Abstract

Versatile, sterically accessible imaging systems capable of in vivo rapid volumetric functional and structural imaging deep in the brain continue to be a limiting factor in neuroscience research. Towards overcoming this obstacle, we present integrated one- and two-photon scanned oblique plane illumination (SOPi, /sōpī/) microscopy which uses a single front-facing microscope objective to provide light-sheet scanning based rapid volumetric imaging capability at subcellular resolution. Our planar scan-mirror based optimized light-sheet architecture allows for non-distorted scanning of volume samples, simplifying accurate reconstruction of the imaged volume. Integration of both one-photon (1P) and two-photon (2P) light-sheet microscopy in the same system allows for easy selection between rapid volumetric imaging and higher resolution imaging in scattering media. Using SOPi, we demonstrate deep, large volume imaging capability inside scattering mouse brain sections and rapid imaging speeds up to 10 volumes per second in zebrafish larvae expressing genetically encoded fluorescent proteins GFP or GCaMP6s. SOPi’s flexibility and steric access makes it adaptable for numerous imaging applications and broadly compatible with orthogonal techniques for actuating or interrogating neuronal structure and activity.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2017 (1)

T. Nöbauer, O. Skocek, A. J. Pernía-Andrade, L. Weilguny, F. M. Traub, M. I. Molodtsov, and A. Vaziri, “Video rate volumetric Ca2+ imaging across cortex using seeded iterative demixing (SID) microscopy,” Nat. Methods 14(8), 811–818 (2017).
[Crossref] [PubMed]

2016 (3)

L. A. Royer, W. C. Lemon, R. K. Chhetri, Y. Wan, M. Coleman, E. W. Myers, and P. J. Keller, “Adaptive light-sheet microscopy for long-term, high-resolution imaging in living organisms,” Nat. Biotechnol. 34(12), 1267–1278 (2016).
[Crossref] [PubMed]

M. B. Sikkel, S. Kumar, V. Maioli, C. Rowlands, F. Gordon, S. E. Harding, A. R. Lyon, K. T. MacLeod, and C. Dunsby, “High speed sCMOS-based oblique plane microscopy applied to the study of calcium dynamics in cardiac myocytes,” J. Biophotonics 9(3), 311–323 (2016).
[Crossref] [PubMed]

X. Xiao, V. F. Geyer, H. Bowne-Anderson, J. Howard, and I. F. Sbalzarini, “Automatic optimal filament segmentation with sub-pixel accuracy using generalized linear models and B-spline level-sets,” Med. Image Anal. 32, 157–172 (2016).
[Crossref] [PubMed]

2015 (3)

L. A. Royer, M. Weigert, U. Günther, N. Maghelli, F. Jug, I. F. Sbalzarini, and E. W. Myers, “ClearVolume: open-source live 3D visualization for light-sheet microscopy,” Nat. Methods 12(6), 480–481 (2015).
[Crossref] [PubMed]

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

T. Li, S. Ota, J. Kim, Z. J. Wong, Y. Wang, X. Yin, and X. Zhang, “Axial plane optical microscopy,” Sci. Rep. 4(1), 7253 (2015).
[Crossref] [PubMed]

2014 (5)

A. D. Edelstein, M. A. Tsuchida, N. Amodaj, H. Pinkard, R. D. Vale, and N. Stuurman, “Advanced methods of microscope control using μManager software,” J. Biol. Methods 1(2), e10 (2014).
[Crossref] [PubMed]

T. R. Thiele, J. C. Donovan, and H. Baier, “Descending control of swim posture by a midbrain nucleus in zebrafish,” Neuron 83(3), 679–691 (2014).
[Crossref] [PubMed]

N. Vladimirov, Y. Mu, T. Kawashima, D. V. Bennett, C. T. Yang, L. L. Looger, P. J. Keller, J. Freeman, and M. B. Ahrens, “Light-sheet functional imaging in fictively behaving zebrafish,” Nat. Methods 11(9), 883–884 (2014).
[Crossref] [PubMed]

