Evolution of cortical geometry and its link to function, behaviour and ecology

Abstract Studies in comparative neuroanatomy and of the fossil record demonstrate the influence of socio-ecological niches on the morphology of the cerebral cortex, but have led to oftentimes conflicting theories about its evolution. Here, we study the relationship between the shape of the cerebral...

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Main Authors: Ernst Schwartz, Karl-Heinz Nenning, Katja Heuer, Nathan Jeffery, Ornella C. Bertrand, Roberto Toro, Gregor Kasprian, Daniela Prayer, Georg Langs
Format: Article
Language:English
Published: Nature Portfolio 2023-04-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-023-37574-x
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author Ernst Schwartz
Karl-Heinz Nenning
Katja Heuer
Nathan Jeffery
Ornella C. Bertrand
Roberto Toro
Gregor Kasprian
Daniela Prayer
Georg Langs
author_facet Ernst Schwartz
Karl-Heinz Nenning
Katja Heuer
Nathan Jeffery
Ornella C. Bertrand
Roberto Toro
Gregor Kasprian
Daniela Prayer
Georg Langs
author_sort Ernst Schwartz
collection DOAJ
description Abstract Studies in comparative neuroanatomy and of the fossil record demonstrate the influence of socio-ecological niches on the morphology of the cerebral cortex, but have led to oftentimes conflicting theories about its evolution. Here, we study the relationship between the shape of the cerebral cortex and the topography of its function. We establish a joint geometric representation of the cerebral cortices of ninety species of extant Euarchontoglires, including commonly used experimental model organisms. We show that variability in surface geometry relates to species’ ecology and behaviour, independent of overall brain size. Notably, ancestral shape reconstruction of the cortical surface and its change during evolution enables us to trace the evolutionary history of localised cortical expansions, modal segregation of brain function, and their association to behaviour and cognition. We find that individual cortical regions follow different sequences of area increase during evolutionary adaptations to dynamic socio-ecological niches. Anatomical correlates of this sequence of events are still observable in extant species, and relate to their current behaviour and ecology. We decompose the deep evolutionary history of the shape of the human cortical surface into spatially and temporally conscribed components with highly interpretable functional associations, highlighting the importance of considering the evolutionary history of cortical regions when studying their anatomy and function.
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spelling doaj.art-c537b50d42aa4540b9f01a2aa03771302023-04-23T11:21:31ZengNature PortfolioNature Communications2041-17232023-04-0114111910.1038/s41467-023-37574-xEvolution of cortical geometry and its link to function, behaviour and ecologyErnst Schwartz0Karl-Heinz Nenning1Katja Heuer2Nathan Jeffery3Ornella C. Bertrand4Roberto Toro5Gregor Kasprian6Daniela Prayer7Georg Langs8Department of Biomedical Imaging and Image-guided Therapy, Computational Imaging Research Lab, Medical University of ViennaDepartment of Biomedical Imaging and Image-guided Therapy, Computational Imaging Research Lab, Medical University of ViennaInstitut Pasteur, Université Paris Cité, Unité de Neuroanatomie Appliquée et ThéoriqueInstitute of Life Course & Medical Sciences, University of LiverpoolInstitut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona Edifici ICTA-ICP, c/ Columnes s/n, Campus de la UAB, 08193 Cerdanyola del Vallès.Institut Pasteur, Université Paris Cité, Unité de Neuroanatomie Appliquée et ThéoriqueDepartment of Biomedical Imaging and Image-guided Therapy, Computational Imaging Research Lab, Medical University of ViennaDepartment of Biomedical Imaging and Image-guided Therapy, Computational Imaging Research Lab, Medical University of ViennaDepartment of Biomedical Imaging and Image-guided Therapy, Computational Imaging Research Lab, Medical University of ViennaAbstract Studies in comparative neuroanatomy and of the fossil record demonstrate the influence of socio-ecological niches on the morphology of the cerebral cortex, but have led to oftentimes conflicting theories about its evolution. Here, we study the relationship between the shape of the cerebral cortex and the topography of its function. We establish a joint geometric representation of the cerebral cortices of ninety species of extant Euarchontoglires, including commonly used experimental model organisms. We show that variability in surface geometry relates to species’ ecology and behaviour, independent of overall brain size. Notably, ancestral shape reconstruction of the cortical surface and its change during evolution enables us to trace the evolutionary history of localised cortical expansions, modal segregation of brain function, and their association to behaviour and cognition. We find that individual cortical regions follow different sequences of area increase during evolutionary adaptations to dynamic socio-ecological niches. Anatomical correlates of this sequence of events are still observable in extant species, and relate to their current behaviour and ecology. We decompose the deep evolutionary history of the shape of the human cortical surface into spatially and temporally conscribed components with highly interpretable functional associations, highlighting the importance of considering the evolutionary history of cortical regions when studying their anatomy and function.https://doi.org/10.1038/s41467-023-37574-x
spellingShingle Ernst Schwartz
Karl-Heinz Nenning
Katja Heuer
Nathan Jeffery
Ornella C. Bertrand
Roberto Toro
Gregor Kasprian
Daniela Prayer
Georg Langs
Evolution of cortical geometry and its link to function, behaviour and ecology
Nature Communications
title Evolution of cortical geometry and its link to function, behaviour and ecology
title_full Evolution of cortical geometry and its link to function, behaviour and ecology
title_fullStr Evolution of cortical geometry and its link to function, behaviour and ecology
title_full_unstemmed Evolution of cortical geometry and its link to function, behaviour and ecology
title_short Evolution of cortical geometry and its link to function, behaviour and ecology
title_sort evolution of cortical geometry and its link to function behaviour and ecology
url https://doi.org/10.1038/s41467-023-37574-x
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