Abnormal topological organization of structural brain networks in schizophrenia

Schizophrenia Research

Volumn 141, Issue 2-3, 2012, Pages 109-118

  Zhang, Yuanchao ^a,b   Lin, Lei ^b,f   Lin, Ching Po ^c   Zhou, Yuan ^d   Chou, Kun Hsien ^c   Lo, Chun Yi ^c   Su, Tung Ping ^c,e   Jiang, Tianzi ^a,b,g  

^a UNIVERSITY OF ELECTRONIC SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b INSTITUTE OF AUTOMATION   (China)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

^d INSTITUTE OF PSYCHOLOGY   (China)

^e TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^f ZHEJIANG UNIVERSITY   (China)

^g UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Betweenness centrality; Cortical thickness; Schizophrenia; Structural network; Topological organization

Indexed keywords

ADULT; AGED; ANTERIOR COMMISSURE; ARTICLE; BRAIN COMMISSURE; BRAIN CORTEX; CONTROLLED STUDY; DISEASE DURATION; FEMALE; HANDEDNESS; HUMAN; LIMBIC CORTEX; MAJOR CLINICAL STUDY; MALE; MEMBRANE STRUCTURE; NERVE CELL NETWORK; NEUROANATOMY; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; ONSET AGE; PRIORITY JOURNAL; SCHIZOPHRENIA;

ADULT; BRAIN; BRAIN MAPPING; DIAGNOSTIC AND STATISTICAL MANUAL OF MENTAL DISORDERS; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE NET; NEURAL PATHWAYS; PSYCHIATRIC STATUS RATING SCALES; SCHIZOPHRENIA; YOUNG ADULT;

EID: 84866945886     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2012.08.021     Document Type: Article

References (73)

