Disrupted axonal fiber connectivity in schizophrenia

Biological Psychiatry

Volumn 69, Issue 1, 2011, Pages 80-89

  Zalesky, Andrew ^a   Fornito, Alex ^a,b   Seal, Marc L ^a   Cocchi, Luca ^a   Westin, Carl Fredrik ^c   Bullmore, Edward T ^b   Egan, Gary F ^a   Pantelis, Christos ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Axonal connectivity; Diffusion tensor imaging; Network; Schizophrenia; Tractography; White matter

Indexed keywords

OLANZAPINE; QUETIAPINE;

ADULT; AGE DISTRIBUTION; ANATOMICAL VARIATION; ARTICLE; BRAIN CORTEX; BRAIN MAPPING; CELL DISRUPTION; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; FEMALE; FRONTAL CORTEX; GENE CLUSTER; HUMAN; INTELLECT; MAJOR CLINICAL STUDY; MALE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE FIBER; OCCIPITAL LOBE; PARIETAL LOBE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SCHIZOPHRENIA; SEX DIFFERENCE; TEMPORAL LOBE; TRACTOGRAPHY; WHITE MATTER;

ADULT; BRAIN MAPPING; CEREBRAL CORTEX; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; NERVE FIBERS, MYELINATED; NERVE NET; NEURAL NETWORKS (COMPUTER); NEURAL PATHWAYS; SCHIZOPHRENIA;

EID: 78650031397     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2010.08.022     Document Type: Article

References (95)

