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Heritability of individualized cortical network topography

Human cortex is patterned by a complex and interdigitated web of large-scale functional networks. Recent methodological breakthroughs reveal variation in the size, shape, and spatial topography of cortical networks across individuals. While spatial network organization emerges across development, is...

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Autores principales: Anderson, Kevin M., Ge, Tian, Kong, Ru, Patrick, Lauren M., Spreng, R. Nathan, Sabuncu, Mert R., Yeo, B. T. Thomas, Holmes, Avram J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7936334/
https://www.ncbi.nlm.nih.gov/pubmed/33622790
http://dx.doi.org/10.1073/pnas.2016271118
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author Anderson, Kevin M.
Ge, Tian
Kong, Ru
Patrick, Lauren M.
Spreng, R. Nathan
Sabuncu, Mert R.
Yeo, B. T. Thomas
Holmes, Avram J.
author_facet Anderson, Kevin M.
Ge, Tian
Kong, Ru
Patrick, Lauren M.
Spreng, R. Nathan
Sabuncu, Mert R.
Yeo, B. T. Thomas
Holmes, Avram J.
author_sort Anderson, Kevin M.
collection PubMed
description Human cortex is patterned by a complex and interdigitated web of large-scale functional networks. Recent methodological breakthroughs reveal variation in the size, shape, and spatial topography of cortical networks across individuals. While spatial network organization emerges across development, is stable over time, and is predictive of behavior, it is not yet clear to what extent genetic factors underlie interindividual differences in network topography. Here, leveraging a nonlinear multidimensional estimation of heritability, we provide evidence that individual variability in the size and topographic organization of cortical networks are under genetic control. Using twin and family data from the Human Connectome Project (n = 1,023), we find increased variability and reduced heritability in the size of heteromodal association networks (h(2): M = 0.34, SD = 0.070), relative to unimodal sensory/motor cortex (h(2): M = 0.40, SD = 0.097). We then demonstrate that the spatial layout of cortical networks is influenced by genetics, using our multidimensional estimation of heritability (h(2)-multi; M = 0.14, SD = 0.015). However, topographic heritability did not differ between heteromodal and unimodal networks. Genetic factors had a regionally variable influence on brain organization, such that the heritability of network topography was greatest in prefrontal, precuneus, and posterior parietal cortex. Taken together, these data are consistent with relaxed genetic control of association cortices relative to primary sensory/motor regions and have implications for understanding population-level variability in brain functioning, guiding both individualized prediction and the interpretation of analyses that integrate genetics and neuroimaging.
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spelling pubmed-79363342021-03-11 Heritability of individualized cortical network topography Anderson, Kevin M. Ge, Tian Kong, Ru Patrick, Lauren M. Spreng, R. Nathan Sabuncu, Mert R. Yeo, B. T. Thomas Holmes, Avram J. Proc Natl Acad Sci U S A Biological Sciences Human cortex is patterned by a complex and interdigitated web of large-scale functional networks. Recent methodological breakthroughs reveal variation in the size, shape, and spatial topography of cortical networks across individuals. While spatial network organization emerges across development, is stable over time, and is predictive of behavior, it is not yet clear to what extent genetic factors underlie interindividual differences in network topography. Here, leveraging a nonlinear multidimensional estimation of heritability, we provide evidence that individual variability in the size and topographic organization of cortical networks are under genetic control. Using twin and family data from the Human Connectome Project (n = 1,023), we find increased variability and reduced heritability in the size of heteromodal association networks (h(2): M = 0.34, SD = 0.070), relative to unimodal sensory/motor cortex (h(2): M = 0.40, SD = 0.097). We then demonstrate that the spatial layout of cortical networks is influenced by genetics, using our multidimensional estimation of heritability (h(2)-multi; M = 0.14, SD = 0.015). However, topographic heritability did not differ between heteromodal and unimodal networks. Genetic factors had a regionally variable influence on brain organization, such that the heritability of network topography was greatest in prefrontal, precuneus, and posterior parietal cortex. Taken together, these data are consistent with relaxed genetic control of association cortices relative to primary sensory/motor regions and have implications for understanding population-level variability in brain functioning, guiding both individualized prediction and the interpretation of analyses that integrate genetics and neuroimaging. National Academy of Sciences 2021-03-02 2021-02-23 /pmc/articles/PMC7936334/ /pubmed/33622790 http://dx.doi.org/10.1073/pnas.2016271118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Anderson, Kevin M.
Ge, Tian
Kong, Ru
Patrick, Lauren M.
Spreng, R. Nathan
Sabuncu, Mert R.
Yeo, B. T. Thomas
Holmes, Avram J.
Heritability of individualized cortical network topography
title Heritability of individualized cortical network topography
title_full Heritability of individualized cortical network topography
title_fullStr Heritability of individualized cortical network topography
title_full_unstemmed Heritability of individualized cortical network topography
title_short Heritability of individualized cortical network topography
title_sort heritability of individualized cortical network topography
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7936334/
https://www.ncbi.nlm.nih.gov/pubmed/33622790
http://dx.doi.org/10.1073/pnas.2016271118
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