Abstract

High-resolution three-dimensional biomolecule distribution information of large samples is essential to understanding their biological structure and function. Here, we proposed a method combining large sample resin embedding with iDISCO immunofluorescence staining to acquire the profile of biomolecules with high spatial resolution. We evaluated the compatibility of plastic embedding with an iDISCO staining technique and found that the fluorophores and the neuronal fine structures could be well preserved in the Lowicryl HM20 resin, and that numerous antibodies and fluorescent tracers worked well upon Lowicryl HM20 resin embedding. Further, using fluorescence Micro-Optical sectioning tomography (fMOST) technology combined with ultra-thin slicing and imaging, we were able to image the immunolabeled large-volume tissues with high resolution.

© 2017 Optical Society of America

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  1. T. Alanentalo, A. Asayesh, H. Morrison, C. E. Lorén, D. Holmberg, J. Sharpe, and U. Ahlgren, “Tomographic molecular imaging and 3D quantification within adult mouse organs,” Nat. Methods 4(1), 31–33 (2007).
    [Crossref] [PubMed]
  2. K. Chung, J. Wallace, S. Y. Kim, S. Kalyanasundaram, A. S. Andalman, T. J. Davidson, J. J. Mirzabekov, K. A. Zalocusky, J. Mattis, A. K. Denisin, S. Pak, H. Bernstein, C. Ramakrishnan, L. Grosenick, V. Gradinaru, and K. Deisseroth, “Structural and molecular interrogation of intact biological systems,” Nature 497(7449), 332–337 (2013).
    [Crossref] [PubMed]
  3. A. H. Coons, H. J. Creech, R. N. Jones, and E. Berliner, “The demonstration of pneumococcal antigen in tissues by the use of fluorescent antibody,” J. Immunol. 45(3), 159–170 (1942).
  4. A. H. Coons and M. H. Kaplan, “Localization of antigen in tissue cells; improvements in a method for the detection of antigen by means of fluorescent antibody,” J. Exp. Med. 91(1), 1–13 (1949).
    [Crossref] [PubMed]
  5. N. Renier, Z. Wu, D. J. Simon, J. Yang, P. Ariel, and M. Tessier-Lavigne, “iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging,” Cell 159(4), 896–910 (2014).
    [Crossref] [PubMed]
  6. S. Karma, J. Homan, C. Stoianovici, and B. Choi, “Enhanced fluorescence imaging with DMSO-mediated optical clearing,” J. Innov. Opt. Health Sci. 3(3), 153–158 (2010).
    [Crossref]
  7. B. Yang, J. B. Treweek, R. P. Kulkarni, B. E. Deverman, C. K. Chen, E. Lubeck, S. Shah, L. Cai, and V. Gradinaru, “Single-cell phenotyping within transparent intact tissue through whole-body clearing,” Cell 158(4), 945–958 (2014).
    [Crossref] [PubMed]
  8. E. Murray, J. H. Cho, D. Goodwin, T. Ku, J. Swaney, S. Y. Kim, H. Choi, Y. G. Park, J. Y. Park, A. Hubbert, M. McCue, S. Vassallo, N. Bakh, M. P. Frosch, V. J. Wedeen, H. S. Seung, and K. Chung, “Simple, scalable proteomic imaging for high-dimensional profiling of intact systems,” Cell 163(6), 1500–1514 (2015).
    [Crossref] [PubMed]
  9. E. A. Susaki, K. Tainaka, D. Perrin, F. Kishino, T. Tawara, T. M. Watanabe, C. Yokoyama, H. Onoe, M. Eguchi, S. Yamaguchi, T. Abe, H. Kiyonari, Y. Shimizu, A. Miyawaki, H. Yokota, and H. R. Ueda, “Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis,” Cell 157(3), 726–739 (2014).
    [Crossref] [PubMed]
  10. H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci. 14(11), 1481–1488 (2011).
    [Crossref] [PubMed]
  11. J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science 296(5567), 541–545 (2002).
    [Crossref] [PubMed]
  12. L. Silvestri, A. L. Allegra Mascaro, J. Lotti, L. Sacconi, and F. S. Pavone, “Advanced optical techniques to explore brain structure and function,” J. Innov. Opt. Health Sci. 6(1), 1230002 (2013).
    [Crossref]
  13. B. A. Wilt, L. D. Burns, E. T. Wei Ho, K. K. Ghosh, E. A. Mukamel, and M. J. Schnitzer, “Advances in light microscopy for neuroscience,” Annu. Rev. Neurosci. 32(1), 435–506 (2009).
    [Crossref] [PubMed]
  14. W. J. Weninger, S. H. Geyer, T. J. Mohun, D. Rasskin-Gutman, T. Matsui, I. Ribeiro, L. F. Costa, J. C. Izpisúa-Belmonte, and G. B. Müller, “High-resolution episcopic microscopy: a rapid technique for high detailed 3D analysis of gene activity in the context of tissue architecture and morphology,” Anat. Embryol. (Berl.) 211(3), 213–221 (2006).
    [Crossref] [PubMed]
  15. A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-optical sectioning tomography to obtain a high-resolution atlas of the mouse brain,” Science 330(6009), 1404–1408 (2010).
    [Crossref] [PubMed]
  16. T. Zheng, Z. Yang, A. Li, X. Lv, Z. Zhou, X. Wang, X. Qi, S. Li, Q. Luo, H. Gong, and S. Zeng, “Visualization of brain circuits using two-photon fluorescence micro-optical sectioning tomography,” Opt. Express 21(8), 9839–9850 (2013).
    [Crossref] [PubMed]
  17. H. Gong, S. Zeng, C. Yan, X. Lv, Z. Yang, T. Xu, Z. Feng, W. Ding, X. Qi, A. Li, J. Wu, and Q. Luo, “Continuously tracing brain-wide long-distance axonal projections in mice at a one-micron voxel resolution,” Neuroimage 74, 87–98 (2013).
    [Crossref] [PubMed]
  18. B. Zhang, A. Li, Z. Yang, J. Wu, Q. Luo, and H. Gong, “Modified Golgi-Cox method for micrometer scale sectioning of the whole mouse brain,” J. Neurosci. Methods 197(1), 1–5 (2011).
    [Crossref] [PubMed]
  19. S. S. Biel, K. Kawaschinski, K. P. Wittern, U. Hintze, and R. Wepf, “From tissue to cellular ultrastructure: closing the gap between micro- and nanostructural imaging,” J. Microsc. 212(1), 91–99 (2003).
    [Crossref] [PubMed]
  20. S. Wessel, S. Pagel, M. Ritter, H. Hohenberg, and R. Wepf, “Topographic Measurements of Real Structures in reflection Confocal Laser Scanning Microscope (CLSM),” Microsc. Microanal. 9(S03), 162–163 (2003).
  21. M. Perkovic, M. Kunz, U. Endesfelder, S. Bunse, C. Wigge, Z. Yu, V. V. Hodirnau, M. P. Scheffer, A. Seybert, S. Malkusch, E. M. Schuman, M. Heilemann, and A. S. Frangakis, “Correlative light- and electron microscopy with chemical tags,” J. Struct. Biol. 186(2), 205–213 (2014).
    [Crossref] [PubMed]
  22. D. Kim, T. J. Deerinck, Y. M. Sigal, H. P. Babcock, M. H. Ellisman, and X. Zhuang, “Correlative stochastic optical reconstruction microscopy and electron microscopy,” PLoS One 10(4), e0124581 (2015).
    [Crossref] [PubMed]
  23. A. Burette, L. Khatri, M. Wyszynski, M. Sheng, E. B. Ziff, and R. J. Weinberg, “Differential cellular and subcellular localization of ampa receptor-binding protein and glutamate receptor-interacting protein,” J. Neurosci. 21(2), 495–503 (2001).
    [PubMed]
  24. Y. Gang, H. Zhou, Y. Jia, L. Liu, X. Liu, G. Rao, L. Li, X. Wang, X. Lv, H. Xiong, Z. Yang, Q. Luo, H. Gong, and S. Zeng, “Embedding and chemical reactivation of green fluorescent protein in the whole mouse brain for optical micro-imaging,” Front. Neurosci. 11, 121 (2017).
    [Crossref] [PubMed]
  25. Y. Sun, H. Yu, D. Zheng, Q. Cao, Y. Wang, D. Harris, and Y. Wang, “Sudan black B reduces autofluorescence in murine renal tissue,” Arch. Pathol. Lab. Med. 135(10), 1335–1342 (2011).
    [Crossref] [PubMed]
  26. H. Gong, D. Xu, J. Yuan, X. Li, C. Guo, J. Peng, Y. Li, L. A. Schwarz, A. Li, B. Hu, B. Xiong, Q. Sun, Y. Zhang, J. Liu, Q. Zhong, T. Xu, S. Zeng, and Q. Luo, “High-throughput dual-colour precision imaging for brain-wide connectome with cytoarchitectonic landmarks at the cellular level,” Nat. Commun. 7, 12142 (2016).
    [Crossref] [PubMed]
  27. T. Yang, T. Zheng, Z. Shang, X. Wang, X. Lv, J. Yuan, and S. Zeng, “Rapid imaging of large tissues using high-resolution stage-scanning microscopy,” Biomed. Opt. Express 6(5), 1867–1875 (2015).
    [Crossref] [PubMed]
  28. J. Wu, Y. He, Z. Yang, C. Guo, Q. Luo, W. Zhou, S. Chen, A. Li, B. Xiong, T. Jiang, and H. Gong, “3D BrainCV: simultaneous visualization and analysis of cells and capillaries in a whole mouse brain with one-micron voxel resolution,” Neuroimage 87, 199–208 (2014).
    [Crossref] [PubMed]
  29. T. Quan, H. Zhou, J. Li, S. Li, A. Li, Y. Li, X. Lv, Q. Luo, H. Gong, and S. Zeng, “NeuroGPS-Tree: automatic reconstruction of large-scale neuronal populations with dense neurites,” Nat. Methods 13(1), 51–54 (2016).
    [PubMed]
  30. J. Li, T. Quan, S. Li, H. Zhou, Q. Luo, H. Gong, and S. Zeng, “Reconstruction of micron resolution mouse brain surface from large-scale imaging dataset using resampling-based variational model,” Sci. Rep. 5(1), 12782 (2015).
    [Crossref] [PubMed]
  31. T. Quan, T. Zheng, Z. Yang, W. Ding, S. Li, J. Li, H. Zhou, Q. Luo, H. Gong, and S. Zeng, “NeuroGPS: automated localization of neurons for brain circuits using L1 minimization model,” Sci. Rep. 3(1), 1414 (2013).
    [Crossref] [PubMed]
  32. S. Li, H. Zhou, T. Quan, J. Li, Y. Li, A. Li, Q. Luo, H. Gong, and S. Zeng, “SparseTracer: the reconstruction of discontinuous neuronal morphology in noisy images,” Neuroinformatics 15(2), 133–149 (2017).
    [Crossref] [PubMed]
  33. S. B. Newman, E. Borysko, and M. Swerdlow, “New sectioning techniques for light and electron microscopy,” Science 110(2846), 66–68 (1949).
    [Crossref] [PubMed]
  34. G. R. Newman and J. A. Hobot, “Resins for combined light and electron microscopy: a half century of development,” Histochem. J. 31(8), 495–505 (1999).
    [Crossref] [PubMed]
  35. Z. Yang, B. Hu, Y. Zhang, Q. Luo, and H. Gong, “Development of a plastic embedding method for large-volume and fluorescent-protein-expressing tissues,” PLoS One 8(4), e60877 (2013).
    [Crossref] [PubMed]
  36. H. Xiong, Z. Zhou, M. Zhu, X. Lv, A. Li, S. Li, L. Li, T. Yang, S. Wang, Z. Yang, T. Xu, Q. Luo, H. Gong, and S. Zeng, “Chemical reactivation of quenched fluorescent protein molecules enables resin-embedded fluorescence microimaging,” Nat. Commun. 5, 3992 (2014).
    [Crossref] [PubMed]
  37. M. A. Karreman, A. V. Agronskaia, E. G. van Donselaar, K. Vocking, F. Fereidouni, B. M. Humbel, C. T. Verrips, A. J. Verkleij, and H. C. Gerritsen, “Optimizing immuno-labeling for correlative fluorescence and electron microscopy on a single specimen,” J. Struct. Biol. 180(2), 382–386 (2012).
    [Crossref] [PubMed]
  38. J. A. Ramos-Vara, “Technical aspects of immunohistochemistry,” Vet. Pathol. 42(4), 405–426 (2005).
    [Crossref] [PubMed]
  39. F. Collman, J. Buchanan, K. D. Phend, K. D. Micheva, R. J. Weinberg, and S. J. Smith, “Mapping synapses by conjugate light-electron array tomography,” J. Neurosci. 35(14), 5792–5807 (2015).
    [Crossref] [PubMed]