1. A. Konrad, and G. Winterer Disturbed structural connectivity in schizophreniaprimary factor in pathology or epiphenomenon? Schizophr Bull 34 2008 72 92
2. D.S. Bassett, E. Bullmore, B.A. Verchinski, V.S. Mattay, D.R. Weinberger, and A. Meyer-Lindenberg Hierarchical organization of human cortical networks in health and schizophrenia J Neurosci 28 2008 9239 9248
3. Y. Li, Y. Liu, J. Li, W. Qin, L. Kuncheng, C. Yu, and T. Jiang Brain anatomical network and intelligence PLoS Comput Biol 5 2009 e1000395
4. Y. Liu, M. Liang, Y. Zhou, Y. He, Y. Hao, and M. Song Disrupted small-world networks in schizophrenia Brain 131 2008 945 961
5. M. Rubinov, S.A. Knock, C.J. Stam, S. Micheloyannis, A.W.F. Harris, L.M. Williams, and M. Breakspear Small-world properties of nonlinear brain activity in schizophrenia Hum Brain Mapp 30 2009 403 416
6. R.L. Bluhm, J. Miller, R.A. Lanius, E.A. Osuch, K. Boksman, and R.W. Neufeld Spontaneous low-frequency fluctuations in the BOLD signal in schizophrenic patients: anomalies in the default network Schizophr Bull 33 2007 1004 1012
7. J. Camchong, A.W. Macdonald, C. Bell, B.A. Mueller, and K.O. Lim Altered functional and anatomical connectivity in schizophrenia [published online ahead of print November 17] Schizophr Bull 2009 10.1093/schbul/sbp131
8. A.G. Garrity, G.D. Pearlson, K. McKiernan, D. Lloyd, K.A. Kiehl, and V.D. Calhoun Aberrant "default mode" functional connectivity in schizophrenia Am J Psychiatry 164 2007 450 457
9. N.C. Andreasen, S. Paradiso, and D.S. O'Leary "Cognitive dysmetria" as an integrative theory of schizophrenia: A dysfunction in cortical-subcortical-cerebellar circuitry? Schizophr Bull 24 1998 203 218
10. E.T. Bullmore, S. Frangou, and R.M. Murray The dysplastic net hypothesis: An integration of developmental and disconnectivity theories of schizophrenia Schizophr Res 28 1997 143 156
11. P. Fletcher, P.J. McKenna, K.J. Friston, C.D. Frith, and R.J. Dolan Abnormal cingulate modulation of fronto-temporal connectivity in schizophrenia Neuroimage 9 1999 337 342
12. K.J. Friston, and C.D. Frith Schizophrenia: A disconnection syndrome? Clin Neurosci 3 1995 89 97
13. K.J. Friston The disconnection hypothesis Schizophr Res 30 1998 115 125
14. K.J. Friston Dysfunctional connectivity in schizophrenia World Psychiatry 1 2002 66 71
15. R.E. Hoffman, M.S. Buchsbaum, M.D. Escobar, R.W. Makuch, K.H. Nuechterlein, and S.M. Guich EEG coherence of prefrontal areas in normal and schizophrenic males during perceptual activation J Neuropsychiatr Clin Neurosci 3 1991 169 175
16. A. Meyer-Lindenberg, J.P. Poline, P.D. Kohn, M.S. Holt, M.F. Egan, D.R. Weinberger, and K.F. Berman Evidence for abnormal cortical functional connectivity during working memory in schizophrenia Am J Psychiatry 158 2001 1809 1817
17. C. Pantelis, T.R. Barnes, and H.E. Nelson Is the concept of frontal-subcortical dementia relevant to schizophrenia? Br J Psychiatry 160 1992 442 460
18. K.E. Stephan, T. Baldeweg, and K.J. Friston Synaptic plasticity and dysconnection in schizophrenia Biol Psychiatry 59 2006 929 939
19. D.R. Weinberger A connectionist approach to the prefrontal cortex J Neuropsychiatr Clin Neurosci 5 1993 241 253
20. G. Winterer, R. Coppola, M.F. Egan, T.E. Goldberg, and D.R. Weinberger Functional and effective frontotemporal connectivity and genetic risk for schizophrenia Biol Psychiatry 54 2003 1181 1192
21. K.E. Stephan, K.J. Friston, and C.D. Frith Dysconnection in schizophrenia: From abnormal synaptic plasticity to failures of self-monitoring Schizophr Bull 35 2009 509 527
22. Y. Hakak, J.R. Walker, C. Li, W.H. Wong, K.L. Davis, and J.D. Buxbaum Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia Proc Natl Acad Sci U S A 98 2001 4746 4751
23. N.A. Uranova, M.F. Casanova, N.M. DeVaughn, D.D. Orlovskaya, and D.V. Denisov Ultrastructural pathology of neuronal connectivity in postmortem brains of schizophrenic patients Schizophr Res 22 1996 81 83
24. Z.J. Daskalakis, B.K. Christensen, P.B. Fitzgerald, and R. Chen Dysfunctional and neural plasticity in patients with schizophrenia Arch Gen Psychiatry 65 2008 378 385
25. T.H. McGlashan, and R.E. Hoffman Schizophrenia as a disorder of developmentally reduced synaptic connectivity Arch Gen Psychiatry 57 2000 637 648
