Abstract

Inverted selective plane illumination microscopy (iSPIM) enables fast, large field-of-view, long term imaging with compatibility with conventional sample mounting. However, the imaging quality can be deteriorated in thick tissues due to sample scattering. Three strategies have been adopted in this paper to optimize the imaging performance of iSPIM on thick tissue imaging: electronic confocal slit detection (eCSD), structured illumination (SI) and the two combined. We compared the image contrast when using SPIM, confocal SPIM (using eCSD alone), SI SPIM (using SI alone) or confocal-SI SPIM (combining both methods) on images of gelatin phantom and highly-scattering fluorescently-stained human tissue. We demonstrate that all the three methods showed remarkable contrast enhancement on both samples compared to iSPIM alone, and SI SPIM and the combined confocal-SI mode outperformed confocal SPIM in contrast enhancement. Moreover, the use of SI at high pattern frequencies outperformed confocal SPIM in terms of optical sectioning capability. However, image signal-to-noise ratio (SNR) was decreased at high pattern frequencies when imaging scattering samples with SI SPIM. By combining eCSD with SI to reduce background signal and noise, the superior optical sectioning performance of SI could be achieved while also maintaining high image SNR.

© 2017 Optical Society of America

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References

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J. Andilla, R. Jorand, O. E. Olarte, A. C. Dufour, M. Cazales, Y. L. E. Montagner, R. Ceolato, N. Riviere, J.-C. Olivo-Marin, P. Loza-Alvarez, and C. Lorenzo, “Imaging tissue-mimic with light sheet microscopy: A comparative guideline,” Sci. Rep. 7, 44939 (2017).
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M. Fantham and C. F. Kaminski, “A new online tool for visualization of volumetric data,” Nat. Publ. Gr. 11, 69 (2017).

2016 (9)

T. Meinert, O. Tietz, K. J. Palme, and A. Rohrbach, “Separation of ballistic and diffusive fluorescence photons in confocal Light-Sheet Microscopy of Arabidopsis roots,” Sci. Rep. 6, 30378 (2016).
[PubMed]

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[PubMed]

M. E. van Royen, E. I. Verhoef, C. F. Kweldam, W. A. van Cappellen, G.-J. Kremers, A. B. Houtsmuller, and G. J. L. H. van Leenders, “Three-dimensional microscopic analysis of clinical prostate specimens,” Histopathology 69(6), 985–992 (2016).
[PubMed]

A. Kumar, R. Christensen, M. Guo, P. Chandris, W. Duncan, Y. Wu, A. Santella, M. Moyle, P. W. Winter, D. Colón-Ramos, Z. Bao, and H. Shroff, “Using stage- and slit-scanning to improve contrast and optical sectioning in dual-view,” Biol. Bull. 231(1), 26–39 (2016).
[PubMed]

L. Silvestri, I. Costantini, L. Sacconi, and F. S. Pavone, “Clearing of fixed tissue: a review from a microscopist’s perspective,” J. Biomed. Opt. 21(8), 081205 (2016).
[PubMed]

Z. Lavagnino, G. Sancataldo, M. d’Amora, P. Follert, D. De Pietri Tonelli, A. Diaspro, and F. Cella Zanacchi, “4D (x-y-z-t) imaging of thick biological samples by means of Two-Photon inverted Selective Plane Illumination Microscopy (2PE-iSPIM),” Sci. Rep. 6, 23923 (2016).
[PubMed]

M. Wang, D. B. Tulman, A. B. Sholl, H. Z. Kimbrell, S. H. Mandava, K. N. Elfer, S. Luethy, M. M. Maddox, W. Lai, B. R. Lee, and J. Q. Brown, “Gigapixel surface imaging of radical prostatectomy specimens for comprehensive detection of cancer-positive surgical margins using structured illumination microscopy,” Sci. Rep. 6, 27419 (2016).
[PubMed]

E. Olson, M. J. Levene, and R. Torres, “Multiphoton microscopy with clearing for three dimensional histology of kidney biopsies,” Biomed. Opt. Express 7(8), 3089–3096 (2016).

Y. Wu, P. Chandris, P. W. Winter, E. Y. Kim, V. Jaumouillé, A. Kumar, M. Guo, J. M. Leung, C. Smith, I. Rey-Suarez, H. Liu, C. M. Waterman, K. S. Ramamurthi, P. J. La Riviere, and H. Shroff, “Simultaneous multiview capture and fusion improves spatial resolution in wide-field and light-sheet microscopy,” Optica 3(8), 897–910 (2016).
[PubMed]

2015 (4)

E. H. K. Stelzer, “Light-sheet fluorescence microscopy for quantitative biology,” Nat. Methods 12(1), 23–26 (2015).
[PubMed]

P. J. Keller, M. B. Ahrens, and J. Freeman, “Light-sheet imaging for systems neuroscience,” Nat. Methods 12(1), 27–29 (2015).
[PubMed]

