Abnormal cortical growth in schizophrenia targets normative modules of synchronized development

Biological Psychiatry

Volumn 76, Issue 6, 2014, Pages 438-446

  Alexander Bloch, Aaron F ^a,b,c   Reiss, Philip T ^d,e   Rapoport, Judith ^a   McAdams, Harry ^a   Giedd, Jay N ^a   Bullmore, Ed T ^b,f,g   Gogtay, Nitin ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^f Cambridgeshire and Peterborough National Health Service Foundation Trust   (United States)

^g GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Neuroimaging; penalized splines; psychosis; system; topology

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN GROWTH; CHILD; COMMUNITY STRUCTURE; CONNECTOME; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); GROWTH CURVE; HUMAN; INFERIOR FRONTAL GYRUS; MAJOR CLINICAL STUDY; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; ORBITAL CORTEX; POSTCENTRAL GYRUS; POSTERIOR CINGULATE; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; RIGHT HEMISPHERE; SCHIZOPHRENIA; SUPERIOR TEMPORAL GYRUS; SUPPLEMENTARY MOTOR AREA; ABNORMALITIES; COMPUTER SIMULATION; FEMALE; MALE; NERVE CELL NETWORK; PATHOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; CEREBRAL CORTEX; CHILD; COMPUTER SIMULATION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; SCHIZOPHRENIA; YOUNG ADULT;

EID: 84907598634     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2014.02.010     Document Type: Article

References (78)

