Abstract

In the last decade, the resolution of optical microscopy has been doubled thanks to linear structured illumination. The resolution has been further improved by combining structured illumination with nonlinear photoresponse. Recently, structured illumination has been combined with point-scanning microscopy. In this paper, we investigate whether, as in wide field acquisition, significant resolution enhancement can be obtained by harnessing the nonlinear response of the sample when point-scanning structured illumination is employed. We compare point scanning with wide field structured illumination microscopy in terms of signal-to-noise ratio. We conclude that superresolution using saturated point-scanning structured illumination is severely restricted to the first nonlinear orders. We identify possibilities for how different beam shapes or nonlinear phenomena might be envisaged for future implementations.

© 2014 Optical Society of America

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References

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    [Crossref]
  5. S. T. Hess, T. P. Girirajan, M. D. Mason, “Ultra-high resolution imaging by fluorescence photoactivation localization microscopy,” Biophys. J. 91, 4258–4272 (2006).
    [Crossref]
  6. E. Rittweger, K. Y. Han, S. E. Irvine, C. Eggeling, S. W. Hell, “STED microscopy reveals crystal colour centres with nanometric resolution,” Nat. Photonics 3, 144–147 (2009).
    [Crossref]
  7. M. G. Gustafsson, “Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution,” Proc. Natl. Acad. Sci. U.S.A. 102, 13081–13086 (2005).
  8. E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, M. G. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A. 109, E135–E143 (2012).
  9. J. Lu, W. Min, J.-A. Conchello, X. S. Xie, J. W. Lichtman, “Super-resolution laser scanning microscopy through spatiotemporal modulation,” Nano Lett. 9, 3883–3889 (2009).
  10. R.-W. Lu, B.-Q. Wang, Q.-X. Zhang, X.-C. Yao, “Super-resolution scanning laser microscopy through virtually structured detection,” Biomed. Opt. Express 4, 1673–1682 (2013).
    [Crossref]
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  22. C. J. Sheppard, S. B. Mehta, R. Heintzmann, “Superresolution by image scanning microscopy using pixel reassignment,” Opt. Lett. 38, 2889–2892 (2013).
    [Crossref]
  23. B.-J. Chang, L.-J. Chou, Y.-C. Chang, S.-Y. Chiang, “Isotropic image in structured illumination microscopy patterned with a spatial light modulator,” Opt. Express 17, 14710–14721 (2009).
    [Crossref]
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2014 (1)

M. Ingaramo, A. G. York, P. Wawrzusin, O. Milberg, A. Hong, R. Weigert, H. Shroff, G. H. Patterson, “Two-photon excitation improves multifocal structured illumination microscopy in thick scattering tissue,” Proc. Natl. Acad. Sci. U.S.A. 111, 5254–5259 (2014).

2013 (7)

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

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110, 21000–21005 (2013).

R.-W. Lu, B.-Q. Wang, Q.-X. Zhang, X.-C. Yao, “Super-resolution scanning laser microscopy through virtually structured detection,” Biomed. Opt. Express 4, 1673–1682 (2013).
[Crossref]

C. H. Yeh, S. Y. Chen, “Two-photon-based structured illumination microscopy applied for superresolution optical biopsy,” Proc. SPIE 8588, 858826 (2013).

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

S. Roth, C. J. Sheppard, K. Wicker, R. Heintzmann, “Optical photon reassignment microscopy (OPRA),” Opt. Nanoscopy 2, 5 (2013).

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

2012 (2)

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, M. G. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A. 109, E135–E143 (2012).

A. G. York, S. H. Parekh, D. Dalle Nogare, R. S. Fischer, K. Temprine, M. Mione, A. B. Chitnis, C. A. Combs, H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Methods 9, 749–754 (2012).
[Crossref]

2011 (1)

2010 (3)

N. D. Lai, D. Zheng, F. Treussart, J.-F. Roch, “Optical determination and magnetic manipulation of a single nitrogen-vacancy color center in diamond nanocrystal,” Adv. Nat. Sci. 1, 015014 (2010).

O. Faklaris, J. Botsoa, T. Sauvage, J.-F. Roch, F. Treussart, “Photoluminescent nanodiamonds: comparison of the photoluminescence saturation properties of the NV color center and a cyanine dye at the single emitter level, and study of the color center concentration under different preparation conditions,” Diamond Rel. Mater. 19, 988–995 (2010).

