Abstract

At the start of this millennium, the principles of structured illumination microscopy (SIM) had been established and the concept of resolution doubling demonstrated experimentally in two dimensions. Breathtaking advances have since taken place, making SIM one of the most powerful and versatile superresolution methods available today, routinely used in the study of biochemical processes in laboratories around the world. In theory there is no inherent limit to the resolution obtainable with certain modalities of SIM, and new variants have the potential to operate at even higher speeds and sensitivity than currently realized. In this review, we focus on the very latest innovations in SIM theory and practice, which are set to continue the revolution of this method into the future. Examples include confocal implementations of the SIM principle, which can be used in combination with two-photon excitation and adaptive optics. We present recent applications of such approaches in the life sciences, which illustrate their potential to revolutionize intravital research, by providing the ability to watch life at the molecular scale, at high speeds, and deep within living organisms. A different variant makes use of standing plasmonic waves or localized surface plasmons to confer performance enhancements to 2D SIM modalities. Research on these latter techniques is in its infancy but already shows great potential for their development into powerful in vitro probes for chemical processes at solid/liquid interfaces. Physical concepts are reviewed in detail, and future directions are presented along which the field might fruitfully develop, holding promise for new discoveries on the molecular scale.

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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2015 (6)

F. Ströhl and C. F. Kaminski, “A joint Richardson–Lucy deconvolution algorithm for the reconstruction of multifocal structured illumination microscopy data,” Methods Appl. Fluoresc. 3, 014002 (2015).

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

T. Azuma and T. Kei, “Super-resolution spinning-disk confocal microscopy using optical photon reassignment,” Opt. Express 23, 15003–15011 (2015).
[Crossref]

M. Ingaramo, A. G. York, E. J. Andrade, K. Rainey, and G. H. Patterson, “Two-photon-like microscopy with orders-of-magnitude lower illumination intensity via two-step fluorescence,” Nat. Commun. 6, 8184 (2015).
[Crossref]

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349, aab3500 (2015).
[Crossref]

B. Thomas, A. Wolstenholme, S. N. Chaudhari, E. T. Kipreos, and P. Kner, “Enhanced resolution through thick tissue with structured illumination and adaptive optics,” J. Biomed. Opt. 20, 026006 (2015).
[Crossref]

2014 (13)

D. M. Shcherbakova, P. Sengupta, J. Lippincott-Schwartz, and V. V. Verkhusha, “Photocontrollable fluorescent proteins for superresolution imaging,” Ann. Rev. Biophys. 43, 303–329 (2014).
[Crossref]

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

P. W. Winter, A. G. York, D. D. 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, 181–191 (2014).
[Crossref]

L.-C. Cheng, C.-H. Lien, Y. Da Sie, Y. Y. Hu, C.-Y. Lin, F.-C. Chien, C. Xu, C. Y. Dong, and S.-J. Chen, “Nonlinear structured-illumination enhanced temporal focusing multiphoton excitation microscopy with a digital micromirror device,” Biomed. Opt. Express 5, 2526–2536 (2014).
[Crossref]

G. P. J. Laporte, N. Stasio, C. J. R. Sheppard, and D. Psaltis, “Resolution enhancement in nonlinear scanning microscopy through post-detection digital computation,” Optica 1, 455–460 (2014).
[Crossref]

F. Wei, D. Lu, H. Shen, W. Wan, J. L. Ponsetto, E. Huang, and Z. Liu, “Wide field super-resolution surface imaging through plasmonic structured illumination microscopy,” Nano Lett. 14, 4634–4639 (2014).
[Crossref]

X. Zeng and M. S. Zubairy, “Nanometer-scale microscopy via graphene plasmons,” Phys. Rev. B 90, 235418 (2014).

J. L. Ponsetto, F. Wei, and Z. Liu, “Localized plasmon assisted structured illumination microscopy for wide-field high-speed dispersion-independent super resolution imaging,” Nanoscale 6, 5807–5812 (2014).
[Crossref]

C. T. Ertsgaard, R. M. Mckoskey, I. S. Rich, and N. C. Lindquist, “Dynamic placement of plasmonic hotspots for super-resolution surface-enhanced Raman scattering,” ACS Nano 8, 10941–10946 (2014).
[Crossref]

V. Hamel, P. Guichard, M. Fournier, R. Guiet, I. Flückiger, A. Seitz, and P. Gönczy, “Correlative multicolor 3D SIM and STORM microscopy,” Biomed. Opt. Express 5, 3326–3336 (2014).
[Crossref]

P. W. Winter and H. Shroff, “Faster fluorescence microscopy: advances in high speed biological imaging,” Curr. Opin. Chem. Biol. 20, 46–53 (2014).
[Crossref]

J. R. Allen, S. T. Ross, and M. W. Davidson, “Structured illumination microscopy for superresolution,” Chem. Phys. Chem. 15, 566–576 (2014).

