Diffusivity and quantitative T1 profile of human visual white matter tracts after retinal ganglion cell damage

Hiromasa Takemura; Shumpei Ogawa; Aviv A. Mezer; Hiroshi Horiguchi; Atsushi Miyazaki; Kenji Matsumoto; Keigo Shikishima; Tadashi Nakano; Yoichiro Masuda

doi:10.1016/j.nicl.2019.101826

Diffusivity and quantitative T1 profile of human visual white matter tracts after retinal ganglion cell damage

Hiromasa Takemura^*, Shumpei Ogawa, Aviv A. Mezer, Hiroshi Horiguchi, Atsushi Miyazaki, Kenji Matsumoto, Keigo Shikishima, Tadashi Nakano, Yoichiro Masuda

^*Corresponding author for this work

Edmond & Lily Safra Center for Brain Sciences

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

22 Scopus citations

Abstract

In patients with retinal ganglion cell diseases, recent diffusion tensor imaging (DTI) studies have revealed structural abnormalities in visual white matter tracts such as the optic tract, and optic radiation. However, the microstructural origin of these diffusivity changes is unknown as DTI metrics involve multiple biological factors and do not correlate directly with specific microstructural properties. In contrast, recent quantitative T1 (qT1) mapping methods provide tissue property measurements relatively specific to myelin volume fractions in white matter. This study aims to improve our understanding of microstructural changes in visual white matter tracts following retinal ganglion cell damage in Leber's hereditary optic neuropathy (LHON) patients by combining DTI and qT1 measurements. We collected these measurements from seven LHON patients and twenty age-matched control subjects. For all individuals, we identified the optic tract and the optic radiation using probabilistic tractography, and evaluated diffusivity and qT1 profiles along them. Both diffusivity and qT1 measurements in the optic tract differed significantly between LHON patients and controls. In the optic radiation, these changes were observed in diffusivity but were not evident in qT1 measurements. This suggests that myelin loss may not explain trans-synaptic diffusivity changes in the optic radiation as a consequence of retinal ganglion cell disease.

Original language	American English
Article number	101826
Journal	NeuroImage: Clinical
Volume	23
DOIs	https://doi.org/10.1016/j.nicl.2019.101826
State	Published - 2019

Bibliographical note

Funding Information:
We thank Garikoitz Lerma-Usabiaga for suggestions in qT1 data collection, Kazuki Iijima in support of subject recruitment, Yusuke Sakai in support of data analysis, and Ariel Rokem for comments on an earlier version of the manuscript. This study was supported by Japan Society for the Promotion of Science (JSPS) KAKENHI ( JP17H04684 , JP15J00412 to H.T.; JP17K18131 to S.O.; JP18K16939 to H.H.; JP19K09982 to Y.M), the Jikei University Research fund (to Y.M.) and Charitable Trust Fund for Ophthalmic Research in Commemoration of Santen Pharmaceutical's Founder (to Y.M. and H.H.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Publisher Copyright:
© 2019 The Authors

Keywords

Leber's hereditary optic neuropathy
MRI
Myelin
Optic radiation
Optic tract
White matter

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Cite this

@article{0b3e989142134b23aefb02bc650952cf,

title = "Diffusivity and quantitative T1 profile of human visual white matter tracts after retinal ganglion cell damage",

abstract = "In patients with retinal ganglion cell diseases, recent diffusion tensor imaging (DTI) studies have revealed structural abnormalities in visual white matter tracts such as the optic tract, and optic radiation. However, the microstructural origin of these diffusivity changes is unknown as DTI metrics involve multiple biological factors and do not correlate directly with specific microstructural properties. In contrast, recent quantitative T1 (qT1) mapping methods provide tissue property measurements relatively specific to myelin volume fractions in white matter. This study aims to improve our understanding of microstructural changes in visual white matter tracts following retinal ganglion cell damage in Leber's hereditary optic neuropathy (LHON) patients by combining DTI and qT1 measurements. We collected these measurements from seven LHON patients and twenty age-matched control subjects. For all individuals, we identified the optic tract and the optic radiation using probabilistic tractography, and evaluated diffusivity and qT1 profiles along them. Both diffusivity and qT1 measurements in the optic tract differed significantly between LHON patients and controls. In the optic radiation, these changes were observed in diffusivity but were not evident in qT1 measurements. This suggests that myelin loss may not explain trans-synaptic diffusivity changes in the optic radiation as a consequence of retinal ganglion cell disease.",

keywords = "Leber's hereditary optic neuropathy, MRI, Myelin, Optic radiation, Optic tract, White matter",

author = "Hiromasa Takemura and Shumpei Ogawa and Mezer, {Aviv A.} and Hiroshi Horiguchi and Atsushi Miyazaki and Kenji Matsumoto and Keigo Shikishima and Tadashi Nakano and Yoichiro Masuda",

