CerebNet: A fast and reliable deep-learning pipeline for detailed cerebellum sub-segmentation

ESMI MRI Study Group

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10 Scopus citations

Abstract

Quantifying the volume of the cerebellum and its lobes is of profound interest in various neurodegenerative and acquired diseases. Especially for the most common spinocerebellar ataxias (SCA), for which the first antisense oligonculeotide-base gene silencing trial has recently started, there is an urgent need for quantitative, sensitive imaging markers at pre-symptomatic stages for stratification and treatment assessment. This work introduces CerebNet, a fully automated, extensively validated, deep learning method for the lobular segmentation of the cerebellum, including the separation of gray and white matter. For training, validation, and testing, T1-weighted images from 30 participants were manually annotated into cerebellar lobules and vermal sub-segments, as well as cerebellar white matter. CerebNet combines FastSurferCNN, a UNet-based 2.5D segmentation network, with extensive data augmentation, e.g. realistic non-linear deformations to increase the anatomical variety, eliminating additional preprocessing steps, such as spatial normalization or bias field correction. CerebNet demonstrates a high accuracy (on average 0.87 Dice and 1.742mm Robust Hausdorff Distance across all structures) outperforming state-of-the-art approaches. Furthermore, it shows high test-retest reliability (average ICC >0.97 on OASIS and Kirby) as well as high sensitivity to disease effects, including the pre-ataxic stage of spinocerebellar ataxia type 3 (SCA3). CerebNet is compatible with FreeSurfer and FastSurfer and can analyze a 3D volume within seconds on a consumer GPU in an end-to-end fashion, thus providing an efficient and validated solution for assessing cerebellum sub-structure volumes. We make CerebNet available as source-code (https://github.com/Deep-MI/FastSurfer).

Original languageEnglish (US)
Article number119703
JournalNeuroImage
Volume264
DOIs
StatePublished - Dec 1 2022

