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A diffusion MRI-based spatiotemporal continuum of the embryonic mouse brain for probing gene–neuroanatomy connections

The embryonic mouse brain undergoes drastic changes in establishing basic anatomical compartments and laying out major axonal connections of the developing brain. Correlating anatomical changes with gene-expression patterns is an essential step toward understanding the mechanisms regulating brain de...

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Autores principales: Wu, Dan, Richards, Linda J., Zhao, Zhiyong, Cao, Zuozhen, Luo, Wanrong, Shao, Wei, Shi, Song-Hai, Miller, Michael I., Mori, Susumu, Blackshaw, Seth, Zhang, Jiangyang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8851557/
https://www.ncbi.nlm.nih.gov/pubmed/35165149
http://dx.doi.org/10.1073/pnas.2111869119
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author Wu, Dan
Richards, Linda J.
Zhao, Zhiyong
Cao, Zuozhen
Luo, Wanrong
Shao, Wei
Shi, Song-Hai
Miller, Michael I.
Mori, Susumu
Blackshaw, Seth
Zhang, Jiangyang
author_facet Wu, Dan
Richards, Linda J.
Zhao, Zhiyong
Cao, Zuozhen
Luo, Wanrong
Shao, Wei
Shi, Song-Hai
Miller, Michael I.
Mori, Susumu
Blackshaw, Seth
Zhang, Jiangyang
author_sort Wu, Dan
collection PubMed
description The embryonic mouse brain undergoes drastic changes in establishing basic anatomical compartments and laying out major axonal connections of the developing brain. Correlating anatomical changes with gene-expression patterns is an essential step toward understanding the mechanisms regulating brain development. Traditionally, this is done in a cross-sectional manner, but the dynamic nature of development calls for probing gene–neuroanatomy interactions in a combined spatiotemporal domain. Here, we present a four-dimensional (4D) spatiotemporal continuum of the embryonic mouse brain from E10.5 to E15.5 reconstructed from diffusion magnetic resonance microscopy (dMRM) data. This study achieved unprecedented high-definition dMRM at 30- to 35-µm isotropic resolution, and together with computational neuroanatomy techniques, we revealed both morphological and microscopic changes in the developing brain. We transformed selected gene-expression data to this continuum and correlated them with the dMRM-based neuroanatomical changes in embryonic brains. Within the continuum, we identified distinct developmental modes comprising regional clusters that shared developmental trajectories and similar gene-expression profiles. Our results demonstrate how this 4D continuum can be used to examine spatiotemporal gene–neuroanatomical interactions by connecting upstream genetic events with anatomical changes that emerge later in development. This approach would be useful for large-scale analysis of the cooperative roles of key genes in shaping the developing brain.
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spelling pubmed-88515572022-08-14 A diffusion MRI-based spatiotemporal continuum of the embryonic mouse brain for probing gene–neuroanatomy connections Wu, Dan Richards, Linda J. Zhao, Zhiyong Cao, Zuozhen Luo, Wanrong Shao, Wei Shi, Song-Hai Miller, Michael I. Mori, Susumu Blackshaw, Seth Zhang, Jiangyang Proc Natl Acad Sci U S A Biological Sciences The embryonic mouse brain undergoes drastic changes in establishing basic anatomical compartments and laying out major axonal connections of the developing brain. Correlating anatomical changes with gene-expression patterns is an essential step toward understanding the mechanisms regulating brain development. Traditionally, this is done in a cross-sectional manner, but the dynamic nature of development calls for probing gene–neuroanatomy interactions in a combined spatiotemporal domain. Here, we present a four-dimensional (4D) spatiotemporal continuum of the embryonic mouse brain from E10.5 to E15.5 reconstructed from diffusion magnetic resonance microscopy (dMRM) data. This study achieved unprecedented high-definition dMRM at 30- to 35-µm isotropic resolution, and together with computational neuroanatomy techniques, we revealed both morphological and microscopic changes in the developing brain. We transformed selected gene-expression data to this continuum and correlated them with the dMRM-based neuroanatomical changes in embryonic brains. Within the continuum, we identified distinct developmental modes comprising regional clusters that shared developmental trajectories and similar gene-expression profiles. Our results demonstrate how this 4D continuum can be used to examine spatiotemporal gene–neuroanatomical interactions by connecting upstream genetic events with anatomical changes that emerge later in development. This approach would be useful for large-scale analysis of the cooperative roles of key genes in shaping the developing brain. National Academy of Sciences 2022-02-14 2022-02-15 /pmc/articles/PMC8851557/ /pubmed/35165149 http://dx.doi.org/10.1073/pnas.2111869119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Wu, Dan
Richards, Linda J.
Zhao, Zhiyong
Cao, Zuozhen
Luo, Wanrong
Shao, Wei
Shi, Song-Hai
Miller, Michael I.
Mori, Susumu
Blackshaw, Seth
Zhang, Jiangyang
A diffusion MRI-based spatiotemporal continuum of the embryonic mouse brain for probing gene–neuroanatomy connections
title A diffusion MRI-based spatiotemporal continuum of the embryonic mouse brain for probing gene–neuroanatomy connections
title_full A diffusion MRI-based spatiotemporal continuum of the embryonic mouse brain for probing gene–neuroanatomy connections
title_fullStr A diffusion MRI-based spatiotemporal continuum of the embryonic mouse brain for probing gene–neuroanatomy connections
title_full_unstemmed A diffusion MRI-based spatiotemporal continuum of the embryonic mouse brain for probing gene–neuroanatomy connections
title_short A diffusion MRI-based spatiotemporal continuum of the embryonic mouse brain for probing gene–neuroanatomy connections
title_sort diffusion mri-based spatiotemporal continuum of the embryonic mouse brain for probing gene–neuroanatomy connections
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8851557/
https://www.ncbi.nlm.nih.gov/pubmed/35165149
http://dx.doi.org/10.1073/pnas.2111869119
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