Structure, Integrity, and Function of the Hypoplastic Corpus Callosum in Spina Bifida Myelomeningocele

Although there are many studies of people with complete or partial hypogenesis of the corpus callosum (CC), little is understood about the hypoplastic CC in which all structures are present but thinned. Spina bifida myelomeningocele (SBM) is a model organism for such studies because many have either a hypogenetic or hypoplastic CC. We used diffusion tensor tractography (DTT) to evaluate the hypoplastic CC in SBM and its relation to interhemispheric functions and intelligence quotient (IQ). Participants were individuals with SBM and an intact or hypoplastic CC (n=28), who were compared to a typically developing comparison group (n=32). Total and regional DTT volume and integrity measures (fractional anisotropy, axial diffusivity, and radial diffusivity) of the CC were related to measures of intelligence (IQ), bimanual motor functioning, and dichotic auditory performance. As predicted, DTT showed variations in volume and integrity that were maximized in the entire CC and the posterior CC. IQ correlated with entire CC volume, anterior and posterior regional CC volumes, and also with measures of integrity. Bimanual motor functioning correlated with the anterior and posterior volumes of the CC but not with any integrity measures. Axial diffusivity in the posterior CC was negatively correlated with right ear dichotic listening performance. The hypoplastic CC is not macrostructurally or microstructurally intact in SBM, even when it appears radiologically intact. Both volume and integrity of the posterior regions were related to reductions in IQ and to interhemispheric processing. These findings may transfer to other disorders characterized by a hypoplastic CC.

[1]  M. Lassonde,et al.  Neuropsychological outcome of corpus callosotomy in children and adolescents. , 1997, Journal of neurosurgical sciences.

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

[3]  T. J. Mathews,et al.  Racial/ethnic differences in the birth prevalence of spina bifida - United States, 1995-2005. , 2009 .

[4]  Hajime Tanaka,et al.  Neuroradiological assessment of visuoperceptual disturbance in children with spina bifida and hydrocephalus , 1997, Developmental medicine and child neurology.

[5]  Catherine Lebel,et al.  Six is enough? Comparison of diffusion parameters measured using six or more diffusion‐encoding gradient directions with deterministic tractography , 2012, Magnetic resonance in medicine.

[6]  Larry A. Kramer,et al.  Morphometric evaluation of the hydrocephalic brain: relationships with cognitive development , 1996, Child's Nervous System.

[7]  Y. Assaf,et al.  Diffusion tensor imaging in hydrocephalus: initial experience. , 2006, AJNR. American journal of neuroradiology.

[8]  N M Thompson,et al.  Cerebral white matter and cognition in hydrocephalic children. , 1992, Archives of neurology.

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

[10]  Larry A. Kramer,et al.  Diffusion tensor tractography quantification of the human corpus callosum fiber pathways across the lifespan , 2009, Brain Research.

[11]  A. Pfefferbaum,et al.  MR Diffusion Tensor Imaging: A Window into White Matter Integrity of the Working Brain , 2010, Neuropsychology Review.

[12]  M. D. Del Bigio,et al.  Chronic hydrocephalus in rats and humans: White matter loss and behavior changes , 2003, Annals of neurology.

[13]  Timothy Edward John Behrens,et al.  Integrity of white matter in the corpus callosum correlates with bimanual co-ordination skills , 2007, NeuroImage.

[14]  J M Fletcher,et al.  Interhemispheric transfer of visual, auditory, tactile, and visuomotor information in children with hydrocephalus and partial agenesis of the corpus callosum. , 1999, Journal of clinical and experimental neuropsychology.

[15]  K. Hasan,et al.  Quantitative diffusion tensor imaging and intellectual outcomes in spina bifida: laboratory investigation. , 2008, Journal of neurosurgery. Pediatrics.

[16]  Jens Frahm,et al.  Topography of the human corpus callosum revisited—Comprehensive fiber tractography using diffusion tensor magnetic resonance imaging , 2006, NeuroImage.

[17]  A. Hunter.  Callosal Agenesis: A Natural Split Brain? , 1995 .

