Global and temporal cortical folding in patients with early-onset schizophrenia.

OBJECTIVE Adult-onset schizophrenia has repeatedly been associated with disturbances in the temporal lobes and alterations in cortical folding, which are thought to reflect neurodevelopmental impairment. Early-onset schizophrenia (EOS; onset before 18 years) is considered to involve even more pronounced neurodevelopmental deviance across a wide range of brain structural measures. We hypothesized that overall alteration of cortical folding also applies to EOS, and EOS involves prominent structural aberrations in superior temporal and collateral sulci. METHOD Magnetic resonance T1 images of 51 patients with EOS and 59 healthy participants were investigated. A fully automated method was applied to the images to extract, label, and measure the sulcus area in the whole cortex. Cortical folding was assessed by computing global sulcal indices (the ratio between total sulcal area and total outer cortex area) for each hemisphere and local sulcal indices (the ratio between the area of labeled sulcus and total outer cortex area in the corresponding hemisphere) for superior temporal and collateral sulci. RESULTS Relative to healthy individuals, patients with EOS had significantly lower global sulcal indices in both hemispheres and a lower local sulcal index in the left collateral sulcus. CONCLUSIONS Reduced hemispheric sulcation appears to be a feature of schizophrenia, irrespective of age at onset. Structural aberration involving the left collateral sulcus may contribute to neurobiological substrate of EOS.

[1]  A. Schleicher,et al.  The ontogeny of human gyrification. , 1995, Cerebral cortex.

[2]  Manzar Ashtari,et al.  Clinical and Neuropsychological Correlates of White Matter Abnormalities in Recent Onset Schizophrenia , 2008, Neuropsychopharmacology.

[3]  P Falkai,et al.  Right frontal hypergyria differentiation in affected and unaffected siblings from families multiply affected with schizophrenia: a morphometric mri study. , 2001, The American journal of psychiatry.

[4]  J. Mazziotta,et al.  Age‐related morphology trends of cortical sulci , 2005, Human brain mapping.

[5]  Javier Quintana,et al.  Right lateral fusiform gyrus dysfunction during facial information processing in schizophrenia , 2003, Biological Psychiatry.

[6]  Pasko Rakic,et al.  Genetic Control of Cortical Convolutions , 2004, Science.

[7]  Thomas Dierks,et al.  Alterations of white matter connectivity in first episode schizophrenia , 2006, Neurobiology of Disease.

[8]  H. Remschmidt Early-onset schizophrenia as a progressive-deteriorating developmental disorder: evidence from child psychiatry , 2002, Journal of Neural Transmission.

[9]  D. Louis Collins,et al.  Object-based morphometry of the cerebral cortex , 2004, IEEE Transactions on Medical Imaging.

[10]  T. Sharma,et al.  The Relationship of Structural Alterations to Cognitive Deficits in Schizophrenia: A Voxel-Based Morphometry Study , 2005, Biological Psychiatry.

[11]  F. Lazeyras,et al.  Mapping the early cortical folding process in the preterm newborn brain. , 2008, Cerebral cortex.

[12]  T. Crow,et al.  Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. , 2005, The American journal of psychiatry.

[13]  Y. Samson,et al.  "Sulcal root" generic model: a hypothesis to overcome the variability of the human cortex folding patterns. , 2005, Neurologia medico-chirurgica.

[14]  A. Schleicher,et al.  The human pattern of gyrification in the cerebral cortex , 2004, Anatomy and Embryology.

[15]  J B Poline,et al.  Cerebral gray and white matter reductions and clinical correlates in patients with early onset schizophrenia , 2001, Schizophrenia Research.

[16]  S. Dehaene,et al.  Functional and Structural Alterations of the Intraparietal Sulcus in a Developmental Dyscalculia of Genetic Origin , 2003, Neuron.

[17]  J. McClellan,et al.  Premorbid functioning in early-onset psychotic disorders. , 2003, Journal of the American Academy of Child and Adolescent Psychiatry.

[18]  Jean-Francois Mangin,et al.  Classification Based on Cortical Folding Patterns , 2007, IEEE Transactions on Medical Imaging.

[19]  Jean-Francois Mangin,et al.  Automatic recognition of cortical sulci of the human brain using a congregation of neural networks , 2002, Medical Image Anal..

[20]  M. Keshavan,et al.  Reduced cortical folding in individuals at high risk for schizophrenia: a pilot study , 2005, Schizophrenia Research.

[21]  Clive Harper,et al.  Localised reductions in gyrification in the posterior cingulate: Schizophrenia and controls , 2007, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[22]  C. Hollis Child and Adolescent (Juvenile Onset) Schizophrenia , 1995, British Journal of Psychiatry.

[23]  Eve C Johnstone,et al.  Gyrification in first-episode schizophrenia: a morphometric study , 2004, Biological Psychiatry.

[24]  J. Pruessner,et al.  Selective abnormal modulation of hippocampal activity during memory formation in first-episode psychosis. , 2007, Archives of general psychiatry.

[25]  N. Andreasen,et al.  Gyrification abnormalities in childhood- and adolescent-onset schizophrenia , 2003, Biological Psychiatry.

[26]  Stephen Lawrie,et al.  Pre-frontal lobe gyrification index in schizophrenia, mental retardation and comorbid groups: An automated study , 2007, NeuroImage.

[27]  Eileen Luders,et al.  Gender differences in cortical complexity , 2004, Nature Neuroscience.

[28]  J. Rapoport,et al.  Mapping adolescent brain change reveals dynamic wave of accelerated gray matter loss in very early-onset schizophrenia , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Babak A. Ardekani,et al.  Early detection of schizophrenia by diffusion weighted imaging , 2006, Psychiatry Research: Neuroimaging.

