White matter alterations in early stages of schizophrenia: A systematic review of diffusion tensor imaging studies

Journal of Neuroimaging

Volumn 24, Issue 2, 2014, Pages 101-110

  Samartzis, Lampros ^a,b   Dima, Danai ^a   Fusar Poli, Paolo ^a   Kyriakopoulos, Marinos ^a,c  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b Athalassa Hospital   (Cyprus)

^c SOUTH LONDON AND MAUDSLEY NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Diffusion tensor imaging; Dysconnectivity; High risk psychosis; Neurodevelopment; Schizophrenia; White matter

Indexed keywords

NEUROLEPTIC AGENT;

AGE; ARTICLE; BRAIN REGION; CORPUS CALLOSUM; DEVELOPMENTAL STAGE; DIFFUSION TENSOR IMAGING; DISEASE COURSE; DISEASE DURATION; DRUG EXPOSURE; FRONTAL CORTEX; HUMAN; LIMBIC SYSTEM; MEDIAL LONGITUDINAL FASCICULUS; MENTAL PATIENT; NEUROPATHOLOGY; PSYCHOPHARMACOTHERAPY; SCHIZOPHRENIA; SYSTEMATIC REVIEW; TEMPORAL CORTEX; UNCINATE FASCICULUS; WHITE MATTER; BRAIN; FEMALE; MYELINATED NERVE; PATHOLOGY; PROCEDURES;

BRAIN; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; NERVE FIBERS, MYELINATED; SCHIZOPHRENIA; WHITE MATTER;

EID: 84896710125     PISSN: 10512284     EISSN: 15526569     Source Type: Journal    
DOI: 10.1111/j.1552-6569.2012.00779.x     Document Type: Article

References (139)

1. Hafner H, Maurer K, Loffler W, et al. The influence of age and sex on the onset and early course of schizophrenia. Br J Psychiat 1993;162:80-86.
2. Walterfang M, Velakoulis D, Whitford TJ, et al. Understanding aberrant white matter development in schizophrenia: an avenue for therapy? Expert Rev Neurotherapeut 2011;11:971-987.
3. Basser PJ. Focal magnetic stimulation of an axon. IEEE Trans Biomed Eng 1994;41:601-606.
4. Basser PJ, Mattiello J, LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 1994;103:247-254.
5. Basser PJ, Mattiello J, LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys J 1994;66:259-267.
6. Le Bihan D, Mangin JF, Poupon C, et al. Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 2001;13:534-546.
7. Le Bihan D, Breton E, Lallemand D, et al. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 1986;161:401-407.
8. Le Bihan D, Poupon C, Amadon A, et al. Artifacts and pitfalls in diffusion MRI. J Magn Reson Imaging 2006;24:478-488.
9. Le Bihan D, Turner R, Douek P, et al. Diffusion MR imaging: clinical applications. Am J Roentgenol 1992;159:591-599.
10. Taylor WD, Hsu E, Krishnan KR, et al. Diffusion tensor imaging: background, potential, and utility in psychiatric research. Biol Psychiatry 2004;55:201-207.
11. Basser PJ, Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 1996;111:209-219.
12. Johansen-Berg H, Rushworth MF. Using diffusion imaging to study human connectional anatomy. Annu Rev Neurosci 2009;32:75-94.
13. Laule C, Vavasour IM, Kolind SH, et al. Magnetic resonance imaging of myelin. Neurotherapeutics 2007;4:460-484.
14. Kubicki M, McCarley R, Westin CF, et al. A review of diffusion tensor imaging studies in schizophrenia. J Psychiatr Res 2007;41:15-30.
15. Pierpaoli C, Jezzard P, Basser PJ, et al. Diffusion tensor MR imaging of the human brain. Radiology 1996;201:637-648.
16. Burzynska AZ, Preuschhof C, Bäckman L, et al. Age-related differences in white matter microstructure: region-specific patterns of diffusivity. Neuroimage 2010;49:2104-2112.
17. Toga AW, Thompson PM, Sowell ER. Mapping brain maturation. Trends Neurosci 2006;29:148-159.
18. Giorgio A, Watkins KE, Douaud G, et al. Changes in white matter microstructure during adolescence. Neuroimage 2008;39:52-61.