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[PubMed]

G. de Medeiros, N. Norlin, S. Gunther, M. Albert, L. Panavaite, U.-M. Fiuza, F. Peri, T. Hiiragi, U. Krzic, and L. Hufnagel, “Confocal multiview light-sheet microscopy,” Nat. Commun. 6, 8881 (2015).
[PubMed]

2014 (3)

L. Gao, L. Shao, B.-C. Chen, and E. Betzig, “3D live fluorescence imaging of cellular dynamics using Bessel beam plane illumination microscopy,” Nat. Protoc. 9(5), 1083–1101 (2014).
[PubMed]

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nat. Protoc. 9(11), 2555–2573 (2014).
[PubMed]

P. W. Winter and H. Shroff, “Faster fluorescence microscopy: Advances in high speed biological imaging,” Curr. Opin. Chem. Biol. 20, 46–53 (2014).
[PubMed]

2013 (2)

Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
[PubMed]

H. L. Fu, J. L. Mueller, M. P. Javid, J. K. Mito, D. G. Kirsch, N. Ramanujam, and J. Q. Brown, “Optimization of a Widefield Structured Illumination Microscope for Non-Destructive Assessment and Quantification of Nuclear Features in Tumor Margins of a Primary Mouse Model of Sarcoma,” PLoS One 8(7), e68868 (2013).
[PubMed]

2012 (6)

2011 (5)

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[PubMed]

P. A. Santi, “Light Sheet Fluorescence Microscopy: A Review,” J. Histochem. Cytochem. 59(2), 129–138 (2011).
[PubMed]

R. S. Fischer, Y. Wu, P. Kanchanawong, H. Shroff, and C. M. Waterman, “Microscopy in 3D: A biologist’s toolbox,” Trends Cell Biol. 21(12), 682–691 (2011).
[PubMed]

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[PubMed]

J. Mertz, “Optical sectioning microscopy with planar or structured illumination,” Nat. Methods 8(10), 811–819 (2011).
[PubMed]

2010 (1)

P. J. Keller, A. D. Schmidt, A. Santella, K. Khairy, Z. Bao, J. Wittbrodt, and E. H. K. Stelzer, “Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy,” Nat. Methods 7(8), 637–642 (2010).
[PubMed]

2008 (1)

2007 (2)

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[PubMed]

T. Breuninger, K. Greger, and E. H. K. Stelzer, “Lateral modulation boosts image quality in single plane illumination fluorescence microscopy,” Opt. Lett. 32(13), 1938–1940 (2007).
[PubMed]

2004 (1)

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[PubMed]

1997 (1)

1969 (1)

Ahrens, M. B.

P. J. Keller, M. B. Ahrens, and J. Freeman, “Light-sheet imaging for systems neuroscience,” Nat. Methods 12(1), 27–29 (2015).
[PubMed]

Albert, M.

G. de Medeiros, N. Norlin, S. Gunther, M. Albert, L. Panavaite, U.-M. Fiuza, F. Peri, T. Hiiragi, U. Krzic, and L. Hufnagel, “Confocal multiview light-sheet microscopy,” Nat. Commun. 6, 8881 (2015).
[PubMed]

Andilla, J.

J. Andilla, R. Jorand, O. E. Olarte, A. C. Dufour, M. Cazales, Y. L. E. Montagner, R. Ceolato, N. Riviere, J.-C. Olivo-Marin, P. Loza-Alvarez, and C. Lorenzo, “Imaging tissue-mimic with light sheet microscopy: A comparative guideline,” Sci. Rep. 7, 44939 (2017).
[PubMed]

Bao, Z.

A. Kumar, R. Christensen, M. Guo, P. Chandris, W. Duncan, Y. Wu, A. Santella, M. Moyle, P. W. Winter, D. Colón-Ramos, Z. Bao, and H. Shroff, “Using stage- and slit-scanning to improve contrast and optical sectioning in dual-view,” Biol. Bull. 231(1), 26–39 (2016).
[PubMed]

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nat. Protoc. 9(11), 2555–2573 (2014).
[PubMed]

Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
[PubMed]

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[PubMed]

P. J. Keller, A. D. Schmidt, A. Santella, K. Khairy, Z. Bao, J. Wittbrodt, and E. H. K. Stelzer, “Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy,” Nat. Methods 7(8), 637–642 (2010).
[PubMed]

Barbastathis, G.

Baumgart, E.

Becker, K.

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[PubMed]

Betzig, E.

L. Gao, L. Shao, B.-C. Chen, and E. Betzig, “3D live fluorescence imaging of cellular dynamics using Bessel beam plane illumination microscopy,” Nat. Protoc. 9(5), 1083–1101 (2014).
[PubMed]

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[PubMed]

Bhattacharya, D.