2017 (2)

Y. Gang, H. Zhou, Y. Jia, L. Liu, X. Liu, G. Rao, L. Li, X. Wang, X. Lv, H. Xiong, Z. Yang, Q. Luo, H. Gong, and S. Zeng, “Embedding and chemical reactivation of green fluorescent protein in the whole mouse brain for optical micro-imaging,” Front. Neurosci. 11, 121 (2017).
[Crossref] [PubMed]

S. Li, H. Zhou, T. Quan, J. Li, Y. Li, A. Li, Q. Luo, H. Gong, and S. Zeng, “SparseTracer: the reconstruction of discontinuous neuronal morphology in noisy images,” Neuroinformatics 15(2), 133–149 (2017).
[Crossref] [PubMed]

2016 (2)

T. Quan, H. Zhou, J. Li, S. Li, A. Li, Y. Li, X. Lv, Q. Luo, H. Gong, and S. Zeng, “NeuroGPS-Tree: automatic reconstruction of large-scale neuronal populations with dense neurites,” Nat. Methods 13(1), 51–54 (2016).
[PubMed]

H. Gong, D. Xu, J. Yuan, X. Li, C. Guo, J. Peng, Y. Li, L. A. Schwarz, A. Li, B. Hu, B. Xiong, Q. Sun, Y. Zhang, J. Liu, Q. Zhong, T. Xu, S. Zeng, and Q. Luo, “High-throughput dual-colour precision imaging for brain-wide connectome with cytoarchitectonic landmarks at the cellular level,” Nat. Commun. 7, 12142 (2016).
[Crossref] [PubMed]

2015 (5)

T. Yang, T. Zheng, Z. Shang, X. Wang, X. Lv, J. Yuan, and S. Zeng, “Rapid imaging of large tissues using high-resolution stage-scanning microscopy,” Biomed. Opt. Express 6(5), 1867–1875 (2015).
[Crossref] [PubMed]

D. Kim, T. J. Deerinck, Y. M. Sigal, H. P. Babcock, M. H. Ellisman, and X. Zhuang, “Correlative stochastic optical reconstruction microscopy and electron microscopy,” PLoS One 10(4), e0124581 (2015).
[Crossref] [PubMed]

J. Li, T. Quan, S. Li, H. Zhou, Q. Luo, H. Gong, and S. Zeng, “Reconstruction of micron resolution mouse brain surface from large-scale imaging dataset using resampling-based variational model,” Sci. Rep. 5(1), 12782 (2015).
[Crossref] [PubMed]

E. Murray, J. H. Cho, D. Goodwin, T. Ku, J. Swaney, S. Y. Kim, H. Choi, Y. G. Park, J. Y. Park, A. Hubbert, M. McCue, S. Vassallo, N. Bakh, M. P. Frosch, V. J. Wedeen, H. S. Seung, and K. Chung, “Simple, scalable proteomic imaging for high-dimensional profiling of intact systems,” Cell 163(6), 1500–1514 (2015).
[Crossref] [PubMed]

F. Collman, J. Buchanan, K. D. Phend, K. D. Micheva, R. J. Weinberg, and S. J. Smith, “Mapping synapses by conjugate light-electron array tomography,” J. Neurosci. 35(14), 5792–5807 (2015).
[Crossref] [PubMed]

2014 (6)

E. A. Susaki, K. Tainaka, D. Perrin, F. Kishino, T. Tawara, T. M. Watanabe, C. Yokoyama, H. Onoe, M. Eguchi, S. Yamaguchi, T. Abe, H. Kiyonari, Y. Shimizu, A. Miyawaki, H. Yokota, and H. R. Ueda, “Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis,” Cell 157(3), 726–739 (2014).
[Crossref] [PubMed]

N. Renier, Z. Wu, D. J. Simon, J. Yang, P. Ariel, and M. Tessier-Lavigne, “iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging,” Cell 159(4), 896–910 (2014).
[Crossref] [PubMed]

M. Perkovic, M. Kunz, U. Endesfelder, S. Bunse, C. Wigge, Z. Yu, V. V. Hodirnau, M. P. Scheffer, A. Seybert, S. Malkusch, E. M. Schuman, M. Heilemann, and A. S. Frangakis, “Correlative light- and electron microscopy with chemical tags,” J. Struct. Biol. 186(2), 205–213 (2014).
[Crossref] [PubMed]

H. Xiong, Z. Zhou, M. Zhu, X. Lv, A. Li, S. Li, L. Li, T. Yang, S. Wang, Z. Yang, T. Xu, Q. Luo, H. Gong, and S. Zeng, “Chemical reactivation of quenched fluorescent protein molecules enables resin-embedded fluorescence microimaging,” Nat. Commun. 5, 3992 (2014).
[Crossref] [PubMed]

B. Yang, J. B. Treweek, R. P. Kulkarni, B. E. Deverman, C. K. Chen, E. Lubeck, S. Shah, L. Cai, and V. Gradinaru, “Single-cell phenotyping within transparent intact tissue through whole-body clearing,” Cell 158(4), 945–958 (2014).
[Crossref] [PubMed]