19. Lebel C, Walker L, Leemans A, et al. Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 2008;40:1044-1055.
20. Ashtari M, Cervellione KL, Hasan KM, et al. White matter development during late adolescence in healthy males: a cross-sectional diffusion tensor imaging study. Neuroimage 2007;35:501-510.
21. Davis KL, Stewart DG, Friedman JI, et al. White matter changes in schizophrenia: evidence for myelin-related dysfunction. Arch Gen Psychiatry 2003;60:443-456.
22. Konrad A, Winterer G. Disturbed structural connectivity in schizophrenia primary factor in pathology or epiphenomenon? Schizophr Bull 2008;34:72-92.
23. Hakak Y, Walker JR, Li C, et al. Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proc Nat Acad Sci USA 2001;98:4746-4751.
24. Torrey EF, Webster M, Knable M, et al. The Stanley foundation brain collection and neuropathology consortium. Schizophr Res 2000;44:151-155.
25. Orlovskaya D, Vostrikov V, Rachmanova V, et al. Decreased numerical density of oligodendroglial cells in postmortem prefrontal cortex in schizophrenia, bipolar affective disorder and major depression. Schizophr Res 2000;41:105-106.
26. Uranova NA, Vostrikov VM, Orlovskaya DD, et al.Oligodendroglial density in the prefrontal cortex in schizophrenia and mood disorders: a study from the Stanley Neuropathology Consortium. Schizophr Res 2004;67:269-275.
27. Segal D, Koschnick JR, Slegers LH, et al. Oligodendrocyte pathophysiology: a new view of schizophrenia. Int J Neuropsychopharmacol 2007;10:503-511.
28. Tkachev D, Mimmack ML, Ryan MM, et al. Oligodendrocyte dysfunction in schizophrenia and bipolar disorder. Lancet 2003;362:798-805.
29. Peirce TR, Bray NJ, Williams NM, et al. Convergent evidence for 2', 3'-cyclic nucleotide 3'-phosphodiesterase as a possible susceptibility gene for schizophrenia. Arch Gen Psychiat 2006;63:18-24.
30. Roussos P, Katsel P, Davis KL, et al. Molecular and genetic evidence for abnormalities in the nodes of Ranvier in schizophrenia. Arch Gen Psychiat 2012;69:7-15.
31. Stevens B, Porta S, Haak LL, et al. Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 2002;36:855-868.
32. Kyriakopoulos M, Bargiotas T, Barker GJ, et al. Diffusion tensor imaging in schizophrenia. Eur Psychiat 2008;23:255-273.
33. Fusar-Poli P, Borgwardt S, Bechdolf A, et al. The psychosis high risk state: a comprehensive state of the art review. Arch Gen Psychiat 2013;70(1):107-120.
34. Fusar-Poli P, Bonoldi I, Yung AR, et al. Predicting psychosis: a meta-analysis of transition outcomes in individuals at high clinical risk. Arch Gen Psychiat 2012;69:1-10.
35. Fusar-Poli P, Bonoldi I, Yung AR, et al. Predicting psychosis: meta-analysis of transition outcomes in individuals at high clinical risk. Arch Gen Psychiat 2012;69:220-229.
36. Fusar-Poli P, Bechdolf A, Taylor M, et al. At risk for schizophrenic or affective psychosis? A meta-analysis of DSM/ICD diagnostic outcomes in individuals at high clinical risk. Schizophr Bull 2012: May 15. doi: 10.1093/schbul/sbs060 [Epub ahead of print].
37. Fusar-Poli P, Deste G, Smieskova R, et al. Cognitive functioning in prodromal psychosis: a meta-analysis. Arch Gen Psychiat 2012;69(6):562-571.
38. Fusar-Poli P, Radua J, McGuire P, et al. Neuroanatomical maps of psychosis onset: voxel-wise meta-analysis of antipsychotic-naive VBM studies. Schizophr Bull 2011: Nov 10. doi: 10.1093/schbul/sbr134 [Epub ahead of print].
