Increased parahippocampal and lingual gyrification in first-episode schizophrenia

OBJECTIVE Cerebral gyrification is attributed to a large extent to genetic and intrauterine/perinatal factors. Hence, investigating gyrification might offer important evidence for disturbed neurodevelopmental mechanisms in schizophrenia. As an extension of recent ROI analyses of gyrification in schizophrenia the present study is the first to compare on a node-by-node basis mean curvature as a sensitive parameter for the identification of local gyrification changes of the whole cortex in first-episode schizophrenia. METHODS A group of 54 patients with first-episode schizophrenia according to DSM-IV and 54 age and gender matched healthy control subjects were included. All participants underwent high-resolution T1-weighted MRI scans on a 1.5 T scanner. Mean curvature was calculated dividing the sum of the principal curvatures by two at each point of the curved surface as implemented in the Freesurfer Software package. Statistical cortical maps were created to estimate gyrification differences between groups based on a clustering approach. RESULTS A significantly increased gyrification was observed in first-episode schizophrenia patients relative to controls in a right parahippocampal-lingual cortex area. The cluster encompassed a surface area of 750 mm². A further analysis of cortical thickness of this cluster demonstrated concurrent significant reduced cortical thickness of this area. CONCLUSIONS This is the first study to reveal an aberrant gyrification of the medial surface in first-episode schizophrenia. This finding is in line with substantial evidence showing medial temporal lobe abnormalities in schizophrenia. The present morphometric data provide further support for an early disruption of cortical maturation in schizophrenia.

[1]  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.

[2]  Kristoffer Hougaard Madsen,et al.  Neural correlates of virtual route recognition in congenital blindness , 2010, Proceedings of the National Academy of Sciences.

[3]  J. Vázquez-Barquero,et al.  Predictors of acute treatment response in patients with a first episode of non-affective psychosis: sociodemographics, premorbid and clinical variables. , 2007, Journal of psychiatric research.

[4]  Eve C. Johnstone,et al.  Increased Prefrontal Gyrification in a Large High-Risk Cohort Characterizes Those Who Develop Schizophrenia and Reflects Abnormal Prefrontal Development , 2007, Biological Psychiatry.

[5]  Christian Gaser,et al.  Reduced cortical thickness in first episode schizophrenia , 2010, Schizophrenia Research.

[6]  Paul M. Thompson,et al.  A curvature-based approach to estimate local gyrification on the cortical surface , 2006, NeuroImage.

[7]  M. Annett The Binomial Distribution of Right, Mixed and Left Handedness , 1967, The Quarterly journal of experimental psychology.

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

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

[10]  J. Reichenbach,et al.  Psychopathological correlates of the entorhinal cortical shape in schizophrenia , 2010, European Archives of Psychiatry and Clinical Neuroscience.

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

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

[13]  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.

[14]  T. Crow,et al.  Temporal-lobe length is reduced, and gyral folding is increased in schizophrenia: a post-mortem study , 1998, Schizophrenia Research.

[15]  M. D’Esposito,et al.  The parahippocampus subserves topographical learning in man , 1996, NeuroImage.

[16]  S. Lawrie,et al.  Increased Right Prefrontal Cortical Folding in Adolescents at Risk of Schizophrenia for Cognitive Reasons , 2008, Biological Psychiatry.

[17]  S. Arnold,et al.  Cellular and Molecular Neuropathology of the Parahippocampal Region in Schizophrenia , 2000, Annals of the New York Academy of Sciences.

[18]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[19]  R. Kikinis,et al.  An in vivo MRI study of prefrontal cortical complexity in first-episode psychosis. , 2005, The American journal of psychiatry.

[20]  H. Barbas,et al.  Developmental mechanics of the primate cerebral cortex , 2005, Anatomy and Embryology.

[21]  J. Suckling,et al.  Cerebral grey, white matter and csf in never-medicated, first-episode schizophrenia , 2007, Schizophrenia Research.

[22]  Enrico Simonotto,et al.  Functional Imaging as a Predictor of Schizophrenia , 2006, Biological Psychiatry.

[23]  D. Weinberger,et al.  Remission in schizophrenia: proposed criteria and rationale for consensus. , 2005, The American journal of psychiatry.

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

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

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

[27]  Paul J. Harrison,et al.  Preferential involvement of excitatory neurons in medial temporal lobe in schizophrenia , 1998, The Lancet.

[28]  P. Matthews,et al.  White matter abnormalities and brain activation in schizophrenia: A combined DTI and fMRI study , 2007, Schizophrenia Research.

[29]  P. McGuire,et al.  Regional Gray Matter Volume in Monozygotic Twins Concordant and Discordant for Schizophrenia , 2010, Biological Psychiatry.

