Abstract

Studying dynamic biological processes, such as heart development and function in zebrafish embryos, often relies on multi-channel fluorescence labeling to distinguish multiple anatomical features, yet also demands high frame rates to capture rapid cell motions. Although a recently proposed method for imaging dynamic samples in transmission or reflection allows to conveniently switch between color imaging or boosting the frame rate by use of spectrally-encoded, temporally-modulated illumination sequences and a hue-encoded shutter (hue-encode shutter method, HESM), the technique is not applicable directly in fluorescence microscopy, where the emitted light spectrum is mostly independent of the excitation wavelength. In this paper, we extend HESM by using samples labeled with multiple fluorophores, whose emission signal can either be used to distinguish multiple anatomical features when imaged in multi-channel mode or, if the fluorophores are co-localized in a dynamic tissue, to increase the frame rate via HESM. We detail the necessary steps to implement this method in a two-color light-sheet microscope to image the beating heart of a zebrafish embryo. Specifically, we propose an adapted laser modulation scheme for illumination, we identify caveats in choosing a suitable multi-color fluorophore labeling strategy, and derive an ℓ1-regularized reconstruction technique that is sufficiently robust to handle the low signal-to-noise ratio and labeling inhomogeneities in the fluorescence images at hand. Using the case of a beating heart in a zebrafish embryo, we experimentally show an increase in the frame rate by a factor two while preserving the ability to image static features labeled in distinct channels, thereby demonstrating the applicability of HESM to fluorescence. With a suitable illumination setup and fluorescent labeling, the method could generalize to other applications where flexibility between multiple channel and high-speed fluorescence imaging is desirable. For fluorophores that are not co-localized, the imaging system is similar to a conventional light sheet microscope.

© 2020 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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  33. Y. A. Pan, T. Freundlich, T. A. Weissman, D. Schoppik, X. C. Wang, S. Zimmerman, B. Ciruna, J. R. Sanes, J. W. Lichtman, and A. F. Schier, “Zebrabow: multispectral cell labeling for cell tracing and lineage analysis in zebrafish,” Development 140(13), 2835–2846 (2013).
    [Crossref]
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    [Crossref]
  35. M. Liebling, J. Vermot, A. S. Forouhar, M. Gharib, M. E. Dickinson, and S. E. Fraser, “Nonuniform temporal alignment of slice sequences for four-dimensional imaging of cyclically deforming embryonic structures,” Proc. IEEE Int. Symp. Biomed. Imag. pp. 1156–1159 (2006).
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    [Crossref]
  37. J. Ohn, J. Yang, S. E. Fraser, R. Lansford, and M. Liebling, “High-speed multicolor microscopy of repeating dynamic processes,” Genesis 49(7), 514–521 (2011).
    [Crossref]
  38. C. Jaques, L. Bapst-Wicht, D. F. Schorderet, and M. Liebling, “Multi-spectral widefield microscopy of the beating heart through post-acquisition synchronization and unmixing,” in 2019 IEEE 16th International Symposium on Biomedical Imaging (ISBI 2019), (2019), pp. 1382–1385.

2019 (4)

C. Jaques, E. Pignat, S. Calinon, and M. Liebling, “Temporal Super-Resolution Microscopy Using a Hue-Encoded Shutter,” Biomed. Opt. Express 10(9), 4727–4741 (2019).
[Crossref]

N. Wagner, N. Norlin, J. Gierten, G. de Medeiros, B. Balázs, J. Wittbrodt, L. Hufnagel, and R. Prevedel, “Instantaneous isotropic volumetric imaging of fast biological processes,” Nat. Methods 16(6), 497–500 (2019).
[Crossref]

S. Dillavou, S. M. Rubinstein, and J. M. Kolinski, “The virtual frame technique: ultrafast imaging with any camera,” Opt. Express 27(6), 8112–8120 (2019).
[Crossref]

Y. Wan, K. McDole, and P. J. Keller, “Light-sheet microscopy and its potential for understanding developmental processes,” Annu. Rev. Cell Dev. Biol. 35(1), 655–681 (2019). PMID: 31299171.
[Crossref]

2016 (1)

K. G. Chan, S. J. Streichan, L. A. Trinh, and M. Liebling, “Simultaneous temporal superresolution and denoising for cardiac fluorescence microscopy,” IEEE Trans. Comput. Imaging 2(3), 348–358 (2016).
[Crossref]

2015 (2)

2013 (4)

P. Llull, X. Liao, X. Yuan, J. Yang, D. Kittle, L. Carin, G. Sapiro, and D. J. Brady, “Coded aperture compressive temporal imaging,” Opt. Express 21(9), 10526 (2013).
[Crossref]

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]

Y. A. Pan, T. Freundlich, T. A. Weissman, D. Schoppik, X. C. Wang, S. Zimmerman, B. Ciruna, J. R. Sanes, J. W. Lichtman, and A. F. Schier, “Zebrabow: multispectral cell labeling for cell tracing and lineage analysis in zebrafish,” Development 140(13), 2835–2846 (2013).
[Crossref]

S. S. Gorthi, D. Schaak, and E. Schonbrun, “Fluorescence imaging of flowing cells using a temporally coded excitation,” Opt. Express 21(4), 5164–5170 (2013).
[Crossref]

2011 (2)

