Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-04T21:08:47.726Z Has data issue: false hasContentIssue false

Abnormalities in connectivity of white-matter tracts in patients with familial and non-familial schizophrenia

Published online by Cambridge University Press:  16 December 2010

Q. Wang
Affiliation:
The Psychiatric Laboratory and Department of Psychiatry, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, China
W. Deng
Affiliation:
The Psychiatric Laboratory and Department of Psychiatry, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, China
C. Huang
Affiliation:
The Psychiatric Laboratory and Department of Psychiatry, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, China
M. Li
Affiliation:
The Psychiatric Laboratory and Department of Psychiatry, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, China
X. Ma
Affiliation:
The Psychiatric Laboratory and Department of Psychiatry, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, China
Y. Wang
Affiliation:
The Psychiatric Laboratory and Department of Psychiatry, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, China
L. Jiang
Affiliation:
The Psychiatric Laboratory and Department of Psychiatry, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, China
S. Lui
Affiliation:
Huaxi MR Research Centre, Department of Radiology, West China Hospital, Sichuan University, Chengdu, China
X. Huang
Affiliation:
Huaxi MR Research Centre, Department of Radiology, West China Hospital, Sichuan University, Chengdu, China
S. E. Chua
Affiliation:
Department of Psychiatry, The University of Hong Kong, Pokfulam, S.A.R. China
C. Cheung
Affiliation:
Department of Psychiatry, The University of Hong Kong, Pokfulam, S.A.R. China
G. M. McAlonan
Affiliation:
Department of Psychiatry, The University of Hong Kong, Pokfulam, S.A.R. China
P. C. Sham
Affiliation:
Department of Psychiatry, The University of Hong Kong, Pokfulam, S.A.R. China
R. M. Murray
Affiliation:
Department of Psychological Medicine and Psychiatry, Institute of Psychiatry, King's College London, UK
D. A. Collier
Affiliation:
MRC SGDP Centre, Institute of Psychiatry, King's College London, UK
Q. Gong*
Affiliation:
Huaxi MR Research Centre, Department of Radiology, West China Hospital, Sichuan University, Chengdu, China
T. Li*
Affiliation:
The Psychiatric Laboratory and Department of Psychiatry, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, China Department of Psychological Medicine and Psychiatry, Institute of Psychiatry, King's College London, UK MRC SGDP Centre, Institute of Psychiatry, King's College London, UK
*
*Address for correspondence: Professors Tao Li or Qiyong Gong, 28 Dian Xin Nan Road, West China Hospital, Chengdu, Sichuan, 610041, P.R. China. (Email: [email protected])
*Address for correspondence: Professors Tao Li or Qiyong Gong, 28 Dian Xin Nan Road, West China Hospital, Chengdu, Sichuan, 610041, P.R. China. (Email: [email protected])

Background

Abnormalities in the connectivity of white-matter (WM) tracts in schizophrenia are supported by evidence from post-mortem investigations, functional and structural magnetic resonance imaging (MRI) and diffusion tensor imaging (DTI). The aims of this study were to explore the microstructural changes in first-episode schizophrenia in a Han Chinese population and to investigate whether a family history of psychiatric disorder is related to the severity of WM tract integrity abnormalities in these patients.

Method

T1-weighted MR and DT images were collected in 68 patients with first-episode schizophrenia [22 with a positive family history (PFH) and 46 with a negative family history (NFH)] and 100 healthy controls. Voxel-based analysis was performed and WM integrity was quantified by fractional anisotropy (FA). Cluster- and voxel-level analyses were performed by using two-sample t tests between patients and controls and/or using a full factorial model with one factor and three levels among the three sample groups (patients with PFH or NFH, and controls), as appropriate.

Results

FA deficits were observed in the patient group, especially in the left temporal lobe and right corpus callosum. This effect was more severe in the non-familial schizophrenia than in the familial schizophrenia subgroup.