[30]  J. Kwon,et al.  Cortical thickness reduction in individuals at ultra-high-risk for psychosis. , 2011, Schizophrenia bulletin.

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

[32]  Chang-Gyu Hahn,et al.  Neurodevelopment, neuroplasticity, and new genes for schizophrenia. , 2005, Progress in brain research.

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

[34]  Dennis Velakoulis,et al.  Surface‐based morphometry of the anterior cingulate cortex in first episode schizophrenia , 2008, Human brain mapping.

[35]  A. Frigessi,et al.  Regional thinning of the cerebral cortex in schizophrenia: Effects of diagnosis, age and antipsychotic medication , 2008, Schizophrenia Research.

[36]  N. Makris,et al.  A methodology for analyzing curvature in the developing brain from preterm to adult , 2008, Int. J. Imaging Syst. Technol..

[37]  Raymond C K Chan,et al.  Facial emotion processing in schizophrenia: a meta-analysis of functional neuroimaging data. , 2010, Schizophrenia bulletin.

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

[39]  R. Woods,et al.  Mapping cortical thickness and gray matter concentration in first episode schizophrenia. , 2005, Cerebral cortex.

[40]  H. Möller,et al.  Pharmacological long-term treatment strategies in first episode schizophrenia , 2004, European Archives of Psychiatry and Clinical Neuroscience.

[41]  J. Reichenbach,et al.  Complex pattern of cortical thinning in schizophrenia: Results from an automated surface based analysis of cortical thickness , 2010, Psychiatry Research: Neuroimaging.

[42]  D. Hubl,et al.  Structural Analysis of Heschl’s Gyrus in Schizophrenia Patients with Auditory Hallucinations , 2009, Neuropsychobiology.

[43]  S. Kiebel,et al.  Detecting Structural Changes in Whole Brain Based on Nonlinear Deformations—Application to Schizophrenia Research , 1999, NeuroImage.

[44]  L. DeLisi The significance of age of onset for schizophrenia. , 1992, Schizophrenia bulletin.

[45]  A M McIntosh,et al.  Prefrontal gyral folding and its cognitive correlates in bipolar disorder and schizophrenia , 2009, Acta psychiatrica Scandinavica.

[46]  S. Arnold The medial temporal lobe in schizophrenia. , 1997, The Journal of neuropsychiatry and clinical neurosciences.

[47]  S. Heckers,et al.  Abnormal cortical folding patterns within Broca's area in schizophrenia: Evidence from structural MRI , 2007, Schizophrenia Research.

[48]  L. Williams,et al.  Voxel-based morphometry in schizophrenia: implications for neurodevelopmental connectivity models, cognition and affect , 2008, Expert review of neurotherapeutics.

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

[50]  B. Turetsky,et al.  Whole-brain morphometric study of schizophrenia revealing a spatially complex set of focal abnormalities. , 2005, Archives of general psychiatry.

[51]  Katherine P. Rankin,et al.  Detecting sarcasm from paralinguistic cues: Anatomic and cognitive correlates in neurodegenerative disease , 2009, NeuroImage.

[52]  M. Keshavan,et al.  Automated MRI parcellation study of regional volume and thickness of prefrontal cortex (PFC) in antipsychotic‐naïve schizophrenia , 2008, Acta psychiatrica Scandinavica.

[53]  R. Buchanan,et al.  Brain morphology and schizophrenia. A magnetic resonance imaging study of limbic, prefrontal cortex, and caudate structures. , 1992, Archives of general psychiatry.

[54]  E. Bullmore,et al.  Meta-Analysis of Gray Matter Anomalies in Schizophrenia: Application of Anatomic Likelihood Estimation and Network Analysis , 2008, Biological Psychiatry.

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

[56]  Marianna D. Eddy,et al.  Regionally localized thinning of the cerebral cortex in schizophrenia , 2003, Schizophrenia Research.

[57]  H. Nicolini,et al.  Heritability of age of onset of psychosis in schizophrenia , 2009, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[58]  Nadim Joni Shah,et al.  Increased neural response related to neutral faces in individuals at risk for psychosis , 2008, NeuroImage.

[59]  T. Crow,et al.  Right hemisphere language functions and schizophrenia: the forgotten hemisphere? , 2005, Brain : a journal of neurology.

[60]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[61]  A. Malla,et al.  Duration of untreated psychosis: a critical examination of the concept and its importance , 2001, Psychological Medicine.

[62]  Trevor R. Norman,et al.  Behavioural studies of spatial working memory dysfunction in schizophrenia: A quantitative literature review , 2007, Psychiatry Research.