Associations of white matter integrity and cortical thickness in patients with schizophrenia and healthy controls.

Typical brain development includes coordinated changes in both white matter (WM) integrity and cortical thickness (CT). These processes have been shown to be disrupted in schizophrenia, which is characterized by abnormalities in WM microstructure and by reduced CT. The aim of this study was to identify patterns of association between WM markers and cortex-wide CT in healthy controls (HCs) and patients with schizophrenia (SCZ). Using diffusion tensor imaging and structural magnetic resonance imaging data of the Mind Clinical Imaging Consortium study (130 HC and 111 SCZ), we tested for associations between (a) fractional anisotropy in selected manually labeled WM pathways (corpus callosum, anterior thalamic radiation, and superior longitudinal fasciculus) and CT, and (b) the number of lesion-like WM regions ("potholes") and CT. In HC, but not SCZ, we found highly significant negative associations between WM integrity and CT in several pathways, including frontal, temporal, and occipital brain regions. Conversely, in SCZ the number of WM potholes correlated with reduced CT in the left lateral temporal gyrus, left fusiform, and left lateral occipital brain area. Taken together, we found differential patterns of association between WM integrity and CT in HC and SCZ. Although the pattern in HC can be explained from a developmental perspective, the reduced gray matter CT in SCZ patients might be the result of focal but spatially heterogeneous disruptions of WM integrity.

[1]  August B. Hollingshead,et al.  Two Factor Index of Social Position , 1957 .

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

[3]  N C Andreasen,et al.  The Comprehensive Assessment of Symptoms and History (CASH). An instrument for assessing diagnosis and psychopathology. , 1992, Archives of general psychiatry.

[4]  P. Rakić,et al.  Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  J. Ehrhardt,et al.  Regional brain abnormalities in schizophrenia measured with magnetic resonance imaging. , 1994, JAMA.

[6]  P. Basser,et al.  Estimation of the effective self-diffusion tensor from the NMR spin echo. , 1994, Journal of magnetic resonance. Series B.

[7]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[8]  F. Benes,et al.  Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. , 1994, Archives of general psychiatry.

[9]  P. Basser.  Inferring microstructural features and the physiological state of tissues from diffusion‐weighted images , 1995, NMR in biomedicine.

[10]  P. Basser,et al.  Toward a quantitative assessment of diffusion anisotropy , 1996, Magnetic resonance in medicine.

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

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

[13]  P. Huttenlocher,et al.  Regional differences in synaptogenesis in human cerebral cortex , 1997, The Journal of comparative neurology.

[14]  T. J. Crow,et al.  Schizophrenia as a transcallosal misconnection syndrome , 1998, Schizophrenia Research.

[15]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

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

[17]  V. Perry,et al.  Axon damage and repair in multiple sclerosis. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[18]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[19]  Alan C. Evans,et al.  Structural maturation of neural pathways in children and adolescents: in vivo study. , 1999, Science.

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

[21]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[22]  R. Murray,et al.  Meta-analysis of regional brain volumes in schizophrenia. , 2000, The American journal of psychiatry.

[23]  S. Rauch,et al.  Schizophrenic subjects show aberrant fMRI activation of dorsolateral prefrontal cortex and basal ganglia during working memory performance , 2000, Biological Psychiatry.

[24]  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.

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

[26]  C. Beaulieu,et al.  The basis of anisotropic water diffusion in the nervous system – a technical review , 2002, NMR in biomedicine.

[27]  A. Dale,et al.  Whole Brain Segmentation Automated Labeling of Neuroanatomical Structures in the Human Brain , 2002, Neuron.

[28]  T. Jernigan,et al.  Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study , 2002, Developmental medicine and child neurology.

[29]  John Russell,et al.  Dysmyelination Revealed through MRI as Increased Radial (but Unchanged Axial) Diffusion of Water , 2002, NeuroImage.

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

[31]  Shu-Wei Sun,et al.  Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia , 2003, NeuroImage.

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

[33]  S. Wakana,et al.  Fiber tract-based atlas of human white matter anatomy. , 2004, Radiology.

[34]  Abraham Z. Snyder,et al.  A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume , 2004, NeuroImage.

[35]  Frederik Barkhof,et al.  White matter lesions and hippocampal atrophy in Alzheimer’s disease , 2004, Neurology.

[36]  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.