B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A.-C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

T. Vettenburg, H. I. Dalgarno, J. Nylk, C. Coll-Lladó, D. E. Ferrier, T. Čižmár, F. J. Gunn-Moore, and K. Dholakia, “Light-sheet microscopy using an Airy beam,” Nat. Methods 11(5), 541–544 (2014).
[Crossref] [PubMed]

2013 (3)

F. O. Fahrbach, V. Gurchenkov, K. Alessandri, P. Nassoy, and A. Rohrbach, “Light-sheet microscopy in thick media using scanned Bessel beams and two-photon fluorescence excitation,” Opt. Express 21(11), 13824–13839 (2013).
[Crossref] [PubMed]

C. Satou, Y. Kimura, H. Hirata, M. L. Suster, K. Kawakami, and S. Higashijima, “Transgenic tools to characterize neuronal properties of discrete populations of zebrafish neurons,” Development 140(18), 3927–3931 (2013).
[Crossref] [PubMed]

P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10(7), 598–599 (2013).
[Crossref] [PubMed]

2012 (3)

E. Baumgart and U. Kubitscheck, “Scanned light sheet microscopy with confocal slit detection,” Opt. Express 20(19), 21805–21814 (2012).
[Crossref] [PubMed]

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

2011 (3)

S. Kumar, D. Wilding, M. B. Sikkel, A. R. Lyon, K. T. MacLeod, and C. Dunsby, “High-speed 2D and 3D fluorescence microscopy of cardiac myocytes,” Opt. Express 19(15), 13839–13847 (2011).
[Crossref] [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).
[Crossref] [PubMed]

T. V. Truong, W. Supatto, D. S. Koos, J. M. Choi, and S. E. Fraser, “Deep and fast live imaging with two-photon scanned light-sheet microscopy,” Nat. Methods 8(9), 757–760 (2011).
[Crossref] [PubMed]

2010 (2)

D. A. Dombeck, C. D. Harvey, L. Tian, L. L. Looger, and D. W. Tank, “Functional imaging of hippocampal place cells at cellular resolution during virtual navigation,” Nat. Neurosci. 13(11), 1433–1440 (2010).
[Crossref] [PubMed]

E. Arthur, N. Amodaj, K. Hoover, R. Vale, and N. Stuurman, “Computer control of microscopes using µManager,” Curr. Protoc. Mol. Biol. 92(1), 14–20 (2010).

2008 (2)

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. K. Stelzer, “Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

C. Dunsby, “Optically sectioned imaging by oblique plane microscopy,” Opt. Express 16(25), 20306–20316 (2008).
[Crossref] [PubMed]

2007 (3)

2006 (4)

C. J. Engelbrecht and E. H. Stelzer, “Resolution enhancement in a light-sheet-based microscope (SPIM),” Opt. Lett. 31(10), 1477–1479 (2006).
[Crossref] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[Crossref] [PubMed]

S. T. Hess, T. P. K. Girirajan, and M. D. Mason, “Ultra-high resolution imaging by fluorescence photoactivation localization microscopy,” Biophys. J. 91(11), 4258–4272 (2006).
[Crossref] [PubMed]

M. Levoy, R. Ng, A. Adams, M. Footer, and M. Horowitz, “Light field microscopy,” ACM Trans. Graph. 25(3), 924 (2006).
[Crossref]

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).
[Crossref] [PubMed]

2003 (2)

P. Theer, M. T. Hasan, and W. Denk, “Two-photon imaging to a depth of 1000 µm in living brains by use of a Ti:Al2O3 regenerative amplifier,” Opt. Lett. 28(12), 1022–1024 (2003).
[Crossref] [PubMed]