J. Ohn, J. Yang, S. E. Fraser, R. Lansford, and M. Liebling, “High-speed multicolor microscopy of repeating dynamic processes,” Genesis 49(7), 514–521 (2011).
[Crossref]

A. Veeraraghavan, D. Reddy, and R. Raskar, “Coded strobing photography: Compressive sensing of high speed periodic videos,” IEEE Trans. Pattern Anal. Mach. Intell. 33(4), 671–686 (2011).
[Crossref]

2010 (2)

G. Bub, M. Tecza, M. Helmes, P. Lee, and P. Kohl, “Temporal pixel multiplexing for simultaneous high-speed, high-resolution imaging.,” Nat. Methods 7(3), 209–211 (2010).
[Crossref]

S. Boyd, N. Parikh, E. Chu, B. Peleato, and J. Eckstein, “Distributed optimization and statistical learning via the alternating direction method of multipliers,” Found. Trends Mach. Learn. 3(1), 1–122 (2010).
[Crossref]

2009 (2)

A. Beck and M. Teboulle, “A fast iterative shrinkage-thresholding algorithm for linear inverse problems,” SIAM J. Imaging Sci. 2(1), 183–202 (2009).
[Crossref]

M. Liebling and H. Ranganathan, “Wavelet domain mutual information synchronization of multimodal cardiac microscopy image sequences,” Proc. SPIE 7446, 744602 (2009).
[Crossref]

2008 (1)

J. Vermot, S. E. Fraser, and M. Liebling, “Fast fluorescence microscopy for imaging the dynamics of embryonic development,” HFSP J. 2(3), 143–155 (2008).
[Crossref]

2006 (1)

R. Raskar, A. Agrawal, and J. Tumblin, “Coded exposure photography: Motion deblurring using fluttered shutter,” ACM Trans. Graph. 25(3), 795–804 (2006).
[Crossref]

2005 (2)

M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy: Wide-field fluorescence imaging with theoretically unlimited resolution,” Proc. Natl. Acad. Sci. 102(37), 13081–13086 (2005).
[Crossref]

N. C. Shaner, P. A. Steinbach, and R. Y. Tsien, “A guide to choosing fluorescent proteins,” Nat. Methods 2(12), 905–909 (2005).
[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]

2002 (1)

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]

1998 (1)

P. J. Verveer, Q. S. Hanley, P. W. Verbeek, L. J. Van Vliet, and T. M. Jovin, “Theory of confocal fluorescence imaging in the programmable array microscope (pam),” J. Microsc. 189(3), 192–198 (1998).
[Crossref]

1996 (1)

R. Tibshirani, “Regression shrinkage and selection via the lasso,” J. Royal Stat. Soc. Ser. B 58(1), 267–288 (1996).
[Crossref]

1992 (2)

P. C. Hansen, “Analysis of discrete ill-posed problems by means of the l-curve,” SIAM Rev. 34(4), 561–580 (1992).
[Crossref]

L. I. Rudin, S. Osher, and E. Fatemi, “Nonlinear total variation based noise removal algorithms,” Phys. D 60(1-4), 259–268 (1992).
[Crossref]

1967 (1)

1966 (1)

1893 (1)

A. Koehler, “Ein neues Beleuchtungsverfahren für mikrophotographische Zwecke,” Zeitschrift für wissenschaftliche Mikroskopie und für Mikroskopische Technik 10, 433–440 (1893).

Agrawal, A.

R. Raskar, A. Agrawal, and J. Tumblin, “Coded exposure photography: Motion deblurring using fluttered shutter,” ACM Trans. Graph. 25(3), 795–804 (2006).
[Crossref]

Baker, H.

J. Marguier, N. Bhatti, H. Baker, M. Harville, and S. Süsstrunk, “Color correction of uncalibrated images for the classification of human skin color,” Proceedings of the 15th IS&T/SID Color Imaging Conference pp. 331–335 (2007).

Balázs, B.

N. Wagner, N. Norlin, J. Gierten, G. de Medeiros, B. Balázs, J. Wittbrodt, L. Hufnagel, and R. Prevedel, “Instantaneous isotropic volumetric imaging of fast biological processes,” Nat. Methods 16(6), 497–500 (2019).
[Crossref]

Bapst-Wicht, L.

C. Jaques, L. Bapst-Wicht, D. F. Schorderet, and M. Liebling, “Multi-spectral widefield microscopy of the beating heart through post-acquisition synchronization and unmixing,” in 2019 IEEE 16th International Symposium on Biomedical Imaging (ISBI 2019), (2019), pp. 1382–1385.

Beck, A.

A. Beck and M. Teboulle, “A fast iterative shrinkage-thresholding algorithm for linear inverse problems,” SIAM J. Imaging Sci. 2(1), 183–202 (2009).
[Crossref]

Bertsekas, D. P.

D. P. Bertsekas, Constrained Optimization and Lagrange Multiplier Methods (Academic Press, 1982).

Bhatti, N.

J. Marguier, N. Bhatti, H. Baker, M. Harville, and S. Süsstrunk, “Color correction of uncalibrated images for the classification of human skin color,” Proceedings of the 15th IS&T/SID Color Imaging Conference pp. 331–335 (2007).

Boyd, S.

S. Boyd, N. Parikh, E. Chu, B. Peleato, and J. Eckstein, “Distributed optimization and statistical learning via the alternating direction method of multipliers,” Found. Trends Mach. Learn. 3(1), 1–122 (2010).
[Crossref]

S. Boyd and L. Vandenberghe, Convex Optimization (Cambridge Press University, 2004).

Brady, D. J.