39. Fusar-Poli P, Borgwardt S, Crescini A, et al. Neuroanatomy of vulnerability to psychosis: a voxel-based meta-analysis. Neurosci Biobehav Rev 2011;35:1175-1185.
40. Smieskova R, Fusar-Poli P, Allen P, et al. Neuroimaging predictors of transition to psychosis-a systematic review and meta-analysis. Neurosci Biobehav Rev 2010;34:1207-1222.
41. Fusar-Poli P, Perez J, Broome M, et al. Neurofunctional correlates of vulnerability to psychosis: a systematic review and meta-analysis. Neurosci Biobehav Rev 2007;31:465-484.
42. Fusar-Poli P, Howes OD, Allen P, et al. Abnormal frontostriatal interactions in people with prodromal signs of psychosis: a multimodal imaging study. Arch Gen Psychiat 2010;67:683-691.
43. Fusar-Poli P, Howes OD, Allen P, et al. Abnormal prefrontal activation directly related to pre-synaptic striatal dopamine dysfunction in people at clinical high risk for psychosis. Mol Psychiat 2011;16:67-75.
44. Crossley NA, Mechelli A, Fusar-Poli P, et al. Superior temporal lobe dysfunction and frontotemporal dysconnectivity in subjects at risk of psychosis and in first-episode psychosis. Hum Brain Mapp 2009;30:4129-4137.
45. Fusar-Poli P, Meyer-Lindenberg A. Striatal presynaptic dopamine in schizophrenia, part II: meta-analysis of 18F./11C. DOPA PET studies. Schizophr Bull. 2012: Jan 26. doi: 10.1093/schbul/sbr180 [Epub ahead of print].
46. Fusar-Poli P, Stone J, Broome M, et al. Thalamic glutamate levels predicts cortical response during executive functioning in subjects at high risk for psychosis. Arch Gen Psychiat 2011;68(9):881-890.
47. Howes O, Montgomery A, Asselin M, et al. Elevated striatal dopamine function linked to prodromal signs of schizophrenia. Arch Gen Psychiat 2009;66:13-20.
48. Fusar-Poli P, Yung A. Should attenuated psychosis syndrome be included in the DSM5? The debate. The Lancet 2012;379:591-592.
49. Ashtari M, Cottone J, Ardekani BA, et al. Disruption of white matter integrity in the inferior longitudinal fasciculus in adolescents with schizophrenia as revealed by fiber tractography. Arch Gen Psychiat 2007;64:1270-1280.
50. Bloemen OJ, de Koning MB, Schmitz N, et al. White-matter markers for psychosis in a prospective ultra-high-risk cohort. Psychol Med 2010;40:1297-1304.
51. Chan WY, Yang GL, Chia MY, et al. White matter abnormalities in first-episode schizophrenia: a combined structural MRI and DTI study. Schizophr Res 119:52-60.
52. Cheung V, Cheung C, McAlonan GM, et al. A diffusion tensor imaging study of structural dysconnectivity in never-medicated, first-episode schizophrenia. Psychol Med 2008;38:877-885.
53. Cheung V, Chiu CP, Law CW, et al. Positive symptoms and white matter microstructure in never-medicated first episode schizophrenia. Psychol Med 2011;41:1709-1719.
54. Dekker N, Schmitz N, Peters BD, et al. Cannabis use and callosal white matter structure and integrity in recent-onset schizophrenia. Psychiat Res 2010;181:51-56.
55. Douaud G, Smith S, Jenkinson M, et al. Anatomically related grey and white matter abnormalities in adolescent-onset schizophrenia. Brain 2007;130:2375-2386.
56. Federspiel A, Begre S, Kiefer C, et al. Alterations of white matter connectivity in first episode schizophrenia. Neurobiol Dis 2006;22:702-709.
57. Friedman JI, Tang C, Carpenter D, et al. Diffusion tensor imaging findings in first-episode and chronic schizophrenia patients. Am J Psychiat 2008;165:1024-1032.
58. Gasparotti R, Valsecchi P, Carletti F, et al. Reduced fractional anisotropy of corpus callosum in first-contact, antipsychotic drug-naive patients with schizophrenia. Schizophr Res 2009;108:41-48.