C. B. Müller, J. Enderlein, “Image scanning microscopy,” Phys. Rev. Lett. 104, 198101 (2010).
[Crossref]

2009 (3)

J. Lu, W. Min, J.-A. Conchello, X. S. Xie, J. W. Lichtman, “Super-resolution laser scanning microscopy through spatiotemporal modulation,” Nano Lett. 9, 3883–3889 (2009).

E. Rittweger, K. Y. Han, S. E. Irvine, C. Eggeling, S. W. Hell, “STED microscopy reveals crystal colour centres with nanometric resolution,” Nat. Photonics 3, 144–147 (2009).
[Crossref]

B.-J. Chang, L.-J. Chou, Y.-C. Chang, S.-Y. Chiang, “Isotropic image in structured illumination microscopy patterned with a spatial light modulator,” Opt. Express 17, 14710–14721 (2009).
[Crossref]

2006 (2)

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
[Crossref]

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

2005 (1)

M. G. Gustafsson, “Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution,” Proc. Natl. Acad. Sci. U.S.A. 102, 13081–13086 (2005).

2000 (1)

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

1999 (1)

1988 (1)

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

1963 (1)

W. Lukosz, M. Marchand, “Optischen abbildung unter überschreitung der beugungsbedingten auflösungsgrenze,” J. Mod. Opt. 10, 241–255 (1963).

Azar, L. N.

Betzig, E.

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
[Crossref]

Bonifacino, J. S.

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
[Crossref]

Botsoa, J.

O. Faklaris, J. Botsoa, T. Sauvage, J.-F. Roch, F. Treussart, “Photoluminescent nanodiamonds: comparison of the photoluminescence saturation properties of the NV color center and a cyanine dye at the single emitter level, and study of the color center concentration under different preparation conditions,” Diamond Rel. Mater. 19, 988–995 (2010).

Brandt, R. A.

Breedijk, R. M.

Bunt, G.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110, 21000–21005 (2013).

Chandris, P.

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

Chang, B.-J.

Chang, H.-C.

Chang, Y.-C.

Chen, S. Y.

C. H. Yeh, S. Y. Chen, “Two-photon-based structured illumination microscopy applied for superresolution optical biopsy,” Proc. SPIE 8588, 858826 (2013).

Chiang, S.-Y.

Chitnis, A.

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Methods 10, 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, H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Methods 9, 749–754 (2012).
[Crossref]

Chou, L.-J.

Clever, M.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110, 21000–21005 (2013).

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, H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Methods 9, 749–754 (2012).
[Crossref]

Conchello, J.-A.

J. Lu, W. Min, J.-A. Conchello, X. S. Xie, J. W. Lichtman, “Super-resolution laser scanning microscopy through spatiotemporal modulation,” Nano Lett. 9, 3883–3889 (2009).

Dalle Nogare, D.

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Methods 10, 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, H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Methods 9, 749–754 (2012).
[Crossref]

Davidson, M. W.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, M. G. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A. 109, E135–E143 (2012).

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
[Crossref]

de Jong, B. E.

De Luca, G. M.

Eggeling, C.

E. Rittweger, K. Y. Han, S. E. Irvine, C. Eggeling, S. W. Hell, “STED microscopy reveals crystal colour centres with nanometric resolution,” Nat. Photonics 3, 144–147 (2009).
[Crossref]

Enderlein, J.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110, 21000–21005 (2013).

C. B. Müller, J. Enderlein, “Image scanning microscopy,” Phys. Rev. Lett. 104, 198101 (2010).
[Crossref]

Faklaris, O.

O. Faklaris, J. Botsoa, T. Sauvage, J.-F. Roch, F. Treussart, “Photoluminescent nanodiamonds: comparison of the photoluminescence saturation properties of the NV color center and a cyanine dye at the single emitter level, and study of the color center concentration under different preparation conditions,” Diamond Rel. Mater. 19, 988–995 (2010).

Fischer, R. S.

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Methods 10, 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, H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Methods 9, 749–754 (2012).
[Crossref]

Fujita, K.

Girirajan, T. P.

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

Großhans, J.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110, 21000–21005 (2013).

Gustafsson, M. G.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, M. G. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A. 109, E135–E143 (2012).

M. G. Gustafsson, “Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution,” Proc. Natl. Acad. Sci. U.S.A. 102, 13081–13086 (2005).

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

Han, K. Y.

E. Rittweger, K. Y. Han, S. E. Irvine, C. Eggeling, S. W. Hell, “STED microscopy reveals crystal colour centres with nanometric resolution,” Nat. Photonics 3, 144–147 (2009).
[Crossref]

Head, J.

