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

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

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.

Original languageEnglish (US)
Article number117346
JournalNeuroImage
Volume223
DOIs
StatePublished - Dec 2020

Bibliographical note

Funding Information:
This work was supported by gifts from Joseph P. Healey, Phyllis Green, and Randolph Cowen to the Child Mind Institute and the NIH BRAIN Initiative R01-MH111439 to C.E.S and M.P.M.; R24 MH11480602 to M.P.M.; NIH NIBIB NAC P41EB015902 , Austrian Science Fund FWF I2714- B31 , and the EU H2020 765148 TRABIT to G.L.; NSF EEC-1707298 and Microsoft Research support to J.T.V.; ERC Consolidator award WANDERINGMINDS 646927 to J.S.; CNRS PICS Grant 288256 to D.S.M.; R01 MH1112439 , and P50 MH109429 to C.E.S.; and Oesterreichische Nationalbank support ( OeNB16725 ) to K-H.N.; We would also like to thank the investigative teams from Oxford (J. Sallet, R.B. Mars, M.F.S. Rushworth), Newcastle (J. Nacef, C.I. Petkov, F. Balezeau, T.D. Griffiths, C. Poirier, A. Thiele, M. Ortiz, M. Schmid, D. Hunter) and UC-Davis (M. Baxter, P. Croxson, J. Morrison), as well as the funding agencies that make their work possible (Oxford: Wellcome Trust, Royal Society, Medical Research Council, UK Biotechnology Biological Sciences Research Council; Newcaste: National Center for 3Rs, NIH, Wellcome Trust, UK Biotechnology Biological Sciences Research Council; UC-Davis: NIA).

Keywords

  • Cross-species alignment
  • Default mode network
  • Evolution
  • Hierarchy
  • Joint embedding

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