Abstract

Super-resolution imaging with photo-activatable or photo-switchable probes is a promising tool in biological applications to reveal previously unresolved intra-cellular details with visible light. This field benefits from developments in the areas of molecular probes, optical systems, and computational post-processing of the data. The joint design of optics and reconstruction processes using double-helix point spread functions (DH-PSF) provides high resolution three-dimensional (3D) imaging over a long depth-of-field. We demonstrate for the first time a method integrating a Fisher information efficient DH-PSF design, a surface relief optical phase mask, and an optimal 3D localization estimator. 3D super-resolution imaging using photo-switchable dyes reveals the 3D microtubule network in mammalian cells with localization precision approaching the information theoretical limit over a depth of 1.2 µm.

© 2012 OSA

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2012 (1)

S. Quirin, S. R. P. Pavani, and R. Piestun, “Optimal 3D single-molecule localization for superresolution microscopy with aberrations and engineered point spread functions,” Proc. Natl. Acad. Sci. U.S.A. 109(3), 675–679 (2012).
[CrossRef] [PubMed]

2011 (6)

D. B. Conkey, R. P. Trivedi, S. R. P. Pavani, I. I. Smalyukh, and R. Piestun, “Three-dimensional parallel particle manipulation and tracking by integrating holographic optical tweezers and engineered point spread functions,” Opt. Express 19(5), 3835–3842 (2011).
[CrossRef] [PubMed]

G. Grover, S. Quirin, C. Fiedler, and R. Piestun, “Photon efficient double-helix PSF microscopy with application to 3D photo-activation localization imaging,” Biomed. Opt. Express 2(11), 3010–3020 (2011).
[CrossRef] [PubMed]

D. Baddeley, M. B. Cannell, and C. Soeller, “Three-dimensional sub-100 nm super-resolution imaging of biological samples using a phase ramp in the objective pupil,” Nano Research 4(6), 589–598 (2011).
[CrossRef]

D. Aquino, A. Schönle, C. Geisler, C. V. Middendorff, C. A. Wurm, Y. Okamura, T. Lang, S. W. Hell, and A. Egner, “Two-color nanoscopy of three-dimensional volumes by 4Pi detection of stochastically switched fluorophores,” Nat. Methods 8(4), 353–359 (2011).
[CrossRef] [PubMed]

S. A. Jones, S.-H. Shim, J. He, and X. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods 8(6), 499–505 (2011).
[CrossRef] [PubMed]

F. Cella Zanacchi, Z. Lavagnino, M. Perrone Donnorso, A. Del Bue, L. Furia, M. Faretta, and A. Diaspro, “Live-cell 3D super-resolution imaging in thick biological samples,” Nat. Methods 8(12), 1047–1049 (2011).
[CrossRef] [PubMed]

2010 (6)

J. Tang, J. Akerboom, A. Vaziri, L. L. Looger, and C. V. Shank, “Near-isotropic 3D optical nanoscopy with photon-limited chromophores,” Proc. Natl. Acad. Sci. U.S.A. 107(22), 10068–10073 (2010).
[CrossRef] [PubMed]

G. Grover, S. R. P. Pavani, and R. Piestun, “Performance limits on three-dimensional particle localization in photon-limited microscopy,” Opt. Lett. 35(19), 3306–3308 (2010).
[CrossRef] [PubMed]

M. A. Thompson, M. D. Lew, M. Badieirostami, and W. E. Moerner, “Localizing and tracking single nanoscale emitters in three dimensions with high spatiotemporal resolution using a double-helix point spread function,” Nano Lett. 10(1), 211–218 (2010).
[CrossRef] [PubMed]

M. A. Thompson, J. M. Casolari, M. Badieirostami, P. O. Brown, and W. E. Moerner, “Three-dimensional tracking of single mRNA particles in Saccharomyces cerevisiae using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 107(42), 17864–17871 (2010).
[CrossRef] [PubMed]

S. Wolter, M. Schüttpelz, M. Tscherepanow, S. VAN DE Linde, M. Heilemann, and M. Sauer, “Real-time computation of subdiffraction-resolution fluorescence images,” J. Microsc. 237(1), 12–22 (2010).
[CrossRef] [PubMed]

K. I. Mortensen, L. S. Churchman, J. A. Spudich, and H. Flyvbjerg, “Optimized localization analysis for single-molecule tracking and super-resolution microscopy,” Nat. Methods 7(5), 377–381 (2010).
[CrossRef] [PubMed]

2009 (3)

S. R. P. Pavani, A. Greengard, and R. Piestun, “Three-dimensional localization with nanometer accuracy using a detector-limited double-helix point spread function system,” Appl. Phys. Lett. 95(2), 021103 (2009).
[CrossRef]

G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
[CrossRef] [PubMed]

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 2995–2999 (2009).
[CrossRef] [PubMed]

2008 (8)

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

R. Schmidt, C. A. Wurm, S. Jakobs, J. Engelhardt, A. Egner, and S. W. Hell, “Spherical nanosized focal spot unravels the interior of cells,” Nat. Methods 5(6), 539–544 (2008).
[CrossRef] [PubMed]

M. Heilemann, S. van de Linde, M. Schüttpelz, R. Kasper, B. Seefeldt, A. Mukherjee, P. Tinnefeld, and M. Sauer, “Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes,” Angew. Chem. Int. Ed. Engl. 47(33), 6172–6176 (2008).
[CrossRef] [PubMed]

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(11), 943–945 (2008).
[CrossRef] [PubMed]

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[CrossRef] [PubMed]

M. F. Juette, T. J. Gould, M. D. Lessard, M. J. Mlodzianoski, B. S. Nagpure, B. T. Bennett, S. T. Hess, and J. Bewersdorf, “Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples,” Nat. Methods 5(6), 527–529 (2008).
[CrossRef] [PubMed]