Bokinsky, A.

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nat. Protoc. 9(11), 2555–2573 (2014).
[PubMed]

Bouchard, M. B.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[PubMed]

Breuninger, T.

Bria, A.

Brown, J. Q.

K. N. Elfer, A. B. Sholl, M. Wang, D. B. Tulman, S. H. Mandava, B. R. Lee, and J. Q. Brown, “DRAQ5 and eosin (‘D&E’) as an analog to hematoxylin and eosin for rapid fluorescence histology of fresh tissues,” PLoS One 11(10), e0165530 (2016).
[PubMed]

M. Wang, D. B. Tulman, A. B. Sholl, H. Z. Kimbrell, S. H. Mandava, K. N. Elfer, S. Luethy, M. M. Maddox, W. Lai, B. R. Lee, and J. Q. Brown, “Gigapixel surface imaging of radical prostatectomy specimens for comprehensive detection of cancer-positive surgical margins using structured illumination microscopy,” Sci. Rep. 6, 27419 (2016).
[PubMed]

H. L. Fu, J. L. Mueller, M. P. Javid, J. K. Mito, D. G. Kirsch, N. Ramanujam, and J. Q. Brown, “Optimization of a Widefield Structured Illumination Microscope for Non-Destructive Assessment and Quantification of Nuclear Features in Tumor Margins of a Primary Mouse Model of Sarcoma,” PLoS One 8(7), e68868 (2013).
[PubMed]

Bruno, R. M.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[PubMed]

Cazales, M.

J. Andilla, R. Jorand, O. E. Olarte, A. C. Dufour, M. Cazales, Y. L. E. Montagner, R. Ceolato, N. Riviere, J.-C. Olivo-Marin, P. Loza-Alvarez, and C. Lorenzo, “Imaging tissue-mimic with light sheet microscopy: A comparative guideline,” Sci. Rep. 7, 44939 (2017).
[PubMed]

Cella Zanacchi, F.

Z. Lavagnino, G. Sancataldo, M. d’Amora, P. Follert, D. De Pietri Tonelli, A. Diaspro, and F. Cella Zanacchi, “4D (x-y-z-t) imaging of thick biological samples by means of Two-Photon inverted Selective Plane Illumination Microscopy (2PE-iSPIM),” Sci. Rep. 6, 23923 (2016).
[PubMed]

Ceolato, R.

J. Andilla, R. Jorand, O. E. Olarte, A. C. Dufour, M. Cazales, Y. L. E. Montagner, R. Ceolato, N. Riviere, J.-C. Olivo-Marin, P. Loza-Alvarez, and C. Lorenzo, “Imaging tissue-mimic with light sheet microscopy: A comparative guideline,” Sci. Rep. 7, 44939 (2017).
[PubMed]

Chandris, P.

A. Kumar, R. Christensen, M. Guo, P. Chandris, W. Duncan, Y. Wu, A. Santella, M. Moyle, P. W. Winter, D. Colón-Ramos, Z. Bao, and H. Shroff, “Using stage- and slit-scanning to improve contrast and optical sectioning in dual-view,” Biol. Bull. 231(1), 26–39 (2016).
[PubMed]

Y. Wu, P. Chandris, P. W. Winter, E. Y. Kim, V. Jaumouillé, A. Kumar, M. Guo, J. M. Leung, C. Smith, I. Rey-Suarez, H. Liu, C. M. Waterman, K. S. Ramamurthi, P. J. La Riviere, and H. Shroff, “Simultaneous multiview capture and fusion improves spatial resolution in wide-field and light-sheet microscopy,” Optica 3(8), 897–910 (2016).
[PubMed]

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nat. Protoc. 9(11), 2555–2573 (2014).
[PubMed]

Chen, B.-C.

L. Gao, L. Shao, B.-C. Chen, and E. Betzig, “3D live fluorescence imaging of cellular dynamics using Bessel beam plane illumination microscopy,” Nat. Protoc. 9(5), 1083–1101 (2014).
[PubMed]

Christensen, R.

A. Kumar, R. Christensen, M. Guo, P. Chandris, W. Duncan, Y. Wu, A. Santella, M. Moyle, P. W. Winter, D. Colón-Ramos, Z. Bao, and H. Shroff, “Using stage- and slit-scanning to improve contrast and optical sectioning in dual-view,” Biol. Bull. 231(1), 26–39 (2016).
[PubMed]

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nat. Protoc. 9(11), 2555–2573 (2014).
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Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
[PubMed]

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[PubMed]

Colón-Ramos, D.

A. Kumar, R. Christensen, M. Guo, P. Chandris, W. Duncan, Y. Wu, A. Santella, M. Moyle, P. W. Winter, D. Colón-Ramos, Z. Bao, and H. Shroff, “Using stage- and slit-scanning to improve contrast and optical sectioning in dual-view,” Biol. Bull. 231(1), 26–39 (2016).
[PubMed]

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[PubMed]

Colón-Ramos, D. A.