J. Shin, H. C. Park, J. M. Topczewska, D. J. Mawdsley, and B. Appel, “Neural cell fate analysis in zebrafish using olig2 BAC transgenics,” Methods Cell Sci. 25(1-2), 7–14 (2003).
[Crossref] [PubMed]

2001 (1)

E. H. W. Meijering, W. J. Niessen, and M. A. Viergever, “Quantitative Evaluation of Convolution-Based Methods for Medical Image Interpolation,” Med. Image Anal. 5(2), 111–126 (2001).
[Crossref] [PubMed]

2000 (1)

M. G. L. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc. 198(2), 82–87 (2000).
[Crossref] [PubMed]

1999 (1)

J. G. McNally, T. Karpova, J. Cooper, and J. A. Conchello, “Three-dimensional imaging by deconvolution microscopy,” Methods 19(3), 373–385 (1999).
[Crossref] [PubMed]

1994 (1)

1902 (1)

H. Siedentopf and R. Zsigmondy, “Uber Sichtbarmachung und Größenbestimmung ultramikoskopischer Teilchen, mit besonderer Anwendung auf Goldrubingläser,” Ann. Phys. 315(1), 1–39 (1902).
[Crossref]

Adams, A.

M. Levoy, R. Ng, A. Adams, M. Footer, and M. Horowitz, “Light field microscopy,” ACM Trans. Graph. 25(3), 924 (2006).
[Crossref]

Ahrens, M. B.

N. Vladimirov, Y. Mu, T. Kawashima, D. V. Bennett, C. T. Yang, L. L. Looger, P. J. Keller, J. Freeman, and M. B. Ahrens, “Light-sheet functional imaging in fictively behaving zebrafish,” Nat. Methods 11(9), 883–884 (2014).
[Crossref] [PubMed]

Alessandri, K.

Amodaj, N.

A. D. Edelstein, M. A. Tsuchida, N. Amodaj, H. Pinkard, R. D. Vale, and N. Stuurman, “Advanced methods of microscope control using μManager software,” J. Biol. Methods 1(2), e10 (2014).
[Crossref] [PubMed]

E. Arthur, N. Amodaj, K. Hoover, R. Vale, and N. Stuurman, “Computer control of microscopes using µManager,” Curr. Protoc. Mol. Biol. 92(1), 14–20 (2010).

Appel, B.

J. Shin, H. C. Park, J. M. Topczewska, D. J. Mawdsley, and B. Appel, “Neural cell fate analysis in zebrafish using olig2 BAC transgenics,” Methods Cell Sci. 25(1-2), 7–14 (2003).
[Crossref] [PubMed]

Arganda-Carreras, I.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Arthur, E.

E. Arthur, N. Amodaj, K. Hoover, R. Vale, and N. Stuurman, “Computer control of microscopes using µManager,” Curr. Protoc. Mol. Biol. 92(1), 14–20 (2010).

Baier, H.

T. R. Thiele, J. C. Donovan, and H. Baier, “Descending control of swim posture by a midbrain nucleus in zebrafish,” Neuron 83(3), 679–691 (2014).
[Crossref] [PubMed]

Bao, 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).
[Crossref] [PubMed]

Bates, M.

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[Crossref] [PubMed]

Baumgart, E.

Bembenek, J. N.

B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A.-C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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N. Vladimirov, Y. Mu, T. Kawashima, D. V. Bennett, C. T. Yang, L. L. Looger, P. J. Keller, J. Freeman, and M. B. Ahrens, “Light-sheet functional imaging in fictively behaving zebrafish,” Nat. Methods 11(9), 883–884 (2014).
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B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A.-C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A.-C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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Botcherby, E. J.

