Regional thinning of cerebral cortical thickness in first-episode and chronic schizophrenia
June Sic Kim
MEG Center, Department of Neurosurgery, Seoul National University Hospital, Seoul, Korea
Search for more papers by this authorCorresponding Author
Chun Kee Chung
MEG Center, Department of Neurosurgery, Seoul National University Hospital, Seoul, Korea
MEG Center, Department of Neurosurgery, Seoul National University Hospital, Seoul, KoreaSearch for more papers by this authorHang Joon Jo
Scientific and Statistical Computing Core, National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20892
Search for more papers by this authorJong Min Lee
Department of Biomedical Engineering, Hanyang University, Seoul, Korea
Search for more papers by this authorJun Soo Kown
Department of Psychiatry, Seoul National University Hospital, Seoul, Korea
Search for more papers by this authorJune Sic Kim
MEG Center, Department of Neurosurgery, Seoul National University Hospital, Seoul, Korea
Search for more papers by this authorCorresponding Author
Chun Kee Chung
MEG Center, Department of Neurosurgery, Seoul National University Hospital, Seoul, Korea
MEG Center, Department of Neurosurgery, Seoul National University Hospital, Seoul, KoreaSearch for more papers by this authorHang Joon Jo
Scientific and Statistical Computing Core, National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20892
Search for more papers by this authorJong Min Lee
Department of Biomedical Engineering, Hanyang University, Seoul, Korea
Search for more papers by this authorJun Soo Kown
Department of Psychiatry, Seoul National University Hospital, Seoul, Korea
Search for more papers by this authorAbstract
First-episode schizophrenia and chronic schizophrenia have different patterns of cortical gray matter loss, due to differences in the period of illness. Differences in the reduction of cortical thickness between first-episode and chronic schizophrenia has not yet been addressed using a technique of measuring cortical thickness. The goal of this study is to identify differences in cerebral cortical thickness between first-episode schizophrenic patients and matched normal controls as well as between chronic schizophrenic patients and matched normal controls. Thirty-five chronic and 24 first-episode schizophrenic patients were compared with each age- and sex-matched control group, respectively. To measure cortical thickness, we utilized an inner and outer cortical surface reconstruction algorithm. Cortical thickness was directly measured as the distance between the two surfaces. Statistical analysis was performed with diffusion smoothing along cortical manifolds, and surface normalization on a sphere model. There were no significant changes in global mean thickness and cerebral gray matter volume in both first-episode and chronic schizophrenia patients. However, we observed regional thinning of cortical thickness, most significantly in the superior temporal gyrus of first-episode schizophrenic patients. In chronic schizophrenia, larger regions including the prefrontal cortex (PF) were significantly thinned compared to the first-episode group. This suggests that the duration of illness affects cortical thinning in the PF, as well as the extent of cortical thinning. © 2012 Wiley Periodicals, Inc. Int J Imaging Syst Technol, 22, 73–80, 2012
REFERENCES
- American Psychiatric Association, Diagnostic and statistical manual of mental disorders, American Psychiatric Press, Washington, DC, 1994.
- W.F.C. Baare,H.E. Hulshoff Pol,R. Hijman,W.P. Mali,M.A. Viergever, andR.S. Kahn, Volumetric analysis of frontal lobe regions in schizophrenia: relation to cognitive function and symptomatology. Biol Psychiatry 45 ( 1999), 1597–1605.
- M.S. Bagary,M.R. Symms,G.J. Barker,S.H. Mutsatsa,E.M. Joyce, andM.A. Ron, Gray and white matter brain abnormalities in first-episode schizophrenia inferred from magnetization transfer imaging. Arch Gen Psychiatry 60 ( 2003), 779–788.
- P.E. Barta,G.D. Pearlson,R.E. Powers,S.S. Richards, andE. Tune, Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. Am J Psychiatry 147 ( 1990), 1457–1462.
- R.M. Bilder,H. Wu,B. Bogerts,G. Degreef,M. Ashtari,J.M. Alvir,P.J. Snyder, andJ.A. Lieberman, Absence of regional hemispheric volume asymmetries in first-episode schizophrenia. Am J Psychiatry 151 ( 1994), 1437–1447.
- J.R. Binder andR.H. Desai, The neurobiology of semantic memory. Trends Cogn Sci 15 ( 2011), 527–536.