Bub, G.

G. Bub, M. Tecza, M. Helmes, P. Lee, and P. Kohl, “Temporal pixel multiplexing for simultaneous high-speed, high-resolution imaging.,” Nat. Methods 7(3), 209–211 (2010).
[Crossref]

Calinon, S.

Carin, L.

Chan, K. G.

K. G. Chan, S. J. Streichan, L. A. Trinh, and M. Liebling, “Simultaneous temporal superresolution and denoising for cardiac fluorescence microscopy,” IEEE Trans. Comput. Imaging 2(3), 348–358 (2016).
[Crossref]

Chu, E.

S. Boyd, N. Parikh, E. Chu, B. Peleato, and J. Eckstein, “Distributed optimization and statistical learning via the alternating direction method of multipliers,” Found. Trends Mach. Learn. 3(1), 1–122 (2010).
[Crossref]

Ciruna, B.

Y. A. Pan, T. Freundlich, T. A. Weissman, D. Schoppik, X. C. Wang, S. Zimmerman, B. Ciruna, J. R. Sanes, J. W. Lichtman, and A. F. Schier, “Zebrabow: multispectral cell labeling for cell tracing and lineage analysis in zebrafish,” Development 140(13), 2835–2846 (2013).
[Crossref]

Cossairt, O.

Cremer, C.

de Medeiros, G.

N. Wagner, N. Norlin, J. Gierten, G. de Medeiros, B. Balázs, J. Wittbrodt, L. Hufnagel, and R. Prevedel, “Instantaneous isotropic volumetric imaging of fast biological processes,” Nat. Methods 16(6), 497–500 (2019).
[Crossref]

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).
[Crossref]

Dickinson, M. E.

M. Liebling, J. Vermot, A. S. Forouhar, M. Gharib, M. E. Dickinson, and S. E. Fraser, “Nonuniform temporal alignment of slice sequences for four-dimensional imaging of cyclically deforming embryonic structures,” Proc. IEEE Int. Symp. Biomed. Imag. pp. 1156–1159 (2006).

Dillavou, S.

Eckstein, J.

S. Boyd, N. Parikh, E. Chu, B. Peleato, and J. Eckstein, “Distributed optimization and statistical learning via the alternating direction method of multipliers,” Found. Trends Mach. Learn. 3(1), 1–122 (2010).
[Crossref]

Eliceiri, K. W.

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]

Fatemi, E.

L. I. Rudin, S. Osher, and E. Fatemi, “Nonlinear total variation based noise removal algorithms,” Phys. D 60(1-4), 259–268 (1992).
[Crossref]

Forouhar, A. S.

M. Liebling, J. Vermot, A. S. Forouhar, M. Gharib, M. E. Dickinson, and S. E. Fraser, “Nonuniform temporal alignment of slice sequences for four-dimensional imaging of cyclically deforming embryonic structures,” Proc. IEEE Int. Symp. Biomed. Imag. pp. 1156–1159 (2006).

Fraser, S. E.

J. Ohn, J. Yang, S. E. Fraser, R. Lansford, and M. Liebling, “High-speed multicolor microscopy of repeating dynamic processes,” Genesis 49(7), 514–521 (2011).
[Crossref]

J. Vermot, S. E. Fraser, and M. Liebling, “Fast fluorescence microscopy for imaging the dynamics of embryonic development,” HFSP J. 2(3), 143–155 (2008).
[Crossref]

M. Liebling, J. Vermot, A. S. Forouhar, M. Gharib, M. E. Dickinson, and S. E. Fraser, “Nonuniform temporal alignment of slice sequences for four-dimensional imaging of cyclically deforming embryonic structures,” Proc. IEEE Int. Symp. Biomed. Imag. pp. 1156–1159 (2006).

Freundlich, T.

Y. A. Pan, T. Freundlich, T. A. Weissman, D. Schoppik, X. C. Wang, S. Zimmerman, B. Ciruna, J. R. Sanes, J. W. Lichtman, and A. F. Schier, “Zebrabow: multispectral cell labeling for cell tracing and lineage analysis in zebrafish,” Development 140(13), 2835–2846 (2013).
[Crossref]

Gharib, M.

M. Liebling, J. Vermot, A. S. Forouhar, M. Gharib, M. E. Dickinson, and S. E. Fraser, “Nonuniform temporal alignment of slice sequences for four-dimensional imaging of cyclically deforming embryonic structures,” Proc. IEEE Int. Symp. Biomed. Imag. pp. 1156–1159 (2006).

Gierten, J.

N. Wagner, N. Norlin, J. Gierten, G. de Medeiros, B. Balázs, J. Wittbrodt, L. Hufnagel, and R. Prevedel, “Instantaneous isotropic volumetric imaging of fast biological processes,” Nat. Methods 16(6), 497–500 (2019).
[Crossref]

Gorthi, S. S.

Gustafsson, M. G. L.

M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy: Wide-field fluorescence imaging with theoretically unlimited resolution,” Proc. Natl. Acad. Sci. 102(37), 13081–13086 (2005).
[Crossref]

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]

Hanley, Q. S.