Conclusions

Overall, these findings support the hypothesis that loss of WM integrity may be an important pathophysiological feature of schizophrenia, with particular implications for brain dysmaturation in non-familial and familial schizophrenia.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Addington, AM, Gornick, MC, Shaw, P, Seal, J, Gogtay, N, Greenstein, D, Clasen, L, Coffey, M, Gochman, P, Long, R, Rapoport, JL (2007). Neuregulin 1 (8p12) and childhood-onset schizophrenia: susceptibility haplotypes for diagnosis and brain developmental trajectories. Molecular Psychiatry 12, 195205.CrossRefGoogle ScholarPubMed
Ardekani, BA, Nierenberg, J, Hoptman, MJ, Javitt, DC, Lim, KO (2003). MRI study of white matter diffusion anisotropy in schizophrenia. Neuroreport 14, 20252029.CrossRefGoogle ScholarPubMed
Ashburner, J, Friston, KJ (2005). Unified segmentation. NeuroImage 26, 839851.CrossRefGoogle ScholarPubMed
Assaf, Y, Pasternak, O (2008). Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. Journal of Molecular Neuroscience 34, 5161.CrossRefGoogle ScholarPubMed
Baare, WF, van Oel, CJ, Hulshoff Pol, HE, Schnack, HG, Durston, S, Sitskoorn, MM, Kahn, RS (2001). Volumes of brain structures in twins discordant for schizophrenia. Archives of General Psychiatry 58, 3340.CrossRefGoogle ScholarPubMed
Bartley, AJ, Jones, DW, Weinberger, DR (1997). Genetic variability of human brain size and cortical gyral patterns. Brain 120, 257269.CrossRefGoogle ScholarPubMed
Bloom, JS, Hynd, GW (2005). The role of the corpus callosum in interhemispheric transfer of information: excitation or inhibition? Neuropsychology Review 15, 5971.CrossRefGoogle ScholarPubMed
Boos, HB, Aleman, A, Cahn, W, Hulshoff Pol, H, Kahn, RS (2007). Brain volumes in relatives of patients with schizophrenia: a meta-analysis. Archives of General Psychiatry 64, 297304.CrossRefGoogle ScholarPubMed
Callicott, JH, Weinberger, DR (1999). Neuropsychiatric dynamics: the study of mental illness using functional magnetic resonance imaging. European Journal of Radiology 30, 95104.CrossRefGoogle Scholar
Cannon, TD, Thompson, PM, van Erp, TG, Toga, AW, Poutanen, VP, Huttunen, M, Lonnqvist, J, Standerskjold-Nordenstam, CG, Narr, KL, Khaledy, M, Zoumalan, CI, Dail, R, Kaprio, J (2002). Cortex mapping reveals regionally specific patterns of genetic and disease-specific gray-matter deficits in twins discordant for schizophrenia. Proceedings of the National Academy of Sciences USA 99, 32283233.CrossRefGoogle ScholarPubMed
Cheung, V, Cheung, C, McAlonan, GM, Deng, Y, Wong, JG, Yip, L, Tai, KS, Khong, PL, Sham, P, Chua, SE (2008). A diffusion tensor imaging study of structural dysconnectivity in never-medicated, first-episode schizophrenia. Psychological Medicine 38, 877885.CrossRefGoogle ScholarPubMed
Cheung, V, Chiu, CPY, Law, CW, Cheung, C, Hui, CLM, Chan, KKS, Sham, PC, Deng, MY, Tai, KS, Khong, Pl, McAlonan, GM, Chua, SE, Chen, E (2010). Positive symptoms and white matter microstructure in never-medicated first-episode schizophrenia. Psychological Medicine. Published online: 1 September 2010. doi:10.1017/S003329171000156X.Google Scholar
