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. 2012 Feb 1;59(3):2088-97.
doi: 10.1016/j.neuroimage.2011.10.038. Epub 2011 Oct 20.

Magnetic susceptibility anisotropy of human brain in vivo and its molecular underpinnings

Wei Li  1 , Bing Wu, Alexandru V Avram, Chunlei Liu
Affiliations

Magnetic susceptibility anisotropy of human brain in vivo and its molecular underpinnings

Wei Li et al. Neuroimage. .

Abstract

Frequency shift of gradient-echo MRI provides valuable information for assessing brain tissues. Recent studies suggest that the frequency and susceptibility contrast depend on white matter fiber orientation. However, the molecular underpinning of the orientation dependence is unclear. In this study, we investigated the orientation dependence of susceptibility of human brain in vivo and mouse brains ex vivo. The source of susceptibility anisotropy in white matter is likely to be myelin as evidenced by the loss of anisotropy in the dysmyelinating shiverer mouse brain. A biophysical model is developed to investigate the effect of the molecular susceptibility anisotropy of myelin components, especially myelin lipids, on the bulk anisotropy observed by MRI. This model provides a consistent interpretation of the orientation dependence of macroscopic magnetic susceptibility in normal mouse brain ex vivo and human brain in vivo and the microscopic origin of anisotropic susceptibility. It is predicted by the theoretical model and illustrated by the experimental data that the magnetic susceptibility of the white matter is least diamagnetic along the fiber direction. This relationship allows an efficient extraction of fiber orientation using susceptibility tensor imaging. These results suggest that anisotropy on the molecular level can be observed on the macroscopic level when the molecules are aligned in a highly ordered manner. Similar to the utilization of magnetic susceptibility anisotropy in elucidating molecular structures, imaging magnetic susceptibility anisotropy may also provide a useful tool for elucidating the microstructure of ordered biological tissues.

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Figures

Fig. 1
Fig. 1. The axon and molecular coordinate systems
A. An electron-micrograph of the white matter fiber architecture of a wild-type mouse (The EM figure is courtesy of Gabriel Corfas, PhD, of Harvard University). B. A schematic representation of the myelin sheath. C. A schematic representation of the radial alignment of membrane lipid molecules. D. The axon coordinate system (x, y and z) and the molecular coordinate system (x′, y′ and z′). The z-axis is parallel to the fiber direction, and the x-axis is in the plane defined by z-axis and H0 direction. The z′-axis is parallel to the z-axis. The angle between x′ and x axes is φ.
Fig. 2
Fig. 2. Orientation dependence of AMS in normal and dysmyelinating shiverer mice
A and D: frequency maps from 3 selected brain orientations. A representative selection of ROI is shown in the lower panel of A. ROIs in the white matter are labeled by red, magenta, and blue colors; ROIs in the corresponding adjacent gray matter are labeled by green, cyan, and yellow colors. B and E: AMS corresponding to the frequency shifts shown in A and D. C and F: AMS difference between white and gray matter. All data points are shown as mean ± standard error. Susceptibility anisotropy is observed in the control mice but not in shiverer mice. The angles shown on the images are the angles between the directions of the white matter segment (red ROI pointed by a red arrow) determined by DTI and the main field, e.g., 0° means that the selected fiber segment is parallel to the main magnetic field. The ROI color in panel A corresponds to the data point color in panel C and F.
Fig. 3
Fig. 3. Frequency maps from different head orientations
A-C shows the frequency maps from one axial slice, and D-F shows frequency maps from another axial slice.
Fig 4
Fig 4. Susceptibility tensors and evidence of susceptibility anisotropy
A: Maps of all 6 elements of the susceptibility tensor of a representative axial slice. The red arrows point to a white matter fiber bundle, which shows significantly different susceptibility along different image axis. B. The diagonal tensor elements in two different sagittal slices. Red arrows point to the sagittal striatum, green and blue arrows point to two segments of corpus callosum, which show different image contrast along different image axis.
Fig. 5
Fig. 5. Principal, mean susceptibilities and susceptibility anisotropy in the human brain
The three principal susceptibilities of the same two slices in Fig. 4 are shown from left to right in a descending order. The increasing image intensity show strong susceptibility anisotropy in the white matter. A reduced level anisotropy is also observed in the gray matter. The region in mean susceptibility map labeled with red color is used for calculation of susceptibility anisotropy.
Fig. 6
Fig. 6. Orientation dependence of AMS in human brain in vivo
A: the overlay of the ROI of white matter (red and blue) and gray matter (green and yellow) on top of the AMS map. B: AMS difference between white and gray matter.
Fig. 7
Fig. 7. Comparison of the eigenvectors of diffusion and susceptibility tensors in the human brain
In the first two rows, both DTI and STI color maps are weighted by the same fractional anisotropy map of DTI for an unbiased comparison. In the bottom row, the STI eigenvector map is weighted by the rescaled mean susceptibility. The corpus callosum/superior corona radiata and the cingulate gyrus (in axial view), as well as the corpus callosum and the cingulate gyrus (in sagittal view) are clearly separated with consistent orientations between STI and DTI (red and green arrows). Differences also exist (white arrows) which may be caused by imperfect image registration.
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