Nanostructure-specific X-ray tomography reveals myelin levels, integrity and axon orientations in mouse and human nervous tissue

Myelin insulates neuronal axons and enables fast signal transmission, constituting a key component of brain development, aging and disease. Yet, myelin-specific imaging of macroscopic samples remains a challenge. Here, we exploit myelin’s nanostructural periodicity, and use small-angle X-ray scatter...

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Published inNature communications Vol. 12; no. 1; pp. 2941 - 13
Main Authors Georgiadis, Marios, Schroeter, Aileen, Gao, Zirui, Guizar-Sicairos, Manuel, Liebi, Marianne, Leuze, Christoph, McNab, Jennifer A., Balolia, Aleezah, Veraart, Jelle, Ades-Aron, Benjamin, Kim, Sunglyoung, Shepherd, Timothy, Lee, Choong H., Walczak, Piotr, Chodankar, Shirish, DiGiacomo, Phillip, David, Gergely, Augath, Mark, Zerbi, Valerio, Sommer, Stefan, Rajkovic, Ivan, Weiss, Thomas, Bunk, Oliver, Yang, Lin, Zhang, Jiangyang, Novikov, Dmitry S., Zeineh, Michael, Fieremans, Els, Rudin, Markus
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 19.05.2021
Nature Publishing Group
Nature Portfolio
Subjects
101/1
14/19
59/57
631/1647/245
631/378/2606
631/535/1261
639/925/930/2735
692/698/1688
96/34
Aging
Animals
Axons
Axons - metabolism
Axons - ultrastructure
BASIC BIOLOGICAL SCIENCES
Biomolecules
Brain
Brain - metabolism
Brain - ultrastructure
Central Nervous System - diagnostic imaging
Central Nervous System - metabolism
Central Nervous System - ultrastructure
Child, Preschool
Female
Histology
Humanities and Social Sciences
Humans
imaging
imaging techniques
Integrity
Magnetic resonance imaging
Magnetic Resonance Imaging - methods
Male
MATERIALS SCIENCE
Mathematical analysis
Medical imaging
Mice
Mice, Inbred C57BL
Mice, Knockout
multidisciplinary
Myelin
Myelin biology and repair
Myelin Proteins - metabolism
Myelin Sheath - metabolism
Myelin Sheath - ultrastructure
Myelination
Nanostructure
Nanostructures - chemistry
Nanostructures - ultrastructure
nervous system
Nervous tissues
Neuroimaging
Neuroimaging - methods
Periodicity
Proof of Concept Study
Quantitative research
SAXS
Scattering, Small Angle
Science
Science (multidisciplinary)
Signal transmission
Small angle X ray scattering
Spinal cord
Spinal Cord - metabolism
Spinal Cord - ultrastructure
Substantia grisea
Tensors
Tomography
Tomography, X-Ray Computed - methods
X-ray scattering
X-rays
Online AccessGet full text

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Abstract Myelin insulates neuronal axons and enables fast signal transmission, constituting a key component of brain development, aging and disease. Yet, myelin-specific imaging of macroscopic samples remains a challenge. Here, we exploit myelin’s nanostructural periodicity, and use small-angle X-ray scattering tensor tomography (SAXS-TT) to simultaneously quantify myelin levels, nanostructural integrity and axon orientations in nervous tissue. Proof-of-principle is demonstrated in whole mouse brain, mouse spinal cord and human white and gray matter samples. Outcomes are validated by 2D/3D histology and compared to MRI measurements sensitive to myelin and axon orientations. Specificity to nanostructure is exemplified by concomitantly imaging different myelin types with distinct periodicities. Finally, we illustrate the method’s sensitivity towards myelin-related diseases by quantifying myelin alterations in dysmyelinated mouse brain. This non-destructive, stain-free molecular imaging approach enables quantitative studies of myelination within and across samples during development, aging, disease and treatment, and is applicable to other ordered biomolecules or nanostructures. Small-angle X-ray scattering (SAXS) combines the high tissue penetration of X-rays with specificity to periodic nanostructures. The authors use SAXS tensor tomography (SAXS-TT) on intact mouse and human brain tissue samples, to quantify myelin levels and determine myelin integrity, myelinated axon orientation, and fibre tracts non-destructively.