59. Hao Y, Liu Z, Jiang T, et al. White matter integrity of the whole brain is disrupted in first-episode schizophrenia. Neuroreport 2006;17:23-26.
60. Hoptman MJ, Nierenberg J, Bertisch HC, et al. A DTI study of white matter microstructure in individuals at high genetic risk for schizophrenia. Schizophr Res 2008;106:115-124.
61. Jacobson S, Kelleher I, Harley M, et al. Structural and functional brain correlates of subclinical psychotic symptoms in 11-13 year old school children. Neuroimage 2010;49:1875-1885.
62. Karlsgodt KH, Niendam TA, Bearden CE, et al. White matter integrity and prediction of social and role functioning in subjects at ultra-high risk for psychosis. Biol Psychiat 2009;66:562-569.
63. Karlsgodt KH, van Erp TG, Poldrack RA, et al. Diffusion tensor imaging of the superior longitudinal fasciculus and working memory in recent-onset schizophrenia. Biol Psychiat 2008;63:512-518.
64. Kawashima T, Nakamura M, Bouix S, et al. Uncinate fasciculus abnormalities in recent onset schizophrenia and affective psychosis: a diffusion tensor imaging study. Schizophr Res 2009;110:119-126.
65. Kendi M, Kendi AT, Lehericy S, et al. Structural and diffusion tensor imaging of the fornix in childhood- and adolescent-onset schizophrenia. J Am Acad Child Adolesc Psychiat 2008;47:826-832.
66. Kong X, Ouyang X, Tao H, et al. Complementary diffusion tensor imaging study of the corpus callosum in patients with first-episode and chronic schizophrenia. J Psychiat Neurosci 2011;36:120-125.
67. Kumra S, Ashtari M, Cervellione KL, et al. White matter abnormalities in early-onset schizophrenia: a voxel-based diffusion tensor imaging study. J Am Acad Child Adolesc Psychiat 2005;44:934-941.
68. Kumra S, Ashtari M, McMeniman M, et al. Reduced frontal white matter integrity in early-onset schizophrenia: a preliminary study. Biol Psychiat 2004;55:1138-1145.
69. Kyriakopoulos M, Perez-Iglesias R, Woolley JB, et al. Effect of age at onset of schizophrenia on white matter abnormalities. Br J Psychiat 2009;195:346-353.
70. Kyriakopoulos M, Vyas NS, Barker GJ, et al. A diffusion tensor imaging study of white matter in early-onset schizophrenia. Biol Psychiat 2008;63:519-523.
71. Luck D, Buchy L, Czechowska Y, et al. Fronto-temporal disconnectivity and clinical short-term outcome in first episode psychosis: a DTI-tractography study. J Psychiat Res 2010;45(3):369-377.
72. Mendelsohn A, Strous RD, Bleich M, et al. Regional axonal abnormalities in first episode schizophrenia: preliminary evidence based on high b-value diffusion-weighted imaging. Psychiat Res 2006;146:223-229.
73. Moriya J, Kakeda S, Abe O, et al. Gray and white matter volumetric and diffusion tensor imaging (DTI) analyses in the early stage of first-episode schizophrenia. Schizophr Res 2010;116:196-203.
74. Perez-Iglesias R, Tordesillas-Gutierrez D, Barker GJ, et al. White matter defects in first episode psychosis patients: a voxelwise analysis of diffusion tensor imaging. Neuroimage 2010;49:199-204.
75. Peters BD, de Haan L, Dekker N, et al. White matter fibertracking in first-episode schizophrenia, schizoaffective patients and subjects at ultra-high risk of psychosis. Neuropsychobiology 2008;58:19-28.
76. Peters BD, de Haan L, Vlieger EJ, et al. Recent-onset schizophrenia and adolescent cannabis use: MRI evidence for structural hyperconnectivity? Psychopharmacol Bull 2009;42:75-88.
77. Peters BD, Dingemans PM, Dekker N, et al. White matter connectivity and psychosis in ultra-high-risk subjects: a diffusion tensor fiber tracking study. Psychiat Res 2010;181:44-50.
