Diffusion Abnormalities and Reduced Volume of the Ventral Cingulum Bundle in Agenesis of the Corpus Callosum: A 3T Imaging Study

BACKGROUND AND PURPOSE: Patients with agenesis of the corpus callosum (AgCC) exhibit cognitive and behavioral impairments that are not replicated by surgical transection of the callosum, suggesting that other anatomic changes may contribute to the observed clinical findings. The purpose of this study was to determine whether the ventral cingulum bundle (VCB) is affected in patients with AgCC by using diffusion tensor imaging (DTI) and volumetry. MATERIALS AND METHODS: Twelve participants with AgCC (8 males and 4 females; mean age, 30 ± 20) and 12 control subjects matched for age and sex (mean age, 37 ± 19) underwent MR imaging and DTI at 3T. 3D fiber tracking of the VCB was generated from DTI and the average fractional anisotropy (FA) was computed for the tracked fibers. Additionally, the volume, cross-sectional area, and length of the VCB were measured by manually drawn regions of interest on thin-section coronal T1-weighted images. The Student t test was used to compare these results. RESULTS: Compared with controls, subjects with AgCC demonstrated significantly reduced FA in the right VCB (P = .0098) and reduced volume and cross-sectional areas of both the left and right VCB (P < .001 for all metrics). The length of the VCB was also significantly reduced in the complete AgCC subgroup compared with controls (P = .030 in the right and P = .046 in the left, respectively). CONCLUSIONS: Patients with AgCC have abnormal microstructure and reduced volume of the VCB, suggesting that abnormalities in intrahemispheric white matter tracts may be an important contributor to the clinical syndrome in patients with AgCC.

[1]  Susumu Mori,et al.  Diffusion tensor MR imaging visualizes the altered hemispheric fiber connection in callosal dysgenesis. , 2004, AJNR. American journal of neuroradiology.

[2]  D Le Bihan,et al.  Human Subinsular Asymmetry Studied by Diffusion Tensor Imaging and Fiber Tracking , 2007, American Journal of Neuroradiology.

[3]  E. Alvord,et al.  Agenesis of the corpus callosum. , 1968, Brain : a journal of neurology.

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

[5]  Renzo Guerrini,et al.  Polymicrogyria and deletion 22q11.2 syndrome: Window to the etiology of a common cortical malformation , 2006, American journal of medical genetics. Part A.

[6]  J Kassubek,et al.  Bilateral language function in callosal agenesis: an fMRI and DTI study. , 2007, Journal of neurology.

[7]  C. Plachez,et al.  Mechanisms regulating the development of the corpus callosum and its agenesis in mouse and human , 2004, Clinical genetics.

[8]  Roger W. Sperry,et al.  Some long-term motor effects of cerebral commissurotomy in man , 1977, Neuropsychologia.

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

[10]  A James Barkovich,et al.  Anomalies of the corpus callosum: an MR analysis of the phenotypic spectrum of associated malformations. , 2006, AJR. American journal of roentgenology.

[11]  H. Utsunomiya,et al.  Arrangement of fiber tracts forming probst bundle in complete callosal agenesis: report of two cases with an evaluation by diffusion tensor tractography , 2006, Acta radiologica.

[12]  D. Javitt,et al.  MRI study of white matter diffusion anisotropy in schizophrenia , 2003, Neuroreport.

[13]  L. Richards,et al.  A role for cingulate pioneering axons in the development of the corpus callosum , 2001, The Journal of comparative neurology.

[14]  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.

[15]  L. W. Wang,et al.  Major brain lesions detected on sonographic screening of apparently normal term neonates , 2004, Neuroradiology.

[16]  P. Basser,et al.  Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. , 1996, Journal of magnetic resonance. Series B.

[17]  Probst Fp.  Congenital defects of the corpus callosum. Morphology and encephalographic appearances. , 1973 .

[18]  Osamu Abe,et al.  Diffusion abnormality in the posterior cingulum and hippocampal volume: correlation with disease progression in Alzheimer's disease. , 2009, Magnetic resonance imaging.

[19]  F. Probst.  Gas Distension of the Lateral Ventricles at Encephalography , 1973, Acta radiologica: diagnosis.

