disorder , 2001, Neurology.

[25]  João Ricardo Sato,et al.  Identification of segregated regions in the functional brain connectome of autistic patients by a combination of fuzzy spectral clustering and entropy analysis. , 2016, Journal of psychiatry & neuroscience : JPN.

[26]  C. Jack,et al.  Alzheimer's Disease Neuroimaging Initiative , 2008 .

[27]  Paul M. Thompson,et al.  Evaluating 35 Methods to Generate Structural Connectomes Using Pairwise Classification , 2017, bioRxiv.

[28]  Xiang Wang,et al.  Unsupervised learning of disease progression models , 2014, KDD.

[29]  Yong Xu,et al.  Sparse Coding for Classification via Discrimination Ensemble , 2016, 2016 IEEE Conference on Computer Vision and Pattern Recognition (CVPR).

[30]  J. H. Ward Hierarchical Grouping to Optimize an Objective Function , 1963 .

[31]  Jesse A. Brown,et al.  Altered functional and structural brain network organization in autism☆ , 2012, NeuroImage: Clinical.

[32]  Andrea Caria,et al.  Anterior insular cortex regulation in autism spectrum disorders , 2015, Front. Behav. Neurosci..

[33]  Deanna Greenstein,et al.  Cortical thickness change in autism during early childhood , 2016, Human brain mapping.

[34]  Guido Gerig,et al.  Altered corpus callosum morphology associated with autism over the first 2 years of life. , 2015, Brain : a journal of neurology.

[35]  Alan C. Evans,et al.  Cortical Thickness Abnormalities in Autism Spectrum Disorders Through Late Childhood, Adolescence, and Adulthood: A Large‐Scale MRI Study , 2017, Cerebral cortex.

[36]  George Zouridakis,et al.  Functional connectivity networks in the autistic and healthy brain assessed using Granger causality , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[37]  Danielle S Bassett,et al.  Brain graphs: graphical models of the human brain connectome. , 2011, Annual review of clinical psychology.

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

[39]  Bernard Zenko,et al.  Is Combining Classifiers with Stacking Better than Selecting the Best One? , 2004, Machine Learning.

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

[41]  Takashi Yamada,et al.  Altered functional organization within the insular cortex in adult males with high-functioning autism spectrum disorder: evidence from connectivity-based parcellation , 2016, Molecular Autism.

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

[43]  J. Belliveau,et al.  Neuroimaging of the functional and structural networks underlying visuospatial vs. linguistic reasoning in high-functioning autism , 2010, Neuropsychologia.

[44]  G. Dawson,et al.  Brain structural abnormalities in young children with autism spectrum disorder , 2002, Neurology.

[45]  J. Piven,et al.  Magnetic resonance imaging and head circumference study of brain size in autism: birth through age 2 years. , 2005, Archives of general psychiatry.

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

[47]  Dinggang Shen,et al.  Diagnosis of Autism Spectrum Disorders Using Multi-Level High-Order Functional Networks Derived From Resting-State Functional MRI , 2018, Front. Hum. Neurosci..

[48]  Meirav Galun,et al.  Fundamental Limitations of Spectral Clustering , 2006, NIPS.

[49]  Nicholas Lange,et al.  Longitudinal changes in cortical thickness in autism and typical development. , 2014, Brain : a journal of neurology.

[50]  Raymond J. Dolan,et al.  Fusiform Gyrus Face Selectivity Relates to Individual Differences in Facial Recognition Ability , 2011, Journal of Cognitive Neuroscience.

[51]  A. Guastella,et al.  An Overview of Autism Spectrum Disorder, Heterogeneity and Treatment Options , 2017, Neuroscience Bulletin.

[52]  Dinggang Shen,et al.  Simultaneous Estimation of Low- and High-Order Functional Connectivity for Identifying Mild Cognitive Impairment , 2018, Front. Neuroinform..

[53]  Jinglei Lv,et al.  Longitudinal Analysis of Brain Recovery after Mild Traumatic Brain Injury Based on Groupwise Consistent Brain Network Clusters , 2015, MICCAI.

[54]  Tsutomu Hashikawa,et al.  Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95–neuroligin , 2007, Nature Neuroscience.

[55]  R. Landa,et al.  Diagnosis of autism spectrum disorders in the first 3 years of life , 2008, Nature Clinical Practice Neurology.

[56]  Junjie Zhu,et al.  Visualization and analysis of single-cell RNA-seq data by kernel-based similarity learning , 2016, bioRxiv.

[57]  Simon Hametner,et al.  Disease-specific molecular events in cortical multiple sclerosis lesions , 2013, Brain : a journal of neurology.

[58]  Bruce Fischl,et al.  FreeSurfer , 2012, NeuroImage.

[59]  Lucina Q. Uddin,et al.  The anterior insula in autism: Under-connected and under-examined , 2009, Neuroscience & Biobehavioral Reviews.

[60]  Catherine Lord,et al.  Autism Spectrum Disorders , 2000, Neuron.

[61]  Islem Rekik,et al.  High-order Connectomic Manifold Learning for Autistic Brain State Identification , 2017, CNI@MICCAI.

[62]  Ghassan Hamarneh,et al.  Machine Learning on Human Connectome Data from MRI , 2016, ArXiv.

[63]  Islem Rekik,et al.  Brain multiplexes reveal morphological connectional biomarkers fingerprinting late brain dementia states , 2018, Scientific Reports.

[64]  C. McDougle,et al.  Structural and functional magnetic resonance imaging of autism spectrum disorders , 2011, Brain Research.

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

[66]  Deng Cai,et al.  Laplacian Score for Feature Selection , 2005, NIPS.

[67]  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.

[68]  Timothy P. L. Roberts,et al.  DTI Based Diagnostic Prediction of a Disease via Pattern Classification , 2010, MICCAI.

[69]  Yang Wang,et al.  Identifying Connectome Module Patterns via New Balanced Multi-graph Normalized Cut , 2015, MICCAI.