Genomic structural equation modeling reveals latent phenotypes in the human cortex with distinct genetic architecture

Abstract Genetic contributions to human cortical structure manifest pervasive pleiotropy. This pleiotropy may be harnessed to identify unique genetically-informed parcellations of the cortex that are neurobiologically distinct from functional, cytoarchitectural, or other cortical parcellation scheme...

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Main Authors: Rajendra A. Morey, Yuanchao Zheng, Henry Bayly, Delin Sun, Melanie E. Garrett, Marianna Gasperi, Adam X. Maihofer, C. Lexi Baird, Katrina L. Grasby, Ashley A. Huggins, Courtney C. Haswell, Paul M. Thompson, Sarah Medland, Daniel E. Gustavson, Matthew S. Panizzon, William S. Kremen, Caroline M. Nievergelt, Allison E. Ashley-Koch, Mark W. Logue
Format: Article
Language:English
Published: Nature Publishing Group 2024-10-01
Series:Translational Psychiatry
Online Access:https://doi.org/10.1038/s41398-024-03152-y
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author Rajendra A. Morey
Yuanchao Zheng
Henry Bayly
Delin Sun
Melanie E. Garrett
Marianna Gasperi
Adam X. Maihofer
C. Lexi Baird
Katrina L. Grasby
Ashley A. Huggins
Courtney C. Haswell
Paul M. Thompson
Sarah Medland
Daniel E. Gustavson
Matthew S. Panizzon
William S. Kremen
Caroline M. Nievergelt
Allison E. Ashley-Koch
Mark W. Logue
author_facet Rajendra A. Morey
Yuanchao Zheng
Henry Bayly
Delin Sun
Melanie E. Garrett
Marianna Gasperi
Adam X. Maihofer
C. Lexi Baird
Katrina L. Grasby
Ashley A. Huggins
Courtney C. Haswell
Paul M. Thompson
Sarah Medland
Daniel E. Gustavson
Matthew S. Panizzon
William S. Kremen
Caroline M. Nievergelt
Allison E. Ashley-Koch
Mark W. Logue
author_sort Rajendra A. Morey
collection DOAJ
description Abstract Genetic contributions to human cortical structure manifest pervasive pleiotropy. This pleiotropy may be harnessed to identify unique genetically-informed parcellations of the cortex that are neurobiologically distinct from functional, cytoarchitectural, or other cortical parcellation schemes. We investigated genetic pleiotropy by applying genomic structural equation modeling (SEM) to map the genetic architecture of cortical surface area (SA) and cortical thickness (CT) for 34 brain regions recently reported in the ENIGMA cortical GWAS. Genomic SEM uses the empirical genetic covariance estimated from GWAS summary statistics with LD score regression (LDSC) to discover factors underlying genetic covariance, which we are denoting genetically informed brain networks (GIBNs). Genomic SEM can fit a multivariate GWAS from summary statistics for each of the GIBNs, which can subsequently be used for LD score regression (LDSC). We found the best-fitting model of cortical SA identified 6 GIBNs and CT identified 4 GIBNs, although sensitivity analyses indicated that other structures were plausible. The multivariate GWASs of the GIBNs identified 74 genome-wide significant (GWS) loci (p < 5 × 10− 8), including many previously implicated in neuroimaging phenotypes, behavioral traits, and psychiatric conditions. LDSC of GIBN GWASs found that SA-derived GIBNs had a positive genetic correlation with bipolar disorder (BPD), and cannabis use disorder, indicating genetic predisposition to a larger SA in the specific GIBN is associated with greater genetic risk of these disorders. A negative genetic correlation was observed between attention deficit hyperactivity disorder (ADHD) and major depressive disorder (MDD). CT GIBNs displayed a negative genetic correlation with alcohol dependence. Even though we observed model instability in our application of genomic SEM to high-dimensional data, jointly modeling the genetic architecture of complex traits and investigating multivariate genetic links across neuroimaging phenotypes offers new insights into the genetics of cortical structure and relationships to psychopathology.