[30]  H. Remschmidt,et al.  Long-term course of adolescent schizophrenia. , 2005, Schizophrenia bulletin.

[31]  Isabelle Bloch,et al.  From 3D magnetic resonance images to structural representations of the cortex topography using topology preserving deformations , 1995, Journal of Mathematical Imaging and Vision.

[32]  Kiralee M. Hayashi,et al.  Dynamically spreading frontal and cingulate deficits mapped in adolescents with schizophrenia. , 2006, Archives of general psychiatry.

[33]  Denis Rivière,et al.  Cortical folding abnormalities in schizophrenia patients with resistant auditory hallucinations , 2008, NeuroImage.

[34]  R. Woods,et al.  Cortical Thinning in Cingulate and Occipital Cortices in First Episode Schizophrenia , 2005, Biological Psychiatry.

[35]  Nitin Gogtay,et al.  Cortical Brain Development in Schizophrenia: Insights From Neuroimaging Studies in Childhood-Onset Schizophrenia , 2007, Schizophrenia bulletin.

[36]  A. Toga,et al.  Abnormal gyral complexity in first-episode schizophrenia , 2004, Biological Psychiatry.

[37]  Yasuhiro Kawasaki,et al.  Temporal lobe gray matter in schizophrenia spectrum: A volumetric MRI study of the fusiform gyrus, parahippocampal gyrus, and middle and inferior temporal gyri , 2006, Schizophrenia Research.

[38]  M. Annett A classification of hand preference by association analysis. , 1970, British journal of psychology.

[39]  K. Vogeley,et al.  Disturbed gyrification of the prefrontal region in male schizophrenic patients: A morphometric postmortem study. , 2000, The American journal of psychiatry.

[40]  W. Welker Why Does Cerebral Cortex Fissure and Fold , 1990 .

[41]  D. V. Essen,et al.  A tension-based theory of morphogenesis and compact wiring in the central nervous system , 1997, Nature.

[42]  Sophia Frangou,et al.  Increased developmental deviance and premorbid dysfunction in early onset schizophrenia , 2003, Schizophrenia Research.

[43]  Stephen Lawrie,et al.  Automated computation of the Gyrification Index in prefrontal lobes: Methods and comparison with manual implementation , 2006, NeuroImage.

[44]  T. Crow,et al.  Anomalous asymmetry of fusiform and parahippocampal gyrus gray matter in schizophrenia: A postmortem study. , 2000, The American journal of psychiatry.

[45]  S. Kay,et al.  The positive and negative syndrome scale (PANSS) for schizophrenia. , 1987, Schizophrenia bulletin.

[46]  Christophe Pallier,et al.  Anatomical correlates of foreign speech sound production. , 2006, Cerebral cortex.

[47]  H. Meltzer,et al.  Age at onset and gender of schizophrenic patients in relation to neuroleptic resistance. , 1997, The American journal of psychiatry.

[48]  Douglas W. Jones,et al.  Cortical abnormality in schizophrenia: An in vivo application of the gyrification index , 1997, Biological Psychiatry.

[49]  S. Frangou,et al.  Pathophysiology of early onset schizophrenia , 2007, International review of psychiatry.

[50]  小野 道夫,et al.  Atlas of the Cerebral Sulci , 1990 .

[51]  Katrin Amunts,et al.  Cortical Folding Patterns and Predicting Cytoarchitecture , 2007, Cerebral cortex.

[52]  Ann E. Maloney,et al.  Treatment of early-onset schizophrenia spectrum disorders (TEOSS): demographic and clinical characteristics. , 2007, Journal of the American Academy of Child and Adolescent Psychiatry.

[53]  L. Opler,et al.  The Positive and Negative Syndrome Scale (PANSS): Rationale and Standardisation , 1989, British Journal of Psychiatry.

[54]  M. Rietschel,et al.  Disturbed frontal gyrification within families affected with schizophrenia. , 2007, Journal of psychiatric research.

[55]  R. Murray,et al.  Superior temporal gyrus abnormalities in early-onset schizophrenia: similarities and differences with adult-onset schizophrenia. , 2001, The American journal of psychiatry.

[56]  Gareth J. Barker,et al.  A Diffusion Tensor Imaging Study of White Matter in Early-Onset Schizophrenia , 2008, Biological Psychiatry.

[57]  J L Rapoport,et al.  The neurodevelopmental model of schizophrenia: update 2005 , 2005, Molecular Psychiatry.

[58]  Claus C. Hilgetag,et al.  Role of Mechanical Factors in the Morphology of the Primate Cerebral Cortex , 2006, PLoS Comput. Biol..

[59]  Dennis Velakoulis,et al.  Structural brain imaging evidence for multiple pathological processes at different stages of brain development in schizophrenia. , 2005, Schizophrenia bulletin.

[60]  R. McCarley,et al.  A review of MRI findings in schizophrenia , 2001, Schizophrenia Research.

[61]  E. Duchesnay,et al.  A framework to study the cortical folding patterns , 2004, NeuroImage.

[62]  G. Busatto,et al.  Reduced cortical folding in schizophrenia: an MRI morphometric study. , 2003, The American journal of psychiatry.

[63]  Gregory G. Brown,et al.  Functional abnormalities of medial temporal cortex during novel picture learning among patients with chronic schizophrenia , 2003, Schizophrenia Research.

[64]  Jerry L Prince,et al.  Cross-sectional and longitudinal analyses of anatomical sulcal changes associated with aging. , 2005, Cerebral cortex.

[65]  Joel Jeffries,et al.  Clinical Handbook of Psychotropic Drugs , 1994 .

[66]  T. Paus Mapping brain maturation and cognitive development during adolescence , 2005, Trends in Cognitive Sciences.

[67]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.