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

[21]  Derek K. Jones,et al.  The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: A Monte Carlo study † , 2004, Magnetic resonance in medicine.

[22]  Maolin Qiu,et al.  Abnormal anterior cingulum integrity in bipolar disorder determined through diffusion tensor imaging , 2008, British Journal of Psychiatry.

[23]  P Ellen Grant,et al.  Bilateral frontoparietal polymicrogyria: Clinical and radiological features in 10 families with linkage to chromosome 16 , 2003, Annals of neurology.

[24]  F. Probst.  Congenital defects of the corpus callosum. Morphology and encephalographic appearances. , 1973, Acta radiologica. Supplementum.

[25]  C. Finley.  Structure of the Human Brain , 1976 .

[26]  R. Adolphs,et al.  Agenesis of the corpus callosum: genetic, developmental and functional aspects of connectivity , 2007, Nature Reviews Neuroscience.

[27]  D. Velakoulis,et al.  A case of schizophrenia with complete agenesis of the corpus callosum. , 2006, Australasian psychiatry : bulletin of Royal Australian and New Zealand College of Psychiatrists.

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

[29]  G M Innocenti,et al.  Schizophrenia, neurodevelopment and corpus callosum , 2003, Molecular Psychiatry.

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

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

[32]  R. Guerrini,et al.  Bilateral frontoparietal polymicrogyria, Lennox‐Gastaut syndrome, and GPR56 gene mutations , 2009, Epilepsia.

[33]  M. O’Sullivan,et al.  Incidence of ALS in Italy , 2001, Neurology.

[34]  Susumu Mori,et al.  Diffusion-tensor MR imaging and fiber tractography: a new method of describing aberrant fiber connections in developmental CNS anomalies. , 2005, Radiographics : a review publication of the Radiological Society of North America, Inc.

[35]  N. Motomura,et al.  Monozygotic twin cases of the agenesis of the corpus callosum with schizophrenic disorder , 2002, Psychiatry and clinical neurosciences.

[36]  K E FOGHT-NIELSEN,et al.  [Agenesis of the corpus callosum]. , 1954, Ugeskrift for laeger.

[37]  S. Bölte,et al.  Social and Behavioral Problems of Children with Agenesis of the Corpus Callosum , 2007, Child psychiatry and human development.

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

[39]  T. Ohnishi,et al.  Progressive changes of white matter integrity in schizophrenia revealed by diffusion tensor imaging , 2007, Psychiatry Research: Neuroimaging.

[40]  Haruyasu Yamada,et al.  Normal aging in the central nervous system: quantitative MR diffusion-tensor analysis , 2002, Neurobiology of Aging.

[41]  B. Fabre,et al.  Trends in elective terminations of pregnancy between 1989 and 2000 in a French county (the Isère) , 2003, Prenatal diagnosis.

[42]  Jerry L. Prince,et al.  Effects of diffusion weighting schemes on the reproducibility of DTI-derived fractional anisotropy, mean diffusivity, and principal eigenvector measurements at 1.5T , 2007, NeuroImage.

[43]  Roberto Lent,et al.  Neuroplasticity in human callosal dysgenesis: a diffusion tensor imaging study. , 2006, Cerebral cortex.

[44]  M. Jeeves,et al.  Bilateral field advantage and evoked potential interhemispheric transmission in commissurotomy and callosal agenesis , 1999, Neuropsychologia.

[45]  Susumu Mori,et al.  Imaging, anatomical, and molecular analysis of callosal formation in the developing human fetal brain. , 2006, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[46]  G. Shaw,et al.  Agenesis of the corpus callosum in California 1983–2003: A population‐based study , 2008, American journal of medical genetics. Part A.

[47]  H I Goldberg,et al.  Corpus callosum and limbic system: neuroanatomic MR evaluation of developmental anomalies. , 1986, Radiology.

[48]  Osamu Abe,et al.  Quantitative evaluation of the pyramidal tract segmented by diffusion tensor tractography: feasibility study in patients with amyotrophic lateral sclerosis. , 2005, Radiation medicine.

[49]  D. O'Leary,et al.  Axons of early generated neurons in cingulate cortex pioneer the corpus callosum , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.