Abstract

Multi-dimensional fluorescence imaging of live animal models demands strong optical sectioning, high spatial resolution, fast image acquisition, and minimal photobleaching. While conventional laser scanning microscopes are capable of deep penetration and sub-cellular resolution, they are generally too slow and causing excessive photobleaching for volumetric or time-lapse imaging. We demonstrate the performance of an augmented line-scan focal modulation microscope (aLSFMM), a high-speed imaging platform that affords above video-rate imaging speed by the use of line scanning. Exceptional background rejection is accomplished by combining a confocal slit with focal modulation. The image quality is further improved by merging the information from simultaneously acquired focal modulation and confocal images. Such a hybrid imaging scheme makes it possible to use very low power excitation light in high-speed imaging, and therefore leads to reduced photobleaching that is desirable for three-dimensional (3D) and four-dimensional (4D) in vivo image acquisition.

© 2017 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

Full Article  |  PDF Article
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References

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2017 (1)

S. Pant, C. Li, Z. Gong, and N. Chen, “Line-scan focal modulation microscopy,” J. Biomed. Opt. 22(5), 50502 (2017).
[PubMed]

2015 (2)

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]

Y. Duan and N. Chen, “Hybrid wide-field and scanning microscopy for high-speed 3D imaging,” Opt. Lett. 40(22), 5251–5254 (2015).
[PubMed]

2014 (2)

Y. Duan, C. J. Sheppard, S. Rehman, and N. Chen, “Analytic method to optimize aperture design in focal modulation microscopy,” Opt. Lett. 39(6), 1677–1680 (2014).
[PubMed]

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[PubMed]

2013 (4)

B. Schmid, G. Shah, N. Scherf, M. Weber, K. Thierbach, C. P. Campos, I. Roeder, P. Aanstad, and J. Huisken, “High-speed panoramic light-sheet microscopy reveals global endodermal cell dynamics,” Nat. Commun. 4, 2207 (2013).
[PubMed]

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nature Methods 10, 413 (2013).

C. Mosimann, A. C. Puller, K. L. Lawson, P. Tschopp, A. Amsterdam, and L. I. Zon, “Site-directed zebrafish transgenesis into single landing sites with the phiC31 integrase system,” Dev. Dyn. 242(8), 949–963 (2013).
[PubMed]

M. Jemielita, M. J. Taormina, A. Delaurier, C. B. Kimmel, and R. Parthasarathy, “Comparing phototoxicity during the development of a zebrafish craniofacial bone using confocal and light sheet fluorescence microscopy techniques,” J. Biophotonics 6(11-12), 920–928 (2013), doi:.
[Crossref] [PubMed]

2012 (3)

2011 (2)

G. Gao, S. P. Chong, C. J. R. Sheppard, and N. Chen, “Considerations of aperture configuration in focal modulation microscopy from the standpoint of modulation depth,” J. Opt. Soc. Am. A 28(4), 496–501 (2011).
[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).
[PubMed]

2010 (3)

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[PubMed]

S. P. Chong, C. H. Wong, C. J. R. Sheppard, and N. Chen, “Focal modulation microscopy: a theoretical study,” Opt. Lett. 35(11), 1804–1806 (2010).
[PubMed]

S. P. Chong, C. H. Wong, K. F. Wong, C. J. R. Sheppard, and N. Chen, “High-speed focal modulation microscopy using acousto-optical modulators,” Biomed. Opt. Express 1(3), 1026–1037 (2010).
[PubMed]

2009 (2)

C. H. Wong, S. P. Chong, C. J. R. Sheppard, and N. Chen, “Simple spatial phase modulator for focal modulation microscopy,” Appl. Opt. 48(17), 3237–3242 (2009).
[PubMed]

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[PubMed]

2008 (3)

L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
[PubMed]

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).
[PubMed]

N. Chen, C.-H. Wong, and C. J. R. Sheppard, “Focal modulation microscopy,” Opt. Express 16(23), 18764–18769 (2008).
[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]

2003 (1)

R. Heintzmann, V. Sarafis, P. Munroe, J. Nailon, Q. S. Hanley, and T. M. Jovin, “Resolution enhancement by subtraction of confocal signals taken at different pinhole sizes,” Micron 34(6-7), 293–300 (2003).
[PubMed]

1999 (1)

1988 (1)

C. J. R. Sheppard and X. Q. Mao, “Confocal microscopes with slit apertures,” J. Mod. Opt. 35, 1169–1185 (1988).

Aanstad, P.