- W. Cahn,H.E. Hulshoff Pol,E.B. Lems,N.E. van Haren,H.G. Schnack,J.A. van der Linden,P.F. Schothorst,H. van Engeland, andR.S. Kahn, Brain volume changes in first-episode schizophrenia: A 1-year follow-up study. Arch Gen Psychiatry 59 ( 2002), 1002–1010.
- V.S. CavinessJr,J. Meyer,N. Makris, andD.N. Kennedy, MRI-based topographic parcellation of the human neocortex: an anatomically specified method with estimate of reliability. J Cogn Neurosci 8 ( 1996), 566–587.
- M.K. Chung, Statistical morphometry in neuroanatomy, McGill University, Montreal, 2001.
- D.L. Collins,P. Neelin,T.M. Peters, andA.C. Evans, Automatic 3D intersubject registration of mr volumetric data in standardized talairach space. J Comput Assist Tomo 18 ( 1994), 192–205.
- D.L. Collins,T.M. Peters, andA.C. Evans, An automated 3D non-linear deformation procedure for determination of gross morphometric variability in human brain, SPIE, R.A. Robb (Editor), vol. 2359, Rochester, 1994, pp. 180–190.
- B. Crespo-Facorro,J.J. Kim,N.C. Andreasen,D.S. O'Leary,A.K. Wiser,J.M. Bailey,G. Harris, andV.A. Magnotta, Human frontal cortex: An MRI-based parcellation method. Neuroimage 10 ( 1999), 500–519.
- B. Crespo-Facorro,J.J. Kim,N.C. Andreasen,R. Spinks,D.S. O'Leary,H.J. Bockholt,G. Harris, andV.A. Magnotta, Cerebral cortex: atopographic segmentation method using magnetic resonance imaging. Psychiatr Res Neuroim 100 ( 2000), 97–126.
- A.M. Dale,B. Fischl, andM.I. Sereno, Cortical surface-based analysis 1: Segmentation and surface reconstruction. NeuroImage 9 ( 1999), 179–194.
- L.E. DeLisi,A.L. Hoff,J.E. Schwartz,G.W. Shields,S.N. Halthore,S.M. Gupta,F.A. Henn, andA.K. Anand, Brain morphology in first-episode schizophrenic-like psychotic patients: A quantitative magnetic resonance imaging study. Biol Psychiatry 29 ( 1991), 159–175.
- A.C. Evans,D.L. Collins,S.R. Mills,E.D. Brown,R.L. Kelly, andT.M. Peters, 3D statistical neuroanatomical models from 305 MRI volumes, Proceedings of IEEE-Nuclear Science Sysmposium and Medical Imaging Conference, San Francisco, C.A.( 1993), 1813–1817.
- A.C. Evans,D.L. Collins, andB. Milner, An MRI-based stereotactic atlas from 250 young normal subjects. J Soc Neurosci Abstr 18 ( 1992), 408.
- D. Fannon,X. Chitnis,V. Doku,L. Tennakoon,S. O'Ceallaigh,W. Soni,A. Sumich,J. Lowe,M. Santamaria, andT. Sharma, Features of structural brain abnormality detected in first-episode psychosis. Am J Psychiatry 157 ( 2000), 1829–1834.
- B. Fischl,A. van der Kouwe,C. Destrieux,E. Halgren,F. Segonne,D.H. Salat,E. Busa,L.J. Seidman,J. Goldstein,D. Kennedy,V. Caviness,N. Makris,B. Rosen, andA.M. Dale, Automatically parcellating the human cerebral cortex. Cereb Cortex 14 ( 2004), 11–22.
- J.M. Fuster, The prefrontal cortex: anatomy, physiology and neuropsychology of the frontal lobe, Raven Press, New York, 1989.
- C.R. Genovese,N.A. Lazar, andT. Nichols, Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage 15 ( 2002), 870–878.
- J.N. Giedd,N.O. Jeffries,J. Blumenthal,F.X. Castellanos,A.C. Vaituzis,T. Fernandez,S.D. Hamburger,H. Liu,J. Nelson,J. Bedwell,L. Tran,M. Lenane,R. Nicolson, andJ.L. Rapoport, Childhood-onset schizophrenia: Progressive brain changes during adolescence. Biol Psychiatry 46 ( 1999), 892–898.
- A.R. Gilbert,D.R. Rosenberg,K. Harenski,S. Spencer,J.A. Sweeney, andM.S. Keshavan, Thalamic volumes in patients with first-episode schizophrenia. Am J Psychiatry 158 ( 2001), 618–624.