1. S.V. Haijma, N. Van Haren, W. Cahn, PCMP Koolschijn, H.E. Hulshoff Pol, and R.S. Kahn Brain volumes in schizophrenia: A meta-analysis in over 18 000 subjects Schizophr Bull 39 2013 1129 1138
2. D.C. Glahn, A.R. Laird, I. Ellison-Wright, S.M. Thelen, J.L. Robinson, and J.L. Lancaster et al. Meta-analysis of gray matter anomalies in schizophrenia: Application of anatomic likelihood estimation and network analysis Biol Psychiatry 64 2008 774 781
3. I. Nenadic, C. Gaser, and H. Sauer Heterogeneity of brain structural variation and the structural imaging endophenotypes in schizophrenia Neuropsychobiology 66 2012 44 49
4. I. Ellison-Wright, and E. Bullmore Meta-analysis of diffusion tensor imaging studies in schizophrenia Schizophr Res 108 2009 3 10
5. R. Honea, T.J. Crow, D. Passingham, and C.E. Mackay Regional deficits in brain volume in schizophrenia: A meta-analysis of voxel-based morphometry studies Am J Psychiatry 162 2005 2233 2245
6. D.S. Bassett, E.T. Bullmore, A. Meyer-Lindenberg, J.A. Apud, D.R. Weinberger, and R. Coppola Cognitive fitness of cost-efficient brain functional networks Proc Natl Acad Sci U S A 106 2009 11747 11752
7. Y. Liu, M. Liang, Y. Zhou, Y. He, Y. Hao, and M. Song et al. Disrupted small-world networks in schizophrenia Brain 131 2008 945 961
8. A. Zalesky, A. Fornito, M.L. Seal, L. Cocchi, C.-F. Westin, and E.T. Bullmore et al. Disrupted axonal fiber connectivity in schizophrenia Biol Psychiatry 69 2011 80 89
9. G. Collin, M.A. de Reus, W. Cahn, H.E. Hulshoff Pol, R.S. Kahn, and M.P. van den Heuvel Disturbed grey matter coupling in schizophrenia Eur Neuropsychopharmacol 23 2013 46 54
10. N. Gogtay, N.S. Vyas, R. Testa, S.J. Wood, and C. Pantelis Age of onset of schizophrenia: Perspectives from structural neuroimaging studies Schizophr Bull 37 2011 504 513
11. J.L. Rapoport, J.N. Giedd, and N. Gogtay Neurodevelopmental model of schizophrenia: Update 2012 Mol Psychiatry 17 2012 1228 1238
12. T. Paus, R. Toro, G. Leonard, J.V. Lerner, R.M. Lerner, and M. Perron et al. Morphological properties of the action-observation cortical network in adolescents with low and high resistance to peer influence Soc Neurosci 3 2008 303 316
13. T. Paus, M. Keshavan, and J.N. Giedd Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9 2008 947 957
14. N. Gogtay, J.N. Giedd, L. Lusk, K.M. Hayashi, D. Greenstein, and A.C. Vaituzis et al. Dynamic mapping of human cortical development during childhood through early adulthood Proc Natl Acad Sci U S A 101 2004 8174 8179
15. D. Greenstein, J. Lerch, P. Shaw, L. Clasen, J. Giedd, and P. Gochman et al. Childhood onset schizophrenia: Cortical brain abnormalities as young adults J Child Psychol Psychiatry 47 2006 1003 1012
16. A. Alexander-Bloch, J.N. Giedd, and E.T. Bullmore Imaging structural covariance between human brain regions Nat Rev Neurosci 14 2013 322 336
17. A. Raznahan, J.P. Lerch, N. Lee, D. Greenstein, G.L. Wallace, and M. Stockman et al. Patterns of coordinated anatomical change in human cortical development: A longitudinal neuroimaging study of maturational coupling Neuron 72 2011 873 884
18. A.F. Alexander-Bloch, A. Raznahan, J. Giedd, and E.T. Bullmore The convergence of maturational change and structural covariance in human cortical networks J Neurosci 33 2013 2889 2899
19. G. Gong, Y. He, Z.J. Chen, and A.C. Evans Convergence and divergence of thickness correlations with diffusion connections across the human cerebral cortex Neuroimage 59 2012 1239 1248
20. D. Ruppert, M.P. Wand, and R.J. Carroll Semiparametric Regression 2003 Cambridge University Press New York
21. S.N. Wood Generalized Additive Models 2006 Chapman & Hall Boca Raton, FL
22. J.P. Lerch, K. Worsley, W.P. Shaw, D.K. Greenstein, R.K. Lenroot, J. Giedd, and A.C. Evans Mapping anatomical correlations across cerebral cortex (MACACC) using cortical thickness from MRI Neuroimage 31 2006 993 1003
23. K. Im, J.-M. Lee, O. Lyttelton, S.H. Kim, A.C. Evans, and S.I. Kim Brain size and cortical structure in the adult human brain Cereb Cortex 18 2008 2181 2191
24. J.S. Kim, V. Singh, J.K. Lee, J. Lerch, Y. Ad-Dab'bagh, and D. MacDonald et al. Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification Neuroimage 27 2005 210 221
25. Wood S, Scheipl F (2012): gamm4: Generalized additive mixed models using mgcv and lme4. R package version 0.1-6. Available at: http://CRAN.R-project.org/ package=gamm4. Accessed July 7, 2013.
