Benchtop mesoSPIM: a next-generation open-source light-sheet microscope for cleared samples.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
27 Mar 2024
Historique:
received: 18 07 2023
accepted: 08 03 2024
medline: 28 3 2024
pubmed: 28 3 2024
entrez: 28 3 2024
Statut: epublish

Résumé

In 2015, we launched the mesoSPIM initiative, an open-source project for making light-sheet microscopy of large cleared tissues more accessible. Meanwhile, the demand for imaging larger samples at higher speed and resolution has increased, requiring major improvements in the capabilities of such microscopes. Here, we introduce the next-generation mesoSPIM ("Benchtop") with a significantly increased field of view, improved resolution, higher throughput, more affordable cost, and simpler assembly compared to the original version. We develop an optical method for testing detection objectives that enables us to select objectives optimal for light-sheet imaging with large-sensor cameras. The improved mesoSPIM achieves high spatial resolution (1.5 µm laterally, 3.3 µm axially) across the entire field of view, magnification up to 20×, and supports sample sizes ranging from sub-mm up to several centimeters while being compatible with multiple clearing techniques. The microscope serves a broad range of applications in neuroscience, developmental biology, pathology, and even physics.

Identifiants

pubmed: 38538644
doi: 10.1038/s41467-024-46770-2
pii: 10.1038/s41467-024-46770-2
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2679

Informations de copyright

© 2024. The Author(s).

