Cross-species functional alignment reveals evolutionary hierarchy within the connectome.


Journal

NeuroImage
ISSN: 1095-9572
Titre abrégé: Neuroimage
Pays: United States
ID NLM: 9215515

Informations de publication

Date de publication:
12 2020
Historique:
received: 20 04 2020
revised: 04 08 2020
accepted: 31 08 2020
pubmed: 12 9 2020
medline: 9 3 2021
entrez: 11 9 2020
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 32916286
pii: S1053-8119(20)30832-6
doi: 10.1016/j.neuroimage.2020.117346
pmc: PMC7871099
mid: NIHMS1659542
pii:
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

117346

Subventions

Organisme : NIMH NIH HHS
ID : R01 MH111439
Pays : United States
Organisme : Biotechnology and Biological Sciences Research Council
Pays : United Kingdom
Organisme : Medical Research Council
Pays : United Kingdom
Organisme : Austrian Science Fund FWF
ID : I 3925
Pays : Austria
Organisme : NIMH NIH HHS
ID : P50 MH109429
Pays : United States
Organisme : NIMH NIH HHS
ID : RF1 MH117428
Pays : United States
Organisme : NIBIB NIH HHS
ID : P41 EB015902
Pays : United States
Organisme : NIMH NIH HHS
ID : R24 MH114806
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom

Informations de copyright

Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.

