Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-11T14:49:20.020Z Has data issue: false hasContentIssue false

Distinct white-matter aberrations in 22q11.2 deletion syndrome and patients at ultra-high risk for psychosis

Published online by Cambridge University Press:  19 May 2016

G. Bakker*
Affiliation:
Department of Psychiatry & Psychology, University of Maastricht, The Netherlands Department of Nuclear Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
M. W. A. Caan
Affiliation:
Department of Radiology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
R. S. Schluter
Affiliation:
Department of Radiology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
O. J. N Bloemen
Affiliation:
Department of Psychiatry & Psychology, University of Maastricht, The Netherlands GGZ Centraal, Center for Mental Health Care Innova, Amersfoort, The Netherlands
F. da Silva- Alves
Affiliation:
Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
M. B. de Koning
Affiliation:
Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands Arkin Mental Health Care, Amsterdam, The Netherlands
E. Boot
Affiliation:
Department of Nuclear Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands The Dalglish Family Hearts and Minds Clinic for Adults with 22q11.2 Deletion Syndrome, Toronto, Ontario, Canada
W. A. M. Vingerhoets
Affiliation:
Department of Psychiatry & Psychology, University of Maastricht, The Netherlands Department of Nuclear Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
D. H. Nieman
Affiliation:
Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
L. de Haan
Affiliation:
Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
J. Booij
Affiliation:
Department of Nuclear Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
T. A. M. J. van Amelsvoort
Affiliation:
Department of Psychiatry & Psychology, University of Maastricht, The Netherlands
*
*Address for correspondence: G. Bakker, MSc, Department of Psychiatry and Psychology, Maastricht University, P.O. Box 616 (Vijv-SN2), 6200 MD Maastricht, The Netherlands. (Email: geor.bakker@maastrichtuniversity.nl)

Abstract

Background

Patients with a deletion at chromosome 22q11.2 (22q11DS) have 30% lifetime risk of developing a psychosis. People fulfilling clinical criteria for ultra-high risk (UHR) for psychosis have 30% risk of developing a psychosis within 2 years. Both high-risk groups show white-matter (WM) abnormalities in microstructure and volume compared to healthy controls (HC), which have been related to psychotic symptoms. Comparisons of WM pathology between these two groups may specify WM markers related to genetic and clinical risk factors.

Method

Fractional anisotropy (FA), axial diffusivity (AD), radial diffusivity (RD) and mean diffusivity (MD) were assessed using diffusion tensor magnetic resonance imaging (MRI), and WM volume with structural MRI, in 23 UHR patients, 21 22q11DS patients, and 33 HC.

Results

Compared to UHR patients 22q11DS patients had (1) lower AD and RD in corpus callosum (CC), cortical fasciculi, and anterior thalamic radiation (ATR), (2) higher FA in CC and ATR, and (3) lower occipital and superior temporal gyrus WM volume. Compared to HC, 22q11DS patients had (1) lower AD and RD throughout cortical fasciculi and (2) higher FA in ATR, CC and inferior fronto-occipital fasciculus. Compared to HC, UHR patients had (1) higher mean MD, RD, and AD in CC, ATR and cortical fasciculi, (2) no differences in FA.

Conclusions

UHR and 22q11DS patients share a susceptibility for developing psychosis yet were characterized by distinct patterns of WM alterations relative to HC. While UHR patients were typified by signs suggestive of aberrant myelination, 22q11DS subjects showed signs suggestive of lower axonal integrity.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2016 