P. J. Verveer, Q. S. Hanley, P. W. Verbeek, L. J. Van Vliet, and T. M. Jovin, “Theory of confocal fluorescence imaging in the programmable array microscope (pam),” J. Microsc. 189(3), 192–198 (1998).
[Crossref]

Hansen, P. C.

P. C. Hansen, “Analysis of discrete ill-posed problems by means of the l-curve,” SIAM Rev. 34(4), 561–580 (1992).
[Crossref]

P. C. Hansen, Discrete inverse problems: insight and algorithms, vol. 7 (Siam, 2010).

Harville, M.

J. Marguier, N. Bhatti, H. Baker, M. Harville, and S. Süsstrunk, “Color correction of uncalibrated images for the classification of human skin color,” Proceedings of the 15th IS&T/SID Color Imaging Conference pp. 331–335 (2007).

Heintzmann, R.

Helmes, M.

G. Bub, M. Tecza, M. Helmes, P. Lee, and P. Kohl, “Temporal pixel multiplexing for simultaneous high-speed, high-resolution imaging.,” Nat. Methods 7(3), 209–211 (2010).
[Crossref]

Hufnagel, L.

N. Wagner, N. Norlin, J. Gierten, G. de Medeiros, B. Balázs, J. Wittbrodt, L. Hufnagel, and R. Prevedel, “Instantaneous isotropic volumetric imaging of fast biological processes,” Nat. Methods 16(6), 497–500 (2019).
[Crossref]

Huisken, J.

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]

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]

Jaques, C.

C. Jaques, E. Pignat, S. Calinon, and M. Liebling, “Temporal Super-Resolution Microscopy Using a Hue-Encoded Shutter,” Biomed. Opt. Express 10(9), 4727–4741 (2019).
[Crossref]

C. Jaques, “Hue-encoded shutter method code,” https://github.com/idiap/hesm_distrib (2019).

C. Jaques, L. Bapst-Wicht, D. F. Schorderet, and M. Liebling, “Multi-spectral widefield microscopy of the beating heart through post-acquisition synchronization and unmixing,” in 2019 IEEE 16th International Symposium on Biomedical Imaging (ISBI 2019), (2019), pp. 1382–1385.

Jovin, T. M.

R. Heintzmann, T. M. Jovin, and C. Cremer, “Saturated patterned excitation microscopy—a concept for optical resolution improvement,” J. Opt. Soc. Am. A 19(8), 1599–1609 (2002).
[Crossref]

P. J. Verveer, Q. S. Hanley, P. W. Verbeek, L. J. Van Vliet, and T. M. Jovin, “Theory of confocal fluorescence imaging in the programmable array microscope (pam),” J. Microsc. 189(3), 192–198 (1998).
[Crossref]

Katsaggelos, A. K.

Keller, P. J.

Y. Wan, K. McDole, and P. J. Keller, “Light-sheet microscopy and its potential for understanding developmental processes,” Annu. Rev. Cell Dev. Biol. 35(1), 655–681 (2019). PMID: 31299171.
[Crossref]

Kittle, D.

Koehler, A.

A. Koehler, “Ein neues Beleuchtungsverfahren für mikrophotographische Zwecke,” Zeitschrift für wissenschaftliche Mikroskopie und für Mikroskopische Technik 10, 433–440 (1893).

Kohl, P.

G. Bub, M. Tecza, M. Helmes, P. Lee, and P. Kohl, “Temporal pixel multiplexing for simultaneous high-speed, high-resolution imaging.,” Nat. Methods 7(3), 209–211 (2010).
[Crossref]

Kolinski, J. M.

Koller, R.

Lansford, R.

J. Ohn, J. Yang, S. E. Fraser, R. Lansford, and M. Liebling, “High-speed multicolor microscopy of repeating dynamic processes,” Genesis 49(7), 514–521 (2011).
[Crossref]

Lee, P.

G. Bub, M. Tecza, M. Helmes, P. Lee, and P. Kohl, “Temporal pixel multiplexing for simultaneous high-speed, high-resolution imaging.,” Nat. Methods 7(3), 209–211 (2010).
[Crossref]

Liao, X.

Lichtman, J. W.

Y. A. Pan, T. Freundlich, T. A. Weissman, D. Schoppik, X. C. Wang, S. Zimmerman, B. Ciruna, J. R. Sanes, J. W. Lichtman, and A. F. Schier, “Zebrabow: multispectral cell labeling for cell tracing and lineage analysis in zebrafish,” Development 140(13), 2835–2846 (2013).
[Crossref]

Liebling, M.

C. Jaques, E. Pignat, S. Calinon, and M. Liebling, “Temporal Super-Resolution Microscopy Using a Hue-Encoded Shutter,” Biomed. Opt. Express 10(9), 4727–4741 (2019).
[Crossref]

K. G. Chan, S. J. Streichan, L. A. Trinh, and M. Liebling, “Simultaneous temporal superresolution and denoising for cardiac fluorescence microscopy,” IEEE Trans. Comput. Imaging 2(3), 348–358 (2016).
[Crossref]

J. Ohn, J. Yang, S. E. Fraser, R. Lansford, and M. Liebling, “High-speed multicolor microscopy of repeating dynamic processes,” Genesis 49(7), 514–521 (2011).
[Crossref]

M. Liebling and H. Ranganathan, “Wavelet domain mutual information synchronization of multimodal cardiac microscopy image sequences,” Proc. SPIE 7446, 744602 (2009).
[Crossref]

J. Vermot, S. E. Fraser, and M. Liebling, “Fast fluorescence microscopy for imaging the dynamics of embryonic development,” HFSP J. 2(3), 143–155 (2008).
[Crossref]

C. Jaques, L. Bapst-Wicht, D. F. Schorderet, and M. Liebling, “Multi-spectral widefield microscopy of the beating heart through post-acquisition synchronization and unmixing,” in 2019 IEEE 16th International Symposium on Biomedical Imaging (ISBI 2019), (2019), pp. 1382–1385.