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

2013 (12)

A. Jost and R. Heintzmann, “Superresolution multidimensional imaging with structured illumination microscopy,” Ann. Rev. Mater. Res. 43, 261–282 (2013).
[Crossref]

R. Fiolka, “Three-dimensional live microscopy beyond the diffraction limit,” J. Opt. 15, 094002 (2013).
[Crossref]

R. Han, Z. Li, Y. Fan, and Y. Jiang, “Recent advances in super-resolution fluorescence imaging and its applications in biology,” J. Genet. Genomics 40, 583–595 (2013).
[Crossref]

Y. Wu, R. Christensen, D. Colón-Ramos, and H. Shroff, “Advanced optical imaging techniques for neurodevelopment,” Curr. Opin. Neurobiol. 23, 1090–1097 (2013).
[Crossref]

A. G. York, P. Chandris, D. D. 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. Methods 10, 1122–1126 (2013).
[Crossref]

C. J. R. Sheppard, S. B. Mehta, and 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, and J. Enderlein, “Resolution doubling in fluorescence microscopy with confocal spinning-disk image scanning microscopy,” Proc. Natl. Acad. Sci. USA 110, 21000–21005 (2013).
[Crossref]

S. Rossberger, G. Best, D. Baddeley, R. Heintzmann, U. Birk, S. Dithmar, and C. Cremer, “Combination of structured illumination and single molecule localization microscopy in one setup,” J. Opt. 15, 094003 (2013).
[Crossref]

A. Chmyrov, J. Keller, T. Grotjohann, M. Ratz, E. D’Este, S. Jakobs, C. Eggeling, and S. W. Hell, “Nanoscopy with more than 100, 000 ‘doughnuts’,” Nat. Methods 10, 737–740 (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, 2644–2656 (2013).
[Crossref]

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

R. Ayuk, H. Giovannini, A. Jost, E. Mudry, J. Girard, T. Mangeat, N. Sandeau, R. Heintzmann, K. Wicker, K. Belkebir, and A. Sentenac, “Structured illumination fluorescence microscopy with distorted excitations using a filtered blind-SIM algorithm,” Opt. Lett. 38, 4723–4726 (2013).
[Crossref]

2012 (3)

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

V. Andresen, K. Pollok, and J. Rinnenthal, “High-resolution intravital microscopy,” PLoS ONE 7, e50915 (2012).
[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. Methods 9, 749–754 (2012).
[Crossref]

2011 (2)

2010 (2)

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2009 (5)

2008 (5)

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R. Fiolka, M. Beck, and A. Stemmer, “Structured illumination in total internal reflection fluorescence microscopy using a spatial light modulator,” Opt. Lett. 33, 1629–1631 (2008).
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L. Shao, B. Isaac, S. Uzawa, D. A. Agard, J. W. Sedat, and M. G. L. Gustafsson, “I5S: wide-field light microscopy with 100-nm-scale resolution in three dimensions,” Biophys. J. 94, 4971–4983 (2008).
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2007 (2)

S. Hell, “Far-field optical nanoscopy,” Science 316, 1153–1158 (2007).
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M. J. Booth, “Adaptive optics in microscopy,” Philos. Trans. Ser. A 365, 2829–2843 (2007).
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2006 (4)

E. Chung, D. Kim, and P. So, “Extended resolution wide-field optical imaging: objective-launched standing-wave total internal reflection fluorescence microscopy,” Opt. Lett. 31, 945–947 (2006).
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E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
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S. T. Hess, T. P. K. Girirajan, and M. D. Mason, “Ultra-high resolution imaging by fluorescence photoactivation localization microscopy,” Biophys. J. 91, 4258–4272 (2006).
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M. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3, 793–796 (2006).
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2005 (2)