78. Peters BD, Schmitz N, Dingemans PM, et al. Preliminary evidence for reduced frontal white matter integrity in subjects at ultra-high-risk for psychosis. Schizophr Res 2009;111:192-193.
79. Price G, Bagary MS, Cercignani M, et al. The corpus callosum in first episode schizophrenia: a diffusion tensor imaging study. J Neurol Neurosurg Psychiat 2005;76:585-587.
80. Price G, Cercignani M, Parker GJ, et al. Abnormal brain connectivity in first-episode psychosis: a diffusion MRI tractography study of the corpus callosum. Neuroimage 2007;35:458-466.
81. Price G, Cercignani M, Parker GJ, et al. White matter tracts in first-episode psychosis: a DTI tractography study of the uncinate fasciculus. Neuroimage 2008;39:949-955.
82. Qiu A, Zhong J, Graham S, et al. Combined analyses of thalamic volume, shape and white matter integrity in first-episode schizophrenia. Neuroimage 2009;47:1163-1171.
83. Szeszko PR, Ardekani BA, Ashtari M, et al. White matter abnormalities in first-episode schizophrenia or schizoaffective disorder: a diffusion tensor imaging study. Am J Psychiat 2005;162:602-605.
84. Szeszko PR, Robinson DG, Ashtari M, et al. Clinical and neuropsychological correlates of white matter abnormalities in recent onset schizophrenia. Neuropsychopharmacology 2008;33:976-984.
85. Tang J, Liao Y, Zhou B, et al. Abnormal anterior cingulum integrity in first episode, early-onset schizophrenia: a diffusion tensor imaging study. Brain Res 2010;1343:199-205.
86. White T, Kendi AT, Lehericy S, et al. Disruption of hippocampal connectivity in children and adolescents with schizophrenia-a voxel-based diffusion tensor imaging study. Schizophr Res 2007;90:302-307.
87. White T, Magnotta VA, Bockholt HJ, et al. Global white matter abnormalities in Schizophrenia: a multisite diffusion tensor imaging study. Schizophr Bull 2011;37(1):222-232.
88. White T, Schmidt M, Karatekin C. White matter 'potholes' in early-onset schizophrenia: a new approach to evaluate white matter microstructure using diffusion tensor imaging. Psychiatry Res 2009;174:110-115.
89. Zou LQ, Xie JX, Yuan HS, et al. Diffusion tensor imaging study of the anterior limb of internal capsules in neuroleptic-naive schizophrenia. Acad Radiol 2008;15:285-289.
90. Douaud G, Mackay C, Andersson J, et al. Schizophrenia delays and alters maturation of the brain in adolescence. Brain 2009;132:2437-2448.
91. James A, Hough M, James S, et al. Greater white and grey matter changes associated with early cannabis use in adolescent-onset schizophrenia (AOS). Schizophr Res 2011;128:91-97.
92. Schneiderman JS, Buchsbaum MS, Haznedar MM, et al. Age and diffusion tensor anisotropy in adolescent and adult patients with schizophrenia. Neuroimage 2009;45:662-671.
93. Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009;6:e1000097. doi:10.1371/journal.pmed.1000097.
94. Munoz Maniega S, Lymer GK, Bastin ME, Marjoram D, et al. A diffusion tensor MRI study of white matter integrity in subjects at high genetic risk of schizophrenia. Schizophr Res 2008;106:132-139.
95. Fornito A, Yung AR, Wood SJ, et al. Anatomic abnormalities of the anterior cingulate cortex before psychosis onset: an MRI study of ultra-high-risk individuals. Biol Psychiat 2008;64:758-765.
96. Shenton ME, Dickey CC, Frumin M, et al. A review of MRI findings in schizophrenia. Schizophr Res 2001;49:1-52.
97. Pantelis C, Yucel M, Wood SJ, et al.Structural brain imaging evidence for multiple pathological processes at different stages of brain development in schizophrenia. Schizophr Bull 2005;31:672-696.
98. Borgwardt SJ, McGuire PK, Aston J, et al. Structural brain abnormalities in individuals with an at-risk mental state who later develop psychosis. Br J Psychiat Suppl 2007;51:s69-75.