Bibliographical note

Funding Information:
We would like to thank Beate Brol, Tim Elter, Isabelle Finkel, and Sophia Wismeth for their contribution to the manual segmentation. This work was supported by the National Ataxia Foundations SCA Young Investigator Award as well as by DZNE institutional funds, by the Federal Ministry of Education and Research of Germany (031L0206, 01GQ1801), and by NIH (R01 LM012719, R01 AG064027, R56 MH121426, and P41 EB030006). JF is fellow of the Hertie Network of excellence in clinical Neuroscience. This publication is an outcome of ESMI, an EU Joint Programme - Neurodegenerative Disease Research (JPND) project (see www.jpnd.eu). The project is supported through the following funding organisations under the aegis of JPND: Germany, Federal Ministry of Education and Research (BMBF; funding codes 01ED1602A/B); Netherlands, The Netherlands Organisation for Health Research and Development; Portugal, Foundation for Science and Technology and Regional Fund for Science and Technology of the Azores; United Kingdom, Medical Research Council. This project has received funding from the European Unions Horizon 2020 research and innovation programme under grant agreement No 643417. For the contribution of the Minnesota site, this work was in part supported by the National Ataxia Foundation and the National Institute of Neurological Disorders and Stroke (NINDS) grant R01NS080816. The Center for Magnetic Resonance Research is supported by the National Institute of Biomedical Imaging and Bioengineering (NIBIB) grant P41 EB027061, and the Institutional Center Cores for Advanced Neuroimaging award P30 NS076408 and S10OD017974 grant. Data used in the preparation of this article for pre-training and augmentation were obtained in part by the OASIS Cross-Sectional with principal investigators D. Marcus, R, Buckner, J, Csernansky J. Morris; P50 AG05681, P01 AG03991, P01 AG026276, R01 AG021910, P20 MH071616, U24 RR021382, and OASIS: Longitudinal: Principal Investigators: D. Marcus, R, Buckner, J. Csernansky, J. Morris; P50 AG05681, P01 AG03991, P01 AG026276, R01 AG021910, P20 MH071616, U24 RR021382. Further, data used in the preparation of this article were obtained from the MIRIAD database. The MIRIAD investigators did not participate in analysis or writing of this report. The MIRIAD dataset is made available through the support of the UK Alzheimer's Society (Grant RF116). The original data collection was funded through an unrestricted educational grant from GlaxoSmithKline (Grant 6GKC). Data used in preparation of this article were obtained from the Alzheimers Disease Neuroimaging Initiative (ADNI) database (adni.loni.usc.edu). As such, the investigators within the ADNI contributed to the design and implementation of ADNI and/or provided data but did not participate in analysis or writing of this report. A complete listing of ADNI investigators can be found at: http://adni.loni.usc.edu/wp-content/uploads/how_to_apply/ADNI_Acknowledgement_List.pdf. Data collection and sharing for this project was funded by the Alzheimer's Disease Neuroimaging Initiative (ADNI) (National Institutes of Health Grant U01 AG024904) and DOD ADNI (Department of Defense award number W81XWH-12-2-0012). ADNI is funded by the National Institute on Aging, the National Institute of Biomedical Imaging and Bioengineering, and through generous contributions from the following: AbbVie, Alzheimers Association; Alzheimers Drug Discovery Foundation; Araclon Biotech; BioClinica, Inc.; Biogen; Bristol-Myers Squibb Company; CereSpir, Inc.; Cogstate; Eisai Inc.; Elan Pharmaceuticals, Inc.; Eli Lilly and Company; EuroImmun; F. Hoffmann-La Roche Ltd and its affiliated company Genentech, Inc.; Fujirebio; GE Healthcare; IXICO Ltd.; Janssen Alzheimer Immunotherapy Research & Development, LLC.; Johnson & Johnson Pharmaceutical Research & Development LLC.; Lumosity; Lundbeck; Merck & Co., Inc.; Meso Scale Diagnostics, LLC.; NeuroRx Research; Neurotrack Technologies; Novartis Pharmaceuticals Corporation; Pfizer Inc.; Piramal Imaging; Servier; Takeda Pharmaceutical Company; and Transition Therapeutics. The Canadian Institutes of Health Research is providing funds to support ADNI clinical sites in Canada. Private sector contributions are facilitated by the Foundation for the National Institutes of Health (www.fnih.org). The grantee organization is the Northern California Institute for Research and Education, and the study is coordinated by the Alzheimers Therapeutic Research Institute at the University of Southern California. ADNI data are disseminated by the Laboratory for Neuro Imaging at the University of Southern California. Data were also provided in part by the Human Connectome Project, WU-Minn Consortium (Principal Investigators: David Van Essen and Kamil Ugurbil; 1U54MH091657) funded by the 16 NIH Institutes and Centers that support the NIH Blueprint for Neuroscience Research; and by the McDonnell Center for Systems Neuroscience at Washington University.

