A generalizable brain extraction net (BEN) for multimodal MRI data from rodents, nonhuman primates, and humans

Abstract
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Abstract

Accurate brain tissue extraction on magnetic resonance imaging (MRI) data is crucial for analyzing brain structure and function. While several conventional tools have been optimized to handle human brain data, there have been no generalizable methods to extract brain tissues for multimodal MRI data from rodents, nonhuman primates, and humans. Therefore, developing a flexible and generalizable method for extracting whole brain tissue across species would allow researchers to analyze and compare experiment results more efficiently. Here, we propose a domain-adaptive and semi-supervised deep neural network, named the Brain Extraction Net (BEN), to extract brain tissues across species, MRI modalities, and MR scanners. We have evaluated BEN on 18 independent datasets, including 783 rodent MRI scans, 246 nonhuman primate MRI scans, and 4,601 human MRI scans, covering five species, four modalities, and six MR scanners with various magnetic field strengths. Compared to conventional toolboxes, the superiority of BEN is illustrated by its robustness, accuracy, and generalizability. Our proposed method not only provides a generalized solution for extracting brain tissue across species but also significantly improves the accuracy of atlas registration, thereby benefiting the downstream processing tasks. As a novel fully automated deep-learning method, BEN is designed as an open-source software to enable high-throughput processing of neuroimaging data across species in preclinical and clinical applications.

Data availability

All data (MRI data, source codes, pretrained weights and replicate demo notebooks for Figure 1-7) are included in the manuscript or available at https://github.com/yu02019/BEN.

The following data sets were generated

(2022) A longitudinal MRI dataset of young adult C57BL6J mouse brain
Zenodo, doi:10.5281/zenodo.6844489.

https://doi.org/10.5281/zenodo.6844489

The following previously published data sets were used

(2020) CAMRI Rat Brain MRI Data
OpenNeuro, doi:10.18112/openneuro.ds002870.v1.0.1.

https://openneuro.org/datasets/ds002870/versions/1.0.0
(2020) CAMRI Mouse Brain MRI Data
OpenNeuro, doi:10.18112/openneuro.ds002868.v1.0.1.

https://openneuro.org/datasets/ds002868/versions/1.0.0
(2018) An Open Resource for Non-human Primate Imaging
Neuron, doi:10.1016/j.neuron.2018.08.039.

https://doi.org/10.1016/j.neuron.2018.08.039
(2018) The Adolescent Brain Cognitive Development (ABCD) study: Imaging acquisition across 21 sites
Developmental Cognitive Neuroscience, doi:10.1016/j.dcn.2018.03.001.

https://abcdstudy.org/scientists/data-sharing/
(2018) Multimodal population brain imaging in the UK Biobank prospective epidemiological study
Nature Neuroscience, doi:10.1038/nn.4393.

https://www.nature.com/articles/nn.4393

Article and author information

Author details

Ziqi Yu

Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-8201-5481
Xiaoyang Han

Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-3007-6079
Wenjing Xu

Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China

Competing interests
No competing interests declared.
Jie Zhang

Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China

Competing interests
No competing interests declared.
Carsten Marr

Institute of AI for Health, Helmholtz Zentrum München, Neuherberg, Germany

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0003-2154-4552
Dinggang Shen

School of Biomedical Engineering, ShanghaiTech University, Shanghai, China

Competing interests
Dinggang Shen, is affiliated with Shanghai United Imaging Intelligence Co., Ltd. He has financial interests to declare..
Tingying Peng

Helmholtz AI, Helmholtz Zentrum München, Neuherberg, Germany

For correspondence
tingying.peng@helmholtz-muenchen.de

Competing interests
No competing interests declared.
Xiao-Yong Zhang

Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China

For correspondence
xiaoyong_zhang@fudan.edu.cn

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-8965-1077
Jianfeng Feng

Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-5987-2258

Funding

National Natural Science Foundation of China (81873893,82171903,92043301)

Xiao-Yong Zhang

Fudan University (the Office of Global Partnerships (Key Projects Development Fund))

Xiao-Yong Zhang

Shanghai Municipal Science and Technology Major Project (No.2018SHZDZX01)

Xiao-Yong Zhang

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

Ethics

Animal experimentation: Partial rodent MRI data collection were approved by the Animal Care and Use Committee of Fudan University, China. The rest rodent data (Rat-T2WI-9.4T and Rat-EPI-9.4T datasets) are publicly available (CARMI: https://openneuro.org/datasets/ds002870/versions/1.0.0). Marmoset MRI data collection were approved by the Animal Care and Use Committee of the Institute of Neuroscience, Chinese Academy of Sciences, China. Macaque MRI data are publicly available from the nonhuman PRIMatE Data Exchange (PRIME-DE) (https://fcon_1000.projects.nitrc.org/indi/indiPRIME.html).

Human subjects: The Zhangjiang International Brain Biobank (ZIB) protocols were approved by the Ethics Committee of Fudan University (AF/SC-03/20200722) and written informed consents were obtained from all volunteers. UK Biobank (UKB) and Adolescent Brain Cognitive Development (ABCD) are publicly available.

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.