Deciphering the developmental order and microstructural patterns of early white matter pathways in a diffusion MRI based fetal brain atlas

White matter (WM) of the fetal brain undergoes rapid development to form early structural connections. Diffusion magnetic resonance imaging (dMRI) has shown to be a useful tool to depict fetal brain WM in utero, and many studies have observed increasing fractional anisotropy and decreasing diffusivi...

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Main Authors: Ruike Chen, Cong Sun, Tingting Liu, Yuhao Liao, Junyan Wang, Yi Sun, Yi Zhang, Guangbin Wang, Dan Wu
Format: Article
Language:English
Published: Elsevier 2022-12-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811922008217
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author Ruike Chen
Cong Sun
Tingting Liu
Yuhao Liao
Junyan Wang
Yi Sun
Yi Zhang
Guangbin Wang
Dan Wu
author_facet Ruike Chen
Cong Sun
Tingting Liu
Yuhao Liao
Junyan Wang
Yi Sun
Yi Zhang
Guangbin Wang
Dan Wu
author_sort Ruike Chen
collection DOAJ
description White matter (WM) of the fetal brain undergoes rapid development to form early structural connections. Diffusion magnetic resonance imaging (dMRI) has shown to be a useful tool to depict fetal brain WM in utero, and many studies have observed increasing fractional anisotropy and decreasing diffusivity in the fetal brain during the second-to-third trimester, whereas others reported non-monotonic changes. Unbiased dMRI atlases of the fetal brain are important for characterizing the developmental trajectories of WM and providing normative references for in utero diagnosis of prenatal abnormalities. To date, the sole fetal brain dMRI atlas was collected from a Caucasian/mixed population and was constructed based on the diffusion tensor model with limited spatial resolution.In this work, we proposed a fiber orientation distribution (FOD) based pipeline for generating fetal brain dMRI atlases, which showed better registration accuracy than a diffusion tensor based pipeline. Based on the FOD-based pipeline, we constructed the first Chinese fetal brain dMRI atlas using 89 dMRI scans of normal fetuses at gestational age between 24 and 38 weeks. Complex non-monotonic trends of tensor- and FOD-derived microstructural parameters in eight WM tracts were observed, which jointly pointed to different phases of microstructural development. Specifically, we speculated that the turning point of the diffusivity trajectory may correspond to the starting point of pre-myelination, based on which, the developmental order of WM tracts can be mapped and the order was in agreement with the order of myelination from histological studies. The normative atlas also provided a reference for the detection of abnormal WM development, such as that in congenital heart disease. Therefore, the established high-order fetal brain dMRI atlas depicted the spatiotemporal pattern of early WM development, and findings may help decipher the distinct microstructural events in utero.
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spelling doaj.art-bf73b55f290e436696358a44453428c82022-12-22T03:52:08ZengElsevierNeuroImage1095-95722022-12-01264119700Deciphering the developmental order and microstructural patterns of early white matter pathways in a diffusion MRI based fetal brain atlasRuike Chen0Cong Sun1Tingting Liu2Yuhao Liao3Junyan Wang4Yi Sun5Yi Zhang6Guangbin Wang7Dan Wu8Key Laboratory for Biomedical Engineering of Ministry of Education, Department of Biomedical Engineering, College of Biomedical Engineering & Instrument Science, Zhejiang University, Hangzhou, ChinaDepartment of Radiology, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, ChinaKey Laboratory for Biomedical Engineering of Ministry of Education, Department of Biomedical Engineering, College of Biomedical Engineering & Instrument Science, Zhejiang University, Hangzhou, ChinaKey Laboratory for Biomedical Engineering of Ministry of Education, Department of Biomedical Engineering, College of Biomedical Engineering & Instrument Science, Zhejiang University, Hangzhou, ChinaZhejiang Lab, Hangzhou, ChinaMR Collaboration, Siemens Healthineers Ltd., Shanghai, ChinaKey Laboratory for Biomedical Engineering of Ministry of Education, Department of Biomedical Engineering, College of Biomedical Engineering & Instrument Science, Zhejiang University, Hangzhou, ChinaDepartment of Radiology, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, China; Department of Radiology, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, Shandong, ChinaKey Laboratory for Biomedical Engineering of Ministry of Education, Department of Biomedical Engineering, College of Biomedical Engineering & Instrument Science, Zhejiang University, Hangzhou, China; Corresponding author at: Zhejiang University, Room 525, Zhou Yiqing Building, Yuquan Campus, Hangzhou 310027, China.White matter (WM) of the fetal brain undergoes rapid development to form early structural connections. Diffusion magnetic resonance imaging (dMRI) has shown to be a useful tool to depict fetal brain WM in utero, and many studies have observed increasing fractional anisotropy and decreasing diffusivity in the fetal brain during the second-to-third trimester, whereas others reported non-monotonic changes. Unbiased dMRI atlases of the fetal brain are important for characterizing the developmental trajectories of WM and providing normative references for in utero diagnosis of prenatal abnormalities. To date, the sole fetal brain dMRI atlas was collected from a Caucasian/mixed population and was constructed based on the diffusion tensor model with limited spatial resolution.In this work, we proposed a fiber orientation distribution (FOD) based pipeline for generating fetal brain dMRI atlases, which showed better registration accuracy than a diffusion tensor based pipeline. Based on the FOD-based pipeline, we constructed the first Chinese fetal brain dMRI atlas using 89 dMRI scans of normal fetuses at gestational age between 24 and 38 weeks. Complex non-monotonic trends of tensor- and FOD-derived microstructural parameters in eight WM tracts were observed, which jointly pointed to different phases of microstructural development. Specifically, we speculated that the turning point of the diffusivity trajectory may correspond to the starting point of pre-myelination, based on which, the developmental order of WM tracts can be mapped and the order was in agreement with the order of myelination from histological studies. The normative atlas also provided a reference for the detection of abnormal WM development, such as that in congenital heart disease. Therefore, the established high-order fetal brain dMRI atlas depicted the spatiotemporal pattern of early WM development, and findings may help decipher the distinct microstructural events in utero.http://www.sciencedirect.com/science/article/pii/S1053811922008217Atlas generationDiffusion MRIFetal brain developmentWhite matterMicrostructure
spellingShingle Ruike Chen
Cong Sun
Tingting Liu
Yuhao Liao
Junyan Wang
Yi Sun
Yi Zhang
Guangbin Wang
Dan Wu
Deciphering the developmental order and microstructural patterns of early white matter pathways in a diffusion MRI based fetal brain atlas
NeuroImage
Atlas generation
Diffusion MRI
Fetal brain development
White matter
Microstructure
title Deciphering the developmental order and microstructural patterns of early white matter pathways in a diffusion MRI based fetal brain atlas
title_full Deciphering the developmental order and microstructural patterns of early white matter pathways in a diffusion MRI based fetal brain atlas
title_fullStr Deciphering the developmental order and microstructural patterns of early white matter pathways in a diffusion MRI based fetal brain atlas
title_full_unstemmed Deciphering the developmental order and microstructural patterns of early white matter pathways in a diffusion MRI based fetal brain atlas
title_short Deciphering the developmental order and microstructural patterns of early white matter pathways in a diffusion MRI based fetal brain atlas
title_sort deciphering the developmental order and microstructural patterns of early white matter pathways in a diffusion mri based fetal brain atlas
topic Atlas generation
Diffusion MRI
Fetal brain development
White matter
Microstructure
url http://www.sciencedirect.com/science/article/pii/S1053811922008217
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