B. Schmid, G. Shah, N. Scherf, M. Weber, K. Thierbach, C. P. Campos, I. Roeder, P. Aanstad, and J. Huisken, “High-speed panoramic light-sheet microscopy reveals global endodermal cell dynamics,” Nat. Commun. 4, 2207 (2013).
[PubMed]

Agard, D. A.

L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
[PubMed]

Ahrens, M. B.

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nature Methods 10, 413 (2013).

Amsterdam, A.

C. Mosimann, A. C. Puller, K. L. Lawson, P. Tschopp, A. Amsterdam, and L. I. Zon, “Site-directed zebrafish transgenesis into single landing sites with the phiC31 integrase system,” Dev. Dyn. 242(8), 949–963 (2013).
[PubMed]

Artigas, D.

Bartoo, A. C.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[PubMed]

Beaurepaire, E.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[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]

Bourgine, P.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[PubMed]

Bozinovic, N.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[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]

Burke, B.

L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
[PubMed]

Campos, C. P.

B. Schmid, G. Shah, N. Scherf, M. Weber, K. Thierbach, C. P. Campos, I. Roeder, P. Aanstad, and J. Huisken, “High-speed panoramic light-sheet microscopy reveals global endodermal cell dynamics,” Nat. Commun. 4, 2207 (2013).
[PubMed]

Cardoso, M. C.

L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
[PubMed]

Carlton, P. M.

L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
[PubMed]

Chen, N.

S. Pant, C. Li, Z. Gong, and N. Chen, “Line-scan focal modulation microscopy,” J. Biomed. Opt. 22(5), 50502 (2017).
[PubMed]

Y. Duan and N. Chen, “Hybrid wide-field and scanning microscopy for high-speed 3D imaging,” Opt. Lett. 40(22), 5251–5254 (2015).
[PubMed]

Y. Duan, C. J. Sheppard, S. Rehman, and N. Chen, “Analytic method to optimize aperture design in focal modulation microscopy,” Opt. Lett. 39(6), 1677–1680 (2014).
[PubMed]

N. Chen and G. Gao, “Multi-contrast focal modulation microscopy for in vivo imaging of thick biological tissues,” Opt. Express 20(11), 12166–12170 (2012).
[PubMed]

G. Gao, S. P. Chong, C. J. R. Sheppard, and N. Chen, “Considerations of aperture configuration in focal modulation microscopy from the standpoint of modulation depth,” J. Opt. Soc. Am. A 28(4), 496–501 (2011).
[PubMed]

S. P. Chong, C. H. Wong, K. F. Wong, C. J. R. Sheppard, and N. Chen, “High-speed focal modulation microscopy using acousto-optical modulators,” Biomed. Opt. Express 1(3), 1026–1037 (2010).
[PubMed]

S. P. Chong, C. H. Wong, C. J. R. Sheppard, and N. Chen, “Focal modulation microscopy: a theoretical study,” Opt. Lett. 35(11), 1804–1806 (2010).
[PubMed]

C. H. Wong, S. P. Chong, C. J. R. Sheppard, and N. Chen, “Simple spatial phase modulator for focal modulation microscopy,” Appl. Opt. 48(17), 3237–3242 (2009).
[PubMed]

N. Chen, C.-H. Wong, and C. J. R. Sheppard, “Focal modulation microscopy,” Opt. Express 16(23), 18764–18769 (2008).
[PubMed]

Choi, J. M.

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).
[PubMed]

Chong, S. P.

Chu, K. K.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[PubMed]

Débarre, D.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[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]

Delaurier, A.

M. Jemielita, M. J. Taormina, A. Delaurier, C. B. Kimmel, and R. Parthasarathy, “Comparing phototoxicity during the development of a zebrafish craniofacial bone using confocal and light sheet fluorescence microscopy techniques,” J. Biophotonics 6(11-12), 920–928 (2013), doi:.
[Crossref] [PubMed]

Donaldson, L.