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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. 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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X. Xiao, V. F. Geyer, H. Bowne-Anderson, J. Howard, and I. F. Sbalzarini, “Automatic optimal filament segmentation with sub-pixel accuracy using generalized linear models and B-spline level-sets,” Med. Image Anal. 32, 157–172 (2016).
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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. 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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T. Vettenburg, H. I. Dalgarno, J. Nylk, C. Coll-Lladó, D. E. Ferrier, T. Čižmár, F. J. Gunn-Moore, and K. Dholakia, “Light-sheet microscopy using an Airy beam,” Nat. Methods 11(5), 541–544 (2014).
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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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J. G. McNally, T. Karpova, J. Cooper, and J. A. Conchello, “Three-dimensional imaging by deconvolution microscopy,” Methods 19(3), 373–385 (1999).
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B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A.-C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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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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Dholakia, K.

T. Vettenburg, H. I. Dalgarno, J. Nylk, C. Coll-Lladó, D. E. Ferrier, T. Čižmár, F. J. Gunn-Moore, and K. Dholakia, “Light-sheet microscopy using an Airy beam,” Nat. Methods 11(5), 541–544 (2014).
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Dombeck, D. A.

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M. B. Sikkel, S. Kumar, V. Maioli, C. Rowlands, F. Gordon, S. E. Harding, A. R. Lyon, K. T. MacLeod, and C. Dunsby, “High speed sCMOS-based oblique plane microscopy applied to the study of calcium dynamics in cardiac myocytes,” J. Biophotonics 9(3), 311–323 (2016).
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P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10(7), 598–599 (2013).
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Engelbrecht, C. J.

English, B. P.

B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A.-C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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Fahrbach, F. O.

Ferrier, D. E.

T. Vettenburg, H. I. Dalgarno, J. Nylk, C. Coll-Lladó, D. E. Ferrier, T. Čižmár, F. J. Gunn-Moore, and K. Dholakia, “Light-sheet microscopy using an Airy beam,” Nat. Methods 11(5), 541–544 (2014).
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M. Levoy, R. Ng, A. Adams, M. Footer, and M. Horowitz, “Light field microscopy,” ACM Trans. Graph. 25(3), 924 (2006).
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Fraser, S. E.

T. V. Truong, W. Supatto, D. S. Koos, J. M. Choi, and S. E. Fraser, “Deep and fast live imaging with two-photon scanned light-sheet microscopy,” Nat. Methods 8(9), 757–760 (2011).
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Freeman, J.

N. Vladimirov, Y. Mu, T. Kawashima, D. V. Bennett, C. T. Yang, L. L. Looger, P. J. Keller, J. Freeman, and M. B. Ahrens, “Light-sheet functional imaging in fictively behaving zebrafish,” Nat. Methods 11(9), 883–884 (2014).
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J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
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Fritz-Laylin, L.

B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A.-C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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X. Xiao, V. F. Geyer, H. Bowne-Anderson, J. Howard, and I. F. Sbalzarini, “Automatic optimal filament segmentation with sub-pixel accuracy using generalized linear models and B-spline level-sets,” Med. Image Anal. 32, 157–172 (2016).
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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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Girirajan, T. P. K.

S. T. Hess, T. P. K. Girirajan, and M. D. Mason, “Ultra-high resolution imaging by fluorescence photoactivation localization microscopy,” Biophys. J. 91(11), 4258–4272 (2006).
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Gordon, F.

M. B. Sikkel, S. Kumar, V. Maioli, C. Rowlands, F. Gordon, S. E. Harding, A. R. Lyon, K. T. MacLeod, and C. Dunsby, “High speed sCMOS-based oblique plane microscopy applied to the study of calcium dynamics in cardiac myocytes,” J. Biophotonics 9(3), 311–323 (2016).
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B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A.-C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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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. 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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Gunn-Moore, F. J.

T. Vettenburg, H. I. Dalgarno, J. Nylk, C. Coll-Lladó, D. E. Ferrier, T. Čižmár, F. J. Gunn-Moore, and K. Dholakia, “Light-sheet microscopy using an Airy beam,” Nat. Methods 11(5), 541–544 (2014).
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L. A. Royer, M. Weigert, U. Günther, N. Maghelli, F. Jug, I. F. Sbalzarini, and E. W. Myers, “ClearVolume: open-source live 3D visualization for light-sheet microscopy,” Nat. Methods 12(6), 480–481 (2015).
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Gustafsson, M. G. L.

