Skip to main content
Top
Published in:

01-04-2023 | Magnetic Resonance Imaging | Research

Multimodal 3D Mouse Brain Atlas Framework with the Skull-Derived Coordinate System

Authors: Johanna Perens, Casper Gravesen Salinas, Urmas Roostalu, Jacob Lercke Skytte, Carsten Gundlach, Jacob Hecksher-Sørensen, Anders Bjorholm Dahl, Tim B. Dyrby

Published in: Neuroinformatics | Issue 2/2023

Login to get access

Abstract

Magnetic resonance imaging (MRI) and light-sheet fluorescence microscopy (LSFM) are technologies that enable non-disruptive 3-dimensional imaging of whole mouse brains. A combination of complementary information from both modalities is desirable for studying neuroscience in general, disease progression and drug efficacy. Although both technologies rely on atlas mapping for quantitative analyses, the translation of LSFM recorded data to MRI templates has been complicated by the morphological changes inflicted by tissue clearing and the enormous size of the raw data sets. Consequently, there is an unmet need for tools that will facilitate fast and accurate translation of LSFM recorded brains to in vivo, non-distorted templates. In this study, we have developed a bidirectional multimodal atlas framework that includes brain templates based on both imaging modalities, region delineations from the Allen’s Common Coordinate Framework, and a skull-derived stereotaxic coordinate system. The framework also provides algorithms for bidirectional transformation of results obtained using either MR or LSFM (iDISCO cleared) mouse brain imaging while the coordinate system enables users to easily assign in vivo coordinates across the different brain templates.
Literature
go back to reference Allen Institute for Brain Science. (2017). Allen Mouse Common coordinate Framework and Reference Atlas. Technical White Paper. Allen Institute for Brain Science. (2017). Allen Mouse Common coordinate Framework and Reference Atlas. Technical White Paper.
go back to reference Breckwoldt, M. O., Bode, J., Sahm, F., Krüwel, T., Solecki, G., Hahn, A., et al. (2019). Correlated MRI and ultramicroscopy (MR-UM) of brain tumors reveals vast heterogeneity of tumor infiltration and neoangiogenesis in preclinical models and human disease. Frontiers in Neuroscience, 13, 1–10. https://doi.org/10.3389/fnins.2018.01004.CrossRef Breckwoldt, M. O., Bode, J., Sahm, F., Krüwel, T., Solecki, G., Hahn, A., et al. (2019). Correlated MRI and ultramicroscopy (MR-UM) of brain tumors reveals vast heterogeneity of tumor infiltration and neoangiogenesis in preclinical models and human disease. Frontiers in Neuroscience, 13, 1–10. https://​doi.​org/​10.​3389/​fnins.​2018.​01004.CrossRef
go back to reference Dong, H. W. (2008). The Allen Reference Atlas: a Digital Color Brain Atlas of the C57BL/6J male mouse. Wiley. Dong, H. W. (2008). The Allen Reference Atlas: a Digital Color Brain Atlas of the C57BL/6J male mouse. Wiley.
go back to reference Franklin, K. B. J., & Paxinos, G. (1997). The mouse brain in stereotaxic coordinates (1st ed.). San Diego: Academic Press. Franklin, K. B. J., & Paxinos, G. (1997). The mouse brain in stereotaxic coordinates (1st ed.). San Diego: Academic Press.
go back to reference Friedmann, D., Pun, A., Adams, E. L., Lui, J. H., Kebschull, J. M., Grutzner, S. M. (2020). Mapping mesoscale axonal projections in the mouse brain using a 3D convolutional network. Proceedings of the National Academy of Sciences, 117(20), 11068–11075. https://doi.org/10.1073/PNAS.1918465117 Friedmann, D., Pun, A., Adams, E. L., Lui, J. H., Kebschull, J. M., Grutzner, S. M. (2020). Mapping mesoscale axonal projections in the mouse brain using a 3D convolutional network. Proceedings of the National Academy of Sciences, 117(20), 11068–11075. https://​doi.​org/​10.​1073/​PNAS.​1918465117
