Structural connectome and connectivity lateralization of the multimodal vestibular cortical network.
Adult
Connectome
/ methods
Female
Functional Laterality
/ physiology
Humans
Magnetic Resonance Imaging
/ methods
Male
Motion Perception
/ physiology
Neural Pathways
/ anatomy & histology
Parietal Lobe
/ anatomy & histology
Somatosensory Cortex
/ anatomy & histology
Vestibule, Labyrinth
/ anatomy & histology
HCP
Insula
MRI
OP2
PIC
PIVC
VPS
Journal
NeuroImage
ISSN: 1095-9572
Titre abrégé: Neuroimage
Pays: United States
ID NLM: 9215515
Informations de publication
Date de publication:
15 11 2020
15 11 2020
Historique:
received:
24
05
2020
revised:
28
07
2020
accepted:
05
08
2020
pubmed:
18
8
2020
medline:
30
3
2021
entrez:
18
8
2020
Statut:
ppublish
Résumé
Unlike other sensory systems, the structural connectivity patterns of the human vestibular cortex remain a matter of debate. Based on their functional properties and hypothesized centrality within the vestibular network, the 'core' cortical regions of this network are thought to be areas in the posterior peri-sylvian cortex, in particular the retro-insula (previously named the posterior insular cortex-PIC), and the subregion OP2 of the parietal operculum. To study the vestibular network, structural connectivity matrices from n=974 healthy individuals drawn from the public Human Connectome Project (HCP) repository were estimated using multi-shell diffusion-weighted data followed by probabilistic tractography and spherical-deconvolution informed filtering of tractograms in combination with subject-specific grey-matter parcellations. Weighted graph-theoretical measures, modularity, and 'hubness' of the multimodal vestibular network were then estimated, and a structural lateralization index was defined in order to assess the difference in fiber density of homonym regions in the right and left hemisphere. Differences in connectivity patterns between OP2 and PIC were also estimated. We found that the bilateral intraparietal sulcus, PIC, and to a lesser degree OP2, are key 'hub' regions within the multimodal vestibular network. PIC and OP2 structural connectivity patterns were lateralized to the left hemisphere, while structural connectivity patterns of the posterior peri-sylvian supramarginal and superior temporal gyri were lateralized to the right hemisphere. These lateralization patterns were independent of handedness. We also found that the structural connectivity pattern of PIC is consistent with a key role of PIC in visuo-vestibular processing and that the structural connectivity pattern of OP2 is consistent with integration of mainly vestibular somato-sensory and motor information. These results suggest an analogy between PIC and the simian visual posterior sylvian (VPS) area and OP2 and the simian parieto-insular vestibular cortex (PIVC). Overall, these findings may provide novel insights to the current models of vestibular function, as well as to the understanding of the complexity and lateralized signs of vestibular syndromes.
Identifiants
pubmed: 32798675
pii: S1053-8119(20)30733-3
doi: 10.1016/j.neuroimage.2020.117247
pmc: PMC7779422
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
117247Subventions
Organisme : NIMH NIH HHS
ID : U54 MH091657
Pays : United States
Organisme : Medical Research Council
ID : MR/P01271X/1
Pays : United Kingdom
Informations de copyright
Copyright © 2020 The Authors. Published by Elsevier Inc. All rights reserved.