S. R. P. Pavani and R. Piestun, “High-efficiency rotating point spread functions,” Opt. Express 16(5), 3484–3489 (2008).
[CrossRef] [PubMed]

S. R. P. Pavani and R. Piestun, “Three dimensional tracking of fluorescent microparticles using a photon-limited double-helix response system,” Opt. Express 16(26), 22048–22057 (2008).
[CrossRef] [PubMed]

2007 (3)

M. Bates, B. Huang, G. T. Dempsey, and X. Zhuang, “Multicolor super-resolution imaging with photo-switchable fluorescent probes,” Science 317(5845), 1749–1753 (2007).
[CrossRef] [PubMed]

M. H. Ulbrich and E. Y. Isacoff, “Subunit counting in membrane-bound proteins,” Nat. Methods 4(4), 319–321 (2007).
[PubMed]

S. Ram, J. Chao, P. Prabhat, E. S. Ward, and R. J. Ober, “A novel approach to determining the three-dimensional location of microscopic objects with applications to 3D particle tracking,” Proc. SPIE64430D, 64430D-7 (2007).
[CrossRef]

2006 (4)

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

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(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

S. T. Hess, T. P. K. Girirajan, and M. D. Mason, “Ultra-high resolution imaging by fluorescence photoactivation localization microscopy,” Biophys. J. 91(11), 4258–4272 (2006).
[CrossRef] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[CrossRef] [PubMed]

2002 (1)

R. Piestun and J. Shamir, “Synthesis of three-dimensional light fields and applications,” Proc. IEEE 90(2), 222–244 (2002).
[CrossRef]

1996 (1)

Y. Y. Schechner, R. Piestun, and J. Shamir, “Wave propagation with rotating intensity distributions,” Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 54(1), R50–R53 (1996).
[CrossRef] [PubMed]

1993 (1)

G. Indebetouw, “Optical Vortices and Their Propagation,” J. Mod. Opt. 40(1), 73–87 (1993).
[CrossRef]

1873 (1)

E. Abbe, “Contributions to the theory of the microscope and microscopic observations (translated from German),” Archiv für Mikroskopische Anatomie 9, 413–468 (1873).
[CrossRef]

Abbe, E.

E. Abbe, “Contributions to the theory of the microscope and microscopic observations (translated from German),” Archiv für Mikroskopische Anatomie 9, 413–468 (1873).
[CrossRef]

Agard, D. A.

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

Akerboom, J.

J. Tang, J. Akerboom, A. Vaziri, L. L. Looger, and C. V. Shank, “Near-isotropic 3D optical nanoscopy with photon-limited chromophores,” Proc. Natl. Acad. Sci. U.S.A. 107(22), 10068–10073 (2010).
[CrossRef] [PubMed]

Aquino, D.

D. Aquino, A. Schönle, C. Geisler, C. V. Middendorff, C. A. Wurm, Y. Okamura, T. Lang, S. W. Hell, and A. Egner, “Two-color nanoscopy of three-dimensional volumes by 4Pi detection of stochastically switched fluorophores,” Nat. Methods 8(4), 353–359 (2011).
[CrossRef] [PubMed]

Baddeley, D.

D. Baddeley, M. B. Cannell, and C. Soeller, “Three-dimensional sub-100 nm super-resolution imaging of biological samples using a phase ramp in the objective pupil,” Nano Research 4(6), 589–598 (2011).
[CrossRef]

Badieirostami, M.

M. A. Thompson, J. M. Casolari, M. Badieirostami, P. O. Brown, and W. E. Moerner, “Three-dimensional tracking of single mRNA particles in Saccharomyces cerevisiae using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 107(42), 17864–17871 (2010).
[CrossRef] [PubMed]

M. A. Thompson, M. D. Lew, M. Badieirostami, and W. E. Moerner, “Localizing and tracking single nanoscale emitters in three dimensions with high spatiotemporal resolution using a double-helix point spread function,” Nano Lett. 10(1), 211–218 (2010).
[CrossRef] [PubMed]

Bates, M.

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[CrossRef] [PubMed]

M. Bates, B. Huang, G. T. Dempsey, and X. Zhuang, “Multicolor super-resolution imaging with photo-switchable fluorescent probes,” Science 317(5845), 1749–1753 (2007).
[CrossRef] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[CrossRef] [PubMed]

Bennett, B. T.

M. F. Juette, T. J. Gould, M. D. Lessard, M. J. Mlodzianoski, B. S. Nagpure, B. T. Bennett, S. T. Hess, and J. Bewersdorf, “Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples,” Nat. Methods 5(6), 527–529 (2008).
[CrossRef] [PubMed]

Betzig, E.

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(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Bewersdorf, J.

M. F. Juette, T. J. Gould, M. D. Lessard, M. J. Mlodzianoski, B. S. Nagpure, B. T. Bennett, S. T. Hess, and J. Bewersdorf, “Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples,” Nat. Methods 5(6), 527–529 (2008).
[CrossRef] [PubMed]

Biteen, J. S.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 2995–2999 (2009).
[CrossRef] [PubMed]

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(11), 943–945 (2008).
[CrossRef] [PubMed]

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(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Bossi, M.

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(11), 943–945 (2008).
[CrossRef] [PubMed]

Brown, P. O.

M. A. Thompson, J. M. Casolari, M. Badieirostami, P. O. Brown, and W. E. Moerner, “Three-dimensional tracking of single mRNA particles in Saccharomyces cerevisiae using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 107(42), 17864–17871 (2010).
[CrossRef] [PubMed]

Burke, B.

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

Cannell, M. B.

D. Baddeley, M. B. Cannell, and C. Soeller, “Three-dimensional sub-100 nm super-resolution imaging of biological samples using a phase ramp in the objective pupil,” Nano Research 4(6), 589–598 (2011).
[CrossRef]

Cardoso, M. C.