1. Achard S., Bullmore E. Efficiency and cost of economical brain functional networks. PLoS Comput. Biol. 2007, 3(2):e17.
2. Achard S., Salvador R., Whitcher B., Suckling J., Bullmore E. A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J. Neurosci. 2006, 26(1):63-72.
3. Andreasen N.C., O'Leary D.S., Flaum M., Nopoulos P., Watkins G.L., Boles Ponto L.L., Hichwa R.D. Hypofrontality in schizophrenia: distributed dysfunctional circuits in neuroleptic-naive patients. Lancet 1997, 349(9067):1730-1734.
4. Andreasen N.C., Nopoulos P., O'Leary D.S., Miller D.D., Wassink T., Flaum M. Defining the phenotype of schizophrenia: cognitive dysmetria and its neural mechanisms. Biol. Psychiatry 1999, 46(7):908-920.
5. Andrews T.J., Halpern S.D., Purves D. Correlated size variations in human visual cortex, lateral geniculate nucleus, and optic tract. J. Neurosci. 1997, 17(8):2859-2868.
6. Bassett D.S., Bullmore E. Small-world brain networks. Neuroscientist 2006, 12(6):512-523.
7. Bassett D.S., Bullmore E., Verchinski B.A., Mattay V.S., Weinberger D.R., Meyer-Lindenberg A. Hierarchical organization of human cortical networks in health and schizophrenia. J. Neurosci. 2008, 28(37):9239-9248.
8. Bluhm R.L., Miller J., Lanius R.A., Osuch E.A., Boksman K., Neufeld R.W., Theberge J., Schaefer B., Williamson P. Spontaneous low-frequency fluctuations in the BOLD signal in schizophrenic patients: anomalies in the default network. Schizophr. Bull. 2007, 33(4):1004-1012.
9. Boksman K., Theberge J., Williamson P., Drost D.J., Malla A., Densmore M., Takhar J., Pavlosky W., Menon R.S., Neufeld R.W. A 4.0-T fMRI study of brain connectivity during word fluency in first-episode schizophrenia. Schizophr. Res. 2005, 75(2-3):247-263.
10. Bullmore E.T., Frangou S., Murray R.M. The dysplastic net hypothesis: an integration of developmental and dysconnectivity theories of schizophrenia. Schizophr. Res. 1997, 28(2-3):143-156.
11. Bullmore E.T., Woodruff P.W., Wright I.C., Rabe-Hesketh S., Howard R.J., Shuriquie N., Murray R.M. Does dysplasia cause anatomical dysconnectivity in schizophrenia?. Schizophr. Res. 1998, 30(2):127-135.
12. Bullmore E.T., Suckling J., Overmeyer S., Rabe-Hesketh S., Taylor E., Brammer M.J. Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans. Med. Imaging 1999, 18(1):32-42.
13. Chen Z.J., He Y., Rosa-Neto P., Germann J., Evans A.C. Revealing modular architecture of human brain structural networks by using cortical thickness from MRI. Cereb. Cortex 2008, 18(10):2374-2381.
14. Cheung V., Cheung C., McAlonan G.M., Deng Y., Wong J.G., Yip L., Tai K.S., Khong P.L., Sham P., Chua S.E. A diffusion tensor imaging study of structural dysconnectivity in never-medicated, first-episode schizophrenia. Psychol. Med. 2008, 38(6):877-885.
15. Dale A.M., Fischl B., Sereno M.I. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 1999, 9(2):179-194.
16. Fischl B., Dale A.M. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc. Natl. Acad. Sci. U. S. A. 2000, 97(20):11050-11055.
17. Fischl B., Sereno M.I., Tootell R.B., Dale A.M. High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum. Brain Mapp. 1999, 8(4):272-284.
18. Fischl B., Sereno M.I., Dale A.M. Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 1999, 9(2):195-207.
19. Fischl B., Liu A., Dale A.M. Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans. Med. Imaging 2001, 20(1):70-80.
20. Foucher J.R., Vidailhet P., Chanraud S., Gounot D., Grucker D., Pins D., Damsa C., Danion J.M. Functional integration in schizophrenia: too little or too much? Preliminary results on fMRI data. Neuroimage 2005, 26(2):374-388.
21. Freeman L.C. A set of measures of centrality based on betweenness. Sociometry 1977, 35-41.
22. Friston K.J. The disconnection hypothesis. Schizophr. Res. 1998, 30(2):115-125.
23. Friston K.J. Schizophrenia and the disconnection hypothesis. Acta Psychiatr. Scand. Suppl. 1999, 395:68-79.
24. Friston K. Disconnection and cognitive dysmetria in schizophrenia. Am. J. Psychiatry 2005, 162(3):429-432.
25. Garrity A.G., Pearlson G.D., McKiernan K., Lloyd D., Kiehl K.A., Calhoun V.D. Aberrant "default mode" functional connectivity in schizophrenia. Am. J. Psychiatry 2007, 164(3):450-457.
26. Genovese C.R., Lazar N.A., Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 2002, 15(4):870-878.
