Local mechanical properties of white matter structures in the human brain

The noninvasive measurement of the mechanical properties of brain tissue using magnetic resonance elastography (MRE) has emerged as a promising method for investigating neurological disorders. To date, brain MRE investigations have been limited to reporting global mechanical properties, though quantification of the stiffness of specific structures in the white matter architecture may be valuable in assessing the localized effects of disease. This paper reports the mechanical properties of the corpus callosum and corona radiata measured in healthy volunteers using MRE and atlas-based segmentation. Both structures were found to be significantly stiffer than overall white matter, with the corpus callosum exhibiting greater stiffness and less viscous damping than the corona radiata. Reliability of both local and global measures was assessed through repeated experiments, and the coefficient of variation for each measure was less than 10%. Mechanical properties within the corpus callosum and corona radiata demonstrated correlations with measures from diffusion tensor imaging pertaining to axonal microstructure.

[1]  K D Paulsen,et al.  An octahedral shear strain-based measure of SNR for 3D MR elastography , 2011, Physics in medicine and biology.

[2]  C. Jack,et al.  Ways toward an early diagnosis in Alzheimer’s disease: The Alzheimer’s Disease Neuroimaging Initiative (ADNI) , 2005, Alzheimer's & Dementia.

[3]  M W Weiner,et al.  Evaluation of treatment effects in Alzheimer's and other neurodegenerative diseases by MRI and MRS , 2006, NMR in biomedicine.

[4]  Hsiao-Fang Liang,et al.  Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosum , 2006, Magnetic resonance in medicine.

[5]  E. H. Clayton,et al.  Transmission, attenuation and reflection of shear waves in the human brain , 2012, Journal of The Royal Society Interface.

[6]  Douglas L. Rosene,et al.  The Geometric Structure of the Brain Fiber Pathways , 2012, Science.

[7]  Lynne E. Bilston,et al.  Combining MR elastography and diffusion tensor imaging for the assessment of anisotropic mechanical properties: A phantom study , 2013, Journal of magnetic resonance imaging : JMRI.

[8]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[9]  R. Sinkus,et al.  Viscoelastic properties of human cerebellum using magnetic resonance elastography. , 2011, Journal of biomechanics.

[10]  J. Georgiadis,et al.  Multiresolution MR elastography using nonlinear inversion. , 2012, Medical physics.

[11]  Ralph Sinkus,et al.  In vivo brain viscoelastic properties measured by magnetic resonance elastography , 2008, NMR in biomedicine.

[12]  B. Morrison,et al.  Dynamic, regional mechanical properties of the porcine brain: indentation in the coronal plane. , 2011, Journal of biomechanical engineering.

[13]  Jeffrey A. Cohen,et al.  Differential diagnosis of suspected multiple sclerosis: a consensus approach , 2008, Multiple sclerosis.

[14]  J Mazziotta,et al.  A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

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

[17]  Mohammad Ali Sahraian,et al.  Role of MRI in diagnosis and treatment of multiple sclerosis , 2010, Clinical Neurology and Neurosurgery.

[18]  F. Velardi,et al.  Anisotropic constitutive equations and experimental tensile behavior of brain tissue , 2006, Biomechanics and modeling in mechanobiology.

[19]  P. Rakić,et al.  Cytological and quantitative characteristics of four cerebral commissures in the rhesus monkey , 1990, The Journal of comparative neurology.

[20]  Dagmar Krefting,et al.  Brain Viscoelasticity Alteration in Chronic-Progressive Multiple Sclerosis , 2012, PloS one.

[21]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

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

[23]  K D Paulsen,et al.  Three‐dimensional subzone‐based reconstruction algorithm for MR elastography , 2001, Magnetic resonance in medicine.

[24]  Dieter Klatt,et al.  In vivo viscoelastic properties of the brain in normal pressure hydrocephalus , 2010, NMR in biomedicine.

[25]  P. Basser,et al.  In vivo measurement of axon diameter distribution in the corpus callosum of rat brain. , 2009, Brain : a journal of neurology.