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2002 (1)

2000 (1)

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1999 (1)

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1995 (1)

1994 (1)

1990 (1)

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1989 (1)

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1988 (1)

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1981 (1)

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1957 (1)

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1896 (1)

L. Rayleigh, “XV. On the theory of optical images, with special reference to the microscope,” Philos. Mag. Ser. 5 42(255), 167–195 (1896).
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1873 (1)

E. Abbe, “Beiträge zur theorie des mikroskops und der mikroskopischen wahrnehmung,” Archiv f. Mikr. Anat. 9, 413–418 (1873).
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L. Shao, B. Isaac, S. Uzawa, D. A. Agard, J. W. Sedat, and M. G. L. Gustafsson, “I5S: wide-field light microscopy with 100-nm-scale resolution in three dimensions,” Biophys. J. 94, 4971–4983 (2008).
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J. R. Allen, S. T. Ross, and M. W. Davidson, “Structured illumination microscopy for superresolution,” Chem. Phys. Chem. 15, 566–576 (2014).

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M. Ingaramo, A. G. York, E. J. Andrade, K. Rainey, and G. H. Patterson, “Two-photon-like microscopy with orders-of-magnitude lower illumination intensity via two-step fluorescence,” Nat. Commun. 6, 8184 (2015).
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D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349, aab3500 (2015).
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Ball, G.

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Bates, M.

M. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3, 793–796 (2006).
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D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349, aab3500 (2015).
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Beck, M.

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Best, G.

S. Rossberger, G. Best, D. Baddeley, R. Heintzmann, U. Birk, S. Dithmar, and C. Cremer, “Combination of structured illumination and single molecule localization microscopy in one setup,” J. Opt. 15, 094003 (2013).
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D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349, aab3500 (2015).
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E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
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S. Rossberger, G. Best, D. Baddeley, R. Heintzmann, U. Birk, S. Dithmar, and C. Cremer, “Combination of structured illumination and single molecule localization microscopy in one setup,” J. Opt. 15, 094003 (2013).
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Bock, H.

J. Fölling, M. Bossi, H. Bock, R. Medda, C. A. Wurm, B. Hein, S. Jakobs, C. Eggeling, and S. W. Hell, “Fluorescence nanoscopy by ground-state depletion and single-molecule return,” Nat. Methods 5, 943–945 (2008).
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Bonifacino, J. S.

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
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M. J. Booth, “Adaptive optics in microscopy,” Philos. Trans. Ser. A 365, 2829–2843 (2007).
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J. Fölling, M. Bossi, H. Bock, R. Medda, C. A. Wurm, B. Hein, S. Jakobs, C. Eggeling, and S. W. Hell, “Fluorescence nanoscopy by ground-state depletion and single-molecule return,” Nat. Methods 5, 943–945 (2008).
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Bunt, G.

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M. Gustafsson, L. Shao, and P. Carlton, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94, 4957–4970 (2008).
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A. G. York, P. Chandris, D. D. 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. Methods 10, 1122–1126 (2013).
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B. Thomas, A. Wolstenholme, S. N. Chaudhari, E. T. Kipreos, and P. Kner, “Enhanced resolution through thick tissue with structured illumination and adaptive optics,” J. Biomed. Opt. 20, 026006 (2015).
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D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349, aab3500 (2015).
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B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, W. Michael, C. Janetopoulos, X. S. Wu, J. A. H. Iii, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. Serdar, D. P. Kiehart, and E. Betzig, “Lattice light sheet microscopy: imaging molecules, cells, and embryos at high spatiotemporal resolution,” Science 346, 1257998 (2014).

Chen, D. C.

Chen, S.-J.

Cheng, L.-C.

Chien, F.-C.

Chitnis, A.

P. W. Winter, A. G. York, D. D. 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, 181–191 (2014).
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A. G. York, P. Chandris, D. D. 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. Methods 10, 1122–1126 (2013).
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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. Methods 9, 749–754 (2012).
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A. Chmyrov, J. Keller, T. Grotjohann, M. Ratz, E. D’Este, S. Jakobs, C. Eggeling, and S. W. Hell, “Nanoscopy with more than 100, 000 ‘doughnuts’,” Nat. Methods 10, 737–740 (2013).
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Cremer, C.