L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. L. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
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M. Bates, B. Huang, G. T. Dempsey, and X. Zhuang, “Multicolor super-resolution imaging with photo-switchable fluorescent probes,” Science 317(5845), 1749–1753 (2007).
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F. Cella Zanacchi, Z. Lavagnino, M. Perrone Donnorso, A. Del Bue, L. Furia, M. Faretta, and A. Diaspro, “Live-cell 3D super-resolution imaging in thick biological samples,” Nat. Methods 8(12), 1047–1049 (2011).
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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(11), 943–945 (2008).
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D. Aquino, A. Schönle, C. Geisler, C. V. Middendorff, C. A. Wurm, Y. Okamura, T. Lang, S. W. Hell, and A. Egner, “Two-color nanoscopy of three-dimensional volumes by 4Pi detection of stochastically switched fluorophores,” Nat. Methods 8(4), 353–359 (2011).
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R. Schmidt, C. A. Wurm, S. Jakobs, J. Engelhardt, A. Egner, and S. W. Hell, “Spherical nanosized focal spot unravels the interior of cells,” Nat. Methods 5(6), 539–544 (2008).
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F. Cella Zanacchi, Z. Lavagnino, M. Perrone Donnorso, A. Del Bue, L. Furia, M. Faretta, and A. Diaspro, “Live-cell 3D super-resolution imaging in thick biological samples,” Nat. Methods 8(12), 1047–1049 (2011).
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G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
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Flyvbjerg, H.

K. I. Mortensen, L. S. Churchman, J. A. Spudich, and H. Flyvbjerg, “Optimized localization analysis for single-molecule tracking and super-resolution microscopy,” Nat. Methods 7(5), 377–381 (2010).
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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(11), 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(11), 4258–4272 (2006).
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L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. L. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
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D. Aquino, A. Schönle, C. Geisler, C. V. Middendorff, C. A. Wurm, Y. Okamura, T. Lang, S. W. Hell, and A. Egner, “Two-color nanoscopy of three-dimensional volumes by 4Pi detection of stochastically switched fluorophores,” Nat. Methods 8(4), 353–359 (2011).
[CrossRef] [PubMed]

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G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
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Hess, S. T.

M. F. Juette, T. J. Gould, M. D. Lessard, M. J. Mlodzianoski, B. S. Nagpure, B. T. Bennett, S. T. Hess, and J. Bewersdorf, “Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples,” Nat. Methods 5(6), 527–529 (2008).
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M. Bates, B. Huang, G. T. Dempsey, and X. Zhuang, “Multicolor super-resolution imaging with photo-switchable fluorescent probes,” Science 317(5845), 1749–1753 (2007).
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G. Indebetouw, “Optical Vortices and Their Propagation,” J. Mod. Opt. 40(1), 73–87 (1993).
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R. Schmidt, C. A. Wurm, S. Jakobs, J. Engelhardt, A. Egner, and S. W. Hell, “Spherical nanosized focal spot unravels the interior of cells,” Nat. Methods 5(6), 539–544 (2008).
[CrossRef] [PubMed]

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(11), 943–945 (2008).
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S. A. Jones, S.-H. Shim, J. He, and X. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods 8(6), 499–505 (2011).
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M. F. Juette, T. J. Gould, M. D. Lessard, M. J. Mlodzianoski, B. S. Nagpure, B. T. Bennett, S. T. Hess, and J. Bewersdorf, “Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples,” Nat. Methods 5(6), 527–529 (2008).
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G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
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M. Heilemann, S. van de Linde, M. Schüttpelz, R. Kasper, B. Seefeldt, A. Mukherjee, P. Tinnefeld, and M. Sauer, “Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes,” Angew. Chem. Int. Ed. Engl. 47(33), 6172–6176 (2008).
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L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. L. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
[CrossRef] [PubMed]

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D. Aquino, A. Schönle, C. Geisler, C. V. Middendorff, C. A. Wurm, Y. Okamura, T. Lang, S. W. Hell, and A. Egner, “Two-color nanoscopy of three-dimensional volumes by 4Pi detection of stochastically switched fluorophores,” Nat. Methods 8(4), 353–359 (2011).
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F. Cella Zanacchi, Z. Lavagnino, M. Perrone Donnorso, A. Del Bue, L. Furia, M. Faretta, and A. Diaspro, “Live-cell 3D super-resolution imaging in thick biological samples,” Nat. Methods 8(12), 1047–1049 (2011).
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L. Schermelleh, P. M. Carlton, S. Haase, L. Shao, L. Winoto, P. Kner, B. Burke, M. C. Cardoso, D. A. Agard, M. G. L. Gustafsson, H. Leonhardt, and J. W. Sedat, “Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy,” Science 320(5881), 1332–1336 (2008).
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M. F. Juette, T. J. Gould, M. D. Lessard, M. J. Mlodzianoski, B. S. Nagpure, B. T. Bennett, S. T. Hess, and J. Bewersdorf, “Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples,” Nat. Methods 5(6), 527–529 (2008).
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M. A. Thompson, M. D. Lew, M. Badieirostami, and W. E. Moerner, “Localizing and tracking single nanoscale emitters in three dimensions with high spatiotemporal resolution using a double-helix point spread function,” Nano Lett. 10(1), 211–218 (2010).
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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(5793), 1642–1645 (2006).
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G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
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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(5793), 1642–1645 (2006).
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S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 2995–2999 (2009).
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J. Tang, J. Akerboom, A. Vaziri, L. L. Looger, and C. V. Shank, “Near-isotropic 3D optical nanoscopy with photon-limited chromophores,” Proc. Natl. Acad. Sci. U.S.A. 107(22), 10068–10073 (2010).
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G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
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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(11), 4258–4272 (2006).
[CrossRef] [PubMed]

