Folding of the Prefrontal Cortex in Schizophrenia: Regional Differences in Gyrification

BACKGROUND Anatomy of prefrontal cortex in schizophrenia has been studied previously by quantifying the degree of gyrification. Conflicting results exist, with some studies showing hypergyria and others showing hypogyria. It is likely that regional variations in cortical folding exist within the prefrontal cortex that could be explored by studying the anatomical subdivisions formed by the sulci and gyri. With surface reconstructions from magnetic resonance imaging, we studied the gyrification within anatomically meaningful subdivisions of prefrontal cortex in schizophrenia. METHODS Prefrontal cortex was studied with an automated method to obtain Local Gyrification Index, reflecting the degree of cortical folding in 57 patients with schizophrenia and 42 control subjects. Regional differences within prefrontal cortex were compared between the two groups with a sulcogyral atlas. Effects of hemisphere and age were subsequently assessed. RESULTS Patients with schizophrenia had significant hypogyria in most prefrontal regions except the frontomarginal region, which showed hypergyria. The normal left > right pattern of prefrontal gyrification was reversed in schizophrenia. Patients with schizophrenia also showed significant age-related reduction in gyrification at the hypogyric regions. CONCLUSIONS The differences between reported findings regarding prefrontal gyrification might reflect regional variation in the nature of the abnormal process of gyrification in schizophrenia. Prefrontal gyrification is significantly influenced by age in schizophrenia, in addition to the influence of neurodevelopmental factors.

[1]  Eve C Johnstone,et al.  Abnormal cortical folding in high-risk individuals: a predictor of the development of schizophrenia? , 2004, Biological Psychiatry.

[2]  Wagner F. Gattaz,et al.  Polymorphisms in genes involved in neurodevelopment may be associated with altered brain morphology in schizophrenia: Preliminary evidence , 2009, Psychiatry Research.

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

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

[5]  Janet B W Williams,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[6]  Karen Faith Berman,et al.  Executive Function, Neural Circuitry, and Genetic Mechanisms in Schizophrenia , 2010, Neuropsychopharmacology.

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

[8]  A. Toga,et al.  Three-Dimensional Statistical Analysis of Sulcal Variability in the Human Brain , 1996, The Journal of Neuroscience.

[9]  A. Schleicher,et al.  Gyrification in the cerebral cortex of primates. , 1989, Brain, behavior and evolution.

[10]  Meritxell Bach Cuadra,et al.  A Surface-Based Approach to Quantify Local Cortical Gyrification , 2008, IEEE Transactions on Medical Imaging.

[11]  P. Dazzan,et al.  Do antipsychotic drugs affect brain structure? A systematic and critical review of MRI findings , 2009, Psychological Medicine.

[12]  Manuel Desco,et al.  Gyral and Sulcal Cortical Thinning in Adolescents with First Episode Early-Onset Psychosis , 2009, Biological Psychiatry.

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

[14]  M. Weissman,et al.  Best estimate of lifetime psychiatric diagnosis: a methodological study. , 1982, Archives of general psychiatry.

[15]  T. Cizadlo,et al.  Quantitative in vivo measurement of gyrification in the human brain: changes associated with aging. , 1999, Cerebral cortex.

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

[17]  C. Yu,et al.  Reduced Cortical Folding in Mental Retardation , 2010, American Journal of Neuroradiology.

[18]  A. Wilson.  The British National Formulary. , 1963, The Practitioner.

[19]  Gabriele Lohmann,et al.  Magnetic resonance imaging of the human frontal cortex reveals differential anterior–posterior variability of sulcal basins , 2005, NeuroImage.

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

[21]  E. Walker,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[22]  Oliver T. Wolf,et al.  Volumetric analysis of the pre-frontal regions: findings in aging and schizophrenia , 2001, Psychiatry Research: Neuroimaging.

[23]  Meritxell Bach Cuadra,et al.  Congenital heart disease affects local gyrification in 22q11.2 deletion syndrome , 2009, Developmental medicine and child neurology.

[24]  J. Sutcliffe,et al.  Normal human aging and early‐stage schizophrenia share common molecular profiles , 2009, Aging cell.

[25]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[26]  J. Lefévre,et al.  A reaction-diffusion model of the human brain development , 2010, 2010 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[27]  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.

[28]  A. Toga,et al.  Mapping brain maturation , 2006, Trends in Neurosciences.

[29]  J. Thiran,et al.  Congenital heart disease affects local gyrification in 22q11.2 deletion syndrome , 2009, Developmental medicine and child neurology.

[30]  G. Sapiro,et al.  The development of gyrification in childhood and adolescence , 2010, Brain and Cognition.

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

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

[33]  Anders M. Dale,et al.  Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature , 2010, NeuroImage.

[34]  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.

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

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

[37]  Gabriele Lohmann,et al.  Automatic labelling of the human cortical surface using sulcal basins , 2000, Medical Image Anal..

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

[39]  Tianzi Jiang,et al.  Decreased gyrification in major depressive disorder , 2009, Neuroreport.

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

[41]  T. Crow,et al.  Sex-dependent effects of schizophrenia: an MRI study of gyral folding, and cortical and white matter volume , 2003, Psychiatry Research: Neuroimaging.

[42]  S. Woods,et al.  Chlorpromazine equivalent doses for the newer atypical antipsychotics. , 2003, The Journal of clinical psychiatry.

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

[44]  Tao Liu,et al.  The effects of age and sex on cortical sulci in the elderly , 2010, NeuroImage.

[45]  Paul M. Thompson,et al.  On the Genetic Architecture of Cortical Folding and Brain Volume in Primates , 2022 .

[46]  Tyrone D. Cannon,et al.  Genetic influences on brain structure , 2001, Nature Neuroscience.

[47]  Nancy Krieger,et al.  A Researcher's Guide to the National Statistics Socio-Economic Classification , 2003 .

[48]  A. B. Prasad,et al.  British National Formulary , 1994 .

[49]  P. Liddle,et al.  Signs and Symptoms of Psychotic Illness (SSPI): A rating scale , 2002, British Journal of Psychiatry.

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

[51]  Andrew C. Stanfield,et al.  Changes in Gyrification Over 4 Years in Bipolar Disorder and Their Association with the Brain-Derived Neurotrophic Factor Valine66 Methionine Variant , 2009, Biological Psychiatry.

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

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

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

[55]  Armand J. Quick,et al.  THE QUICK TEST , 1951 .