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

Heintzmann, R.

S. Roth, C. J. Sheppard, K. Wicker, R. Heintzmann, “Optical photon reassignment microscopy (OPRA),” Opt. Nanoscopy 2, 5 (2013).

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

Hell, S. W.

E. Rittweger, K. Y. Han, S. E. Irvine, C. Eggeling, S. W. Hell, “STED microscopy reveals crystal colour centres with nanometric resolution,” Nat. Photonics 3, 144–147 (2009).
[Crossref]

T. A. Klar, S. W. Hell, “Subdiffraction resolution in far-field fluorescence microscopy,” Opt. Lett. 24, 954–956 (1999).
[Crossref]

Hess, H. F.

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
[Crossref]

Hess, S. T.

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

Hoebe, R. A.

Hong, A.

M. Ingaramo, A. G. York, P. Wawrzusin, O. Milberg, A. Hong, R. Weigert, H. Shroff, G. H. Patterson, “Two-photon excitation improves multifocal structured illumination microscopy in thick scattering tissue,” Proc. Natl. Acad. Sci. U.S.A. 111, 5254–5259 (2014).

Ingaramo, M.

M. Ingaramo, A. G. York, P. Wawrzusin, O. Milberg, A. Hong, R. Weigert, H. Shroff, G. H. Patterson, “Two-photon excitation improves multifocal structured illumination microscopy in thick scattering tissue,” Proc. Natl. Acad. Sci. U.S.A. 111, 5254–5259 (2014).

Irvine, S. E.

E. Rittweger, K. Y. Han, S. E. Irvine, C. Eggeling, S. W. Hell, “STED microscopy reveals crystal colour centres with nanometric resolution,” Nat. Photonics 3, 144–147 (2009).
[Crossref]

Johansson, G. A.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, M. G. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A. 109, E135–E143 (2012).

Kamps-Hughes, N.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, M. G. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A. 109, E135–E143 (2012).

Kawano, S.

Kawata, S.

Kehlenbach, R. H.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110, 21000–21005 (2013).

Klar, T. A.

Lai, N. D.

N. D. Lai, D. Zheng, F. Treussart, J.-F. Roch, “Optical determination and magnetic manipulation of a single nitrogen-vacancy color center in diamond nanocrystal,” Adv. Nat. Sci. 1, 015014 (2010).

Lichtman, J. W.

J. Lu, W. Min, J.-A. Conchello, X. S. Xie, J. W. Lichtman, “Super-resolution laser scanning microscopy through spatiotemporal modulation,” Nano Lett. 9, 3883–3889 (2009).

Lindwasser, O. W.

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
[Crossref]

Lippincott-Schwartz, J.

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
[Crossref]

Lu, J.

J. Lu, W. Min, J.-A. Conchello, X. S. Xie, J. W. Lichtman, “Super-resolution laser scanning microscopy through spatiotemporal modulation,” Nano Lett. 9, 3883–3889 (2009).

Lu, R.-W.

Lukosz, W.

W. Lukosz, M. Marchand, “Optischen abbildung unter überschreitung der beugungsbedingten auflösungsgrenze,” J. Mod. Opt. 10, 241–255 (1963).

Macklin, J. J.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, M. G. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A. 109, E135–E143 (2012).

Manders, E. M.

Marchand, M.

W. Lukosz, M. Marchand, “Optischen abbildung unter überschreitung der beugungsbedingten auflösungsgrenze,” J. Mod. Opt. 10, 241–255 (1963).

Mason, M. D.

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

Mehta, S. B.

Milberg, O.

M. Ingaramo, A. G. York, P. Wawrzusin, O. Milberg, A. Hong, R. Weigert, H. Shroff, G. H. Patterson, “Two-photon excitation improves multifocal structured illumination microscopy in thick scattering tissue,” Proc. Natl. Acad. Sci. U.S.A. 111, 5254–5259 (2014).

Min, W.

J. Lu, W. Min, J.-A. Conchello, X. S. Xie, J. W. Lichtman, “Super-resolution laser scanning microscopy through spatiotemporal modulation,” Nano Lett. 9, 3883–3889 (2009).

Mione, M.

A. G. York, S. H. Parekh, D. Dalle Nogare, R. S. Fischer, K. Temprine, M. Mione, A. B. Chitnis, C. A. Combs, H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Methods 9, 749–754 (2012).
[Crossref]

Müller, C. B.