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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(11), 943–945 (2008).
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D. Aquino, A. Schönle, C. Geisler, C. V. Middendorff, C. A. Wurm, Y. Okamura, T. Lang, S. W. Hell, and A. Egner, “Two-color nanoscopy of three-dimensional volumes by 4Pi detection of stochastically switched fluorophores,” Nat. Methods 8(4), 353–359 (2011).
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M. F. Juette, T. J. Gould, M. D. Lessard, M. J. Mlodzianoski, B. S. Nagpure, B. T. Bennett, S. T. Hess, and J. Bewersdorf, “Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples,” Nat. Methods 5(6), 527–529 (2008).
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M. A. Thompson, J. M. Casolari, M. Badieirostami, P. O. Brown, and W. E. Moerner, “Three-dimensional tracking of single mRNA particles in Saccharomyces cerevisiae using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 107(42), 17864–17871 (2010).
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M. A. Thompson, M. D. Lew, M. Badieirostami, and W. E. Moerner, “Localizing and tracking single nanoscale emitters in three dimensions with high spatiotemporal resolution using a double-helix point spread function,” Nano Lett. 10(1), 211–218 (2010).
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S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 2995–2999 (2009).
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K. I. Mortensen, L. S. Churchman, J. A. Spudich, and H. Flyvbjerg, “Optimized localization analysis for single-molecule tracking and super-resolution microscopy,” Nat. Methods 7(5), 377–381 (2010).
[CrossRef] [PubMed]

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M. Heilemann, S. van de Linde, M. Schüttpelz, R. Kasper, B. Seefeldt, A. Mukherjee, P. Tinnefeld, and M. Sauer, “Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes,” Angew. Chem. Int. Ed. Engl. 47(33), 6172–6176 (2008).
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M. F. Juette, T. J. Gould, M. D. Lessard, M. J. Mlodzianoski, B. S. Nagpure, B. T. Bennett, S. T. Hess, and J. Bewersdorf, “Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples,” Nat. Methods 5(6), 527–529 (2008).
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S. Ram, J. Chao, P. Prabhat, E. S. Ward, and R. J. Ober, “A novel approach to determining the three-dimensional location of microscopic objects with applications to 3D particle tracking,” Proc. SPIE64430D, 64430D-7 (2007).
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D. Aquino, A. Schönle, C. Geisler, C. V. Middendorff, C. A. Wurm, Y. Okamura, T. Lang, S. W. Hell, and A. Egner, “Two-color nanoscopy of three-dimensional volumes by 4Pi detection of stochastically switched fluorophores,” Nat. Methods 8(4), 353–359 (2011).
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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(5793), 1642–1645 (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(5793), 1642–1645 (2006).
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Pavani, S. R. P.

S. Quirin, S. R. P. Pavani, and R. Piestun, “Optimal 3D single-molecule localization for superresolution microscopy with aberrations and engineered point spread functions,” Proc. Natl. Acad. Sci. U.S.A. 109(3), 675–679 (2012).
[CrossRef] [PubMed]

D. B. Conkey, R. P. Trivedi, S. R. P. Pavani, I. I. Smalyukh, and R. Piestun, “Three-dimensional parallel particle manipulation and tracking by integrating holographic optical tweezers and engineered point spread functions,” Opt. Express 19(5), 3835–3842 (2011).
[CrossRef] [PubMed]

G. Grover, S. R. P. Pavani, and R. Piestun, “Performance limits on three-dimensional particle localization in photon-limited microscopy,” Opt. Lett. 35(19), 3306–3308 (2010).
[CrossRef] [PubMed]

S. R. P. Pavani, A. Greengard, and R. Piestun, “Three-dimensional localization with nanometer accuracy using a detector-limited double-helix point spread function system,” Appl. Phys. Lett. 95(2), 021103 (2009).
[CrossRef]

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 2995–2999 (2009).
[CrossRef] [PubMed]

S. R. P. Pavani and R. Piestun, “Three dimensional tracking of fluorescent microparticles using a photon-limited double-helix response system,” Opt. Express 16(26), 22048–22057 (2008).
[CrossRef] [PubMed]

S. R. P. Pavani and R. Piestun, “High-efficiency rotating point spread functions,” Opt. Express 16(5), 3484–3489 (2008).
[CrossRef] [PubMed]

Perrone Donnorso, M.

F. Cella Zanacchi, Z. Lavagnino, M. Perrone Donnorso, A. Del Bue, L. Furia, M. Faretta, and A. Diaspro, “Live-cell 3D super-resolution imaging in thick biological samples,” Nat. Methods 8(12), 1047–1049 (2011).
[CrossRef] [PubMed]

Piestun, R.

S. Quirin, S. R. P. Pavani, and R. Piestun, “Optimal 3D single-molecule localization for superresolution microscopy with aberrations and engineered point spread functions,” Proc. Natl. Acad. Sci. U.S.A. 109(3), 675–679 (2012).
[CrossRef] [PubMed]

G. Grover, S. Quirin, C. Fiedler, and R. Piestun, “Photon efficient double-helix PSF microscopy with application to 3D photo-activation localization imaging,” Biomed. Opt. Express 2(11), 3010–3020 (2011).
[CrossRef] [PubMed]

D. B. Conkey, R. P. Trivedi, S. R. P. Pavani, I. I. Smalyukh, and R. Piestun, “Three-dimensional parallel particle manipulation and tracking by integrating holographic optical tweezers and engineered point spread functions,” Opt. Express 19(5), 3835–3842 (2011).
[CrossRef] [PubMed]

G. Grover, S. R. P. Pavani, and R. Piestun, “Performance limits on three-dimensional particle localization in photon-limited microscopy,” Opt. Lett. 35(19), 3306–3308 (2010).
[CrossRef] [PubMed]