J. Wu, Y. He, Z. Yang, C. Guo, Q. Luo, W. Zhou, S. Chen, A. Li, B. Xiong, T. Jiang, and H. Gong, “3D BrainCV: simultaneous visualization and analysis of cells and capillaries in a whole mouse brain with one-micron voxel resolution,” Neuroimage 87, 199–208 (2014).
[Crossref] [PubMed]

2013 (6)

T. Quan, T. Zheng, Z. Yang, W. Ding, S. Li, J. Li, H. Zhou, Q. Luo, H. Gong, and S. Zeng, “NeuroGPS: automated localization of neurons for brain circuits using L1 minimization model,” Sci. Rep. 3(1), 1414 (2013).
[Crossref] [PubMed]

L. Silvestri, A. L. Allegra Mascaro, J. Lotti, L. Sacconi, and F. S. Pavone, “Advanced optical techniques to explore brain structure and function,” J. Innov. Opt. Health Sci. 6(1), 1230002 (2013).
[Crossref]

T. Zheng, Z. Yang, A. Li, X. Lv, Z. Zhou, X. Wang, X. Qi, S. Li, Q. Luo, H. Gong, and S. Zeng, “Visualization of brain circuits using two-photon fluorescence micro-optical sectioning tomography,” Opt. Express 21(8), 9839–9850 (2013).
[Crossref] [PubMed]

H. Gong, S. Zeng, C. Yan, X. Lv, Z. Yang, T. Xu, Z. Feng, W. Ding, X. Qi, A. Li, J. Wu, and Q. Luo, “Continuously tracing brain-wide long-distance axonal projections in mice at a one-micron voxel resolution,” Neuroimage 74, 87–98 (2013).
[Crossref] [PubMed]

K. Chung, J. Wallace, S. Y. Kim, S. Kalyanasundaram, A. S. Andalman, T. J. Davidson, J. J. Mirzabekov, K. A. Zalocusky, J. Mattis, A. K. Denisin, S. Pak, H. Bernstein, C. Ramakrishnan, L. Grosenick, V. Gradinaru, and K. Deisseroth, “Structural and molecular interrogation of intact biological systems,” Nature 497(7449), 332–337 (2013).
[Crossref] [PubMed]

Z. Yang, B. Hu, Y. Zhang, Q. Luo, and H. Gong, “Development of a plastic embedding method for large-volume and fluorescent-protein-expressing tissues,” PLoS One 8(4), e60877 (2013).
[Crossref] [PubMed]

2012 (1)

M. A. Karreman, A. V. Agronskaia, E. G. van Donselaar, K. Vocking, F. Fereidouni, B. M. Humbel, C. T. Verrips, A. J. Verkleij, and H. C. Gerritsen, “Optimizing immuno-labeling for correlative fluorescence and electron microscopy on a single specimen,” J. Struct. Biol. 180(2), 382–386 (2012).
[Crossref] [PubMed]

2011 (3)

Y. Sun, H. Yu, D. Zheng, Q. Cao, Y. Wang, D. Harris, and Y. Wang, “Sudan black B reduces autofluorescence in murine renal tissue,” Arch. Pathol. Lab. Med. 135(10), 1335–1342 (2011).
[Crossref] [PubMed]

H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci. 14(11), 1481–1488 (2011).
[Crossref] [PubMed]

B. Zhang, A. Li, Z. Yang, J. Wu, Q. Luo, and H. Gong, “Modified Golgi-Cox method for micrometer scale sectioning of the whole mouse brain,” J. Neurosci. Methods 197(1), 1–5 (2011).
[Crossref] [PubMed]

2010 (2)

S. Karma, J. Homan, C. Stoianovici, and B. Choi, “Enhanced fluorescence imaging with DMSO-mediated optical clearing,” J. Innov. Opt. Health Sci. 3(3), 153–158 (2010).
[Crossref]

A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-optical sectioning tomography to obtain a high-resolution atlas of the mouse brain,” Science 330(6009), 1404–1408 (2010).
[Crossref] [PubMed]

2009 (1)

B. A. Wilt, L. D. Burns, E. T. Wei Ho, K. K. Ghosh, E. A. Mukamel, and M. J. Schnitzer, “Advances in light microscopy for neuroscience,” Annu. Rev. Neurosci. 32(1), 435–506 (2009).
[Crossref] [PubMed]

2007 (1)

T. Alanentalo, A. Asayesh, H. Morrison, C. E. Lorén, D. Holmberg, J. Sharpe, and U. Ahlgren, “Tomographic molecular imaging and 3D quantification within adult mouse organs,” Nat. Methods 4(1), 31–33 (2007).
[Crossref] [PubMed]

2006 (1)

W. J. Weninger, S. H. Geyer, T. J. Mohun, D. Rasskin-Gutman, T. Matsui, I. Ribeiro, L. F. Costa, J. C. Izpisúa-Belmonte, and G. B. Müller, “High-resolution episcopic microscopy: a rapid technique for high detailed 3D analysis of gene activity in the context of tissue architecture and morphology,” Anat. Embryol. (Berl.) 211(3), 213–221 (2006).
[Crossref] [PubMed]

2005 (1)

J. A. Ramos-Vara, “Technical aspects of immunohistochemistry,” Vet. Pathol. 42(4), 405–426 (2005).
[Crossref] [PubMed]

2003 (2)

S. S. Biel, K. Kawaschinski, K. P. Wittern, U. Hintze, and R. Wepf, “From tissue to cellular ultrastructure: closing the gap between micro- and nanostructural imaging,” J. Microsc. 212(1), 91–99 (2003).
[Crossref] [PubMed]

S. Wessel, S. Pagel, M. Ritter, H. Hohenberg, and R. Wepf, “Topographic Measurements of Real Structures in reflection Confocal Laser Scanning Microscope (CLSM),” Microsc. Microanal. 9(S03), 162–163 (2003).

2002 (1)

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science 296(5567), 541–545 (2002).
[Crossref] [PubMed]

2001 (1)

A. Burette, L. Khatri, M. Wyszynski, M. Sheng, E. B. Ziff, and R. J. Weinberg, “Differential cellular and subcellular localization of ampa receptor-binding protein and glutamate receptor-interacting protein,” J. Neurosci. 21(2), 495–503 (2001).
[PubMed]

1999 (1)

G. R. Newman and J. A. Hobot, “Resins for combined light and electron microscopy: a half century of development,” Histochem. J. 31(8), 495–505 (1999).
[Crossref] [PubMed]

1949 (2)

S. B. Newman, E. Borysko, and M. Swerdlow, “New sectioning techniques for light and electron microscopy,” Science 110(2846), 66–68 (1949).
[Crossref] [PubMed]

A. H. Coons and M. H. Kaplan, “Localization of antigen in tissue cells; improvements in a method for the detection of antigen by means of fluorescent antibody,” J. Exp. Med. 91(1), 1–13 (1949).
[Crossref] [PubMed]

1942 (1)

A. H. Coons, H. J. Creech, R. N. Jones, and E. Berliner, “The demonstration of pneumococcal antigen in tissues by the use of fluorescent antibody,” J. Immunol. 45(3), 159–170 (1942).

Abe, T.

E. A. Susaki, K. Tainaka, D. Perrin, F. Kishino, T. Tawara, T. M. Watanabe, C. Yokoyama, H. Onoe, M. Eguchi, S. Yamaguchi, T. Abe, H. Kiyonari, Y. Shimizu, A. Miyawaki, H. Yokota, and H. R. Ueda, “Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis,” Cell 157(3), 726–739 (2014).
[Crossref] [PubMed]

Agronskaia, A. V.

M. A. Karreman, A. V. Agronskaia, E. G. van Donselaar, K. Vocking, F. Fereidouni, B. M. Humbel, C. T. Verrips, A. J. Verkleij, and H. C. Gerritsen, “Optimizing immuno-labeling for correlative fluorescence and electron microscopy on a single specimen,” J. Struct. Biol. 180(2), 382–386 (2012).
[Crossref] [PubMed]

Ahlgren, U.

