Abstract

For decades, the confocal microscope has represented one of the dominant imaging systems in biomedical imaging at sub-cellular length scales. Recently, however, it has increasingly been replaced by a related, but more powerful successor technique termed image scanning microscopy (ISM). In this article, we present ISM capable of measuring spectroscopic information such as that contained in fluorescence or Raman images. Compared to established confocal spectroscopic imaging systems, our implementation offers similar spectral resolution, but higher spatial resolution and detection efficiency. Color sensitivity is achieved by a grating placed in the detection path in conjunction with a camera collecting both spatial and spectral information. The multidimensional data is processed using multi-view maximum likelihood image reconstruction. Our findings are supported by numerical simulations and experiments on micro beads and double-stained HeLa cells.

Published by The Optical Society under the terms of the Creative Commons Attribution 4.0 License. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

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2019 (1)

M. Castello, G. Tortarolo, M. Buttafava, T. Deguchi, F. Villa, S. Koho, L. Pesce, M. Oneto, S. Pelicci, L. Lanzanó, and P. Bianchini, “A robust and versatile platform for image scanning microscopy enabling super-resolution FLIM,” Nat. Meth. 16175–178 (2019).
[Crossref]

2018 (1)

J. N. Mait, G. W. Euliss, and R. A. Athale, “Computational imaging,” Advances in Optics and Photonics 10(2), 409–483 (2018).
[Crossref]

2017 (2)

I. Gregor, M. Spiecker, R. Petrovsky, J. Großhans, R. Ros, and J. Enderlein, “Rapid nonlinear image scanning microscopy,” Nat. Meth.,  14(11), 1087 (2017).
[Crossref]

C. Roider, R. Piestun, and A. Jesacher,“3D image scanning microscopy with engineered excitation and detection,” Optica 4(11), 1373–1381 (2017).
[Crossref]

2016 (3)

2015 (3)

2014 (4)

2013 (7)

A. Backer, M. Backlund, M. Lew, and W. Moerner, “Single-molecule orientation measurements with a quadrated pupil,” Opt. Lett. 38, 1521–1523 (2013).
[Crossref] [PubMed]

C. J. Sheppard, S. B. Mehta, and R. Heintzmann, “Superresolution by image scanning microscopy using pixel reassignment,” Opt. Lett. 38(15) 2889–2892 (2013).
[Crossref] [PubMed]

B. Redding, S. M. Popoff, and H. Cao, “All-fiber spectrometer based on speckle pattern reconstruction,” Opt. Express 21(5), 6584–6600 (2013).
[Crossref] [PubMed]

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, and J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” PNAS,  110(52), 21000–21005 (2013).
[Crossref] [PubMed]

S. Roth, C. J. R. Sheppard, K. Wicker, and R. Heintzmann, “Optical Photon Reassignment Microscopy,” Optical Nanoscopy 2(1), 5 (2013).
[Crossref]

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, and H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Meth. 10(11), 1122–1126 (2013).
[Crossref]

G. M. R. De Luca, R. M. P. Breedijk, R. A. J. Brandt, C. H. C. Zeelenberg, B. E. de Jong, W. Timmermans, L. N. Azar, R. A. Hoebe, S. Stallinga, and E. M. M. Manders, “Re-scan confocal microscopy: scanning twice for better resolution,”Biomed. Opt. Express 4(11), 2644–2656 (2013).
[Crossref] [PubMed]

2012 (3)

A. G. York, S. H. Parekh, D. Dalle Nogare, R. S. Fischer, K. Temprine, M. Mione, A. B. Chitnis, C. A. Combs, and H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Meth. 9(7), 749 (2012).
[Crossref]

D. Axelrod, “Fluorescence excitation and imaging of single molecules near dielectric-coated and bare surfaces: a theoretical study,” J. Microsc. 247(2), 147–160 (2012).
[Crossref] [PubMed]

M. P. Backlund, M. D. Lew, A. S. Backer, S. J. Sahl, G. Grover, A. Agrawal, R. Piestun, and W. E. Moerner, “Simultaneous, accurate measurement of the 3D position and orientation of single molecules,” Proc. Natl. Acad. Sci. USA 109, 19087 (2012).

2010 (1)

C. Müller and J. Enderlein, “Image Scanning Microscopy,” Phys. Rev. Lett. 104(19), 198101 (2010).
[Crossref] [PubMed]

2009 (1)

2006 (1)

A. Greengard, Y. Y. Schechner, and R. Piestun, “Depth from diffracted rotation,” Opt. Lett., 31(2), 181–183 (2006).
[Crossref] [PubMed]

2004 (1)

J. M. Lerner and R. M. Zucker, “Calibration and validation of confocal spectral imaging systems,” Cytometry Part A 62(1), 8–34 (2004).
[Crossref]

2003 (1)

T. Zimmermann, J. Rietdorf, and R. Pepperkok, “Spectral imaging and its applications in live cell microscopy,” FEBS letters 546(1), 87–92 (2003).
[Crossref] [PubMed]

2002 (2)

M. Martinez-Corral, M. T. Caballero, E. H. K. Stelzer, and J. Swoger, “Tailoring the axial shape of the point spread function using the Toraldo concept,” Opt. Express 10(1), 98–103 (2002).
[Crossref] [PubMed]