S. R. P. Pavani, A. Greengard, and R. Piestun, “Three-dimensional localization with nanometer accuracy using a detector-limited double-helix point spread function system,” Appl. Phys. Lett. 95(2), 021103 (2009).
[CrossRef]

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 2995–2999 (2009).
[CrossRef] [PubMed]

S. R. P. Pavani and R. Piestun, “Three dimensional tracking of fluorescent microparticles using a photon-limited double-helix response system,” Opt. Express 16(26), 22048–22057 (2008).
[CrossRef] [PubMed]

S. R. P. Pavani and R. Piestun, “High-efficiency rotating point spread functions,” Opt. Express 16(5), 3484–3489 (2008).
[CrossRef] [PubMed]

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

R. Piestun and J. Shamir, “Synthesis of three-dimensional light fields and applications,” Proc. IEEE 90(2), 222–244 (2002).
[CrossRef]

Y. Y. Schechner, R. Piestun, and J. Shamir, “Wave propagation with rotating intensity distributions,” Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 54(1), R50–R53 (1996).
[CrossRef] [PubMed]

Prabhat, P.

S. Ram, J. Chao, P. Prabhat, E. S. Ward, and R. J. Ober, “A novel approach to determining the three-dimensional location of microscopic objects with applications to 3D particle tracking,” Proc. SPIE64430D, 64430D-7 (2007).
[CrossRef]

Quirin, S.

S. Quirin, S. R. P. Pavani, and R. Piestun, “Optimal 3D single-molecule localization for superresolution microscopy with aberrations and engineered point spread functions,” Proc. Natl. Acad. Sci. U.S.A. 109(3), 675–679 (2012).
[CrossRef] [PubMed]

G. Grover, S. Quirin, C. Fiedler, and R. Piestun, “Photon efficient double-helix PSF microscopy with application to 3D photo-activation localization imaging,” Biomed. Opt. Express 2(11), 3010–3020 (2011).
[CrossRef] [PubMed]

Ram, S.

S. Ram, J. Chao, P. Prabhat, E. S. Ward, and R. J. Ober, “A novel approach to determining the three-dimensional location of microscopic objects with applications to 3D particle tracking,” Proc. SPIE64430D, 64430D-7 (2007).
[CrossRef]

Rust, M. J.

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[CrossRef] [PubMed]

Sauer, M.

S. Wolter, M. Schüttpelz, M. Tscherepanow, S. VAN DE Linde, M. Heilemann, and M. Sauer, “Real-time computation of subdiffraction-resolution fluorescence images,” J. Microsc. 237(1), 12–22 (2010).
[CrossRef] [PubMed]

M. Heilemann, S. van de Linde, M. Schüttpelz, R. Kasper, B. Seefeldt, A. Mukherjee, P. Tinnefeld, and M. Sauer, “Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes,” Angew. Chem. Int. Ed. Engl. 47(33), 6172–6176 (2008).
[CrossRef] [PubMed]

Schechner, Y. Y.

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

Y. Y. Schechner, R. Piestun, and J. Shamir, “Wave propagation with rotating intensity distributions,” Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 54(1), R50–R53 (1996).
[CrossRef] [PubMed]

Schermelleh, L.

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

Schmidt, R.

R. Schmidt, C. A. Wurm, S. Jakobs, J. Engelhardt, A. Egner, and S. W. Hell, “Spherical nanosized focal spot unravels the interior of cells,” Nat. Methods 5(6), 539–544 (2008).
[CrossRef] [PubMed]

Schönle, A.

D. Aquino, A. Schönle, C. Geisler, C. V. Middendorff, C. A. Wurm, Y. Okamura, T. Lang, S. W. Hell, and A. Egner, “Two-color nanoscopy of three-dimensional volumes by 4Pi detection of stochastically switched fluorophores,” Nat. Methods 8(4), 353–359 (2011).
[CrossRef] [PubMed]

Schüttpelz, M.

S. Wolter, M. Schüttpelz, M. Tscherepanow, S. VAN DE Linde, M. Heilemann, and M. Sauer, “Real-time computation of subdiffraction-resolution fluorescence images,” J. Microsc. 237(1), 12–22 (2010).
[CrossRef] [PubMed]

M. Heilemann, S. van de Linde, M. Schüttpelz, R. Kasper, B. Seefeldt, A. Mukherjee, P. Tinnefeld, and M. Sauer, “Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes,” Angew. Chem. Int. Ed. Engl. 47(33), 6172–6176 (2008).
[CrossRef] [PubMed]

Sedat, J. W.

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

Seefeldt, B.

M. Heilemann, S. van de Linde, M. Schüttpelz, R. Kasper, B. Seefeldt, A. Mukherjee, P. Tinnefeld, and M. Sauer, “Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes,” Angew. Chem. Int. Ed. Engl. 47(33), 6172–6176 (2008).
[CrossRef] [PubMed]

Shamir, J.

R. Piestun and J. Shamir, “Synthesis of three-dimensional light fields and applications,” Proc. IEEE 90(2), 222–244 (2002).
[CrossRef]

Y. Y. Schechner, R. Piestun, and J. Shamir, “Wave propagation with rotating intensity distributions,” Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 54(1), R50–R53 (1996).
[CrossRef] [PubMed]

Shank, C. V.

J. Tang, J. Akerboom, A. Vaziri, L. L. Looger, and C. V. Shank, “Near-isotropic 3D optical nanoscopy with photon-limited chromophores,” Proc. Natl. Acad. Sci. U.S.A. 107(22), 10068–10073 (2010).
[CrossRef] [PubMed]

Shao, L.

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

Shim, S.-H.