AbstractList Myelin insulates neuronal axons and enables fast signal transmission, constituting a key component of brain development, aging and disease. Yet, myelin-specific imaging of macroscopic samples remains a challenge. Here, we exploit myelin's nanostructural periodicity, and use small-angle X-ray scattering tensor tomography (SAXS-TT) to simultaneously quantify myelin levels, nanostructural integrity and axon orientations in nervous tissue. Proof-of-principle is demonstrated in whole mouse brain, mouse spinal cord and human white and gray matter samples. Outcomes are validated by 2D/3D histology and compared to MRI measurements sensitive to myelin and axon orientations. Specificity to nanostructure is exemplified by concomitantly imaging different myelin types with distinct periodicities. Finally, we illustrate the method's sensitivity towards myelin-related diseases by quantifying myelin alterations in dysmyelinated mouse brain. This non-destructive, stain-free molecular imaging approach enables quantitative studies of myelination within and across samples during development, aging, disease and treatment, and is applicable to other ordered biomolecules or nanostructures.Myelin insulates neuronal axons and enables fast signal transmission, constituting a key component of brain development, aging and disease. Yet, myelin-specific imaging of macroscopic samples remains a challenge. Here, we exploit myelin's nanostructural periodicity, and use small-angle X-ray scattering tensor tomography (SAXS-TT) to simultaneously quantify myelin levels, nanostructural integrity and axon orientations in nervous tissue. Proof-of-principle is demonstrated in whole mouse brain, mouse spinal cord and human white and gray matter samples. Outcomes are validated by 2D/3D histology and compared to MRI measurements sensitive to myelin and axon orientations. Specificity to nanostructure is exemplified by concomitantly imaging different myelin types with distinct periodicities. Finally, we illustrate the method's sensitivity towards myelin-related diseases by quantifying myelin alterations in dysmyelinated mouse brain. This non-destructive, stain-free molecular imaging approach enables quantitative studies of myelination within and across samples during development, aging, disease and treatment, and is applicable to other ordered biomolecules or nanostructures.
Myelin insulates neuronal axons and enables fast signal transmission, constituting a key component of brain development, aging and disease. Yet, myelin-specific imaging of macroscopic samples remains a challenge. Here, we exploit myelin’s nanostructural periodicity, and use small-angle X-ray scattering tensor tomography (SAXS-TT) to simultaneously quantify myelin levels, nanostructural integrity and axon orientations in nervous tissue. Proof-of-principle is demonstrated in whole mouse brain, mouse spinal cord and human white and gray matter samples. Outcomes are validated by 2D/3D histology and compared to MRI measurements sensitive to myelin and axon orientations. Specificity to nanostructure is exemplified by concomitantly imaging different myelin types with distinct periodicities. Finally, we illustrate the method’s sensitivity towards myelin-related diseases by quantifying myelin alterations in dysmyelinated mouse brain. This non-destructive, stain-free molecular imaging approach enables quantitative studies of myelination within and across samples during development, aging, disease and treatment, and is applicable to other ordered biomolecules or nanostructures.
Myelin insulates neuronal axons and enables fast signal transmission, constituting a key component of brain development, aging and disease. Yet, myelin-specific imaging of macroscopic samples remains a challenge. Here, we exploit myelin’s nanostructural periodicity, and use small-angle X-ray scattering tensor tomography (SAXS-TT) to simultaneously quantify myelin levels, nanostructural integrity and axon orientations in nervous tissue. Proof-of-principle is demonstrated in whole mouse brain, mouse spinal cord and human white and gray matter samples. Outcomes are validated by 2D/3D histology and compared to MRI measurements sensitive to myelin and axon orientations. Specificity to nanostructure is exemplified by concomitantly imaging different myelin types with distinct periodicities. Finally, we illustrate the method’s sensitivity towards myelin-related diseases by quantifying myelin alterations in dysmyelinated mouse brain. This non-destructive, stain-free molecular imaging approach enables quantitative studies of myelination within and across samples during development, aging, disease and treatment, and is applicable to other ordered biomolecules or nanostructures. Small-angle X-ray scattering (SAXS) combines the high tissue penetration of X-rays with specificity to periodic nanostructures. The authors use SAXS tensor tomography (SAXS-TT) on intact mouse and human brain tissue samples, to quantify myelin levels and determine myelin integrity, myelinated axon orientation, and fibre tracts non-destructively.
Small-angle X-ray scattering (SAXS) combines the high tissue penetration of X-rays with specificity to periodic nanostructures. The authors use SAXS tensor tomography (SAXS-TT) on intact mouse and human brain tissue samples, to quantify myelin levels and determine myelin integrity, myelinated axon orientation, and fibre tracts non-destructively.