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive Aberration Correction in a Confocal Microscope”,” P. Natl. Acad. Sci. USA,  99(9), 5788–5792 (2002).
[Crossref]

2001 (1)

B. K. Ford, C. E. Volin, S. M Murphy, R. M. Lynch, and M. R. Descour, “Computed tomography-based spectral imaging for fluorescence microscopy,” Biophys. J. 80(2) 986–993 (2001).
[Crossref] [PubMed]

2000 (1)

J. Campos, J. C. Escalera, C. J. Sheppard, and M. J. Yzuel, “Axially invariant pupil filters," J. Mod. Opt. 47(1), 57–68 (2000).
[Crossref]

1995 (1)

1991 (1)

1988 (1)

C. J. R. Sheppard, “Super-resolution in Confocal Imaging,” Optik 80(2), 53–54 (1988).

1986 (1)

1985 (1)

Z. S. Hegedus, “Annular pupil arrays,” J. Mod. Opt. 32(7), 815–826 (1985).

1974 (1)

L. B. Lucy, “An iterative technique for the rectification of observed distributions”,” Astron. J. 79, 745 (1974).
[Crossref]

1972 (1)

W. H. Richardson, “Bayesian-Based Iterative Method of Image Restoration,” JOSA 62(1), 55–59 (1972).
[Crossref]

Agrawal, A.

M. P. Backlund, M. D. Lew, A. S. Backer, S. J. Sahl, G. Grover, A. Agrawal, R. Piestun, and W. E. Moerner, “Simultaneous, accurate measurement of the 3D position and orientation of single molecules,” Proc. Natl. Acad. Sci. USA 109, 19087 (2012).

Athale, R. A.

J. N. Mait, G. W. Euliss, and R. A. Athale, “Computational imaging,” Advances in Optics and Photonics 10(2), 409–483 (2018).
[Crossref]

Axelrod, D.

D. Axelrod, “Fluorescence excitation and imaging of single molecules near dielectric-coated and bare surfaces: a theoretical study,” J. Microsc. 247(2), 147–160 (2012).
[Crossref] [PubMed]

Azar, L. N.

Azuma, T.

Bachmann, M.

M. Bachmann, F. Fiederling, and M. Bastmeyer, “Practical limitations of superresolution imaging due to conventional sample preparation revealed by a direct comparison of CLSM, SIM and dSTORM,” J. of Microsc. 262(3), 306–315 (2016).
[Crossref]

Backer, A.

Backer, A. S.

M. P. Backlund, M. D. Lew, A. S. Backer, S. J. Sahl, G. Grover, A. Agrawal, R. Piestun, and W. E. Moerner, “Simultaneous, accurate measurement of the 3D position and orientation of single molecules,” Proc. Natl. Acad. Sci. USA 109, 19087 (2012).

Backlund, M.

Backlund, M. P.

M. P. Backlund, M. D. Lew, A. S. Backer, S. J. Sahl, G. Grover, A. Agrawal, R. Piestun, and W. E. Moerner, “Simultaneous, accurate measurement of the 3D position and orientation of single molecules,” Proc. Natl. Acad. Sci. USA 109, 19087 (2012).

Bastmeyer, M.

M. Bachmann, F. Fiederling, and M. Bastmeyer, “Practical limitations of superresolution imaging due to conventional sample preparation revealed by a direct comparison of CLSM, SIM and dSTORM,” J. of Microsc. 262(3), 306–315 (2016).
[Crossref]

Bernet, S.

Bianchini, P.

M. Castello, G. Tortarolo, M. Buttafava, T. Deguchi, F. Villa, S. Koho, L. Pesce, M. Oneto, S. Pelicci, L. Lanzanó, and P. Bianchini, “A robust and versatile platform for image scanning microscopy enabling super-resolution FLIM,” Nat. Meth. 16175–178 (2019).
[Crossref]

Booth, M. J.

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive Aberration Correction in a Confocal Microscope”,” P. Natl. Acad. Sci. USA,  99(9), 5788–5792 (2002).
[Crossref]

Brandt, R. A. J.

Breedijk, R. M. P.

Broeken, J.

Bunt, G.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, and J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” PNAS,  110(52), 21000–21005 (2013).
[Crossref] [PubMed]

Buttafava, M.

M. Castello, G. Tortarolo, M. Buttafava, T. Deguchi, F. Villa, S. Koho, L. Pesce, M. Oneto, S. Pelicci, L. Lanzanó, and P. Bianchini, “A robust and versatile platform for image scanning microscopy enabling super-resolution FLIM,” Nat. Meth. 16175–178 (2019).
[Crossref]

Caballero, M. T.

Campos, J.

J. Campos, J. C. Escalera, C. J. Sheppard, and M. J. Yzuel, “Axially invariant pupil filters," J. Mod. Opt. 47(1), 57–68 (2000).
[Crossref]

Cao, H.

Castello, M.

M. Castello, G. Tortarolo, M. Buttafava, T. Deguchi, F. Villa, S. Koho, L. Pesce, M. Oneto, S. Pelicci, L. Lanzanó, and P. Bianchini, “A robust and versatile platform for image scanning microscopy enabling super-resolution FLIM,” Nat. Meth. 16175–178 (2019).
[Crossref]

Cathey, W. T.