Funding Information:
We would like to thank Beate Brol, Tim Elter, Isabelle Finkel, and Sophia Wismeth for their contribution to the manual segmentation. This work was supported by the National Ataxia Foundations SCA Young Investigator Award as well as by DZNE institutional funds, by the Federal Ministry of Education and Research of Germany (031L0206, 01GQ1801), and by NIH (R01 LM012719, R01 AG064027, R56 MH121426, and P41 EB030006). JF is fellow of the Hertie Network of excellence in clinical Neuroscience. This publication is an outcome of ESMI, an EU Joint Programme - Neurodegenerative Disease Research (JPND) project (see www.jpnd.eu ). The project is supported through the following funding organisations under the aegis of JPND: Germany, Federal Ministry of Education and Research (BMBF; funding codes 01ED1602A/B); Netherlands, The Netherlands Organisation for Health Research and Development; Portugal, Foundation for Science and Technology and Regional Fund for Science and Technology of the Azores; United Kingdom, Medical Research Council. This project has received funding from the European Unions Horizon 2020 research and innovation programme under grant agreement No 643417. For the contribution of the Minnesota site, this work was in part supported by the National Ataxia Foundation and the National Institute of Neurological Disorders and Stroke (NINDS) grant R01NS080816. The Center for Magnetic Resonance Research is supported by the National Institute of Biomedical Imaging and Bioengineering (NIBIB) grant P41 EB027061, and the Institutional Center Cores for Advanced Neuroimaging award P30 NS076408 and S10OD017974 grant. Data used in the preparation of this article for pre-training and augmentation were obtained in part by the OASIS Cross-Sectional with principal investigators D. Marcus, R, Buckner, J, Csernansky J. Morris; P50 AG05681, P01 AG03991, P01 AG026276, R01 AG021910, P20 MH071616, U24 RR021382, and OASIS: Longitudinal: Principal Investigators: D. Marcus, R, Buckner, J. Csernansky, J. Morris; P50 AG05681, P01 AG03991, P01 AG026276, R01 AG021910, P20 MH071616, U24 RR021382. Further, data used in the preparation of this article were obtained from the MIRIAD database. The MIRIAD investigators did not participate in analysis or writing of this report. The MIRIAD dataset is made available through the support of the UK Alzheimer’s Society (Grant RF116). The original data collection was funded through an unrestricted educational grant from GlaxoSmithKline (Grant 6GKC). Data used in preparation of this article were obtained from the Alzheimers Disease Neuroimaging Initiative (ADNI) database (adni.loni.usc.edu). As such, the investigators within the ADNI contributed to the design and implementation of ADNI and/or provided data but did not participate in analysis or writing of this report. A complete listing of ADNI investigators can be found at: http://adni.loni.usc.edu/wp-content/uploads/how_to_apply/ADNI_Acknowledgement_List.pdf . Data collection and sharing for this project was funded by the Alzheimer’s Disease Neuroimaging Initiative (ADNI) (National Institutes of Health Grant U01 AG024904) and DOD ADNI (Department of Defense award number W81XWH-12-2-0012). ADNI is funded by the National Institute on Aging , the National Institute of Biomedical Imaging and Bioengineering, and through generous contributions from the following: AbbVie, Alzheimers Association; Alzheimers Drug Discovery Foundation; Araclon Biotech; BioClinica, Inc.; Biogen; Bristol-Myers Squibb Company; CereSpir, Inc.; Cogstate; Eisai Inc.; Elan Pharmaceuticals, Inc.; Eli Lilly and Company; EuroImmun; F. Hoffmann-La Roche Ltd and its affiliated company Genentech, Inc.; Fujirebio; GE Healthcare; IXICO Ltd.; Janssen Alzheimer Immunotherapy Research & Development, LLC.; Johnson & Johnson Pharmaceutical Research & Development LLC.; Lumosity; Lundbeck; Merck & Co., Inc.; Meso Scale Diagnostics, LLC.; NeuroRx Research; Neurotrack Technologies; Novartis Pharmaceuticals Corporation; Pfizer Inc.; Piramal Imaging; Servier; Takeda Pharmaceutical Company; and Transition Therapeutics. The Canadian Institutes of Health Research is providing funds to support ADNI clinical sites in Canada. Private sector contributions are facilitated by the Foundation for the National Institutes of Health ( www.fnih.org ). The grantee organization is the Northern California Institute for Research and Education, and the study is coordinated by the Alzheimers Therapeutic Research Institute at the University of Southern California. ADNI data are disseminated by the Laboratory for Neuro Imaging at the University of Southern California. Data were also provided in part by the Human Connectome Project, WU-Minn Consortium (Principal Investigators: David Van Essen and Kamil Ugurbil; 1U54MH091657) funded by the 16 NIH Institutes and Centers that support the NIH Blueprint for Neuroscience Research ; and by the McDonnell Center for Systems Neuroscience at Washington University.

Publisher Copyright:
© 2022 The Author(s)

Keywords

  • CerebNet
  • Cerebellum
  • Computational neuroimaging
  • Deep learning

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