Axon fiber orientation as the source of T1 relaxation anisotropy in white matter: A study on corpus callosum in vivo and ex vivo

Risto A. Kauppinen; Jeromy Thothard; Henri P.P. Leskinen; Pramod K. Pisharady; Eppu Manninen; Mikko Kettunen; Christophe Lenglet; Olli H.J. Gröhn; Michael Garwood; Mikko J. Nissi

doi:10.1002/mrm.29667

Axon fiber orientation as the source of T₁ relaxation anisotropy in white matter: A study on corpus callosum in vivo and ex vivo

Risto A. Kauppinen, Jeromy Thothard, Henri P.P. Leskinen, Pramod K. Pisharady, Eppu Manninen, Mikko Kettunen, Christophe Lenglet, Olli H.J. Gröhn, Michael Garwood, Mikko J. Nissi

Center for Magnetic Resonance Research

Research output: Contribution to journal › Article › peer-review

3 Scopus citations

Abstract

Purpose: Recent studies indicate that T₁ in white matter (WM) is influenced by fiber orientation in B₀. The purpose of the study was to investigate the interrelationships between axon fiber orientation in corpus callosum (CC) and T₁ relaxation time in humans in vivo as well as in rat brain ex vivo. Methods: Volunteers were scanned for relaxometric and diffusion MRI at 3 T and 7 T. Angular T₁ plots from WM were computed using fractional anisotropy and fiber-to-field-angle maps. T₁ and fiber-to-field angle were measured in five sections of CC to estimate the effects of inherently varying fiber orientations on T₁ within the same tracts in vivo. Ex vivo rat-brain preparation encompassing posterior CC was rotated in B₀ and T₁, and diffusion MRI images acquired at 9.4 T. T₁ angular plots were determined at several rotation angles in B₀. Results: Angular T₁ plots from global WM provided reference for estimated fiber orientation–linked T₁ changes within CC. In anterior midbody of CC in vivo, where small axons are dominantly present, a shift in axon orientation is accompanied by a change in T₁, matching that estimated from WM T₁ data. In CC, where large and giant axons are numerous, the measured T₁ change is about 2-fold greater than the estimated one. Ex vivo rotation of the same midsagittal CC region of interest produced angular T₁ plots at 9.4 T, matching those observed at 7 T in vivo. Conclusion: These data causally link axon fiber orientation in B₀ to the T₁ relaxation anisotropy in WM.

Original language	English (US)
Pages (from-to)	708-721
Number of pages	14
Journal	Magnetic resonance in medicine
Volume	90
Issue number	2
DOIs	https://doi.org/10.1002/mrm.29667
State	Published - Aug 2023

Bibliographical note

Funding Information:
This study was supported by NIBIB (RO3 EB027873), National Institutes of Health (P41 EB027061 and P30 NS076408), and a grant from the Academy of Finland (#325146). The authors thank Euro-BioImaging (www.eurobioimaging.eu) for providing access to imaging technologies and services via the Finnish Biomedical Imaging Node (Kuopio Biomedical Imaging Unit, part of Biocenter Kuopio, University of Eastern Finland, Kuopio, Finland).

Funding Information:
This study was supported by NIBIB (RO3 EB027873), National Institutes of Health (P41 EB027061 and P30 NS076408), and a grant from the Academy of Finland (#325146). The authors thank Euro‐BioImaging ( www.eurobioimaging.eu ) for providing access to imaging technologies and services via the Finnish Biomedical Imaging Node (Kuopio Biomedical Imaging Unit, part of Biocenter Kuopio, University of Eastern Finland, Kuopio, Finland).

Publisher Copyright:
© 2023 The Authors. Magnetic Resonance in Medicine published by Wiley Periodicals LLC on behalf of International Society for Magnetic Resonance in Medicine.

