Using light and X-ray scattering to untangle complex neuronal orientations and validate diffusion MRI

Disentangling human brain connectivity requires an accurate description of nerve fiber trajectories, unveiled via detailed mapping of axonal orientations. However, this is challenging because axons can cross one another on a micrometer scale. Diffusion magnetic resonance imaging (dMRI) can be used t...

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Main Authors: Miriam Menzel, David Gräßel, Ivan Rajkovic, Michael M Zeineh, Marios Georgiadis
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/84024
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author Miriam Menzel
David Gräßel
Ivan Rajkovic
Michael M Zeineh
Marios Georgiadis
author_facet Miriam Menzel
David Gräßel
Ivan Rajkovic
Michael M Zeineh
Marios Georgiadis
author_sort Miriam Menzel
collection DOAJ
description Disentangling human brain connectivity requires an accurate description of nerve fiber trajectories, unveiled via detailed mapping of axonal orientations. However, this is challenging because axons can cross one another on a micrometer scale. Diffusion magnetic resonance imaging (dMRI) can be used to infer axonal connectivity because it is sensitive to axonal alignment, but it has limited spatial resolution and specificity. Scattered light imaging (SLI) and small-angle X-ray scattering (SAXS) reveal axonal orientations with microscopic resolution and high specificity, respectively. Here, we apply both scattering techniques on the same samples and cross-validate them, laying the groundwork for ground-truth axonal orientation imaging and validating dMRI. We evaluate brain regions that include unidirectional and crossing fibers in human and vervet monkey brain sections. SLI and SAXS quantitatively agree regarding in-plane fiber orientations including crossings, while dMRI agrees in the majority of voxels with small discrepancies. We further use SAXS and dMRI to confirm theoretical predictions regarding SLI determination of through-plane fiber orientations. Scattered light and X-ray imaging can provide quantitative micrometer 3D fiber orientations with high resolution and specificity, facilitating detailed investigations of complex fiber architecture in the animal and human brain.
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spelling doaj.art-64cba2b2aa1b461b94bcef9b0ad25dee2023-06-06T06:31:06ZengeLife Sciences Publications LtdeLife2050-084X2023-05-011210.7554/eLife.84024Using light and X-ray scattering to untangle complex neuronal orientations and validate diffusion MRIMiriam Menzel0https://orcid.org/0000-0002-6042-7490David Gräßel1https://orcid.org/0000-0003-3228-8048Ivan Rajkovic2Michael M Zeineh3Marios Georgiadis4https://orcid.org/0000-0003-0733-4559Department of Imaging Physics, Faculty of Applied Sciences, Delft University of Technology, Delft, Netherlands; Institute of Neuroscience and Medicine (INM-1), Forschungszentrum Jülich GmbH, Jülich, GermanyInstitute of Neuroscience and Medicine (INM-1), Forschungszentrum Jülich GmbH, Jülich, GermanyStanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, Standford, United StatesDepartment of Radiology, Stanford School of Medicine, Stanford, United StatesDepartment of Radiology, Stanford School of Medicine, Stanford, United StatesDisentangling human brain connectivity requires an accurate description of nerve fiber trajectories, unveiled via detailed mapping of axonal orientations. However, this is challenging because axons can cross one another on a micrometer scale. Diffusion magnetic resonance imaging (dMRI) can be used to infer axonal connectivity because it is sensitive to axonal alignment, but it has limited spatial resolution and specificity. Scattered light imaging (SLI) and small-angle X-ray scattering (SAXS) reveal axonal orientations with microscopic resolution and high specificity, respectively. Here, we apply both scattering techniques on the same samples and cross-validate them, laying the groundwork for ground-truth axonal orientation imaging and validating dMRI. We evaluate brain regions that include unidirectional and crossing fibers in human and vervet monkey brain sections. SLI and SAXS quantitatively agree regarding in-plane fiber orientations including crossings, while dMRI agrees in the majority of voxels with small discrepancies. We further use SAXS and dMRI to confirm theoretical predictions regarding SLI determination of through-plane fiber orientations. Scattered light and X-ray imaging can provide quantitative micrometer 3D fiber orientations with high resolution and specificity, facilitating detailed investigations of complex fiber architecture in the animal and human brain.https://elifesciences.org/articles/84024brain connectivityX-ray scatteringlight scatteringneuroimagingcorona radiatavervet monkey
spellingShingle Miriam Menzel
David Gräßel
Ivan Rajkovic
Michael M Zeineh
Marios Georgiadis
Using light and X-ray scattering to untangle complex neuronal orientations and validate diffusion MRI
eLife
brain connectivity
X-ray scattering
light scattering
neuroimaging
corona radiata
vervet monkey
title Using light and X-ray scattering to untangle complex neuronal orientations and validate diffusion MRI
title_full Using light and X-ray scattering to untangle complex neuronal orientations and validate diffusion MRI
title_fullStr Using light and X-ray scattering to untangle complex neuronal orientations and validate diffusion MRI
title_full_unstemmed Using light and X-ray scattering to untangle complex neuronal orientations and validate diffusion MRI
title_short Using light and X-ray scattering to untangle complex neuronal orientations and validate diffusion MRI
title_sort using light and x ray scattering to untangle complex neuronal orientations and validate diffusion mri
topic brain connectivity
X-ray scattering
light scattering
neuroimaging
corona radiata
vervet monkey
url https://elifesciences.org/articles/84024
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