26. P.J. Basser, J. Mattiello, and D. LeBihan Diffusion tensor MR imaging of the human brain Radiology 201 1996 637 648
27. J. Foong, M.R. Symms, G.J. Barker, M. Maier, F.G. Woermann, D.H. Miller, and M.A. Ron Neuropathological abnormalities in schizophrenia: Evidence from magnetization transfer imaging Brain 124 2001 882 892
28. R.A.A. Kanaan, J.S. Kim, W.E. Kaufmann, G.D. Pearlson, G.J. Barker, and P.K. McGuire Diffusion tensor imaging in schizophrenia Biol Psychiatry 58 2005 921 929
29. M. Kubicki, R.W. McCarley, and M.E. Shenton Evidence for white matter abnormalities in schizophrenia Curr Opin Psychiatry 18 2005 121 134
30. I. Feinberg Schizophrenia: Caused by a fault in programmed synaptic elimination during adolescence? J Psychiatr Res 17 1982 319 334
31. I. Ellison-Wright, D.C. Glahn, A.R. Laird, S.M. Thelen, and E. Bullmore The anatomy of first-episode and chronic schizophrenia: An anatomical likelihood estimation meta-analysis Am J Psychiatry 165 2008 1015 1023
32. G. Gong, Y. He, L. Concha, C. Lebel, D.W. Gross, A.C. Evans, and C. Beaulieu Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography Cereb Cortex 9 2009 524 536
33. G. Gong, P. Rosa-Neto, F. Carbonell, Z.J. Chen, Y. He, and A.C. Evans Age- and gender-related differences in the cortical anatomical network J Neurosci 29 2009 15684 15693
34. P. Hagmann, M. Kurant, X. Gigandet, P. Thiran, V.J. Wedeen, R. Meuli, and J.-P. Thiran Mapping human whole-brain structural networks with diffusion MRI PLoS ONE 2 2007 e597
35. P. Hagmann, L. Cammoun, X. Gigandent, R. Meuli, C.J. Honey, V.J. Wedeen, and O. Sporns Mapping the structural core of the human cerebral cortex PLoS Biol 6 2008 e159
36. Y. Iturria-Medina, R.C. Sotero, E.J. Canales-Rodrguez, Y. Alemn-Gmez, and L. Melie-Garca Studying the human brain anatomical network via diffusion-weighted MRI and graph theory Neuroimage 40 2008 1064 1076
37. A. Zalesky, and A. Fornito A DTI-derived measure of cortico-cortical connectivity IEEE Trans Med Imaging 28 2009 1023 1036
38. A. Zalesky, A. Fornito, I.H. Harding, L. Cocchi, M. Ycel, C. Pantelis, and E.T. Bullmore Whole-brain anatomical networks: Does the choice of nodes matter? Neuroimage 50 2010 970 983
39. E. Bullmore, and O. Sporns Complex brain networks: Graph theoretical analysis of structural and functional systems Nat Rev Neurosci 10 2009 186 198
40. D.J. Castle, A. Jablensky, J.J. McGrath, V. Carr, V. Morgan, and A. Waterreus The diagnostic interview for psychoses (DIP): Development, reliability and applications Psychol Med 36 2006 69 80
41. D. Wechsler Manual for the Wechsler Adult Intelligence Scale (WAIS-R) 1981 Psychological Corporation San Antonio, Texas
42. R. Salvador, A. Pena, D.K. Menon, T. Adrian Carpenter, J.D. Pickard, and E. Bullmore Formal characterization and extension of the linearized diffusion tensor model Hum Brain Mapp 24 2005 144 155
43. P.J. Basser Inferring microstructural features and the physiological state of tissues from diffusion-weighted images NMR Biomed 8 1995 333 344
44. P.J. Basser, S. Pajevic, C. Pierpaoli, J. Duda, and A. Aldroubi In vivo fiber tractography using DT-MRI data Magn Reson Med 44 2000 625 632
45. M. Catani, R.J. Howard, S. Pajevic, and D.K. Jones Virtual in vivo interactive dissection of white matter fasciculi in the human brain Neuroimage 17 2002 77 94
46. M. Catani Diffusion tensor magnetic resonance imaging tractography in cognitive disorders Curr Opin Neurol 19 2006 599 606
47. T.E. Conturo, N.F. Lori, T.S. Cull, E. Akbudak, A.Z. Snyder, and J.S. Shimony Tracking neuronal fiber pathways in the living human brain Proc Natl Acad Sci U S A 96 1999 10422 10427
48. C.J. Honey, O. Sporns, L. Cammoun, X. Gigandet, J.-P. Thiran, R. Meuli, and P. Hagmann Predicting human resting-state functional connectivity from structural connectivity Proc Natl Acad Sci U S A 106 2009 2035 2040
49. C.-H. Park, S.Y. Kim, Y.-H. Kim, and K. Kim Comparison of the small-world topology between anatomical and functional connectivity in the human brain Phys A 387 2008 5958 5962