26. S.N. Wood Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models J R Stat Soc Series B Stat Methodol 73 2010 3 36
27. S.N. Wood Stable and efficient multiple smoothing parameter estimation for generalized additive models J Am Stat Assoc 99 2004 673 686
28. S.N. Wood Thin plate regression splines J R Stat Soc Series B Stat Methodol 65 2003 95 114
29. S.N. Wood Modelling and smoothing parameter estimation with multiple quadratic penalties J R Stat Soc Series B Stat Methodol 62 2000 413 428
30. Reiss P, Chen Y-H, Huang L, Huo L (2012): vows: Voxelwise semiparametrics. R package version 0.2-0. Available at: http://CRAN.R-project. org/package=vows. Accessed July 7, 2013.
31. Maechler M, Rousseeuw P, Struyf A, Hubert M, Hornik K (2012): cluster: Cluster Analysis Basics and Extensions. R package version 1.14.3. Available at: http://CRAN.R-project.org/package=cluster. Accessed July 7, 2013.
32. K. Hornik A CLUE for CLUster ensembles J Stat Softw 14 2005 65 72
33. Hornik K, Bohm W (2012): clue: Cluster Ensembles. R package version 0.3-45. Available at: http://CRAN.R-project.org/package=clue. Accessed July 7, 2013.
34. P.T. Reiss, and R.T. Ogden Functional principal component regression and functional partial least squares J Am Stat Assoc 102 2007 984 996
35. N.M. Laird, and J.H. Ware Random-effects models for longitudinal data Biometrics 38 1982 963 974
36. M.P. Wand, and J.T. Ormerod On semiparametric regression with O'Sullivan penalized splines Aust N Z J Stat 50 2008 179 198
37. T. Hastie, and R. Tibshirani Varying-coefficient models J R Stat Soc Series B Stat Methodol 55 1993 757 796
38. S.N. Wood On p-values for smooth components of an extended generalized additive model Biometrika 100 2013 221 228
39. Y. Benjamini, A.M. Krieger, and D. Yekutieli Adaptive linear step-up procedures that control the false discovery rate Biometrika 93 2006 491 507
40. B.W. Silverman Smoothed functional principal components analysis by choice of norm Ann Stat 24 1996 1 24
41. Kaufman L, Rousseeuw P (1987): Clustering by means of medoids. In: Dodge Y, editor. Statistical Data Analysis Based on the L1 - Norm and Related Methods. Amsterdam: North Holland, 405-416
42. T. Tarpey, and K.K.J. Kinateder Clustering functional data J Classification 20 2003 93 114
43. P.E. Vértes, A.F. Alexander-Bloch, N. Gogtay, J.N. Giedd, J.L. Rapoport, and E.T. Bullmore Simple models of human brain functional networks Proc Natl Acad Sci U S A 109 2012 5868 5873
44. A.F. Alexander-Bloch, P.E. Vértes, R. Stidd, F. Lalonde, L. Clasen, and J. Rapoport et al. The anatomical distance of functional connections predicts brain network topology in health and schizophrenia Cereb Cortex 23 2013 127 138
45. M. Kaiser, and S. Varier Evolution and development of brain networks: From Caenorhabditis elegans to Homo sapiens Network 22 2011 143 147
46. E. Bullmore, and O. Sporns The economy of brain network organization Nat Rev Neurosci 13 2012 336 349
47. J.N. Giedd, J. Blumenthal, N.O. Jeffries, F.X. Castellanos, H. Liu, and A. Zijdenbos et al. Brain development during childhood and adolescence: A longitudinal MRI study Nat Neurosci 2 1999 861 863
48. J.P. Lerch, A.P. Yiu, A. Martinez-Canabal, T. Pekar, V.D. Bohbot, and P.W. Frankland et al. Maze training in mice induces MRI-detectable brain shape changes specific to the type of learning Neuroimage 54 2011 2086 2095
49. P.R. Huttenlocher Synapse elimination and plasticity in developing human cerebral cortex Am J Ment Defic 88 1984 488 496
50. A. Raznahan, P. Shaw, F. Lalonde, M. Stockman, G.L. Wallace, and D. Greenstein et al. How does your cortex grow? J Neurosci 31 2011 7174 7177
51. P. Shaw, N.J. Kabani, J.P. Lerch, K. Eckstrand, R. Lenroot, and N. Gogtay et al. Neurodevelopmental trajectories of the human cerebral cortex J Neurosci 28 2008 3586 3594
52. A.M. Fjell, K.B. Walhovd, L.T. Westlye, Y. ∅stby, C.K. Tamnes, and T.L. Jernigan et al. When does brain aging accelerate? Dangers of quadratic fits in cross-sectional studies Neuroimage 50 2010 1376 1383
53. Z.J. Chen, Y. He, P. Rosa-Neto, G. Gong, and A.C. Evans Age-related alterations in the modular organization of structural cortical network by using cortical thickness from MRI Neuroimage 56 2011 235 245