C. B. Müller, J. Enderlein, “Image scanning microscopy,” Phys. Rev. Lett. 104, 198101 (2010).
[Crossref]

Olenych, S.

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
[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, H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Methods 9, 749–754 (2012).
[Crossref]

Patterson, G. H.

M. Ingaramo, A. G. York, P. Wawrzusin, O. Milberg, A. Hong, R. Weigert, H. Shroff, G. H. Patterson, “Two-photon excitation improves multifocal structured illumination microscopy in thick scattering tissue,” Proc. Natl. Acad. Sci. U.S.A. 111, 5254–5259 (2014).

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
[Crossref]

Pfaff, J.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110, 21000–21005 (2013).

Pieper, C.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110, 21000–21005 (2013).

Rego, E. H.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, M. G. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A. 109, E135–E143 (2012).

Rittweger, E.

E. Rittweger, K. Y. Han, S. E. Irvine, C. Eggeling, S. W. Hell, “STED microscopy reveals crystal colour centres with nanometric resolution,” Nat. Photonics 3, 144–147 (2009).
[Crossref]

Roch, J.-F.

O. Faklaris, J. Botsoa, T. Sauvage, J.-F. Roch, F. Treussart, “Photoluminescent nanodiamonds: comparison of the photoluminescence saturation properties of the NV color center and a cyanine dye at the single emitter level, and study of the color center concentration under different preparation conditions,” Diamond Rel. Mater. 19, 988–995 (2010).

N. D. Lai, D. Zheng, F. Treussart, J.-F. Roch, “Optical determination and magnetic manipulation of a single nitrogen-vacancy color center in diamond nanocrystal,” Adv. Nat. Sci. 1, 015014 (2010).

Roth, S.

S. Roth, C. J. Sheppard, K. Wicker, R. Heintzmann, “Optical photon reassignment microscopy (OPRA),” Opt. Nanoscopy 2, 5 (2013).

Ruhlandt, A.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110, 21000–21005 (2013).

Sauvage, T.

O. Faklaris, J. Botsoa, T. Sauvage, J.-F. Roch, F. Treussart, “Photoluminescent nanodiamonds: comparison of the photoluminescence saturation properties of the NV color center and a cyanine dye at the single emitter level, and study of the color center concentration under different preparation conditions,” Diamond Rel. Mater. 19, 988–995 (2010).

Schulz, O.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110, 21000–21005 (2013).

Shao, L.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, M. G. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A. 109, E135–E143 (2012).

Sheppard, C. J.

S. Roth, C. J. Sheppard, K. Wicker, R. Heintzmann, “Optical photon reassignment microscopy (OPRA),” Opt. Nanoscopy 2, 5 (2013).

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

Sheppard, C. J. R.

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

Shroff, H.

M. Ingaramo, A. G. York, P. Wawrzusin, O. Milberg, A. Hong, R. Weigert, H. Shroff, G. H. Patterson, “Two-photon excitation improves multifocal structured illumination microscopy in thick scattering tissue,” Proc. Natl. Acad. Sci. U.S.A. 111, 5254–5259 (2014).

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Methods 10, 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, H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Methods 9, 749–754 (2012).
[Crossref]

Smith, N. I.

Sougrat, R.

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
[Crossref]

Stallinga, S.

Temprine, K.

A. G. York, S. H. Parekh, D. Dalle Nogare, R. S. Fischer, K. Temprine, M. Mione, A. B. Chitnis, C. A. Combs, H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Methods 9, 749–754 (2012).
[Crossref]

Timmermans, W.

Treussart, F.

N. D. Lai, D. Zheng, F. Treussart, J.-F. Roch, “Optical determination and magnetic manipulation of a single nitrogen-vacancy color center in diamond nanocrystal,” Adv. Nat. Sci. 1, 015014 (2010).

O. Faklaris, J. Botsoa, T. Sauvage, J.-F. Roch, F. Treussart, “Photoluminescent nanodiamonds: comparison of the photoluminescence saturation properties of the NV color center and a cyanine dye at the single emitter level, and study of the color center concentration under different preparation conditions,” Diamond Rel. Mater. 19, 988–995 (2010).

Tzeng, Y.-K.

Wang, B.-Q.

Wawrzusin, P.

M. Ingaramo, A. G. York, P. Wawrzusin, O. Milberg, A. Hong, R. Weigert, H. Shroff, G. H. Patterson, “Two-photon excitation improves multifocal structured illumination microscopy in thick scattering tissue,” Proc. Natl. Acad. Sci. U.S.A. 111, 5254–5259 (2014).