[37]  Suzanne E. Welcome,et al.  Longitudinal Mapping of Cortical Thickness and Brain Growth in Normal Children , 2022 .

[38]  E. Knudsen.  Sensitive Periods in the Development of the Brain and Behavior , 2004, Journal of Cognitive Neuroscience.

[39]  I. Gottesman,et al.  Theories of schizophrenia: a genetic-inflammatory-vascular synthesis , 2005, BMC Medical Genetics.

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

[41]  V. Schmithorst,et al.  Cognitive functions correlate with white matter architecture in a normal pediatric population: A diffusion tensor MRI study , 2005, Human brain mapping.

[42]  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.

[43]  P. Renshaw,et al.  White matter hyperintensities and their association with suicidality in depressed young adults. , 2005, Journal of affective disorders.

[44]  Lin He,et al.  Catechol-O-methyltransferase gene Val/Met functional polymorphism and risk of schizophrenia: A large-scale association study plus meta-analysis , 2005, Biological Psychiatry.

[45]  Anders M. Dale,et al.  Regional cortical thickness matters in recall after months more than minutes , 2006, NeuroImage.

[46]  Anders M. Dale,et al.  Reliability of MRI-derived measurements of human cerebral cortical thickness: The effects of field strength, scanner upgrade and manufacturer , 2006, NeuroImage.

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

[48]  B. J. Casey,et al.  What have we learned about cognitive development from neuroimaging? , 2006, Neuropsychologia.

[49]  Cheuk Y. Tang,et al.  Diffusion tensor imaging of frontal lobe white matter tracts in schizophrenia , 2006, Annals of general psychiatry.

[50]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[51]  Anders M. Dale,et al.  Reliability in multi-site structural MRI studies: Effects of gradient non-linearity correction on phantom and human data , 2006, NeuroImage.

[52]  K. Lim,et al.  Advances in white matter imaging: A review of in vivo magnetic resonance methodologies and their applicability to the study of development and aging , 2006, Neuroscience & Biobehavioral Reviews.

[53]  Arthur W Toga,et al.  Relationships between IQ and regional cortical gray matter thickness in healthy adults. , 2007, Cerebral cortex.

[54]  M. Yücel,et al.  Neuroimaging and emerging psychotic disorders: The Melbourne ultra-high risk studies , 2007, International review of psychiatry.

[55]  R. Kikinis,et al.  A review of diffusion tensor imaging studies in schizophrenia. , 2007, Journal of psychiatric research.

[56]  Theo G. M. van Erp,et al.  Diffusion Tensor Imaging of the Superior Longitudinal Fasciculus and Working Memory in Recent-Onset Schizophrenia , 2008, Biological Psychiatry.

[57]  André J. W. van der Kouwe,et al.  Detection of cortical thickness correlates of cognitive performance: Reliability across MRI scan sessions, scanners, and field strengths , 2008, NeuroImage.

[58]  Alex Fornito,et al.  Abnormal white matter microstructure in schizophrenia: A voxelwise analysis of axial and radial diffusivity , 2008, Schizophrenia Research.

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

[60]  Heidi Johansen-Berg,et al.  Changes in white matter microstructure during adolescence , 2008, NeuroImage.

[61]  Gareth J. Barker,et al.  Diffusion tensor imaging in schizophrenia , 2008, European Psychiatry.

[62]  David G C Owens,et al.  Brain structure and function changes during the development of schizophrenia: the evidence from studies of subjects at increased genetic risk. , 2007, Schizophrenia bulletin.

[63]  K. Lim,et al.  Diffusion Tensor Imaging in Psychiatric Disorders , 2008, Topics in magnetic resonance imaging : TMRI.

[64]  E. Bullmore,et al.  Meta-analysis of diffusion tensor imaging studies in schizophrenia , 2009, Schizophrenia Research.

[65]  Joaquín Goñi,et al.  Contribution of white matter lesions to gray matter atrophy in multiple sclerosis: evidence from voxel-based analysis of T1 lesions in the visual pathway. , 2009, Archives of neurology.

[66]  A. Mack,et al.  Cortical Brain Development in Nonpsychotic Siblings of Patients With Childhood-Onset Schizophrenia , 2009 .

[67]  A. Meyer-Lindenberg,et al.  Widespread reductions of cortical thickness in schizophrenia and spectrum disorders and evidence of heritability. , 2009, Archives of general psychiatry.

