The impact of fibre orientation on T1-relaxation and apparent tissue water content in white matter

ObjectiveRecent MRI studies have shown that the orientation of nerve fibres relative to the main magnetic field affects the R2*(= 1/T2*) relaxation rate in white matter (WM) structures. The underlying physical causes have been discussed in several studies but are still not completely understood. However, understanding these effects in detail is of great importance since this might serve as a basis for the development of new diagnostic tools and/or improve quantitative susceptibility mapping techniques. Therefore, in addition to the known angular dependence of R2*, the current study investigates the relationship between fibre orientation and the longitudinal relaxation rate, R1 (= 1/T1), as well as the apparent water content.Materials and methodsFor a group of 16 healthy subjects, a series of gradient echo, echo-planar and diffusion weighted images were acquired at 3T from which the decay rates, the apparent water content and the diffusion direction were reconstructed. The diffusion weighted data were used to determine the angle between the principle fibre direction and the main magnetic field to examine the angular dependence of R1 and apparent water content.ResultsThe obtained results demonstrate that both parameters depend on the fibre orientation and exhibit a positive correlation with the angle between fibre direction and main magnetic field.ConclusionThese observations could be helpful to improve and/or constrain existing biophysical models of brain microstructure by imposing additional constraints resulting from the observed angular dependence R1 and apparent water content in white matter.

[1]  Paul M. Matthews,et al.  Brain Microstructure Reveals Early Abnormalities more than Two Years prior to Clinical Progression from Mild Cognitive Impairment to Alzheimer's Disease , 2013, The Journal of Neuroscience.

[2]  R. Bryant,et al.  Translational dynamics of water at the phospholipid interface. , 2013, The journal of physical chemistry. B.

[3]  Karla L. Miller,et al.  Detecting microstructural properties of white matter based on compartmentalization of magnetic susceptibility , 2013, NeuroImage.

[4]  J. Caillé,et al.  Early structural changes in acute MS lesions assessed by serial magnetization transfer studies , 1998, Neurology.

[5]  Mark Bydder,et al.  The magic angle effect: A source of artifact, determinant of image contrast, and technique for imaging , 2007, Journal of magnetic resonance imaging : JMRI.

[6]  Dmitriy A Yablonskiy,et al.  Biophysical mechanisms of myelin‐induced water frequency shifts , 2014, Magnetic resonance in medicine.

[7]  G. B. Pike,et al.  Quantitative imaging of magnetization transfer exchange and relaxation properties in vivo using MRI , 2001, Magnetic resonance in medicine.

[8]  Nadim Joni Shah,et al.  Fast quantitative mapping of absolute water content with full brain coverage , 2008, NeuroImage.

[9]  Jeff H. Duyn,et al.  Micro-compartment specific T2 ⁎ relaxation in the brain , 2013, NeuroImage.

[10]  Zang-Hee Cho,et al.  Origin of B0 orientation dependent R2 * (=1/T2 *) in white matter , 2013, NeuroImage.

[11]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[12]  Nikos Evangelou,et al.  Quantitative pathological evidence for axonal loss in normal appearing white matter in multiple sclerosis , 2000, Annals of neurology.

[13]  A. MacKay,et al.  The influence of white matter fibre orientation on MR signal phase and decay , 2011, NMR in biomedicine.

[14]  H. Neeb,et al.  Rapid myelin water content mapping on clinical MR systems. , 2012, Zeitschrift für Medizinische Physik.

[15]  Klaus Scheffler,et al.  Specific white matter tissue microstructure changes associated with obesity , 2016, NeuroImage.

[16]  A. Sukstanskii,et al.  On the role of neuronal magnetic susceptibility and structure symmetry on gradient echo MR signal formation , 2014, Magnetic resonance in medicine.

[17]  Bing Wu,et al.  Magnetic susceptibility anisotropy of human brain in vivo and its molecular underpinnings , 2012, NeuroImage.

[18]  Y. Lange,et al.  Diffusion processes in lipid-water lamellar phases. , 1972, Biochimica et biophysica acta.

[19]  Jeff H. Duyn,et al.  The contribution of myelin to magnetic susceptibility-weighted contrasts in high-field MRI of the brain , 2012, NeuroImage.