Keywords

T relaxation
microstructure
relaxation anisotropy
white matter

PubMed: MeSH publication types

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

Access

10.1002/mrm.29667

OpenUrl availability

Full text

Cite this

Kauppinen, R. A., Thothard, J., Leskinen, H. P. P., Pisharady, P. K., Manninen, E., Kettunen, M., Lenglet, C., Gröhn, O. H. J., Garwood, M., & Nissi, M. J. (2023). Axon fiber orientation as the source of T₁ relaxation anisotropy in white matter: A study on corpus callosum in vivo and ex vivo. Magnetic resonance in medicine, 90(2), 708-721. https://doi.org/10.1002/mrm.29667

@article{6a3c30174b8342538081795bad3084f6,

title = "Axon fiber orientation as the source of T1 relaxation anisotropy in white matter: A study on corpus callosum in vivo and ex vivo",

abstract = "Purpose: Recent studies indicate that T1 in white matter (WM) is influenced by fiber orientation in B0. The purpose of the study was to investigate the interrelationships between axon fiber orientation in corpus callosum (CC) and T1 relaxation time in humans in vivo as well as in rat brain ex vivo. Methods: Volunteers were scanned for relaxometric and diffusion MRI at 3 T and 7 T. Angular T1 plots from WM were computed using fractional anisotropy and fiber-to-field-angle maps. T1 and fiber-to-field angle were measured in five sections of CC to estimate the effects of inherently varying fiber orientations on T1 within the same tracts in vivo. Ex vivo rat-brain preparation encompassing posterior CC was rotated in B0 and T1, and diffusion MRI images acquired at 9.4 T. T1 angular plots were determined at several rotation angles in B0. Results: Angular T1 plots from global WM provided reference for estimated fiber orientation–linked T1 changes within CC. In anterior midbody of CC in vivo, where small axons are dominantly present, a shift in axon orientation is accompanied by a change in T1, matching that estimated from WM T1 data. In CC, where large and giant axons are numerous, the measured T1 change is about 2-fold greater than the estimated one. Ex vivo rotation of the same midsagittal CC region of interest produced angular T1 plots at 9.4 T, matching those observed at 7 T in vivo. Conclusion: These data causally link axon fiber orientation in B0 to the T1 relaxation anisotropy in WM.",

keywords = "T relaxation, microstructure, relaxation anisotropy, white matter",

author = "Kauppinen, {Risto A.} and Jeromy Thothard and Leskinen, {Henri P.P.} and Pisharady, {Pramod K.} and Eppu Manninen and Mikko Kettunen and Christophe Lenglet and Gr{\"o}hn, {Olli H.J.} and Michael Garwood and Nissi, {Mikko J.}",

note = "Funding Information: This study was supported by NIBIB (RO3 EB027873), National Institutes of Health (P41 EB027061 and P30 NS076408), and a grant from the Academy of Finland (#325146). The authors thank Euro-BioImaging (www.eurobioimaging.eu) for providing access to imaging technologies and services via the Finnish Biomedical Imaging Node (Kuopio Biomedical Imaging Unit, part of Biocenter Kuopio, University of Eastern Finland, Kuopio, Finland). Funding Information: This study was supported by NIBIB (RO3 EB027873), National Institutes of Health (P41 EB027061 and P30 NS076408), and a grant from the Academy of Finland (#325146). The authors thank Euro‐BioImaging ( www.eurobioimaging.eu ) for providing access to imaging technologies and services via the Finnish Biomedical Imaging Node (Kuopio Biomedical Imaging Unit, part of Biocenter Kuopio, University of Eastern Finland, Kuopio, Finland). Publisher Copyright: {\textcopyright} 2023 The Authors. Magnetic Resonance in Medicine published by Wiley Periodicals LLC on behalf of International Society for Magnetic Resonance in Medicine.",

year = "2023",

month = aug,

doi = "10.1002/mrm.29667",

language = "English (US)",

volume = "90",

pages = "708--721",

journal = "Magnetic resonance in medicine",

issn = "0740-3194",

publisher = "John Wiley and Sons Inc.",

number = "2",

}

TY - JOUR

T1 - Axon fiber orientation as the source of T1 relaxation anisotropy in white matter

T2 - A study on corpus callosum in vivo and ex vivo

AU - Kauppinen, Risto A.

AU - Thothard, Jeromy

AU - Leskinen, Henri P.P.

AU - Pisharady, Pramod K.

AU - Manninen, Eppu

AU - Kettunen, Mikko

AU - Lenglet, Christophe

AU - Gröhn, Olli H.J.

AU - Garwood, Michael

AU - Nissi, Mikko J.