Chandris, P.

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, and H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Meth. 10(11), 1122–1126 (2013).
[Crossref]

Chitnis, A.

P. W. Winter, A. G. York, D. Dalle Nogare, M. Ingaramo, R. Christensen, A. Chitnis, G. H. Patterson, and H. Shroff, “Two-photon instant structured illumination microscopy improves the depth penetration of super-resolution imaging in thick scattering samples,” Optica 1(3), 181–191 (2014).
[Crossref] [PubMed]

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, and H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Meth. 10(11), 1122–1126 (2013).
[Crossref]

Chitnis, A. B.

A. G. York, S. H. Parekh, D. Dalle Nogare, R. S. Fischer, K. Temprine, M. Mione, A. B. Chitnis, C. A. Combs, and H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Meth. 9(7), 749 (2012).
[Crossref]

Christensen, R.

Clever, M.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, and J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” PNAS,  110(52), 21000–21005 (2013).
[Crossref] [PubMed]

Combs, C. A.

A. G. York, S. H. Parekh, D. Dalle Nogare, R. S. Fischer, K. Temprine, M. Mione, A. B. Chitnis, C. A. Combs, and H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Meth. 9(7), 749 (2012).
[Crossref]

Dalle Nogare, D.

P. W. Winter, A. G. York, D. Dalle Nogare, M. Ingaramo, R. Christensen, A. Chitnis, G. H. Patterson, and H. Shroff, “Two-photon instant structured illumination microscopy improves the depth penetration of super-resolution imaging in thick scattering samples,” Optica 1(3), 181–191 (2014).
[Crossref] [PubMed]

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, and H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Meth. 10(11), 1122–1126 (2013).
[Crossref]

A. G. York, S. H. Parekh, D. Dalle Nogare, R. S. Fischer, K. Temprine, M. Mione, A. B. Chitnis, C. A. Combs, and H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Meth. 9(7), 749 (2012).
[Crossref]

de Jong, B. E.

De Luca, G. M. R.

Deguchi, T.

M. Castello, G. Tortarolo, M. Buttafava, T. Deguchi, F. Villa, S. Koho, L. Pesce, M. Oneto, S. Pelicci, L. Lanzanó, and P. Bianchini, “A robust and versatile platform for image scanning microscopy enabling super-resolution FLIM,” Nat. Meth. 16175–178 (2019).
[Crossref]

DeLuca, J.

Descour, M. R.

B. K. Ford, C. E. Volin, S. M Murphy, R. M. Lynch, and M. R. Descour, “Computed tomography-based spectral imaging for fluorescence microscopy,” Biophys. J. 80(2) 986–993 (2001).
[Crossref] [PubMed]

Dowski, E. R.

Enderlein, J.

I. Gregor, M. Spiecker, R. Petrovsky, J. Großhans, R. Ros, and J. Enderlein, “Rapid nonlinear image scanning microscopy,” Nat. Meth.,  14(11), 1087 (2017).
[Crossref]

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, and J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” PNAS,  110(52), 21000–21005 (2013).
[Crossref] [PubMed]

C. Müller and J. Enderlein, “Image Scanning Microscopy,” Phys. Rev. Lett. 104(19), 198101 (2010).
[Crossref] [PubMed]

Escalera, J. C.

J. Campos, J. C. Escalera, C. J. Sheppard, and M. J. Yzuel, “Axially invariant pupil filters," J. Mod. Opt. 47(1), 57–68 (2000).
[Crossref]

Euliss, G. W.

J. N. Mait, G. W. Euliss, and R. A. Athale, “Computational imaging,” Advances in Optics and Photonics 10(2), 409–483 (2018).
[Crossref]

Fiederling, F.

M. Bachmann, F. Fiederling, and M. Bastmeyer, “Practical limitations of superresolution imaging due to conventional sample preparation revealed by a direct comparison of CLSM, SIM and dSTORM,” J. of Microsc. 262(3), 306–315 (2016).
[Crossref]

Fischer, R. S.

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, and H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Meth. 10(11), 1122–1126 (2013).
[Crossref]

A. G. York, S. H. Parekh, D. Dalle Nogare, R. S. Fischer, K. Temprine, M. Mione, A. B. Chitnis, C. A. Combs, and H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Meth. 9(7), 749 (2012).
[Crossref]

Ford, B. K.

B. K. Ford, C. E. Volin, S. M Murphy, R. M. Lynch, and M. R. Descour, “Computed tomography-based spectral imaging for fluorescence microscopy,” Biophys. J. 80(2) 986–993 (2001).
[Crossref] [PubMed]

Greengard, A.

A. Greengard, Y. Y. Schechner, and R. Piestun, “Depth from diffracted rotation,” Opt. Lett., 31(2), 181–183 (2006).
[Crossref] [PubMed]

Gregor, I.

I. Gregor, M. Spiecker, R. Petrovsky, J. Großhans, R. Ros, and J. Enderlein, “Rapid nonlinear image scanning microscopy,” Nat. Meth.,  14(11), 1087 (2017).
[Crossref]

Großhans, J.

