Cross-species functional alignment reveals evolutionary hierarchy within the connectome

Evolution provides an important window into how cortical organization shapes function and vice versa. The complex mosaic of changes in brain morphology and functional organization that have shaped the mammalian cortex during evolution, complicates attempts to chart cortical differences across specie...

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Main Authors: Ting Xu, Karl-Heinz Nenning, Ernst Schwartz, Seok-Jun Hong, Joshua T. Vogelstein, Alexandros Goulas, Damien A. Fair, Charles E. Schroeder, Daniel S. Margulies, Jonny Smallwood, Michael P. Milham, Georg Langs
Format: Article
Language:English
Published: Elsevier 2020-12-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811920308326
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spelling doaj-5ef264ee6f7e418ba8daa2c0327dc6062020-11-25T03:59:58ZengElsevierNeuroImage1095-95722020-12-01223117346Cross-species functional alignment reveals evolutionary hierarchy within the connectomeTing Xu0Karl-Heinz Nenning1Ernst Schwartz2Seok-Jun Hong3Joshua T. Vogelstein4Alexandros Goulas5Damien A. Fair6Charles E. Schroeder7Daniel S. Margulies8Jonny Smallwood9Michael P. Milham10Georg Langs11Center for the Developing Brain, Child Mind Institute, New York, NY, USA; Corresponding author.Computational Imaging Research Lab, Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, AustriaComputational Imaging Research Lab, Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, AustriaCenter for the Developing Brain, Child Mind Institute, New York, NY, USADepartment of Biomedical Engineering, Institute for Computational Medicine, Kavli Neuroscience Discovery Institute, Johns Hopkins University, MD, USAInstitute of Computational Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg University, Hamburg, GermanyAdvanced Imaging Research Center, Oregon Health & Science University, Portland, OR, USACenter for Biomedical Imaging and Neuromodulation, Nathan Kline Institute, Orangeburg, NY, USA; Departments of neurosurgery and Psychiatry, Columbia University College of Physicians and Surgeons, New York, NY, USACentre National de la Recherche Scientifique (CNRS) UMR 7225, Frontlab, Institut du Cerveau et de la Moelle Epinière, Paris, FranceDepartment of Psychology, Queen's University, Kingston, Ontario, Canada; Psychology Department, University of York, York, UKCenter for the Developing Brain, Child Mind Institute, New York, NY, USA; Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute, Orangeburg, NY, USAComputational Imaging Research Lab, Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Austria; Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, MA, USAEvolution provides an important window into how cortical organization shapes function and vice versa. The complex mosaic of changes in brain morphology and functional organization that have shaped the mammalian cortex during evolution, complicates attempts to chart cortical differences across species. It limits our ability to fully appreciate how evolution has shaped our brain, especially in systems associated with unique human cognitive capabilities that lack anatomical homologues in other species. Here, we develop a function-based method for cross-species alignment that enables the quantification of homologous regions between humans and rhesus macaques, even when their location is decoupled from anatomical landmarks. Critically, we find cross-species similarity in functional organization reflects a gradient of evolutionary change that decreases from unimodal systems and culminates with the most pronounced changes in posterior regions of the default mode network (angular gyrus, posterior cingulate and middle temporal cortices). Our findings suggest that the establishment of the default mode network, as the apex of a cognitive hierarchy, has changed in a complex manner during human evolution – even within subnetworks.http://www.sciencedirect.com/science/article/pii/S1053811920308326Cross-species alignmentJoint embeddingEvolutionHierarchyDefault mode network
collection DOAJ
language English
format Article
sources DOAJ
author Ting Xu
Karl-Heinz Nenning
Ernst Schwartz
Seok-Jun Hong
Joshua T. Vogelstein
Alexandros Goulas
Damien A. Fair
Charles E. Schroeder
Daniel S. Margulies
Jonny Smallwood
Michael P. Milham
Georg Langs
spellingShingle Ting Xu
Karl-Heinz Nenning
Ernst Schwartz
Seok-Jun Hong
Joshua T. Vogelstein
Alexandros Goulas
Damien A. Fair
Charles E. Schroeder
Daniel S. Margulies
Jonny Smallwood
Michael P. Milham
Georg Langs
Cross-species functional alignment reveals evolutionary hierarchy within the connectome
NeuroImage
Cross-species alignment
Joint embedding
Evolution
Hierarchy
Default mode network
author_facet Ting Xu
Karl-Heinz Nenning
Ernst Schwartz
Seok-Jun Hong
Joshua T. Vogelstein
Alexandros Goulas
Damien A. Fair
Charles E. Schroeder
Daniel S. Margulies
Jonny Smallwood
Michael P. Milham
Georg Langs
author_sort Ting Xu
title Cross-species functional alignment reveals evolutionary hierarchy within the connectome
title_short Cross-species functional alignment reveals evolutionary hierarchy within the connectome
title_full Cross-species functional alignment reveals evolutionary hierarchy within the connectome
title_fullStr Cross-species functional alignment reveals evolutionary hierarchy within the connectome
title_full_unstemmed Cross-species functional alignment reveals evolutionary hierarchy within the connectome
title_sort cross-species functional alignment reveals evolutionary hierarchy within the connectome
publisher Elsevier
series NeuroImage
issn 1095-9572
publishDate 2020-12-01
description Evolution provides an important window into how cortical organization shapes function and vice versa. The complex mosaic of changes in brain morphology and functional organization that have shaped the mammalian cortex during evolution, complicates attempts to chart cortical differences across species. It limits our ability to fully appreciate how evolution has shaped our brain, especially in systems associated with unique human cognitive capabilities that lack anatomical homologues in other species. Here, we develop a function-based method for cross-species alignment that enables the quantification of homologous regions between humans and rhesus macaques, even when their location is decoupled from anatomical landmarks. Critically, we find cross-species similarity in functional organization reflects a gradient of evolutionary change that decreases from unimodal systems and culminates with the most pronounced changes in posterior regions of the default mode network (angular gyrus, posterior cingulate and middle temporal cortices). Our findings suggest that the establishment of the default mode network, as the apex of a cognitive hierarchy, has changed in a complex manner during human evolution – even within subnetworks.
topic Cross-species alignment
Joint embedding
Evolution
Hierarchy
Default mode network
url http://www.sciencedirect.com/science/article/pii/S1053811920308326
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