Myelin insulates neuronal axons and enables fast signal transmission, constituting a key component of brain development, aging and disease. Yet, myelin-specific imaging of macroscopic samples remains a challenge. Here, we exploit myelin’s nanostructural periodicity, and use small-angle X-ray scattering tensor tomography (SAXS-TT) to simultaneously quantify myelin levels, nanostructural integrity and axon orientations in nervous tissue. Proof-of-principle is demonstrated in whole mouse brain, mouse spinal cord and human white and gray matter samples. Outcomes are validated by 2D/3D histology and compared to MRI measurements sensitive to myelin and axon orientations. Specificity to nanostructure is exemplified by concomitantly imaging different myelin types with distinct periodicities. Finally, we illustrate the method’s sensitivity towards myelin-related diseases by quantifying myelin alterations in dysmyelinated mouse brain. This non-destructive, stain-free molecular imaging approach enables quantitative studies of myelination within and across samples during development, aging, disease and treatment, and is applicable to other ordered biomolecules or nanostructures.Small-angle X-ray scattering (SAXS) combines the high tissue penetration of X-rays with specificity to periodic nanostructures. The authors use SAXS tensor tomography (SAXS-TT) on intact mouse and human brain tissue samples, to quantify myelin levels and determine myelin integrity, myelinated axon orientation, and fibre tracts non-destructively.
ArticleNumber 2941
Author Kim, Sunglyoung
Georgiadis, Marios
Walczak, Piotr
Zerbi, Valerio
Veraart, Jelle
Chodankar, Shirish
Novikov, Dmitry S.
Leuze, Christoph
Gao, Zirui
Liebi, Marianne
Fieremans, Els
Schroeter, Aileen
Sommer, Stefan
Bunk, Oliver
David, Gergely
Weiss, Thomas
Shepherd, Timothy
Balolia, Aleezah
McNab, Jennifer A.
Zeineh, Michael
Rajkovic, Ivan
Ades-Aron, Benjamin
Augath, Mark
Zhang, Jiangyang
Lee, Choong H.
Guizar-Sicairos, Manuel
Yang, Lin
Rudin, Markus
DiGiacomo, Phillip
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CorporateAuthor Brookhaven National Laboratory (BNL), Upton, NY (United States)
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
CorporateAuthor_xml – name: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
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Snippet Myelin insulates neuronal axons and enables fast signal transmission, constituting a key component of brain development, aging and disease. Yet,...
Small-angle X-ray scattering (SAXS) combines the high tissue penetration of X-rays with specificity to periodic nanostructures. The authors use SAXS tensor...
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SubjectTerms 101/1
14/19
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631/378/2606
631/535/1261
639/925/930/2735
692/698/1688
96/34
Aging
Animals
Axons
Axons - metabolism
Axons - ultrastructure
BASIC BIOLOGICAL SCIENCES
Biomolecules
Brain
Brain - metabolism
Brain - ultrastructure
Central Nervous System - diagnostic imaging
Central Nervous System - metabolism
Central Nervous System - ultrastructure
Child, Preschool
Female
Histology
Humanities and Social Sciences
Humans
imaging
imaging techniques
Integrity
Magnetic resonance imaging
Magnetic Resonance Imaging - methods
Male
MATERIALS SCIENCE
Mathematical analysis
Medical imaging
Mice
Mice, Inbred C57BL
Mice, Knockout
multidisciplinary
Myelin
Myelin biology and repair
Myelin Proteins - metabolism
Myelin Sheath - metabolism
Myelin Sheath - ultrastructure
Myelination
Nanostructure
Nanostructures - chemistry
Nanostructures - ultrastructure
nervous system
Nervous tissues
Neuroimaging
Neuroimaging - methods
Periodicity
Proof of Concept Study
Quantitative research
SAXS
Scattering, Small Angle
Science
Science (multidisciplinary)
Signal transmission
Small angle X ray scattering
Spinal cord
Spinal Cord - metabolism
Spinal Cord - ultrastructure
Substantia grisea
Tensors
Tomography
Tomography, X-Ray Computed - methods
X-ray scattering
X-rays
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Title Nanostructure-specific X-ray tomography reveals myelin levels, integrity and axon orientations in mouse and human nervous tissue
URI https://link.springer.com/article/10.1038/s41467-021-22719-7
https://www.ncbi.nlm.nih.gov/pubmed/34011929
https://www.proquest.com/docview/2529006648
https://www.proquest.com/docview/2529929036
https://www.osti.gov/servlets/purl/1808596
https://pubmed.ncbi.nlm.nih.gov/PMC8134484
https://research.chalmers.se/publication/524180
https://doaj.org/article/35fab30941ac43ca99ab4a14e671a883
Volume 12
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