go back to reference Hof, P. R., Young, W. G., Bloom, F. E., Belichenko, P., & Celio, M. R. (2000). Comparative cytoarchitectonic atlas of the C57BL/6 and 129/Sv mouse brains (1st ed.). Amsterdam: Elsevier. Hof, P. R., Young, W. G., Bloom, F. E., Belichenko, P., & Celio, M. R. (2000). Comparative cytoarchitectonic atlas of the C57BL/6 and 129/Sv mouse brains (1st ed.). Amsterdam: Elsevier.
go back to reference Jacobowitz, D. M., & Abbott, L. C. (1997). Chemoarchitectonic atlas of the developing mouse brain (1st ed.). Boca Raton: CRC Press.CrossRef Jacobowitz, D. M., & Abbott, L. C. (1997). Chemoarchitectonic atlas of the developing mouse brain (1st ed.). Boca Raton: CRC Press.CrossRef
go back to reference Kaufman, M. (1992). Atlas of Mouse Development (1st ed.). London: Academic Press. Kaufman, M. (1992). Atlas of Mouse Development (1st ed.). London: Academic Press.
go back to reference Lee, B. C., Lin, M. K., Fu, Y., Hata, J., Miller, M. I., & Mitra, P. P. (2021). Multimodal cross-registration and quantification of metric distortions in marmoset whole brain histology using diffeomorphic mappings. Journal of Comparative Neurology, 529(2), 281–295. https://doi.org/10.1002/CNE.24946.CrossRefPubMed Lee, B. C., Lin, M. K., Fu, Y., Hata, J., Miller, M. I., & Mitra, P. P. (2021). Multimodal cross-registration and quantification of metric distortions in marmoset whole brain histology using diffeomorphic mappings. Journal of Comparative Neurology, 529(2), 281–295. https://​doi.​org/​10.​1002/​CNE.​24946.CrossRefPubMed
go back to reference Massalimova, A., Ni, R., Nitsch, R. M., Reisert, M., von Elverfeldt, D., & Klohs, J. (2021). Diffusion Tensor Imaging reveals whole-brain microstructural changes in the P301L mouse model of Tauopathy. Neurodegenrative diseases, 20, 173–184. https://doi.org/10.1159/000515754.CrossRef Massalimova, A., Ni, R., Nitsch, R. M., Reisert, M., von Elverfeldt, D., & Klohs, J. (2021). Diffusion Tensor Imaging reveals whole-brain microstructural changes in the P301L mouse model of Tauopathy. Neurodegenrative diseases, 20, 173–184. https://​doi.​org/​10.​1159/​000515754.CrossRef
go back to reference Matthews, P. M., & Jezzard, P. (2004). Functional magnetic resonance imaging. Journal of Neurology Neurosurgery & Psychiatry, 75, 6–12. Matthews, P. M., & Jezzard, P. (2004). Functional magnetic resonance imaging. Journal of Neurology Neurosurgery & Psychiatry, 75, 6–12.
go back to reference Patel, J. (2018). The mouse brain: a 3D atlas registering MRI, CT, and histological sections in three cardinal planes. John Hopkins University. Patel, J. (2018). The mouse brain: a 3D atlas registering MRI, CT, and histological sections in three cardinal planes. John Hopkins University.
go back to reference Roostalu, U., Salinas, C. B. G., Thorbek, D. D., Skytte, J. L., Fabricius, K., Barkholt, P., et al. (2019). Quantitative whole-brain 3D imaging of tyrosine hydroxylase-labeled neuron architecture in the mouse MPTP model of Parkinson’s disease. Disease Models and Mechanisms, 12(11), https://doi.org/10.1242/dmm.042200. Roostalu, U., Salinas, C. B. G., Thorbek, D. D., Skytte, J. L., Fabricius, K., Barkholt, P., et al. (2019). Quantitative whole-brain 3D imaging of tyrosine hydroxylase-labeled neuron architecture in the mouse MPTP model of Parkinson’s disease. Disease Models and Mechanisms, 12(11), https://​doi.​org/​10.​1242/​dmm.​042200.