50. P. Skudlarski, K. Jagnnathan, V.D. Calhoun, M. Hampson, B.A. Skudlarska, and G. Pearlson Measuring brain connectivity: Diffusion tensor imaging validates resting state temporal correlations Neuroimage 43 2008 554 561
51. Y. He, Z.J. Chen, and A.C. Evans Structural insights into aberrant topological patterns of large-scale cortical networks in Alzheimer's disease J Neurosci 28 2008 57564766
52. Y. He, A. Dagher, Z. Chen, A. Charil, A. Zijdenbos, K. Worsley, and A. Evans Impaired small-world efficiency in structural cortical networks in multiple sclerosis associated with white matter lesion load Brain 132 2009 3366 3379
53. M. Rubinov, and O. Sporns Complex network measures of brain connectivity: Uses and interpretations Neuroimage 52 2010 1059 1069
54. T.E. Nichols, and A.P. Holmes Nonparametric permutation tests for functional neuroimaging: A primer with examples Hum Brain Mapp 15 2001 1 25
55. C.R. Genovese, N.A. Lazar, and T. Nichols Thresholding of statistical maps in functional neuroimaging using the false discovery rate Neuroimage 15 2002 870 878
56. A. Zalesky, A. Fornito, and E.T. Bullmore Network-based statistic: Identifying differences in brain networks Neuroimage 53 2010 1197 1207
57. S. Achard, and E. Bullmore Efficiency and cost of economical brain functional networks PLoS Comput Biol 3 2007 e17
58. V. Latora, and M. Marchiori Efficient behavior of small-world networks Phys Rev Lett 87 2001 198 701
59. O. Sporns, G. Tononi, and G.M. Edelman Theoretical neuroanatomy: Relating anatomical and functional connectivity in graphs and cortical connection matrices Cereb Cortex 10 2000 127 141
60. N. Tzourio-Mazoyer, B. Landeau, D. Papathanassiou, F. Crivello, O. Etard, and N. Delcroix Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain Neuroimage 15 2002 273 289
61. M. Kubicki, C.F. Westin, P.G. Nestor, C.G. Wible, M. Frumin, and S.E. Maier Cingulate fasciculus integrity disruption in schizophrenia: A magnetic resonance diffusion tensor imaging study Biol Psychiatry 54 2003 1171 1180
62. M.L. Seal, M. Yucel, A. Fornito, S.J. Wood, B.J. Harrison, and M. Walterfang Abnormal white matter microstructure in schizophrenia: A voxelwise analysis of axial and radial diffusivity Schizophr Res 101 2008 106 110
63. Z. Sun, F. Wang, L. Cui, J. Breeze, X. Du, and X. Wang Abnormal anterior cingulum in patients with schizophrenia: A diffusion tensor imaging study Neuroreport 14 2003 1833 1836 (Pubitemid 37372613)
64. F. Wang, Z. Sun, L. Cui, X. Du, X. Wang, and H. Zhang Anterior cingulum abnormalities in male patients with schizophrenia determined through diffusion tensor imaging Am J Psychiatry 161 2004 573 575
65. V. Cheung, C. Cheung, G.M. McAlonan, Y. Deng, J.G. Wong, and L. Yip A diffusion tensor imaging study of structural disconnectivity in never-medicated, first-episode schizophrenia Psychol Med 38 2008 877 885
66. R. Gasparotti, P. Valsecchi, F. Carletti, A. Galluzzo, R. Liserre, B. Cesana, and E. Sacchetti Reduced fractional anisotropy of corpus callosum in first-contact, antipsychotic drug-naive patients with schizophrenia Schizophr Res 108 2009 41 48
67. M. Kubicki, M. Styner, S. Bouix, G. Gerig, D. Markant, and K. Smith Reduced interhemispheric connectivity in schizophrenia-tractography based segmentation of the corpus callosum Schizophr Res 106 2008 125 131
68. M. Walterfang, A. Yung, A.G. Wood, D.C. Reutens, L. Phillips, and S.J. Wood Corpus callosum shape alterations in individuals prior to the onset of psychosis Schizophr Res 103 2008 1 10
69. M. Walterfang, A.G. Wood, D.C. Reutens, S.J. Wood, J. Chen, and D. Velakoulis Morphology of the corpus callosum at different stages of schizophrenia: Cross-sectional study in first-episode and chronic illness Br J Psychiatry 192 2008 429 434
70. F.M. Benes Neurobiological investigations in cingulate cortex of schizophrenic brain Schizophr Bull 19 1993 537 549
71. A. Fornito, M. Yucel, B. Dean, S.J. Wood, and C. Pantelis Anatomical abnormalities of the anterior cingulate cortex in schizophrenia: Bridging the gap between neuroimaging and neuropathology Schizophr Bull 35 2009 973 993
72. D.C. Glahn, A.R. Laird, I. Ellison-Wright, S.M. Thelen, J.L. Robinson, and J.L. Lancaster Meta-analysis of gray matter anomalies in schizophrenia: Application of anatomic likelihood estimation and network analysis Biol Psychiatry 64 2008 774 781