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nat. Protoc. 9(11), 2555–2573 (2014).
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Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
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L. Silvestri, I. Costantini, L. Sacconi, and F. S. Pavone, “Clearing of fixed tissue: a review from a microscopist’s perspective,” J. Biomed. Opt. 21(8), 081205 (2016).
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Z. Lavagnino, G. Sancataldo, M. d’Amora, P. Follert, D. De Pietri Tonelli, A. Diaspro, and F. Cella Zanacchi, “4D (x-y-z-t) imaging of thick biological samples by means of Two-Photon inverted Selective Plane Illumination Microscopy (2PE-iSPIM),” Sci. Rep. 6, 23923 (2016).
[PubMed]

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T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[PubMed]

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G. de Medeiros, N. Norlin, S. Gunther, M. Albert, L. Panavaite, U.-M. Fiuza, F. Peri, T. Hiiragi, U. Krzic, and L. Hufnagel, “Confocal multiview light-sheet microscopy,” Nat. Commun. 6, 8881 (2015).
[PubMed]

De Pietri Tonelli, D.

Z. Lavagnino, G. Sancataldo, M. d’Amora, P. Follert, D. De Pietri Tonelli, A. Diaspro, and F. Cella Zanacchi, “4D (x-y-z-t) imaging of thick biological samples by means of Two-Photon inverted Selective Plane Illumination Microscopy (2PE-iSPIM),” Sci. Rep. 6, 23923 (2016).
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H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[PubMed]

Del Bene, F.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[PubMed]

Deussing, J. M.

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[PubMed]

Diaspro, A.

Z. Lavagnino, G. Sancataldo, M. d’Amora, P. Follert, D. De Pietri Tonelli, A. Diaspro, and F. Cella Zanacchi, “4D (x-y-z-t) imaging of thick biological samples by means of Two-Photon inverted Selective Plane Illumination Microscopy (2PE-iSPIM),” Sci. Rep. 6, 23923 (2016).
[PubMed]

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H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[PubMed]

Du, Z.

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[PubMed]

Dufour, A. C.

J. Andilla, R. Jorand, O. E. Olarte, A. C. Dufour, M. Cazales, Y. L. E. Montagner, R. Ceolato, N. Riviere, J.-C. Olivo-Marin, P. Loza-Alvarez, and C. Lorenzo, “Imaging tissue-mimic with light sheet microscopy: A comparative guideline,” Sci. Rep. 7, 44939 (2017).
[PubMed]

Duncan, W.

A. Kumar, R. Christensen, M. Guo, P. Chandris, W. Duncan, Y. Wu, A. Santella, M. Moyle, P. W. Winter, D. Colón-Ramos, Z. Bao, and H. Shroff, “Using stage- and slit-scanning to improve contrast and optical sectioning in dual-view,” Biol. Bull. 231(1), 26–39 (2016).
[PubMed]

Dunsby, C.

Eder, M.

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[PubMed]

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M. Wang, D. B. Tulman, A. B. Sholl, H. Z. Kimbrell, S. H. Mandava, K. N. Elfer, S. Luethy, M. M. Maddox, W. Lai, B. R. Lee, and J. Q. Brown, “Gigapixel surface imaging of radical prostatectomy specimens for comprehensive detection of cancer-positive surgical margins using structured illumination microscopy,” Sci. Rep. 6, 27419 (2016).
[PubMed]

K. N. Elfer, A. B. Sholl, M. Wang, D. B. Tulman, S. H. Mandava, B. R. Lee, and J. Q. Brown, “DRAQ5 and eosin (‘D&E’) as an analog to hematoxylin and eosin for rapid fluorescence histology of fresh tissues,” PLoS One 11(10), e0165530 (2016).
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F. O. Fahrbach and A. Rohrbach, “Propagation stability of self-reconstructing Bessel beams enables contrast-enhanced imaging in thick media,” Nat. Commun. 3, 632 (2012).
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Fantham, M.

M. Fantham and C. F. Kaminski, “A new online tool for visualization of volumetric data,” Nat. Publ. Gr. 11, 69 (2017).

Fischer, R. S.

Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
[PubMed]

R. S. Fischer, Y. Wu, P. Kanchanawong, H. Shroff, and C. M. Waterman, “Microscopy in 3D: A biologist’s toolbox,” Trends Cell Biol. 21(12), 682–691 (2011).
[PubMed]

Fiuza, U.-M.

G. de Medeiros, N. Norlin, S. Gunther, M. Albert, L. Panavaite, U.-M. Fiuza, F. Peri, T. Hiiragi, U. Krzic, and L. Hufnagel, “Confocal multiview light-sheet microscopy,” Nat. Commun. 6, 8881 (2015).
[PubMed]

Follert, P.