[26]  Ralph Sinkus,et al.  Demyelination reduces brain parenchymal stiffness quantified in vivo by magnetic resonance elastography , 2012, Proceedings of the National Academy of Sciences.

[27]  F. Aboitiz,et al.  One hundred million years of interhemispheric communication: the history of the corpus callosum. , 2003, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[28]  D. Klatt,et al.  Three-dimensional analysis of shear wave propagation observed by in vivo magnetic resonance elastography of the brain. , 2007, Acta biomaterialia.

[29]  van der Tpj Tom Sande,et al.  Mechanical properties of brain tissue by indentation: interregional variation. , 2010, Journal of the mechanical behavior of biomedical materials.

[30]  Ivan Cohen,et al.  In Vivo Mapping of Brain Elasticity in Small Animals Using Shear Wave Imaging , 2011, IEEE Transactions on Medical Imaging.

[31]  John B Weaver,et al.  Brain mechanical property measurement using MRE with intrinsic activation , 2012, Physics in medicine and biology.

[32]  Jürgen Braun,et al.  Magnetic resonance elastography reveals altered brain viscoelasticity in experimental autoimmune encephalomyelitis , 2012, NeuroImage: Clinical.

[33]  Dieter Klatt,et al.  Alteration of brain viscoelasticity after shunt treatment in normal pressure hydrocephalus , 2012, Neuroradiology.

[34]  C. Jack,et al.  Decreased brain stiffness in Alzheimer's disease determined by magnetic resonance elastography , 2011, Journal of magnetic resonance imaging : JMRI.

[35]  Dieter Klatt,et al.  The impact of aging and gender on brain viscoelasticity , 2009, NeuroImage.

[36]  Michael I. Miller,et al.  Multi-Modal MRI Analysis with Disease-Specific Spatial Filtering: Initial Testing to Predict Mild Cognitive Impairment Patients Who Convert to Alzheimer’s Disease , 2011, Front. Neur..

[37]  Jürgen Braun,et al.  Fractal network dimension and viscoelastic powerlaw behavior: I. A modeling approach based on a coarse-graining procedure combined with shear oscillatory rheometry , 2012, Physics in medicine and biology.

[38]  K D Paulsen,et al.  Effects of frequency- and direction-dependent elastic materials on linearly elastic MRE image reconstructions , 2010, Physics in medicine and biology.

[39]  A. Manduca,et al.  Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. , 1995, Science.

[40]  Frauke Zipp,et al.  MR-elastography reveals degradation of tissue integrity in multiple sclerosis , 2010, NeuroImage.

[41]  P. Hagmann,et al.  Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging , 2005, Magnetic resonance in medicine.

[42]  John C. Mazziotta,et al.  A Probabilistic Atlas and Reference System for the Human Brain , 2001 .

[43]  Arthur W. Toga,et al.  Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template , 2008, NeuroImage.

[44]  S. Margulies,et al.  A fiber-reinforced composite model of the viscoelastic behavior of the brainstem in shear. , 1999, Journal of biomechanics.

[45]  Matthias Taupitz,et al.  Fractal network dimension and viscoelastic powerlaw behavior: II. An experimental study of structure-mimicking phantoms by magnetic resonance elastography , 2012, Physics in medicine and biology.

[46]  Jürgen Braun,et al.  In vivo waveguide elastography of white matter tracts in the human brain , 2012, Magnetic resonance in medicine.

[47]  K. Trinkaus,et al.  Quantification of increased cellularity during inflammatory demyelination. , 2011, Brain : a journal of neurology.

[48]  Jürgen Braun,et al.  Multifrequency inversion in magnetic resonance elastography , 2012, Physics in medicine and biology.

[49]  Curtis L. Johnson,et al.  Magnetic resonance elastography of the brain using multishot spiral readouts with self‐navigated motion correction , 2013, Magnetic resonance in medicine.

[50]  Dagmar Krefting,et al.  The Influence of Physiological Aging and Atrophy on Brain Viscoelastic Properties in Humans , 2011, PloS one.

[51]  M. Prange,et al.  Regional, directional, and age-dependent properties of the brain undergoing large deformation. , 2002, Journal of biomechanical engineering.