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J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science 296(5567), 541–545 (2002).
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D. Kim, T. J. Deerinck, Y. M. Sigal, H. P. Babcock, M. H. Ellisman, and X. Zhuang, “Correlative stochastic optical reconstruction microscopy and electron microscopy,” PLoS One 10(4), e0124581 (2015).
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B. Yang, J. B. Treweek, R. P. Kulkarni, B. E. Deverman, C. K. Chen, E. Lubeck, S. Shah, L. Cai, and V. Gradinaru, “Single-cell phenotyping within transparent intact tissue through whole-body clearing,” Cell 158(4), 945–958 (2014).
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K. Chung, J. Wallace, S. Y. Kim, S. Kalyanasundaram, A. S. Andalman, T. J. Davidson, J. J. Mirzabekov, K. A. Zalocusky, J. Mattis, A. K. Denisin, S. Pak, H. Bernstein, C. Ramakrishnan, L. Grosenick, V. Gradinaru, and K. Deisseroth, “Structural and molecular interrogation of intact biological systems,” Nature 497(7449), 332–337 (2013).
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H. Gong, D. Xu, J. Yuan, X. Li, C. Guo, J. Peng, Y. Li, L. A. Schwarz, A. Li, B. Hu, B. Xiong, Q. Sun, Y. Zhang, J. Liu, Q. Zhong, T. Xu, S. Zeng, and Q. Luo, “High-throughput dual-colour precision imaging for brain-wide connectome with cytoarchitectonic landmarks at the cellular level,” Nat. Commun. 7, 12142 (2016).
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J. Wu, Y. He, Z. Yang, C. Guo, Q. Luo, W. Zhou, S. Chen, A. Li, B. Xiong, T. Jiang, and H. Gong, “3D BrainCV: simultaneous visualization and analysis of cells and capillaries in a whole mouse brain with one-micron voxel resolution,” Neuroimage 87, 199–208 (2014).
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J. Wu, Y. He, Z. Yang, C. Guo, Q. Luo, W. Zhou, S. Chen, A. Li, B. Xiong, T. Jiang, and H. Gong, “3D BrainCV: simultaneous visualization and analysis of cells and capillaries in a whole mouse brain with one-micron voxel resolution,” Neuroimage 87, 199–208 (2014).
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Y. Gang, H. Zhou, Y. Jia, L. Liu, X. Liu, G. Rao, L. Li, X. Wang, X. Lv, H. Xiong, Z. Yang, Q. Luo, H. Gong, and S. Zeng, “Embedding and chemical reactivation of green fluorescent protein in the whole mouse brain for optical micro-imaging,” Front. Neurosci. 11, 121 (2017).
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H. Gong, S. Zeng, C. Yan, X. Lv, Z. Yang, T. Xu, Z. Feng, W. Ding, X. Qi, A. Li, J. Wu, and Q. Luo, “Continuously tracing brain-wide long-distance axonal projections in mice at a one-micron voxel resolution,” Neuroimage 74, 87–98 (2013).
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M. Perkovic, M. Kunz, U. Endesfelder, S. Bunse, C. Wigge, Z. Yu, V. V. Hodirnau, M. P. Scheffer, A. Seybert, S. Malkusch, E. M. Schuman, M. Heilemann, and A. S. Frangakis, “Correlative light- and electron microscopy with chemical tags,” J. Struct. Biol. 186(2), 205–213 (2014).
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W. J. Weninger, S. H. Geyer, T. J. Mohun, D. Rasskin-Gutman, T. Matsui, I. Ribeiro, L. F. Costa, J. C. Izpisúa-Belmonte, and G. B. Müller, “High-resolution episcopic microscopy: a rapid technique for high detailed 3D analysis of gene activity in the context of tissue architecture and morphology,” Anat. Embryol. (Berl.) 211(3), 213–221 (2006).
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K. Chung, J. Wallace, S. Y. Kim, S. Kalyanasundaram, A. S. Andalman, T. J. Davidson, J. J. Mirzabekov, K. A. Zalocusky, J. Mattis, A. K. Denisin, S. Pak, H. Bernstein, C. Ramakrishnan, L. Grosenick, V. Gradinaru, and K. Deisseroth, “Structural and molecular interrogation of intact biological systems,” Nature 497(7449), 332–337 (2013).
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E. Murray, J. H. Cho, D. Goodwin, T. Ku, J. Swaney, S. Y. Kim, H. Choi, Y. G. Park, J. Y. Park, A. Hubbert, M. McCue, S. Vassallo, N. Bakh, M. P. Frosch, V. J. Wedeen, H. S. Seung, and K. Chung, “Simple, scalable proteomic imaging for high-dimensional profiling of intact systems,” Cell 163(6), 1500–1514 (2015).
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F. Collman, J. Buchanan, K. D. Phend, K. D. Micheva, R. J. Weinberg, and S. J. Smith, “Mapping synapses by conjugate light-electron array tomography,” J. Neurosci. 35(14), 5792–5807 (2015).
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K. Chung, J. Wallace, S. Y. Kim, S. Kalyanasundaram, A. S. Andalman, T. J. Davidson, J. J. Mirzabekov, K. A. Zalocusky, J. Mattis, A. K. Denisin, S. Pak, H. Bernstein, C. Ramakrishnan, L. Grosenick, V. Gradinaru, and K. Deisseroth, “Structural and molecular interrogation of intact biological systems,” Nature 497(7449), 332–337 (2013).
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E. A. Susaki, K. Tainaka, D. Perrin, F. Kishino, T. Tawara, T. M. Watanabe, C. Yokoyama, H. Onoe, M. Eguchi, S. Yamaguchi, T. Abe, H. Kiyonari, Y. Shimizu, A. Miyawaki, H. Yokota, and H. R. Ueda, “Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis,” Cell 157(3), 726–739 (2014).
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W. J. Weninger, S. H. Geyer, T. J. Mohun, D. Rasskin-Gutman, T. Matsui, I. Ribeiro, L. F. Costa, J. C. Izpisúa-Belmonte, and G. B. Müller, “High-resolution episcopic microscopy: a rapid technique for high detailed 3D analysis of gene activity in the context of tissue architecture and morphology,” Anat. Embryol. (Berl.) 211(3), 213–221 (2006).
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T. Alanentalo, A. Asayesh, H. Morrison, C. E. Lorén, D. Holmberg, J. Sharpe, and U. Ahlgren, “Tomographic molecular imaging and 3D quantification within adult mouse organs,” Nat. Methods 4(1), 31–33 (2007).
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W. J. Weninger, S. H. Geyer, T. J. Mohun, D. Rasskin-Gutman, T. Matsui, I. Ribeiro, L. F. Costa, J. C. Izpisúa-Belmonte, and G. B. Müller, “High-resolution episcopic microscopy: a rapid technique for high detailed 3D analysis of gene activity in the context of tissue architecture and morphology,” Anat. Embryol. (Berl.) 211(3), 213–221 (2006).
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H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci. 14(11), 1481–1488 (2011).
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K. Chung, J. Wallace, S. Y. Kim, S. Kalyanasundaram, A. S. Andalman, T. J. Davidson, J. J. Mirzabekov, K. A. Zalocusky, J. Mattis, A. K. Denisin, S. Pak, H. Bernstein, C. Ramakrishnan, L. Grosenick, V. Gradinaru, and K. Deisseroth, “Structural and molecular interrogation of intact biological systems,” Nature 497(7449), 332–337 (2013).
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E. Murray, J. H. Cho, D. Goodwin, T. Ku, J. Swaney, S. Y. Kim, H. Choi, Y. G. Park, J. Y. Park, A. Hubbert, M. McCue, S. Vassallo, N. Bakh, M. P. Frosch, V. J. Wedeen, H. S. Seung, and K. Chung, “Simple, scalable proteomic imaging for high-dimensional profiling of intact systems,” Cell 163(6), 1500–1514 (2015).
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E. Murray, J. H. Cho, D. Goodwin, T. Ku, J. Swaney, S. Y. Kim, H. Choi, Y. G. Park, J. Y. Park, A. Hubbert, M. McCue, S. Vassallo, N. Bakh, M. P. Frosch, V. J. Wedeen, H. S. Seung, and K. Chung, “Simple, scalable proteomic imaging for high-dimensional profiling of intact systems,” Cell 163(6), 1500–1514 (2015).
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L. Silvestri, A. L. Allegra Mascaro, J. Lotti, L. Sacconi, and F. S. Pavone, “Advanced optical techniques to explore brain structure and function,” J. Innov. Opt. Health Sci. 6(1), 1230002 (2013).
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T. Zheng, Z. Yang, A. Li, X. Lv, Z. Zhou, X. Wang, X. Qi, S. Li, Q. Luo, H. Gong, and S. Zeng, “Visualization of brain circuits using two-photon fluorescence micro-optical sectioning tomography,” Opt. Express 21(8), 9839–9850 (2013).
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H. Gong, S. Zeng, C. Yan, X. Lv, Z. Yang, T. Xu, Z. Feng, W. Ding, X. Qi, A. Li, J. Wu, and Q. Luo, “Continuously tracing brain-wide long-distance axonal projections in mice at a one-micron voxel resolution,” Neuroimage 74, 87–98 (2013).
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W. J. Weninger, S. H. Geyer, T. J. Mohun, D. Rasskin-Gutman, T. Matsui, I. Ribeiro, L. F. Costa, J. C. Izpisúa-Belmonte, and G. B. Müller, “High-resolution episcopic microscopy: a rapid technique for high detailed 3D analysis of gene activity in the context of tissue architecture and morphology,” Anat. Embryol. (Berl.) 211(3), 213–221 (2006).
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N. Renier, Z. Wu, D. J. Simon, J. Yang, P. Ariel, and M. Tessier-Lavigne, “iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging,” Cell 159(4), 896–910 (2014).
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W. J. Weninger, S. H. Geyer, T. J. Mohun, D. Rasskin-Gutman, T. Matsui, I. Ribeiro, L. F. Costa, J. C. Izpisúa-Belmonte, and G. B. Müller, “High-resolution episcopic microscopy: a rapid technique for high detailed 3D analysis of gene activity in the context of tissue architecture and morphology,” Anat. Embryol. (Berl.) 211(3), 213–221 (2006).
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S. Wessel, S. Pagel, M. Ritter, H. Hohenberg, and R. Wepf, “Topographic Measurements of Real Structures in reflection Confocal Laser Scanning Microscope (CLSM),” Microsc. Microanal. 9(S03), 162–163 (2003).

