Disruption of white matter integrity in the inferior longitudinal fasciculus in adolescents with schizophrenia as revealed by fiber tractography.

Introduction: There is increasing evidence that schizophrenia is characterized by abnormalities in white matter. The authors investigated the integrity of white matter tracts in adolescents with schizophrenia. Methods: Cross-sectional, case-control, whole-brain, voxel-based analysis and fiber tractography using diffusion tensor magnetic resonance imaging conducted at a university research institute. Forty-four individuals (age range, 11-18 years), 23 with a DSM-IV diagnosis of schizophrenia or schizoaffective disorder and 21 demographically similar healthy controls participated in the study. Results: Voxelwise analysis revealed that adolescents with schizophrenia had reduced fractional anisotropy within the left inferior temporal (P < 0.001) and occipital (P < 0.001) regions. Tractography was performed to extract the left and the right inferior longitudinal fasciculi (ILF). Measuring the mean diffusion indices along the left ILF, patients had significantly reduced fractional anis otropy (P < 0.001) as well as significantly increased radial diffusivity (P < 0.001) and trace (P = 0.003) after adjusting for differences in a measure thought to reflect premorbid intelligence, Wide Range Achievement Test 3 reading scores. Exploratory analyses revealed that patients with a history of visual hallucinations had lower fractional anisotropy in the left ILF (P = 0.02) than patients without visual hallucinations. Conclusions: Our findings, which benefited from greater image resolution and methodological control than previous studies conducted in adolescents with schizophrenia, provide strong evidence for lower white matter integrity in the left ILF, particularly for patients with a history of visual hallucinations.

[1]  E. Ross Sensory-specific and fractional disorders of recent memory in man. I. Isolated loss of visual recent memory. , 1980, Archives of neurology.

[2]  M. Woerner,et al.  Anchoring the BPRS: an aid to improved reliability. , 1988, Psychopharmacology bulletin.

[3]  R. Dworkin,et al.  Social Competence Deficits in Adolescents at Risk for Schizophrenia , 1994, The Journal of nervous and mental disease.

[4]  J L Rapoport,et al.  Looking for childhood-onset schizophrenia: the first 71 cases screened. , 1994, Journal of the American Academy of Child and Adolescent Psychiatry.

[5]  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.

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

[7]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[8]  Emotion recognition and social competence in chronic schizophrenia. , 1996 .

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

[10]  D. Penn,et al.  The relationship of social cognition to ward behavior in chronic schizophrenia , 1996, Schizophrenia Research.

[11]  N. Ryan,et al.  Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[12]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[13]  I. Kovács,et al.  Late maturation of visual spatial integration in humans. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[14]  M. Solaiyappan,et al.  In vivo three‐dimensional reconstruction of rat brain axonal projections by diffusion tensor imaging , 1999, Magnetic resonance in medicine.

[15]  N G Papadakis,et al.  A comparative study of acquisition schemes for diffusion tensor imaging using MRI. , 1999, Journal of magnetic resonance.

[16]  I. Kovács Human development of perceptual organization , 2000, Vision Research.

[17]  Sinisa Pajevic,et al.  Color schemes to represent the orientation of anisotropic tissues from diffusion tensor data: Application to white matter fiber tract mapping in the human brain , 1999, Magnetic resonance in medicine.

[18]  J. Foong,et al.  Neuropathological abnormalities of the corpus callosum in schizophrenia: a diffusion tensor imaging study , 2000, Journal of neurology, neurosurgery, and psychiatry.

[19]  S. Lawrie,et al.  Diffusion tensor imaging (DTI) and proton magnetic resonance spectroscopy (1H MRS) in schizophrenic subjects and normal controls , 2001, Psychiatry Research: Neuroimaging.

[20]  D. Moore Textbook of clinical neuropsychiatry , 2001 .

[21]  James C. Gee,et al.  Spatial transformations of diffusion tensor magnetic resonance images , 2001, IEEE Transactions on Medical Imaging.

[22]  S. Skare,et al.  Abnormal brain white matter in schizophrenia: a diffusion tensor imaging study , 2001, Neuroreport.

[23]  N. Uranova,et al.  Electron microscopy of oligodendroglia in severe mental illness , 2001, Brain Research Bulletin.

[24]  Daphne Bavelier,et al.  Human brain plasticity: evidence from sensory deprivation and altered language experience. , 2002, Progress in brain research.

[25]  H. Moser,et al.  Imaging cortical association tracts in the human brain using diffusion‐tensor‐based axonal tracking , 2002, Magnetic resonance in medicine.

[26]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[27]  J. Breeze,et al.  Abnormal anterior cingulum in patients with schizophrenia: a diffusion tensor imaging study , 2003, Neuroreport.

[28]  R. Kikinis,et al.  Cingulate fasciculus integrity disruption in schizophrenia: a magnetic resonance diffusion tensor imaging study , 2003, Biological Psychiatry.

[29]  W. Strik,et al.  Reduced hippocampal anisotropy related to anteriorization of alpha EEG in schizophrenia , 2003, Neuroreport.

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

[31]  S. Lawrie,et al.  Structural disconnectivity in schizophrenia: a diffusion tensor magnetic resonance imaging study , 2003, British Journal of Psychiatry.

[32]  Philip D. Harvey,et al.  White matter changes in schizophrenia: evidence for myelin-related dysfunction. , 2003, Archives of general psychiatry.

