Systematic cortical thickness and curvature patterns in primates.
Cortical folding
Cortical thickness
Curvature
Primates
Shape index
Sulcal depth
Journal
NeuroImage
ISSN: 1095-9572
Titre abrégé: Neuroimage
Pays: United States
ID NLM: 9215515
Informations de publication
Date de publication:
09 2023
09 2023
Historique:
received:
29
01
2023
revised:
11
07
2023
accepted:
17
07
2023
medline:
14
8
2023
pubmed:
30
7
2023
entrez:
29
7
2023
Statut:
ppublish
Résumé
Humans are known to have significant and consistent differences in thickness throughout the cortex, with thick outer gyral folds and thin inner sulcal folds. Our previous work has suggested a mechanical basis for this thickness pattern, with the forces generated during cortical folding leading to thick gyri and thin sulci, and shown that cortical thickness varies along a gyral-sulcal spectrum in humans. While other primate species are expected to exhibit similar patterns of cortical thickness, it is currently unknown how these patterns scale across different sizes, forms, and foldedness. Among primates, brains vary enormously from roughly the size of a grape to the size of a grapefruit, and from nearly smooth to dramatically folded; of these, human brains are the largest and most folded. These variations in size and form make comparative neuroanatomy a rich resource for investigating common trends that transcend differences between species. In this study, we examine 12 primate species in order to cover a wide range of sizes and forms, and investigate the scaling of their cortical thickness relative to the surface geometry. The 12 species were selected due to the public availability of either reconstructed surfaces and/or population templates. After obtaining or reconstructing 3D surfaces from publicly available neuroimaging data, we used our surface-based computational pipeline (https://github.com/mholla/curveball) to analyze patterns of cortical thickness and folding with respect to size (total surface area), geometry (i.e. curvature, shape, and sulcal depth), and foldedness (gyrification). In all 12 species, we found consistent cortical thickness variations along a gyral-sulcal spectrum, with convex shapes thicker than concave shapes and saddle shapes in between. Furthermore, we saw an increasing thickness difference between gyri and sulci as brain size increases. Our results suggest a systematic folding mechanism relating local cortical thickness to geometry. Finally, all of our reconstructed surfaces and morphometry data are available for future research in comparative neuroanatomy.
Identifiants
pubmed: 37516374
pii: S1053-8119(23)00434-2
doi: 10.1016/j.neuroimage.2023.120283
pmc: PMC10443624
mid: NIHMS1924378
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
120283Subventions
Organisme : NIMH NIH HHS
ID : K23 MH087770
Pays : United States
Organisme : NIMH NIH HHS
ID : R03 MH096321
Pays : United States
Organisme : NINDS NIH HHS
ID : R24 NS092988
Pays : United States
Informations de copyright
Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of competing interest The authors declare that they have no conflict of interest.
Références
J Hirnforsch. 1999;39(3):335-47
pubmed: 10536866
Biophys J. 2009 Feb 18;96(4):1661-70
pubmed: 19217881
Comput Biomed Res. 1996 Jun;29(3):162-73
pubmed: 8812068