DeLisi, LE (2001). Speech disorder in schizophrenia: review of the literature and exploration of its relation to the uniquely human capacity for language. Schizophrenia Bulletin 27, 481496.CrossRefGoogle Scholar
DeLisi, LE, Dauphinais, ID, Gershon, ES (1988). Perinatal complications and reduced size of brain limbic structures in familial schizophrenia. Schizophrenia Bulletin 14, 185191.CrossRefGoogle ScholarPubMed
Firbank, MJ, Harrison, RM, Williams, ED, Coulthard, A (2000). Quality assurance for MRI: practical experience. British Journal of Radiology 73, 376383.CrossRefGoogle ScholarPubMed
Friston, KJ (1998). The disconnection hypothesis. Schizophrenia Research 30, 115125.CrossRefGoogle ScholarPubMed
Friston, KJ, Frith, CD (1995). Schizophrenia: a disconnection syndrome? Clinical Neuroscience 3, 8997.Google ScholarPubMed
Gasparotti, R, Valsecchi, P, Carletti, F, Galluzzo, A, Liserre, R, Cesana, B, Sacchetti, E (2009). Reduced fractional anisotropy of corpus callosum in first-contact, antipsychotic drug-naive patients with schizophrenia. Schizophrenia Research 108, 4148.CrossRefGoogle ScholarPubMed
Gogtay, N, Sporn, A, Clasen, LS, Greenstein, D, Giedd, JN, Lenane, M, Gochman, PA, Zijdenbos, A, Rapoport, JL (2003). Structural brain MRI abnormalities in healthy siblings of patients with childhood-onset schizophrenia. American Journal of Psychiatry 160, 569571.CrossRefGoogle ScholarPubMed
Goldman, AL, Pezawas, L, Mattay, VS, Fischl, B, Verchinski, BA, Zoltick, B, Weinberger, DR, Meyer-Lindenberg, A (2008). Heritability of brain morphology related to schizophrenia: a large-scale automated magnetic resonance imaging segmentation study. Biological Psychiatry 63, 475483.CrossRefGoogle ScholarPubMed
Gottesman, II, Gould, TD (2003). The endophenotype concept in psychiatry: etymology and strategic intentions. American Journal of Psychiatry 160, 636645.CrossRefGoogle ScholarPubMed
Green, MF, Olivier, B, Crawley, JN, Penn, DL, Silverstein, S (2005). Social cognition in schizophrenia: recommendations from the Measurement and Treatment Research to Improve Cognition in Schizophrenia New Approaches Conference. Schizophrenia Bulletin 31, 882887.CrossRefGoogle ScholarPubMed
Hall, RC (1995). Global assessment of functioning. A modified scale. Psychosomatics 36, 267275.CrossRefGoogle ScholarPubMed
Harrison, PJ (1999). The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain 122, 593624.CrossRefGoogle ScholarPubMed
Harrison, PJ (2004). The hippocampus in schizophrenia: a review of the neuropathological evidence and its pathophysiological implications. Psychopharmacology (Berlin) 174, 151162.CrossRefGoogle ScholarPubMed
Harrison, PJ, Weinberger, DR (2005). Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Molecular Psychiatry 10, 4068.CrossRefGoogle ScholarPubMed
Ho, BC (2007). MRI brain volume abnormalities in young, nonpsychotic relatives of schizophrenia probands are associated with subsequent prodromal symptoms. Schizophrenia Research 96, 113.CrossRefGoogle ScholarPubMed
