title: Hierarchical organization of human cortical networks in health and schizophrenia.
abstract: The complex organization of connectivity in the human brain is incompletely understood. Recently, topological measures based on graph theory have provided a new approach to quantify large-scale cortical networks. These methods have been applied to anatomical connectivity data on nonhuman species, and cortical networks have been shown to have small-world topology, associated with high local and global efficiency of information transfer. Anatomical networks derived from cortical thickness measurements have shown the same organizational properties of the healthy human brain, consistent with similar results reported in functional networks derived from resting state functional magnetic resonance imaging (MRI) and magnetoencephalographic data. Here we show, using anatomical networks derived from analysis of inter-regional covariation of gray matter volume in MRI data on 259 healthy volunteers, that classical divisions of cortex (multimodal, unimodal, and transmodal) have some distinct topological attributes. Although all cortical divisions shared nonrandom properties of small-worldness and efficient wiring (short mean Euclidean distance between connected regions), the multimodal network had a hierarchical organization, dominated by frontal hubs with low clustering, whereas the transmodal network was assortative. Moreover, in a sample of 203 people with schizophrenia, multimodal network organization was abnormal, as indicated by reduced hierarchy, the loss of frontal and the emergence of nonfrontal hubs, and increased connection distance. We propose that the topological differences between divisions of normal cortex may represent the outcome of different growth processes for multimodal and transmodal networks and that neurodevelopmental abnormalities in schizophrenia specifically impact multimodal cortical organization.
authors.affiliation: Clinical Brain Disorders Branch, Genes Cognition and Psychosis Program, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland 20892, USA.
authors.forename: Danielle S
authors.initials: DS
authors.lastname: Bassett
authors.forename: Edward
authors.initials: E
authors.lastname: Bullmore
authors.forename: Beth A
authors.initials: BA
authors.lastname: Verchinski
authors.forename: Venkata S
authors.initials: VS
authors.lastname: Mattay
authors.forename: Daniel R
authors.initials: DR
authors.lastname: Weinberger
authors.forename: Andreas
authors.initials: A
authors.lastname: Meyer-Lindenberg
mesh_terms: D000328:Adult; D001931:Brain Mapping; D016022:Case-Control Studies; D002540:Cerebral Cortex / Q000473:pathology*; D005260:Female; D006801:Humans; D007091:Image Processing, Computer-Assisted; D008279:Magnetic Resonance Imaging / Q000379:methods; D008297:Male; D008875:Middle Aged; D008959:Models, Neurological; D009434:Neural Pathways / Q000473:pathology*; D012559:Schizophrenia / Q000473:pathology*
references.citation: Cereb Cortex. 1999 Jun;9(4):366-78
references.pmid: 10426416
references.citation: Am J Psychiatry. 2004 Feb;161(2):322-31
references.pmid: 14754782
references.citation: Biol Psychiatry. 2005 Dec 15;58(12):921-9
references.pmid: 16043134
references.citation: Psychol Med. 1997 Nov;27(6):1257-66
references.pmid: 9403897
references.citation: Proc Natl Acad Sci U S A. 2006 Mar 21;103(12):4723-8
references.pmid: 16537428
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2003 Feb;67(2 Pt 2):026112
references.pmid: 12636753
references.citation: Schizophr Res. 1998 Mar 10;30(2):115-25
references.pmid: 9549774
references.citation: Phys Rev Lett. 2001 Nov 5;87(19):198701
references.pmid: 11690461
references.citation: Am J Psychiatry. 1992 Jul;149(7):890-7
references.pmid: 1609867
