Clinically feasible brain morphometric similarity network construction approaches with restricted magnetic resonance imaging acquisitions

Morphometric similarity networks (MSNs) estimate organization of the cortex as a biologically meaningful set of similarities between anatomical features at the macro- and microstructural level, derived from multiple structural MRI (sMRI) sequences. These networks are clinically relevant, predicting 40% variance in IQ. However, the sequences required (T1w, T2w, DWI) to produce these networks are longer acquisitions, less feasible in some populations. Thus, estimating MSNs using features from T1w sMRI is attractive to clinical and developmental neuroscience. We studied whether reduced-feature approaches approximate the original MSN model as a potential tool to investigate brain structure. In a large, homogenous dataset of healthy young adults (from the Human Connectome Project, HCP), we extended previous investigations of reduced-feature MSNs by comparing not only T1w-derived networks, but also additional MSNs generated with fewer MR sequences, to their full acquisition counterparts. We produce MSNs that are highly similar at the edge level to those generated with multimodal imaging; however, the nodal topology of the networks differed. These networks had limited predictive validity of generalized cognitive ability. Overall, when multimodal imaging is not available or appropriate, T1w-restricted MSN construction is feasible, provides an appropriate estimate of the MSN, and could be a useful approach to examine outcomes in future studies.

[1]  Casey Paquola,et al.  Transcriptomic and Cellular Decoding of Regional Brain Vulnerability to Neurodevelopmental Disorders , 2019, bioRxiv.

[2]  Stamatios N. Sotiropoulos,et al.  An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging , 2016, NeuroImage.

[3]  Chunlan Yang,et al.  Construction of Individual Morphological Brain Networks with Multiple Morphometric Features , 2017, Front. Neuroanat..

[4]  Vince D. Calhoun,et al.  Chronnectomic patterns and neural flexibility underlie executive function , 2017, NeuroImage.

[5]  Michel Tenenhaus,et al.  PLS generalised linear regression , 2005, Comput. Stat. Data Anal..

[6]  D. Tulsky,et al.  V. NIH Toolbox Cognition Battery (CB): measuring working memory. , 2013, Monographs of the Society for Research in Child Development.

[7]  G Kishi,et al.  Reliability and Validity , 1999 .

[8]  M. Dylan Tisdall,et al.  Quantitative assessment of structural image quality , 2018, NeuroImage.

[9]  Timothy O. Laumann,et al.  Informatics and Data Mining Tools and Strategies for the Human Connectome Project , 2011, Front. Neuroinform..

[10]  M. Maumy-Bertrand,et al.  plsRglm: Partial least squares linear and generalized linear regression for processing incomplete datasets by cross-validation and bootstrap techniques with R , 2018, 1810.01005.

[11]  John O. Willis,et al.  Wechsler Intelligence Scale for Children–Fourth Edition , 2014 .

[12]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[13]  Luís Torgo,et al.  Resampling strategies for regression , 2015, Expert Syst. J. Knowl. Eng..

[14]  Anthony Randal McIntosh,et al.  Partial Least Squares (PLS) methods for neuroimaging: A tutorial and review , 2011, NeuroImage.

[15]  Stefan Skare,et al.  How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging , 2003, NeuroImage.

[16]  S. Weintraub,et al.  NIH Toolbox Cognition Battery (CB): Validation of Executive Function Measures in Adults , 2014, Journal of the International Neuropsychological Society.

[17]  A. Dale,et al.  Whole Brain Segmentation Automated Labeling of Neuroanatomical Structures in the Human Brain , 2002, Neuron.

[18]  Weihao Zheng,et al.  Multi-Feature Based Network Revealing the Structural Abnormalities in Autism Spectrum Disorder , 2021, IEEE Transactions on Affective Computing.

[19]  Vince D. Calhoun,et al.  Multimodal neural correlates of cognitive control in the Human Connectome Project , 2017, NeuroImage.

[20]  Philip David Zelazo,et al.  The Dimensional Change Card Sort (DCCS): a method of assessing executive function in children , 2006, Nature Protocols.

[21]  Edward T. Bullmore,et al.  Fundamentals of Brain Network Analysis , 2016 .

[22]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.

[23]  Ninon Burgos,et al.  New advances in the Clinica software platform for clinical neuroimaging studies , 2019 .

[24]  Michael Breakspear,et al.  Graph analysis of the human connectome: Promise, progress, and pitfalls , 2013, NeuroImage.