- P.S. Goldman-Rakic andL.D. Selemon, Functional and anatomical aspects of prefrontal pathology in schizophrenia. Schizophr Bull 23 ( 1997), 437–458.
- R.E. Gur,P.E. Cowell,A. Latshaw,B.I. Turetsky,R.I. Grossman,S.E. Arnold,W.B. Bilker, andR.C. Gur, Reduced dorsal and orbital prefrontal gray matter volumes in schizophrenia. Arch Gen Psychiatry 57 ( 2000), 761–768.
- R.E. Gur,P. Cowell,B.I. Turetsky,F. Gallacher,T. Cannon,W. Bilker, andR.C. Gur, A follow-up magnetic resonance imaging study of schizophrenia. Relationship of neuroanatomical changes to clinical and neurobehavioral measures. Arch Gen Psychiatry 55 ( 1998), 145–152.
- U. Habel,N. Chechko,K. Pauly,K. Koch,V. Backes,N. Seiferth,N.J. Shah,T. Stocker,F. Schneider, andT. Kellemann, Neural correlates of emotion recognition in schizophrenia. Schizophrenia Res 122 ( 2010), 113–123.
- Y. Hirayasu,M.E. Shenton,D.F. Salisbury,C.C. Dickey,I.A. Fischer,P. Mazzoni,T. Kisler,H. Arakaki,J.S. Kwon,J.E. Anderson,D. Yurgelun-Todd,M. Tohen, andR.W. McCarley, Lower left temporal lobe MRI volumes in patients with first-episode schizophrenia compared with psychotic patients with first-episode affective disorder and normal subjects. Am J Psychiatry 155 ( 1998), 1384–1391.
- Y. Hirayasu,R.W. McCarley,D.F. Salisbury,S. Tanaka,J.S. Kwon,M.Frumin,D. Snyderman,D. Yurgelun-Todd,R. Kikinis,F.A. Jolesz, andM.E. Shenton, Planum temporale and heschl gyrus volume reduction in schizophrenia: A magnetic resonance imaging study of first-episode patients. Arch Gen Psychiatry 57 ( 2000), 692–699.
- Y. Hirayasu,S. Tanaka,M.E. Shenton,D.F. Salisbury,M.A. DeSantis,J.J. Levitt,C. Wible,D. Yurgelun-Todd,R. Kikinis,F.A. Jolesz, andR.W. McCarley, Prefrontal gray matter volume reduction in first episode schizophrenia. Cereb Cortex 11 ( 2001), 374–381.
- H.E. Hulshoff Pol,H.G. Schnack,R.C. Mandl,N.E. van Haren,H. Koning,D.L. Collins,A.C. Evans, andR.S. Kahn, Focal gray matter density changes in schizophrenia. Arch Gen Psychiatry 58 ( 2001), 1118–1125.
- D.E. Job,H.C. Whalley,S. McConnell,M. Glabus,E.C. Johnstone, andS.M. Lawrie, Voxel-based morphometry of grey matter densities in subjects at high risk of schizophrenia. Schizophr Res 64 ( 2003), 1–13.
- N. Kabani,G. Le Goualher,D. MacDonald, andA.C. Evans, Measurement of cortical thickness using an automated 3-d algorithm: A validation study. Neuroimage 13 ( 2001), 375–380.
- K. Kasai,M.E. Shenton,D.F. Salisbury,Y. Hirayasu,C.U. Lee,A.A.Ciszewski,D. Yurgelun-Todd,R. Kikinis,F.A. Jolesz, andR.W. McCarley, Progressive decrease of left superior temporal gyrus gray matter volume in patients with first-episode schizophrenia. Am J Psychiatry 160 ( 2003), 156–164.
- S.R. Kay, The positive and negative syndromes scale (PANSS) for schizophrenia. Schizophr. Bull. 13 ( 1987), 261–267.
- J.J. Kim,B. Crespo-Facorro,N.C. Andreasen,D.S. O'Leary,B. Zhang,G. Harris, andV.A. Magnotta, An MRI-based parcellation method for the temporal lobe. Neuroimage 11 ( 2000), 271–288.
- J.S. Kim,V. Singh,J.K. Lee,J. Lerch,Y. Ad-Dab'bagh,D. MacDonald,J.M. Lee,S.I. Kim, andA.C. Evans, 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.
- M. Kubicki,M.E. Shenton,D.F. Salisbury,Y. Hirayasu,K. Kasai,R. Kikinis,F.A. Jolesz, andR.W. McCarley, Voxel-based morphometric analysis of gray matter in first episode schizophrenia. Neuroimage 17 ( 2002), 1711–1719.