S. Rossberger, G. Best, D. Baddeley, R. Heintzmann, U. Birk, S. Dithmar, and C. Cremer, “Combination of structured illumination and single molecule localization microscopy in one setup,” J. Opt. 15, 094003 (2013).
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R. Heintzmann, T. M. Jovin, and C. Cremer, “Saturated patterned excitation microscopy: a concept for optical resolution improvement,” J. Opt. Soc. Am. A 19, 1599–1609 (2002).
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R. Heintzmann and C. Cremer, “Laterally modulated excitation microscopy: improvement of resolution by using a diffraction grating,” Proc. SPIE 3568, 185–196 (1999).
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A. Chmyrov, J. Keller, T. Grotjohann, M. Ratz, E. D’Este, S. Jakobs, C. Eggeling, and S. W. Hell, “Nanoscopy with more than 100, 000 ‘doughnuts’,” Nat. Methods 10, 737–740 (2013).
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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. Methods 9, 749–754 (2012).
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D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349, aab3500 (2015).
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J. R. Allen, S. T. Ross, and M. W. Davidson, “Structured illumination microscopy for superresolution,” Chem. Phys. Chem. 15, 566–576 (2014).

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E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313, 1642–1645 (2006).
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G. Ball, R. M. Parton, R. S. Hamilton, and I. Davis, A Cell Biologist’s Guide to High Resolution Imaging, 1st ed. (Elsevier, 2012), Vol. 504.

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W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248, 73–76 (1990).
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S. Rossberger, G. Best, D. Baddeley, R. Heintzmann, U. Birk, S. Dithmar, and C. Cremer, “Combination of structured illumination and single molecule localization microscopy in one setup,” J. Opt. 15, 094003 (2013).
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Eggeling, C.

A. Chmyrov, J. Keller, T. Grotjohann, M. Ratz, E. D’Este, S. Jakobs, C. Eggeling, and S. W. Hell, “Nanoscopy with more than 100, 000 ‘doughnuts’,” Nat. Methods 10, 737–740 (2013).
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J. Fölling, M. Bossi, H. Bock, R. Medda, C. A. Wurm, B. Hein, S. Jakobs, C. Eggeling, and S. W. Hell, “Fluorescence nanoscopy by ground-state depletion and single-molecule return,” Nat. Methods 5, 943–945 (2008).
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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,” Proc. Natl. Acad. Sci. USA 110, 21000–21005 (2013).
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B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, W. Michael, C. Janetopoulos, X. S. Wu, J. A. H. Iii, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. Serdar, D. P. Kiehart, and E. Betzig, “Lattice light sheet microscopy: imaging molecules, cells, and embryos at high spatiotemporal resolution,” Science 346, 1257998 (2014).

Ertsgaard, C. T.

C. T. Ertsgaard, R. M. Mckoskey, I. S. Rich, and N. C. Lindquist, “Dynamic placement of plasmonic hotspots for super-resolution surface-enhanced Raman scattering,” ACS Nano 8, 10941–10946 (2014).
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A. G. York, P. Chandris, D. D. 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. Methods 10, 1122–1126 (2013).
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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. Methods 9, 749–754 (2012).
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J. Fölling, M. Bossi, H. Bock, R. Medda, C. A. Wurm, B. Hein, S. Jakobs, C. Eggeling, and S. W. Hell, “Fluorescence nanoscopy by ground-state depletion and single-molecule return,” Nat. Methods 5, 943–945 (2008).
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S. T. Hess, T. P. K. Girirajan, and M. D. Mason, “Ultra-high resolution imaging by fluorescence photoactivation localization microscopy,” Biophys. J. 91, 4258–4272 (2006).
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Großhans, 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,” Proc. Natl. Acad. Sci. USA 110, 21000–21005 (2013).
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A. Chmyrov, J. Keller, T. Grotjohann, M. Ratz, E. D’Este, S. Jakobs, C. Eggeling, and S. W. Hell, “Nanoscopy with more than 100, 000 ‘doughnuts’,” Nat. Methods 10, 737–740 (2013).
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E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, and M. G. L. Gustafsson, “PNAS plus: nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution,” Proc. Natl. Acad. Sci. USA 109, E135–E143 (2012).
[Crossref]

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Figures (8)

Fig. 1.
Fig. 1.