[25]  E. Bullmore,et al.  Imaging structural co-variance between human brain regions , 2013, Nature Reviews Neuroscience.

[26]  Dafnis Batalle,et al.  Annual Research Review: Not just a small adult brain: understanding later neurodevelopment through imaging the neonatal brain , 2017, Journal of child psychology and psychiatry, and allied disciplines.

[27]  E. Bullmore,et al.  The Convergence of Maturational Change and Structural Covariance in Human Cortical Networks , 2013, The Journal of Neuroscience.

[28]  M. Stone Cross‐Validatory Choice and Assessment of Statistical Predictions , 1976 .

[29]  Jerry Slotkin,et al.  VIII. NIH Toolbox Cognition Battery (CB): composite scores of crystallized, fluid, and overall cognition. , 2013, Monographs of the Society for Research in Child Development.

[30]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[31]  Corson N. Areshenkoff,et al.  The Unity and Diversity of Executive Functions: A Systematic Review and Re-Analysis of Latent Variable Studies , 2018, Psychological bulletin.

[32]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[33]  Kirstie Whitaker,et al.  Cortical patterning of abnormal morphometric similarity in psychosis is associated with brain expression of schizophrenia related genes , 2018, bioRxiv.

[34]  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.

[35]  Mark E. Bastin,et al.  Neonatal Morphometric Similarity Networks Predict Atypical Brain Development Associated with Preterm Birth , 2018, CNI@MICCAI.

[36]  Abraham Z. Snyder,et al.  Function in the human connectome: Task-fMRI and individual differences in behavior , 2013, NeuroImage.

[37]  Peter B. Jones,et al.  Morphometric Similarity Networks Detect Microscale Cortical Organization and Predict Inter-Individual Cognitive Variation , 2017, Neuron.

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

[39]  Angelo Bifone,et al.  Structural covariance networks in the mouse brain , 2016, NeuroImage.

[40]  D. Wechsler Wechsler Adult Intelligence Scale , 2021, Encyclopedia of Evolutionary Psychological Science.

[41]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[42]  D. V. van Essen,et al.  Mapping Human Cortical Areas In Vivo Based on Myelin Content as Revealed by T1- and T2-Weighted MRI , 2011, The Journal of Neuroscience.

[43]  Andreas Hahn,et al.  Making Sense of Connectivity , 2018, The international journal of neuropsychopharmacology.

[44]  E. Bullmore,et al.  Cortical patterning of abnormal morphometric similarity in psychosis is associated with brain expression of schizophrenia-related genes , 2018, Proceedings of the National Academy of Sciences.

[45]  Robert K. Heaton,et al.  Reliability and Validity of Composite Scores from the NIH Toolbox Cognition Battery in Adults , 2014, Journal of the International Neuropsychological Society.

[46]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

[47]  Vince D. Calhoun,et al.  Multimodal neural correlates of cognitive control in the Human Connectome Project , 2017 .

[48]  Suzanne E. Welcome,et al.  Longitudinal Mapping of Cortical Thickness and Brain Growth in Normal Children , 2022 .

[49]  D. Wechsler,et al.  Wechsler Adult Intelligence Scale—Fourth Edition (WAIS-IV) , 2010 .

[50]  N. Mantel The detection of disease clustering and a generalized regression approach. , 1967, Cancer research.

[51]  R. Mccall,et al.  The Genetic and Environmental Origins of Learning Abilities and Disabilities in the Early School , 2007, Monographs of the Society for Research in Child Development.

[52]  Claus C. Hilgetag,et al.  Principles of ipsilateral and contralateral cortico-cortical connectivity in the mouse , 2015, Brain Structure and Function.

[53]  M. Roth A quantitative assessment , 1987 .

[54]  D. Wechsler Wechsler Intelligence Scale for Children , 2020, Definitions.

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

[56]  Jongin Kim,et al.  Identification of Alzheimer's disease and mild cognitive impairment using multimodal sparse hierarchical extreme learning machine , 2018, Human brain mapping.

[57]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[58]  Lianne H. Scholtens,et al.  Multiscale examination of cytoarchitectonic similarity and human brain connectivity , 2018, Network Neuroscience.

[59]  Davide Ballabio,et al.  Evaluation of model predictive ability by external validation techniques , 2010 .

[60]  Stamatios N. Sotiropoulos,et al.  Non-parametric representation and prediction of single- and multi-shell diffusion-weighted MRI data using Gaussian processes , 2015, NeuroImage.