Front Aging Neurosci. 2021 Feb 03;13:625931
pubmed: 33613271
Cereb Cortex. 2013 May;23(5):1208-17
pubmed: 22586139
Neuroimage. 2016 Jan 15;125:780-790
pubmed: 26550941
Neuroimage. 2021 Aug 1;236:118082
pubmed: 33882349
Elife. 2020 Nov 23;9:
pubmed: 33226338
Neurobiol Aging. 2012 Jan;33(1):200.e23-31
pubmed: 20801549
Neuroinformatics. 2011 Dec;9(4):381-400
pubmed: 21373993
Neuroimage. 2021 Feb 15;227:117671
pubmed: 33359348
Neuroimage. 2020 Jul 15;215:116800
pubmed: 32276072
Brain Struct Funct. 2021 Nov;226(8):2497-2509
pubmed: 34264391
Cortex. 2019 Sep;118:315-326
pubmed: 30503630
Proc Biol Sci. 2015 Oct 7;282(1816):20151853
pubmed: 26400745
J Neurosci Methods. 2011 Oct 30;202(1):17-27
pubmed: 21889536
Commun Biol. 2019 May 20;2:191
pubmed: 31123715
J Biomech Eng. 2010 Jul;132(7):071013
pubmed: 20590291
Neuron. 2018 Oct 10;100(1):61-74.e2
pubmed: 30269990
Dev Biol. 1984 Apr;102(2):379-89
pubmed: 6706005
Cereb Cortex. 2016 Jan;26(1):257-267
pubmed: 25246511
Med Image Anal. 2009 Apr;13(2):269-85
pubmed: 19068276
Brain Behav Evol. 2014;84(1):19-30
pubmed: 25139259
Science. 1975 Jul 4;189(4196):18-21
pubmed: 1135626
Dev Neurobiol. 2010 Feb 15;70(3):135-49
pubmed: 19950193
Cereb Cortex. 2020 Oct 07;:
pubmed: 33026423
Neuroimage. 2008 May 1;40(4):1701-10
pubmed: 18325790
Eur J Neurosci. 2007 May;25(9):2705-12
pubmed: 17459107
Brain Struct Funct. 2013 Nov;218(6):1451-62
pubmed: 23135358
Brain Topogr. 2021 Jul;34(4):430-441
pubmed: 34008053
J Neurosci Methods. 2014 Jun 15;230:37-50
pubmed: 24785589
Trends Neurosci. 2013 May;36(5):275-84
pubmed: 23415112
Cortex. 2019 Sep;118:275-291
pubmed: 31235272
Brain Behav Evol. 1985;27(1):28-40
pubmed: 3836731
IEEE Trans Med Imaging. 2001 Jan;20(1):45-57
pubmed: 11293691
Neuroimage. 2014 Oct 1;99:166-79
pubmed: 24879923
Brain Behav Evol. 1988;32(1):17-26
pubmed: 3056571
Hum Brain Mapp. 2022 Apr 15;43(6):2064-2084
pubmed: 35098606
Proc Natl Acad Sci U S A. 2019 Jul 23;116(30):15253-15261
pubmed: 31285343
Phys Rev Lett. 2018 Nov 30;121(22):228002
pubmed: 30547630
Anat Embryol (Berl). 2005 Dec;210(5-6):411-7
pubmed: 16175385
Proc Natl Acad Sci U S A. 2019 Dec 26;116(52):26173-26180
pubmed: 31871175
Neuron. 2013 Oct 30;80(3):633-47
pubmed: 24183016
Brain Behav Evol. 1989;34(3):143-50
pubmed: 2512000
Cereb Cortex. 2020 Apr 14;30(4):2434-2451
pubmed: 31808811
PLoS Biol. 2019 Apr 18;17(4):e3000042
pubmed: 30998673
Ann Biomed Eng. 2015 Jul;43(7):1640-53
pubmed: 25824370
Prog Neurobiol. 1989;32(2):137-58
pubmed: 2645619
Cereb Cortex. 2022 Jun 16;32(13):2831-2842
pubmed: 34849623
Neuroimage. 2014 Nov 1;101:59-67
pubmed: 24983715
Neuroimage Clin. 2021;30:102600
pubmed: 33741307
Science. 2015 Jul 3;349(6243):74-7
pubmed: 26138976
Sci Adv. 2022 Mar 11;8(10):eabi5209
pubmed: 35275722
Prog Brain Res. 2012;195:373-90
pubmed: 22230637
Front Comput Neurosci. 2017 Aug 15;11:76
pubmed: 28860983
Cereb Cortex. 2011 Jul;21(7):1674-94
pubmed: 21127018
Sci Rep. 2015 Sep 25;5:14477
pubmed: 26404042
Brain Struct Funct. 2015 Sep;220(5):2475-83
pubmed: 25511709
PLoS One. 2018 Jun 6;13(6):e0198335
pubmed: 29874295
Neuroimage. 2021 Feb 1;226:117620
pubmed: 33307224
PLoS One. 2013;8(2):e55977
pubmed: 23418488
Proc Natl Acad Sci U S A. 2000 Sep 26;97(20):11050-5
pubmed: 10984517
Mol Psychiatry. 2014 Jun;19(6):659-67
pubmed: 23774715
Neurology. 2002 Mar 12;58(5):695-701