Hof, PR, Haroutunian, V, Friedrich, VL Jr., Byne, W, Buitron, C, Perl, DP, Davis, KL (2003). Loss and altered spatial distribution of oligodendrocytes in the superior frontal gyrus in schizophrenia. Biological Psychiatry 53, 10751085.CrossRefGoogle ScholarPubMed
Honea, RA, Meyer-Lindenberg, A, Hobbs, KB, Pezawas, L, Mattay, VS, Egan, MF, Verchinski, B, Passingham, RE, Weinberger, DR, Callicott, JH (2008). Is gray matter volume an intermediate phenotype for schizophrenia? A voxel-based morphometry study of patients with schizophrenia and their healthy siblings. Biological Psychiatry 63, 465474.CrossRefGoogle ScholarPubMed
Hulshoff Pol, HE, Schnack, HG, Mandl, RC, Brans, RG, van Haren, NE, Baare, WF, van Oel, CJ, Collins, DL, Evans, AC, Kahn, RS (2006 a). Gray and white matter density changes in monozygotic and same-sex dizygotic twins discordant for schizophrenia using voxel-based morphometry. NeuroImage 31, 482488.CrossRefGoogle ScholarPubMed
Hulshoff Pol, HE, Schnack, HG, Mandl, RC, Cahn, W, Collins, DL, Evans, AC, Kahn, RS (2004). Focal white matter density changes in schizophrenia: reduced inter-hemispheric connectivity. NeuroImage 21, 2735.CrossRefGoogle ScholarPubMed
Hulshoff Pol, HE, Schnack, HG, Posthuma, D, Mandl, RC, Baare, WF, van Oel, C, van Haren, NE, Collins, DL, Evans, AC, Amunts, K, Burgel, U, Zilles, K, de Geus, E, Boomsma, DI, Kahn, RS (2006 b). Genetic contributions to human brain morphology and intelligence. Journal of Neuroscience 26, 1023510242.CrossRefGoogle ScholarPubMed
Jia, Z, Huang, X, Wu, Q, Zhang, T, Lui, S, Zhang, J, Amatya, N, Kuang, W, Chan, RC, Kemp, GJ, Mechelli, A, Gong, Q (2010). High-field magnetic resonance imaging of suicidality in patients with major depressive disorder. American Journal of Psychiatry 167, 13811390.CrossRefGoogle ScholarPubMed
Job, DE, Whalley, HC, Johnstone, EC, Lawrie, SM (2005). Grey matter changes over time in high risk subjects developing schizophrenia. NeuroImage 25, 10231030.CrossRefGoogle ScholarPubMed
Job, DE, Whalley, HC, McConnell, S, Glabus, M, Johnstone, EC, Lawrie, SM (2003). Voxel-based morphometry of grey matter densities in subjects at high risk of schizophrenia. Schizophrenia Research 64, 113.CrossRefGoogle ScholarPubMed
Job, DE, Whalley, HC, McIntosh, AM, Owens, DG, Johnstone, EC, Lawrie, SM (2006). Grey matter changes can improve the prediction of schizophrenia in subjects at high risk. BMC Medicine 4, 29.CrossRefGoogle ScholarPubMed
Kanaan, RAA, Kim, J-S, Kaufmann, WE, Pearlson, GD, Barker, GJ, McGuire, PK (2005). Diffusion tensor imaging in schizophrenia. Biological Psychiatry 58, 921929.CrossRefGoogle ScholarPubMed
Karlsgodt, KH, van Erp, TGM, Poldrack, RA, Bearden, CE, Nuechterlein, KH, Cannon, TD (2008). Diffusion tensor imaging of the superior longitudinal fasciculus and working memory in recent-onset schizophrenia. Biological Psychiatry 63, 512518.CrossRefGoogle ScholarPubMed
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261276.CrossRefGoogle ScholarPubMed
Ke, X, Tang, T, Hong, S, Hang, Y, Zou, B, Li, H, Zhou, Z, Ruan, Z, Lu, Z, Tao, G (2009). White matter impairments in autism, evidence from voxel-based morphometry and diffusion tensor imaging. Brain Research 1265, 171177.CrossRefGoogle ScholarPubMed