Ross, A.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science 296(5567), 541–545 (2002).
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L. Silvestri, A. L. Allegra Mascaro, J. Lotti, L. Sacconi, and F. S. Pavone, “Advanced optical techniques to explore brain structure and function,” J. Innov. Opt. Health Sci. 6(1), 1230002 (2013).
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H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci. 14(11), 1481–1488 (2011).
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M. Perkovic, M. Kunz, U. Endesfelder, S. Bunse, C. Wigge, Z. Yu, V. V. Hodirnau, M. P. Scheffer, A. Seybert, S. Malkusch, E. M. Schuman, M. Heilemann, and A. S. Frangakis, “Correlative light- and electron microscopy with chemical tags,” J. Struct. Biol. 186(2), 205–213 (2014).
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B. A. Wilt, L. D. Burns, E. T. Wei Ho, K. K. Ghosh, E. A. Mukamel, and M. J. Schnitzer, “Advances in light microscopy for neuroscience,” Annu. Rev. Neurosci. 32(1), 435–506 (2009).
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M. Perkovic, M. Kunz, U. Endesfelder, S. Bunse, C. Wigge, Z. Yu, V. V. Hodirnau, M. P. Scheffer, A. Seybert, S. Malkusch, E. M. Schuman, M. Heilemann, and A. S. Frangakis, “Correlative light- and electron microscopy with chemical tags,” J. Struct. Biol. 186(2), 205–213 (2014).
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H. Gong, D. Xu, J. Yuan, X. Li, C. Guo, J. Peng, Y. Li, L. A. Schwarz, A. Li, B. Hu, B. Xiong, Q. Sun, Y. Zhang, J. Liu, Q. Zhong, T. Xu, S. Zeng, and Q. Luo, “High-throughput dual-colour precision imaging for brain-wide connectome with cytoarchitectonic landmarks at the cellular level,” Nat. Commun. 7, 12142 (2016).
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E. Murray, J. H. Cho, D. Goodwin, T. Ku, J. Swaney, S. Y. Kim, H. Choi, Y. G. Park, J. Y. Park, A. Hubbert, M. McCue, S. Vassallo, N. Bakh, M. P. Frosch, V. J. Wedeen, H. S. Seung, and K. Chung, “Simple, scalable proteomic imaging for high-dimensional profiling of intact systems,” Cell 163(6), 1500–1514 (2015).
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M. Perkovic, M. Kunz, U. Endesfelder, S. Bunse, C. Wigge, Z. Yu, V. V. Hodirnau, M. P. Scheffer, A. Seybert, S. Malkusch, E. M. Schuman, M. Heilemann, and A. S. Frangakis, “Correlative light- and electron microscopy with chemical tags,” J. Struct. Biol. 186(2), 205–213 (2014).
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Sharpe, J.

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H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci. 14(11), 1481–1488 (2011).
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L. Silvestri, A. L. Allegra Mascaro, J. Lotti, L. Sacconi, and F. S. Pavone, “Advanced optical techniques to explore brain structure and function,” J. Innov. Opt. Health Sci. 6(1), 1230002 (2013).
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Simon, D. J.

N. Renier, Z. Wu, D. J. Simon, J. Yang, P. Ariel, and M. Tessier-Lavigne, “iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging,” Cell 159(4), 896–910 (2014).
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F. Collman, J. Buchanan, K. D. Phend, K. D. Micheva, R. J. Weinberg, and S. J. Smith, “Mapping synapses by conjugate light-electron array tomography,” J. Neurosci. 35(14), 5792–5807 (2015).
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Y. Sun, H. Yu, D. Zheng, Q. Cao, Y. Wang, D. Harris, and Y. Wang, “Sudan black B reduces autofluorescence in murine renal tissue,” Arch. Pathol. Lab. Med. 135(10), 1335–1342 (2011).
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E. Murray, J. H. Cho, D. Goodwin, T. Ku, J. Swaney, S. Y. Kim, H. Choi, Y. G. Park, J. Y. Park, A. Hubbert, M. McCue, S. Vassallo, N. Bakh, M. P. Frosch, V. J. Wedeen, H. S. Seung, and K. Chung, “Simple, scalable proteomic imaging for high-dimensional profiling of intact systems,” Cell 163(6), 1500–1514 (2015).
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S. B. Newman, E. Borysko, and M. Swerdlow, “New sectioning techniques for light and electron microscopy,” Science 110(2846), 66–68 (1949).
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E. A. Susaki, K. Tainaka, D. Perrin, F. Kishino, T. Tawara, T. M. Watanabe, C. Yokoyama, H. Onoe, M. Eguchi, S. Yamaguchi, T. Abe, H. Kiyonari, Y. Shimizu, A. Miyawaki, H. Yokota, and H. R. Ueda, “Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis,” Cell 157(3), 726–739 (2014).
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E. A. Susaki, K. Tainaka, D. Perrin, F. Kishino, T. Tawara, T. M. Watanabe, C. Yokoyama, H. Onoe, M. Eguchi, S. Yamaguchi, T. Abe, H. Kiyonari, Y. Shimizu, A. Miyawaki, H. Yokota, and H. R. Ueda, “Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis,” Cell 157(3), 726–739 (2014).
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Tessier-Lavigne, M.

N. Renier, Z. Wu, D. J. Simon, J. Yang, P. Ariel, and M. Tessier-Lavigne, “iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging,” Cell 159(4), 896–910 (2014).
[Crossref] [PubMed]

Treweek, J. B.

B. Yang, J. B. Treweek, R. P. Kulkarni, B. E. Deverman, C. K. Chen, E. Lubeck, S. Shah, L. Cai, and V. Gradinaru, “Single-cell phenotyping within transparent intact tissue through whole-body clearing,” Cell 158(4), 945–958 (2014).
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E. A. Susaki, K. Tainaka, D. Perrin, F. Kishino, T. Tawara, T. M. Watanabe, C. Yokoyama, H. Onoe, M. Eguchi, S. Yamaguchi, T. Abe, H. Kiyonari, Y. Shimizu, A. Miyawaki, H. Yokota, and H. R. Ueda, “Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis,” Cell 157(3), 726–739 (2014).
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M. A. Karreman, A. V. Agronskaia, E. G. van Donselaar, K. Vocking, F. Fereidouni, B. M. Humbel, C. T. Verrips, A. J. Verkleij, and H. C. Gerritsen, “Optimizing immuno-labeling for correlative fluorescence and electron microscopy on a single specimen,” J. Struct. Biol. 180(2), 382–386 (2012).
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M. A. Karreman, A. V. Agronskaia, E. G. van Donselaar, K. Vocking, F. Fereidouni, B. M. Humbel, C. T. Verrips, A. J. Verkleij, and H. C. Gerritsen, “Optimizing immuno-labeling for correlative fluorescence and electron microscopy on a single specimen,” J. Struct. Biol. 180(2), 382–386 (2012).
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M. A. Karreman, A. V. Agronskaia, E. G. van Donselaar, K. Vocking, F. Fereidouni, B. M. Humbel, C. T. Verrips, A. J. Verkleij, and H. C. Gerritsen, “Optimizing immuno-labeling for correlative fluorescence and electron microscopy on a single specimen,” J. Struct. Biol. 180(2), 382–386 (2012).
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M. A. Karreman, A. V. Agronskaia, E. G. van Donselaar, K. Vocking, F. Fereidouni, B. M. Humbel, C. T. Verrips, A. J. Verkleij, and H. C. Gerritsen, “Optimizing immuno-labeling for correlative fluorescence and electron microscopy on a single specimen,” J. Struct. Biol. 180(2), 382–386 (2012).
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K. Chung, J. Wallace, S. Y. Kim, S. Kalyanasundaram, A. S. Andalman, T. J. Davidson, J. J. Mirzabekov, K. A. Zalocusky, J. Mattis, A. K. Denisin, S. Pak, H. Bernstein, C. Ramakrishnan, L. Grosenick, V. Gradinaru, and K. Deisseroth, “Structural and molecular interrogation of intact biological systems,” Nature 497(7449), 332–337 (2013).
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A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-optical sectioning tomography to obtain a high-resolution atlas of the mouse brain,” Science 330(6009), 1404–1408 (2010).
[Crossref] [PubMed]

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H. Xiong, Z. Zhou, M. Zhu, X. Lv, A. Li, S. Li, L. Li, T. Yang, S. Wang, Z. Yang, T. Xu, Q. Luo, H. Gong, and S. Zeng, “Chemical reactivation of quenched fluorescent protein molecules enables resin-embedded fluorescence microimaging,” Nat. Commun. 5, 3992 (2014).
[Crossref] [PubMed]

Wang, X.