[33]  Derek K. Jones,et al.  Occipito-temporal connections in the human brain. , 2003, Brain : a journal of neurology.

[34]  V. Wedeen,et al.  Reduction of eddy‐current‐induced distortion in diffusion MRI using a twice‐refocused spin echo , 2003, Magnetic resonance in medicine.

[35]  D. Javitt,et al.  BRAIN IMAGING NEUROREPORT , 2005 .

[36]  Dai Zhang,et al.  A diffusion tensor imaging study of middle and superior cerebellar peduncle in male patients with schizophrenia , 2003, Neuroscience Letters.

[37]  Manzar Ashtari,et al.  Reduced frontal white matter integrity in Early-Onset schizophrenia: a preliminary study , 2004, Biological Psychiatry.

[38]  Zhiguo Sun,et al.  Anterior cingulum abnormalities in male patients with schizophrenia determined through diffusion tensor imaging. , 2004, The American journal of psychiatry.

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

[40]  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.

[41]  Osamu Abe,et al.  The optimal trackability threshold of fractional anisotropy for diffusion tensor tractography of the corticospinal tract. , 2004, Magnetic resonance in medical sciences : MRMS : an official journal of Japan Society of Magnetic Resonance in Medicine.

[42]  D. Hubl,et al.  Pathways that make voices: white matter changes in auditory hallucinations. , 2004, Archives of general psychiatry.

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

[44]  Vahram Haroutunian,et al.  Variations in myelin and oligodendrocyte-related gene expression across multiple brain regions in schizophrenia: A gene ontology study , 2005, Schizophrenia Research.

[45]  Babak A. Ardekani,et al.  Quantitative comparison of algorithms for inter-subject registration of 3D volumetric brain MRI scans , 2005, Journal of Neuroscience Methods.

[46]  G. Stebbins,et al.  Repeated visual hallucinations in Parkinson's disease as disturbed external/internal perceptions: Focused review and a new integrative model , 2005, Movement disorders : official journal of the Movement Disorder Society.

[47]  D. Javitt,et al.  Early-stage visual processing and cortical amplification deficits in schizophrenia. , 2005, Archives of general psychiatry.

[48]  V. Haroutunian,et al.  Variations in differential gene expression patterns across multiple brain regions in schizophrenia , 2005, Schizophrenia Research.

[49]  Nina Kohn,et al.  Neurocognitive Profile in Adolescents with Early-Onset Schizophrenia: Clinical Correlates , 2005, Biological Psychiatry.

[50]  Manzar Ashtari,et al.  White matter abnormalities in early-onset schizophrenia: a voxel-based diffusion tensor imaging study. , 2005, Journal of the American Academy of Child and Adolescent Psychiatry.

[51]  V. Menon,et al.  White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. , 2005, Cerebral cortex.

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

[53]  Jun Yoshino,et al.  Demyelination increases radial diffusivity in corpus callosum of mouse brain , 2005, NeuroImage.

[54]  Babak A. Ardekani,et al.  ttention-Deficit/Hyperactivity Disorder: Preliminary Diffusion Tensor Imaging Study , 2005 .

[55]  Carl-Fredrik Westin,et al.  DTI and MTR abnormalities in schizophrenia: Analysis of white matter integrity , 2005, NeuroImage.

[56]  Manzar Ashtari,et al.  White matter abnormalities in first-episode schizophrenia or schizoaffective disorder: a diffusion tensor imaging study. , 2005, The American journal of psychiatry.

[57]  M. Brüne Emotion recognition, ‘theory of mind,’ and social behavior in schizophrenia , 2005, Psychiatry Research.

[58]  G Price,et al.  The corpus callosum in first episode schizophrenia: a diffusion tensor imaging study , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[59]  Philip K. McGuire,et al.  Diffusion Tensor Imaging in Schizophrenia , 2005, Biological Psychiatry.

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

[61]  Takashi Hanakawa,et al.  Diffusion-tensor fiber tractography: intraindividual comparison of 3.0-T and 1.5-T MR imaging. , 2006, Radiology.

[62]  Tianzi Jiang,et al.  White matter integrity of the whole brain is disrupted in first-episode schizophrenia , 2006, Neuroreport.

[63]  Hangyi Jiang,et al.  DtiStudio: Resource program for diffusion tensor computation and fiber bundle tracking , 2006, Comput. Methods Programs Biomed..

[64]  A. Pfefferbaum,et al.  Selective age-related degradation of anterior callosal fiber bundles quantified in vivo with fiber tracking. , 2006, Cerebral cortex.

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

[66]  Manzar Ashtari,et al.  Neuroimaging Studies of Children with Serious Emotional Disturbances: A Selective Review , 2007, Canadian journal of psychiatry. Revue canadienne de psychiatrie.

[67]  P. McGuire,et al.  Medial temporal lobe activity at recognition increases with the duration of mnemonic delay during an object working memory task , 2007, Human brain mapping.

[68]  Paul Allen,et al.  Inner speech models of auditory verbal hallucinations: Evidence from behavioural and neuroimaging studies , 2007, International review of psychiatry.

[69]  Gareth J. Barker,et al.  Abnormal brain connectivity in first-episode psychosis: A diffusion MRI tractography study of the corpus callosum , 2007, NeuroImage.

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

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