Kim, DI, Mathalon, DH, Ford, JM, Mannell, M, Turner, JA, Brown, GG, Belger, A, Gollub, R, Lauriello, J, Wible, C, O'Leary, D, Lim, K, Toga, A, Potkin, SG, Birn, F, Calhoun, VD (2009). Auditory oddball deficits in schizophrenia: an independent component analysis of the fMRI multisite function BIRN study. Schizophrenia Bulletin 35, 6781.CrossRefGoogle ScholarPubMed
Koolschijn, PC, van Haren, NE, Hulshoff Pol, HE, Kahn, RS (2008). Hypothalamus volume in twin pairs discordant for schizophrenia. European Neuropsychopharmacology 18, 312315.CrossRefGoogle ScholarPubMed
Kubicki, M, McCarley, R, Westin, C-F, Park, H-J, Maier, S, Kikinis, R, Jolesz, FA, Shenton, ME (2007). A review of diffusion tensor imaging studies in schizophrenia. Journal of Psychiatric Research 41, 1530.CrossRefGoogle ScholarPubMed
Kubicki, M, Shenton, ME, Salisbury, DF, Hirayasu, Y, Kasai, K, Kikinis, R, Jolesz, FA, McCarley, RW (2002 a). Voxel-based morphometric analysis of gray matter in first episode schizophrenia. NeuroImage 17, 17111719.CrossRefGoogle ScholarPubMed
Kubicki, M, Westin, CF, Maier, SE, Frumin, M, Nestor, PG, Salisbury, DF, Kikinis, R, Jolesz, FA, McCarley, RW, Shenton, ME (2002 b). Uncinate fasciculus findings in schizophrenia: a magnetic resonance diffusion tensor imaging study. American Journal of Psychiatry 159, 813820.CrossRefGoogle ScholarPubMed
Kubicki, M, Westin, CF, McCarley, RW, Shenton, ME (2005). The application of DTI to investigate white matter abnormalities in schizophrenia. Annals of the New York Academy of Sciences 1064, 134148.CrossRefGoogle ScholarPubMed
Kubicki, M, Westin, CF, Nestor, PG, Wible, CG, Frumin, M, Maier, SE, Kikinis, R, Jolesz, FA, McCarley, RW, Shenton, ME (2003). Cingulate fasciculus integrity disruption in schizophrenia: a magnetic resonance diffusion tensor imaging study. Biological Psychiatry 54, 11711180.CrossRefGoogle ScholarPubMed
Lawrie, SM, Buechel, C, Whalley, HC, Frith, CD, Friston, KJ, Johnstone, EC (2002). Reduced frontotemporal functional connectivity in schizophrenia associated with auditory hallucinations. Biological Psychiatry 51, 10081011.CrossRefGoogle ScholarPubMed
Lee, K, Yoshida, T, Kubicki, M, Bouix, S, Westin, CF, Kindlmann, G, Niznikiewicz, M, Cohen, A, McCarley, RW, Shenton, ME (2009). Increased diffusivity in superior temporal gyrus in patients with schizophrenia: a diffusion tensor imaging study. Schizophrenia Research 108, 3340.CrossRefGoogle ScholarPubMed
Lim, KO, Hedehus, M, Moseley, M, de Crespigny, A, Sullivan, EV, Pfefferbaum, A (1999). Compromised white matter tract integrity in schizophrenia inferred from diffusion tensor imaging. Archives of General Psychiatry 56, 367374.CrossRefGoogle ScholarPubMed
Liu, Y, Liang, M, Zhou, Y, He, Y, Hao, Y, Song, M, Yu, C, Liu, H, Liu, Z, Jiang, T (2008). Disrupted small-world networks in schizophrenia. Brain 131, 945961.CrossRefGoogle ScholarPubMed