73. B.E. Snitz, A. MacDonald, J.D. Cohen, R.Y. Cho, T. Becker, and C.S. Carter Lateral and medial hypofrontality in first-episode schizophrenia: Functional activity in a medication-naive state and effects of short-term atypical antipsychotic treatment Am J Psychiatry 162 2005 2322 2329
74. R.L. Buckner, J. Sepulcre, T. Talukdar, F.M. Krienen, H. Liu, and T. Hedden Cortical hubs revealed by intrinsic functional connectivity: Mapping, assessment of stability, and relation to Alzheimer's disease J Neurosci 29 2009 1860 1873
75. D.A. Gusnard, and M.E. Raichle Searching for a baseline: Functional imaging and the resting human brain Nat Rev Neurosci 2 2001 685 694
76. A. Fornito, M. Yucel, J. Patti, S.J. Wood, and C. Pantelis Mapping grey matter reductions in schizophrenia: An anatomical likelihood estimation analysis of voxel-based morphometry studies Schizophr Res 108 2009 104 113
77. A. Fornito, M. Yucel, S.J. Wood, C. Adamson, D. Velakoulis, and M.M. Saling Surface-based morphometry of the anterior cingulate cortex in first episode schizophrenia Hum Brain Mapp 29 2008 478 489
78. I. Ellison-Wright, and E. Bullmore Meta-analysis of diffusion tensor imaging studies in schizophrenia Schizophr Res 108 2009 3 10
79. M.P. van den Heuvel, C.J. Stam, R.S. Kahn, and H.E. Hulshoff Pol Efficiency of functional brain networks and intellectual performance J Neurosci 29 2009 7619 7624
80. W.A.H. Rushton Theory of the effects of fibre size in medulated nerve J Physiol 115 1951 101 122
81. M.E. Shenton, C.C. Dickey, M. Frumin, and R.W. McCarley A review of MRI findings in schizophrenia Schizophr Res 49 2001 1 52
82. B.A. Ardekani, J. Nierenberg, M.J. Hoptman, D.C. Javitt, and K.O. Lim MRI study of white matter diffusion anisotropy in schizophrenia Neuroreport 14 2003 2025 2029
83. R.A. Kanaan, S.S. Shergill, G.J. Barker, M. Catani, V.W. Ng, and R. Howard Tract-specific anisotropy measurements in diffusion tensor imaging Psychiatry Res 146 2006 73 82 (Pubitemid 43269991)
84. L.J. O'Donnell, C.-F. Westin, and A.J. Golby Tract-based morphometry for white matter group analysis Neuroimage 45 2009 832 844
85. J.S. Oh, M. Kubicki, G. Rosenberger, S. Bouix, J.J. Levitt, and R.W. McCarley Thalmo-frontal white matter alterations in chronic schizophrenia: A quantitative diffusion tractography study Hum Brain Mapp 30 2009 3812 3825
86. S. Mori, B.J. Crain, V.P. Chacko, and P.C. Van Zijl Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging Ann Neurol 45 1999 265 269
87. T.E. Behrens, H.J. Berg, S. Jbabdi, M.F. Rushworth, and M.W. Woolrich Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? Neuroimage 34 2007 144 155
88. T.E. Behrens, M.W. Woolrich, M. Jenkinson, H. Johansen-Berg, R.G. Nunes, and S. Clare Characterization and propagation of uncertainty in diffusion-weighted MR imaging Magn Reson Med 50 2003 1077 1088
89. S. Jbabdi, M.W. Woolrich, J.L.R. Anderson, and T.E.J. Behrens A Bayesian framework for global tractography Neuroimage 37 2007 116 129
90. A. Zalesky Diffusion tensor magnetic resonance imaging (DT-MRI) fiber tracking: A shortest paths approach IEEE Trans Med Imaging 27 2008 1458 1471
91. R.W. Heinrichs, and K.K. Zakzanis Neurocognitive deficit in schizophrenia: A quantitative review of the evidence Neuropsychology 12 1998 426 445
92. R. Kanaan, G. Barker, M. Brammer, V. Giampietro, S. Shergill, and J. Woolley White matter microstructure in schizophrenia: Effects of disorder, duration and medication Br J Psychiatry 194 2009 236 242
93. W. Wen, P.S. Sachdev, J.J. Li, X. Chen, and K.J. Anstey White matter hyperintensities in the forties: Their prevalence and topography in an epidemiological sample aged 4488 Hum Brain Mapp 30 2009 1155 1167
94. R. Schmidt, C. Enzinger, S. Ropele, H. Schmidt, and F. Fazekas Progression of cerebral white matter lesions; 6-year results of the Austrian Stroke Prevention Study Lancet 361 2003 2046 2048
95. P. Skudlarski, K. Jagannathan, K. Anderson, M.C. Stevens, V.D. Calhoun, B.A. Skudlarska, and G. Pearlson Brain connectivity is not only lower but different in schizophrenia: A combined anatomical and functional approach Biol Psychiatry 68 2010 61 69