note = "Funding Information: We thank Garikoitz Lerma-Usabiaga for suggestions in qT1 data collection, Kazuki Iijima in support of subject recruitment, Yusuke Sakai in support of data analysis, and Ariel Rokem for comments on an earlier version of the manuscript. This study was supported by Japan Society for the Promotion of Science (JSPS) KAKENHI ( JP17H04684 , JP15J00412 to H.T.; JP17K18131 to S.O.; JP18K16939 to H.H.; JP19K09982 to Y.M), the Jikei University Research fund (to Y.M.) and Charitable Trust Fund for Ophthalmic Research in Commemoration of Santen Pharmaceutical's Founder (to Y.M. and H.H.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Publisher Copyright: {\textcopyright} 2019 The Authors",

year = "2019",

doi = "10.1016/j.nicl.2019.101826",

language = "American English",

volume = "23",

journal = "NeuroImage: Clinical",

issn = "2213-1582",

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TY - JOUR

T1 - Diffusivity and quantitative T1 profile of human visual white matter tracts after retinal ganglion cell damage

AU - Takemura, Hiromasa

AU - Ogawa, Shumpei

AU - Mezer, Aviv A.

AU - Horiguchi, Hiroshi

AU - Miyazaki, Atsushi

AU - Matsumoto, Kenji

AU - Shikishima, Keigo

AU - Nakano, Tadashi

AU - Masuda, Yoichiro

N1 - Funding Information: We thank Garikoitz Lerma-Usabiaga for suggestions in qT1 data collection, Kazuki Iijima in support of subject recruitment, Yusuke Sakai in support of data analysis, and Ariel Rokem for comments on an earlier version of the manuscript. This study was supported by Japan Society for the Promotion of Science (JSPS) KAKENHI ( JP17H04684 , JP15J00412 to H.T.; JP17K18131 to S.O.; JP18K16939 to H.H.; JP19K09982 to Y.M), the Jikei University Research fund (to Y.M.) and Charitable Trust Fund for Ophthalmic Research in Commemoration of Santen Pharmaceutical's Founder (to Y.M. and H.H.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Publisher Copyright: © 2019 The Authors

PY - 2019

Y1 - 2019

N2 - In patients with retinal ganglion cell diseases, recent diffusion tensor imaging (DTI) studies have revealed structural abnormalities in visual white matter tracts such as the optic tract, and optic radiation. However, the microstructural origin of these diffusivity changes is unknown as DTI metrics involve multiple biological factors and do not correlate directly with specific microstructural properties. In contrast, recent quantitative T1 (qT1) mapping methods provide tissue property measurements relatively specific to myelin volume fractions in white matter. This study aims to improve our understanding of microstructural changes in visual white matter tracts following retinal ganglion cell damage in Leber's hereditary optic neuropathy (LHON) patients by combining DTI and qT1 measurements. We collected these measurements from seven LHON patients and twenty age-matched control subjects. For all individuals, we identified the optic tract and the optic radiation using probabilistic tractography, and evaluated diffusivity and qT1 profiles along them. Both diffusivity and qT1 measurements in the optic tract differed significantly between LHON patients and controls. In the optic radiation, these changes were observed in diffusivity but were not evident in qT1 measurements. This suggests that myelin loss may not explain trans-synaptic diffusivity changes in the optic radiation as a consequence of retinal ganglion cell disease.

AB - In patients with retinal ganglion cell diseases, recent diffusion tensor imaging (DTI) studies have revealed structural abnormalities in visual white matter tracts such as the optic tract, and optic radiation. However, the microstructural origin of these diffusivity changes is unknown as DTI metrics involve multiple biological factors and do not correlate directly with specific microstructural properties. In contrast, recent quantitative T1 (qT1) mapping methods provide tissue property measurements relatively specific to myelin volume fractions in white matter. This study aims to improve our understanding of microstructural changes in visual white matter tracts following retinal ganglion cell damage in Leber's hereditary optic neuropathy (LHON) patients by combining DTI and qT1 measurements. We collected these measurements from seven LHON patients and twenty age-matched control subjects. For all individuals, we identified the optic tract and the optic radiation using probabilistic tractography, and evaluated diffusivity and qT1 profiles along them. Both diffusivity and qT1 measurements in the optic tract differed significantly between LHON patients and controls. In the optic radiation, these changes were observed in diffusivity but were not evident in qT1 measurements. This suggests that myelin loss may not explain trans-synaptic diffusivity changes in the optic radiation as a consequence of retinal ganglion cell disease.

KW - Leber's hereditary optic neuropathy

KW - MRI

KW - Myelin

KW - Optic radiation

KW - Optic tract

KW - White matter

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U2 - 10.1016/j.nicl.2019.101826

DO - 10.1016/j.nicl.2019.101826

M3 - Article

C2 - 31026624

AN - SCOPUS:85064511474

SN - 2213-1582

VL - 23

JO - NeuroImage: Clinical

JF - NeuroImage: Clinical

M1 - 101826

ER -

Diffusivity and quantitative T1 profile of human visual white matter tracts after retinal ganglion cell damage

Abstract

Bibliographical note

Keywords

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