27. Goldman A.L., Pezawas L., Mattay V.S., Fischl B., Verchinski B.A., Chen Q., Weinberger D.R., Meyer-Lindenberg A. Widespread reductions of cortical thickness in schizophrenia and spectrum disorders and evidence of heritability. Arch. Gen. Psychiatry 2009, 66(5):467-477.
28. Gong G., He Y., Concha L., Lebel C., Gross D.W., Evans A.C., Beaulieu C. Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. Cereb. Cortex 2009, 19(3):524-536.
29. Han X., Jovicich J., Salat D., van der Kouwe A., Quinn B., Czanner S., Busa E., Pacheco J., Albert M., Killiany R., Maguire P., Rosas D., Makris N., Dale A., Dickerson B., Fischl B. Reliability of MRI-derived measurements of human cerebral cortical thickness: the effects of field strength, scanner upgrade and manufacturer. Neuroimage 2006, 32(1):180-194.
30. He Y., Chen Z.J., Evans A.C. Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cereb. Cortex 2007, 17(10):2407-2419.
31. He Y., Chen Z., Evans A. Structural insights into aberrant topological patterns of large-scale cortical networks in Alzheimer's disease. J. Neurosci. 2008, 28(18):4756-4766.
32. Hill K., Mann L., Laws K.R., Stephenson C.M., Nimmo-Smith I., McKenna P.J. Hypofrontality in schizophrenia: a meta-analysis of functional imaging studies. Acta Psychiatr. Scand. 2004, 110(4):243-256.
33. Hirayasu Y. Brain imaging in schizophrenia. Neuropathology 2007, 27(6):601-603.
34. Honea R., Crow T.J., Passingham D., Mackay C.E. Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. Am. J. Psychiatry 2005, 162(12):2233-2245.
35. Honey G.D., Bullmore E.T., Sharma T. De-coupling of cognitive performance and cerebral functional response during working memory in schizophrenia. Schizophr. Res. 2002, 53(1-2):45-56.
36. Honey G.D., Pomarol-Clotet E., Corlett P.R., Honey R.A., McKenna P.J., Bullmore E.T., Fletcher P.C. Functional dysconnectivity in schizophrenia associated with attentional modulation of motor function. Brain 2005, 128(Pt 11):2597-2611.
37. Humphries M.D., Gurney K., Prescott T.J. The brainstem reticular formation is a small-world, not scale-free, network. Proc. Biol. Sci. 2006, 273(1585):503-511.
38. Johansen-Berg H., Behrens T.E.J. Diffusion MRI: From Quantitative Measurement to In-vivo Neuroanatomy 2009, Academic Press.
39. Kay S.R., Fiszbein A., Opler L.A. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 1987, 13(2):261-276.
40. Kim J.J., Ho Seok J., Park H.J., Soo Lee D., Chul Lee M., Kwon J.S. Functional disconnection of the semantic networks in schizophrenia. Neuroreport 2005, 16(4):355-359.
41. Kuperberg G.R., Broome M.R., McGuire P.K., David A.S., Eddy M., Ozawa F., Goff D., West W.C., Williams S.C., van der Kouwe A.J., Salat D.H., Dale A.M., Fischl B. Regionally localized thinning of the cerebral cortex in schizophrenia. Arch. Gen. Psychiatry 2003, 60(9):878-888.
42. Latora V., Marchiori M. Efficient behavior of small-world networks. Phys. Rev. Lett. 2001, 87(19):198701.
43. Lawrie S.M., Buechel C., Whalley H.C., Frith C.D., Friston K.J., Johnstone E.C. Reduced frontotemporal functional connectivity in schizophrenia associated with auditory hallucinations. Biol. Psychiatry 2002, 51(12):1008-1011.
44. Lerch J.P., Worsley K., Shaw W.P., Greenstein D.K., Lenroot R.K., Giedd J., Evans A.C. Mapping anatomical correlations across cerebral cortex (MACACC) using cortical thickness from MRI. Neuroimage 2006, 31(3):993-1003.
45. Liang M., Zhou Y., Jiang T., Liu Z., Tian L., Liu H., Hao Y. Widespread functional disconnectivity in schizophrenia with resting-state functional magnetic resonance imaging. Neuroreport 2006, 17(2):209-213.
46. Liu Y., Liang M., Zhou Y., He Y., Hao Y., Song M., Yu C., Liu H., Liu Z., Jiang T. Disrupted small-world networks in schizophrenia. Brain 2008, 131(Pt 4):945-961.
47. Maslov S., Sneppen K. Specificity and stability in topology of protein networks. Science 2002, 296(5569):910-913.
48. Mechelli A., Friston K.J., Frackowiak R.S., Price C.J. Structural covariance in the human cortex. J. Neurosci. 2005, 25(36):8303-8310.
49. Mesulam M.M. From sensation to cognition. Brain 1998, 121(Pt 6):1013-1052.
50. Micheloyannis S., Pachou E., Stam C.J., Breakspear M., Bitsios P., Vourkas M., Erimaki S., Zervakis M. Small-world networks and disturbed functional connectivity in schizophrenia. Schizophr. Res. 2006, 87(1-3):60-66.
51. Mitelman S.A., Buchsbaum M.S., Brickman A.M., Shihabuddin L. Cortical intercorrelations of frontal area volumes in schizophrenia. Neuroimage 2005, 27(4):753-770.