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B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A.-C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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Harding, S. E.

M. B. Sikkel, S. Kumar, V. Maioli, C. Rowlands, F. Gordon, S. E. Harding, A. R. Lyon, K. T. MacLeod, and C. Dunsby, “High speed sCMOS-based oblique plane microscopy applied to the study of calcium dynamics in cardiac myocytes,” J. Biophotonics 9(3), 311–323 (2016).
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J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
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Harvey, C. D.

D. A. Dombeck, C. D. Harvey, L. Tian, L. L. Looger, and D. W. Tank, “Functional imaging of hippocampal place cells at cellular resolution during virtual navigation,” Nat. Neurosci. 13(11), 1433–1440 (2010).
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Hasan, M. T.

Hell, S. W.

Hess, S. T.

S. T. Hess, T. P. K. Girirajan, and M. D. Mason, “Ultra-high resolution imaging by fluorescence photoactivation localization microscopy,” Biophys. J. 91(11), 4258–4272 (2006).
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Higashijima, S.

C. Satou, Y. Kimura, H. Hirata, M. L. Suster, K. Kawakami, and S. Higashijima, “Transgenic tools to characterize neuronal properties of discrete populations of zebrafish neurons,” Development 140(18), 3927–3931 (2013).
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Hillman, E. M.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. 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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C. Satou, Y. Kimura, H. Hirata, M. L. Suster, K. Kawakami, and S. Higashijima, “Transgenic tools to characterize neuronal properties of discrete populations of zebrafish neurons,” Development 140(18), 3927–3931 (2013).
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M. Levoy, R. Ng, A. Adams, M. Footer, and M. Horowitz, “Light field microscopy,” ACM Trans. Graph. 25(3), 924 (2006).
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X. Xiao, V. F. Geyer, H. Bowne-Anderson, J. Howard, and I. F. Sbalzarini, “Automatic optimal filament segmentation with sub-pixel accuracy using generalized linear models and B-spline level-sets,” Med. Image Anal. 32, 157–172 (2016).
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P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10(7), 598–599 (2013).
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J. Huisken and D. Y. R. Stainier, “Even fluorescence excitation by multidirectional selective plane illumination microscopy (mSPIM),” Opt. Lett. 32(17), 2608–2610 (2007).
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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).
[Crossref] [PubMed]

Janetopoulos, C.

B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A.-C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

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L. A. Royer, M. Weigert, U. Günther, N. Maghelli, F. Jug, I. F. Sbalzarini, and E. W. Myers, “ClearVolume: open-source live 3D visualization for light-sheet microscopy,” Nat. Methods 12(6), 480–481 (2015).
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Juskaitis, R.

Karpova, T.

J. G. McNally, T. Karpova, J. Cooper, and J. A. Conchello, “Three-dimensional imaging by deconvolution microscopy,” Methods 19(3), 373–385 (1999).
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C. Satou, Y. Kimura, H. Hirata, M. L. Suster, K. Kawakami, and S. Higashijima, “Transgenic tools to characterize neuronal properties of discrete populations of zebrafish neurons,” Development 140(18), 3927–3931 (2013).
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Kawashima, T.