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

Weigert, R.

M. Ingaramo, A. G. York, P. Wawrzusin, O. Milberg, A. Hong, R. Weigert, H. Shroff, G. H. Patterson, “Two-photon excitation improves multifocal structured illumination microscopy in thick scattering tissue,” Proc. Natl. Acad. Sci. U.S.A. 111, 5254–5259 (2014).

Wicker, K.

S. Roth, C. J. Sheppard, K. Wicker, R. Heintzmann, “Optical photon reassignment microscopy (OPRA),” Opt. Nanoscopy 2, 5 (2013).

Winoto, L.

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, M. G. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A. 109, E135–E143 (2012).

Wouters, F. S.

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110, 21000–21005 (2013).

Xie, X. S.

J. Lu, W. Min, J.-A. Conchello, X. S. Xie, J. W. Lichtman, “Super-resolution laser scanning microscopy through spatiotemporal modulation,” Nano Lett. 9, 3883–3889 (2009).

Yamanaka, M.

Yao, X.-C.

Yeh, C. H.

C. H. Yeh, S. Y. Chen, “Two-photon-based structured illumination microscopy applied for superresolution optical biopsy,” Proc. SPIE 8588, 858826 (2013).

York, A. G.

M. Ingaramo, A. G. York, P. Wawrzusin, O. Milberg, A. Hong, R. Weigert, H. Shroff, G. H. Patterson, “Two-photon excitation improves multifocal structured illumination microscopy in thick scattering tissue,” Proc. Natl. Acad. Sci. U.S.A. 111, 5254–5259 (2014).

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Methods 10, 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, H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Methods 9, 749–754 (2012).
[Crossref]

Zeelenberg, C. H.

Zhang, Q.-X.

Zheng, D.

N. D. Lai, D. Zheng, F. Treussart, J.-F. Roch, “Optical determination and magnetic manipulation of a single nitrogen-vacancy color center in diamond nanocrystal,” Adv. Nat. Sci. 1, 015014 (2010).

Adv. Nat. Sci. (1)

N. D. Lai, D. Zheng, F. Treussart, J.-F. Roch, “Optical determination and magnetic manipulation of a single nitrogen-vacancy color center in diamond nanocrystal,” Adv. Nat. Sci. 1, 015014 (2010).

Biomed. Opt. Express (3)

Biophys. J. (1)

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

Diamond Rel. Mater. (1)

O. Faklaris, J. Botsoa, T. Sauvage, J.-F. Roch, F. Treussart, “Photoluminescent nanodiamonds: comparison of the photoluminescence saturation properties of the NV color center and a cyanine dye at the single emitter level, and study of the color center concentration under different preparation conditions,” Diamond Rel. Mater. 19, 988–995 (2010).

J. Microsc. (1)

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

J. Mod. Opt. (1)

W. Lukosz, M. Marchand, “Optischen abbildung unter überschreitung der beugungsbedingten auflösungsgrenze,” J. Mod. Opt. 10, 241–255 (1963).

Nano Lett. (1)

J. Lu, W. Min, J.-A. Conchello, X. S. Xie, J. W. Lichtman, “Super-resolution laser scanning microscopy through spatiotemporal modulation,” Nano Lett. 9, 3883–3889 (2009).

Nat. Methods (2)

A. G. York, S. H. Parekh, D. Dalle Nogare, R. S. Fischer, K. Temprine, M. Mione, A. B. Chitnis, C. A. Combs, H. Shroff, “Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy,” Nat. Methods 9, 749–754 (2012).
[Crossref]

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

Nat. Photonics (1)

E. Rittweger, K. Y. Han, S. E. Irvine, C. Eggeling, S. W. Hell, “STED microscopy reveals crystal colour centres with nanometric resolution,” Nat. Photonics 3, 144–147 (2009).
[Crossref]

Opt. Express (1)

Opt. Lett. (2)

Opt. Nanoscopy (1)

S. Roth, C. J. Sheppard, K. Wicker, R. Heintzmann, “Optical photon reassignment microscopy (OPRA),” Opt. Nanoscopy 2, 5 (2013).

