Abstract

Structured illumination microscopy (SIM) is an established microscopy technique typically used to image samples at resolutions beyond the diffraction limit. Until now, however, achieving sub-diffraction resolution has predominantly been limited to intensity-based imaging modalities. Here, we introduce an analogue to conventional SIM that allows sub-diffraction resolution, quantitative phase-contrast imaging of optically transparent objects. We demonstrate sub-diffraction resolution amplitude and quantitative-phase imaging of phantom targets and enhanced resolution quantitative-phase imaging of cells. We report a phase accuracy to within 5% and phase noise of 0.06 rad.

© 2013 OSA

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References

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    [CrossRef]

2013

Y. Cotte, F. Toy, P. Jourdain, N. Pavillon, D. Boss, P. Magistretti, P. Marquet, and C. Depeursinge, “Marker-free phase nanoscopy,” Nat. Photonics7(2), 113–117 (2013).
[CrossRef]

J. Chen, Y. Xu, X. Lv, X. Lai, and S. Zeng, “Super-resolution differential interference contrast microscopy by structured illumination,” Opt. Express21(1), 112–121 (2013).
[CrossRef] [PubMed]

2012

K. Chu, Z. J. Smith, S. Wachsmann-Hogiu, and S. Lane, “Super-resolved spatial light interference microscopy,” J. Opt. Soc. Am. A29(3), 344–351 (2012).
[CrossRef] [PubMed]

B. Bhaduri, H. Pham, M. Mir, and G. Popescu, “Diffraction phase microscopy with white light,” Opt. Lett.37(6), 1094–1096 (2012).
[CrossRef] [PubMed]

S. Chowdhury, A. H. Dhalla, and J. Izatt, “Structured oblique illumination microscopy for enhanced resolution imaging of non-fluorescent, coherently scattering samples,” Biomed. Opt. Express3(8), 1841–1854 (2012).
[CrossRef] [PubMed]

N. Pavillon, J. Kühn, C. Moratal, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Early Cell Death Detection with Digital Holographic Microscopy,” PLoS ONE7(1), e30912 (2012).
[CrossRef] [PubMed]

M. Kim, Y. Choi, C. Fang-Yen, Y. Sung, K. Kim, R. R. Dasari, M. S. Feld, and W. Choi, “Three-dimensional differential interference contrast microscopy using synthetic aperture imaging,” J. Biomed. Opt.17(2), 026003 (2012).
[CrossRef] [PubMed]

2011

2010

2009

P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods6(5), 339–342 (2009).
[CrossRef] [PubMed]

N. T. Shaked, M. T. Rinehart, and A. Wax, “Dual-interference-channel quantitative-phase microscopy of live cell dynamics,” Opt. Lett.34(6), 767–769 (2009).
[CrossRef] [PubMed]

2008

S. Shroff, J. Fienup, and D. Williams, “OTF compensation in structured illumination superresolution images,” Proc. SPIE7094, 709402, 709402-11 (2008).
[CrossRef]

M. Bates, B. Huang, and X. Zhuang, “Super-resolution microscopy by nanoscale localization of photo-switchable fluorescent probes,” Curr. Opin. Chem. Biol.12(5), 505–514 (2008).
[CrossRef] [PubMed]

2006

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods3(10), 793–796 (2006).
[CrossRef] [PubMed]

2000

M. G. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc.198(2), 82–87 (2000).
[CrossRef] [PubMed]

1995

S. W. Hell and M. Kroug, “Ground-state-depletion fluorscence microscopy: A concept for breaking the diffraction resolution limit,” Appl. Phys. (Berl.)60(5), 495–497 (1995).
[CrossRef]

1994

1992

1967

1966

Bates, M.

M. Bates, B. Huang, and X. Zhuang, “Super-resolution microscopy by nanoscale localization of photo-switchable fluorescent probes,” Curr. Opin. Chem. Biol.12(5), 505–514 (2008).
[CrossRef] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods3(10), 793–796 (2006).
[CrossRef] [PubMed]

Bhaduri, B.

Boss, D.

Y. Cotte, F. Toy, P. Jourdain, N. Pavillon, D. Boss, P. Magistretti, P. Marquet, and C. Depeursinge, “Marker-free phase nanoscopy,” Nat. Photonics7(2), 113–117 (2013).
[CrossRef]

Chen, J.

Chhun, B. B.

P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods6(5), 339–342 (2009).
[CrossRef] [PubMed]

Choi, W.

M. Kim, Y. Choi, C. Fang-Yen, Y. Sung, K. Kim, R. R. Dasari, M. S. Feld, and W. Choi, “Three-dimensional differential interference contrast microscopy using synthetic aperture imaging,” J. Biomed. Opt.17(2), 026003 (2012).
[CrossRef] [PubMed]

Choi, Y.