S. A. Jones, S.-H. Shim, J. He, and X. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods 8(6), 499–505 (2011).
[CrossRef] [PubMed]

Shtengel, G.

G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
[CrossRef] [PubMed]

Smalyukh, I. I.

Soeller, C.

D. Baddeley, M. B. Cannell, and C. Soeller, “Three-dimensional sub-100 nm super-resolution imaging of biological samples using a phase ramp in the objective pupil,” Nano Research 4(6), 589–598 (2011).
[CrossRef]

Sougrat, R.

G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
[CrossRef] [PubMed]

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(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Spudich, J. A.

K. I. Mortensen, L. S. Churchman, J. A. Spudich, and H. Flyvbjerg, “Optimized localization analysis for single-molecule tracking and super-resolution microscopy,” Nat. Methods 7(5), 377–381 (2010).
[CrossRef] [PubMed]

Tang, J.

J. Tang, J. Akerboom, A. Vaziri, L. L. Looger, and C. V. Shank, “Near-isotropic 3D optical nanoscopy with photon-limited chromophores,” Proc. Natl. Acad. Sci. U.S.A. 107(22), 10068–10073 (2010).
[CrossRef] [PubMed]

Thompson, M. A.

M. A. Thompson, J. M. Casolari, M. Badieirostami, P. O. Brown, and W. E. Moerner, “Three-dimensional tracking of single mRNA particles in Saccharomyces cerevisiae using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 107(42), 17864–17871 (2010).
[CrossRef] [PubMed]

M. A. Thompson, M. D. Lew, M. Badieirostami, and W. E. Moerner, “Localizing and tracking single nanoscale emitters in three dimensions with high spatiotemporal resolution using a double-helix point spread function,” Nano Lett. 10(1), 211–218 (2010).
[CrossRef] [PubMed]

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 2995–2999 (2009).
[CrossRef] [PubMed]

Tinnefeld, P.

M. Heilemann, S. van de Linde, M. Schüttpelz, R. Kasper, B. Seefeldt, A. Mukherjee, P. Tinnefeld, and M. Sauer, “Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes,” Angew. Chem. Int. Ed. Engl. 47(33), 6172–6176 (2008).
[CrossRef] [PubMed]

Trivedi, R. P.

Tscherepanow, M.

S. Wolter, M. Schüttpelz, M. Tscherepanow, S. VAN DE Linde, M. Heilemann, and M. Sauer, “Real-time computation of subdiffraction-resolution fluorescence images,” J. Microsc. 237(1), 12–22 (2010).
[CrossRef] [PubMed]

Twieg, R. J.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 2995–2999 (2009).
[CrossRef] [PubMed]

Ulbrich, M. H.

M. H. Ulbrich and E. Y. Isacoff, “Subunit counting in membrane-bound proteins,” Nat. Methods 4(4), 319–321 (2007).
[PubMed]

VAN DE Linde, S.

S. Wolter, M. Schüttpelz, M. Tscherepanow, S. VAN DE Linde, M. Heilemann, and M. Sauer, “Real-time computation of subdiffraction-resolution fluorescence images,” J. Microsc. 237(1), 12–22 (2010).
[CrossRef] [PubMed]

M. Heilemann, S. van de Linde, M. Schüttpelz, R. Kasper, B. Seefeldt, A. Mukherjee, P. Tinnefeld, and M. Sauer, “Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes,” Angew. Chem. Int. Ed. Engl. 47(33), 6172–6176 (2008).
[CrossRef] [PubMed]

Vaziri, A.

J. Tang, J. Akerboom, A. Vaziri, L. L. Looger, and C. V. Shank, “Near-isotropic 3D optical nanoscopy with photon-limited chromophores,” Proc. Natl. Acad. Sci. U.S.A. 107(22), 10068–10073 (2010).
[CrossRef] [PubMed]

Wang, W.

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[CrossRef] [PubMed]

Ward, E. S.

S. Ram, J. Chao, P. Prabhat, E. S. Ward, and R. J. Ober, “A novel approach to determining the three-dimensional location of microscopic objects with applications to 3D particle tracking,” Proc. SPIE64430D, 64430D-7 (2007).
[CrossRef]

Waterman, C. M.

G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
[CrossRef] [PubMed]

Winoto, L.

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

Wolter, S.

S. Wolter, M. Schüttpelz, M. Tscherepanow, S. VAN DE Linde, M. Heilemann, and M. Sauer, “Real-time computation of subdiffraction-resolution fluorescence images,” J. Microsc. 237(1), 12–22 (2010).
[CrossRef] [PubMed]

Wurm, C. A.

D. Aquino, A. Schönle, C. Geisler, C. V. Middendorff, C. A. Wurm, Y. Okamura, T. Lang, S. W. Hell, and A. Egner, “Two-color nanoscopy of three-dimensional volumes by 4Pi detection of stochastically switched fluorophores,” Nat. Methods 8(4), 353–359 (2011).
[CrossRef] [PubMed]

R. Schmidt, C. A. Wurm, S. Jakobs, J. Engelhardt, A. Egner, and S. W. Hell, “Spherical nanosized focal spot unravels the interior of cells,” Nat. Methods 5(6), 539–544 (2008).
[CrossRef] [PubMed]

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(11), 943–945 (2008).
[CrossRef] [PubMed]

Zhuang, X.