go back to reference Rosen, G. D., Williams, A. G., Capra, J. A., Connolly, M. T., Cruz, B., Lu, L. (2000). The Mouse Brain Library. Int Mouse Genome Conference 14, (166). www.mbl.org Rosen, G. D., Williams, A. G., Capra, J. A., Connolly, M. T., Cruz, B., Lu, L. (2000). The Mouse Brain Library. Int Mouse Genome Conference 14, (166). www.​mbl.​org
go back to reference Sidman, R. L., Angevine, J. B., & Taber-Pierce, E. (1971). Atlas of the mouse brain and spinal cord (Commonwealth Fund Publications). Cambridge: Harvard University Press. Sidman, R. L., Angevine, J. B., & Taber-Pierce, E. (1971). Atlas of the mouse brain and spinal cord (Commonwealth Fund Publications). Cambridge: Harvard University Press.
go back to reference Skovbjerg, G., Roostalu, U., Hansen, H. H., Lutz, T. A., le Foll, C., Salinas, C. G., et al. (2021). Whole-brain mapping of amylin-induced neuronal activity in receptor activity–modifying protein 1/3 knockout mice. European Journal of Neuroscience, 54(1), 4154–4166. https://doi.org/10.1111/EJN.15254.CrossRef Skovbjerg, G., Roostalu, U., Hansen, H. H., Lutz, T. A., le Foll, C., Salinas, C. G., et al. (2021). Whole-brain mapping of amylin-induced neuronal activity in receptor activity–modifying protein 1/3 knockout mice. European Journal of Neuroscience, 54(1), 4154–4166. https://​doi.​org/​10.​1111/​EJN.​15254.CrossRef
go back to reference Stolp, H. B., Ball, G., So, P. W., Tournier, J. D., Jones, M., Thornton, C., & Edwards, A. D. (2018). Voxel-wise comparisons of cellular microstructure and diffusion-MRI in mouse hippocampus using 3D bridging of optically-clear histology with Neuroimaging Data (3D-BOND). Scientific Reports, 8(1), 1–12. https://doi.org/10.1038/s41598-018-22295-9.CrossRef Stolp, H. B., Ball, G., So, P. W., Tournier, J. D., Jones, M., Thornton, C., & Edwards, A. D. (2018). Voxel-wise comparisons of cellular microstructure and diffusion-MRI in mouse hippocampus using 3D bridging of optically-clear histology with Neuroimaging Data (3D-BOND). Scientific Reports, 8(1), 1–12. https://​doi.​org/​10.​1038/​s41598-018-22295-9.CrossRef
go back to reference Umadevi Venkataraju, K. U., Gornet, J., Murugaiyan, G., Wu, Z., & Osten, P. (2019). Development of brain templates for whole brain atlases. Progress in Biomedical Optics and Imaging - Proceedings of SPIE, 10865, 1086511. https://doi.org/10.1117/12.2505295 Umadevi Venkataraju, K. U., Gornet, J., Murugaiyan, G., Wu, Z., & Osten, P. (2019). Development of brain templates for whole brain atlases. Progress in Biomedical Optics and Imaging - Proceedings of SPIE, 10865, 1086511. https://​doi.​org/​10.​1117/​12.​2505295
go back to reference Valverde, F. (2004). Golgi atlas of the postnatal mouse brain. New York: Springer-Verlag. Valverde, F. (2004). Golgi atlas of the postnatal mouse brain. New York: Springer-Verlag.
Metadata
Title
Multimodal 3D Mouse Brain Atlas Framework with the Skull-Derived Coordinate System
Authors
Johanna Perens
Casper Gravesen Salinas
Urmas Roostalu
Jacob Lercke Skytte
Carsten Gundlach
Jacob Hecksher-Sørensen
Anders Bjorholm Dahl
Tim B. Dyrby
Publication date
01-04-2023
Publisher
Springer US
Published in
Neuroinformatics / Issue 2/2023
Print ISSN: 1539-2791
Electronic ISSN: 1559-0089
DOI
https://doi.org/10.1007/s12021-023-09623-9

Other articles of this Issue 2/2023

Neuroinformatics 2/2023 Go to the issue

Advances in Alzheimer's

Alzheimer's research and care is changing rapidly. Keep up with the latest developments from key international conferences, together with expert insights on how to integrate these advances into practice.

This content is intended for healthcare professionals outside of the UK.

Supported by:
  • Lilly
Developed by: Springer Healthcare IME
Learn more