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

Ashburner, J (2007). A fast diffeomorphic image registration algorithm. NeuroImage 38, 95113.Google Scholar
Bakiri, Y, Burzomato, V, Frugier, G, Hamilton, NB, Káradóttir, R, Attwell, D (2009). Glutamatergic signaling in the brain's white matter. Neuroscience 158, 266274.Google Scholar
Barazany, D, Basser, PJ, Assaf, Y (2009). In vivo measurement of axon diameter distribution in the corpus callosum of rat brain. Brain 132, 12101220.CrossRefGoogle ScholarPubMed
Beaulieu, C (2002). The basis of anisotropic water diffusion in the nervous system - a technical review. NMR in Biomedicine 15, 435455.Google Scholar
Bloemen, OJN, de Koning, MB, Schmitz, N, Nieman, DH, Becker, HE, de Haan, L, Dingemans, P, Linszen, DH, van Amelsvoort, Ta MJ (2010). White-matter markers for psychosis in a prospective ultra-high-risk cohort. Psychological Medicine 40, 12971304.Google Scholar
Boot, E, van Amelsvoort, Ta MJ (2012). Neuroimaging correlates of 22q11.2 deletion syndrome: implications for schizophrenia research. Current Topics in Medicinal Chemistry 12, 23032313.Google Scholar
Braskie, MN, Jahanshad, N, Toga, AW, McMahon, KL, de Zubicaray, GI, Martin, NG, Wright, MJ, Thompson, PM (2012). How a common variant in the growth factor receptor gene, NTRK1, affects white matter. Bioarchitecture 2, 181184.Google Scholar
Caan, MWA, Khedoe, G, Poot, D, den Dekker, A, Olabarriaga, S, Grimbergen, K, van Vliet, L, Vos, F (2010). Adaptive noise filtering for accurate and precise diffusion estimation in fiber crossings. Medical Image Computing and Computer-Assisted Intervention 13, 167174.Google Scholar
Carletti, F, Woolley, JB, Bhattacharyya, S, Perez-Iglesias, R, Fusar Poli, P, Valmaggia, L, Broome, MR, Bramon, E, Johns, L, Giampietro, V, Williams, SCR, Barker, GJ, McGuire, PK (2012). Alterations in white matter evident before the onset of psychosis. Schizophrenia Bulletin 38, 11701179.Google Scholar
Cavanna, AE, Trimble, MR (2006). The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129, 564583.CrossRefGoogle ScholarPubMed
Chaddock, C, Lee, L, Newton, J, Baldeweg, T, Frackwoiak, R, Skuse, D (2006). A combined VBM and DTI investigation of brain structure and connectivity in 22q11 Deletion Syndrome. Proceedings of the International Society for Magnetic Resonance in Medicine 14, 3445.Google Scholar
Clemm von Hohenberg, C, Pasternak, O, Kubicki, M, Ballinger, T, Vu, M-A., Swisher, T, Green, K, Giwerc, M, Dahlben, B, Goldstein, JM, Woo, T-UW, Petryshen, TL, Mesholam-Gately, RI, Woodberry, Ka., Thermenos, HW, Mulert, C, McCarley, RW, Seidman, LJ, Shenton, ME (2013). White matter microstructure in individuals at clinical high risk of psychosis: a whole-brain diffusion tensor imaging study. Schizophrenia Bulletin 40, 895903.Google Scholar
Colpak, AI, Kurne, AT, Oguz, KK, Has, AC, Dolgun, A, Kansu, T (2015). White matter involvement beyond the optic nerves in CRION as assessed by diffusion tensor imaging. International Journal of Neuroscience 125, 1017.CrossRefGoogle ScholarPubMed
Da Silva Alves, F, Schmitz, N, Bloemen, O, van der Meer, J, Meijer, J, Boot, E, Nederveen, A, de Haan, L, Linszen, D, van Amelsvoort, T (2011). White matter abnormalities in adults with 22q11 deletion syndrome with and without schizophrenia. Schizophrenia Research 132, 7583.Google Scholar