99. Koutsouleris N, Meisenzahl EM, Davatzikos C, et al. Use of neuroanatomical pattern classification to identify subjects in at-risk mental states of psychosis and predict disease transition. Arch Gen Psychiat 2009;66:700-712.
100. Pantelis C, Velakoulis D, McGorry PD, et al. Neuroanatomical abnormalities before and after onset of psychosis: a cross-sectional and longitudinal MRI comparison. Lancet 2003;361:281-288.
101. Smieskova R, Fusar-Poli P, Allen P, et al. Neuroimaging predictors of transition to psychosis-a systematic review and meta-analysis. Neurosci Biobehav Rev 2010;34:1207-1222.
102. Fornito A, Yucel M, Dean B, et al. Anatomical abnormalities of the anterior cingulate cortex in schizophrenia: bridging the gap between neuroimaging and neuropathology. Schizophr Bull 2009;35:973-993.
103. Camchong J, Macdonald AW, 3rd, Bell C, et al. Altered functional and anatomical connectivity in Schizophrenia. Schizophr Bull 2009;37:640-650.
104. Fusar-Poli P, Crossley N, Woolley J, et al. White matter alterations related to P300 abnormalities in individuals at high risk for psychosis: an MRI-EEG study. J Psychiat Neurosci 2011;36:239-248.
105. Allen P, Stephan KE, Mechelli A, et al. Cingulate activity and fronto-temporal connectivity in people with prodromal signs of psychosis. Neuroimage 2010;49:947-955.
106. Sabb FW, van Erp TG, Hardt ME, et al. Language network dysfunction as a predictor of outcome in youth at clinical high risk for psychosis. Schizophr Res 2010;116:173-183.
107. Gogtay N, Giedd JN, Lusk L, et al. Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci USA 2004;101:8174-8179.
108. White T, Andreasen NC, Nopoulos P, et al. Gyrification abnormalities in childhood- and adolescent-onset schizophrenia. Biol Psychiat 2003;54:418-426.
109. Voets NL, Hough MG, Douaud G, et al. Evidence for abnormalities of cortical development in adolescent-onset schizophrenia. Neuroimage 2008;43:665-675.
110. Carpenter DM, Tang CY, Friedman JI, et al. Temporal characteristics of tract-specific anisotropy abnormalities in schizophrenia. Neuroreport 2008;19:1369-1372.
111. Rosenberger G, Kubicki M, Nestor PG, et al. Age-related deficits in fronto-temporal connections in schizophrenia: a diffusion tensor imaging study. Schizophr Res 2008;102:181-188.
112. Christensen J, Holcomb J, Garver DL. State-related changes in cerebral white matter may underlie psychosis exacerbation. Psychiat Res 2004;130:71-78.
113. Garver DL, Holcomb JA, Christensen JD. Heterogeneity of response to antipsychotics from multiple disorders in the schizophrenia spectrum. J Clin Psychiat 2000;61:964-972; quiz 73.
114. Garver DL, Holcomb JA, Christensen JD. Compromised myelin integrity during psychosis with repair during remission in drug-responding schizophrenia. Int J Neuropsychopharmacol 2008;11:49-61.
115. DeLisi LE, Szulc KU, Bertisch H, et al. Early detection of schizophrenia by diffusion weighted imaging. Psychiat Res: Neuroimaging 2006;148:61-66.
116. Cahn W, Hulshoff Pol HE, Caspers E, et al. Cannabis and brain morphology in recent-onset schizophrenia. Schizophr Res 2004;67:305-307.
117. Szeszko PR, Robinson DG, Sevy S, et al. Anterior cingulate grey-matter deficits and cannabis use in first-episode schizophrenia. Br J Psychiat 2007;190:230-236.
118. Kubicki M, Westin CF, McCarley RW, et al. The application of DTI to investigate white matter abnormalities in schizophrenia. Ann NY Acad Sci 2005;1064:134-148.
119. Smith SM, Jenkinson M, Johansen-Berg H, et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 2006;31:1487-1505.
120. Taveggia C, Thaker P, Petrylak A, et al. Type III neuregulin-1 promotes oligodendrocyte myelination. Glia 2008;56:284-293.