McDonald, C, Marshall, N, Sham, PC, Bullmore, ET, Schulze, K, Chapple, B, Bramon, E, Filbey, F, Quraishi, S, Walshe, M, Murray, RM (2006). Regional brain morphometry in patients with schizophrenia or bipolar disorder and their unaffected relatives. American Journal of Psychiatry 163, 478487.CrossRefGoogle ScholarPubMed
Minami, T, Nobuhara, K, Okugawa, G, Takase, K, Yoshida, T, Sawada, S, Ha-Kawa, S, Ikeda, K, Kinoshita, T (2003). Diffusion tensor magnetic resonance imaging of disruption of regional white matter in schizophrenia. Neuropsychobiology 47, 141145.CrossRefGoogle ScholarPubMed
Narr, KL, Hageman, N, Woods, RP, Hamilton, LS, Clark, K, Phillips, O, Shattuck, DW, Asarnow, RF, Toga, AW, Nuechterlein, KH (2009). Mean diffusivity: a biomarker for CSF-related disease and genetic liability effects in schizophrenia. Psychiatry Research 171, 2032.CrossRefGoogle ScholarPubMed
Narr, KL, Thompson, PM, Szeszko, P, Robinson, D, Jang, S, Woods, RP, Kim, S, Hayashi, KM, Asunction, D, Toga, AW, Bilder, RM (2004). Regional specificity of hippocampal volume reductions in first-episode schizophrenia. NeuroImage 21, 15631575.CrossRefGoogle ScholarPubMed
Phillips, OR, Nuechterlein, KH, Clark, KA, Hamilton, LS, Asarnow, RF, Hageman, NS, Toga, AW, Narr, KL (2009). Fiber tractography reveals disruption of temporal lobe white matter tracts in schizophrenia. Schizophrenia Research 107, 3038.CrossRefGoogle ScholarPubMed
Price, G, Bagary, MS, Cercignani, M, Altmann, DR, Ron, MA (2005). The corpus callosum in first episode schizophrenia: a diffusion tensor imaging study. Journal of Neurology, Neurosurgery, and Psychiatry 76, 585587.CrossRefGoogle ScholarPubMed
Rabinowicz, EF, Silipo, G, Goldman, R, Javitt, DC (2000). Auditory sensory dysfunction in schizophrenia: imprecision or distractibility? Archives of General Psychiatry 57, 11491155.CrossRefGoogle ScholarPubMed
Ridgway, GR, Omar, R, Ourselin, S, Hill, DL, Warren, JD, Fox, NC (2009). Issues with threshold masking in voxel-based morphometry of atrophied brains. Neuroimage 44, 99111.CrossRefGoogle ScholarPubMed
Rijsdijk, FV, van Haren, NE, Picchioni, MM, McDonald, C, Toulopoulou, T, Hulshoff Pol, HE, Kahn, RS, Murray, R, Sham, PC (2005). Brain MRI abnormalities in schizophrenia: same genes or same environment? Psychological Medicine 35, 13991409.CrossRefGoogle ScholarPubMed
Rotarska-Jagiela, A, Schonmeyer, R, Oertel, V, Haenschel, C, Vogeley, K, Linden, DE (2008). The corpus callosum in schizophrenia – volume and connectivity changes affect specific regions. NeuroImage 39, 15221532.CrossRefGoogle ScholarPubMed
Schneider, F, Habel, U, Reske, M, Kellermann, T, Stocker, T, Shah, NJ, Zilles, K, Braus, DF, Schmitt, A, Schlosser, R, Wagner, M, Frommann, I, Kircher, T, Rapp, A, Meisenzahl, E, Ufer, S, Ruhrmann, S, Thienel, R, Sauer, H, Henn, FA, Gaebel, W (2007). Neural correlates of working memory dysfunction in first-episode schizophrenia patients: an fMRI multi-center study. Schizophrenia Research 89, 198210.CrossRefGoogle ScholarPubMed
Schulze, K, McDonald, C, Frangou, S, Sham, P, Grech, A, Toulopoulou, T, Walshe, M, Sharma, T, Sigmundsson, T, Taylor, M, Murray, RM (2003). Hippocampal volume in familial and nonfamilial schizophrenic probands and their unaffected relatives. Biological Psychiatry 53, 562570.CrossRefGoogle ScholarPubMed