I. Gregor, M. Spiecker, R. Petrovsky, J. Großhans, R. Ros, and J. Enderlein, “Rapid nonlinear image scanning microscopy,” Nat. Meth.,  14(11), 1087 (2017).
[Crossref]

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, and J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” PNAS,  110(52), 21000–21005 (2013).
[Crossref] [PubMed]

Grover, G.

M. P. Backlund, M. D. Lew, A. S. Backer, S. J. Sahl, G. Grover, A. Agrawal, R. Piestun, and W. E. Moerner, “Simultaneous, accurate measurement of the 3D position and orientation of single molecules,” Proc. Natl. Acad. Sci. USA 109, 19087 (2012).

Head, J.

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, and H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Meth. 10(11), 1122–1126 (2013).
[Crossref]

Hegedus, Z.

Hegedus, Z. S.

Z. S. Hegedus, “Annular pupil arrays,” J. Mod. Opt. 32(7), 815–826 (1985).

Heintzmann, R.

Hoebe, R. A.

Hoogendoorn, E.

M. Ingaramo, A. G. York, E. Hoogendoorn, M. Postma, H. Shroff, and G. H. Patterson, "Richardson-Lucy deconvolution as a general tool for combining images with complementary strengths," ChemPhysChem 15(4), 794–800 (2014).
[Crossref] [PubMed]

Huff, J.

J. Huff, “The Airyscan detector from ZEISS: confocal imaging with improved signal-to-noise ratio and super-resolution,”. Nat. Meth. 12(12), 1205 (2015).

Ingaramo, M.

M. Ingaramo, A. G. York, E. Hoogendoorn, M. Postma, H. Shroff, and G. H. Patterson, "Richardson-Lucy deconvolution as a general tool for combining images with complementary strengths," ChemPhysChem 15(4), 794–800 (2014).
[Crossref] [PubMed]

P. W. Winter, A. G. York, D. Dalle Nogare, M. Ingaramo, R. Christensen, A. Chitnis, G. H. Patterson, and H. Shroff, “Two-photon instant structured illumination microscopy improves the depth penetration of super-resolution imaging in thick scattering samples,” Optica 1(3), 181–191 (2014).
[Crossref] [PubMed]

Jesacher, A.

Juskaitis, R.

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive Aberration Correction in a Confocal Microscope”,” P. Natl. Acad. Sci. USA,  99(9), 5788–5792 (2002).
[Crossref]

Kehlenbach, R. H.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, and J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” PNAS,  110(52), 21000–21005 (2013).
[Crossref] [PubMed]

Kei, T.

Koho, S.

M. Castello, G. Tortarolo, M. Buttafava, T. Deguchi, F. Villa, S. Koho, L. Pesce, M. Oneto, S. Pelicci, L. Lanzanó, and P. Bianchini, “A robust and versatile platform for image scanning microscopy enabling super-resolution FLIM,” Nat. Meth. 16175–178 (2019).
[Crossref]

Lanzanó, L.

M. Castello, G. Tortarolo, M. Buttafava, T. Deguchi, F. Villa, S. Koho, L. Pesce, M. Oneto, S. Pelicci, L. Lanzanó, and P. Bianchini, “A robust and versatile platform for image scanning microscopy enabling super-resolution FLIM,” Nat. Meth. 16175–178 (2019).
[Crossref]

Lerner, J. M.

J. M. Lerner and R. M. Zucker, “Calibration and validation of confocal spectral imaging systems,” Cytometry Part A 62(1), 8–34 (2004).
[Crossref]

Lew, M.

Lew, M. D.

M. P. Backlund, M. D. Lew, A. S. Backer, S. J. Sahl, G. Grover, A. Agrawal, R. Piestun, and W. E. Moerner, “Simultaneous, accurate measurement of the 3D position and orientation of single molecules,” Proc. Natl. Acad. Sci. USA 109, 19087 (2012).

Lucy, L. B.

L. B. Lucy, “An iterative technique for the rectification of observed distributions”,” Astron. J. 79, 745 (1974).
[Crossref]

Lynch, R. M.

B. K. Ford, C. E. Volin, S. M Murphy, R. M. Lynch, and M. R. Descour, “Computed tomography-based spectral imaging for fluorescence microscopy,” Biophys. J. 80(2) 986–993 (2001).
[Crossref] [PubMed]

Mait, J. N.

J. N. Mait, G. W. Euliss, and R. A. Athale, “Computational imaging,” Advances in Optics and Photonics 10(2), 409–483 (2018).
[Crossref]

Manders, E. M. M.

Martinez-Corral, M.

Mehta, S. B.

Mione, M.

A. G. York, S. H. Parekh, D. Dalle Nogare, R. S. Fischer, K. Temprine, M. Mione, A. B. Chitnis, C. A. Combs, and H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Meth. 9(7), 749 (2012).
[Crossref]

Moerner, W.

Moerner, W. E.

M. P. Backlund, M. D. Lew, A. S. Backer, S. J. Sahl, G. Grover, A. Agrawal, R. Piestun, and W. E. Moerner, “Simultaneous, accurate measurement of the 3D position and orientation of single molecules,” Proc. Natl. Acad. Sci. USA 109, 19087 (2012).

Müller, C.