M. Kim, Y. Choi, C. Fang-Yen, Y. Sung, K. Kim, R. R. Dasari, M. S. Feld, and W. Choi, “Three-dimensional differential interference contrast microscopy using synthetic aperture imaging,” J. Biomed. Opt.17(2), 026003 (2012).
[CrossRef] [PubMed]

Chowdhury, S.

Chu, K.

Cotte, Y.

Y. Cotte, F. Toy, P. Jourdain, N. Pavillon, D. Boss, P. Magistretti, P. Marquet, and C. Depeursinge, “Marker-free phase nanoscopy,” Nat. Photonics7(2), 113–117 (2013).
[CrossRef]

Dasari, R. R.

M. Kim, Y. Choi, C. Fang-Yen, Y. Sung, K. Kim, R. R. Dasari, M. S. Feld, and W. Choi, “Three-dimensional differential interference contrast microscopy using synthetic aperture imaging,” J. Biomed. Opt.17(2), 026003 (2012).
[CrossRef] [PubMed]

Depeursinge, C.

Y. Cotte, F. Toy, P. Jourdain, N. Pavillon, D. Boss, P. Magistretti, P. Marquet, and C. Depeursinge, “Marker-free phase nanoscopy,” Nat. Photonics7(2), 113–117 (2013).
[CrossRef]

N. Pavillon, J. Kühn, C. Moratal, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Early Cell Death Detection with Digital Holographic Microscopy,” PLoS ONE7(1), e30912 (2012).
[CrossRef] [PubMed]

Dhalla, A. H.

Ding, H.

Fang-Yen, C.

M. Kim, Y. Choi, C. Fang-Yen, Y. Sung, K. Kim, R. R. Dasari, M. S. Feld, and W. Choi, “Three-dimensional differential interference contrast microscopy using synthetic aperture imaging,” J. Biomed. Opt.17(2), 026003 (2012).
[CrossRef] [PubMed]

Feld, M. S.

M. Kim, Y. Choi, C. Fang-Yen, Y. Sung, K. Kim, R. R. Dasari, M. S. Feld, and W. Choi, “Three-dimensional differential interference contrast microscopy using synthetic aperture imaging,” J. Biomed. Opt.17(2), 026003 (2012).
[CrossRef] [PubMed]

Fienup, J.

S. Shroff, J. Fienup, and D. Williams, “OTF compensation in structured illumination superresolution images,” Proc. SPIE7094, 709402, 709402-11 (2008).
[CrossRef]

Gillette, M. U.

Griffis, E. R.

P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods6(5), 339–342 (2009).
[CrossRef] [PubMed]

Gustafsson, M. G.

M. G. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc.198(2), 82–87 (2000).
[CrossRef] [PubMed]

Gustafsson, M. G. L.

P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods6(5), 339–342 (2009).
[CrossRef] [PubMed]

Hell, S. W.

S. W. Hell and M. Kroug, “Ground-state-depletion fluorscence microscopy: A concept for breaking the diffraction resolution limit,” Appl. Phys. (Berl.)60(5), 495–497 (1995).
[CrossRef]

S. W. Hell and J. Wichmann, “Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy,” Opt. Lett.19(11), 780–782 (1994).
[CrossRef] [PubMed]

Huang, B.

M. Bates, B. Huang, and X. Zhuang, “Super-resolution microscopy by nanoscale localization of photo-switchable fluorescent probes,” Curr. Opin. Chem. Biol.12(5), 505–514 (2008).
[CrossRef] [PubMed]

Hussain, A.

Izatt, J.

Jourdain, P.

Y. Cotte, F. Toy, P. Jourdain, N. Pavillon, D. Boss, P. Magistretti, P. Marquet, and C. Depeursinge, “Marker-free phase nanoscopy,” Nat. Photonics7(2), 113–117 (2013).
[CrossRef]

N. Pavillon, J. Kühn, C. Moratal, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Early Cell Death Detection with Digital Holographic Microscopy,” PLoS ONE7(1), e30912 (2012).
[CrossRef] [PubMed]

Kim, K.

M. Kim, Y. Choi, C. Fang-Yen, Y. Sung, K. Kim, R. R. Dasari, M. S. Feld, and W. Choi, “Three-dimensional differential interference contrast microscopy using synthetic aperture imaging,” J. Biomed. Opt.17(2), 026003 (2012).
[CrossRef] [PubMed]

Kim, M.

M. Kim, Y. Choi, C. Fang-Yen, Y. Sung, K. Kim, R. R. Dasari, M. S. Feld, and W. Choi, “Three-dimensional differential interference contrast microscopy using synthetic aperture imaging,” J. Biomed. Opt.17(2), 026003 (2012).
[CrossRef] [PubMed]

Kner, P.

