Cross-species functional alignment reveals evolutionary hierarchy within the connectome

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

doi:10.1016/j.neuroimage.2020.117346

Cross-species functional alignment reveals evolutionary hierarchy within the connectome

Neuroimage. 2020 Dec:223:117346. doi: 10.1016/j.neuroimage.2020.117346. Epub 2020 Sep 9.

Authors

Affiliations

¹ Center for the Developing Brain, Child Mind Institute, New York, NY, USA. Electronic address: ting.xu@childmind.org.
² Computational Imaging Research Lab, Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Austria.
³ Center for the Developing Brain, Child Mind Institute, New York, NY, USA.
⁴ Department of Biomedical Engineering, Institute for Computational Medicine, Kavli Neuroscience Discovery Institute, Johns Hopkins University, MD, USA.
⁵ Institute of Computational Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg University, Hamburg, Germany.
⁶ Advanced Imaging Research Center, Oregon Health & Science University, Portland, OR, USA.
⁷ Center 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, USA.
⁸ Centre National de la Recherche Scientifique (CNRS) UMR 7225, Frontlab, Institut du Cerveau et de la Moelle Epinière, Paris, France.
⁹ Department of Psychology, Queen's University, Kingston, Ontario, Canada; Psychology Department, University of York, York, UK.
¹⁰ Center for the Developing Brain, Child Mind Institute, New York, NY, USA; Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute, Orangeburg, NY, USA.
¹¹ Computational 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, USA.

Abstract

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.

Keywords: Cross-species alignment; Default mode network; Evolution; Hierarchy; Joint embedding.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Biological Evolution*
Cerebral Cortex / physiology*
Connectome / methods*
Humans
Macaca mulatta
Magnetic Resonance Imaging*
Neural Pathways / physiology
Species Specificity

Abstract

Publication types

MeSH terms

Grants and funding