- M. Kubota,J. Miyata,H. Yoshida,K. Hirao,H. Fujiwara,R. Kawada,S.Fujimoto,Y. Tanaka,A. Sasamoto,N. Sawamoto,H. Fukuyama,T. Murai, Age-related cortical thinning in schizophrenia. Schizophrenia Res 125 ( 2011), 21–29.
- G.R. Kuperberg,M.R. Broome,P.K. McGuire,A.S. David,M. Eddy,F. Ozawa,D. Goff,W.C. West,S.C. Williams,A.J. van der Kouwe,D.H. Salat,A.M. Dale, andB. Fischl, Regionally localized thinning of the cerebral cortex in schizophrenia. Arch Gen Psychiatry 60 ( 2003), 878–888.
- M. LeMay, Radiological, developmental, and fossil asymmetries, N Geschwind, AM Galaburda(Editors), Harvard University Press, Cambridge MA/London England, 26–42, 1984.
- K.O. Lim,W. Tew,M. Kushner,K. Chow,B. Matsumoto, andL.E. DeLisi, Cortical gray matter volume deficit in patients with first-episode schizophrenia. Am J Psychiatry 153 ( 1996), 1548–1553.
- O. Lyttelton,M. Boucher,S. Robbins, andA. Evans, An unbiased iterative group registration template for cortical surface analysis. Neuroimage 34 ( 2007), 1535–44
- C.-M. Ma andS.-Y. Wan, A medial-surface oriented 3-D two-subfield thinning algorithm. Pattern Recognition Letters 22 ( 2001), 1439–1446.
- D. MacDonald,N. Kabani,D. Avis, andA.C. Evans, Automated 3-D extraction of inner and outer surfaces of cerebral cortex from MRI. NeuroImage 12 ( 2000), 340–356.
- A.L. Madsen,A. Karle,P. Rubin,M. Cortsen,H.S. Andersen, andR.Hemmingsen, Progressive atrophy of the frontal lobes in first-episode schizophrenia: Interaction with clinical course and neuroleptic treatment. Acta Psychiatr Scand 100 ( 1999), 367–374.
- D.H. Mathalon,E.V. Sullivan,K.O. Lim, andA. Pfefferbaum, Progressive brain volume changes and the clinical course of schizophrenia in men: A longitudinal magnetic resonance imaging study. Arch Gen Psychiatry 58 ( 2001), 148–157.
- R.W. McCarley,S.F. Faux,M.E. Shenton,P.G. Nestor, andJ. Adams, Event-related potentials in schizophrenia: Their biological and clinical correlates and a new model of schizophrenic pathophysiology. Schizophr Res 4 ( 1991), 209–231.
- R.W. McCarley,C.G. Wible,M. Frumin,Y. Hirayasu,J.J. Levitt,I.A. Fischer, andM.E. Shenton, MRI anatomy of schizophrenia. Biol Psychiatry 45 ( 1999), 1099–1119.
- R.W. McCarley,D.F. Salisbury,Y. Hirayasu,D.A. Yurgelun-Todd,M. Tohen,C. Zarate,R. Kikinis,F.A. Jolesz, andM.E. Shenton, Association between smaller left posterior superior temporal gyrus volume on magnetic resonance imaging and smaller left temporal p300 amplitude in first-episode schizophrenia. Arch Gen Psychiatry 59 ( 2002), 321–331.
- E.K. Miller, The prefrontal cortex: Complex neural properties for complex behavior. Neuron 22 ( 1999), 15–17.
- V. Molina,J. Sanz,F. Sarramea,C. Benito, andT. Palomo, Lower prefrontal gray matter volume in schizophrenia in chronic but not in first episode schizophrenia patients. Psychiatry Res 131 ( 2004), 45–56.
- K.L. Narr,R.M. Bilder,A.W. Toga,R.P. Woods,D.E. Rex,P.R. Szeszko,D. Robinson,S. Sevy,H. Gunduz-Bruce,Y.P. Wang,H. DeLuca, andP.M. Thompson, Mapping cortical thickness and gray matter concentration in first episode schizophrenia. Cereb Cortex 15 ( 2005), 708–719.
- P. Nopoulos,I. Torres,M. Flaum,N.C. Andreasen,J.C. Ehrhardt, andW.T. Yuh, Brain morphology in first-episode schizophrenia. Am J Psychiatry 152 ( 1995), 1721–1723.