N. Vladimirov, Y. Mu, T. Kawashima, D. V. Bennett, C. T. Yang, L. L. Looger, P. J. Keller, J. Freeman, and M. B. Ahrens, “Light-sheet functional imaging in fictively behaving zebrafish,” Nat. Methods 11(9), 883–884 (2014).
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J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
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P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. K. Stelzer, “Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy,” Science 322(5904), 1065–1069 (2008).
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L. A. Royer, M. Weigert, U. Günther, N. Maghelli, F. Jug, I. F. Sbalzarini, and E. W. Myers, “ClearVolume: open-source live 3D visualization for light-sheet microscopy,” Nat. Methods 12(6), 480–481 (2015).
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T. Li, S. Ota, J. Kim, Z. J. Wong, Y. Wang, X. Yin, and X. Zhang, “Axial plane optical microscopy,” Sci. Rep. 4(1), 7253 (2015).
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X. Xiao, V. F. Geyer, H. Bowne-Anderson, J. Howard, and I. F. Sbalzarini, “Automatic optimal filament segmentation with sub-pixel accuracy using generalized linear models and B-spline level-sets,” Med. Image Anal. 32, 157–172 (2016).
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Nat. Biotechnol. (1)

L. A. Royer, W. C. Lemon, R. K. Chhetri, Y. Wan, M. Coleman, E. W. Myers, and P. J. Keller, “Adaptive light-sheet microscopy for long-term, high-resolution imaging in living organisms,” Nat. Biotechnol. 34(12), 1267–1278 (2016).
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Nat. Methods (9)

T. V. Truong, W. Supatto, D. S. Koos, J. M. Choi, and S. E. Fraser, “Deep and fast live imaging with two-photon scanned light-sheet microscopy,” Nat. Methods 8(9), 757–760 (2011).
[Crossref] [PubMed]

N. Vladimirov, Y. Mu, T. Kawashima, D. V. Bennett, C. T. Yang, L. L. Looger, P. J. Keller, J. Freeman, and M. B. Ahrens, “Light-sheet functional imaging in fictively behaving zebrafish,” Nat. Methods 11(9), 883–884 (2014).
[Crossref] [PubMed]

P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10(7), 598–599 (2013).
[Crossref] [PubMed]

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Supplementary Material (7)

NameDescription
» Visualization 1       Visualization 1. Geometrically corrected volume reconstruction after application of affine transformation to the acquired stack of 600 frames captured by 1P SOPi system to cover a volume of 850×325×500 µm3 in a fixed 1 mm thick slice of Thy1GFP trans
» Visualization 2       Visualization 2. Geometrically corrected volume reconstruction after application of affine transformation to the acquired stack of 600 frames captured by 2P SOPi system to cover a volume of 750×270×500 µm3 in a fixed 1 mm thick slice of Thy1GFP trans
» Visualization 3       Visualization 3. 3D volume rendering of the cerebellum of a GFP expressing zebrafish, acquired using a Zeiss LSM 710 confocal microscope. The scanned section is ~450×300×200 µm3 (20 minutes acquisition time).
» Visualization 4       Visualization 4. Volume rendering of the cerebellum region of the same GFP-expressing zebrafish as in Visualization 3, scanned using 2P light-sheet on SOPi (6 seconds acquisition time).
» Visualization 5       Visualization 5. Volume rendering of the same cerebellum region of GFP expressing fish as shown in Visualization 3 scanned using 1P light-sheet on SOPi (1 second acquisition time).
» Visualization 6       Visualization 6. Video showing the activity in a GCaMP6s expressing zebrafish larva. A 30 second recording of activity from all the 10 optical segments covering the hind-brain and spinal cord of zebrafish, spanning 850×300×50 µm3. The whole volume wa
» Visualization 7       Visualization 7. The 4D visualization showing 3D volume rendering of same 30 second recording of data shown in Video 9. The video plays at 5x speed. The rotation of view is introduced via post-processing of 3D data for enhanced visualization of featu

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Figures (7)