Références

Spalteholz, W. Über das Durchsichtigmachen von menschlichen und tierischen Präparaten und seine theoretischen Bedingungen, nebst Anhang: Über Knochenfärbung 2nd edn. (S. Hirzel, 1914).
Siedentopf, H. & Zsigmondy, R. Uber Sichtbarmachung und Größenbestimmung ultramikoskopischer Teilchen, mit besonderer Anwendung auf Goldrubingläser. Ann. Phys. 315, 1–39 (1902).
doi: 10.1002/andp.19023150102
Ueda, H. R. et al. Tissue clearing and its applications in neuroscience. Nat. Rev. Neurosci. 21, 61–79 (2020).
pubmed: 31896771 pmcid: 8121164 doi: 10.1038/s41583-019-0250-1
Ueda, H. R. et al. Whole-brain profiling of cells and circuits in mammals by tissue clearing and light-sheet microscopy. Neuron 106, 369–387 (2020).
pubmed: 32380050 pmcid: 7213014 doi: 10.1016/j.neuron.2020.03.004
Dodt, H. U. et al. Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain. Nat. Methods 4, 331–336 (2007).
pubmed: 17384643 doi: 10.1038/nmeth1036
Ertürk, A. et al. Three-dimensional imaging of solvent-cleared organs using 3DISCO. Nat. Protoc. 7, 1983–1995 (2012).
pubmed: 23060243 doi: 10.1038/nprot.2012.119
Hama, H. et al. Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain. Nat. Neurosci. 14, 1481–1488 (2011).
pubmed: 21878933 doi: 10.1038/nn.2928
Chung, K. et al. Structural and molecular interrogation of intact biological systems. Nature 497, 332–337 (2013).
pubmed: 23575631 pmcid: 4092167 doi: 10.1038/nature12107
Voie, A. H., Burns, D. H. & Spelman, F. A. Orthogonal-plane fluorescence optical sectioning: three-dimensional imaging of macroscopic biological specimens. J. Microsc. 170, 229–236 (1993).
pubmed: 8371260 doi: 10.1111/j.1365-2818.1993.tb03346.x
Topilko, T. et al. Edinger–Westphal peptidergic neurons enable maternal preparatory nesting. Neuron 110, 1385–1399.e8 (2022).
pubmed: 35123655 pmcid: 9090132 doi: 10.1016/j.neuron.2022.01.012
Menegas, W. et al. Dopamine neurons projecting to the posterior striatum form an anatomically distinct subclass. eLife 4, e10032 (2015).
pubmed: 26322384 pmcid: 4598831 doi: 10.7554/eLife.10032
Lerner, T. N. et al. Intact-brain analyses reveal distinct information carried by SNc dopamine subcircuits. Cell 162, 635–647 (2015).
pubmed: 26232229 pmcid: 4790813 doi: 10.1016/j.cell.2015.07.014
Kirschenbaum, D. et al. Whole-brain microscopy reveals distinct temporal and spatial efficacy of anti–Aβ therapies. EMBO Mol. Med. 15, e16789 (2023).
pubmed: 36382364 doi: 10.15252/emmm.202216789
Lowenstein, E. D. et al. Prox2 and Runx3 vagal sensory neurons regulate esophageal motility. Neuron https://doi.org/10.1016/j.neuron.2023.04.025 (2023).
Belle, M. et al. Tridimensional visualization and analysis of early human development. Cell 169, 161–173.e12 (2017).
pubmed: 28340341 doi: 10.1016/j.cell.2017.03.008
Aguilera–Castrejon, A. et al. Ex utero mouse embryogenesis from pre-gastrulation to late organogenesis. Nature 593, 119–124 (2021).
pubmed: 33731940 doi: 10.1038/s41586-021-03416-3
Naert, T. et al. Deep learning is widely applicable to phenotyping embryonic development and disease. Development 148, dev199664 (2021).
pubmed: 34739029 pmcid: 8602947 doi: 10.1242/dev.199664
Kirst, C. et al. Mapping the fine-scale organization and plasticity of the brain vasculature. Cell 180, 780–795.e25 (2020).
pubmed: 32059781 doi: 10.1016/j.cell.2020.01.028
Kathe, C. et al. The neurons that restore walking after paralysis. Nature 611, 540–547 (2022).
pubmed: 36352232 pmcid: 9668750 doi: 10.1038/s41586-022-05385-7
Schepanski, S. et al. Pregnancy-induced maternal microchimerism shapes neurodevelopment and behavior in mice. Nat. Commun. 13, 4571 (2022).
pubmed: 35931682 pmcid: 9356013 doi: 10.1038/s41467-022-32230-2
Cai, R. et al. Whole-mouse clearing and imaging at the cellular level with vDISCO. Nat. Protoc. 18, 1197–1242 (2023).
pubmed: 36697871 doi: 10.1038/s41596-022-00788-2