references.citation: PLoS One. 2007 Oct 17;2(10):e1049
references.pmid: 17940613
references.citation: Schizophr Bull. 2007 Jul;33(4):921-31
references.pmid: 17548845
references.citation: Nature. 1998 Jun 4;393(6684):440-2
references.pmid: 9623998
references.citation: Behav Brain Res. 2002 Sep 20;135(1-2):69-74
references.pmid: 12356436
references.citation: Arch Gen Psychiatry. 2005 Apr;62(4):379-86
references.pmid: 15809405
references.citation: Nature. 1990 Feb 15;343(6259):644-7
references.pmid: 2304536
references.citation: Neuroscientist. 2006 Dec;12(6):512-23
references.pmid: 17079517
references.citation: Nat Neurosci. 2005 Jun;8(6):828-34
references.pmid: 15880108
references.citation: Neurosci Res. 2005 Mar;51(3):309-15
references.pmid: 15710495
references.citation: Philos Trans R Soc Lond B Biol Sci. 2000 Jan 29;355(1393):91-110
references.pmid: 10703046
references.citation: Am J Psychiatry. 2001 Nov;158(11):1809-17
references.pmid: 11691686
references.citation: Proc Natl Acad Sci U S A. 2004 Mar 16;101(11):3747-52
references.pmid: 15007165
references.citation: Cereb Cortex. 2005 Sep;15(9):1332-42
references.pmid: 15635061
references.citation: Neuron. 2002 Apr 25;34(3):341-7
references.pmid: 11988166
references.citation: Neuroimage. 2001 Jul;14(1 Pt 1):21-36
references.pmid: 11525331
references.citation: Schizophr Res. 1997 Dec 19;28(2-3):143-56
references.pmid: 9468349
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2004 Sep;70(3 Pt 2):037101
references.pmid: 15524673
references.citation: Cereb Cortex. 2008 Oct;18(10):2374-81
references.pmid: 18267952
references.citation: Philos Trans R Soc Lond B Biol Sci. 2000 Jan 29;355(1393):111-26
references.pmid: 10703047
references.citation: Arch Gen Psychiatry. 2002 Jun;59(6):553-8
references.pmid: 12044198
references.citation: Phys Rev Lett. 2002 Nov 11;89(20):208701
references.pmid: 12443515
references.citation: Biol Psychiatry. 2001 Dec 1;50(11):825-44
references.pmid: 11743939
references.citation: Biophys J. 2007 Jul 1;93(1):225-31
references.pmid: 17172302
references.citation: Neuroimage. 2006 Jul 1;31(3):993-1003
references.pmid: 16624590
references.citation: Cereb Cortex. 2004 May;14(5):586-93
references.pmid: 15054074
references.citation: Proc Natl Acad Sci U S A. 2006 Dec 19;103(51):19518-23
references.pmid: 17159150
references.citation: J Neurosci. 2006 Jan 4;26(1):63-72
references.pmid: 16399673
references.citation: Brain. 1998 Jun;121 ( Pt 6):1013-52
references.pmid: 9648540
references.citation: J Neurosci. 2004 Nov 10;24(45):10099-102
references.pmid: 15537879
references.citation: J Neurosci. 2005 Sep 7;25(36):8303-10
references.pmid: 16148238
references.citation: Cereb Cortex. 2000 Feb;10(2):127-41
references.pmid: 10667981
references.citation: Am J Psychiatry. 2000 Aug;157(8):1309-16
references.pmid: 10910796
references.citation: Proc Biol Sci. 2006 Feb 22;273(1585):503-11
references.pmid: 16615219
references.citation: Nature. 1992 Jul 9;358(6382):152-5
references.pmid: 1614547
references.citation: PLoS Comput Biol. 2007 Feb 2;3(2):e17
references.pmid: 17274684
references.citation: J Neurocytol. 1993 Sep;22(9):689-95
references.pmid: 7903688
references.citation: Am J Psychiatry. 2005 Dec;162(12):2233-45
references.pmid: 16330585
references.citation: Phys Rev Lett. 2004 Apr 30;92(17):178702
references.pmid: 15169201
references.citation: Cereb Cortex. 2007 Oct;17(10):2407-19
references.pmid: 17204824
references.citation: Neural Comput. 2004 Oct;16(10):2067-78
references.pmid: 15333207
references.citation: J Psychiatr Res. 2007 Jan-Feb;41(1-2):15-30
references.pmid: 16023676
references.citation: Am J Psychiatry. 2008 Aug;165(8):1015-23
references.pmid: 18381902
references.citation: Schizophr Res. 1988 Jan-Feb;1(1):47-53
references.pmid: 3154506