54. Z.J. Chen, Y. He, P. Rosa-Neto, J. Germann, and A.C. Evans Revealing modular architecture of human brain structural networks by using cortical thickness from MRI Cereb Cortex 18 2008 2374 2381
55. T.H. McGlashan, and R.E. Hoffman Schizophrenia as a disorder of developmentally reduced synaptic connectivity Arch Gen Psychiatry 57 2000 637 648
56. I. Feinberg Schizophrenia: Caused by a fault in programmed synaptic elimination during adolescence? J Psychiatr Res 17 1982-1983 319 334
57. D.A. Lewis Development of the prefrontal cortex during adolescence: Insights into vulnerable neural circuits in schizophrenia Neuropsychopharmacology 16 1997 385 398
58. D.A. Lewis, D. Cruz, S. Eggan, and S. Erickson Postnatal development of prefrontal inhibitory circuits and the pathophysiology of cognitive dysfunction in schizophrenia Ann N Y Acad Sci 1021 2004 64 76
59. K.H. Choi, M.E. Zepp, B.W. Higgs, C.S. Weickert, and M.J. Webster Expression profiles of schizophrenia susceptibility genes during human prefrontal cortical development J Psychiatry Neurosci 34 2009 450 458
60. D. Arion, S. Horváth, D.A. Lewis, and K. Mirnics Infragranular gene expression disturbances in the prefrontal cortex in schizophrenia: Signature of altered neural development? Neurobiol Dis 37 2010 738 746
61. L. Ronan, N.L. Voets, M. Hough, C. Mackay, N. Roberts, and J. Suckling et al. Consistency and interpretation of changes in millimeter-scale cortical intrinsic curvature across three independent datasets in schizophrenia Neuroimage 63 2012 611 621
62. V.W.V. Jaddoe, C.M. van Duijn, A.J. van der Heijden, J.P. Mackenbach, H.A. Moll, and E.A.P. Steegers et al. The Generation R Study: Design and cohort update 2010 Eur J Epidemiol 25 2010 823 841
63. A. Fornito, A. Zalesky, C. Pantelis, and E.T. Bullmore Schizophrenia, neuroimaging and connectomics Neuroimage 62 2012 2296 2314
64. M.P. van den Heuvel, R.C.W. Mandl, C.J. Stam, R.S. Kahn, and H.E. Hulshoff Pol Aberrant frontal and temporal complex network structure in schizophrenia: A graph theoretical analysis J Neurosci 30 2010 15915 15926
65. J.E. Schmitt, R.K. Lenroot, S.E. Ordaz, G.L. Wallace, J.P. Lerch, and A.C. Evans et al. Variance decomposition of MRI-based covariance maps using genetically informative samples and structural equation modeling Neuroimage 47 2009 56 64
66. L.M. Rimol, M.S. Panizzon, C. Fennema-Notestine, L.T. Eyler, B. Fischl, and C.E. Franz et al. Cortical thickness is influenced by regionally specific genetic factors Biol Psychiatry 67 2010 493 499
67. C.-H. Chen, E.D. Gutierrez, W. Thompson, M.S. Panizzon, T.L. Jernigan, and L.T. Eyler et al. Hierarchical genetic organization of human cortical surface area Science 335 2012 1634 1636
68. M.H. Johnson Functional brain development in humans Nat Rev Neurosci 2 2001 475 483
69. A. Karmiloff-Smith Development itself is the key to understanding developmental disorders Trends Cogn Sci 2 1998 389 398
70. N. Sugiura Further analysis of the data by Akaike's information criterion and the finite corrections Comm Stat Theor Meth 7 1978 13 26
71. P.T. Reiss, L. Huang, Y.H. Chen, L. Huo, T. Tarpey, and M. Mennes Massively parallel nonparametric regression, with an application to developmental brain mapping J Comput Graph Stat 23 2014 232 248
72. P.J. Green, and B.W. Silverman Nonparametric Regression and Generalized Linear Models 1994 Chapman & Hall Boca Raton, FL
73. R.W. Heinrichs, and K.K. Zakzanis Neurocognitive deficit in schizophrenia: A quantitative review of the evidence Neuropsychology 12 1998 426 445
74. N. Gogtay, D. Greenstein, M. Lenane, L. Clasen, W. Sharp, and P. Gochman et al. Cortical brain development in nonpsychotic siblings of patients with childhood-onset schizophrenia Arch Gen Psychiatry 64 2007 772 780
75. P. Satz, and M.F. Green Atypical handedness in schizophrenia: Some methodological and theoretical issues Schizophr Bull 25 1999 63 78
76. I. Sommer, N. Ramsey, R. Kahn, A. Aleman, and A. Bouma Handedness, language lateralisation and anatomical asymmetry in schizophrenia: Meta-analysis Br J Psychiatry 178 2001 344 351
77. M. Dragovic, and G. Hammond Handedness in schizophrenia: A quantitative review of evidence Acta Psychiatr Scand 111 2005 410 419
78. A. Deep-Soboslay, T.M. Hyde, J.P. Callicott, M.S. Lener, B.A. Verchinski, and J.A. Apud et al. Handedness, heritability, neurocognition and brain asymmetry in schizophrenia Brain 133 2010 3113 3122