Shenton, ME, Dickey, CC, Frumin, M, McCarley, RW (2001). A review of MRI findings in schizophrenia. Schizophrenia Research 49, 152.CrossRefGoogle ScholarPubMed
Steel, RM, Bastin, ME, McConnell, S, Marshall, I, Cunningham-Owens, DG, Lawrie, SM, Johnstone, EC, Best, JJ (2001). Diffusion tensor imaging (DTI) and proton magnetic resonance spectroscopy (1H MRS) in schizophrenic subjects and normal controls. Psychiatry Research 106, 161170.CrossRefGoogle ScholarPubMed
Sun, Z, Wang, F, Cui, L, Breeze, J, Du, X, Wang, X, Cong, Z, Zhang, H, Li, B, Hong, N, Zhang, D (2003). Abnormal anterior cingulum in patients with schizophrenia: a diffusion tensor imaging study. Neuroreport 14, 18331836.CrossRefGoogle ScholarPubMed
Thompson, PM, Vidal, C, Giedd, JN, Gochman, P, Blumenthal, J, Nicolson, R, Toga, AW, Rapoport, JL (2001). Mapping adolescent brain change reveals dynamic wave of accelerated gray matter loss in very early-onset schizophrenia. Proceedings of the National Academy of Sciences USA 98, 1165011655.CrossRefGoogle ScholarPubMed
Van Erp, TG, Saleh, PA, Rosso, IM, Huttunen, M, Lonnqvist, J, Pirkola, T, Salonen, O, Valanne, L, Poutanen, VP, Standertskjold-Nordenstam, CG, Cannon, TD (2002). Contributions of genetic risk and fetal hypoxia to hippocampal volume in patients with schizophrenia or schizoaffective disorder, their unaffected siblings, and healthy unrelated volunteers. American Journal of Psychiatry 159, 15141520.CrossRefGoogle ScholarPubMed
Wang, F, Sun, Z, Cui, L, Du, X, Wang, X, Zhang, H, Cong, Z, Hong, N, Zhang, D (2004). Anterior cingulum abnormalities in male patients with schizophrenia determined through diffusion tensor imaging. American Journal of Psychiatry 161, 573575.CrossRefGoogle ScholarPubMed
Wang, F, Sun, Z, Du, X, Wang, X, Cong, Z, Zhang, H, Zhang, D, Hong, N (2003). A diffusion tensor imaging study of middle and superior cerebellar peduncle in male patients with schizophrenia. Neuroscience Letters 348, 135138.CrossRefGoogle ScholarPubMed
Winterer, G, Konrad, A, Vucurevic, G, Musso, F, Stoeter, P, Dahmen, N (2008). Association of 5′ end neuregulin-1 (NRG1) gene variation with subcortical medial frontal microstructure in humans. NeuroImage 40, 712718.CrossRefGoogle ScholarPubMed
Wood, SJ, Yucel, M, Velakoulis, D, Phillips, LJ, Yung, AR, Brewer, W, McGorry, PD, Pantelis, C (2005). Hippocampal and anterior cingulate morphology in subjects at ultra-high-risk for psychosis: the role of family history of psychotic illness. Schizophrenia Research 75, 295301.CrossRefGoogle ScholarPubMed
Xu, B, Roos, JL, Levy, S, van Rensburg, EJ, Gogos, JA, Karayiorgou, M (2008). Strong association of de novo copy number mutations with sporadic schizophrenia. Nature Genetics 40, 880885.CrossRefGoogle ScholarPubMed
Yamada, M, Hirao, K, Namiki, C, Hanakawa, T, Fukuyama, H, Hayashi, T, Murai, T (2007). Social cognition and frontal lobe pathology in schizophrenia: a voxel-based morphometric study. NeuroImage 35, 292298.CrossRefGoogle ScholarPubMed