Duan, Y.

Duloquin, L.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[PubMed]

Fahrbach, F. O.

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[PubMed]

Faure, E.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[PubMed]

Ford, T. N.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[PubMed]

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).
[PubMed]

Gao, G.

Gmitro, A. F.

Gong, Z.

S. Pant, C. Li, Z. Gong, and N. Chen, “Line-scan focal modulation microscopy,” J. Biomed. Opt. 22(5), 50502 (2017).
[PubMed]

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).
[PubMed]

Gualda, E. J.

Gunther, S.

U. Krzic, S. Gunther, T. E. Saunders, S. J. Streichan, and L. Hufnagel, “Multiview light-sheet microscope for rapid in toto imaging,” Nat. Methods 9(7), 730–733 (2012).
[PubMed]

Gustafsson, M. G.

L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
[PubMed]

Haase, S.

L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
[PubMed]

Hanley, Q. S.

R. Heintzmann, V. Sarafis, P. Munroe, J. Nailon, Q. S. Hanley, and T. M. Jovin, “Resolution enhancement by subtraction of confocal signals taken at different pinhole sizes,” Micron 34(6-7), 293–300 (2003).
[PubMed]

Heintzmann, R.

R. Heintzmann, V. Sarafis, P. Munroe, J. Nailon, Q. S. Hanley, and T. M. Jovin, “Resolution enhancement by subtraction of confocal signals taken at different pinhole sizes,” Micron 34(6-7), 293–300 (2003).
[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]

Hombach, S.

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[PubMed]

Hopkins, M. F.

Hourtoule, C.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[PubMed]

Hufnagel, L.

U. Krzic, S. Gunther, T. E. Saunders, S. J. Streichan, and L. Hufnagel, “Multiview light-sheet microscope for rapid in toto imaging,” Nat. Methods 9(7), 730–733 (2012).
[PubMed]

Huisken, J.

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[PubMed]

B. Schmid, G. Shah, N. Scherf, M. Weber, K. Thierbach, C. P. Campos, I. Roeder, P. Aanstad, and J. Huisken, “High-speed panoramic light-sheet microscopy reveals global endodermal cell dynamics,” Nat. Commun. 4, 2207 (2013).
[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]

Jemielita, M.

M. Jemielita, M. J. Taormina, A. Delaurier, C. B. Kimmel, and R. Parthasarathy, “Comparing phototoxicity during the development of a zebrafish craniofacial bone using confocal and light sheet fluorescence microscopy techniques,” J. Biophotonics 6(11-12), 920–928 (2013), doi:.
[Crossref] [PubMed]

Jovin, T. M.

R. Heintzmann, V. Sarafis, P. Munroe, J. Nailon, Q. S. Hanley, and T. M. Jovin, “Resolution enhancement by subtraction of confocal signals taken at different pinhole sizes,” Micron 34(6-7), 293–300 (2003).
[PubMed]

Keller, P. J.

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nature Methods 10, 413 (2013).

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).
[PubMed]

Kimmel, C. B.

M. Jemielita, M. J. Taormina, A. Delaurier, C. B. Kimmel, and R. Parthasarathy, “Comparing phototoxicity during the development of a zebrafish craniofacial bone using confocal and light sheet fluorescence microscopy techniques,” J. Biophotonics 6(11-12), 920–928 (2013), doi:.
[Crossref] [PubMed]

Kner, P.

L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
[PubMed]

Koos, D. S.

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).
[PubMed]

Krzic, U.

U. Krzic, S. Gunther, T. E. Saunders, S. J. Streichan, and L. Hufnagel, “Multiview light-sheet microscope for rapid in toto imaging,” Nat. Methods 9(7), 730–733 (2012).
[PubMed]

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]

Lawson, K. L.

C. Mosimann, A. C. Puller, K. L. Lawson, P. Tschopp, A. Amsterdam, and L. I. Zon, “Site-directed zebrafish transgenesis into single landing sites with the phiC31 integrase system,” Dev. Dyn. 242(8), 949–963 (2013).
[PubMed]

Leonhardt, H.