M. Liebling, J. Vermot, A. S. Forouhar, M. Gharib, M. E. Dickinson, and S. E. Fraser, “Nonuniform temporal alignment of slice sequences for four-dimensional imaging of cyclically deforming embryonic structures,” Proc. IEEE Int. Symp. Biomed. Imag. pp. 1156–1159 (2006).

Llull, P.

Lukosz, W.

Marguier, J.

J. Marguier, N. Bhatti, H. Baker, M. Harville, and S. Süsstrunk, “Color correction of uncalibrated images for the classification of human skin color,” Proceedings of the 15th IS&T/SID Color Imaging Conference pp. 331–335 (2007).

Matsuda, N.

McDole, K.

Y. Wan, K. McDole, and P. J. Keller, “Light-sheet microscopy and its potential for understanding developmental processes,” Annu. Rev. Cell Dev. Biol. 35(1), 655–681 (2019). PMID: 31299171.
[Crossref]

Niederberger, T.

Norlin, N.

N. Wagner, N. Norlin, J. Gierten, G. de Medeiros, B. Balázs, J. Wittbrodt, L. Hufnagel, and R. Prevedel, “Instantaneous isotropic volumetric imaging of fast biological processes,” Nat. Methods 16(6), 497–500 (2019).
[Crossref]

Ohn, J.

J. Ohn, J. Yang, S. E. Fraser, R. Lansford, and M. Liebling, “High-speed multicolor microscopy of repeating dynamic processes,” Genesis 49(7), 514–521 (2011).
[Crossref]

Osher, S.

L. I. Rudin, S. Osher, and E. Fatemi, “Nonlinear total variation based noise removal algorithms,” Phys. D 60(1-4), 259–268 (1992).
[Crossref]

Pan, Y. A.

Y. A. Pan, T. Freundlich, T. A. Weissman, D. Schoppik, X. C. Wang, S. Zimmerman, B. Ciruna, J. R. Sanes, J. W. Lichtman, and A. F. Schier, “Zebrabow: multispectral cell labeling for cell tracing and lineage analysis in zebrafish,” Development 140(13), 2835–2846 (2013).
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S. Boyd, N. Parikh, E. Chu, B. Peleato, and J. Eckstein, “Distributed optimization and statistical learning via the alternating direction method of multipliers,” Found. Trends Mach. Learn. 3(1), 1–122 (2010).
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Pitrone, P. G.

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[Crossref]

Preibisch, S.

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]

Prevedel, R.

N. Wagner, N. Norlin, J. Gierten, G. de Medeiros, B. Balázs, J. Wittbrodt, L. Hufnagel, and R. Prevedel, “Instantaneous isotropic volumetric imaging of fast biological processes,” Nat. Methods 16(6), 497–500 (2019).
[Crossref]

Ranganathan, H.

M. Liebling and H. Ranganathan, “Wavelet domain mutual information synchronization of multimodal cardiac microscopy image sequences,” Proc. SPIE 7446, 744602 (2009).
[Crossref]

Raskar, R.

A. Veeraraghavan, D. Reddy, and R. Raskar, “Coded strobing photography: Compressive sensing of high speed periodic videos,” IEEE Trans. Pattern Anal. Mach. Intell. 33(4), 671–686 (2011).
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R. Raskar, A. Agrawal, and J. Tumblin, “Coded exposure photography: Motion deblurring using fluttered shutter,” ACM Trans. Graph. 25(3), 795–804 (2006).
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A. Veeraraghavan, D. Reddy, and R. Raskar, “Coded strobing photography: Compressive sensing of high speed periodic videos,” IEEE Trans. Pattern Anal. Mach. Intell. 33(4), 671–686 (2011).
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Y. A. Pan, T. Freundlich, T. A. Weissman, D. Schoppik, X. C. Wang, S. Zimmerman, B. Ciruna, J. R. Sanes, J. W. Lichtman, and A. F. Schier, “Zebrabow: multispectral cell labeling for cell tracing and lineage analysis in zebrafish,” Development 140(13), 2835–2846 (2013).
[Crossref]

Sapiro, G.

Schaak, D.

Schier, A. F.

Y. A. Pan, T. Freundlich, T. A. Weissman, D. Schoppik, X. C. Wang, S. Zimmerman, B. Ciruna, J. R. Sanes, J. W. Lichtman, and A. F. Schier, “Zebrabow: multispectral cell labeling for cell tracing and lineage analysis in zebrafish,” Development 140(13), 2835–2846 (2013).
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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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Schonbrun, E.

Schoppik, D.

Y. A. Pan, T. Freundlich, T. A. Weissman, D. Schoppik, X. C. Wang, S. Zimmerman, B. Ciruna, J. R. Sanes, J. W. Lichtman, and A. F. Schier, “Zebrabow: multispectral cell labeling for cell tracing and lineage analysis in zebrafish,” Development 140(13), 2835–2846 (2013).
[Crossref]

Schorderet, D. F.