Díaz-Caneja, CM, Pina-Camacho, L, Rodríguez-Quiroga, A, Fraguas, D, Parellada, M, Arango, C (2015). Predictors of outcome in early-onset psychosis: a systematic review. Schizophrenia 1, 14005.Google Scholar
Fournier, AE, Gould, GC, Liu, BP, Strittmatter, SM (2002). Truncated soluble Nogo receptor binds Nogo-66 and blocks inhibition of axon growth by myelin. Journal of Neuroscience 22, 88768883.Google Scholar
Fournier, AE, GrandPre, T, Strittmatter, SM (2001). Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409, 341346.CrossRefGoogle ScholarPubMed
Fusar-Poli, P, Borgwardt, S, Bechdolf, A, Addington, J, Riecher-Rössler, A, Schultze-Lutter, F, Keshavan, M, Wood, S, Ruhrmann, S, Seidman, LJ, Valmaggia, L, Cannon, T, Velthorst, E, De Haan, L, Cornblatt, B, Bonoldi, I, Birchwood, M, McGlashan, T, Carpenter, W, McGorry, P, Klosterkötter, J, McGuire, P, Yung, A (2013). The psychosis high-risk state: a comprehensive state-of-the-art review. JAMA Psychiatry 70, 107120.Google Scholar
Fusar-Poli, P, Crossley, N, Woolley, J, Carletti, F, Perez-Iglesias, R, Broome, M, Johns, L, Tabraham, P, Bramon, E, McGuire, P (2011). White matter alterations related to P300 abnormalities in individuals at high risk for psychosis: an MRI-EEG study. Journal of Psychiatry & Neuroscience 36, 239248.CrossRefGoogle ScholarPubMed
Gee, DG, Cannon, TD (2011). Prediction of conversion to psychosis: review and future directions. Revista brasileira de psiquiatria 33 (Suppl. 2), s129s42.CrossRefGoogle ScholarPubMed
Ghosh, S, Basu, A, Kumaran, SS, Khushu, S (2010). Functional mapping of language networks in the normal brain using a word-association task. Indian Journal of Radiology & Imaging 20, 182187.Google Scholar
Gothelf, D, Feinstein, C, Thompson, T, Gu, E, Penniman, L, Van Stone, E, Kwon, H, Eliez, S, Reiss, AL (2007). Risk factors for the emergence of psychotic disorders in adolescents with 22q11.2 deletion syndrome. American Journal of Psychiatry 164, 663669.CrossRefGoogle ScholarPubMed
Haijma, SV, Van Haren, N, Cahn, W, Koolschijn, PCMP, Hulshoff Pol, HE, Kahn, RS (2013). Brain volumes in schizophrenia: a meta-analysis in over 18 000 subjects. Schizophrenia Bulletin 39, 11291138.Google Scholar
Harsan, LA, Poulet, P, Guignard, B, Steibel, J, Parizel, N, de Sousa, PL, Boehm, N, Grucker, D, Ghandour, MS (2006). Brain dysmyelination and recovery assessment by noninvasive in vivo diffusion tensor magnetic resonance imaging. Journal of Neuroscience Research 83, 392402.Google Scholar
Henry, JC, van Amelsvoort, T, Morris, RG, Owen, MJ, Murphy, DGM, Murphy, KC (2002). An investigation of the neuropsychological profile in adults with velo-cardio-facial syndrome (VCFS). Neuropsychologia 40, 471478.Google Scholar
Hua, K, Zhang, J, Wakana, S, Jiang, H, Li, X, Reich, DS, Calabresi, Pa, Pekar, JJ, van Zijl, PCM, Mori, S (2008). Tract probability maps in stereotaxic spaces: analyses of white matter anatomy and tract-specific quantification. NeuroImage 39, 336347.CrossRefGoogle ScholarPubMed
Jalbrzikowski, M, Villalon-Reina, JE, Karlsgodt, KH, Senturk, D, Chow, C, Thompson, PM, Bearden, CE (2014). Altered white matter microstructure is associated with social cognition and psychotic symptoms in 22q11.2 microdeletion syndrome. Frontiers in Behavioral Neuroscience 8, 393.Google Scholar
