Cortical folding abnormalities in schizophrenia patients with resistant auditory hallucinations

Gray matter volume and functional abnormalities have been reported in language-related cortex in schizophrenia patients with auditory hallucinations. Such abnormalities might denote abnormal cortical folding development, which can now be investigated using gyrification measures. Anatomic magnetic resonance images (MRIs) were obtained from 30 schizophrenia patients screened for resistant auditory hallucinations and 28 control subjects. We searched for overall gyrification abnormalities in the whole cortex as well as localized abnormalities in language-related cortex, assuming that gyrification is associated with brain sulcation. A fully automated method was applied to MRIs to extract, label and measure the sulcus area in the whole cortex. Gyrification was assessed using both global and local sulcal indices, respectively the ratio between total sulcal area, or area of each labeled sulcus, and outer cortex area. For both hemispheres, the patients had a lower global sulcal index. The local sulcal index decrease was not homogeneous across the whole cortex. It was more significant in the superior temporal sulcus bilaterally, in the left middle frontal sulcus and in the diagonal branch of left sylvian fissure (Broca's area). Findings suggest abnormalities in cortical gyrification in these patients. Sulcal abnormalities in language-related cortex might underlie these patients' particular vulnerability to hallucinations.

[1]  C. Büchel,et al.  Neuroanatomy of "hearing voices": a frontotemporal brain structural abnormality associated with auditory hallucinations in schizophrenia. , 2004, Cerebral cortex.

[2]  John Suckling,et al.  A computational morphometric MRI study of schizophrenia: effects of hallucinations. , 2002, Cerebral cortex.

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

[4]  R. Murray,et al.  Increased blood flow in Broca's area during auditory hallucinations in schizophrenia , 1993, The Lancet.

[5]  J. Colover,et al.  Auditory hallucinations and perception of external speech. , 1995, Lancet.

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

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

[8]  M. Kurachi,et al.  Left superior temporal blood flow increases in schizophrenic and schizophreniform patients with auditory hallucination: A longitudinal case study using123I-IMP SPECT , 2005, European Archives of Psychiatry and Clinical Neuroscience.

[9]  G. Jackson,et al.  Neurobiological findings in early phase schizophrenia , 2000, Brain Research Reviews.

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

[11]  Jamila Andoh,et al.  Left superior temporal gyrus activation during sentence perception negatively correlates with auditory hallucination severity in schizophrenia patients , 2006, Schizophrenia Research.

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

[13]  M. Stephane,et al.  Imaging auditory verbal hallucinations during their occurrence. , 2000, The Journal of neuropsychiatry and clinical neurosciences.

[14]  R. Kahn,et al.  Perception, mental imagery and reality discrimination in hallucinating and non-hallucinating schizophrenic patients. , 2000, The British journal of clinical psychology.

[15]  J. Pardo,et al.  About the mechanisms of auditory verbal hallucinations: a positron emission tomographic study. , 2006, Journal of psychiatry & neuroscience : JPN.

[16]  N. Andreasen,et al.  Symptom dimensions and brain morphology in schizophrenia and related psychotic disorders. , 1995, Journal of psychiatric research.

[17]  E. B. Southard,et al.  ON THE TOPOGRAPHICAL DISTRIBUTION OF CORTEX LESIONS AND ANOMALIES IN DEMENTIA PRÆCOX, WITH SOME ACCOUNT OF THEIR FUNCTIONAL SIGNIFICANCE , 1914 .

[18]  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.

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

[20]  Paul Allen,et al.  Misattribution of speech and impaired connectivity in patients with auditory verbal hallucinations , 2007, Human brain mapping.

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

[22]  N. Tarrier,et al.  Scales to measure dimensions of hallucinations and delusions: the psychotic symptom rating scales (PSYRATS) , 1999, Psychological Medicine.

[23]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

[24]  A. Korten,et al.  Early manifestations and first-contact incidence of schizophrenia in different cultures: A preliminary report on the initial evaluation phase of the WHO Collaborative Study on Determinants of Outcome of Severe Mental Disorders , 1986, Psychological Medicine.

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

[26]  T. Crow Is schizophrenia the price that Homo sapiens pays for language? , 1997, Schizophrenia Research.

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

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

[29]  D. Louis Collins,et al.  Brain morphometry using 3D moment invariants , 2004, Medical Image Anal..

[30]  Kuniyoshi L Sakai,et al.  Language Acquisition and Brain Development , 2005, Science.