C. Müller and J. Enderlein, “Image Scanning Microscopy,” Phys. Rev. Lett. 104(19), 198101 (2010).
[Crossref] [PubMed]

Murphy, S. M

B. K. Ford, C. E. Volin, S. M Murphy, R. M. Lynch, and M. R. Descour, “Computed tomography-based spectral imaging for fluorescence microscopy,” Biophys. J. 80(2) 986–993 (2001).
[Crossref] [PubMed]

Neil, M. A. A.

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive Aberration Correction in a Confocal Microscope”,” P. Natl. Acad. Sci. USA,  99(9), 5788–5792 (2002).
[Crossref]

Okamoto, T.

Oneto, M.

M. Castello, G. Tortarolo, M. Buttafava, T. Deguchi, F. Villa, S. Koho, L. Pesce, M. Oneto, S. Pelicci, L. Lanzanó, and P. Bianchini, “A robust and versatile platform for image scanning microscopy enabling super-resolution FLIM,” Nat. Meth. 16175–178 (2019).
[Crossref]

Parekh, S. H.

A. G. York, S. H. Parekh, D. Dalle Nogare, R. S. Fischer, K. Temprine, M. Mione, A. B. Chitnis, C. A. Combs, and H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Meth. 9(7), 749 (2012).
[Crossref]

Patterson, G. H.

M. Ingaramo, A. G. York, E. Hoogendoorn, M. Postma, H. Shroff, and G. H. Patterson, "Richardson-Lucy deconvolution as a general tool for combining images with complementary strengths," ChemPhysChem 15(4), 794–800 (2014).
[Crossref] [PubMed]

P. W. Winter, A. G. York, D. Dalle Nogare, M. Ingaramo, R. Christensen, A. Chitnis, G. H. Patterson, and H. Shroff, “Two-photon instant structured illumination microscopy improves the depth penetration of super-resolution imaging in thick scattering samples,” Optica 1(3), 181–191 (2014).
[Crossref] [PubMed]

Pavani, S.

Pelicci, S.

M. Castello, G. Tortarolo, M. Buttafava, T. Deguchi, F. Villa, S. Koho, L. Pesce, M. Oneto, S. Pelicci, L. Lanzanó, and P. Bianchini, “A robust and versatile platform for image scanning microscopy enabling super-resolution FLIM,” Nat. Meth. 16175–178 (2019).
[Crossref]

Pepperkok, R.

T. Zimmermann, J. Rietdorf, and R. Pepperkok, “Spectral imaging and its applications in live cell microscopy,” FEBS letters 546(1), 87–92 (2003).
[Crossref] [PubMed]

Pesce, L.

M. Castello, G. Tortarolo, M. Buttafava, T. Deguchi, F. Villa, S. Koho, L. Pesce, M. Oneto, S. Pelicci, L. Lanzanó, and P. Bianchini, “A robust and versatile platform for image scanning microscopy enabling super-resolution FLIM,” Nat. Meth. 16175–178 (2019).
[Crossref]

Petrovsky, R.

I. Gregor, M. Spiecker, R. Petrovsky, J. Großhans, R. Ros, and J. Enderlein, “Rapid nonlinear image scanning microscopy,” Nat. Meth.,  14(11), 1087 (2017).
[Crossref]

Pfaff, J.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, and J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” PNAS,  110(52), 21000–21005 (2013).
[Crossref] [PubMed]

Pieper, C.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, and J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” PNAS,  110(52), 21000–21005 (2013).
[Crossref] [PubMed]

Piestun, R.

Popoff, S. M.

Postma, M.

M. Ingaramo, A. G. York, E. Hoogendoorn, M. Postma, H. Shroff, and G. H. Patterson, "Richardson-Lucy deconvolution as a general tool for combining images with complementary strengths," ChemPhysChem 15(4), 794–800 (2014).
[Crossref] [PubMed]

Redding, B.

Richardson, W. H.

W. H. Richardson, “Bayesian-Based Iterative Method of Image Restoration,” JOSA 62(1), 55–59 (1972).
[Crossref]

Rieger, B.

Rietdorf, J.

T. Zimmermann, J. Rietdorf, and R. Pepperkok, “Spectral imaging and its applications in live cell microscopy,” FEBS letters 546(1), 87–92 (2003).
[Crossref] [PubMed]

Ritsch-Marte, M.

Roider, C.

Ros, R.

I. Gregor, M. Spiecker, R. Petrovsky, J. Großhans, R. Ros, and J. Enderlein, “Rapid nonlinear image scanning microscopy,” Nat. Meth.,  14(11), 1087 (2017).
[Crossref]

Roth, S.

S. Roth, C. J. R. Sheppard, K. Wicker, and R. Heintzmann, “Optical Photon Reassignment Microscopy,” Optical Nanoscopy 2(1), 5 (2013).
[Crossref]

Ruhlandt, A.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, and J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” PNAS,  110(52), 21000–21005 (2013).
[Crossref] [PubMed]

Sahl, S. J.

M. P. Backlund, M. D. Lew, A. S. Backer, S. J. Sahl, G. Grover, A. Agrawal, R. Piestun, and W. E. Moerner, “Simultaneous, accurate measurement of the 3D position and orientation of single molecules,” Proc. Natl. Acad. Sci. USA 109, 19087 (2012).

Sarafis, V.

Schechner, Y. Y.