Wang, Y.

Y. Sun, H. Yu, D. Zheng, Q. Cao, Y. Wang, D. Harris, and Y. Wang, “Sudan black B reduces autofluorescence in murine renal tissue,” Arch. Pathol. Lab. Med. 135(10), 1335–1342 (2011).
[Crossref] [PubMed]

Y. Sun, H. Yu, D. Zheng, Q. Cao, Y. Wang, D. Harris, and Y. Wang, “Sudan black B reduces autofluorescence in murine renal tissue,” Arch. Pathol. Lab. Med. 135(10), 1335–1342 (2011).
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E. A. Susaki, K. Tainaka, D. Perrin, F. Kishino, T. Tawara, T. M. Watanabe, C. Yokoyama, H. Onoe, M. Eguchi, S. Yamaguchi, T. Abe, H. Kiyonari, Y. Shimizu, A. Miyawaki, H. Yokota, and H. R. Ueda, “Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis,” Cell 157(3), 726–739 (2014).
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S. Wessel, S. Pagel, M. Ritter, H. Hohenberg, and R. Wepf, “Topographic Measurements of Real Structures in reflection Confocal Laser Scanning Microscope (CLSM),” Microsc. Microanal. 9(S03), 162–163 (2003).

Wigge, C.

M. Perkovic, M. Kunz, U. Endesfelder, S. Bunse, C. Wigge, Z. Yu, V. V. Hodirnau, M. P. Scheffer, A. Seybert, S. Malkusch, E. M. Schuman, M. Heilemann, and A. S. Frangakis, “Correlative light- and electron microscopy with chemical tags,” J. Struct. Biol. 186(2), 205–213 (2014).
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B. A. Wilt, L. D. Burns, E. T. Wei Ho, K. K. Ghosh, E. A. Mukamel, and M. J. Schnitzer, “Advances in light microscopy for neuroscience,” Annu. Rev. Neurosci. 32(1), 435–506 (2009).
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S. S. Biel, K. Kawaschinski, K. P. Wittern, U. Hintze, and R. Wepf, “From tissue to cellular ultrastructure: closing the gap between micro- and nanostructural imaging,” J. Microsc. 212(1), 91–99 (2003).
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J. Wu, Y. He, Z. Yang, C. Guo, Q. Luo, W. Zhou, S. Chen, A. Li, B. Xiong, T. Jiang, and H. Gong, “3D BrainCV: simultaneous visualization and analysis of cells and capillaries in a whole mouse brain with one-micron voxel resolution,” Neuroimage 87, 199–208 (2014).
[Crossref] [PubMed]

H. Gong, S. Zeng, C. Yan, X. Lv, Z. Yang, T. Xu, Z. Feng, W. Ding, X. Qi, A. Li, J. Wu, and Q. Luo, “Continuously tracing brain-wide long-distance axonal projections in mice at a one-micron voxel resolution,” Neuroimage 74, 87–98 (2013).
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B. Zhang, A. Li, Z. Yang, J. Wu, Q. Luo, and H. Gong, “Modified Golgi-Cox method for micrometer scale sectioning of the whole mouse brain,” J. Neurosci. Methods 197(1), 1–5 (2011).
[Crossref] [PubMed]

A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-optical sectioning tomography to obtain a high-resolution atlas of the mouse brain,” Science 330(6009), 1404–1408 (2010).
[Crossref] [PubMed]

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N. Renier, Z. Wu, D. J. Simon, J. Yang, P. Ariel, and M. Tessier-Lavigne, “iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging,” Cell 159(4), 896–910 (2014).
[Crossref] [PubMed]

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A. Burette, L. Khatri, M. Wyszynski, M. Sheng, E. B. Ziff, and R. J. Weinberg, “Differential cellular and subcellular localization of ampa receptor-binding protein and glutamate receptor-interacting protein,” J. Neurosci. 21(2), 495–503 (2001).
[PubMed]

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H. Gong, D. Xu, J. Yuan, X. Li, C. Guo, J. Peng, Y. Li, L. A. Schwarz, A. Li, B. Hu, B. Xiong, Q. Sun, Y. Zhang, J. Liu, Q. Zhong, T. Xu, S. Zeng, and Q. Luo, “High-throughput dual-colour precision imaging for brain-wide connectome with cytoarchitectonic landmarks at the cellular level,” Nat. Commun. 7, 12142 (2016).
[Crossref] [PubMed]

J. Wu, Y. He, Z. Yang, C. Guo, Q. Luo, W. Zhou, S. Chen, A. Li, B. Xiong, T. Jiang, and H. Gong, “3D BrainCV: simultaneous visualization and analysis of cells and capillaries in a whole mouse brain with one-micron voxel resolution,” Neuroimage 87, 199–208 (2014).
[Crossref] [PubMed]

Xiong, H.

Y. Gang, H. Zhou, Y. Jia, L. Liu, X. Liu, G. Rao, L. Li, X. Wang, X. Lv, H. Xiong, Z. Yang, Q. Luo, H. Gong, and S. Zeng, “Embedding and chemical reactivation of green fluorescent protein in the whole mouse brain for optical micro-imaging,” Front. Neurosci. 11, 121 (2017).
[Crossref] [PubMed]

H. Xiong, Z. Zhou, M. Zhu, X. Lv, A. Li, S. Li, L. Li, T. Yang, S. Wang, Z. Yang, T. Xu, Q. Luo, H. Gong, and S. Zeng, “Chemical reactivation of quenched fluorescent protein molecules enables resin-embedded fluorescence microimaging,” Nat. Commun. 5, 3992 (2014).
[Crossref] [PubMed]

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H. Gong, D. Xu, J. Yuan, X. Li, C. Guo, J. Peng, Y. Li, L. A. Schwarz, A. Li, B. Hu, B. Xiong, Q. Sun, Y. Zhang, J. Liu, Q. Zhong, T. Xu, S. Zeng, and Q. Luo, “High-throughput dual-colour precision imaging for brain-wide connectome with cytoarchitectonic landmarks at the cellular level,” Nat. Commun. 7, 12142 (2016).
[Crossref] [PubMed]

Xu, T.

H. Gong, D. Xu, J. Yuan, X. Li, C. Guo, J. Peng, Y. Li, L. A. Schwarz, A. Li, B. Hu, B. Xiong, Q. Sun, Y. Zhang, J. Liu, Q. Zhong, T. Xu, S. Zeng, and Q. Luo, “High-throughput dual-colour precision imaging for brain-wide connectome with cytoarchitectonic landmarks at the cellular level,” Nat. Commun. 7, 12142 (2016).
[Crossref] [PubMed]

H. Xiong, Z. Zhou, M. Zhu, X. Lv, A. Li, S. Li, L. Li, T. Yang, S. Wang, Z. Yang, T. Xu, Q. Luo, H. Gong, and S. Zeng, “Chemical reactivation of quenched fluorescent protein molecules enables resin-embedded fluorescence microimaging,” Nat. Commun. 5, 3992 (2014).
[Crossref] [PubMed]

H. Gong, S. Zeng, C. Yan, X. Lv, Z. Yang, T. Xu, Z. Feng, W. Ding, X. Qi, A. Li, J. Wu, and Q. Luo, “Continuously tracing brain-wide long-distance axonal projections in mice at a one-micron voxel resolution,” Neuroimage 74, 87–98 (2013).
[Crossref] [PubMed]

Yamaguchi, S.

E. A. Susaki, K. Tainaka, D. Perrin, F. Kishino, T. Tawara, T. M. Watanabe, C. Yokoyama, H. Onoe, M. Eguchi, S. Yamaguchi, T. Abe, H. Kiyonari, Y. Shimizu, A. Miyawaki, H. Yokota, and H. R. Ueda, “Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis,” Cell 157(3), 726–739 (2014).
[Crossref] [PubMed]

Yan, C.

H. Gong, S. Zeng, C. Yan, X. Lv, Z. Yang, T. Xu, Z. Feng, W. Ding, X. Qi, A. Li, J. Wu, and Q. Luo, “Continuously tracing brain-wide long-distance axonal projections in mice at a one-micron voxel resolution,” Neuroimage 74, 87–98 (2013).
[Crossref] [PubMed]

A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-optical sectioning tomography to obtain a high-resolution atlas of the mouse brain,” Science 330(6009), 1404–1408 (2010).
[Crossref] [PubMed]

Yang, B.

