Hierarchical organization of human cortical networks in health and schizophrenia.
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.
Bassett
Danielle S
DS
Clinical Brain Disorders Branch, Genes Cognition and Psychosis Program, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland 20892, USA.
Bullmore
Edward
E
Verchinski
Beth A
BA
Mattay
Venkata S
VS
Weinberger
Daniel R
DR
Meyer-Lindenberg
Andreas
A
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*
Cereb Cortex. 1999 Jun;9(4):366-78
10426416
Am J Psychiatry. 2004 Feb;161(2):322-31
14754782
Biol Psychiatry. 2005 Dec 15;58(12):921-9
16043134
Psychol Med. 1997 Nov;27(6):1257-66
9403897
Proc Natl Acad Sci U S A. 2006 Mar 21;103(12):4723-8
16537428
Phys Rev E Stat Nonlin Soft Matter Phys. 2003 Feb;67(2 Pt 2):026112
12636753
Schizophr Res. 1998 Mar 10;30(2):115-25
9549774
Phys Rev Lett. 2001 Nov 5;87(19):198701
11690461
Am J Psychiatry. 1992 Jul;149(7):890-7
1609867
PLoS One. 2007 Oct 17;2(10):e1049
17940613
Schizophr Bull. 2007 Jul;33(4):921-31
17548845
Nature. 1998 Jun 4;393(6684):440-2
9623998
Behav Brain Res. 2002 Sep 20;135(1-2):69-74
12356436
Arch Gen Psychiatry. 2005 Apr;62(4):379-86
15809405
Nature. 1990 Feb 15;343(6259):644-7
2304536
Neuroscientist. 2006 Dec;12(6):512-23
17079517
Nat Neurosci. 2005 Jun;8(6):828-34
15880108
Neurosci Res. 2005 Mar;51(3):309-15
15710495
Philos Trans R Soc Lond B Biol Sci. 2000 Jan 29;355(1393):91-110
10703046
Am J Psychiatry. 2001 Nov;158(11):1809-17
11691686
Proc Natl Acad Sci U S A. 2004 Mar 16;101(11):3747-52
15007165
Cereb Cortex. 2005 Sep;15(9):1332-42
15635061
Neuron. 2002 Apr 25;34(3):341-7
11988166
Neuroimage. 2001 Jul;14(1 Pt 1):21-36
11525331
Schizophr Res. 1997 Dec 19;28(2-3):143-56
9468349
Phys Rev E Stat Nonlin Soft Matter Phys. 2004 Sep;70(3 Pt 2):037101
15524673
Cereb Cortex. 2008 Oct;18(10):2374-81
18267952
Philos Trans R Soc Lond B Biol Sci. 2000 Jan 29;355(1393):111-26
10703047
Arch Gen Psychiatry. 2002 Jun;59(6):553-8
12044198
Phys Rev Lett. 2002 Nov 11;89(20):208701
12443515
Biol Psychiatry. 2001 Dec 1;50(11):825-44
11743939
Biophys J. 2007 Jul 1;93(1):225-31
17172302
Neuroimage. 2006 Jul 1;31(3):993-1003
16624590
Cereb Cortex. 2004 May;14(5):586-93
15054074
Proc Natl Acad Sci U S A. 2006 Dec 19;103(51):19518-23
17159150
J Neurosci. 2006 Jan 4;26(1):63-72
16399673
Brain. 1998 Jun;121 ( Pt 6):1013-52
9648540
J Neurosci. 2004 Nov 10;24(45):10099-102
15537879
J Neurosci. 2005 Sep 7;25(36):8303-10
16148238
Cereb Cortex. 2000 Feb;10(2):127-41
10667981
Am J Psychiatry. 2000 Aug;157(8):1309-16
10910796
Proc Biol Sci. 2006 Feb 22;273(1585):503-11
16615219
Nature. 1992 Jul 9;358(6382):152-5
1614547
PLoS Comput Biol. 2007 Feb 2;3(2):e17
17274684
J Neurocytol. 1993 Sep;22(9):689-95
7903688
Am J Psychiatry. 2005 Dec;162(12):2233-45
16330585
Phys Rev Lett. 2004 Apr 30;92(17):178702
15169201
Cereb Cortex. 2007 Oct;17(10):2407-19
17204824
Neural Comput. 2004 Oct;16(10):2067-78
15333207
J Psychiatr Res. 2007 Jan-Feb;41(1-2):15-30
16023676
Am J Psychiatry. 2008 Aug;165(8):1015-23
18381902
Schizophr Res. 1988 Jan-Feb;1(1):47-53
3154506