Mai, H. et al. Whole mouse body histology using standard IgG antibodies. Nat. Biotechnol. https://doi.org/10.1038/s41587-023-01846-0 (2023).
Zhao, S. et al. Cellular and molecular probing of intact human organs. Cell 180, 796–812.e19 (2020).
pubmed: 32059778 pmcid: 7557154 doi: 10.1016/j.cell.2020.01.030
Glaser, A. K. et al. Multi-immersion open-top light-sheet microscope for high-throughput imaging of cleared tissues. Nat. Commun. 10, 2781 (2019).
Glaser, A. K. et al. Light-sheet microscopy for slide-free non-destructive pathology of large clinical specimens. Nat. Biomed. Eng. 1, 0084 (2017).
pubmed: 29750130 pmcid: 5940348 doi: 10.1038/s41551-017-0084
Glaser, A. K. et al. A hybrid open-top light-sheet microscope for versatile multi-scale imaging of cleared tissues. Nat. Methods 19, 613–619 (2022).
pubmed: 35545715 pmcid: 9214839 doi: 10.1038/s41592-022-01468-5
Alarcon, M. R. et al. Scientific CMOS sensors in astronomy: QHY600 and QHY411. Preprint at https://doi.org/10.48550/arXiv.2302.03700 (2023).
Ichimura, T. et al. Exploring rare cellular activity in more than one million cells by a transscale scope. Sci. Rep. 11, 16539 (2021).
pubmed: 34400683 pmcid: 8368064 doi: 10.1038/s41598-021-95930-7
McConnell, G. et al. A novel optical microscope for imaging large embryos and tissue volumes with sub-cellular resolution throughout. eLife 5, e18659 (2016).
pubmed: 27661778 pmcid: 5035146 doi: 10.7554/eLife.18659
Glaser, A. et al. Expansion-assisted selective plane illumination microscopy for nanoscale imaging of centimeter-scale tissues. eLife 12:RP91979, https://doi.org/10.7554/eLife.91979.1 (2023).
Boehm, U. et al. QUAREP-LiMi: a community endeavor to advance quality assessment and reproducibility in light microscopy. Nat. Methods 18, 1423–1426 (2021).
pubmed: 34021279 pmcid: 9443067 doi: 10.1038/s41592-021-01162-y
Faklaris, O. et al. Quality assessment in light microscopy for routine use through simple tools and robust metrics. J. Cell Biol. 221, e202107093 (2022).
pubmed: 36173380 pmcid: 9526251 doi: 10.1083/jcb.202107093
Voigt, F. F. et al. The mesoSPIM initiative: open-source light-sheet microscopes for imaging cleared tissue. Nat. Methods 16, 1105–1108 (2019).
Dean, K. M., Roudot, P., Welf, E. S., Danuser, G. & Fiolka, R. Deconvolution-free Subcellular Imaging with axially swept light sheet microscopy. Biophys. J. 108, 2807–2815 (2015).
pubmed: 26083920 pmcid: 4472079 doi: 10.1016/j.bpj.2015.05.013
Chakraborty, T. et al. Light-sheet microscopy of cleared tissues with isotropic, subcellular resolution. Nat. Methods 16, 1109–1113 (2019).
pubmed: 31673159 pmcid: 6924633 doi: 10.1038/s41592-019-0615-4
Dean, K. M. et al. Isotropic imaging across spatial scales with axially swept light-sheet microscopy. Nat. Protoc. 17, 2025–2053 (2022).
pubmed: 35831614 pmcid: 10111370 doi: 10.1038/s41596-022-00706-6
Power, R. M. & Huisken, J. A guide to light-sheet fluorescence microscopy for multiscale imaging. Nat. Methods 14, 360–373 (2017).
pubmed: 28362435 doi: 10.1038/nmeth.4224
Feng, G. et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41–51 (2000).
pubmed: 11086982 doi: 10.1016/S0896-6273(00)00084-2
Royon, A. & Converset, N. Quality control of fluorescence imaging systems. Opt. Photoniks 12, 22–25 (2017).
doi: 10.1002/opph.201700005
Dube, B., Cicala, R., Closz, A. & Rolland, J. P. How good is your lens? assessing performance with MTF full-field displays. Appl. Opt. 56, 5661–5667 (2017).
pubmed: 29047708 doi: 10.1364/AO.56.005661
Cicala, R. Developing a rapid MTF test for photo and video lenses. Lensrentals Blog https://www.lensrentals.com/blog/2018/06/developing-a-rapid-mtf-test-for-photo-and-video-lenses/ (2018).
Voigt, F. F. et al. MesoSPIM control: an open-source acquisition software for light-sheet microscopy written in Python and Qt (1.8.3). Zenodo https://doi.org/10.5281/zenodo.6109314 (2024).