B. Yang, J. B. Treweek, R. P. Kulkarni, B. E. Deverman, C. K. Chen, E. Lubeck, S. Shah, L. Cai, and V. Gradinaru, “Single-cell phenotyping within transparent intact tissue through whole-body clearing,” Cell 158(4), 945–958 (2014).
[Crossref] [PubMed]

Yang, J.

N. Renier, Z. Wu, D. J. Simon, J. Yang, P. Ariel, and M. Tessier-Lavigne, “iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging,” Cell 159(4), 896–910 (2014).
[Crossref] [PubMed]

Yang, T.

T. Yang, T. Zheng, Z. Shang, X. Wang, X. Lv, J. Yuan, and S. Zeng, “Rapid imaging of large tissues using high-resolution stage-scanning microscopy,” Biomed. Opt. Express 6(5), 1867–1875 (2015).
[Crossref] [PubMed]

H. Xiong, Z. Zhou, M. Zhu, X. Lv, A. Li, S. Li, L. Li, T. Yang, S. Wang, Z. Yang, T. Xu, Q. Luo, H. Gong, and S. Zeng, “Chemical reactivation of quenched fluorescent protein molecules enables resin-embedded fluorescence microimaging,” Nat. Commun. 5, 3992 (2014).
[Crossref] [PubMed]

Yang, Z.

Y. Gang, H. Zhou, Y. Jia, L. Liu, X. Liu, G. Rao, L. Li, X. Wang, X. Lv, H. Xiong, Z. Yang, Q. Luo, H. Gong, and S. Zeng, “Embedding and chemical reactivation of green fluorescent protein in the whole mouse brain for optical micro-imaging,” Front. Neurosci. 11, 121 (2017).
[Crossref] [PubMed]

J. Wu, Y. He, Z. Yang, C. Guo, Q. Luo, W. Zhou, S. Chen, A. Li, B. Xiong, T. Jiang, and H. Gong, “3D BrainCV: simultaneous visualization and analysis of cells and capillaries in a whole mouse brain with one-micron voxel resolution,” Neuroimage 87, 199–208 (2014).
[Crossref] [PubMed]

H. Xiong, Z. Zhou, M. Zhu, X. Lv, A. Li, S. Li, L. Li, T. Yang, S. Wang, Z. Yang, T. Xu, Q. Luo, H. Gong, and S. Zeng, “Chemical reactivation of quenched fluorescent protein molecules enables resin-embedded fluorescence microimaging,” Nat. Commun. 5, 3992 (2014).
[Crossref] [PubMed]

T. Zheng, Z. Yang, A. Li, X. Lv, Z. Zhou, X. Wang, X. Qi, S. Li, Q. Luo, H. Gong, and S. Zeng, “Visualization of brain circuits using two-photon fluorescence micro-optical sectioning tomography,” Opt. Express 21(8), 9839–9850 (2013).
[Crossref] [PubMed]

Z. Yang, B. Hu, Y. Zhang, Q. Luo, and H. Gong, “Development of a plastic embedding method for large-volume and fluorescent-protein-expressing tissues,” PLoS One 8(4), e60877 (2013).
[Crossref] [PubMed]

T. Quan, T. Zheng, Z. Yang, W. Ding, S. Li, J. Li, H. Zhou, Q. Luo, H. Gong, and S. Zeng, “NeuroGPS: automated localization of neurons for brain circuits using L1 minimization model,” Sci. Rep. 3(1), 1414 (2013).
[Crossref] [PubMed]

H. Gong, S. Zeng, C. Yan, X. Lv, Z. Yang, T. Xu, Z. Feng, W. Ding, X. Qi, A. Li, J. Wu, and Q. Luo, “Continuously tracing brain-wide long-distance axonal projections in mice at a one-micron voxel resolution,” Neuroimage 74, 87–98 (2013).
[Crossref] [PubMed]

B. Zhang, A. Li, Z. Yang, J. Wu, Q. Luo, and H. Gong, “Modified Golgi-Cox method for micrometer scale sectioning of the whole mouse brain,” J. Neurosci. Methods 197(1), 1–5 (2011).
[Crossref] [PubMed]

Yokota, H.

E. A. Susaki, K. Tainaka, D. Perrin, F. Kishino, T. Tawara, T. M. Watanabe, C. Yokoyama, H. Onoe, M. Eguchi, S. Yamaguchi, T. Abe, H. Kiyonari, Y. Shimizu, A. Miyawaki, H. Yokota, and H. R. Ueda, “Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis,” Cell 157(3), 726–739 (2014).
[Crossref] [PubMed]

Yokoyama, C.

E. A. Susaki, K. Tainaka, D. Perrin, F. Kishino, T. Tawara, T. M. Watanabe, C. Yokoyama, H. Onoe, M. Eguchi, S. Yamaguchi, T. Abe, H. Kiyonari, Y. Shimizu, A. Miyawaki, H. Yokota, and H. R. Ueda, “Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis,” Cell 157(3), 726–739 (2014).
[Crossref] [PubMed]

Yu, H.

Y. Sun, H. Yu, D. Zheng, Q. Cao, Y. Wang, D. Harris, and Y. Wang, “Sudan black B reduces autofluorescence in murine renal tissue,” Arch. Pathol. Lab. Med. 135(10), 1335–1342 (2011).
[Crossref] [PubMed]

Yu, Z.

M. Perkovic, M. Kunz, U. Endesfelder, S. Bunse, C. Wigge, Z. Yu, V. V. Hodirnau, M. P. Scheffer, A. Seybert, S. Malkusch, E. M. Schuman, M. Heilemann, and A. S. Frangakis, “Correlative light- and electron microscopy with chemical tags,” J. Struct. Biol. 186(2), 205–213 (2014).
[Crossref] [PubMed]

Yuan, J.

H. Gong, D. Xu, J. Yuan, X. Li, C. Guo, J. Peng, Y. Li, L. A. Schwarz, A. Li, B. Hu, B. Xiong, Q. Sun, Y. Zhang, J. Liu, Q. Zhong, T. Xu, S. Zeng, and Q. Luo, “High-throughput dual-colour precision imaging for brain-wide connectome with cytoarchitectonic landmarks at the cellular level,” Nat. Commun. 7, 12142 (2016).
[Crossref] [PubMed]

T. Yang, T. Zheng, Z. Shang, X. Wang, X. Lv, J. Yuan, and S. Zeng, “Rapid imaging of large tissues using high-resolution stage-scanning microscopy,” Biomed. Opt. Express 6(5), 1867–1875 (2015).
[Crossref] [PubMed]

Zalocusky, K. A.

K. Chung, J. Wallace, S. Y. Kim, S. Kalyanasundaram, A. S. Andalman, T. J. Davidson, J. J. Mirzabekov, K. A. Zalocusky, J. Mattis, A. K. Denisin, S. Pak, H. Bernstein, C. Ramakrishnan, L. Grosenick, V. Gradinaru, and K. Deisseroth, “Structural and molecular interrogation of intact biological systems,” Nature 497(7449), 332–337 (2013).
[Crossref] [PubMed]

Zeng, S.

Y. Gang, H. Zhou, Y. Jia, L. Liu, X. Liu, G. Rao, L. Li, X. Wang, X. Lv, H. Xiong, Z. Yang, Q. Luo, H. Gong, and S. Zeng, “Embedding and chemical reactivation of green fluorescent protein in the whole mouse brain for optical micro-imaging,” Front. Neurosci. 11, 121 (2017).
[Crossref] [PubMed]

S. Li, H. Zhou, T. Quan, J. Li, Y. Li, A. Li, Q. Luo, H. Gong, and S. Zeng, “SparseTracer: the reconstruction of discontinuous neuronal morphology in noisy images,” Neuroinformatics 15(2), 133–149 (2017).
[Crossref] [PubMed]

H. Gong, D. Xu, J. Yuan, X. Li, C. Guo, J. Peng, Y. Li, L. A. Schwarz, A. Li, B. Hu, B. Xiong, Q. Sun, Y. Zhang, J. Liu, Q. Zhong, T. Xu, S. Zeng, and Q. Luo, “High-throughput dual-colour precision imaging for brain-wide connectome with cytoarchitectonic landmarks at the cellular level,” Nat. Commun. 7, 12142 (2016).
[Crossref] [PubMed]

T. Quan, H. Zhou, J. Li, S. Li, A. Li, Y. Li, X. Lv, Q. Luo, H. Gong, and S. Zeng, “NeuroGPS-Tree: automatic reconstruction of large-scale neuronal populations with dense neurites,” Nat. Methods 13(1), 51–54 (2016).
[PubMed]

J. Li, T. Quan, S. Li, H. Zhou, Q. Luo, H. Gong, and S. Zeng, “Reconstruction of micron resolution mouse brain surface from large-scale imaging dataset using resampling-based variational model,” Sci. Rep. 5(1), 12782 (2015).
[Crossref] [PubMed]