Jung, WH, Jang, JH, Byun, MS, An, SK, Kwon, JS (2010). Structural brain alterations in individuals at ultra-high risk for psychosis: a review of magnetic resonance imaging studies and future directions. Journal of Korean Medical Science 25, 17001709.Google Scholar
Karlsgodt, KH, Niendam, TA, Bearden, CE, Cannon, TD (2009). White matter integrity and prediction of social and role functioning in subjects at ultra-high risk for psychosis. Biological Psychiatry 66, 562569.CrossRefGoogle ScholarPubMed
Kates, WR, Antshel, KM, Faraone, SV, Fremont, WP, Higgins, AM, Shprintzen, RJ, Botti, J-A, Kelchner, L, McCarthy, C (2011). Neuroanatomic predictors to prodromal psychosis in velocardiofacial syndrome (22q11.2 deletion syndrome): a longitudinal study. Biological Psychiatry 69, 945952.Google Scholar
Kates, WR, Olszewski, AK, Gnirke, MH, Kikinis, Z, Nelson, J, Antshel, KM, Fremont, W, Radoeva, PD, Middleton, FA, Shenton, ME, Coman, IL (2015). White matter microstructural abnormalities of the cingulum bundle in youths with 22q11.2 deletion syndrome: associations with medication, neuropsychological function, and prodromal symptoms of psychosis. Schizophrenia Research 161, 7684.Google Scholar
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261276.Google Scholar
Kikinis, Z, Asami, T, Bouix, S, Finn, CT, Ballinger, T, Tworog-Dube, E, Kucherlapati, R, Kikinis, R, Shenton, ME, Kubicki, M (2012). Reduced fractional anisotropy and axial diffusivity in white matter in 22q11.2 deletion syndrome: a pilot study. Schizophrenia Research 141, 3539.Google Scholar
Kubicki, M, Carley, RW, Shenton, ME (2012). Evidence for white matter abnormalities in schizophrenia. Current Opinion Psychiatry 29, 9971003.Google Scholar
Maynard, TM, Haskell, GT, Lieberman, JA, LaMantia, A-S (2002). 22q11 DS: genomic mechanisms and gene function in DiGeorge/velocardiofacial syndrome. International Journal of Developmental Neuroscience 20, 407419.Google Scholar
Maynard, TM, Haskell, GT, Peters, AZ, Sikich, L, Lieberman, JA, LaMantia, A-S (2003). A comprehensive analysis of 22q11 gene expression in the developing and adult brain. Proceedings of the National Academy of Sciences USA 100, 1443314438.Google Scholar
Meechan, DW, Tucker, ES, Maynard, TM, LaMantia, A-S (2012). Cxcr4 regulation of interneuron migration is disrupted in 22q11.2 deletion syndrome. Proceedings of the National Academy of Sciences USA 109, 1860118606.Google Scholar
Miller, TJ, McGlashan, TH, Rosen, JL, Cadenhead, K, Cannon, T, Ventura, J, McFarlane, W, Perkins, DO, Pearlson, GD, Woods, SW (2003). Prodromal assessment with the structured interview for prodromal syndromes and the scale of prodromal symptoms: predictive validity, interrater reliability, and training to reliability. Schizophrenia Bulletin 29, 703715.CrossRefGoogle ScholarPubMed
Mitelman, SA, Brickman, AM, Shihabuddin, L, Newmark, RE, Hazlett, EA, Haznedar, MM, Buchsbaum, MS (2007). A comprehensive assessment of gray and white matter volumes and their relationship to outcome and severity in schizophrenia. NeuroImage 37, 449462.Google Scholar
Mitelman, SA, Shihabuddin, L, Brickman, AM, Hazlett, EA, Buchsbaum, MS (2003). MRI assessment of gray and white matter distribution in Brodmann's areas of the cortex in patients with schizophrenia with good and poor outcomes. American Journal of Psychiatry 160, 21542168.Google Scholar