[68]  Sophia Frangou,et al.  Recent diffusion tensor imaging findings in early stages of schizophrenia , 2009, Current opinion in psychiatry.

[69]  Mara Cercignani,et al.  Exploring the relationship between white matter and gray matter damage in early primary progressive multiple sclerosis: An in vivo study with TBSS and VBM , 2009, Human brain mapping.

[70]  Michele T. Diaz,et al.  Voxel-based morphometric multisite collaborative study on schizophrenia. , 2009, Schizophrenia bulletin.

[71]  Tonya White,et al.  White matter ‘potholes’ in early-onset schizophrenia: A new approach to evaluate white matter microstructure using diffusion tensor imaging , 2009, Psychiatry Research: Neuroimaging.

[72]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[73]  Anders M. Dale,et al.  MRI-derived measurements of human subcortical, ventricular and intracranial brain volumes: Reliability effects of scan sessions, acquisition sequences, data analyses, scanner upgrade, scanner vendors and field strengths , 2009, NeuroImage.

[74]  M. Pompili,et al.  White matter hyperintensities, suicide risk and late-onset affective disorders: an overview of the current literature. , 2010, La Clinica terapeutica.

[75]  L. Westlye,et al.  Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. , 2010, Cerebral cortex.

[76]  Abraham Z Snyder,et al.  Age-related decline in the microstructural integrity of white matter in children with early- and continuously-treated PKU: a DTI study of the corpus callosum. , 2010, Molecular genetics and metabolism.

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

[78]  Randy L. Gollub,et al.  The COMT Val108/158Met polymorphism and medial temporal lobe volumetry in patients with schizophrenia and healthy adults , 2009, NeuroImage.

[79]  Anderson M. Winkler,et al.  Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies , 2010, NeuroImage.

[80]  Alan C. Evans,et al.  Brain Plasticity and Intellectual Ability Are Influenced by Shared Genes , 2010, The Journal of Neuroscience.

[81]  Gary J. Robertson,et al.  Wide‐Range Achievement Test , 2010 .

[82]  C. Westin,et al.  Corpus Callosum Abnormalities and Their Association with Psychotic Symptoms in Patients with Schizophrenia , 2010, Biological Psychiatry.

[83]  Daniel Güllmar,et al.  Neural activation and radial diffusivity in schizophrenia: combined fMRI and diffusion tensor imaging study. , 2011, The British journal of psychiatry : the journal of mental science.

[84]  Timothy Edward John Behrens,et al.  Automated Probabilistic Reconstruction of White-Matter Pathways in Health and Disease Using an Atlas of the Underlying Anatomy , 2011, Front. Neuroinform..

[85]  A. Mechelli,et al.  Dysconnectivity in schizophrenia: Where are we now? , 2011, Neuroscience & Biobehavioral Reviews.

[86]  D J Holt,et al.  Striatal function in relation to negative symptoms in schizophrenia , 2011, Psychological Medicine.

[87]  Vincent A Magnotta,et al.  Global white matter abnormalities in schizophrenia: a multisite diffusion tensor imaging study. , 2011, Schizophrenia bulletin.

[88]  P. Schofield,et al.  The Genetics of White Matter Lesions , 2011, CNS neuroscience & therapeutics.

[89]  K. Walhovd,et al.  Morphometry and connectivity of the fronto-parietal verbal working memory network in development , 2011, Neuropsychologia.

[90]  C. Lebel,et al.  Diffusion tensor imaging of white matter tract evolution over the lifespan , 2012, NeuroImage.

[91]  Scott R Sponheim,et al.  Associations of cortical thickness and cognition in patients with schizophrenia and healthy controls. , 2012, Schizophrenia bulletin.

[92]  Jürgen R. Reichenbach,et al.  Disrupted white matter connectivity is associated with reduced cortical thickness in the cingulate cortex in schizophrenia , 2013, Cortex.

[93]  Randy L. Gollub,et al.  Spatial characteristics of white matter abnormalities in schizophrenia. , 2013, Schizophrenia bulletin.

[94]  N. Andreasen.  Scale for the Assessment of Negative Symptoms , 2014 .

[95]  Ignazio,et al.  Una coppia nella setta: tra libertà di adesione e rischi di abusi , 2015 .