S. A. Jones, S.-H. Shim, J. He, and X. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods 8(6), 499–505 (2011).
[CrossRef] [PubMed]

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[CrossRef] [PubMed]

M. Bates, B. Huang, G. T. Dempsey, and X. Zhuang, “Multicolor super-resolution imaging with photo-switchable fluorescent probes,” Science 317(5845), 1749–1753 (2007).
[CrossRef] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[CrossRef] [PubMed]

Angew. Chem. Int. Ed. Engl. (1)

M. Heilemann, S. van de Linde, M. Schüttpelz, R. Kasper, B. Seefeldt, A. Mukherjee, P. Tinnefeld, and M. Sauer, “Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes,” Angew. Chem. Int. Ed. Engl. 47(33), 6172–6176 (2008).
[CrossRef] [PubMed]

Appl. Phys. Lett. (1)

S. R. P. Pavani, A. Greengard, and R. Piestun, “Three-dimensional localization with nanometer accuracy using a detector-limited double-helix point spread function system,” Appl. Phys. Lett. 95(2), 021103 (2009).
[CrossRef]

Archiv für Mikroskopische Anatomie (1)

E. Abbe, “Contributions to the theory of the microscope and microscopic observations (translated from German),” Archiv für Mikroskopische Anatomie 9, 413–468 (1873).
[CrossRef]

Biomed. Opt. Express (1)

Biophys. J. (1)

S. T. Hess, T. P. K. Girirajan, and M. D. Mason, “Ultra-high resolution imaging by fluorescence photoactivation localization microscopy,” Biophys. J. 91(11), 4258–4272 (2006).
[CrossRef] [PubMed]

J. Microsc. (1)

S. Wolter, M. Schüttpelz, M. Tscherepanow, S. VAN DE Linde, M. Heilemann, and M. Sauer, “Real-time computation of subdiffraction-resolution fluorescence images,” J. Microsc. 237(1), 12–22 (2010).
[CrossRef] [PubMed]

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G. Indebetouw, “Optical Vortices and Their Propagation,” J. Mod. Opt. 40(1), 73–87 (1993).
[CrossRef]

Nano Lett. (1)

M. A. Thompson, M. D. Lew, M. Badieirostami, and W. E. Moerner, “Localizing and tracking single nanoscale emitters in three dimensions with high spatiotemporal resolution using a double-helix point spread function,” Nano Lett. 10(1), 211–218 (2010).
[CrossRef] [PubMed]

Nano Research (1)

D. Baddeley, M. B. Cannell, and C. Soeller, “Three-dimensional sub-100 nm super-resolution imaging of biological samples using a phase ramp in the objective pupil,” Nano Research 4(6), 589–598 (2011).
[CrossRef]

Nat. Methods (9)

D. Aquino, A. Schönle, C. Geisler, C. V. Middendorff, C. A. Wurm, Y. Okamura, T. Lang, S. W. Hell, and A. Egner, “Two-color nanoscopy of three-dimensional volumes by 4Pi detection of stochastically switched fluorophores,” Nat. Methods 8(4), 353–359 (2011).
[CrossRef] [PubMed]

S. A. Jones, S.-H. Shim, J. He, and X. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods 8(6), 499–505 (2011).
[CrossRef] [PubMed]

F. Cella Zanacchi, Z. Lavagnino, M. Perrone Donnorso, A. Del Bue, L. Furia, M. Faretta, and A. Diaspro, “Live-cell 3D super-resolution imaging in thick biological samples,” Nat. Methods 8(12), 1047–1049 (2011).
[CrossRef] [PubMed]

M. F. Juette, T. J. Gould, M. D. Lessard, M. J. Mlodzianoski, B. S. Nagpure, B. T. Bennett, S. T. Hess, and J. Bewersdorf, “Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples,” Nat. Methods 5(6), 527–529 (2008).
[CrossRef] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[CrossRef] [PubMed]

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(11), 943–945 (2008).
[CrossRef] [PubMed]

R. Schmidt, C. A. Wurm, S. Jakobs, J. Engelhardt, A. Egner, and S. W. Hell, “Spherical nanosized focal spot unravels the interior of cells,” Nat. Methods 5(6), 539–544 (2008).
[CrossRef] [PubMed]

M. H. Ulbrich and E. Y. Isacoff, “Subunit counting in membrane-bound proteins,” Nat. Methods 4(4), 319–321 (2007).
[PubMed]

K. I. Mortensen, L. S. Churchman, J. A. Spudich, and H. Flyvbjerg, “Optimized localization analysis for single-molecule tracking and super-resolution microscopy,” Nat. Methods 7(5), 377–381 (2010).
[CrossRef] [PubMed]

Opt. Express (3)

Opt. Lett. (2)

Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics (1)

Y. Y. Schechner, R. Piestun, and J. Shamir, “Wave propagation with rotating intensity distributions,” Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 54(1), R50–R53 (1996).
[CrossRef] [PubMed]

Proc. IEEE (1)

R. Piestun and J. Shamir, “Synthesis of three-dimensional light fields and applications,” Proc. IEEE 90(2), 222–244 (2002).
[CrossRef]

Proc. Natl. Acad. Sci. U.S.A. (5)

S. Quirin, S. R. P. Pavani, and R. Piestun, “Optimal 3D single-molecule localization for superresolution microscopy with aberrations and engineered point spread functions,” Proc. Natl. Acad. Sci. U.S.A. 109(3), 675–679 (2012).
[CrossRef] [PubMed]

G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, “Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 3125–3130 (2009).
[CrossRef] [PubMed]

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106(9), 2995–2999 (2009).
[CrossRef] [PubMed]

J. Tang, J. Akerboom, A. Vaziri, L. L. Looger, and C. V. Shank, “Near-isotropic 3D optical nanoscopy with photon-limited chromophores,” Proc. Natl. Acad. Sci. U.S.A. 107(22), 10068–10073 (2010).
[CrossRef] [PubMed]

M. A. Thompson, J. M. Casolari, M. Badieirostami, P. O. Brown, and W. E. Moerner, “Three-dimensional tracking of single mRNA particles in Saccharomyces cerevisiae using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 107(42), 17864–17871 (2010).
[CrossRef] [PubMed]

Proc. SPIE (1)

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Supplementary Material (2)

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Figures (10)

Fig. 1
Fig. 1

SPINDLE PSF design with background noise. (a) and (b) are two DH-PSF (DH-1 and DH-S) pupil plane phase masks. (c) and (d) are cross-sections of two PSF designs (DH-1 and DH-S) optimized for different depth ranges and background noise. From left to right the images show the simulated PSF at various defocus positions for a 1.45NA microscope and λ = 660 nm. The scale bar is 500 nm. (e) Comparison of 3D localization methods via the Average Cramer Rao Bound (CRB3D) over 1 µm range with changing background. The calculation parameters for shot-noise limited CRB are 1.45NA 100X system, λ = 660 nm, pixel size = 16 µm, 3000 detected photons at focus. No readout noise is assumed.