Références

Proc Natl Acad Sci U S A. 2016 Nov 1;113(44):12574-12579
pubmed: 27791099
Ann N Y Acad Sci. 2014 May;1316:29-52
pubmed: 24502540
Cereb Cortex. 2015 Oct;25(10):3654-72
pubmed: 25249407
Nat Commun. 2014 Jul 22;5:4469
pubmed: 25047085
Nat Neurosci. 2018 Sep;21(9):1251-1259
pubmed: 30082915
Neuron. 2010 Feb 25;65(4):550-62
pubmed: 20188659
Proc Natl Acad Sci U S A. 2015 Jul 28;112(30):9454-9
pubmed: 26170314
Neuroimage. 2016 Jan 15;125:311-331
pubmed: 26515902
Neuron. 2015 Aug 5;87(3):657-70
pubmed: 26212711
Neuroimage. 2020 Jul 15;215:116800
pubmed: 32276072
Proc Natl Acad Sci U S A. 2008 Dec 9;105(49):19514-9
pubmed: 19033466
Proc Natl Acad Sci U S A. 2019 Apr 2;116(14):7101-7106
pubmed: 30886094
Neuron. 2018 Oct 10;100(1):61-74.e2
pubmed: 30269990
Elife. 2020 Mar 23;9:
pubmed: 32202497
Prog Brain Res. 2012;195:91-102
pubmed: 22230624
PLoS Biol. 2019 May 10;17(5):e3000259
pubmed: 31075099
Nature. 2000 Jun 29;405(6790):1055-8
pubmed: 10890446
Front Neuroanat. 2012 Jul 26;6:29
pubmed: 22855672
J Neurosci. 2016 Jun 22;36(25):6758-70
pubmed: 27335406
Neuroimage. 2012 Jul 16;61(4):1428-43
pubmed: 22446492
J Neurosci. 2015 May 20;35(20):7695-714
pubmed: 25995460
Trends Neurosci. 2016 Dec;39(12):813-829
pubmed: 27884462
Cell Rep. 2018 Apr 10;23(2):429-441
pubmed: 29642002
PLoS Biol. 2019 May 20;17(5):e3000284
pubmed: 31107870
Brain Behav Evol. 2014;84(1):19-30
pubmed: 25139259
Cereb Cortex. 1991 Jan-Feb;1(1):1-47
pubmed: 1822724
Cereb Cortex. 2015 Oct;25(10):3278-89
pubmed: 24904067
Cereb Cortex. 2019 Aug 14;29(9):3891-3901
pubmed: 30357354
J Neurosci. 2013 Feb 20;33(8):3259-75
pubmed: 23426655
J Neurosci. 2013 Jul 24;33(30):12255-74
pubmed: 23884933
Nat Methods. 2012 Feb 05;9(3):277-82
pubmed: 22306809
Elife. 2015 Jan 15;4:
pubmed: 25590651
Cereb Cortex. 2017 Jun 1;27(6):3471-3484
pubmed: 28419201
Cortex. 2019 Sep;118:275-291
pubmed: 31235272
Proc Natl Acad Sci U S A. 2018 Nov 27;115(48):12295-12300
pubmed: 30420501
Elife. 2018 May 11;7:
pubmed: 29749930
J Comp Neurol. 2000 Dec 4;428(1):112-37
pubmed: 11058227
Neuroscientist. 2013 Feb;19(1):76-87
pubmed: 22785104
Proc Natl Acad Sci U S A. 2010 Jul 20;107(29):13135-40
pubmed: 20624964
Neuron. 2017 Jul 19;95(2):457-471.e5
pubmed: 28728026
Trends Cogn Sci. 2014 Jan;18(1):46-55
pubmed: 24501779
Neuroimage. 2018 Apr 15;170:83-94
pubmed: 28666880
Braz J Med Biol Res. 2002 Dec;35(12):1485-98
pubmed: 12436190
Sci Adv. 2019 Jan 09;5(1):eaat7854
pubmed: 30662942
Cortex. 2019 Sep;118:38-50
pubmed: 30808550
PLoS Comput Biol. 2014 Mar 27;10(3):e1003529
pubmed: 24676052
J Neurosci. 2011 Aug 10;31(32):11597-616
pubmed: 21832190
Proc Natl Acad Sci U S A. 2017 Nov 28;114(48):12821-12826
pubmed: 29078345
Curr Opin Neurobiol. 1994 Apr;4(2):157-65
pubmed: 8038571
Neuroimage. 2013 Oct 15;80:105-24
pubmed: 23668970
Neuroimage. 2017 Aug 1;156:456-465
pubmed: 28416451
Proc Biol Sci. 2013 Mar 27;280(1759):20130269
pubmed: 23536600
Cell. 2017 Jul 13;170(2):226-247
pubmed: 28708995
Soc Cogn Affect Neurosci. 2017 Jul 1;12(7):1047-1062
pubmed: 28402561
Cereb Cortex. 2017 Feb 1;27(2):981-997
pubmed: 28184415
Nat Commun. 2019 Jul 31;10(1):3437
pubmed: 31366944
Ann N Y Acad Sci. 2009 Mar;1156:44-67
pubmed: 19338502
Neuroimage. 2013 Apr 1;69:120-5
pubmed: 23261640
Proc Natl Acad Sci U S A. 2018 Feb 13;115(7):E1598-E1607
pubmed: 29382744
Neuron. 2007 Oct 25;56(2):209-25
pubmed: 17964241
Neuron. 2014 Feb 5;81(3):700-13
pubmed: 24485097
Brain Behav Evol. 2018;91(3):158-169
pubmed: 30099464
Neuroimage. 2019 May 1;191:441-456
pubmed: 30802514
J Neurosci. 2011 Mar 16;31(11):4087-100
pubmed: 21411650
J Comp Neurol. 1991 Aug 22;310(4):475-506
pubmed: 1939733
Brain Struct Funct. 2016 Nov;221(8):4059-4071
pubmed: 26627483
Nat Commun. 2015 Nov 17;6:8901
pubmed: 26573340
Neuroimage. 2014 Oct 15;100:414-26
pubmed: 24939340
Brain. 1998 Jun;121 ( Pt 6):1013-52
pubmed: 9648540
J Neurosci Methods. 2016 Aug 30;269:46-60
pubmed: 27189889
Proc Natl Acad Sci U S A. 2018 May 29;115(22):E5183-E5192
pubmed: 29739891
J Neurosci. 2013 Sep 18;33(38):15120-5
pubmed: 24048842
J Neurosci. 2011 Sep 7;31(36):12954-62
pubmed: 21900574
Cereb Cortex. 2018 Nov 1;28(11):3829-3841
pubmed: 29045561
Biol Psychiatry Cogn Neurosci Neuroimaging. 2019 Jun;4(6):543-553
pubmed: 31072758
Trends Cogn Sci. 2013 Feb;17(2):89-98
pubmed: 23313359
Cereb Cortex. 2012 Oct;22(10):2227-40
pubmed: 22052704
Commun Biol. 2020 Apr 2;3(1):156
pubmed: 32242085
Nat Commun. 2019 Apr 29;10(1):1976
pubmed: 31036823
J Comp Neurol. 2000 Sep 25;425(3):447-70
pubmed: 10972944
Proc Natl Acad Sci U S A. 2014 Dec 30;111(52):18745-50
pubmed: 25512496
Phys Life Rev. 2019 Dec;31:233-239
pubmed: 30738760
Cereb Cortex. 2014 Jan;24(1):17-36
pubmed: 23010748
Nat Commun. 2015 Jul 14;6:7717
pubmed: 26171589
Neuroimage. 2018 May 1;171:393-401
pubmed: 29339310
Cortex. 2019 Sep;118:51-64
pubmed: 30979504
PLoS Biol. 2017 May 4;15(5):e2001379
pubmed: 28472038
Cereb Cortex. 2017 Aug 1;27(8):3890-3905
pubmed: 27405331
Nat Rev Neurosci. 2017 Nov;18(11):645-657
pubmed: 28951610
Trends Cogn Sci. 2018 Nov;22(11):1026-1037
pubmed: 30241910
Adv Neural Inf Process Syst. 2010;1:1225-1233
pubmed: 24808719
F1000Prime Rep. 2013 Apr 02;5:10
pubmed: 23585928
Trends Cogn Sci. 2013 Dec;17(12):648-65
pubmed: 24210963
Nature. 2016 Aug 11;536(7615):171-178
pubmed: 27437579
Neuroimage. 2019 Feb 1;186:487-496
pubmed: 30447291
Nat Neurosci. 2011 Apr;14(4):423-5
pubmed: 21378972
Proc Natl Acad Sci U S A. 2018 Sep 11;115(37):9318-9323
pubmed: 30150393
Neuron. 2007 Oct 25;56(2):201-8
pubmed: 17964240
J Neurophysiol. 2011 Sep;106(3):1125-65
pubmed: 21653723
PLoS Biol. 2014 Sep 02;12(9):e1001940
pubmed: 25180883
Front Neurosci. 2014 Oct 06;8:298
pubmed: 25339857