P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods6(5), 339–342 (2009).
[CrossRef] [PubMed]

Kroug, M.

S. W. Hell and M. Kroug, “Ground-state-depletion fluorscence microscopy: A concept for breaking the diffraction resolution limit,” Appl. Phys. (Berl.)60(5), 495–497 (1995).
[CrossRef]

Kühn, J.

N. Pavillon, J. Kühn, C. Moratal, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Early Cell Death Detection with Digital Holographic Microscopy,” PLoS ONE7(1), e30912 (2012).
[CrossRef] [PubMed]

Lai, X.

Lane, S.

Leith, E. N.

Lukosz, W.

Lv, X.

Magistretti, P.

Y. Cotte, F. Toy, P. Jourdain, N. Pavillon, D. Boss, P. Magistretti, P. Marquet, and C. Depeursinge, “Marker-free phase nanoscopy,” Nat. Photonics7(2), 113–117 (2013).
[CrossRef]

Magistretti, P. J.

N. Pavillon, J. Kühn, C. Moratal, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Early Cell Death Detection with Digital Holographic Microscopy,” PLoS ONE7(1), e30912 (2012).
[CrossRef] [PubMed]

Marquet, P.

Y. Cotte, F. Toy, P. Jourdain, N. Pavillon, D. Boss, P. Magistretti, P. Marquet, and C. Depeursinge, “Marker-free phase nanoscopy,” Nat. Photonics7(2), 113–117 (2013).
[CrossRef]

N. Pavillon, J. Kühn, C. Moratal, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Early Cell Death Detection with Digital Holographic Microscopy,” PLoS ONE7(1), e30912 (2012).
[CrossRef] [PubMed]

Millet, L. J.

Mir, M.

Moratal, C.

N. Pavillon, J. Kühn, C. Moratal, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Early Cell Death Detection with Digital Holographic Microscopy,” PLoS ONE7(1), e30912 (2012).
[CrossRef] [PubMed]

Mudassar, A. A.

Pavillon, N.

Y. Cotte, F. Toy, P. Jourdain, N. Pavillon, D. Boss, P. Magistretti, P. Marquet, and C. Depeursinge, “Marker-free phase nanoscopy,” Nat. Photonics7(2), 113–117 (2013).
[CrossRef]

N. Pavillon, J. Kühn, C. Moratal, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Early Cell Death Detection with Digital Holographic Microscopy,” PLoS ONE7(1), e30912 (2012).
[CrossRef] [PubMed]

Pham, H.

Popescu, G.

Rinehart, M. T.

Rogers, J. A.

Rust, M. J.

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods3(10), 793–796 (2006).
[CrossRef] [PubMed]

Shaked, N. T.

Shroff, S.

S. Shroff, J. Fienup, and D. Williams, “OTF compensation in structured illumination superresolution images,” Proc. SPIE7094, 709402, 709402-11 (2008).
[CrossRef]

Smith, Z. J.

Sun, P. C.

Sung, Y.

M. Kim, Y. Choi, C. Fang-Yen, Y. Sung, K. Kim, R. R. Dasari, M. S. Feld, and W. Choi, “Three-dimensional differential interference contrast microscopy using synthetic aperture imaging,” J. Biomed. Opt.17(2), 026003 (2012).
[CrossRef] [PubMed]

Toy, F.

Y. Cotte, F. Toy, P. Jourdain, N. Pavillon, D. Boss, P. Magistretti, P. Marquet, and C. Depeursinge, “Marker-free phase nanoscopy,” Nat. Photonics7(2), 113–117 (2013).
[CrossRef]

Unarunotai, S.

Wachsmann-Hogiu, S.

Wang, Z.

Wax, A.

Wichmann, J.

Williams, D.

S. Shroff, J. Fienup, and D. Williams, “OTF compensation in structured illumination superresolution images,” Proc. SPIE7094, 709402, 709402-11 (2008).
[CrossRef]

Winoto, L.

P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods6(5), 339–342 (2009).
[CrossRef] [PubMed]

Xu, Y.

Zeng, S.

Zhuang, X.

M. Bates, B. Huang, and X. Zhuang, “Super-resolution microscopy by nanoscale localization of photo-switchable fluorescent probes,” Curr. Opin. Chem. Biol.12(5), 505–514 (2008).
[CrossRef] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods3(10), 793–796 (2006).
[CrossRef] [PubMed]

Appl. Opt.

Appl. Phys. (Berl.)

S. W. Hell and M. Kroug, “Ground-state-depletion fluorscence microscopy: A concept for breaking the diffraction resolution limit,” Appl. Phys. (Berl.)60(5), 495–497 (1995).
[CrossRef]

Biomed. Opt. Express

Curr. Opin. Chem. Biol.