Fig. 2
Fig. 2

Influence on the PSF of the number and distribution of vortex singularities in the pupil function. (a) The left column shows the pupil phase function (phase mask) with an increasing number of vortex singularities N and constant spacing d between them. The corresponding in-focus PSFs are shown in the right column. (b) Shows the change in the phase mask (left) and PSF at focus (right) as the spacing d increases with a constant N = 9.

Fig. 3
Fig. 3

Schematic of the SPINDLE microscope. The sample in the rose chamber is mounted on a piezo nanopositioner and imaged with a Nikon 1.45, 100X objective and 200 mm Nikon tube lens. The DH-PSF-S is implemented by a 4F relay setup formed by two 100 mm focal length lenses. The DH phase mask is placed at a plane conjugate to the pupil plane of the objective. The final image is formed on the EMCCD. The illumination lasers (641 nm Coherent Cube used for turn off and 488 nm Argon -ion for activation) are used in synchronization with the camera in the scheme shown on the top right.

Fig. 4
Fig. 4

Calibration and Phase Retrieval Interpolation: (a) Images of the 3D DH-PSF for various defocus positions. This data is taken with red beads (660/680 200 nm diameter from Invitrogen) fixed on cover slide and used as calibration for SPINDLE data analysis. (b) Result of phase retrieval to create continuous 3D PSF. This is used for maximum likelihood 3D position estimation of molecules. (c) Flowchart for processing of SPINDLE data. The image from the camera is filtered and potential molecule candidates are found (marked with black asteriks). Each candidate image is passed on to the estimator to find 3D position and number of detected photons. (d) Experimentally determined precision of a fluorescent bead compared with the CRB calculated for a 1 photon/pixel background under experimental conditions (see text).

Fig. 5
Fig. 5

(a) and (b) Comparison of classical fluorescence imaging and 3D SPINDLE imaging of tubulin of PtK1 cells (Rat Kangaroo Epithelial cells) using an antibody labeled with Alexa-647 and Alexa-488 dyes. (c) and (d) Zoomed in view of the boxed region in (a) and (b) to show details of microtubule structure. Colormap shows the z position. Scale bars are 1µm. (e) shows side-view of the boxed region in (d) and (f) shows a histogram of axial localizations to show separation of microtubules in z (Media 1 - the microtubules are shown in 3D from different views ). (g) and (h) show transverse and axial cross-sections of the microtubule pointed with red arrow in (d) (Media 2 - the super-resolved microtubule is shown in 3D overlaid on the normal fluorescence image).

Fig. 6
Fig. 6

Precision analysis of the SPINDLE data. (a) Precisions per localization in x, y and z directions for different number of photons per image. Theoretical √CRB values calculated for the same system parameters with 30 background photons/pixel and the probability density function for the EMCCD are shown for comparison with the experiment. The theoretical values correspond to √Avg(CRB) for 1.2 µm range. (b) and (c) Histograms of x, y and z estimated positions for molecules detected with 1100 photons and 5000 photons per image, respectively. The measured precision values for (b) and (c) are σ(x,y,z) = (22,29,52) nm and σ(x,y,z) = (7,11,22) nm.

Fig. 7
Fig. 7

(a)-(b) Comparison of 3D localization methods via the Average Cramer Rao Bound (CRB3D) over 800 nm and 2 µm ranges with changing background. The calculation parameters for shot-noise limited CRB are 1.45NA, λ = 660 nm, pixel size = 16 µm, 3000 detected photons at focus. (c) shows the CRB for each dimension (x,y and z) and the 3D CRB varying with z for background of 6 photons/pixel.

Fig. 8
Fig. 8

Determination of noise in the experiment. The histogram of pixel values was obtained by taking 200 frames and 200x200 window size. The histogram was fitted with the given EMCCD probability distribution. From this fitting, the parameter values obtained are m = 27.5 camera counts per photons and p = 123 photons.

Fig. 9
Fig. 9

Statistical analysis of molecules with respect to number of cycles ON. (a) Histogram of molecules based on number of images they were ON in a SPINDLE experiment. Total number of estimations using 30,000 frames was 121715. The majority of molecules are ON for a single image. (b) Distribution of 55481 estimations which were found to be ON for a single image with the number of photons per image. (c) Distribution with number of photons per image for 20820 estimations, each of which was found to be related to molecules ON four or more images in the experiment. The two distributions are similar showing that precision values (in Fig. 6) calculated from molecules which were ON for 4 or more images can be used for the entire data set, including the molecules which were ON for a single image.

Fig. 10
Fig. 10

(a) Normal fluorescence image of microtubules region and (b) 3D SPINDLE image of the same region. The depth is shown in colormap.

Equations (3)

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E pupil ( r,θ )=circ( r R )exp( iarg( k=M M ( r e iθ r k e i θ k ) ) )
PSF( x,y,z )= | 1 { H( u,v )exp[ i π λ n oil N A 2 dz( u 2 + v 2 ) ] } | 2
G p,m ( c )= e p δ( c )+ p cm e c m p Bessel I 1 ( 2 cp m )

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