Z. Lavagnino, G. Sancataldo, M. d’Amora, P. Follert, D. De Pietri Tonelli, A. Diaspro, and F. Cella Zanacchi, “4D (x-y-z-t) imaging of thick biological samples by means of Two-Photon inverted Selective Plane Illumination Microscopy (2PE-iSPIM),” Sci. Rep. 6, 23923 (2016).
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Freeman, J.

P. J. Keller, M. B. Ahrens, and J. Freeman, “Light-sheet imaging for systems neuroscience,” Nat. Methods 12(1), 27–29 (2015).
[PubMed]

Fu, H. L.

H. L. Fu, J. L. Mueller, M. P. Javid, J. K. Mito, D. G. Kirsch, N. Ramanujam, and J. Q. Brown, “Optimization of a Widefield Structured Illumination Microscope for Non-Destructive Assessment and Quantification of Nuclear Features in Tumor Margins of a Primary Mouse Model of Sarcoma,” PLoS One 8(7), e68868 (2013).
[PubMed]

Galbraith, C. G.

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[PubMed]

Galbraith, J. A.

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[PubMed]

Gandler, W.

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nat. Protoc. 9(11), 2555–2573 (2014).
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Gao, L.

L. Gao, L. Shao, B.-C. Chen, and E. Betzig, “3D live fluorescence imaging of cellular dynamics using Bessel beam plane illumination microscopy,” Nat. Protoc. 9(5), 1083–1101 (2014).
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N. Hagen, L. Gao, and T. S. Tkaczyk, “Quantitative sectioning and noise analysis for structured illumination microscopy,” Opt. Express 20(1), 403–413 (2012).
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T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[PubMed]

Ghitani, A.

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
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Greger, K.

Grueber, W. B.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
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Gunther, S.

G. de Medeiros, N. Norlin, S. Gunther, M. Albert, L. Panavaite, U.-M. Fiuza, F. Peri, T. Hiiragi, U. Krzic, and L. Hufnagel, “Confocal multiview light-sheet microscopy,” Nat. Commun. 6, 8881 (2015).
[PubMed]

Guo, M.

Y. Wu, P. Chandris, P. W. Winter, E. Y. Kim, V. Jaumouillé, A. Kumar, M. Guo, J. M. Leung, C. Smith, I. Rey-Suarez, H. Liu, C. M. Waterman, K. S. Ramamurthi, P. J. La Riviere, and H. Shroff, “Simultaneous multiview capture and fusion improves spatial resolution in wide-field and light-sheet microscopy,” Optica 3(8), 897–910 (2016).
[PubMed]

A. Kumar, R. Christensen, M. Guo, P. Chandris, W. Duncan, Y. Wu, A. Santella, M. Moyle, P. W. Winter, D. Colón-Ramos, Z. Bao, and H. Shroff, “Using stage- and slit-scanning to improve contrast and optical sectioning in dual-view,” Biol. Bull. 231(1), 26–39 (2016).
[PubMed]

Hagen, N.

Hiiragi, T.

G. de Medeiros, N. Norlin, S. Gunther, M. Albert, L. Panavaite, U.-M. Fiuza, F. Peri, T. Hiiragi, U. Krzic, and L. Hufnagel, “Confocal multiview light-sheet microscopy,” Nat. Commun. 6, 8881 (2015).
[PubMed]

Hillman, E. M. C.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[PubMed]

Houtsmuller, A. B.

M. E. van Royen, E. I. Verhoef, C. F. Kweldam, W. A. van Cappellen, G.-J. Kremers, A. B. Houtsmuller, and G. J. L. H. van Leenders, “Three-dimensional microscopic analysis of clinical prostate specimens,” Histopathology 69(6), 985–992 (2016).
[PubMed]

Hufnagel, L.

G. de Medeiros, N. Norlin, S. Gunther, M. Albert, L. Panavaite, U.-M. Fiuza, F. Peri, T. Hiiragi, U. Krzic, and L. Hufnagel, “Confocal multiview light-sheet microscopy,” Nat. Commun. 6, 8881 (2015).
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J. Huisken, “Slicing embryos gently with laser light sheets,” BioEssays 34(5), 406–411 (2012).
[PubMed]

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[PubMed]

Iannello, G.

Jährling, N.

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[PubMed]

Jaumouillé, V.

Javid, M. P.

H. L. Fu, J. L. Mueller, M. P. Javid, J. K. Mito, D. G. Kirsch, N. Ramanujam, and J. Q. Brown, “Optimization of a Widefield Structured Illumination Microscope for Non-Destructive Assessment and Quantification of Nuclear Features in Tumor Margins of a Primary Mouse Model of Sarcoma,” PLoS One 8(7), e68868 (2013).
[PubMed]

Jorand, R.