L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
[PubMed]

Li, C.

S. Pant, C. Li, Z. Gong, and N. Chen, “Line-scan focal modulation microscopy,” J. Biomed. Opt. 22(5), 50502 (2017).
[PubMed]

Li, J. M.

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nature Methods 10, 413 (2013).

Licea-Rodriguez, J.

Lim, D.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[PubMed]

Loza-Alvarez, P.

Luengo-Oroz, M. A.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[PubMed]

Mann, R. S.

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]

Mao, X. Q.

C. J. R. Sheppard and X. Q. Mao, “Confocal microscopes with slit apertures,” J. Mod. Opt. 35, 1169–1185 (1988).

Mayer, J.

Mendes, C. S.

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]

Mertz, J.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[PubMed]

Mickoleit, M.

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[PubMed]

Mosimann, C.

C. Mosimann, A. C. Puller, K. L. Lawson, P. Tschopp, A. Amsterdam, and L. I. Zon, “Site-directed zebrafish transgenesis into single landing sites with the phiC31 integrase system,” Dev. Dyn. 242(8), 949–963 (2013).
[PubMed]

Munroe, P.

R. Heintzmann, V. Sarafis, P. Munroe, J. Nailon, Q. S. Hanley, and T. M. Jovin, “Resolution enhancement by subtraction of confocal signals taken at different pinhole sizes,” Micron 34(6-7), 293–300 (2003).
[PubMed]

Nailon, J.

R. Heintzmann, V. Sarafis, P. Munroe, J. Nailon, Q. S. Hanley, and T. M. Jovin, “Resolution enhancement by subtraction of confocal signals taken at different pinhole sizes,” Micron 34(6-7), 293–300 (2003).
[PubMed]

Olarte, O. E.

Olivier, N.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[PubMed]

Orger, M. B.

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nature Methods 10, 413 (2013).

Palero, J. A.

Pant, S.

S. Pant, C. Li, Z. Gong, and N. Chen, “Line-scan focal modulation microscopy,” J. Biomed. Opt. 22(5), 50502 (2017).
[PubMed]

Parthasarathy, R.

M. Jemielita, M. J. Taormina, A. Delaurier, C. B. Kimmel, and R. Parthasarathy, “Comparing phototoxicity during the development of a zebrafish craniofacial bone using confocal and light sheet fluorescence microscopy techniques,” J. Biophotonics 6(11-12), 920–928 (2013), doi:.
[Crossref] [PubMed]

Peyriéras, N.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[PubMed]

Puller, A. C.

C. Mosimann, A. C. Puller, K. L. Lawson, P. Tschopp, A. Amsterdam, and L. I. Zon, “Site-directed zebrafish transgenesis into single landing sites with the phiC31 integrase system,” Dev. Dyn. 242(8), 949–963 (2013).
[PubMed]

Rangel-Rojo, R.

Rehman, S.

Reischauer, S.

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[PubMed]

Robson, D. N.

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nature Methods 10, 413 (2013).

Rocha-Mendoza, I.

Roeder, I.

B. Schmid, G. Shah, N. Scherf, M. Weber, K. Thierbach, C. P. Campos, I. Roeder, P. Aanstad, and J. Huisken, “High-speed panoramic light-sheet microscopy reveals global endodermal cell dynamics,” Nat. Commun. 4, 2207 (2013).
[PubMed]

Rouse, A. R.

Sabharwal, Y. S.

Santos, A.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[PubMed]

Santos, S.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[PubMed]

Sarafis, V.

R. Heintzmann, V. Sarafis, P. Munroe, J. Nailon, Q. S. Hanley, and T. M. Jovin, “Resolution enhancement by subtraction of confocal signals taken at different pinhole sizes,” Micron 34(6-7), 293–300 (2003).
[PubMed]

Saunders, T. E.

U. Krzic, S. Gunther, T. E. Saunders, S. J. Streichan, and L. Hufnagel, “Multiview light-sheet microscope for rapid in toto imaging,” Nat. Methods 9(7), 730–733 (2012).
[PubMed]

Savy, T.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[PubMed]

Scherf, N.