- T. Ohnuma,M. Kimura,T. Takahashi,N. Iwamoto, andH. Arai, A magnetic resonance imaging study in first-episode disorganized-type patients with schizophrenia. Psychiatry Clin Neurosci 51 ( 1997), 9–15.
- T. Onitsuka,M.E. Shenton,D.F. Salisbury,C.C. Dickey,K. Kasai,S.K. Toner,M. Frumin,R. Kikinis,F.A. Jolesz, andR.W. McCarley, Middle and inferior temporal gyrus gray matter volume abnormalities in chronic schizophrenia: An MRI study. Am J Psychiatry 161 ( 2004), 1603–1611.
- C. Pantelis,F.Z. Barber,T.R. Barnes,H.E. Nelson,A.M. Owen, andT.W. Robbins, Comparison of set-shifting ability in patients with chronic schizophrenia and frontal lobe damage. Schizophr Res 37 ( 1999), 251–270.
- J. Rademacher,A.M. Galaburda,D.N. Kennedy,P.A. Filipek,V.S.Caviness, Human cerebral cortex localization, parcellation and morphometry with magnetic resonance imaging. J Cogn Neurosci 4 ( 1992), 352–374.
- J.L. Rapoport,J.N. Giedd,J. Blumenthal,S. Hamburger,N. Jeffries,T. Fernandez,R. Nicolson,J. Bedwell,M. Lenane,A. Zijdenbos,T. Paus, andA. Evans, Progressive cortical change during adolescence in childhood-onset schizophrenia. A longitudinal magnetic resonance imaging study. Arch Gen Psychiatry 56 ( 1999), 649–654.
- K. Razi,K.P. Greene,M. Sakuma,S. Ge,M. Kushner, andL.E. DeLisi, Reduction of the parahippocampal gyrus and the hippocampus in patients with chronic schizophrenia. Br J Psychiatry 174 ( 1999), 512–519.
- S.M. Robbins, Anatomical standardization of the human brain in euclidean 3-space and on the cortical 2-manifold. School of computer science, McGill University, Montreal, 2003.
- D.F. Salisbury,M.E. Shenton,C.B. Griggs,A. Bonner-Jackson, andR.W. McCarley, Mismatch negativity in chronic schizophrenia and first-episode schizophrenia. Arch Gen Psychiatry 59 ( 2002), 686–694.
- C.C. Schultz,K. Koch,G. Wagner,I. Nenadic,C. Schachtzabel,D. Gullmar,J.R. Reichenbach,H. Sauer, and R.G. Schlosser, Reduced anterior cingulate cognitive activation is associated with prefrontal-temporal cortical thinning in schizophrenia, Biol Psychiatry 71 ( 2012), 146–153.
- M.E. Shenton,C.C. Dickey,M. Frumin, andR.W. McCarley, A review of MRI findings in schizophrenia. Schizophr Res 49 ( 2001), 1–52.
- M.E. Shenton,R. Kikinis,F.A. Jolesz,S.D. Pollak,M. LeMay,C.G. Wible,H. Hokama,J. Martin,D. Metcalf,M. Coleman, and R.W. McCarley. Abnormalities of the left temporal lobe and thought disorder in schizophrenia. A quantitative magnetic resonance imaging study. N Engl J Med 327 ( 1992), 604–612.
- J.G. Sled,A.P. Zijdenbos, andA.C. Evans, A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17 ( 1998), 87–97.
- E.E. Smith andJ. Jonides, Storage and executive processes in the frontal lobes. Science 283 ( 1999), 1657–1661.
- E.R. Sowell,P.M. Thompson,C.M. Leonard,S.E. Welcome,E. Kan, andA.W. Toga, Longitudinal mapping of cortical thickness and brain growth in normal children. J Neurosci 24 ( 2004), 8223–8231.
- W. Sperling,P. Martus,H. Kober,S. Bleich, andJ. Kornhuber, Spontaneous, slow and fast magnetoencephalographic activity in patients with schizophrenia. Schizophr Res 58 ( 2002), no. 2–3, 189–199.
- H. Steinmetz,J. Rademacher,Y.X. Huang,H. Hefter,K. Zilles,A. Thron, andH.J. Freund, Cerebral asymmetry: Mr planimetry of the human planum temporale. J Comput Assist Tomogr 13 ( 1989), 996–1005.