Mondelli, V, Cattaneo, A, Belvederi Murri, M, Di Forti, M, Handley, R, Hepgul, N, Miorelli, A, Navari, S, Papadopoulos, AS, Aitchison, KJ, Morgan, C, Murray, RM, Dazzan, P, Pariante, CM (2011). Stress and inflammation reduce brain-derived neurotrophic factor expression in first-episode psychosis: a pathway to smaller hippocampal volume. Journal of Clinical Psychiatry 72, 16771684.Google Scholar
Mori, S, Wakana, S, van Zijl, PCM, Nagae-Poetscher, LM (2005). MRI Atlas of Human White Matter. Elsevier.Google Scholar
Murphy, KC, Jones, La, Owen, MJ (1999). High rates of schizophrenia in adults with velo-cardio-facial syndrome. Archives of General Psychiatry 56, 940945.Google Scholar
Nakamura, K, Kawasaki, Y, Takahashi, T, Furuichi, A, Noguchi, K, Seto, H, Suzuki, M (2012). Reduced white matter fractional anisotropy and clinical symptoms in schizophrenia: a voxel-based diffusion tensor imaging study. Psychiatry Research 202, 233238.Google Scholar
Nichols, TE, Holmes, AP (2002). Nonparametric permutation tests for functional neuroimaging: a primer with examples. Human Brain Mapping 15, 125.Google Scholar
Paus, T (2010). Growth of white matter in the adolescent brain: myelin or axon? Brain and Cognition 72, 2635.CrossRefGoogle ScholarPubMed
Paus, T, Pesaresi, M, French, L (2014). White matter as a transport system. Neuroscience 276, 117125.Google Scholar
Perlstein, MD, Chohan, MR, Coman, IL, Antshel, KM, Fremont, WP, Gnirke, MH, Kikinis, Z, Middleton, FA, Radoeva, PD, Shenton, ME, Kates, WR (2014). White matter abnormalities in 22q11.2 deletion syndrome: preliminary associations with the Nogo-66 receptor gene and symptoms of psychosis. Schizophrenia Research 152, 117123.Google Scholar
Peters, BD, de Haan, L, Dekker, N, Blaas, J, Becker, HE, Dingemans, PM, Akkerman, EM, Majoie, CB, van Amelsvoort, T, den Heeten, GJ, Linszen, DH (2008). White matter fibertracking in first-episode schizophrenia, schizoaffective patients and subjects at ultra-high risk of psychosis. Neuropsychobiology 58, 1928.Google Scholar
Peters, BD, Dingemans, PM, Dekker, N, Blaas, J, Akkerman, E, Van Amelsvoort, TA, Majoie, CB, Den Heeten, GJ, Linszen, DH, De Haan, L (2010). White matter connectivity and psychosis in ultra-high-risk subjects: a diffusion tensor fiber tracking study. Psychiatry Research 181, 4450.Google Scholar
Peters, BD, Ikuta, T, Derosse, P, John, M, Burdick, KE, Gruner, P, Prendergast, DM, Szeszko, PR, Malhotra, AK (2014). Age-related differences in white matter tract microstructure are associated with cognitive performance from childhood to adulthood. Biological Psychiatry 75, 248256.CrossRefGoogle ScholarPubMed
Peters, BD, Karlsgodt, KH (2014). White matter development in the early stages of psychosis. Schizophrenia Research 161, 6169.Google Scholar
Peters, BD, Schmitz, N, Dingemans, PM, van Amelsvoort, TA, Linszen, DH, de Haan, L, Majoie, CB, den Heeten, GJ (2009). Preliminary evidence for reduced frontal white matter integrity in subjects at ultra-high-risk for psychosis. Schizophrenia Research 111, 192193.Google Scholar
Pettersson-Yeo, W, Allen, P, Benetti, S, McGuire, P, Mechelli, A (2011). Dysconnectivity in schizophrenia: where are we now? Neuroscience and Biobehavioral Reviews 35, 11101124.CrossRefGoogle ScholarPubMed