[18]  René Westerhausen,et al.  Interhemispheric transfer time and structural properties of the corpus callosum , 2006, Neuroscience Letters.

[19]  G. Geffen,et al.  Interhemispheric control of manual motor activity , 1994, Behavioural Brain Research.

[20]  E. Zaidel,et al.  Anatomical-behavioral relationships: Corpus callosum morphometry and hemispheric specialization , 1994, Behavioural Brain Research.

[21]  M. Sperling,et al.  Corpus callosotomy in refractory idiopathic generalized epilepsy , 2006, Seizure.

[22]  J. Giedd.  Structural Magnetic Resonance Imaging of the Adolescent Brain , 2004, Annals of the New York Academy of Sciences.

[23]  A. Scheibel,et al.  Fiber composition of the human corpus callosum , 1992, Brain Research.

[24]  P. Lachenbruch.  Statistical Power Analysis for the Behavioral Sciences (2nd ed.) , 1989 .

[25]  K. Hugdahl.  Dichotic Listening in the study of auditory laterality. , 2003 .

[26]  J. O’Kusky,et al.  The corpus callosum is larger with right‐hemisphere cerebral speech dominance , 1988, Annals of neurology.

[27]  J. Drake,et al.  Spinal lesion level in spina bifida: a source of neural and cognitive heterogeneity. , 2005, Journal of neurosurgery.

[28]  B. Peterson,et al.  Functional significance of individual variations in callosal area , 1995, Neuropsychologia.

[29]  M. A. Merrill,et al.  Stanford-Binet Intelligence Scale , 1972 .

[30]  S. F. Witelson.  Hand and sex differences in the isthmus and genu of the human corpus callosum. A postmortem morphological study. , 1989, Brain : a journal of neurology.

[31]  M. Gazzaniga,et al.  Dichotic testing of partial and complete split brain subjects , 1975, Neuropsychologia.

[32]  Khader M Hasan,et al.  A framework for quality control and parameter optimization in diffusion tensor imaging: theoretical analysis and validation. , 2007, Magnetic resonance imaging.

[33]  Maureen Dennis,et al.  Auditory interhemispheric transfer in relation to patterns of partial agenesis and hypoplasia of the corpus callosum in spina bifida meningomyelocele , 2008, Journal of the International Neuropsychological Society.

[34]  André J. W. van der Kouwe,et al.  The relationship between diffusion tensor imaging and volumetry as measures of white matter properties , 2008, NeuroImage.

[35]  Maria Blatow,et al.  DTI of commissural fibers in patients with Chiari II-malformation , 2009, NeuroImage.

[36]  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.

[37]  Guido Gerig,et al.  Diffusion tensor imaging: Application to the study of the developing brain. , 2007, Journal of the American Academy of Child and Adolescent Psychiatry.

[38]  Khader M Hasan,et al.  Retrospective measurement of the diffusion tensor eigenvalues from diffusion anisotropy and mean diffusivity in DTI , 2006, Magnetic resonance in medicine.

[39]  M. Dennis,et al.  The old and the new: supratentorial MR findings in Chiari II malformation , 2008, Child's Nervous System.

[40]  J. Fletcher,et al.  The Cerebellum in Children with Spina Bifida and Chiari II Malformation: Quantitative Volumetrics by Region , 2010, The Cerebellum.

[41]  Khader M Hasan,et al.  Transcallosal connectivity and cortical rhythms: findings in children with spina bifida , 2009, Neuroreport.

[42]  Maureen Dennis,et al.  Idiom comprehension deficits in relation to corpus callosum agenesis and hypoplasia in children with spina bifida meningomyelocele , 2005, Brain and Language.

[43]  L. Kramer,et al.  Partial agenesis of the corpus callosum in spina bifida meningomyelocele and potential compensatory mechanisms , 2009, Journal of clinical and experimental neuropsychology.

[44]  Christian Beaulieu,et al.  Voxel based versus region of interest analysis in diffusion tensor imaging of neurodevelopment , 2007, NeuroImage.