A. Greengard, Y. Y. Schechner, and R. Piestun, “Depth from diffracted rotation,” Opt. Lett., 31(2), 181–183 (2006).
[Crossref] [PubMed]

Schulz, O.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, and J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” PNAS,  110(52), 21000–21005 (2013).
[Crossref] [PubMed]

Sheppard, C. J.

C. J. Sheppard, S. B. Mehta, and R. Heintzmann, “Superresolution by image scanning microscopy using pixel reassignment,” Opt. Lett. 38(15) 2889–2892 (2013).
[Crossref] [PubMed]

J. Campos, J. C. Escalera, C. J. Sheppard, and M. J. Yzuel, “Axially invariant pupil filters," J. Mod. Opt. 47(1), 57–68 (2000).
[Crossref]

Sheppard, C. J. R.

S. Roth, C. J. R. Sheppard, K. Wicker, and R. Heintzmann, “Optical Photon Reassignment Microscopy,” Optical Nanoscopy 2(1), 5 (2013).
[Crossref]

C. J. R. Sheppard, “Super-resolution in Confocal Imaging,” Optik 80(2), 53–54 (1988).

Shroff, H.

M. Ingaramo, A. G. York, E. Hoogendoorn, M. Postma, H. Shroff, and G. H. Patterson, "Richardson-Lucy deconvolution as a general tool for combining images with complementary strengths," ChemPhysChem 15(4), 794–800 (2014).
[Crossref] [PubMed]

P. W. Winter, A. G. York, D. Dalle Nogare, M. Ingaramo, R. Christensen, A. Chitnis, G. H. Patterson, and H. Shroff, “Two-photon instant structured illumination microscopy improves the depth penetration of super-resolution imaging in thick scattering samples,” Optica 1(3), 181–191 (2014).
[Crossref] [PubMed]

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, and H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Meth. 10(11), 1122–1126 (2013).
[Crossref]

A. G. York, S. H. Parekh, D. Dalle Nogare, R. S. Fischer, K. Temprine, M. Mione, A. B. Chitnis, C. A. Combs, and H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Meth. 9(7), 749 (2012).
[Crossref]

Spiecker, M.

I. Gregor, M. Spiecker, R. Petrovsky, J. Großhans, R. Ros, and J. Enderlein, “Rapid nonlinear image scanning microscopy,” Nat. Meth.,  14(11), 1087 (2017).
[Crossref]

Stallinga, S.

Stelzer, E. H. K.

Swoger, J.

Temprine, K.

A. G. York, S. H. Parekh, D. Dalle Nogare, R. S. Fischer, K. Temprine, M. Mione, A. B. Chitnis, C. A. Combs, and H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Meth. 9(7), 749 (2012).
[Crossref]

Timmermans, W.

Tortarolo, G.

M. Castello, G. Tortarolo, M. Buttafava, T. Deguchi, F. Villa, S. Koho, L. Pesce, M. Oneto, S. Pelicci, L. Lanzanó, and P. Bianchini, “A robust and versatile platform for image scanning microscopy enabling super-resolution FLIM,” Nat. Meth. 16175–178 (2019).
[Crossref]

Villa, F.

M. Castello, G. Tortarolo, M. Buttafava, T. Deguchi, F. Villa, S. Koho, L. Pesce, M. Oneto, S. Pelicci, L. Lanzanó, and P. Bianchini, “A robust and versatile platform for image scanning microscopy enabling super-resolution FLIM,” Nat. Meth. 16175–178 (2019).
[Crossref]

Volin, C. E.

B. K. Ford, C. E. Volin, S. M Murphy, R. M. Lynch, and M. R. Descour, “Computed tomography-based spectral imaging for fluorescence microscopy,” Biophys. J. 80(2) 986–993 (2001).
[Crossref] [PubMed]

Wawrzusin, P.

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, and H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Meth. 10(11), 1122–1126 (2013).
[Crossref]

Wicker, K.

S. Roth, C. J. R. Sheppard, K. Wicker, and R. Heintzmann, “Optical Photon Reassignment Microscopy,” Optical Nanoscopy 2(1), 5 (2013).
[Crossref]

Wilson, T.

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive Aberration Correction in a Confocal Microscope”,” P. Natl. Acad. Sci. USA,  99(9), 5788–5792 (2002).
[Crossref]

Winter, P. W.

Wouters, F. S.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, and J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” PNAS,  110(52), 21000–21005 (2013).
[Crossref] [PubMed]

Yamaguchi, I.

York, A. G.

P. W. Winter, A. G. York, D. Dalle Nogare, M. Ingaramo, R. Christensen, A. Chitnis, G. H. Patterson, and H. Shroff, “Two-photon instant structured illumination microscopy improves the depth penetration of super-resolution imaging in thick scattering samples,” Optica 1(3), 181–191 (2014).
[Crossref] [PubMed]

M. Ingaramo, A. G. York, E. Hoogendoorn, M. Postma, H. Shroff, and G. H. Patterson, "Richardson-Lucy deconvolution as a general tool for combining images with complementary strengths," ChemPhysChem 15(4), 794–800 (2014).
[Crossref] [PubMed]

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, and H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Meth. 10(11), 1122–1126 (2013).
[Crossref]

A. G. York, S. H. Parekh, D. Dalle Nogare, R. S. Fischer, K. Temprine, M. Mione, A. B. Chitnis, C. A. Combs, and H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Meth. 9(7), 749 (2012).
[Crossref]

Yzuel, M. J.