C. Jaques, L. Bapst-Wicht, D. F. Schorderet, and M. Liebling, “Multi-spectral widefield microscopy of the beating heart through post-acquisition synchronization and unmixing,” in 2019 IEEE 16th International Symposium on Biomedical Imaging (ISBI 2019), (2019), pp. 1382–1385.

Schuster, G.

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N. C. Shaner, P. A. Steinbach, and R. Y. Tsien, “A guide to choosing fluorescent proteins,” Nat. Methods 2(12), 905–909 (2005).
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Steinbach, P. A.

N. C. Shaner, P. A. Steinbach, and R. Y. Tsien, “A guide to choosing fluorescent proteins,” Nat. Methods 2(12), 905–909 (2005).
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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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K. G. Chan, S. J. Streichan, L. A. Trinh, and M. Liebling, “Simultaneous temporal superresolution and denoising for cardiac fluorescence microscopy,” IEEE Trans. Comput. Imaging 2(3), 348–358 (2016).
[Crossref]

Stuyvenberg, L.

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]

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J. Marguier, N. Bhatti, H. Baker, M. Harville, and S. Süsstrunk, “Color correction of uncalibrated images for the classification of human skin color,” Proceedings of the 15th IS&T/SID Color Imaging Conference pp. 331–335 (2007).

Swoger, J.

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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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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K. G. Chan, S. J. Streichan, L. A. Trinh, and M. Liebling, “Simultaneous temporal superresolution and denoising for cardiac fluorescence microscopy,” IEEE Trans. Comput. Imaging 2(3), 348–358 (2016).
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N. C. Shaner, P. A. Steinbach, and R. Y. Tsien, “A guide to choosing fluorescent proteins,” Nat. Methods 2(12), 905–909 (2005).
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R. Raskar, A. Agrawal, and J. Tumblin, “Coded exposure photography: Motion deblurring using fluttered shutter,” ACM Trans. Graph. 25(3), 795–804 (2006).
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J. Vermot, S. E. Fraser, and M. Liebling, “Fast fluorescence microscopy for imaging the dynamics of embryonic development,” HFSP J. 2(3), 143–155 (2008).
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M. Liebling, J. Vermot, A. S. Forouhar, M. Gharib, M. E. Dickinson, and S. E. Fraser, “Nonuniform temporal alignment of slice sequences for four-dimensional imaging of cyclically deforming embryonic structures,” Proc. IEEE Int. Symp. Biomed. Imag. pp. 1156–1159 (2006).

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P. J. Verveer, Q. S. Hanley, P. W. Verbeek, L. J. Van Vliet, and T. M. Jovin, “Theory of confocal fluorescence imaging in the programmable array microscope (pam),” J. Microsc. 189(3), 192–198 (1998).
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Y. Wan, K. McDole, and P. J. Keller, “Light-sheet microscopy and its potential for understanding developmental processes,” Annu. Rev. Cell Dev. Biol. 35(1), 655–681 (2019). PMID: 31299171.
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Y. A. Pan, T. Freundlich, T. A. Weissman, D. Schoppik, X. C. Wang, S. Zimmerman, B. Ciruna, J. R. Sanes, J. W. Lichtman, and A. F. Schier, “Zebrabow: multispectral cell labeling for cell tracing and lineage analysis in zebrafish,” Development 140(13), 2835–2846 (2013).
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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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Y. A. Pan, T. Freundlich, T. A. Weissman, D. Schoppik, X. C. Wang, S. Zimmerman, B. Ciruna, J. R. Sanes, J. W. Lichtman, and A. F. Schier, “Zebrabow: multispectral cell labeling for cell tracing and lineage analysis in zebrafish,” Development 140(13), 2835–2846 (2013).
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N. Wagner, N. Norlin, J. Gierten, G. de Medeiros, B. Balázs, J. Wittbrodt, L. Hufnagel, and R. Prevedel, “Instantaneous isotropic volumetric imaging of fast biological processes,” Nat. Methods 16(6), 497–500 (2019).
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Yuan, X.

Zimmerman, S.

Y. A. Pan, T. Freundlich, T. A. Weissman, D. Schoppik, X. C. Wang, S. Zimmerman, B. Ciruna, J. R. Sanes, J. W. Lichtman, and A. F. Schier, “Zebrabow: multispectral cell labeling for cell tracing and lineage analysis in zebrafish,” Development 140(13), 2835–2846 (2013).
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ACM Trans. Graph. (1)

R. Raskar, A. Agrawal, and J. Tumblin, “Coded exposure photography: Motion deblurring using fluttered shutter,” ACM Trans. Graph. 25(3), 795–804 (2006).
[Crossref]

Annu. Rev. Cell Dev. Biol. (1)

Y. Wan, K. McDole, and P. J. Keller, “Light-sheet microscopy and its potential for understanding developmental processes,” Annu. Rev. Cell Dev. Biol. 35(1), 655–681 (2019). PMID: 31299171.
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Biomed. Opt. Express (1)

Development (1)