M. Bates, B. Huang, and X. Zhuang, “Super-resolution microscopy by nanoscale localization of photo-switchable fluorescent probes,” Curr. Opin. Chem. Biol.12(5), 505–514 (2008).
[CrossRef] [PubMed]

J. Biomed. Opt.

M. Kim, Y. Choi, C. Fang-Yen, Y. Sung, K. Kim, R. R. Dasari, M. S. Feld, and W. Choi, “Three-dimensional differential interference contrast microscopy using synthetic aperture imaging,” J. Biomed. Opt.17(2), 026003 (2012).
[CrossRef] [PubMed]

J. Microsc.

M. G. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc.198(2), 82–87 (2000).
[CrossRef] [PubMed]

J. Opt. Soc. Am.

J. Opt. Soc. Am. A

Nat. Methods

P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, “Super-resolution video microscopy of live cells by structured illumination,” Nat. Methods6(5), 339–342 (2009).
[CrossRef] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods3(10), 793–796 (2006).
[CrossRef] [PubMed]

Nat. Photonics

Y. Cotte, F. Toy, P. Jourdain, N. Pavillon, D. Boss, P. Magistretti, P. Marquet, and C. Depeursinge, “Marker-free phase nanoscopy,” Nat. Photonics7(2), 113–117 (2013).
[CrossRef]

Opt. Express

Opt. Lett.

PLoS ONE

N. Pavillon, J. Kühn, C. Moratal, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Early Cell Death Detection with Digital Holographic Microscopy,” PLoS ONE7(1), e30912 (2012).
[CrossRef] [PubMed]

Proc. SPIE

S. Shroff, J. Fienup, and D. Williams, “OTF compensation in structured illumination superresolution images,” Proc. SPIE7094, 709402, 709402-11 (2008).
[CrossRef]

Other

J. Pawley, Handbook of Biological Confocal Microscopy (Springer Science + Business Media, 1989).

W. J. Smith, Modern Lens Design, 2nd Ed (McGraw-Hill Professional Engineering, 2005).

M. Born and E. Wolf, Principles of Optics (Cambridge University Press, Cambridge, UK, 1959).

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Figures (5)

Fig. 1
Fig. 1

Optical system based on an off-axis interferometric transmission microscope configuration. Single mode 532 nm Gaussian beam illumination is split into sample and reference arms of interferometer by a beam splitter (BS). In the sample arm, the first 4f system Fourier filters through only the +/− 1 orders of the diffraction grating (DG) and images them onto the sample (S) plane to create a structured illumination pattern. The resulting sample diffraction is coherently imaged via the second 4f system to a CMOS camera and interfered by the reference wave.

Fig. 2
Fig. 2

Holographic reconstruction is shown for orthogonal (i.e., wide-field) illumination (a-d) and structured illumination imaging (e-h) before post-processing for enhanced resolution. (a,e) Raw interferograms at image plane are shown for orthogonal and structured illumination imaging and (b,f) associated Fourier spectra. In inset of (a) note the horizontal fringes from off-axis reference wave illumination, and in inset of (e) note overlapping horizontal fringes from off-axis reference wave illumination and vertical fringes from structured illumination (c,g) Digitally filtered and DC centered spectra from (b,f) and corresponding (d,h) inverse Fourier reconstructions are shown.

Fig. 3
Fig. 3

Enhanced resolution reconstruction showing Fourier spectra (i) and associated amplitude of inverse Fourier transform (ii). (a) Diffraction limited image of sample under orthogonal (wide-field) illumination (b,c) Enhanced resolution field amplitude reconstructions from horizontal and vertical sinusoidal structured illumination of the sample (d) Final enhanced resolution amplitude reconstruction containing enhanced resolution information from both orientations

Fig. 4
Fig. 4

(a) Diffraction-limited and (b) enhanced-resolution images and corresponding Fourier spectrum of a blazed grating are shown. (c) We simulate the phase profile of ideal (blue dashed line), diffraction-limited (WF, green dashed line), and enhanced-resolution (SI-QPM, pink solid line) imaging of the grating and show the corresponding bandpasses on the sample’s power spectrum. (e) This simulation is experimentally verified by taking cross-cuts from the diffraction-limited and enhanced-resolution images, as shown in dashed yellow in (a,b), and comparing to the expected ideal simulated blaze profile.

Fig. 5
Fig. 5

Comparison are of diffraction limited (WF) and enhanced resolution (SI-QPM) quantitative phase imaging of mesenchymal stem cells. Images are color-coded for quantitative phase delays through the sample. Scale bars on upper left correspond to 10 µm. Close-up comparisons of 3 regions (A,B,C) are shown below along with an associated line profile (marked in yellow).

Metrics