Radoeva, PD, Coman, IL, Antshel, KM, Fremont, W, McCarthy, CS, Kotkar, A, Wang, D, Shprintzen, RJ, Kates, WR (2012). Atlas-based white matter analysis in individuals with velo-cardio-facial syndrome (22q11.2 deletion syndrome) and unaffected siblings. Behavioral and Brain Functions Behavioral and brain functions: BBF 8, 38.Google Scholar
Rueckert, D, Sonoda, LI, Hayes, C, Hill, DL, Leach, MO, Hawkes, DJ (1999). Nonrigid registration using free-form deformations: application to breast MR images. IEEE Transactions on Medical Imaging 18, 712721.Google Scholar
Sasaki, T, Pasternak, O, Mayinger, M, Muehlmann, M, Savadjiev, P, Bouix, S, Kubicki, M, Fredman, E, Dahlben, B, Helmer, KG, Johnson, AM, Holmes, JD, Forwell, LA, Skopelja, EN, Shenton, ME, Echlin, PS, Koerte, IK (2014). Hockey Concussion Education Project, Part 3. White matter microstructure in ice hockey players with a history of concussion: a diffusion tensor imaging study. Journal of Neurosurgery 120, 882890.CrossRefGoogle ScholarPubMed
Schneider, M, Schaer, M, Mutlu, AK, Menghetti, S, Glaser, B, Debbané, M, Eliez, S (2014). Clinical and cognitive risk factors for psychotic symptoms in 22q11.2 deletion syndrome: a transversal and longitudinal approach. European Child & Adolescent Psychiatry 23, 425436.CrossRefGoogle ScholarPubMed
Schwartz, ED, Cooper, ET, Fan, Y, Jawad, AF, Chin, C-L, Nissanov, J, Hackney, DB (2005). MRI diffusion coefficients in spinal cord correlate with axon morphometry. Neuroreport 16, 7376.Google Scholar
Shahand, S, Benabdelkader, A, Jaghoori, MM, Mourabit, M al, Huguet, J, Caan, MWA, van Kampen, AHC, Olabarriaga, SD (2015). A data-centric neuroscience gateway: design, implementation, and experiences. Concurrency and Computation: Practice and Experience 27, 489506.Google Scholar
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E, Hergueta, T, Baker, R, Dunbar, GC (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59 (Suppl 2), 2233; quiz 34–57.Google Scholar
Shereen, A, Nemkul, N, Yang, D, Adhami, F, Dunn, RS, Hazen, ML, Nakafuku, M, Ning, G, Lindquist, DM, Kuan, C-Y (2011). Ex vivo diffusion tensor imaging and neuropathological correlation in a murine model of hypoxia-ischemia-induced thrombotic stroke. Journal of Cerebral Blood Flow and Metabolism 31, 11551169.Google Scholar
Sinderberry, B, Brown, S, Hammond, P, Stevens, AF, Schall, U, Murphy, DGM, Murphy, KC, Campbell, LE (2013). Subtypes in 22q11.2 deletion syndrome associated with behaviour and neurofacial morphology. Research in Developmental Disabilities 34, 116125.CrossRefGoogle ScholarPubMed
Smith, SM, Jenkinson, M, Johansen-Berg, H, Rueckert, D, Nichols, TE, Mackay, CE, Watkins, KE, Ciccarelli, O, Cader, MZ, Matthews, PM, Behrens, TEJ (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 31, 14871505.Google Scholar
Song, S-K, Sun, S-W, Ju, W-K, Lin, S-J, Cross, AH, Neufeld, AH (2003). Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. NeuroImage 20, 17141722.CrossRefGoogle ScholarPubMed
Song, S-K, Sun, S-W, Ramsbottom, MJ, Chang, C, Russell, J, Cross, AH (2002). Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. NeuroImage 17, 14291436.Google Scholar
Song, S-K, Yoshino, J, Le, TQ, Lin, S-J, Sun, S-W, Cross, AH, Armstrong, RC (2005). Demyelination increases radial diffusivity in corpus callosum of mouse brain. NeuroImage 26, 132140.Google Scholar
