Constructing and optimizing 3D atlases from 2D data with application to the developing mouse brain

Abstract
Data availability
Article and author information
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Abstract

3D imaging data necessitate 3D reference atlases for accurate quantitative interpretation. Existing computational methods to generate 3D atlases from 2D-derived atlases result in extensive artifacts, while manual curation approaches are labor-intensive. We present a computational approach for 3D atlas construction that substantially reduces artifacts by identifying anatomical boundaries in the underlying imaging data and using these to guide 3D transformation. Anatomical boundaries also allow extension of atlases to complete edge regions. Applying these methods to the eight developmental stages in the Allen Developing Mouse Brain Atlas (ADMBA) led to more comprehensive and accurate atlases. We generated imaging data from fifteen whole mouse brains to validate atlas performance and observed qualitative and quantitative improvement (37% greater alignment between atlas and anatomical boundaries). We provide the pipeline as the MagellanMapper software and the eight 3D reconstructed ADMBA atlases. These resources facilitate whole-organ quantitative analysis between samples and across development.

Data availability

The full 3D generated atlases and wild-type brain images are being deposited with the Human Brain Project EBRAINS data platform. All data analyses are included in the manuscript and supporting files.

The following data sets were generated

1. Young D
2. Yu W
3. Sanders SJ
(2020) E11.5 3D Edge-Aware Refined Atlas Derived from the Allen Developing Mouse Brain Atlas
EBRAINS , 10.25493/H9A3-GFT.

https://doi.org/10.25493%2FH9A3-GFT
1. Young D
2. Yu W
3. Sanders SJ
(2020) E13.5 3D Edge-Aware Refined Atlas Derived from the Allen Developing Mouse Brain Atlas
EBRAINS , 10.25493/YP9K-YMW.

https://doi.org/10.25493%2FYP9K-YMW
1. Young D
2. Yu W
3. Sanders SJ
(2020) E15.5 3D Edge-Aware Refined Atlas Derived from the Allen Developing Mouse Brain Atlas
EBRAINS , 10.25493/EXET-XND.

https://doi.org/10.25493%2FEXET-XND
1. Young D
2. Yu W
3. Sanders SJ
(2020) E18.5 3D Edge-Aware Refined Atlas Derived from the Allen Developing Mouse Brain Atlas
EBRAINS , 10.25493/X4ZT-ARE.

https://doi.org/10.25493%2FX4ZT-ARE
1. Young D
2. Yu W
3. Sanders SJ
(2020) P4 3D Edge-Aware Refined Atlas Derived from the Allen Developing Mouse Brain Atlas
EBRAINS , 10.25493/QYP4-5VQ.

https://doi.org/10.25493%2FQYP4-5VQ
1. Young D
2. Yu W
3. Sanders SJ
(2020) P14 3D Edge-Aware Refined Atlas Derived from the Allen Developing Mouse Brain Atlas
EBRAINS , 10.25493/QYP4-5VQ.

https://doi.org/10.25493%2FQYP4-5VQ
1. Young D
2. Yu W
3. Sanders SJ
(2020) P28 3D Edge-Aware Refined Atlas Derived from the Allen Developing Mouse Brain Atlas
EBRAINS , 10.25493/YW1E-6BW.

https://doi.org/10.25493%2FYW1E-6BW
1. Young D
2. Yu W
3. Sanders SJ
(2020) P56 3D Edge-Aware Refined Atlas Derived from the Allen Developing Mouse Brain Atlas
EBRAINS , 10.25493/MYPD-QB8.

https://doi.org/10.25493%2FYW1E-6BW

The following previously published data sets were used

1. C. L. Thompson
2. L. Ng
3. V. Menon
4. S. Martinez
5. C.-K. Lee
6. K. Glattfelder
7. S. M. Sunkin
8. A. Henry
9. C. Lau
10. C. Dang
11. R. Garcia-Lopez
12. A. Martinez-Ferre
13. A. Pombero
14. J. L. R. Rubenstein
15. W. B. Wakeman
16. J. Hohmann
17. N. Dee
18. A. J. Sodt
19. R. Young
20. K. Smith
21. T.-N. Nguyen
22. J. Kidney
23. L. Kuan
24. A. Jeromin
25. A. Kaykas
26. J. Miller
27. D. Page
28. G. Orta
29. A. Bernard
30. Z. Riley
31. S. Smith
32. P. Wohnoutka
33. M. J. Hawrylycz
34. L. Puelles
35. and A. R. Jones
(2014) A high-resolution spatiotemporal atlas of gene expression of the developing mouse brain
10.1016/j.neuron.2014.05.033.

https://doi.org/10.1016/j.neuron.2014.05.033

Article and author information

Author details

David M Young

Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, San Francisco, United States

Competing interests
The authors declare that no competing interests exist.
Siavash Fazel Darbandi

Psychiatry, University of California, San Francisco, San Francisco, United States

Competing interests
The authors declare that no competing interests exist.
Grace Schwartz

Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, San Francisco, United States

Competing interests
The authors declare that no competing interests exist.
Zachary Bonzell

Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, San Francisco, United States

Competing interests
The authors declare that no competing interests exist.
Deniz Yuruk

Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, San Francisco, United States

Competing interests
The authors declare that no competing interests exist.
Mai Nojima

Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, San Francisco, United States

Competing interests
The authors declare that no competing interests exist.
Laurent C Gole

Institute of Molecular and Cellular Biology, Agency for Science, Technology and Research, Singapore, Singapore

Competing interests
The authors declare that no competing interests exist.
John LR Rubenstein

Department of Psychiatry, University of California, San Francisco, San Francisco, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-4414-7667
Weimiao Yu

Institute of Molecular and Cellular Biology, Agency for Science, Technology and Research, Singapore, Singapore

Competing interests
The authors declare that no competing interests exist.
Stephan J Sanders

Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, San Francisco, United States

For correspondence
stephan.sanders@ucsf.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-9112-5148

Funding

Brain and Behavior Research Foundation (NARSAD Young Investigator Grant)

Stephan J Sanders

National Institute of Mental Health (U01 MH122681)

Stephan J Sanders

National Institute of Mental Health (R01 MH109901)

Stephan J Sanders

National Institute of Neurological Disorders and Stroke (R01 NS099099)

John LR Rubenstein

The authors declare that the funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All procedures and animal care were approved and performed in accordance with institutional guidelines from the University of California San Francisco Laboratory Animal Research Center (LARC). All animal handling complied with the approved Institutional Animal Care and Use Committee (IACUC) protocol (AN180174-02) at the University of California San Francisco.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.