Examination of Frontal and Parietal Tectocortical Attention Pathways in Spina Bifida Meningomyelocele Using Probabilistic Diffusion Tractography

Abnormalities of the midbrain tectum are common but variable malformations in spina bifida meningomyelocele (SBM) and have been linked to neuropsychological deficits in attention orienting. The degree to which variations in tectum structure influence white matter (WM) connectivity to cortical regions is unknown. To assess the relationship of tectal structure and connectivity to frontal and parietal cortical regions, probabilistic diffusion tractography was performed on 106 individuals (80 SBM, 26 typically developing [TD]) to isolate anterior versus posterior tectocortical WM pathways. Results showed that those with SBM exhibited significantly reduced tectal volume, along with decreased fractional anisotropy (FA) in posterior but not anterior tectocortical WM pathways when compared with TD individuals. The group with SBM also showed greater within-subject discrepancies between frontal and parietal WM integrity compared with the TD group. Of those with SBM, qualitative classification of tectal beaking based on radiological review was associated with increased axial diffusivity across both anterior and posterior tectocortical pathways, relative to individuals with SBM and a normal appearing tectum. These results support previous volumetric findings of greater impairment to posterior versus anterior brain regions in SBM, and quantifiably relate tectal volume, tectocortical WM integrity, and tectal malformations in this population.

[1]  R. Adams,et al.  Limbic tract anomalies in pediatric myelomeningocele and Chiari II malformation: anatomic correlations with memory and learning--initial investigation. , 2006, Radiology.

[2]  Xiaoping Hu,et al.  Chimpanzee (Pan troglodytes) Precentral Corticospinal System Asymmetry and Handedness: A Diffusion Magnetic Resonance Imaging Study , 2010, PloS one.

[3]  Shreesh P Mysore,et al.  The role of a midbrain network in competitive stimulus selection , 2011, Current Opinion in Neurobiology.

[4]  G. V. Simpson,et al.  Dynamic Activation of Frontal, Parietal, and Sensory Regions Underlying Anticipatory Visual Spatial Attention , 2011, The Journal of Neuroscience.

[5]  D. Mclone,et al.  Neurosurgical management of spina bifida: research issues. , 2010, Developmental disabilities research reviews.

[6]  Jenifer Juranek,et al.  Anomalous development of brain structure and function in spina bifida myelomeningocele. , 2010, Developmental disabilities research reviews.

[7]  Bradford C. Dickerson,et al.  A reliable protocol for the manual segmentation of the human amygdala and its subregions using ultra-high resolution MRI , 2012, NeuroImage.

[8]  M. Knaap,et al.  The effect of intracranial pressure on myelination and the relationship with neurodevelopment in infantile hydrocephalus , 1997, Developmental medicine and child neurology.

[9]  R. E. Schmidt,et al.  Toward accurate diagnosis of white matter pathology using diffusion tensor imaging , 2007, Magnetic resonance in medicine.

[10]  Karl J. Friston,et al.  Functional Anatomy of Visual Search: Regional Segregations within the Frontal Eye Fields and Effective Connectivity of the Superior Colliculus , 2002, NeuroImage.

[11]  Heather B. Taylor,et al.  Early information processing among infants with and without spina bifida. , 2010, Infant behavior & development.

[12]  Peter W Dicke,et al.  Neuron-specific contribution of the superior colliculus to overt and covert shifts of attention , 2004, Nature Neuroscience.

[13]  J. Fletcher,et al.  Introduction: Spina bifida--a multidisciplinary perspective. , 2010, Developmental disabilities research reviews.

[14]  Nikos Makris,et al.  Automatically parcellating the human cerebral cortex. , 2004, Cerebral cortex.

[15]  A. Ashley-Koch,et al.  Epidemiologic and genetic aspects of spina bifida and other neural tube defects. , 2010, Developmental disabilities research reviews.

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

[17]  W. J. Oakes,et al.  Degree of tectal beaking correlates to the presence of nystagmus in children with Chiari II malformation , 2004, Child's Nervous System.

[18]  Anders M. Dale,et al.  Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex , 2001, IEEE Transactions on Medical Imaging.

[19]  M. Posner,et al.  The attention system of the human brain. , 1990, Annual review of neuroscience.

[20]  Y. Kinoshita,et al.  Neuronal damage in hydrocephalus and its restoration by shunt insertion in experimental hydrocephalus: a study involving the neurofilament-immunostaining method. , 2006, Journal of neurosurgery.

[21]  Anders M. Dale,et al.  Sequence-independent segmentation of magnetic resonance images , 2004, NeuroImage.

[22]  Daniel Rueckert,et al.  Automatic Cortical Segmentation in the Developing Brain , 2007, IPMI.

[23]  Richard J Krauzlis,et al.  Inactivation of primate superior colliculus impairs covert selection of signals for perceptual judgments , 2010, Nature Neuroscience.

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

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

[26]  B. Merker Consciousness without a cerebral cortex: A challenge for neuroscience and medicine , 2007, Behavioral and Brain Sciences.

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

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

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

[30]  Joshua I. Breier,et al.  Neocortical reorganization in spina bifida , 2008, NeuroImage.

[31]  S. Holland,et al.  Diffusion Tensor Imaging Properties and Neurobehavioral Outcomes in Children with Hydrocephalus , 2013, American Journal of Neuroradiology.

[32]  M. Shokunbi,et al.  The relationship between ventricular dilatation, neuropathological and neurobehavioural changes in hydrocephalic rats , 2012, Fluids and Barriers of the CNS.

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

[34]  Benoit M. Dawant,et al.  Morphometric analysis of white matter lesions in MR images: method and validation , 1994, IEEE Trans. Medical Imaging.

[35]  Timothy Edward John Behrens,et al.  Characterization and propagation of uncertainty in diffusion‐weighted MR imaging , 2003, Magnetic resonance in medicine.

[36]  Nadim Joni Shah,et al.  Probabilistic fibre tract analysis of cytoarchitectonically defined human inferior parietal lobule areas reveals similarities to macaques , 2011, NeuroImage.

[37]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[38]  Richard J Krauzlis,et al.  Inactivation of primate superior colliculus biases target choice for smooth pursuit, saccades, and button press responses. , 2010, Journal of neurophysiology.

[39]  A. Sereno,et al.  Disruption of Reflexive Attention and Eye Movements in an Individual with a Collicular Lesion , 2006, Journal of clinical and experimental neuropsychology.

[40]  J. Drake,et al.  Space-based inhibition of return in children with spina bifida. , 2005, Neuropsychology.

[41]  Yuchuan Ding,et al.  Effects of hydrocephalus and ventriculoperitoneal shunt therapy on afferent and efferent connections in the feline sensorimotor cortex. , 2004, Journal of neurosurgery.

[42]  E. Knudsen,et al.  Control from below: the role of a midbrain network in spatial attention , 2011, The European journal of neuroscience.

[43]  G. D'aliberti,et al.  Myelomeningocele: long-term neurosurgical treatment and follow-up in 202 patients. , 2007, Journal of neurosurgery.

[44]  J. Drake,et al.  Covert orienting to exogenous and endogenous cues in children with spina bifida , 2005, Neuropsychologia.

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

[46]  Luis Concha,et al.  Diffusion tensor imaging of time-dependent axonal and myelin degradation after corpus callosotomy in epilepsy patients , 2006, NeuroImage.