Références
J Neurophysiol. 2014 Nov 15;112(10):2481-91
pubmed: 25185806
Brain. 2006 Feb;129(Pt 2):293-305
pubmed: 16371409
Neuroimage. 2012 Mar;60(1):162-9
pubmed: 22209784
PLoS One. 2009 May 29;4(5):e5737
pubmed: 19478939
Front Integr Neurosci. 2014 Jun 02;8:47
pubmed: 24917796
J Neurosci. 2010 Feb 24;30(8):3022-42
pubmed: 20181599
Neuropsychologia. 1971 Mar;9(1):97-113
pubmed: 5146491
Front Integr Neurosci. 2013 Dec 26;7:101
pubmed: 24421761
J Comp Neurol. 1994 Jan 15;339(3):421-37
pubmed: 7510732
Front Hum Neurosci. 2012 Apr 10;6:78
pubmed: 22514528
Neuroimage. 2018 Sep;178:224-237
pubmed: 29787866
Science. 2005 Apr 15;308(5720):416-9
pubmed: 15831760
Neuroimage. 2002 Nov;17(3):1384-93
pubmed: 12414278
Neuroimage. 2008 Oct 1;42(4):1508-18
pubmed: 18644454
Cortex. 2016 May;78:55-69
pubmed: 27007069
Front Psychol. 2014 Feb 18;5:82
pubmed: 24600414
Neuropsychologia. 2003;41(4):504-15
pubmed: 12559166
Neuroimage. 2014 Feb 15;87:18-31
pubmed: 24246491
Cereb Cortex. 2006 Feb;16(2):254-67
pubmed: 15888607
Stroke. 2012 Jun;43(6):1654-6
pubmed: 22382159
Curr Biol. 2014 Aug 18;24(16):1866-73
pubmed: 25065755
Neuroscience. 2016 Jun 14;325:10-9
pubmed: 27001175
J Neurol. 2015 Jan;262(1):214-5
pubmed: 25346066
Neurology. 2012 Mar 6;78(10):728-35
pubmed: 22357719
Trends Neurosci. 1998 Jun;21(6):254-9
pubmed: 9641538
Nat Commun. 2019 Mar 29;10(1):1417
pubmed: 30926845
Neuroimage. 2013 Oct 15;80:125-43
pubmed: 23702418
Arch Clin Neuropsychol. 1986;1(4):357-69
pubmed: 14591416
Hum Brain Mapp. 2017 Feb;38(2):715-726
pubmed: 27677756
J Stat Mech. 2005 Feb 1;2005(P02001):nihpa35573
pubmed: 18159217
Curr Opin Neurol. 2018 Feb;31(1):96-104
pubmed: 29189299
Biomed Res Int. 2014;2014:615854
pubmed: 25061610
Neuropsychologia. 2019 Apr;127:113-122
pubmed: 30831119
Cortex. 2015 Aug;69:60-7
pubmed: 25989442
NMR Biomed. 2019 Apr;32(4):e3785
pubmed: 28945294
Neuroimage. 2015 Jan 1;104:221-30
pubmed: 25315789
Neuroimage. 2005 Jul 1;26(3):721-32
pubmed: 15955481
Brain Connect. 2018 May;8(4):235-244
pubmed: 29571264
Neuropsychologia. 2007 Jan 28;45(2):209-28
pubmed: 16949111
Med Hypotheses. 1999 Jun;52(6):497-503
pubmed: 10459828
J Neurophysiol. 2016 Aug 1;116(2):263-71
pubmed: 27075535
Neuroimage. 2013 May 1;71:114-24
pubmed: 23321153
J Comp Neurol. 1993 Jun 1;332(1):89-104
pubmed: 7685782
Nat Rev Neurosci. 2011 Apr;12(4):217-30
pubmed: 21415848
Neuropsychologia. 2012 May;50(6):1010-7
pubmed: 21756924
Science. 1998 May 8;280(5365):921-4
pubmed: 9572740
Neuroimage. 2016 Nov 15;142:512-521
pubmed: 27395391
J Comp Neurol. 1992 Dec 15;326(3):375-401
pubmed: 1281845
Neuroimage. 2012 Aug 15;62(2):782-90