B. Schmid, G. Shah, N. Scherf, M. Weber, K. Thierbach, C. P. Campos, I. Roeder, P. Aanstad, and J. Huisken, “High-speed panoramic light-sheet microscopy reveals global endodermal cell dynamics,” Nat. Commun. 4, 2207 (2013).
[PubMed]

Schermelleh, L.

L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
[PubMed]

Schmid, B.

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[PubMed]

B. Schmid, G. Shah, N. Scherf, M. Weber, K. Thierbach, C. P. Campos, I. Roeder, P. Aanstad, and J. Huisken, “High-speed panoramic light-sheet microscopy reveals global endodermal cell dynamics,” Nat. Commun. 4, 2207 (2013).
[PubMed]

Schmidt, A. D.

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).
[PubMed]

Sedat, J. W.

L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
[PubMed]

Shah, G.

B. Schmid, G. Shah, N. Scherf, M. Weber, K. Thierbach, C. P. Campos, I. Roeder, P. Aanstad, and J. Huisken, “High-speed panoramic light-sheet microscopy reveals global endodermal cell dynamics,” Nat. Commun. 4, 2207 (2013).
[PubMed]

Shao, L.

L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
[PubMed]

Sharpe, J.

Sheppard, C. J.

Sheppard, C. J. R.

Singh, S. K.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[PubMed]

Solinas, X.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[PubMed]

Stelzer, E. H. K.

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).
[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]

Streichan, S. J.

U. Krzic, S. Gunther, T. E. Saunders, S. J. Streichan, and L. Hufnagel, “Multiview light-sheet microscope for rapid in toto imaging,” Nat. Methods 9(7), 730–733 (2012).
[PubMed]

Supatto, W.

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).
[PubMed]

Swoger, J.

Taormina, M. J.

M. Jemielita, M. J. Taormina, A. Delaurier, C. B. Kimmel, and R. Parthasarathy, “Comparing phototoxicity during the development of a zebrafish craniofacial bone using confocal and light sheet fluorescence microscopy techniques,” J. Biophotonics 6(11-12), 920–928 (2013), doi:.
[Crossref] [PubMed]

Thierbach, K.

B. Schmid, G. Shah, N. Scherf, M. Weber, K. Thierbach, C. P. Campos, I. Roeder, P. Aanstad, and J. Huisken, “High-speed panoramic light-sheet microscopy reveals global endodermal cell dynamics,” Nat. Commun. 4, 2207 (2013).
[PubMed]

Truong, T. V.

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).
[PubMed]

Tschopp, P.

C. Mosimann, A. C. Puller, K. L. Lawson, P. Tschopp, A. Amsterdam, and L. I. Zon, “Site-directed zebrafish transgenesis into single landing sites with the phiC31 integrase system,” Dev. Dyn. 242(8), 949–963 (2013).
[PubMed]

Veilleux, I.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[PubMed]

Voleti, V.

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]

Weber, M.

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[PubMed]

B. Schmid, G. Shah, N. Scherf, M. Weber, K. Thierbach, C. P. Campos, I. Roeder, P. Aanstad, and J. Huisken, “High-speed panoramic light-sheet microscopy reveals global endodermal cell dynamics,” Nat. Commun. 4, 2207 (2013).
[PubMed]

Winoto, L.

L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
[PubMed]

Wittbrodt, J.

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).
[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]

Wong, C. H.

Wong, C.-H.

Wong, K. F.

Zon, L. I.

C. Mosimann, A. C. Puller, K. L. Lawson, P. Tschopp, A. Amsterdam, and L. I. Zon, “Site-directed zebrafish transgenesis into single landing sites with the phiC31 integrase system,” Dev. Dyn. 242(8), 949–963 (2013).
[PubMed]

Appl. Opt. (2)

Biomed. Opt. Express (2)

Dev. Dyn. (1)

C. Mosimann, A. C. Puller, K. L. Lawson, P. Tschopp, A. Amsterdam, and L. I. Zon, “Site-directed zebrafish transgenesis into single landing sites with the phiC31 integrase system,” Dev. Dyn. 242(8), 949–963 (2013).
[PubMed]

