Abstract
Human brain tissue is a heterogeneous material, consisting of soft outer grey matter tethered internally by stiffer cords of white matter. These white matter tracts conduct electrical impulses between grey matter regions, thereby underpinning neuronal communication. Understanding the material properties of white matter is thus crucial for understanding brain function generally. Efforts to assess white matter microstructure are currently hampered by the inherent limitations of reconstruction by diffusion imaging. Techniques typically represent white matter structures with single scalars that are often difficult to interpret. Here, we address these issues by introducing tools from materials physics for the characterization of white matter microstructure. We investigate structure on a mesoscopic scale by analyzing its homogeneity and determining which regions of the brain are structurally homogeneous, or ‘crystalline’ in the context of materials physics. We find that crystallinity provides novel information and varies across the brain along interpretable lines of anatomical difference, with highest homogeneity in regions adjacent to the corpus callosum, a large interhemispheric tract. Furthermore, crystallinity is markedly reliable across iterative measurement, yet also varies between individual human volunteers, making it potentially useful for examining individual differences in white matter along several dimensions including sex and age. We also parcellate white matter into ‘crystal grains’, or contiguous sets of voxels of high structural similarity, and find overlap with a common atlas of distinct white matter areas. Finally, we characterize the shapes of individual diffusion signatures through another tool from materials physics—bond-orientational order parameters—to locate fiber crossings and fascicles. Our results provide new means of assessing white matter microstructure on multiple length scales, and open multiple avenues of future inquiry involving soft matter physics and neuroscience.
Highlights
The fields of soft matter and diffusion MRI, each relative newcomers in their respective scientific corners, may seem at first glance quite unrelated
We determine which regions of the brain are structurally homogeneous, or “crystalline” in the context of materials science, and which are structurally heterogeneous, or “disordered.” We find that white matter homogeneity, or crystallinity, provides information about neuronal architecture that is independent of other structural measurements often used in the neuroimaging community such as fractional anisotropy and mean diffusivity
We first demonstrate that crystallinity varies across the brain in a meaningful and interpretable way, and provides new structural information that is not measured by other diffusion metrics commonly used in the neuroimaging community
Summary
The fields of soft matter and diffusion MRI, each relative newcomers in their respective scientific corners, may seem at first glance quite unrelated. Diffusion MRI, by contrast, lies at the intersection of engineering and neuroscience, and is focused primarily on characterizing microstructure in a very specific macroscale organ, the brain[1]. Both fields, are concerned with understanding structure, and its relationship to function. The orientation of myelinated white matter structures is estimated in millimeterscale regions of the brain based on observed magnetic resonance (MR) signal changes related to water diffusion. Local white matter orientation distribution functions (ODFs) can be used to track large white matter fascicles[5] between cortical regions. White matter connectivity underlies normal brain function, and disruption of these connections is hypothesized to contribute to a variety of pathologies that may arise in abnormal development and following injury[6]
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