pubmed: 11889230
J Comput Neurosci. 2017 Jun;42(3):217-229
pubmed: 28271301
Neuroimage. 2016 Jul 15;135:163-76
pubmed: 27150231
Neuroimage. 2021 Feb 15;227:117622
pubmed: 33301944
Nat Rev Neurosci. 2019 Mar;20(3):161-176
pubmed: 30610227
Brain Behav Evol. 2018;91(3):158-169
pubmed: 30099464
Cereb Cortex. 2020 Jul 30;30(9):5014-5027
pubmed: 32377664
Proc Natl Acad Sci U S A. 2008 Aug 26;105(34):12593-8
pubmed: 18689685
Nature. 1997 Jan 23;385(6614):313-8
pubmed: 9002514
Front Neuroanat. 2014 Mar 27;8:15
pubmed: 24723857
Neuroimage. 2015 Aug 15;117:408-16
pubmed: 26037056
Neuroimage. 2011 Aug 1;57(3):856-65
pubmed: 21640841
Neuroimage. 2020 Mar;208:116450
pubmed: 31821869
Prog Brain Res. 1988;73:15-37
pubmed: 3047794
J Neurosci. 2018 Jan 24;38(4):776-783
pubmed: 29367288
J Neurosci. 2013 Mar 20;33(12):5241-8
pubmed: 23516289
Proc Mach Learn Res. 2022 Jul;172:508-520
pubmed: 37220495
Proc Natl Acad Sci U S A. 2018 May 29;115(22):E5183-E5192
pubmed: 29739891
Neuroimage. 2018 Apr 15;170:121-131
pubmed: 28461058
Brain Res. 2005 Aug 2;1052(1):71-81
pubmed: 16018988
Front Cell Neurosci. 2019 Aug 20;13:381
pubmed: 31481878
Magn Reson Imaging. 2009 Oct;27(8):1163-74
pubmed: 19249168
NMR Biomed. 1997 Jun-Aug;10(4-5):171-8
pubmed: 9430344
Cereb Cortex. 2008 Sep;18(9):2181-91
pubmed: 18234686
J Hum Evol. 1999 Aug;37(2):191-223
pubmed: 10444351
Cereb Cortex. 1995 Jan-Feb;5(1):56-63
pubmed: 7719130
Neuroimage. 2016 Jul 15;135:177-85
pubmed: 27153982
Hum Brain Mapp. 2017 Dec;38(12):5890-5904
pubmed: 28856766
Neuroimage. 2010 Nov 15;53(3):1103-8
pubmed: 20176115
Neuroimage. 2001 Feb;13(2):375-80
pubmed: 11162277
Biomech Model Mechanobiol. 2021 Apr;20(2):555-567
pubmed: 33151429
Proc Biol Sci. 2021 Feb 10;288(1944):20202987
pubmed: 33563125
Neuroimage. 2022 Apr 15;250:118965
pubmed: 35122965
Brain Behav Evol. 2011;77(2):65-6
pubmed: 21372555
Phys Biol. 2013 Feb;10(1):016005
pubmed: 23357794
Neuroimage. 2004 Oct;23(2):724-38
pubmed: 15488422
Lab Anim (NY). 2020 May;49(5):139-143
pubmed: 32332897
Neuroimage. 2021 Feb 1;226:117519
pubmed: 33227425
Neuron. 2020 Feb 19;105(4):600-603
pubmed: 32078795
Sci Rep. 2016 Nov 17;6:37272
pubmed: 27853245
Neuroimage. 2005 Jan 1;24(1):163-73
pubmed: 15588607
Proc Natl Acad Sci U S A. 2015 Dec 15;112(50):15462-7
pubmed: 26575625
Hum Brain Mapp. 2015 Dec;36(12):5183-95
pubmed: 26417847
Proc Natl Acad Sci U S A. 2014 Sep 2;111(35):12667-72
pubmed: 25136099
Neuroimage. 2006 Jul 1;31(3):1116-28
pubmed: 16545965
Cereb Cortex. 1994 Jan-Feb;4(1):78-96
pubmed: 8180493
Cereb Cortex. 2004 Jul;14(7):721-30
pubmed: 15054051
Neurobiol Aging. 2013 Oct;34(10):2248-60
pubmed: 23623601
Front Neuroanat. 2012 Feb 02;6:3
pubmed: 22347170
Neuroimage. 2021 Apr 1;229:117726
pubmed: 33484849
Neuron. 2022 Jan 5;110(1):16-20
pubmed: 34731649
Neuroimage. 2013 Jan 15;65:336-48
pubmed: 23041529
Cereb Cortex. 2005 Dec;15(12):1900-13
pubmed: 15758198
Neuroinformatics. 2014 Oct;12(4):535-42
pubmed: 24789776
Neuroimage. 2012 Aug 15;62(2):774-81
pubmed: 22248573
Proc Natl Acad Sci U S A. 2011 Aug 9;108(32):13029-34
pubmed: 21788499
Dement Geriatr Cogn Dis Extra. 2014 Jul 01;4(2):221-7
pubmed: 25177330
Anat Rec (Hoboken). 2012 Jul;295(7):1065-74
pubmed: 22593081
Nat Neurosci. 2016 Aug 26;19(9):1175-87
pubmed: 27571196
Cereb Cortex. 2012 Dec;22(12):2831-9
pubmed: 22190432