Vladimirov, N. npy2bdv: writing numpy arrays to Fiji/BigDataViewer HDF5 files (v.1.0.8). Zenodo https://doi.org/10.5281/zenodo.6148906 (2022).
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772 doi: 10.1038/nmeth.2019
Pietzsch, T., Saalfeld, S., Preibisch, S. & Tomancak, P. BigDataViewer: visualization and processing for large image data sets. Nat. Methods 12, 481–483 (2015).
pubmed: 26020499 doi: 10.1038/nmeth.3392
Dumoulin, A. & Stoeckli, E. T. Looking for guidance – models and methods to study axonal navigation. Neuroscience 508, 30–39 (2023).
pubmed: 35940454 doi: 10.1016/j.neuroscience.2022.08.005
Renier, N. et al. Mapping of brain activity by automated volume analysis of immediate early genes. Cell 165, 1789–1802 (2016).
pubmed: 27238021 pmcid: 4912438 doi: 10.1016/j.cell.2016.05.007
Hildebrand, S., Schueth, A., Herrler, A., Galuske, R. & Roebroeck, A. Scalable labeling for cytoarchitectonic characterization of large optically cleared human neocortex samples. Sci. Rep. 9, 10880 (2019).
pubmed: 31350519 pmcid: 6659684 doi: 10.1038/s41598-019-47336-9
Fritsch, E. & Rossman, G. An update on color in gems. Part 2: colors involving multiple atoms and color centers. Gems Gemol. 24, 3–15 (1988).
doi: 10.5741/GEMS.24.1.3
Tilley, R. J. D. Defects in Solids. (Wiley, Hoboken, 2008).
Tilley, R. J. D. Colour and the Optical Properties of Materials, 2nd edn. (Wiley, Chichester, 2011).
Masuda, K. et al. Novel techniques for high precision refractive index measurements, and application to assessing neutron damage and dose in crystals. Nucl. Instrum. Methods Phys. Res. Sect. Accel. Spectrometers Detect. Assoc. Equip. 784, 198–201 (2015).
doi: 10.1016/j.nima.2014.11.031
Mosbacher, Y. et al. Wide band spectroscopic response of monocrystallines to low dose neutron and gamma radiation. arXiv preprint arXiv:1902.10668 (2019).
Cogswell, B. K., Goel, A. & Huber, P. Passive low-energy nuclear-recoil detection with color centers. Phys. Rev. Appl. 16, 064060 (2021).
doi: 10.1103/PhysRevApplied.16.064060
Alfonso, K. et al. Passive low energy nuclear recoil detection with color centers–PALEOCCENE. arXiv preprint arXiv:2203.05525 (2022).
Baum, S. et al. Mineral detection of neutrinos and dark matter. A whitepaper. Phys. Dark Universe 41, 101245 (2023).
doi: 10.1016/j.dark.2023.101245
Otomo, K., Omura, T., Nozawa, Y., Saito, Y. & Susaki, E. A. descSPIM: affordable and easy-to-build light-sheet microscopy for tissue clearing technique users. Preprint at https://doi.org/10.1101/2023.05.02.539136 (2023).
Hörl, D. et al. BigStitcher: reconstructing high-resolution image datasets of cleared and expanded samples. Nat. Methods 16, 870–874 (2019).
pubmed: 31384047 doi: 10.1038/s41592-019-0501-0
Sjölander, D. et al. Establishing the fluorescent amyloid ligand h-FTAA for studying human tissues with systemic and localized amyloid. Amyloid 23, 98–108 (2016).
pubmed: 26987044 doi: 10.3109/13506129.2016.1158159
Cai, R. et al. Panoptic imaging of transparent mice reveals whole-body neuronal projections and skull–meninges connections. Nat. Neurosci. 22, 317–327 (2019).
pubmed: 30598527 doi: 10.1038/s41593-018-0301-3
Tainaka, K. et al. Whole-body imaging with single-cell resolution by tissue decolorization. Cell 159, 911–924 (2014).
pubmed: 25417165 doi: 10.1016/j.cell.2014.10.034
McIlvaine, T. C. A buffer solution for colorimetric comparison. J. Biol. Chem. 49, 183–186 (1921).
doi: 10.1016/S0021-9258(18)86000-8
Klingberg, A. et al. Fully automated evaluation of total glomerular number and capillary tuft size in nephritic kidneys using lightsheet microscopy. J. Am. Soc. Nephrol. 28, 452–459 (2017).
pubmed: 27487796 doi: 10.1681/ASN.2016020232
Attenuation coefficients and scattering Table. https://physics.nist.gov/PhysRefData/XrayMassCoef/ComTab/fluoride.html (2023).
Walt, Svander et al. scikit-image: image processing in Python. PeerJ 2, e453 (2014).
pubmed: 25024921 pmcid: 4081273 doi: 10.7717/peerj.453