N1 - Funding Information: This study was supported by NIBIB (RO3 EB027873), National Institutes of Health (P41 EB027061 and P30 NS076408), and a grant from the Academy of Finland (#325146). The authors thank Euro-BioImaging (www.eurobioimaging.eu) for providing access to imaging technologies and services via the Finnish Biomedical Imaging Node (Kuopio Biomedical Imaging Unit, part of Biocenter Kuopio, University of Eastern Finland, Kuopio, Finland). Funding Information: This study was supported by NIBIB (RO3 EB027873), National Institutes of Health (P41 EB027061 and P30 NS076408), and a grant from the Academy of Finland (#325146). The authors thank Euro‐BioImaging ( www.eurobioimaging.eu ) for providing access to imaging technologies and services via the Finnish Biomedical Imaging Node (Kuopio Biomedical Imaging Unit, part of Biocenter Kuopio, University of Eastern Finland, Kuopio, Finland). Publisher Copyright: © 2023 The Authors. Magnetic Resonance in Medicine published by Wiley Periodicals LLC on behalf of International Society for Magnetic Resonance in Medicine.

PY - 2023/8

Y1 - 2023/8

N2 - Purpose: Recent studies indicate that T1 in white matter (WM) is influenced by fiber orientation in B0. The purpose of the study was to investigate the interrelationships between axon fiber orientation in corpus callosum (CC) and T1 relaxation time in humans in vivo as well as in rat brain ex vivo. Methods: Volunteers were scanned for relaxometric and diffusion MRI at 3 T and 7 T. Angular T1 plots from WM were computed using fractional anisotropy and fiber-to-field-angle maps. T1 and fiber-to-field angle were measured in five sections of CC to estimate the effects of inherently varying fiber orientations on T1 within the same tracts in vivo. Ex vivo rat-brain preparation encompassing posterior CC was rotated in B0 and T1, and diffusion MRI images acquired at 9.4 T. T1 angular plots were determined at several rotation angles in B0. Results: Angular T1 plots from global WM provided reference for estimated fiber orientation–linked T1 changes within CC. In anterior midbody of CC in vivo, where small axons are dominantly present, a shift in axon orientation is accompanied by a change in T1, matching that estimated from WM T1 data. In CC, where large and giant axons are numerous, the measured T1 change is about 2-fold greater than the estimated one. Ex vivo rotation of the same midsagittal CC region of interest produced angular T1 plots at 9.4 T, matching those observed at 7 T in vivo. Conclusion: These data causally link axon fiber orientation in B0 to the T1 relaxation anisotropy in WM.

AB - Purpose: Recent studies indicate that T1 in white matter (WM) is influenced by fiber orientation in B0. The purpose of the study was to investigate the interrelationships between axon fiber orientation in corpus callosum (CC) and T1 relaxation time in humans in vivo as well as in rat brain ex vivo. Methods: Volunteers were scanned for relaxometric and diffusion MRI at 3 T and 7 T. Angular T1 plots from WM were computed using fractional anisotropy and fiber-to-field-angle maps. T1 and fiber-to-field angle were measured in five sections of CC to estimate the effects of inherently varying fiber orientations on T1 within the same tracts in vivo. Ex vivo rat-brain preparation encompassing posterior CC was rotated in B0 and T1, and diffusion MRI images acquired at 9.4 T. T1 angular plots were determined at several rotation angles in B0. Results: Angular T1 plots from global WM provided reference for estimated fiber orientation–linked T1 changes within CC. In anterior midbody of CC in vivo, where small axons are dominantly present, a shift in axon orientation is accompanied by a change in T1, matching that estimated from WM T1 data. In CC, where large and giant axons are numerous, the measured T1 change is about 2-fold greater than the estimated one. Ex vivo rotation of the same midsagittal CC region of interest produced angular T1 plots at 9.4 T, matching those observed at 7 T in vivo. Conclusion: These data causally link axon fiber orientation in B0 to the T1 relaxation anisotropy in WM.

KW - T relaxation

KW - microstructure

KW - relaxation anisotropy

KW - white matter

UR - http://www.scopus.com/inward/record.url?scp=85158140947&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85158140947&partnerID=8YFLogxK

U2 - 10.1002/mrm.29667

DO - 10.1002/mrm.29667

M3 - Article

C2 - 37145027

AN - SCOPUS:85158140947

SN - 0740-3194

VL - 90

SP - 708

EP - 721

JO - Magnetic resonance in medicine

JF - Magnetic resonance in medicine

IS - 2

ER -