Crystallinity characterization of white matter in the human brain

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 proper...

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Main Authors: Erin G Teich, Matthew Cieslak, Barry Giesbrecht, Jean M Vettel, Scott T Grafton, Theodore D Satterthwaite, Danielle S Bassett
Format: Article
Language:English
Published: IOP Publishing 2021-01-01
Series:New Journal of Physics
Subjects:
Online Access:https://doi.org/10.1088/1367-2630/ac1286
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author Erin G Teich
Matthew Cieslak
Barry Giesbrecht
Jean M Vettel
Scott T Grafton
Theodore D Satterthwaite
Danielle S Bassett
author_facet Erin G Teich
Matthew Cieslak
Barry Giesbrecht
Jean M Vettel
Scott T Grafton
Theodore D Satterthwaite
Danielle S Bassett
author_sort Erin G Teich
collection DOAJ
description 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.
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spelling doaj.art-060376bb36284f26a52b3bb1206ae9ca2023-08-08T15:41:26ZengIOP PublishingNew Journal of Physics1367-26302021-01-0123707304710.1088/1367-2630/ac1286Crystallinity characterization of white matter in the human brainErin G Teich0https://orcid.org/0000-0001-7553-7054Matthew Cieslak1https://orcid.org/0000-0002-1931-4734Barry Giesbrecht2https://orcid.org/0000-0002-1976-1251Jean M Vettel3Scott T Grafton4Theodore D Satterthwaite5Danielle S Bassett6https://orcid.org/0000-0002-6183-4493Department of Bioengineering, School of Engineering & Applied Science, University of Pennsylvania , Philadelphia, PA 19104, United States of AmericaDepartment of Psychiatry, Perelman School of Medicine, University of Pennsylvania , Philadelphia, PA 19104, United States of AmericaDepartment of Psychological & Brain Sciences, University of California , Santa Barbara, CA 93117, United States of AmericaArmy Research Laboratory , Aberdeen Proving Ground, MD 21005, United States of AmericaDepartment of Psychological & Brain Sciences, University of California , Santa Barbara, CA 93117, United States of AmericaDepartment of Psychiatry, Perelman School of Medicine, University of Pennsylvania , Philadelphia, PA 19104, United States of AmericaDepartment of Bioengineering, School of Engineering & Applied Science, University of Pennsylvania , Philadelphia, PA 19104, United States of America; Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania , Philadelphia, PA 19104, United States of America; Department of Physics and Astronomy, College of Arts & Sciences, University of Pennsylvania , Philadelphia, PA 19104, United States of America; Department of Electrical and Systems Engineering, School of Engineering & Applied Science, University of Pennsylvania , Philadelphia, PA 19104, United States of America; Department of Neurology, Perelman School of Medicine, University of Pennsylvania , Philadelphia, PA 19104, United States of America; Santa Fe Institute , Santa Fe, NM 87501, United States of AmericaHuman 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.https://doi.org/10.1088/1367-2630/ac1286diffusion MRIwhite mattercrystallinitystructural characterization
spellingShingle Erin G Teich
Matthew Cieslak
Barry Giesbrecht
Jean M Vettel
Scott T Grafton
Theodore D Satterthwaite
Danielle S Bassett
Crystallinity characterization of white matter in the human brain
New Journal of Physics
diffusion MRI
white matter
crystallinity
structural characterization
title Crystallinity characterization of white matter in the human brain
title_full Crystallinity characterization of white matter in the human brain
title_fullStr Crystallinity characterization of white matter in the human brain
title_full_unstemmed Crystallinity characterization of white matter in the human brain
title_short Crystallinity characterization of white matter in the human brain
title_sort crystallinity characterization of white matter in the human brain
topic diffusion MRI
white matter
crystallinity
structural characterization
url https://doi.org/10.1088/1367-2630/ac1286
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