Auteurs

Nikita Vladimirov (N)

Brain Research Institute, University of Zurich, Zurich, Switzerland. vladimirov@hifo.uzh.ch.
University Research Priority Program (URPP), Adaptive Brain Circuits in Development and Learning, University of Zurich, Zurich, Switzerland. vladimirov@hifo.uzh.ch.
Center for Microscopy and Image Analysis (ZMB), University of Zurich, Zurich, Switzerland. vladimirov@hifo.uzh.ch.

Fabian F Voigt (FF)

Brain Research Institute, University of Zurich, Zurich, Switzerland.
Neuroscience Center Zurich (ZNZ), University of Zurich, Zurich, Switzerland.
Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA, USA.

Thomas Naert (T)

Institute of Anatomy and Zurich Kidney Center (ZKC), University of Zurich, Zurich, Switzerland.

Gabriela R Araujo (GR)

Department of Physics, University of Zurich, Zurich, Switzerland.

Ruiyao Cai (R)

Institute for Tissue Engineering and Regenerative Medicine (iTERM), Helmholtz Center Munich, Neuherberg, Germany.
Institute for Stroke and Dementia Research, Klinikum der Universität München, Ludwig-Maximilians University Munich, Munich, Germany.
Department of Biology, Stanford University, Stanford, CA, USA.

Anna Maria Reuss (AM)

Neuroscience Center Zurich (ZNZ), University of Zurich, Zurich, Switzerland.
Institute of Neuropathology, University Hospital Zurich, Zurich, Switzerland.

Shan Zhao (S)

Department of Quantitative Biomedicine, University of Zurich, Zurich, Switzerland.

Patricia Schmid (P)

Institute of Anatomy and Zurich Kidney Center (ZKC), University of Zurich, Zurich, Switzerland.

Sven Hildebrand (S)

Department of Cognitive Neuroscience, Faculty of Psychology & Neuroscience, Maastricht University, Maastricht, The Netherlands.

Martina Schaettin (M)

Neuroscience Center Zurich (ZNZ), University of Zurich, Zurich, Switzerland.
Department of Molecular Life Sciences, University of Zurich, Zurich, Switzerland.

Dominik Groos (D)

Brain Research Institute, University of Zurich, Zurich, Switzerland.

José María Mateos (JM)

Center for Microscopy and Image Analysis (ZMB), University of Zurich, Zurich, Switzerland.

Philipp Bethge (P)

Brain Research Institute, University of Zurich, Zurich, Switzerland.
Neuroscience Center Zurich (ZNZ), University of Zurich, Zurich, Switzerland.

Taiyo Yamamoto (T)

Institute of Anatomy and Zurich Kidney Center (ZKC), University of Zurich, Zurich, Switzerland.

Valentino Aerne (V)

Department of Physics, University of Zurich, Zurich, Switzerland.

Alard Roebroeck (A)

Department of Cognitive Neuroscience, Faculty of Psychology & Neuroscience, Maastricht University, Maastricht, The Netherlands.

Ali Ertürk (A)

Institute for Tissue Engineering and Regenerative Medicine (iTERM), Helmholtz Center Munich, Neuherberg, Germany.
Institute for Stroke and Dementia Research, Klinikum der Universität München, Ludwig-Maximilians University Munich, Munich, Germany.

Adriano Aguzzi (A)

Neuroscience Center Zurich (ZNZ), University of Zurich, Zurich, Switzerland.
Institute of Neuropathology, University Hospital Zurich, Zurich, Switzerland.

Urs Ziegler (U)

Center for Microscopy and Image Analysis (ZMB), University of Zurich, Zurich, Switzerland.

Esther Stoeckli (E)

University Research Priority Program (URPP), Adaptive Brain Circuits in Development and Learning, University of Zurich, Zurich, Switzerland.
Neuroscience Center Zurich (ZNZ), University of Zurich, Zurich, Switzerland.
Department of Molecular Life Sciences, University of Zurich, Zurich, Switzerland.

Laura Baudis (L)

Department of Physics, University of Zurich, Zurich, Switzerland.

Soeren S Lienkamp (SS)

Institute of Anatomy and Zurich Kidney Center (ZKC), University of Zurich, Zurich, Switzerland.

Fritjof Helmchen (F)

Brain Research Institute, University of Zurich, Zurich, Switzerland. helmchen@hifo.uzh.ch.
University Research Priority Program (URPP), Adaptive Brain Circuits in Development and Learning, University of Zurich, Zurich, Switzerland. helmchen@hifo.uzh.ch.
Neuroscience Center Zurich (ZNZ), University of Zurich, Zurich, Switzerland. helmchen@hifo.uzh.ch.

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