J. Campos, J. C. Escalera, C. J. Sheppard, and M. J. Yzuel, “Axially invariant pupil filters," J. Mod. Opt. 47(1), 57–68 (2000).
[Crossref]

Zeelenberg, C. H. C.

Zimmermann, T.

T. Zimmermann, J. Rietdorf, and R. Pepperkok, “Spectral imaging and its applications in live cell microscopy,” FEBS letters 546(1), 87–92 (2003).
[Crossref] [PubMed]

Zucker, R. M.

J. M. Lerner and R. M. Zucker, “Calibration and validation of confocal spectral imaging systems,” Cytometry Part A 62(1), 8–34 (2004).
[Crossref]

Advances in Optics and Photonics (1)

J. N. Mait, G. W. Euliss, and R. A. Athale, “Computational imaging,” Advances in Optics and Photonics 10(2), 409–483 (2018).
[Crossref]

Appl. Opt. (1)

Astron. J. (1)

L. B. Lucy, “An iterative technique for the rectification of observed distributions”,” Astron. J. 79, 745 (1974).
[Crossref]

Biomed. Opt. Express (1)

Biophys. J. (1)

B. K. Ford, C. E. Volin, S. M Murphy, R. M. Lynch, and M. R. Descour, “Computed tomography-based spectral imaging for fluorescence microscopy,” Biophys. J. 80(2) 986–993 (2001).
[Crossref] [PubMed]

ChemPhysChem (1)

M. Ingaramo, A. G. York, E. Hoogendoorn, M. Postma, H. Shroff, and G. H. Patterson, "Richardson-Lucy deconvolution as a general tool for combining images with complementary strengths," ChemPhysChem 15(4), 794–800 (2014).
[Crossref] [PubMed]

Cytometry Part A (1)

J. M. Lerner and R. M. Zucker, “Calibration and validation of confocal spectral imaging systems,” Cytometry Part A 62(1), 8–34 (2004).
[Crossref]

FEBS letters (1)

T. Zimmermann, J. Rietdorf, and R. Pepperkok, “Spectral imaging and its applications in live cell microscopy,” FEBS letters 546(1), 87–92 (2003).
[Crossref] [PubMed]

J. Microsc. (1)

D. Axelrod, “Fluorescence excitation and imaging of single molecules near dielectric-coated and bare surfaces: a theoretical study,” J. Microsc. 247(2), 147–160 (2012).
[Crossref] [PubMed]

J. Mod. Opt. (2)

J. Campos, J. C. Escalera, C. J. Sheppard, and M. J. Yzuel, “Axially invariant pupil filters," J. Mod. Opt. 47(1), 57–68 (2000).
[Crossref]

Z. S. Hegedus, “Annular pupil arrays,” J. Mod. Opt. 32(7), 815–826 (1985).

J. of Microsc. (1)

M. Bachmann, F. Fiederling, and M. Bastmeyer, “Practical limitations of superresolution imaging due to conventional sample preparation revealed by a direct comparison of CLSM, SIM and dSTORM,” J. of Microsc. 262(3), 306–315 (2016).
[Crossref]

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

JOSA (1)

W. H. Richardson, “Bayesian-Based Iterative Method of Image Restoration,” JOSA 62(1), 55–59 (1972).
[Crossref]

Nat. Meth (2)

I. Gregor, M. Spiecker, R. Petrovsky, J. Großhans, R. Ros, and J. Enderlein, “Rapid nonlinear image scanning microscopy,” Nat. Meth.,  14(11), 1087 (2017).
[Crossref]

J. Huff, “The Airyscan detector from ZEISS: confocal imaging with improved signal-to-noise ratio and super-resolution,”. Nat. Meth. 12(12), 1205 (2015).

Nat. Meth. (3)

M. Castello, G. Tortarolo, M. Buttafava, T. Deguchi, F. Villa, S. Koho, L. Pesce, M. Oneto, S. Pelicci, L. Lanzanó, and P. Bianchini, “A robust and versatile platform for image scanning microscopy enabling super-resolution FLIM,” Nat. Meth. 16175–178 (2019).
[Crossref]

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, and H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Meth. 10(11), 1122–1126 (2013).
[Crossref]

A. G. York, S. H. Parekh, D. Dalle Nogare, R. S. Fischer, K. Temprine, M. Mione, A. B. Chitnis, C. A. Combs, and H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Meth. 9(7), 749 (2012).
[Crossref]

Opt. Express (6)

Opt. Lett (1)

A. Greengard, Y. Y. Schechner, and R. Piestun, “Depth from diffracted rotation,” Opt. Lett., 31(2), 181–183 (2006).
[Crossref] [PubMed]

Opt. Lett. (5)

Optica (3)

Optical Nanoscopy (1)

S. Roth, C. J. R. Sheppard, K. Wicker, and R. Heintzmann, “Optical Photon Reassignment Microscopy,” Optical Nanoscopy 2(1), 5 (2013).
[Crossref]

Optik (1)