Illumination modes in (a) wide-field imaging, (b) wide-field SIM, and (c) spot-scanning SIM. (b) In wide-field SIM, two laser beams illuminate the back focal plane of the condenser lens to form an interference pattern in the sample plane. Placing the foci of the illumination beams close to the periphery of the entrance pupil of the illumination condenser generates an illumination pattern with high spatial frequency on the sample; the higher this frequency, the better the achievable resolution. The effective OTF is then a convolution of the objective OTF and the spatial frequency spectrum of the illumination pattern (three delta functions). (c) The same principle holds true for spot-scanning SIM. Here, the back focal plane of the objective is filled completely with illumination light, thus producing a diffraction-limited spot in the sample plane. The spatial frequency content of the effective OTF is again the convolution of the spatial frequency content in the illumination pattern and the objective’s OTF. (a) In wide-field imaging, this convolution is performed with a delta function; i.e., the OTF support is not increased.

Fig. 2.
Fig. 2.

PSF in a confocal microscope. Depending on the setup of a confocal microscope, its resolving power changes as described by Eq. (4). (a) If a diffraction-limited spot is illuminated but all of the generated fluorescence is imaged onto a large photodiode (convolution with D ( x ) 1 ), the resulting resolution is the PSF of the excitation light. (b) If the whole sample is illuminated but only a tiny part of the fluorescence is transmitted onto the detector—the rest is blocked by a pinhole—then the resolution as defined by the detection PSF is achieved. (c) Combining both point illumination and point detection with a tiny pinhole offers doubled resolution in the form of a confocal PSF that is the multiplication of the excitation and detection PSF. AU, Airy unit.

Fig. 3.
Fig. 3.

Comparison of spot-scanning SIM techniques. In a conventional scanning confocal microscope, superresolution can only be achieved if a small pinhole is used [12], which is not practicable due to low signal levels in this case. In ISM [33], the point detector is replaced by a detector array to capture the entire shape of the excitation spot for each scan position in an individual image and process those images accordingly. In MSIM [37], the long acquisition time (10 min) of ISM is decreased via heavy parallelization of the imaging process, boosting fram-rates 1000-fold. OPRA [40] is an all-optical implementation of ISM in the sense that all the postprocessing is done on the fly using additional lenses and scanner units to produce a superresolved image directly on the camera. Due to the limited speed of the scanners, the frame rate of OPRA is limited to 0.5 frames per second [39]. This limit can be overcome, similar to MSIM, via parallelization: the respective technique is called instant SIM, or iSIM [34,42]. This technique can provide imaging rates of over 100 frames per second through the use of multifocal illumination patterns in combination with microlens arrays for analogue processing in superresolution, and can thus outperform other SIM modalities in terms of imaging speed.

Fig. 4.
Fig. 4.

Superresolution imaging, deep and fast. (a)–(c) iSIM is the fastest SIM technique to date (to our knowledge) and was used here to unveil the dynamics of the endoplasmic reticulum in human lung fibroblasts at frame rates of 100 Hz. The images reveal the rapid polymerization and depolymerization of the microtubule constituting the endoplasmic reticulum scaffold, revealing details that had been invisible before the advent of iSIM. Scale bars are 10 μm, 5 μm, and 200 nm, respectively. (d), (e) For deep tissue imaging, two-photon MSIM can be used, which enhances both resolution and, importantly, contrast when compared to conventional wide-field imaging. Shown is the salivary gland of a Drosophila melanogaster imaged (d) in wide-field and (e) by two-photon MSIM [44] in x z view (Scale bar 5 μm), imaged at 40 μm depth in the sample. Reprinted by permission from Macmillan Publishers Ltd: [Nature Methods] [34] copyright (2013) and from Ingaramo et al. [44].

Fig. 5.
Fig. 5.