52. Mitelman S.A., Byne W., Kemether E.M., Hazlett E.A., Buchsbaum M.S. Metabolic disconnection between the mediodorsal nucleus of the thalamus and cortical Brodmann's areas of the left hemisphere in schizophrenia. Am. J. Psychiatry 2005, 162(9):1733-1735.
53. Mitelman S.A., Shihabuddin L., Brickman A.M., Buchsbaum M.S. Cortical intercorrelations of temporal area volumes in schizophrenia. Schizophr. Res. 2005, 76(2-3):207-229.
54. Narr K.L., Bilder R.M., Toga A.W., Woods R.P., Rex D.E., Szeszko P.R., Robinson D., Sevy S., Gunduz-Bruce H., Wang Y.P., DeLuca H., Thompson P.M. Mapping cortical thickness and gray matter concentration in first episode schizophrenia. Cereb. Cortex 2005, 15(6):708-719.
55. Salvador R., Suckling J., Coleman M.R., Pickard J.D., Menon D., Bullmore E. Neurophysiological architecture of functional magnetic resonance images of human brain. Cereb. Cortex 2005, 15(9):1332-1342.
56. Seiferth N.Y., Pauly K., Kellermann T., Shah N.J., Ott G., Herpertz-Dahlmann B., Kircher T., Schneider F., Habel U. Neuronal correlates of facial emotion discrimination in early onset schizophrenia. Neuropsychopharmacology 2009, 34(2):477-487.
57. Sporns O., Zwi J.D. The small world of the cerebral cortex. Neuroinformatics 2004, 2(2):145-162.
58. Sporns O., Tononi G., Edelman G.M. Theoretical neuroanatomy: relating anatomical and functional connectivity in graphs and cortical connection matrices. Cereb. Cortex 2000, 10(2):127-141.
59. Stephan K.E., Baldeweg T., Friston K.J. Synaptic plasticity and dysconnection in schizophrenia. Biol. Psychiatry 2006, 59(10):929-939.
60. Tan H.Y., Sust S., Buckholtz J.W., Mattay V.S., Meyer-Lindenberg A., Egan M.F., Weinberger D.R., Callicott J.H. Dysfunctional prefrontal regional specialization and compensation in schizophrenia. Am. J. Psychiatry 2006, 163(11):1969-1977.
61. Taylor S.F., Kang J., Brege I.S., Tso I.F., Hosanagar A., Johnson T.D. Meta-analysis of functional neuroimaging studies of emotion perception and experience in schizophrenia. Biol. Psychiatry 2012, 71(2):136-145.
62. Tian L., Wang J., Yan C., He Y. Hemisphere- and gender-related differences in small-world brain networks: a resting-state functional MRI study. Neuroimage 2011, 54(1):191-202.
63. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15(1):273-289.
64. van den Heuvel M.P., Mandl R.C., Stam C.J., Kahn R.S., Hulshoff Pol H.E. Aberrant frontal and temporal complex network structure in schizophrenia: a graph theoretical analysis. J. Neurosci. 2010, 30(47):15915-15926.
65. Watts D.J., Strogatz S.H. Collective dynamics of 'small-world' networks. Nature 1998, 393(6684):440-442.
66. White T., Andreasen N.C., Nopoulos P., Magnotta V. Gyrification abnormalities in childhood- and adolescent-onset schizophrenia. Biol. Psychiatry 2003, 54(4):418-426.
67. Whitfield-Gabrieli S., Thermenos H.W., Milanovic S., Tsuang M.T., Faraone S.V., McCarley R.W., Shenton M.E., Green A.I., Nieto-Castanon A., LaViolette P., Wojcik J., Gabrieli J.D., Seidman L.J. Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(4):1279-1284.
68. Woodruff P.W., Wright I.C., Shuriquie N., Russouw H., Rushe T., Howard R.J., Graves M., Bullmore E.T., Murray R.M. Structural brain abnormalities in male schizophrenics reflect fronto-temporal dissociation. Psychol. Med. 1997, 27(6):1257-1266.
69. Wright I.C., Rabe-Hesketh S., Woodruff P.W., David A.S., Murray R.M., Bullmore E.T. Meta-analysis of regional brain volumes in schizophrenia. Am. J. Psychiatry 2000, 157(1):16-25.
70. Yao Z., Zhang Y., Lin L., Zhou Y., Xu C., Jiang T. Abnormal cortical networks in mild cognitive impairment and Alzheimer's disease. PLoS Comput. Biol. 2010, 6(11):e1001006.
71. Zalesky A., Fornito A., Seal M.L., Cocchi L., Westin C.F., Bullmore E.T., Egan G.F., Pantelis C. Disrupted axonal fiber connectivity in schizophrenia. Biol. Psychiatry 2011, 69(1):80-89.
72. Zhou Y., Liang M., Tian L., Wang K., Hao Y., Liu H., Liu Z., Jiang T. Functional disintegration in paranoid schizophrenia using resting-state fMRI. Schizophr. Res. 2007, 97(1-3):194-205.
73. Zhou Y., Shu N., Liu Y., Song M., Hao Y., Liu H., Yu C., Liu Z., Jiang T. Altered resting-state functional connectivity and anatomical connectivity of hippocampus in schizophrenia. Schizophr. Res. 2008, 100(1-3):120-132.