C. J. R. Sheppard, “Super-resolution in Confocal Imaging,” Optik 80(2), 53–54 (1988).

P. Natl. Acad. Sci. USA (1)

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive Aberration Correction in a Confocal Microscope”,” P. Natl. Acad. Sci. USA,  99(9), 5788–5792 (2002).
[Crossref]

Phys. Rev. Lett. (1)

C. Müller and J. Enderlein, “Image Scanning Microscopy,” Phys. Rev. Lett. 104(19), 198101 (2010).
[Crossref] [PubMed]

PNAS (1)

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, and J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” PNAS,  110(52), 21000–21005 (2013).
[Crossref] [PubMed]

Proc. Natl. Acad. Sci. USA (1)

M. P. Backlund, M. D. Lew, A. S. Backer, S. J. Sahl, G. Grover, A. Agrawal, R. Piestun, and W. E. Moerner, “Simultaneous, accurate measurement of the 3D position and orientation of single molecules,” Proc. Natl. Acad. Sci. USA 109, 19087 (2012).

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Figures (9)

Fig. 1
Fig. 1 (a) Traditional ISM setup. The signal generated in the excitation focus is imaged onto a pixelated detector. Each pixel m records a low-signal but high-resolution confocal image Im, which are computationally combined to a bright high resolution image of the specimen. (b) Spectrally sensitive eISM setup. A Ronchi phase grating in the detection pupil serves as dispersive element. The 1st and -1st diffraction orders are recorded at each sample scanpoint. The images at the bottom show movements of diffraction orders on the camera for two different scenarios: When the excitation spot is scanned from left to right over a monochromatic point source, all diffraction orders undergo the same movement: They slightly follow the excitation spot along the scanning direction. On the other hand, if the color of the source changes, using a binary grating is advantageous, because the altered distance between the two orders allows for discriminating this case from changes caused by the scanspot-sweep.
Fig. 2
Fig. 2 (a) Graphical representation of the excitation and detection PSFs hex and hdet. Their spatial shapes are close to Gaussian, their orientations with respect to the wavelength axis straight and sloped, respectively. The steepness of the slope is determined by the period of the grating in the detection path. (b) Visualization of Eq. (2), which describes the formation of pixel-dependent PSFs hm by spatially translating the detection PSF to the position of pixel m and subsequent multiplications with the excitation PSF.
Fig. 3
Fig. 3 Numerical simulations to assess the imaging properties: (a) x-λ-cross section through the simulated PSF of a typical detector pixel. Its FWHM values along the spatial and spectral directions serve as estimate for the achievable resolutions. (b) Properties of object used for simulations. (c) Brightest single-pixel-image with shot noise. (d) Retrieved object after 1500 iterations.
Fig. 4
Fig. 4 Imaging simulations of grating structures with broader emission spectra at the spatial resolution threshold. (a) and (b) show reconstructions of horizontal and vertical gratings. (c) shows results from monochromatic confocal imaging for two different pinhole sizes as well as ISM. The error bars in (d) express remaining differences between ground truth and reconstructions. Due to remaining spatio-spectral crosstalk, the vertical grating image shows larger errors than the horizontal one, but is still better than the confocal images.
Fig. 5
Fig. 5 Experimental results from the imaging of fluorescent micro beads using regular (a) and spectral (b) ISM. Along the dispersion direction (horizontal) the resolution of regular ISM is slightly better. The spectral mode, however, was capable to identify individual “TetraSpeck” beads (indicated by white arrows and shown in blue). The retrieved emission spectra are shown in (c).
Fig. 6
Fig. 6 Experimental results from the imaging of double-stained HeLa cells (NA=1.4). (a), (b) show different regions within cells; 1st row: composite false-color image, tubulin (OregonGreen488) is shown in orange and actin (STAR440) in blue. 2nd, 3rd rows: individual contributions from tubulin and actin. (c) Emission spectra retrieved from the eISM measurement. (d) Emission spectra measured with a commercial spectrometer.
Fig. 7
Fig. 7 Demonstration of parallel excitation in color eISM. (a) multiple excitation foci are generated using a fan-out mask displayed on the SLM in the excitation pupil. (b) The binary phase grating in the detection pupil creates diffraction orders which are read out simultaneously. The spots showing no dispersion are the zero orders of the detection phase mask. The zero order of the excitation mask is outside the displayed area.
Fig. 8
Fig. 8 (a) The raw data consists of camera ROIs containing the diffraction orders recorded at every scanpoint. (b) Confocal image of a particular pixel.
Fig. 9
Fig. 9 Comparing deconvolution results of data produced using blazed and binary phase gratings. The assumed object is a fluorescent 2D structure consisting of horizontal and vertical lines measuring 2.4×2.4 μm2. Its spatial structure and emission wavelength spectrum are shown in (a). The object estimates at three different wavelengths (λ1, λ2, λ3) after 400 deconvolution iterations are shown in (b). The estimate based on blazed grating data exhibits a wavelength-dependent positional drift, which is indicated by the red dashed line.

Equations (4)

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I m ( x s , y s ) ( ρ * 3 D h m ) ( x s , y s , λ c ) .
h m ( x , y , λ ) = h e x ( x , y ) ( P m 2 D h d e t ) ( x , y , λ ) .
I ˜ m ( x , y ) = n I m , n ( x , y + n a m ) ,
a m = 1 1 + λ e m ( m ) / λ 0 r .

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