J. Andilla, R. Jorand, O. E. Olarte, A. C. Dufour, M. Cazales, Y. L. E. Montagner, R. Ceolato, N. Riviere, J.-C. Olivo-Marin, P. Loza-Alvarez, and C. Lorenzo, “Imaging tissue-mimic with light sheet microscopy: A comparative guideline,” Sci. Rep. 7, 44939 (2017).
[PubMed]

Juskaitis, R.

Kaminski, C. F.

M. Fantham and C. F. Kaminski, “A new online tool for visualization of volumetric data,” Nat. Publ. Gr. 11, 69 (2017).

Kanchanawong, P.

R. S. Fischer, Y. Wu, P. Kanchanawong, H. Shroff, and C. M. Waterman, “Microscopy in 3D: A biologist’s toolbox,” Trends Cell Biol. 21(12), 682–691 (2011).
[PubMed]

Keller, P. J.

P. J. Keller, M. B. Ahrens, and J. Freeman, “Light-sheet imaging for systems neuroscience,” Nat. Methods 12(1), 27–29 (2015).
[PubMed]

P. J. Keller, A. D. Schmidt, A. Santella, K. Khairy, Z. Bao, J. Wittbrodt, and E. H. K. Stelzer, “Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy,” Nat. Methods 7(8), 637–642 (2010).
[PubMed]

Khairy, K.

P. J. Keller, A. D. Schmidt, A. Santella, K. Khairy, Z. Bao, J. Wittbrodt, and E. H. K. Stelzer, “Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy,” Nat. Methods 7(8), 637–642 (2010).
[PubMed]

Kim, E. Y.

Kimbrell, H. Z.

M. Wang, D. B. Tulman, A. B. Sholl, H. Z. Kimbrell, S. H. Mandava, K. N. Elfer, S. Luethy, M. M. Maddox, W. Lai, B. R. Lee, and J. Q. Brown, “Gigapixel surface imaging of radical prostatectomy specimens for comprehensive detection of cancer-positive surgical margins using structured illumination microscopy,” Sci. Rep. 6, 27419 (2016).
[PubMed]

Kirsch, D. G.

H. L. Fu, J. L. Mueller, M. P. Javid, J. K. Mito, D. G. Kirsch, N. Ramanujam, and J. Q. Brown, “Optimization of a Widefield Structured Illumination Microscope for Non-Destructive Assessment and Quantification of Nuclear Features in Tumor Margins of a Primary Mouse Model of Sarcoma,” PLoS One 8(7), e68868 (2013).
[PubMed]

Kremers, G.-J.

M. E. van Royen, E. I. Verhoef, C. F. Kweldam, W. A. van Cappellen, G.-J. Kremers, A. B. Houtsmuller, and G. J. L. H. van Leenders, “Three-dimensional microscopic analysis of clinical prostate specimens,” Histopathology 69(6), 985–992 (2016).
[PubMed]

Krzic, U.

G. de Medeiros, N. Norlin, S. Gunther, M. Albert, L. Panavaite, U.-M. Fiuza, F. Peri, T. Hiiragi, U. Krzic, and L. Hufnagel, “Confocal multiview light-sheet microscopy,” Nat. Commun. 6, 8881 (2015).
[PubMed]

Kubitscheck, U.

Kumar, A.

A. Kumar, R. Christensen, M. Guo, P. Chandris, W. Duncan, Y. Wu, A. Santella, M. Moyle, P. W. Winter, D. Colón-Ramos, Z. Bao, and H. Shroff, “Using stage- and slit-scanning to improve contrast and optical sectioning in dual-view,” Biol. Bull. 231(1), 26–39 (2016).
[PubMed]

Y. Wu, P. Chandris, P. W. Winter, E. Y. Kim, V. Jaumouillé, A. Kumar, M. Guo, J. M. Leung, C. Smith, I. Rey-Suarez, H. Liu, C. M. Waterman, K. S. Ramamurthi, P. J. La Riviere, and H. Shroff, “Simultaneous multiview capture and fusion improves spatial resolution in wide-field and light-sheet microscopy,” Optica 3(8), 897–910 (2016).
[PubMed]

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nat. Protoc. 9(11), 2555–2573 (2014).
[PubMed]

Kweldam, C. F.

M. E. van Royen, E. I. Verhoef, C. F. Kweldam, W. A. van Cappellen, G.-J. Kremers, A. B. Houtsmuller, and G. J. L. H. van Leenders, “Three-dimensional microscopic analysis of clinical prostate specimens,” Histopathology 69(6), 985–992 (2016).
[PubMed]

La Riviere, P. J.

Lacefield, C.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[PubMed]

Lai, W.