Y. A. Pan, T. Freundlich, T. A. Weissman, D. Schoppik, X. C. Wang, S. Zimmerman, B. Ciruna, J. R. Sanes, J. W. Lichtman, and A. F. Schier, “Zebrabow: multispectral cell labeling for cell tracing and lineage analysis in zebrafish,” Development 140(13), 2835–2846 (2013).
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Found. Trends Mach. Learn. (1)

S. Boyd, N. Parikh, E. Chu, B. Peleato, and J. Eckstein, “Distributed optimization and statistical learning via the alternating direction method of multipliers,” Found. Trends Mach. Learn. 3(1), 1–122 (2010).
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Genesis (1)

J. Ohn, J. Yang, S. E. Fraser, R. Lansford, and M. Liebling, “High-speed multicolor microscopy of repeating dynamic processes,” Genesis 49(7), 514–521 (2011).
[Crossref]

HFSP J. (1)

J. Vermot, S. E. Fraser, and M. Liebling, “Fast fluorescence microscopy for imaging the dynamics of embryonic development,” HFSP J. 2(3), 143–155 (2008).
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IEEE Trans. Comput. Imaging (1)

K. G. Chan, S. J. Streichan, L. A. Trinh, and M. Liebling, “Simultaneous temporal superresolution and denoising for cardiac fluorescence microscopy,” IEEE Trans. Comput. Imaging 2(3), 348–358 (2016).
[Crossref]

IEEE Trans. Pattern Anal. Mach. Intell. (1)

A. Veeraraghavan, D. Reddy, and R. Raskar, “Coded strobing photography: Compressive sensing of high speed periodic videos,” IEEE Trans. Pattern Anal. Mach. Intell. 33(4), 671–686 (2011).
[Crossref]

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Nat. Methods (4)

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]

G. Bub, M. Tecza, M. Helmes, P. Lee, and P. Kohl, “Temporal pixel multiplexing for simultaneous high-speed, high-resolution imaging.,” Nat. Methods 7(3), 209–211 (2010).
[Crossref]

N. Wagner, N. Norlin, J. Gierten, G. de Medeiros, B. Balázs, J. Wittbrodt, L. Hufnagel, and R. Prevedel, “Instantaneous isotropic volumetric imaging of fast biological processes,” Nat. Methods 16(6), 497–500 (2019).
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[Crossref]

Opt. Express (4)

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Proc. SPIE (1)

M. Liebling and H. Ranganathan, “Wavelet domain mutual information synchronization of multimodal cardiac microscopy image sequences,” Proc. SPIE 7446, 744602 (2009).
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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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Supplementary Material (4)

NameDescription
» Visualization 1       This video shows hue-encoded data acquired (left) with the corresponding reconstructions next to them (right). The reconstructions have a double frame rate compared to the acquisitions, and are monochrome.
» Visualization 2       This video corresponds to Figure 4 in the paper. It shows hue-encoded acquisitions with the corresponding reconstructions applied in a region of interest (ROI).
» Visualization 3       This video corresponds to Figure 6 in the paper. It shows a comparison between unregularized least-squares (LSTSQ) and alternating direction method of multiplier (ADMM) reconstructions.
» Visualization 4       This video shows a 3D+time reconstruction of the beating heart of a zebrafish embryo. We acquired a z-stack of videos, using the method presented in the paper at each z-position to boost the imaging frame rate.

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Figures (6)