[20]  M. Filippi,et al.  Magnetisation transfer ratios of contrast-enhancing and nonenhancing lesions in multiple sclerosis , 1996, Neuroradiology.

[21]  Bernd Weber,et al.  Multicentre absolute myelin water content mapping: Development of a whole brain atlas and application to low-grade multiple sclerosis☆ , 2012, NeuroImage: Clinical.

[22]  P. Basser,et al.  Heterogeneous anisotropic magnetic susceptibility of the myelin‐water layers causes local magnetic field perturbations in axons , 2017, NMR in biomedicine.

[23]  U. Klose,et al.  The in vivo influence of white matter fiber orientation towards B0 on T2* in the human brain , 2010, NMR in biomedicine.

[24]  A. Peters.  The effects of normal aging on myelin and nerve fibers: A review , 2002, Journal of neurocytology.

[25]  R. Bowtell,et al.  Fiber orientation-dependent white matter contrast in gradient echo MRI , 2012, Proceedings of the National Academy of Sciences.

[26]  C. Laule,et al.  Water content and myelin water fraction in multiple sclerosis , 2004, Journal of Neurology.

[27]  M Filippi,et al.  Long-term changes of magnetization transfer-derived measures from patients with relapsing-remitting and secondary progressive multiple sclerosis. , 1999, AJNR. American journal of neuroradiology.

[28]  Thomas H. B. FitzGerald,et al.  Widespread age-related differences in the human brain microstructure revealed by quantitative magnetic resonance imaging , 2014, Neurobiology of Aging.

[29]  P. Roy,et al.  Age-Related Differences in White Matter Integrity in Healthy Human Brain: Evidence from Structural MRI and Diffusion Tensor Imaging , 2016, Magnetic resonance insights.

[30]  Heidi Johansen-Berg,et al.  Myelin water imaging reflects clinical variability in multiple sclerosis , 2012, NeuroImage.

[31]  Dong-Hyun Kim,et al.  Mechanisms of T2* anisotropy and gradient echo myelin water imaging , 2017, NMR in biomedicine.

[32]  Karla L Miller,et al.  The effect of realistic geometries on the susceptibility‐weighted MR signal in white matter , 2017, Magnetic resonance in medicine.

[33]  A. D. McLachlan,et al.  Introduction to magnetic resonance : with applications to chemistry and chemical physics , 1967 .

[34]  Nadim Joni Shah,et al.  Fully-automated detection of cerebral water content changes: Study of age- and gender-related H2O patterns with quantitative MRI , 2006, NeuroImage.

[35]  Harald E. Möller,et al.  Orientation dependence of magnetization transfer parameters in human white matter , 2015, NeuroImage.

[36]  Anthony Traboulsee,et al.  Orientation Dependent MR Signal Decay Differentiates between People with MS, Their Asymptomatic Siblings and Unrelated Healthy Controls , 2015, PloS one.

[37]  J. Duyn.  Frequency shifts in the myelin water compartment , 2014, Magnetic resonance in medicine.

[38]  B. Trapp,et al.  Structure of the Myelinated Axon , 2004 .

[39]  Bing Wu,et al.  High-field (9.4T) MRI of brain dysmyelination by quantitative mapping of magnetic susceptibility , 2011, NeuroImage.

[40]  M Rovaris,et al.  Changes in the normal appearing brain tissue and cognitive impairment in multiple sclerosis , 2000, Journal of neurology, neurosurgery, and psychiatry.

[41]  Jeff H. Duyn,et al.  T2*-based fiber orientation mapping , 2011, NeuroImage.

[42]  D. Arnold,et al.  Evolution of focal and diffuse magnetisation transfer abnormalities in multiple sclerosis , 2003, Journal of Neurology.

[43]  S. Nelson,et al.  Multislice Brain Myelin Water Fractions at 3T in Multiple Sclerosis , 2007, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[44]  M. Cavaglià,et al.  Regional variation in brain capillary density and vascular response to ischemia , 2001, Brain Research.

[45]  Se-Hong Oh,et al.  Origin of B 0 orientation dependent R 2 * ( = 1 / T 2 * ) in white matter : magic angle effect vs . magnetic susceptibility , 2012 .

[46]  P. Burger,et al.  MR imaging of compact white matter pathways. , 1988, AJNR. American journal of neuroradiology.