T. Yang, T. Zheng, Z. Shang, X. Wang, X. Lv, J. Yuan, and S. Zeng, “Rapid imaging of large tissues using high-resolution stage-scanning microscopy,” Biomed. Opt. Express 6(5), 1867–1875 (2015).
[Crossref] [PubMed]

H. Xiong, Z. Zhou, M. Zhu, X. Lv, A. Li, S. Li, L. Li, T. Yang, S. Wang, Z. Yang, T. Xu, Q. Luo, H. Gong, and S. Zeng, “Chemical reactivation of quenched fluorescent protein molecules enables resin-embedded fluorescence microimaging,” Nat. Commun. 5, 3992 (2014).
[Crossref] [PubMed]

T. Zheng, Z. Yang, A. Li, X. Lv, Z. Zhou, X. Wang, X. Qi, S. Li, Q. Luo, H. Gong, and S. Zeng, “Visualization of brain circuits using two-photon fluorescence micro-optical sectioning tomography,” Opt. Express 21(8), 9839–9850 (2013).
[Crossref] [PubMed]

T. Quan, T. Zheng, Z. Yang, W. Ding, S. Li, J. Li, H. Zhou, Q. Luo, H. Gong, and S. Zeng, “NeuroGPS: automated localization of neurons for brain circuits using L1 minimization model,” Sci. Rep. 3(1), 1414 (2013).
[Crossref] [PubMed]

H. Gong, S. Zeng, C. Yan, X. Lv, Z. Yang, T. Xu, Z. Feng, W. Ding, X. Qi, A. Li, J. Wu, and Q. Luo, “Continuously tracing brain-wide long-distance axonal projections in mice at a one-micron voxel resolution,” Neuroimage 74, 87–98 (2013).
[Crossref] [PubMed]

A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-optical sectioning tomography to obtain a high-resolution atlas of the mouse brain,” Science 330(6009), 1404–1408 (2010).
[Crossref] [PubMed]

Zhang, B.

B. Zhang, A. Li, Z. Yang, J. Wu, Q. Luo, and H. Gong, “Modified Golgi-Cox method for micrometer scale sectioning of the whole mouse brain,” J. Neurosci. Methods 197(1), 1–5 (2011).
[Crossref] [PubMed]

A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-optical sectioning tomography to obtain a high-resolution atlas of the mouse brain,” Science 330(6009), 1404–1408 (2010).
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Figures (8)

Fig. 1
Fig. 1

Immunofluorescence-labeled brain slices before and after resin embedding. (a) Images of labeled brain slices before and after GMA, Lowicryl HM20 or LR White resin embedding, respectively. All slices were immunolabeled by primary antibody (anti-TH), and were labeled with the various secondary antibodies conjugated with four fluorescent dyes: CF488, CF568, CY3, or CY5, respectively. All images were taken at a 0.42 × 0.42 × 1 μm3 voxel size on an LSM780 confocal microscope (ZEISS). (b) Fluorescent intensity change of immunostained brain slices after being embedding with different resins. We calculated the fluorescent intensity changes from labeled neuronal somas. The fluorescent intensities were compared before and after resin embedding using ImageJ software. The values in the bar graph are given as the means ± SD (n = 25 neurons from three slices for each independent sample). (c) Small shifts occurred in the absorption spectra of the dyes (CF488, CF568, CY3, and CY5) in Lowicryl HM20 resin polymer, compared to those in PBS buffer. Scale bar in (a): 50 μm.

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Fig. 2
Fig. 2

Preservation of immunofluorescence labeled fine details of neurite in resin-embedded brain tissue. (a) Fluorescence image of neurons labeled by PRV-GFP virus; slices were imaged after immunofluorescent labeling (b), and after resin embedding (c). (d) Fluorescent intensities of pixels crossed by red, purple, and green lines (shown in a, b, c, respectively) are plotted in the corresponding colors. (e) Morphology of neurons labeled by RV-DsRed virus before immunostaining, after immunofluorescent labeling (f), and after resin embedding (g). (h) Fluorescent intensities of pixels crossed by the red, purple, and green dashed lines (shown in e, f, and g, respectively) are plotted in the corresponding color. Images in panels (a-c) were recorded at a 0.42 × 0.42 × 1.00 μm3 voxel size using a confocal microscope (LSM780, ZEISS) with a 20 × 1.0 NA water objective. Images in panels (e-g) were recorded at a 0.21 × 0.21 × 1.00 μm3 voxel size using a confocal microscope (LSM780, ZEISS) with a 40 × 1.0 NA oil objective. All the images represent maximum intensity z-projections of 20-μm-thickness. Scale bar: (a-g) 50 μm.

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Fig. 3
Fig. 3

Resin embedding is compatible with various antibodies and fluorescent tracers staining in brain tissue. (a-i) Images of immune- and fluorescent tracer-labeled neurons in mouse brain tissue after Lowicryl HM20 resin embedding. (a) Immunolabeling of TdTomato-labeled mouse cortex from ChAT-cre; Rosa26lsl-tdTomato transgenic mice. (b) TH-immunolabeled thalamic neurons in C57 mouse brain tissue. (c) Immunolabeling of GFP-expressing hippocampal neurons from a Thy1-GFP-M transgenic mouse. (d-h) Mouse brain slices were immunolabeled by FoxP2 (d), cFos (e), parvalbumin (f), cholera toxin beta (g), and PSD-95 (h), respectively. Images in panel a-h were acquired on an LSM780 confocal microscope (ZEISS). (i) 3D volume image of immnofluorescent signals (Alexa 488) labeled by parvalbumin in mouse cortex, images were acquired by a two-photon microscope (LSM780). Scale bar: (a-g) 50 μm; (h) 10 μm.

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Fig. 4
Fig. 4

Fluorescent images of Lectin-DyLight 594 labeled vasculature in the brain tissue after Lowicryl HM20 resin embedding. (a) Maximum intensity projections of a 20-μm-thick coronal slice. (b-d) Corresponding magnification of regions indicated in (a). (e-g) High magnification images of the boxed regions in (b-d), respectively. All images were acquired using 20 × (NA = 1.0), at a 0.42 × 0.42 × 1.00 μm3 voxel size on a confocal microscope (LSM780, ZEISS). Scale bars: (a) 1 mm; (b-d) 100 μm; (e-g) 30 μm.

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Fig. 5
Fig. 5

Imaging large volume immunolabeled mouse brain tissue after Lowicryl HM20 resin embedding. (a) 3D presentation of the TH immunolabeled mouse brain block. Enlargements of the fine structures of TH-positive axonal fibers in the cortex (b) and TH-positive soma located in the thalamus (c). Images were acquired by successive high-resolution stage-scanning microscopy at a 0.16 × 0.16 × 1.00 μm3 voxel size. (a) 6200 × 5000 × 1200 μm3; (b) 480 × 480 × 380 μm3; (c) 480 × 480 × 510 μm3.

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Fig. 6
Fig. 6

Effects of SBB on background fluorescence in the resin embedded brain tissue. Images obtained from immunostained brain tissue that were embedded in resin (HM20, GMA and LR white) with (g-l) and without 0.2% SBB (control, a-f), respectively. Mouse brain tissue was immunostained with anti-tyrosine hydroxylase primary antibody and CF488 or CY3-conjugated secondary antibodies. All images were recorded at 0.17 × 0.17 μm/pixel on the same wide field microscope (Nikon Ni-E) at room temperature. Scale bar: (a-l): 50 μm.

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Fig. 7
Fig. 7

Schematic diagram for three-dimensional fluorescent imaging. The resin-embedded biological sample was mounted on a precision motion stage that moves between the stage-scanning microscopy and the microtome. Strip imaging methods combined with line illumination were applied for rapid surface imaging. After the surface layer of specimen was imaged, the recorded layer (1-μm thick) was removed by a fixed diamond knife. The sectioning-imaging cycles was repeated for collecting three-dimensional imaging data sets.

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Fig. 8
Fig. 8

Comparison of signal and background fluorescence of the images obtained using successive high-resolution stage-scanning block-face imaging. (a) Maximal intensity projections of the 100-mm thickness z-stacks images without preprocessing. Image stacks were selected from the same data set in Fig. 5. The mean signal intensity was measured from the red dashed circle area. The mean value of the background was measured from a blue dashed line drawn across the background area close to soma. The fluorescent signal intensity was calculated by subtracting the mean value of background from the mean value of the soma. (b) The normalized fluorescent intensities of signal value were compared with background values. 36 somas were measured from different images of the same data set. This result shows that the signal-to-background ratio is 15.1 ± 5.5. (c) Fluorescent intensities of pixels crossed by the blue, green and red lines were plotted in curves with the corresponding color in (a). The signal-to-background ratio values are given as the means ± SD.

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Tables (4)

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Table 1 Primary antibodies tested on mouse brain tissue.

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Table 2 Secondary antibodies tested on mouse brain tissue.

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Table 3 Fluorescent tracers and dyes tested on mouse brain tissue.

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Table 4 The cutting performance of the polymerized tissue block.

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