Fig. 1
Fig. 1 Scanning architecture of SOPi. (a) SOPi is assembled by integrating a planar scan mirror based scanning geometry (shown in inset) into the OPM design. MO: microscope objective, BFP: back focal plane. (b) Part of assembled SOPi design showing the intended action of the scan mirror to control the scanning of light-sheet without a change in tilt while simultaneously de-scanning the fluorescence signal to provide a stationary emission beam.
Fig. 2
Fig. 2 Optimization of scanning geometry. (a) Scanning architecture with on-axis excitation beam. (b) Shifting the scan-mirror provides an offset in the incident beam to produce an oblique light-sheet. The point of reflection is centered at back-focal plane of L2 and shifts around it as G1 scans. (c) Shifting of excitation beam from its zero-position (as shown in (a)) to produce desired oblique light-sheet. The point of reflection is no longer centered at back-focal plane of L2 and shifts as G1 scans. (f) Ray-tracing based numerically measured scanned beam-position at the numerical detector plane. (g) Numerically measured scanned beam-tilt at the detection plane.
Fig. 3
Fig. 3 SOPi system. (a) Schematic diagram describing the full optical layout of SOPi. Inset shows the scanning arrangement to create and sweep light-sheet in sample volume. MO: microscope objective, DM: dichroic mirror, LD: laser diode, M: mirror. (b) Calculation of effective acceptance angle of SOPi system.
Fig. 4
Fig. 4 Affine transformation for correct volume reconstruction. (a) Light-sheet orientation in a cylindrical object and corresponding image section acquired on camera. (b) Geometrical transformations to reconstruct the scanned volume.
Fig. 5
Fig. 5 Imaging microbeads for estimating resolution. (a) 1P SOPi microscopy of microbeads. (b) 2P SOPi microscopy of microbeads. Insets in (a) and (b) show enhanced images to help see low intensity artifacts. (c) Normalized intensity line plot through one microbead.
Fig. 6
Fig. 6 Imaging mouse brain slices using SOPi. (a) A widefield fluorescence image of 1 mm thick slice of Thy1-GFP adult mouse, along with a highlighted area of the hippocampus imaged under SOPi setup. (b) Volumetric reconstruction of SOPi acquired 1P light-sheet images by z-stacking frames. (c) Affine transformed 3D reconstruction of 1P light-sheet scanned volume which matches the view of the dentate gyrus as expected from (a). The inset shows a zoomed in version to illustrate finer dendritic details of dentate gyrus granule neurons. (d) Affine transformed 3D reconstruction of the same volume scanned by 2P light-sheet on SOPi setup. Inset image demonstrates superior dendritic imaging compared to their 1P light-sheet imaged copy in (c). Two arrows (pink, green) facilitate direct comparison of the same dendritic region in 1P and 2P imaging.
Fig. 7
Fig. 7 Imaging zebrafish larvae. (a) A high resolution confocal imaging of zebrafish cerebellum in nacre Tg(Olig2:GFP) fish acquired in 20 min. (b) The same cerebellar region imaged with 2P SOPi setup in 6 seconds. (c) The same cerebellar region imaged using 1P SOPi setup in 1 second. (d) Schematic diagram showing the arrangement for rapid volumetric GCaMP imaging of Tg(VGlut2a:Gal4;UAS:GCaMP6s) zebrafish hind-brain and spinal cord using a fast scanning 1P light-sheet in the SOPi setup. The volume scan consists of 10 segments, covered at rate of 100 fps leading to 10 VPS scan speed. (e) Left, GCaMP fluorescence in a subset of active cells during spontaneous activity, shown as standard deviation based intensity projections of the frames corresponding to slice position I and VIII in scanned volume (I-X). Right, GCaMP imaging traces corresponding to neurons 1-10 in optical sections I and VIII (30 sec).

Equations (2)

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[ x y z 1 ] = [ a x x a x y a x z a x t a y x a y y a y z a y t a z x a z y a z z a z t 0 0 0 1 ] [ x i y i z i 1 ] .
M s h × M s c = [ 1 0 0 0 0 1 0 0 0 1 1 0 0 0 0 1 ] × [ 1 0 0 0 0 1 / 2 0 0 0 0 1 0 0 0 0 1 ] = [ 1 0 0 0 0 1 / 2 0 0 0 1 / 2 1 0 0 0 0 1 ] .

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