J. Biomed. Opt. (2)

S. Pant, C. Li, Z. Gong, and N. Chen, “Line-scan focal modulation microscopy,” J. Biomed. Opt. 22(5), 50502 (2017).
[PubMed]

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[PubMed]

J. Biophotonics (1)

M. Jemielita, M. J. Taormina, A. Delaurier, C. B. Kimmel, and R. Parthasarathy, “Comparing phototoxicity during the development of a zebrafish craniofacial bone using confocal and light sheet fluorescence microscopy techniques,” J. Biophotonics 6(11-12), 920–928 (2013), doi:.
[Crossref] [PubMed]

J. Mod. Opt. (1)

C. J. R. Sheppard and X. Q. Mao, “Confocal microscopes with slit apertures,” J. Mod. Opt. 35, 1169–1185 (1988).

J. Opt. Soc. Am. A (1)

Micron (1)

R. Heintzmann, V. Sarafis, P. Munroe, J. Nailon, Q. S. Hanley, and T. M. Jovin, “Resolution enhancement by subtraction of confocal signals taken at different pinhole sizes,” Micron 34(6-7), 293–300 (2003).
[PubMed]

Nat. Commun. (1)

B. Schmid, G. Shah, N. Scherf, M. Weber, K. Thierbach, C. P. Campos, I. Roeder, P. Aanstad, and J. Huisken, “High-speed panoramic light-sheet microscopy reveals global endodermal cell dynamics,” Nat. Commun. 4, 2207 (2013).
[PubMed]

Nat. Methods (3)

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).
[PubMed]

U. Krzic, S. Gunther, T. E. Saunders, S. J. Streichan, and L. Hufnagel, “Multiview light-sheet microscope for rapid in toto imaging,” Nat. Methods 9(7), 730–733 (2012).
[PubMed]

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[PubMed]

Nat. Photonics (1)

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]

Nature Methods (1)

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nature Methods 10, 413 (2013).

Opt. Express (2)

Opt. Lett. (3)

Science (4)

L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
[PubMed]

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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Supplementary Material (5)

NameDescription
» Visualization 1       2D SPIM image sequence of zebrafish heart acquired at 100 fps.
» Visualization 2       2D aLSFMM image sequence of zebrafish heart acquired at 100 fps.
» Visualization 3       3D image rendering based on ImageJ 3D Viewer
» Visualization 4       3D image rendering based on ImageJ 3D projection.
» Visualization 5       3D visualization of a beating zebrafish heart based on 3D projection.

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Figures (5)

Fig. 1
Fig. 1

LSFMM design. (a) Schematic of an LSFMM system. EOM: electro optic phase modulator, whose fast axis is either vertically or horizontally oriented; SP: spatial polarizer; PA: polarization analyzer; G1 and G2: synchronized galvanometer mirrors; CL: cylindrical lens; BS: beam splitter (10/90); L1, L2, L3: lenses; LP1, LP2: lens pairs; EF: emission filter. (b) Polarizing optics. The spatial polarizer (SP) consists of four zones of alternating horizontal and vertical polarization directions. It is followed by the polarization analyzer (PA) with a polarization direction at 45°, parallel to the polarization of the collimated laser beam entering the EOM.

Fig. 2
Fig. 2

aLSFMM image formation process. (a) A raw image obtained from a 3 dpf zebrafish. The zoomed-in picture (inset) clearly shows intensity modulation along the horizontal direction. (b) LSCM image and (c) LSFMM image were retrieved from the same raw image. (d) The aLSFMM image that combines information from (b) and (c).

Fig. 3
Fig. 3

Image quality comparison. (a) Ventricle and atrium of a 13 dpf zebrafish larva visualized with a SPIM system. (b) aLSFMM heart image of another 13 dpf zebrafish larva. (c) Intensity profile along the yellow line in (a). (d) Intensity profile along the yellow line in (b).

Fig. 4
Fig. 4

3D image rendering. (a), (b), and (c), 3D zebrafish heart visualized with ImageJ 3D viewer. (d), (e), and (f), ImageJ 3D projections of the same 3D model.

Fig. 5
Fig. 5

Montage of a beating zebrafish heart based on 3D projection.

Equations (2)

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A=L( F ς )+H( C )
L+H=I

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