Stüber, C, Morawski, M, Schäfer, A, Labadie, C, Wähnert, M, Leuze, C, Streicher, M, Barapatre, N, Reimann, K, Geyer, S, Spemann, D, Turner, R (2014). Myelin and iron concentration in the human brain: a quantitative study of MRI contrast. NeuroImage 93, 95106.Google Scholar
Sun, D, Phillips, L, Velakoulis, D, Yung, A, McGorry, PD, Wood, SJ, van Erp, TGM, Thompson, PM, Toga, AW, Cannon, TD, Pantelis, C (2009). Progressive brain structural changes mapped as psychosis develops in ‘at risk’ individuals. Schizophrenia Research 108, 8592.Google Scholar
Sundram, F, Campbell, LE, Azuma, R, Daly, E, Bloemen, OJN, Barker, GJ, Chitnis, X, Jones, DK, van Amelsvoort, T, Murphy, KC, Murphy, DGM (2010). White matter microstructure in 22q11 deletion syndrome: a pilot diffusion tensor imaging and voxel-based morphometry study of children and adolescents. Journal of Neurodevelopmental Disorders 2, 7792.Google Scholar
Szeszko, PR, Robinson, DG, Ikuta, T, Peters, BD, Gallego, JA, Kane, J, Malhotra, AK (2014). White matter changes associated with antipsychotic treatment in first-episode psychosis. Neuropsychopharmacology 39, 13241331.Google Scholar
Tan, GM, Arnone, D, McIntosh, AM, Ebmeier, KP (2009). Meta-analysis of magnetic resonance imaging studies in chromosome 22q11.2 deletion syndrome (velocardiofacial syndrome). Elsevier B.V. Schizophrenia Research 115, 173181.CrossRefGoogle ScholarPubMed
van Os, J, Kapur, S (2009). Schizophrenia. Lancet 374, 635645.Google Scholar
van Os, J, Rutten, BP, Poulton, R (2008). Gene-environment interactions in schizophrenia: review of epidemiological findings and future directions. Schizophrenia Bulletin 34, 10661082.CrossRefGoogle ScholarPubMed
Wakana, S, Caprihan, A, Panzenboeck, MM, Fallon, JH, Perry, M, Gollub, RL, Hua, K, Zhang, J, Jiang, H, Dubey, P, Blitz, A, van Zijl, P, Mori, S (2007). Reproducibility of quantitative tractography methods applied to cerebral white matter. NeuroImage 36, 630644.Google Scholar
Walterfang, M, McGuire, PK, Yung, AR, Phillips, LJ, Velakoulis, D, Wood, SJ, Suckling, J, Bullmore, ET, Brewer, W, Soulsby, B, Desmond, P, McGorry, PD, Pantelis, C (2008). White matter volume changes in people who develop psychosis. British Journal of Psychiatry 193, 210215.Google Scholar
Wang, Q, Cheung, C, Deng, W, Li, M, Huang, C, Ma, X, Wang, Y, Jiang, L, Sham, PC, Collier, DA, Gong, Q, Chua, SE, McAlonan, GM, Li, T (2013). White-matter microstructure in previously drug-naive patients with schizophrenia after 6 weeks of treatment. Psychological Medicine 43, 23012309.Google Scholar
Whitford, TJ, Kubicki, M, Shenton, ME (2011). Diffusion tensor imaging, structural connectivity, and schizophrenia. Schizophrenia Research and Treatment 2011, 709523.Google Scholar
Witthaus, H, Brüne, M, Kaufmann, C, Bohner, G, Ozgürdal, S, Gudlowski, Y, Heinz, A, Klingebiel, R, Juckel, G (2008). White matter abnormalities in subjects at ultra high-risk for schizophrenia and first-episode schizophrenic patients. Schizophrenia Research 102, 141149.CrossRefGoogle ScholarPubMed
Zalesky, A (2011). Moderating registration misalignment in voxelwise comparisons of DTI data: a performance evaluation of skeleton projection. Magnetic Resonance Imaging 29, 111125.Google Scholar