Fig. 1.
Fig. 1. Hue-encoded shutter for fluorescence light-sheet microscopy. (a) The excitation objective (EO) transmits consecutive pulses of different wavelengths within the exposure time $E$ of one frame. The sample ( $\boldsymbol{x}$ ) contains co-localized fluorophores (e.g. green and red fluorescent proteins) that respond to the excitation by emitting fluorescent light. The sample may also contain static regions that can be labeled with a single fluorophore type. The color sensor of the camera (CAM) captures the light emitted over the entire exposure time through the detection objective (DO). (b) Acquired (raw) multi-channel images (c) Our proposed method converts the color frames to multiple monochrome frames at a higher frame rate (here, by a factor 2) in a region of interest that contains dynamic features. The color information can be preserved in static regions outside of the region of interest.
Fig. 2.
Fig. 2. Fluo-HESM requires co-localized multi-color fluorescent labeling. (Top row) HESM [3] assumes a bright field microscopy setup, where the illumination light is transmitted through (or reflected by) a sample then captured by an RGB camera. The transmitted (or reflected) spectrum directly depends on the combination of the illumination spectrum and the sample’s spectral transmittance. HESM relies on using a temporally-variable spectrum in the illumination, which can be decoded following capture with an RGB camera. (Middle row) If using a single fluorophore and two different illumination sources (C and D), the emission from the sample only changes in overall intensity, but the shape of the emission spectrum remains unchanged. Hence, temporal modulation of the illumination spectrum would not univocally modulate the spectral shape of the emission and HESM could therefore not be used as-is to improve the frame-rate. (Bottom row) In this paper, we propose to use two light sources E and F and a sample labeled with two co-localized fluorophore species such that the combined emitted light spectrum is directly dependent on temporal modulation patterns of the illumination spectrum, making the use of HESM to improve the frame rate possible.
Fig. 3.
Fig. 3. Forward matrix $\boldsymbol{S\Gamma }$ combines temporal illuminations patterns of two lasers and the combined absorption and emission responses of the two fluorophores, together with the spectral response of the camera. Notice that the left part of the matrix $\boldsymbol{S}$ , boxed in green, contains repetitions of the temporal function of the green laser: $s_1[i]$ and the right part of $\boldsymbol{S}$ contains the same information for the blue laser. We also framed in green, respectively blue, the part that corresponds to the green, respectively blue, laser in the $\boldsymbol{\Gamma }$ matrix which expresses the efficiency of each fluorophore to the lasers combined with the sensitivity of the camera to the fluorescence emission spectra.
Fig. 4.
Fig. 4. Fluo-HESM allows simultaneous fast imaging of the beating heart and color imaging of its surroundings. (a),(e) two consecutive acquired frames. (b)-(d), respectively (f)-(h) are the red, green and blue layers of the image in (a), respectively (e). (i)-(l) reconstructed frames using Algorithm 1 with $\lambda =0.001$ . The super-resolution factor is 2, hence for two acquired frames, we observe 4 reconstructed frames. Note that there are 60 milliseconds between the two acquired frames (a) and (e) and 30 milliseconds between the super-resolved region in frames (i)-(l), framed in a white rectangle. Outside of this region, our method allows keeping the color information. On (j), we marked two regions with drastically different colors, green (osac-3-8-2195-i001) and orange ( $\clubsuit$ ). Standard imaging, in the presence of a single fluorophore species, would only produce frames (c) and (g), respectively (b) and (f) using samples labeled with only green fluorescent proteins, respectively only red fluorescent proteins. With Fluo-HESM, there are twice the number of these frames. This is also visible in Visualization 4, which shows a comparison between standard light-sheet data and reconstructions from our method in 3D+time. To highlight the link between this data and the schematic of Fig. 1, (a) and (e) on this figure correspond to Fig. 1(b) and (i)-(l) to Fig. 1(c). See Visualization 1 and Visualization 2 for the full movie. Fish orientation indicated: anterior (A), posterior (P), right (R) and left (L). Scale bar: 100 $\mu$ m.
Fig. 5.
Fig. 5. A static region is required to calibrate our method. The region must also have a similar red over green (R/G) ratio than in the heart. (a) Hue-encoded light-sheet image of a 2 days post-fertilization zebrafish heart. The ventricle (V), the atrium (At) and the pericardium (p) are outlined. (b) The ratio R/G of each pixel on the image in (a). Notice that the ratio R/G is not homogeneous over the whole image. In order to calibrate our method, we need a static region with the same ratio R/G as in the heart; it is shown in (d). (d’) shows the histogram of values within (d). Similarly, (c’) and (e’) show histograms of their corresponding regions (c) and (e). Notice that the calibration region (d) has a histogram similar to that of the heart (c), with a maximum centered around 1.5. Since Histogram (e’) is different from Histograms (c’) and (d’), our method would require an additional calibration to be usable in Area (e). Fish orientation indicated: anterior (A), posterior (P), right (R) and left (L). Scale bar: 100 $\mu$ m.
Fig. 6.
Fig. 6. Fluo-HESM is robust to fluorescence labeling inhomogeneities thanks to the temporal $\ell$ 1 regularization. (a)-(b) Composite color images and temporal super-resolution reconstructions. The dynamic area of the scene (c), with the beating heart, has been manually selected and inside of (c), the frame rate is twice that of outside. This illustrates the ability to choose between fast single hue imaging and slow color imaging. (d) Reconstructions at the location shown on (c) with a heart symbol (osac-3-8-2195-i001) using least-squares (without regularization, LSTSQ) or ADMM. The TV regularization we used in Eq. (9) favors piecewise constant reconstructions and preserves sharp edges. (e) Reconstructions at the location shown on (c) with a club symbol ( $\clubsuit$ ) using LSTSQ or ADMM. At this location, there is little motion of the sample, and the LSTSQ reconstructions oscillate a lot, while the ADMM reconstructions show little motion, justifying the use of ADMM over LSTSQ. Within (c), we assigned a hue to the reconstructed images, that we measured at calibration. Scale bar: 100 $\mu$ m. See Visualization 2 and additional Visualization 3 on a different sample.

Equations (9)

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y c , k = t k t k + E = 1 L f = 1 F γ c , f b f , s ( t ) x ( t ) d t + d c ,
x ( t ) = i Z x [ i ] β 0 ( ( t i ) Q ) ,
y c , k = d c + = 1 L f = 1 F γ c , f b f , t k t k + E s ( t ) i = 0 Q 1 x [ t k , i ] β 0 ( ( t E Q i ) Q ) d t = d c + = 1 L f = 1 F γ c , f b f , i = 0 Q 1 x [ t k , i ] t k + E Q i t k + E Q ( i + 1 ) s ( t ) d t s [ t k , i ] ,
y k = S Γ x k + d 0 ,
Γ = ( ( γ 1 , 1 b 1 , + γ 1 , 2 b 2 , ) I 2 ( γ 2 , 1 b 1 , + γ 2 , 2 b 2 , ) I 2 ( γ 3 , 1 b 1 , + γ 3 , 2 b 2 , ) I 2 ) ,
x k = arg min x k y k d 0 S Γ x k 2 2
x = arg min x 1 2 y d A x 2 2 + λ T x 1 ,
minimize  1 2 y d A x 2 2 + λ u 1 such that  T x = u ,
L ( x , u , y ) = y A x d 2 2 + λ u 1 + z ( T x u ) + ( ρ / 2 ) T x u 2 2 ,

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