[31]  C Nahmias,et al.  Regional Brain Metabolism During Auditory Hallucinations in Chronic Schizophrenia , 1990, British Journal of Psychiatry.

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

[33]  Thomas Dierks,et al.  The spatiotemporal pattern of auditory cortical responses during verbal hallucinations , 2005, NeuroImage.

[34]  Isabelle Bloch,et al.  A primal sketch of the cortex mean curvature: a morphogenesis based approach to study the variability of the folding patterns , 2003, IEEE Transactions on Medical Imaging.

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

[36]  Peter G. Morris,et al.  The functional anatomy of auditory hallucinations in schizophrenia , 2000, Psychiatry Research: Neuroimaging.

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

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

[39]  R Tandon,et al.  Superior temporal gyrus in schizophrenia: a volumetric magnetic resonance imaging study , 2000, Schizophrenia Research.

[40]  A. Simmons,et al.  Are auditory hallucinations the consequence of abnormal cerebral lateralization? A morphometric MRI study of the sylvian fissure and planum temporale , 2001, Biological Psychiatry.

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

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

[43]  Nancy C. Andreasen,et al.  Negative symptoms in schizophrenia , 1982 .

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

[45]  David Moratal,et al.  Emotional words induce enhanced brain activity in schizophrenic patients with auditory hallucinations , 2007, Psychiatry Research: Neuroimaging.

[46]  S. Rossell,et al.  Are auditory–verbal hallucinations associated with auditory affective processing deficits? , 2005, Schizophrenia Research.

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

[48]  山浦 晶 Atlas of the Cerebral Sulci, Michio Ono, Stefan Kubik and Chad D. Abernathey著, Georg Thieme Verlag, Stuttgart, New York 1990(らいぶらりい) , 1992 .

[49]  Mario Beauregard,et al.  Cerebral activity associated with auditory verbal hallucinations: a functional magnetic resonance imaging case study. , 2002, Journal of psychiatry & neuroscience : JPN.

[50]  L. DeLisi,et al.  Speech disorder in schizophrenia: review of the literature and exploration of its relation to the uniquely human capacity for language. , 2001, Schizophrenia bulletin.

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

[52]  M. Annett,et al.  The theory of an agnosic right shift gene in schizophrenia and autism , 1999, Schizophrenia Research.

[53]  Pasko Rakic,et al.  Neuroscience. Genetic control of cortical convolutions. , 2004, Science.

[54]  N C Andreasen,et al.  Negative symptoms in schizophrenia , 1982 .

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

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

[57]  K. Hugdahl,et al.  MR MORPHOMETRY ANALYSIS OF GREY MATTER VOLUME REDUCTION IN SCHIZOPHRENIA: ASSOCIATION WITH HALLUCINATIONS , 2006, The International journal of neuroscience.

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

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

[60]  Richard S. J. Frackowiak,et al.  A functional neuroanatomy of hallucinations in schizophrenia , 1995, Nature.

[61]  C. Levitan,et al.  Superior temporal gyral volumes and laterality correlates of auditory hallucinations in schizophrenia , 1999, Biological Psychiatry.

[62]  Niels G. Waller The Scale for the Assessment of Negative Symptoms , 1995 .

[63]  Peter B. Jones,et al.  Spatial and temporal mapping of neural activity associated with auditory hallucinations , 1999, The Lancet.

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

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

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

[67]  M J Brammer,et al.  Modality specific neural correlates of auditory and somatic hallucinations , 2001, Journal of neurology, neurosurgery, and psychiatry.

[68]  A. Addington,et al.  The neurodevelopmental model of schizophrenia: update 2005 , 2005, Molecular Psychiatry.

[69]  Michael D. Hunter,et al.  Male and female voices activate distinct regions in the male brain , 2005, NeuroImage.

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

[71]  A Pfefferbaum,et al.  Abnormalities of the left temporal lobe in schizophrenia. , 1992, The New England journal of medicine.

[72]  R. Murray,et al.  Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. , 2000, Archives of general psychiatry.

[73]  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.

[74]  W. Singer,et al.  Activation of Heschl’s Gyrus during Auditory Hallucinations , 1999, Neuron.

[75]  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.

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

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

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

[79]  Paul Allen,et al.  Neural correlates of the misattribution of speech in schizophrenia , 2007, British Journal of Psychiatry.

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

[81]  G D Pearlson,et al.  Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. , 1990, The American journal of psychiatry.