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spelling doaj-art-c70e4e39177a4a89ac4215e867dc171d2025-08-20T02:11:49ZengNature Publishing GroupTranslational Psychiatry2158-31882024-10-0114111110.1038/s41398-024-03152-yGenomic structural equation modeling reveals latent phenotypes in the human cortex with distinct genetic architectureRajendra A. Morey0Yuanchao Zheng1Henry Bayly2Delin Sun3Melanie E. Garrett4Marianna Gasperi5Adam X. Maihofer6C. Lexi Baird7Katrina L. Grasby8Ashley A. Huggins9Courtney C. Haswell10Paul M. Thompson11Sarah Medland12Daniel E. Gustavson13Matthew S. Panizzon14William S. Kremen15Caroline M. Nievergelt16Allison E. Ashley-Koch17Mark W. Logue18Brain Imaging and Analysis Center, Duke UniversityNational Center for PTSD, VA Boston Healthcare SystemNational Center for PTSD, VA Boston Healthcare SystemBrain Imaging and Analysis Center, Duke UniversityVISN 6 MIRECC, VA Health Care System, Croasdaile DriveVA Center of Excellence for Stress and Mental Health, VA San Diego Healthcare SystemResearch Service VA, San Diego Healthcare SystemBrain Imaging and Analysis Center, Duke UniversityPsychiatric Genetics, QIMR, Berghofer Medical Research InstituteBrain Imaging and Analysis Center, Duke UniversityBrain Imaging and Analysis Center, Duke UniversityImaging Genetics Center, Stevens Neuroimaging & Informatics Institute Keck School of Medicine University of Southern CaliforniaQueensland Institute for Medical Research, Berghofer Medical Research InstituteInstitute for Behavioral Genetics, University of Colorado BoulderStein Institute for Research on Aging, University of California San DiegoStein Institute for Research on Aging, University of California San DiegoVA Center of Excellence for Stress and Mental Health, VA San Diego Healthcare SystemVISN 6 MIRECC, VA Health Care System, Croasdaile DriveNational Center for PTSD, VA Boston Healthcare SystemAbstract Genetic contributions to human cortical structure manifest pervasive pleiotropy. This pleiotropy may be harnessed to identify unique genetically-informed parcellations of the cortex that are neurobiologically distinct from functional, cytoarchitectural, or other cortical parcellation schemes. We investigated genetic pleiotropy by applying genomic structural equation modeling (SEM) to map the genetic architecture of cortical surface area (SA) and cortical thickness (CT) for 34 brain regions recently reported in the ENIGMA cortical GWAS. Genomic SEM uses the empirical genetic covariance estimated from GWAS summary statistics with LD score regression (LDSC) to discover factors underlying genetic covariance, which we are denoting genetically informed brain networks (GIBNs). Genomic SEM can fit a multivariate GWAS from summary statistics for each of the GIBNs, which can subsequently be used for LD score regression (LDSC). We found the best-fitting model of cortical SA identified 6 GIBNs and CT identified 4 GIBNs, although sensitivity analyses indicated that other structures were plausible. The multivariate GWASs of the GIBNs identified 74 genome-wide significant (GWS) loci (p < 5 × 10− 8), including many previously implicated in neuroimaging phenotypes, behavioral traits, and psychiatric conditions. LDSC of GIBN GWASs found that SA-derived GIBNs had a positive genetic correlation with bipolar disorder (BPD), and cannabis use disorder, indicating genetic predisposition to a larger SA in the specific GIBN is associated with greater genetic risk of these disorders. A negative genetic correlation was observed between attention deficit hyperactivity disorder (ADHD) and major depressive disorder (MDD). CT GIBNs displayed a negative genetic correlation with alcohol dependence. Even though we observed model instability in our application of genomic SEM to high-dimensional data, jointly modeling the genetic architecture of complex traits and investigating multivariate genetic links across neuroimaging phenotypes offers new insights into the genetics of cortical structure and relationships to psychopathology.https://doi.org/10.1038/s41398-024-03152-y
spellingShingle Rajendra A. Morey
Yuanchao Zheng
Henry Bayly
Delin Sun
Melanie E. Garrett
Marianna Gasperi
Adam X. Maihofer
C. Lexi Baird
Katrina L. Grasby
Ashley A. Huggins
Courtney C. Haswell
Paul M. Thompson
Sarah Medland
Daniel E. Gustavson
Matthew S. Panizzon
William S. Kremen
Caroline M. Nievergelt
Allison E. Ashley-Koch
Mark W. Logue
Genomic structural equation modeling reveals latent phenotypes in the human cortex with distinct genetic architecture
Translational Psychiatry
title Genomic structural equation modeling reveals latent phenotypes in the human cortex with distinct genetic architecture
title_full Genomic structural equation modeling reveals latent phenotypes in the human cortex with distinct genetic architecture
title_fullStr Genomic structural equation modeling reveals latent phenotypes in the human cortex with distinct genetic architecture
title_full_unstemmed Genomic structural equation modeling reveals latent phenotypes in the human cortex with distinct genetic architecture
title_short Genomic structural equation modeling reveals latent phenotypes in the human cortex with distinct genetic architecture
title_sort genomic structural equation modeling reveals latent phenotypes in the human cortex with distinct genetic architecture
url https://doi.org/10.1038/s41398-024-03152-y
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