Auteurs

Ting Xu (T)

Center for the Developing Brain, Child Mind Institute, New York, NY, USA. Electronic address: ting.xu@childmind.org.

Karl-Heinz Nenning (KH)

Computational Imaging Research Lab, Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Austria.

Ernst Schwartz (E)

Computational Imaging Research Lab, Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Austria.

Seok-Jun Hong (SJ)

Center for the Developing Brain, Child Mind Institute, New York, NY, USA.

Joshua T Vogelstein (JT)

Department of Biomedical Engineering, Institute for Computational Medicine, Kavli Neuroscience Discovery Institute, Johns Hopkins University, MD, USA.

Alexandros Goulas (A)

Institute of Computational Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg University, Hamburg, Germany.

Damien A Fair (DA)

Advanced Imaging Research Center, Oregon Health & Science University, Portland, OR, USA.

Charles E Schroeder (CE)

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.

Daniel S Margulies (DS)

Centre National de la Recherche Scientifique (CNRS) UMR 7225, Frontlab, Institut du Cerveau et de la Moelle Epinière, Paris, France.

Jonny Smallwood (J)

Department of Psychology, Queen's University, Kingston, Ontario, Canada; Psychology Department, University of York, York, UK.

Michael P Milham (MP)

Center for the Developing Brain, Child Mind Institute, New York, NY, USA; Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute, Orangeburg, NY, USA.

Georg Langs (G)

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.

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