Two-photon imaging with an all-optical ISM system. (a) Anesthetized nematode larva imaged in two colors. The larva’s neurons expressing the protein GFP are clearly visible in green. The body of the larva was imaged using autofluorescence and appears red in the image. (b)–(f) Enlarged regions demonstrate the power of this technique to visualize biological processes inside live animal neurons. The yellow and magenta arrows point to fascicles of the nerve cords. (g) Eye of a 40 h old zebrafish. The images visualize the microtubule network inside the eye, and the magenta arrows point to locations where cells undergo mitosis, clearly visible from the opposing arrangement of microtubule bundles. Images reprinted from Winter et al. [45], with permission. Scale bars: (a) 60 μm; (b) 20 μm; (c), (d) 4 μm; (e), (f) 5 μm.

Fig. 6.
Fig. 6.

Principle of resolution improvement in plasmonic SIM. In conventional mounting media such as air, water, or oil, the relation between the angular frequency ω and the wave vector k of the illumination light is linear. Hence, the maximum resolution in conventional SIM, as defined by the sum frequency of illumination wave vector k air and emission wave vector k em k air , is approximately twice that of wide-field imaging. At the interface between a metal and an insulator, the dispersion relationship becomes nonlinear, due to the influence of the materials’ dielectric functions ε 1 and ε 2 , which are themselves functions of ω . It is therefore possible to generate spatial frequencies that are far beyond those permitted by the diffraction limit in conventional imaging media. Note that this is not inconsistent with Abbe theory, because plasmons are near-field phenomena and thus not constrained by diffraction.

Fig. 7.
Fig. 7.

Pattern generation in plasmonic SIM (PSIM). In contrast to conventional SIM, only a single illumination beam is required in PSIM. A plasmonic standing wave pattern can be created with a single wave incident on a metal coated coverslip, featuring tiny slits that are periodically distributed on the surface on a micrometer scale [60]. The angle of incidence of the excitation light is as close as possible to the SPP acceptance angle θ SPP . Due to the slits, the illumination light can couple into the coating and travel along the surface in both directions from the slit. The interference of two counterpropagating SPPs thus creates a fringe pattern with spatial frequency k SPP that is beyond the cutoff frequency of conventional SIM.

Fig. 8.
Fig. 8.

Pattern generation in localized plasmon SIM (LPSIM). (a) Light from a single beam incident on a nanostructured substrate creates localized plasmon resonances with dimensions below the diffraction limit. Note that the angle of incidence θ is not critical in generating localized plasmons and can be very different from the acceptance angle θ SPP required for PSIM (see Fig. 7). However, the shape of the localized plasmon field pattern is strongly dependent on θ , as shown in (b)–(f), and can thus be as a method to induce “pattern shifts” as required for the reconstruction of superresolved images from the raw data. In this configuration the limiting factor is not the diffraction of light but the precision at which nanostructures and field patterns can be produced. Images in (a)–(f) are adapted from Ponsetto et al. [65] with permission of The Royal Society of Chemistry. LPSIM is compatible also with marker-free imaging and could be combined with surface enhanced Raman spectroscopy (SERS) [67]. That this is, in principle, possible is shown in (g), which represents an optical micrograph of a collagen fibril, and (h), the respective superresolved LPSIM-SERS image. The color scale represents the relative intensity of the detected signal. Images in (g), (h) reprinted with permission from C. T. Ertsgaard, R. M. Mckoskey, I. S. Rich, and N. C. Lindquist, “Dynamic Placement of Plasmonic Hotspots for Super-Resolution Surface-Enhanced Raman Scattering,” ACS Nano 8, 10941–10946 (2014).Copyright (2014) American Chemical Society.

Tables (1)

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Table 1. Comparison of Spot-Scanning SIM and Plasmonic Wide-Field SIM

Equations (6)

Equations on this page are rendered with MathJax. Learn more.

i ( x ) = [ s ( x ) × e ( x ) ] h ( x ) .
I ( k ) = [ S ( k ) E ( k ) ] × H ( k ) .
I ( k ) = [ S ( k ) ( δ ( k ) + 1 2 δ ( k k e ) + 1 2 δ ( k + k e ) ) ] × H ( k ) = [ S ( k ) + 1 2 S ( k k e ) + 1 2 S ( k + k e ) ] × H ( k ) .
i ( x ) = [ h ex ( x ) δ ( x ) ] × [ h det ( x ) D ( x ) ] .
k = ω c .
k SPP = ω c ( ε metal ( ω ) ε insulator ( ω ) ε metal ( ω ) + ε insulator ( ω ) ) 1 2 .

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