M. Wang, D. B. Tulman, A. B. Sholl, H. Z. Kimbrell, S. H. Mandava, K. N. Elfer, S. Luethy, M. M. Maddox, W. Lai, B. R. Lee, and J. Q. Brown, “Gigapixel surface imaging of radical prostatectomy specimens for comprehensive detection of cancer-positive surgical margins using structured illumination microscopy,” Sci. Rep. 6, 27419 (2016).
[PubMed]

Lavagnino, Z.

Z. Lavagnino, G. Sancataldo, M. d’Amora, P. Follert, D. De Pietri Tonelli, A. Diaspro, and F. Cella Zanacchi, “4D (x-y-z-t) imaging of thick biological samples by means of Two-Photon inverted Selective Plane Illumination Microscopy (2PE-iSPIM),” Sci. Rep. 6, 23923 (2016).
[PubMed]

Lee, B. R.

M. Wang, D. B. Tulman, A. B. Sholl, H. Z. Kimbrell, S. H. Mandava, K. N. Elfer, S. Luethy, M. M. Maddox, W. Lai, B. R. Lee, and J. Q. Brown, “Gigapixel surface imaging of radical prostatectomy specimens for comprehensive detection of cancer-positive surgical margins using structured illumination microscopy,” Sci. Rep. 6, 27419 (2016).
[PubMed]

K. N. Elfer, A. B. Sholl, M. Wang, D. B. Tulman, S. H. Mandava, B. R. Lee, and J. Q. Brown, “DRAQ5 and eosin (‘D&E’) as an analog to hematoxylin and eosin for rapid fluorescence histology of fresh tissues,” PLoS One 11(10), e0165530 (2016).
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P. W. Winter and H. Shroff, “Faster fluorescence microscopy: Advances in high speed biological imaging,” Curr. Opin. Chem. Biol. 20, 46–53 (2014).
[PubMed]

Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
[PubMed]

Wittbrodt, J.

P. J. Keller, A. D. Schmidt, A. Santella, K. Khairy, Z. Bao, J. Wittbrodt, and E. H. K. Stelzer, “Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy,” Nat. Methods 7(8), 637–642 (2010).
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J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
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Wu, Y.

A. Kumar, R. Christensen, M. Guo, P. Chandris, W. Duncan, Y. Wu, A. Santella, M. Moyle, P. W. Winter, D. Colón-Ramos, Z. Bao, and H. Shroff, “Using stage- and slit-scanning to improve contrast and optical sectioning in dual-view,” Biol. Bull. 231(1), 26–39 (2016).
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Y. Wu, P. Chandris, P. W. Winter, E. Y. Kim, V. Jaumouillé, A. Kumar, M. Guo, J. M. Leung, C. Smith, I. Rey-Suarez, H. Liu, C. M. Waterman, K. S. Ramamurthi, P. J. La Riviere, and H. Shroff, “Simultaneous multiview capture and fusion improves spatial resolution in wide-field and light-sheet microscopy,” Optica 3(8), 897–910 (2016).
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A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nat. Protoc. 9(11), 2555–2573 (2014).
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Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
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R. S. Fischer, Y. Wu, P. Kanchanawong, H. Shroff, and C. M. Waterman, “Microscopy in 3D: A biologist’s toolbox,” Trends Cell Biol. 21(12), 682–691 (2011).
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Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
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York, A. G.

Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
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Zhi, C.

Zieglgänsberger, W.

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J. Huisken, “Slicing embryos gently with laser light sheets,” BioEssays 34(5), 406–411 (2012).
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A. Kumar, R. Christensen, M. Guo, P. Chandris, W. Duncan, Y. Wu, A. Santella, M. Moyle, P. W. Winter, D. Colón-Ramos, Z. Bao, and H. Shroff, “Using stage- and slit-scanning to improve contrast and optical sectioning in dual-view,” Biol. Bull. 231(1), 26–39 (2016).
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Biomed. Opt. Express (1)

Curr. Opin. Chem. Biol. (1)

P. W. Winter and H. Shroff, “Faster fluorescence microscopy: Advances in high speed biological imaging,” Curr. Opin. Chem. Biol. 20, 46–53 (2014).
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Histopathology (1)

M. E. van Royen, E. I. Verhoef, C. F. Kweldam, W. A. van Cappellen, G.-J. Kremers, A. B. Houtsmuller, and G. J. L. H. van Leenders, “Three-dimensional microscopic analysis of clinical prostate specimens,” Histopathology 69(6), 985–992 (2016).
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J. Biomed. Opt. (1)

L. Silvestri, I. Costantini, L. Sacconi, and F. S. Pavone, “Clearing of fixed tissue: a review from a microscopist’s perspective,” J. Biomed. Opt. 21(8), 081205 (2016).
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P. A. Santi, “Light Sheet Fluorescence Microscopy: A Review,” J. Histochem. Cytochem. 59(2), 129–138 (2011).
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Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
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H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
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M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
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Nat. Protoc. (2)

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nat. Protoc. 9(11), 2555–2573 (2014).
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Sci. Rep. (4)