pubmed: 21979382
Exp Brain Res. 1994;99(1):164-9
pubmed: 7925790
Neuroimage. 2019 Nov 15;202:116137
pubmed: 31473352
J Comp Neurol. 1992 Dec 15;326(3):423-41
pubmed: 1469120
Annu Rev Neurosci. 2008;31:389-410
pubmed: 18558861
Neuroimage. 2012 Mar;60(1):409-18
pubmed: 22245639
Front Neurol. 2017 Oct 25;8:552
pubmed: 29118736
J Neurophysiol. 2018 Sep 1;120(3):1438-1450
pubmed: 29995604
Brain Res Cogn Brain Res. 2001 Dec;12(3):441-9
pubmed: 11689304
Hum Brain Mapp. 2018 Mar;39(3):1449-1466
pubmed: 29266522
Neuroimage. 2013 Feb 15;67:298-312
pubmed: 23238430
Neuroimage. 2010 Sep;52(3):1059-69
pubmed: 19819337
Front Neurol. 2019 Aug 13;10:874
pubmed: 31456740
Exp Brain Res. 1999 Aug;127(4):355-70
pubmed: 10480271
Brain Struct Funct. 2016 Apr;221(3):1291-308
pubmed: 25552315
J Neurosci. 2011 Aug 17;31(33):12036-52
pubmed: 21849564
Brain. 2005 Sep;128(Pt 9):2052-67
pubmed: 15947061
Brain Imaging Behav. 2019 Jun;13(3):798-809
pubmed: 29860587
Ann Phys Rehabil Med. 2017 Jun;60(3):124-129
pubmed: 26874577
Neuroimage. 2011 Feb 1;54(3):2033-44
pubmed: 20851191
Magn Reson Med. 2013 Jun;69(6):1534-40
pubmed: 23625329
Cereb Cortex. 2010 Aug;20(8):1964-73
pubmed: 20034998
Cereb Cortex. 2003 Sep;13(9):994-1007
pubmed: 12902399
J Neurol. 2017 Oct;264(Suppl 1):55-62
pubmed: 28315957
Neuroimage. 2007 May 1;35(4):1459-72
pubmed: 17379540
Neuroimage. 2008 Jan 1;39(1):19-31
pubmed: 17919936
Hum Brain Mapp. 2020 Jan;41(1):185-193
pubmed: 31520516
J Neurophysiol. 2014 Jun 15;111(12):2445-64
pubmed: 24671533
Neuropsychologia. 1989;27(5):729-35
pubmed: 2739895
Neuroimage. 2017 Jan 15;145(Pt A):118-129
pubmed: 27666386
Neuroscience. 2012 Jun 14;212:159-79
pubmed: 22516007
Neuroimage. 2016 Feb 15;127:287-297
pubmed: 26687667
Ann N Y Acad Sci. 2011 Sep;1233:177-86
pubmed: 21950991
J Neurol. 2012 Feb;259(2):277-83
pubmed: 21830093
Eur J Neurosci. 2009 Aug;30(4):703-13
pubmed: 19674088
Neuroimage. 2005 May 1;25(4):1325-35
pubmed: 15850749
Brain Res Rev. 2011 Jun 24;67(1-2):119-46
pubmed: 21223979
Neuroimage. 2014 Dec;103:411-426
pubmed: 25109526
Front Integr Neurosci. 2014 Jul 04;8:53
pubmed: 25071481
Sci Rep. 2012;2:336
pubmed: 22468223
J Neurosci. 2011 Aug 10;31(32):11617-27
pubmed: 21832191
Brain. 2011 Oct;134(Pt 10):3059-70
pubmed: 21624927
Nature. 2016 Aug 11;536(7615):171-178
pubmed: 27437579
Exp Brain Res. 1996 Dec;112(3):523-6
pubmed: 9007554
Brain. 2016 Feb;139(Pt 2):392-403
pubmed: 26719385
Cereb Cortex. 1999 Oct-Nov;9(7):705-11
pubmed: 10554993
Cereb Cortex. 2016 Aug;26(8):3508-26
pubmed: 27230218
Ann Neurol. 2014 Oct;76(4):609-19
pubmed: 25142204
Phys Rev Lett. 2001 Nov 5;87(19):198701
pubmed: 11690461