121. Roy K, Murtie JC, El-Khodor BF, et al. Loss of erbB signaling in oligodendrocytes alters myelin and dopaminergic function, a potential mechanism for neuropsychiatric disorders. Proc Natl Acad Sci USA 2007;104:8131-8136.
122. Bellon A, Krebs MO, Jay TM. Factoring neurotrophins into a neurite-based pathophysiological model of schizophrenia. Prog Neurobiol 2011;94:77-90.
123. Bellon A. New genes associated with schizophrenia in neurite formation: a review of cell culture experiments. Mol Psychiat 2007;12:620-629.
124. Kircher T, Krug A, Markov V, et al. Genetic variation in the schizophrenia-risk gene neuregulin 1 correlates with brain activation and impaired speech production in a verbal fluency task in healthy individuals. Hum Brain Mapp 2009;30:3406-3416.
125. Kircher T, Thienel R, Wagner M, et al. Neuregulin 1 ICE-single nucleotide polymorphism in first episode schizophrenia correlates with cerebral activation in fronto-temporal areas. Eur Arch Psychiat Clin Neurosci 2009;259:72-79.
126. Konrad A, Vucurevic G, Musso F, et al. ErbB4 genotype predicts left frontotemporal structural connectivity in human brain. Neuropsychopharmacology 2009;34:641-650.
127. McIntosh AM, Moorhead TW, Job D, et al. The effects of a neuregulin 1 variant on white matter density and integrity. Mol Psychiat 2008;13:1054-1059.
128. Sprooten E, Lymer GK, Munoz Maniega S, et al. The relationship of anterior thalamic radiation integrity to psychosis risk associated neuregulin-1 variants. Mol Psychiat 2009;14:237-238, 3.
129. Wang F, Jiang T, Sun Z, et al. Neuregulin 1 genetic variation and anterior cingulum integrity in patients with schizophrenia and healthy controls. J Psychiat Neurosci 2009;34:181-186.
130. Lawrie SM, Hall J, McIntosh AM, et al. Neuroimaging and molecular genetics of schizophrenia: pathophysiological advances and therapeutic potential. Br J Pharmacol 2008;153 (Suppl 1):S120-S124.
131. McIntosh AM, Baig BJ, Hall J, et al. Relationship of catechol-O-methyltransferase variants to brain structure and function in a population at high risk of psychosis. Biol Psychiat 2007;61:1127-1134.
132. Prata DP, Mechelli A, Fu CH, et al. Epistasis between the DAT 3' UTR VNTR and the COMT Val158Met SNP on cortical function in healthy subjects and patients with schizophrenia. Proc Natl Acad Sci USA 2009;106:13600-13605.
133. Prata DP, Mechelli A, Fu CH, et al. Opposite effects of catechol-O-methyltransferase Val158Met on cortical function in healthy subjects and patients with schizophrenia. Biol Psychiat 2009;65:473-480.
134. Thomason ME, Dougherty RF, Colich NL, et al. COMT genotype affects prefrontal white matter pathways in children and adolescents. Neuroimage 2010;53:926-934.
135. Liu B, Song M, Li J, et al. Prefrontal-related functional connectivities within the default network are modulated by COMT val158met in healthy young adults. J Neurosci 2010;30:64-69.
136. Liu B, Li J, Yu C, et al. Haplotypes of catechol-O-methyltransferase modulate intelligence-related brain white matter integrity. Neuroimage 2010;50:243-249.
137. Ehrlich S, Morrow EM, Roffman JL, et al. The COMT Val108/158Met polymorphism and medial temporal lobe volumetry in patients with schizophrenia and healthy adults. Neuroimage 2010;53:992-1000.
138. Meyer-Lindenberg A, Nichols T, Callicott JH, et al. Impact of complex genetic variation in COMT on human brain function. Mol Psychiat 2006;11:867-877, 797.
139. Henze R, Brunner R, Thiemann U, et al. The Optic Radiation and the Cerebellar Peduncles in Adolescents with First-Admission Schizophrenia-A Diffusion Tensor Imaging Study. J Neuroimaging 2014;24:111-116.