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Figures (8)

Fig. 1
Fig. 1

Schematic of iSPIM system. A virtual light sheet generated by one of the micro-mirror scanners that scans in the y(y') direction rapidly illuminates the sample at an oblique 45° angle from one objective. The emission signal from the sample is then collected by the other objective perpendicular to the illumination objective and is imaged with the camera at the same side with the detection objective. Compared to the traditional xyz coordinates, a new set of coordinates of x'y'z' for iSPIM is used. x' axis is along the illumination direction, z' is the same as the traditional x axis which is the direction that the stage moves to create a 3D stack, and y' is the same with y. BS: beam splitter. MM: micro-mirror scanner. TL: tube lens. DM + F: dichroic mirror + emission filter.

Fig. 2
Fig. 2

Scheme of synchronization of electronic confocal rolling and beam scanning. (A) shows the non-linearity of the scanner movement over the whole FOV with linear input voltage. (B) is a mock look-up table showing the possible relations between beam position and linear input voltage. The bottom row is a corresponding example of the customized voltage.

Fig. 3
Fig. 3

MIPs of 81 shifted x'y' slices in the direction of z' with SPIM mode (A) and confocal SPIM (slit size: 9.75 μm) (B). Three random subsets indicated with the yellow boxes in A and the red boxes in B are shown in C-E. Pictures with yellow border are from A, and with red border are from B.

Fig. 4
Fig. 4

MIPs of 81 shifted x'y' slices along z' in different imaging modes. For better comparison, a nonlinear gamma transformation (γ = 0.4) was applied to each image and 0.3% of pixels were saturated in the lookup table. Quantitative measurement of the 81 raw x'y' images shows that compared to SPIM mode alone, confocal SPIM with 9.75 μm slit size was 1.11 ± 0.02 (SD) times better on image contrast, SI SPIM at frequency of 0.16 was 2.76 ± 0.15 (SD) times better, and the combined mode with 9.75 μm slit size and frequency of 0.16 was 2.80 ± 0.1 times better. The intensity range of the four images is 29665 ± 1196 (SD). Scale bar: 10 μm.

Fig. 5
Fig. 5

Contrast comparison among different imaging modes. Same position from a PI stained prostate tissue was imaged with SPIM (global exposure mode) (A), confocal SPIM (B, C), SI SPIM (D-F), and confocal-SI SPIM(G-I) respectively. The parameters used in different modes were labeled in the lower part of each image. (D) and (H) had the best contrast. However, the image contrast at SI SPIM mode with frequency of 0.16 was decreased to even lower than SPIM mode (F, J) due to the decreased SNR. By adding confocal detection to SI (I), the contrast can be maintained by improving SNR. For better visualization and comparison, 0.5% of pixels were saturated in the lookup table. The yellow line in (A) separates the in-focus right part and the scattering left part which can be rejected in other modes. The red line in (J) indicates the size of the beam waist. (K) Contrast comparison between SPIM mode and Confocal-SI mode versus depth. The yellow stars indicate the top surface of the sample, which is where the illumination light originates. The green and blue dash lines indicate two different depths along x', with distance of about 175 μm. Scalebar, 50 μm.

Fig. 6
Fig. 6

Comparison of illumination pattern modulation depth versus normalized grid frequency at global mode and confocal mode with different slit sizes (A). Corresponding pattern images at grid frequency of 0.16 at global mode and confocal mode with different slit sizes (B). For better visualization and comparison, images in B were normalized to show the min-max intensity.

Fig. 7
Fig. 7

Axial resolution verses pattern frequency at different modes. 20 beads were calculated in each parameter. Compared to the axial resolution in SPIM mode only, all of the other modes have p-values <0.01 at alpha = 0.05 significance level, and have significantly smaller axial resolution than the SPIM mode (Global with no SI, leftmost blue bar).

Fig. 8
Fig. 8

Comparison of X-Y and X-Z planes from volumes of PI stained prostate sample imaged by SPIM (A), confocal SPIM with slit size of 9.75 μm (B) and confocal-SI SPIM with slit size of 9.75μm and normalized frequency of 0.16 (C). For better visualization and comparison, the minimum intensity displayed were all 0, and the colormap was scaled to match the range of the intensities. To compare the differences of the imaging details, smaller regions from the yellow box in the SPIM mode (D), confocal SPIM mode (F) and confocal-SI mode (G) were shown. 0.3% of the pixels were saturated in E and F for better visualization. The volumes were reconstructed with Amira. Scale bar in A-C: 250 µm, D-F: 100 μm.

Tables (1)

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Table 1 Contrast enhancement over SPIM mode among different modes and parameters

Equations (1)

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I sectioned = ( I 1 I 2 ) 2 + ( I 1 I 3 ) 2 + ( I 2 I 3 ) 2