Optik (1)

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

Phys. Rev. Lett. (1)

C. B. Müller, J. Enderlein, “Image scanning microscopy,” Phys. Rev. Lett. 104, 198101 (2010).
[Crossref]

Proc. Natl. Acad. Sci. U.S.A. (4)

O. Schulz, C. Pieper, M. Clever, J. Pfaff, A. Ruhlandt, R. H. Kehlenbach, F. S. Wouters, J. Großhans, G. Bunt, J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110, 21000–21005 (2013).

M. G. Gustafsson, “Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution,” Proc. Natl. Acad. Sci. U.S.A. 102, 13081–13086 (2005).

E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, M. G. Gustafsson, “Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. U.S.A. 109, E135–E143 (2012).

M. Ingaramo, A. G. York, P. Wawrzusin, O. Milberg, A. Hong, R. Weigert, H. Shroff, G. H. Patterson, “Two-photon excitation improves multifocal structured illumination microscopy in thick scattering tissue,” Proc. Natl. Acad. Sci. U.S.A. 111, 5254–5259 (2014).

Proc. SPIE (1)

C. H. Yeh, S. Y. Chen, “Two-photon-based structured illumination microscopy applied for superresolution optical biopsy,” Proc. SPIE 8588, 858826 (2013).

Science (1)

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
[Crossref]

Supplementary Material (1)

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Figures (6)

Fig. 1.
Fig. 1.

Linear imaging of fluorescent NDs with an 0.8 NA objective. (a) WF image, obtained by pixel reassignment with factor 1 (see [22]), (c) digital temporal scanning SIM image, (d) digital spatial scanning SIM image, and (e) pixel reassignement image. (b) Intensity profiles along the yellow dashed line for the different techniques. The signal from a single subdiffraction fluorescent ND gives an estimation of the lateral resolution improvement. The FWHM is 500 nm in the WF image and 285 nm with the linear processing techniques. It corresponds to a 1.75 times improvement in lateral resolution. Scale bars are 500 nm.

Fig. 2.
Fig. 2.

Simulated data on photon budget influence on linear imaging of fluorescent nanoparticles. (a)  3.2 μm × 3.2 μm sample composed of five 25 nm particles. The number on each picture indicates the total number of excitation photons incident on the sample during the acquisition (excitation dose) relatively to the weaker one. (b) WF image. (c)–(e) Point-scanning SIM with increasing excitation doses. (d), (f), (h) WF-SIM with the same respective doses. The comparison of (d) and (g) indicates that the WF method is clearly superior in terms of SNR. (e) and (h) show that the two methods are equivalent with a bright enough sample.

Fig. 3.
Fig. 3.

Experimental demonstration of CNS microscopy on fluorescent NDs with a 0.8NA objective. (a) WF image, (b) linear digital temporal scanning SIM image, and (c) saturated CNS image. Scale bars are 500 nm. (d) As in the previous figure, intensity profile along the yellow dashed line to measure the lateral resolution. The FWHM is 500 nm in the WF image, 285 nm with the linear processing, and 195 nm in the nonlinear image. Consequently, saturated scanning SIM enhances the resolution by a factor of 2.6 compared to a WF microscope.

Fig. 4.
Fig. 4.

Zoomed images on the dashed red squares area in Figs. 3(a)3(c), showing that two fluorescent NDs separated by 300 nm are resolved. The intensity profile along the yellow dashed line proves they are resolved.

Fig. 5.
Fig. 5.

Simulated data on photon budget influence on nonlinear imaging of fluorescent nanoparticles. The peak excitation intensity is the same for CNS and WF structured illumination. The numbers in the upper left corners of the images give the fluorescence quantum yield normalized to the weaker one. (a) Equivalent excitation intensity patterns obtained with saturation of fluorescent NDs with a peak intensity of 2 MW / cm 2 . The blue curve is the WF structured illumination, and the red curve is the focused one. (b)–(d) Linear SIM data with doubling gain in resolution. Scanning SIM gives a better reconstruction under those conditions (at the cost of a higher excitation dose). (e), (f) With 10 times more emitted photons, the first-order nonlinear reconstruction gives a better image with WF-SIM. (g), (h) With 100 times more photons the second-order nonlinear reconstruction gives a four times improvement in resolution with WF-SIM, while the point-scanning SIM fails.

Fig. 6.
Fig. 6.

Nonlinear imaging of fluorescent NDs with a 1.4 NA objective. (a) WF image, (b) STED image, and (c) STED CNS image. Scale bars are 500 nm. (d) Intensity profile along a single fluorescent ND showing the improvement in resolution. The measured FWHM is 280 nm for WF, 125 nm for STED, and 98 nm for STED scanning SIM.

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