- M. Suzuki,S. Yuasa,Y. Minabe,M. Murata, andM. Kurachi, Left superior temporal blood flow increases in schizophrenic and schizophreniform patients with auditory hallucination: A longitudinal case study using 123i-imp spect. Eur Arch Psychiatry Clin Neurosci 242 ( 1993), 257–261.
- A. Szulc,B. Galinska,E. Tarasow,J. Walecki,W. Dzienis,B. Kubas, andA. Czernikiewicz, [clinical and neuropsychological correlates of proton magnetic resonance spectroscopy detected metabolites in brains of first-episodeand schizophrenic patients]. Psychiatr Pol 37 ( 2003), 977–988.
- J. Talairach,P. Tournoux. Co-planar stereotaxic atlas of the human brain, Thieme Medical Publishers, New York, 1988.
- P. Thompson,J.L. Rapoport,T.D. Cannon, andA.W. Toga, Imaging the brain as schizophrenia develops: Dynamic & genetic brain maps. Prim Psychiatry 9 ( 2002), 40–47.
- P.M. Thompson,C. Vidal,J.N. Giedd,P. Gochman,J. Blumenthal,R. Nicolson,A.W. Toga, andJ.L. Rapoport, Mapping adolescent brain change reveals dynamic wave of accelerated gray matter loss in very early-onset schizophrenia. Proc Natl Acad Sci U S A 98 ( 2001), 11650–11655.
- B. Turetsky,P.E. Cowell,R.C. Gur,R.I. Grossman,D.L. Shtasel, andR.E. Gur, Frontal and temporal lobe brain volumes in schizophrenia. Relationship to symptoms and clinical subtype. Arch Gen Psychiatry 52 ( 1995), 1061–1070.
- G.W. Van Hoesen,R.J. Morecraft,K. Semendeferi, Functional neuroanatomy of the limbic system and prefrontal cortex, Baltimore, Williams & Wilkins, 1996, pp. 113–143.
- D. Velakoulis,C. Pantelis,P.D. McGorry,P. Dudgeon,W. Brewer,M. Cook,P. Desmond,N. Bridle,P. Tierney,V. Murrie,B. Singh, andD. Copolov, Hippocampal volume in first-episode psychoses and chronic schizophrenia: A high-resolution magnetic resonance imaging study. Arch Gen Psychiatry 56 ( 1999), 133–141.
- D.R. Weinberger,E.F. Torrey,A.N. Neophytides, andR.J. Wyatt, Structural abnormalities in the cerebral cortex of chronic schizophrenic patients. Arch Gen Psychiatry 36 ( 1979), 935–939.
- A.B. Whitworth,M. Honeder,C. Kremser,G. Kemmler,S. Felber,A. Hausmann,C. Wanko,H. Wechdorn,F. Aichner,C.H. Stuppaeck, andW.W. Fleischhacker, Hippocampal volume reduction in male schizophrenic patients. Schizophr Res 31 ( 1998), 73–81.
- L.C. Wiegand,S.K. Warfield,J.J. Levitt,Y. Hirayasu,D.F. Salisbury,S. Heckers,C.C. Dickey,R. Kikinis,F.A. Jolesz,R.W. McCarley, andM.E. Shenton, Prefrontal cortical thickness in first-episode psychosis: A magnetic resonance imaging study. Biol Psychiatry 55 ( 2004), 131–140.
- I.C. Wright,S. Rabe-Hesketh,P.W. Woodruff,A.S. David,R.M. Murray, andE.T. Bullmore, Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry 157 ( 2000), 16–25.
- U.C. Yoon,J.M. Lee,J.J. Kim,I.Y. Kim,J.S. Kwon,S.I. Kim, Modified MRI-based parcellation method for cerebral cortex using successive fuzzy clustering and boundary detection. Ann Biomed Eng 31 ( 2003), 441–447.
- A.P. Zijdenbos,A.C. Evans,F. Riahi,J.G. Sled,J. Chui, andV. Kollokian, Automatic quantification of multiple sclerosis lesion volume using stereotaxic space, Proc. 4th Intl. Conf. on Visualization in BioMed. Computing VBC, Hamburg, Germany( 1996), 439–448.
- A.P. Zijdenbos,R. Forghani, andA.C. Evans, Automatic quantification of ms lesions in 3D MRI brain data sets: Validation of insect, MICCAI( 1998), 439–448.
- R.B. Zipursky,E.K. Lambe,S. Kapur, andD.J. Mikulis, Cerebral gray matter volume deficits in first episode psychosis. Arch Gen Psychiatry 55 ( 1998), 540–546.