Abstract

A woofer–tweeter adaptive optical structured illumination microscope (AOSIM) is presented. By combining a low-spatial-frequency large-stroke deformable mirror (woofer) with a high-spatial-frequency low-stroke deformable mirror (tweeter), we are able to remove both large-amplitude and high-order aberrations. In addition, using the structured illumination method, as compared to widefield microscopy, the AOSIM can accomplish high-resolution imaging and possesses better sectioning capability. The AOSIM was tested by correcting a large aberration from a trial lens in the conjugate plane of the microscope objective aperture. The experimental results show that the AOSIM has a point spread function with an FWHM that is 140 nm wide (using a water immersion objective lens with NA=1.1) after correcting a large aberration (5.9 μm peak-to-valley wavefront error with 2.05 μm RMS aberration). After structured light illumination is applied, the results show that we are able to resolve two beads that are separated by 145 nm, 1.62× below the diffraction limit of 235 nm. Furthermore, we demonstrate the application of the AOSIM in the field of bioimaging. The sample under investigation was a green-fluorescent-protein-labeled Drosophila embryo. The aberrations from the refractive index mismatch between the microscope objective, the immersion fluid, the cover slip, and the sample itself are well corrected. Using AOSIM we were able to increase the SNR for our Drosophila embryo sample by 5×.

© 2017 Chinese Laser Press

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References

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M. Pedrazzani, V. Loriette, P. Tchenio, S. Benrezzak, D. Nutarelli, and A. Fragola, “Sensorless adaptive optics implementation in widefield optical sectioning microscopy inside in vivo Drosophila brain,” J. Biomed. Opt. 21, 036006 (2016).
[Crossref]

M. R. Reinig, S. W. Novak, X. Tao, L. A. Bentolila, D. G. Roberts, A. MacKenzie-Graham, S. E. Godshalk, M. A. Raven, D. W. Knowles, and J. Kubby, “Enhancing image quality in cleared tissue with adaptive optics,” J. Biomed. Opt. 21, 121508 (2016).
[Crossref]

2015 (5)

2014 (3)

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[Crossref]

M. Kissel, M. Reinig, O. Azucena, J. J. Diaz Leon, and J. Kubby, “Development and testing of an AO-structured illumination microscope,” Proc. SPIE 8978, 89780G (2014).
[Crossref]

A. Masson, M. Pedrazzani, S. Benrezzak, P. Tchenio, T. Preat, and D. Nutarelli, “Micromirror structured illumination microscope for high-speed in vivo drosophila brain imaging,” Opt. Express 22, 1243–1256 (2014).
[Crossref]

2013 (3)

2012 (2)

2011 (5)

2010 (2)

O. Azucena, J. Crest, J. Cao, W. Sullivan, P. Kner, D. Gavel, D. Dillon, S. Olivier, and J. Kubby, “Wavefront aberration measurements and corrections through thick tissue using fluorescent microsphere reference beacons,” Opt. Express 18, 17521–17532 (2010).
[Crossref]

P. Kner, J. W. Sedat, D. A. Agard, and Z. Kam, “High-resolution widefield microscopy with adaptive optics for spherical aberration correction and motionless focusing,” J. Microsc. 237, 136–147 (2010).
[Crossref]

2009 (2)

2008 (3)

D. Debarre, E. J. Botcherby, M. J. Booth, and T. Wilson, “Adaptive optics for structured illumination microscopy,” Opt. Express 16, 9290–9305 (2008).
[Crossref]

S. A. Shroff, J. R. Fienup, and D. R. Williams, “OTF compensation in structured illumination superresolution images,” Proc. SPIE 7094, 709402 (2008).

M. G. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94, 4957–4970 (2008).
[Crossref]

2007 (1)

2006 (2)

M. Booth, “Wave front sensor-less adaptive optics: a model-based approach using sphere packings,” Opt. Express 14, 1339–1352 (2006).
[Crossref]

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

2005 (2)

M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy: widefield fluorescence imaging with theoretically unlimited resolution,” Proc. Natl. Acad. Sci. USA 102, 13081–13086 (2005).
[Crossref]

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2, 932–940 (2005).
[Crossref]

2002 (1)

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. USA 99, 5788–5792 (2002).
[Crossref]

2001 (1)

B. C. Platt and R. Shack, “History and principles of Shack–Hartmann wavefront sensing,” J. Refractive Surg. 17, S573–S577 (2001).

2000 (2)

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

M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Doubling the lateral resolution of wide-field fluorescence microscopy using structured illumination,” Proc. SPIE 3919, 141–150 (2000).

1997 (1)

1995 (1)

M. Rajadhyaksha, M. Grossman, D. Esterowitz, R. H. Webb, and R. R. Anderson, “In vivo confocal scanning laser microscopy of human skin: melanin provides strong contrast,” J. Invest. Dermatol. 104, 946–952 (1995).
[Crossref]

1994 (1)

Agard, D. A.

P. Kner, J. W. Sedat, D. A. Agard, and Z. Kam, “High-resolution widefield microscopy with adaptive optics for spherical aberration correction and motionless focusing,” J. Microsc. 237, 136–147 (2010).
[Crossref]

M. G. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94, 4957–4970 (2008).
[Crossref]

M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Doubling the lateral resolution of wide-field fluorescence microscopy using structured illumination,” Proc. SPIE 3919, 141–150 (2000).

Anderson, R. R.

M. Rajadhyaksha, M. Grossman, D. Esterowitz, R. H. Webb, and R. R. Anderson, “In vivo confocal scanning laser microscopy of human skin: melanin provides strong contrast,” J. Invest. Dermatol. 104, 946–952 (1995).
[Crossref]

Artigas, D.

Aviles-Espinosa, R.

Azucena, O.

Benrezzak, S.

M. Pedrazzani, V. Loriette, P. Tchenio, S. Benrezzak, D. Nutarelli, and A. Fragola, “Sensorless adaptive optics implementation in widefield optical sectioning microscopy inside in vivo Drosophila brain,” J. Biomed. Opt. 21, 036006 (2016).
[Crossref]

A. Masson, M. Pedrazzani, S. Benrezzak, P. Tchenio, T. Preat, and D. Nutarelli, “Micromirror structured illumination microscope for high-speed in vivo drosophila brain imaging,” Opt. Express 22, 1243–1256 (2014).
[Crossref]

Bentolila, L. A.

M. R. Reinig, S. W. Novak, X. Tao, L. A. Bentolila, D. G. Roberts, A. MacKenzie-Graham, S. E. Godshalk, M. A. Raven, D. W. Knowles, and J. Kubby, “Enhancing image quality in cleared tissue with adaptive optics,” J. Biomed. Opt. 21, 121508 (2016).
[Crossref]

Betzig, E.

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

Bonifacino, J. S.

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

Booth, M.

Booth, M. J.

Botcherby, E. J.

Cande, W. Z.

M. G. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94, 4957–4970 (2008).
[Crossref]

Cao, J.

Carlton, P. M.

M. G. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94, 4957–4970 (2008).
[Crossref]

Chakrova, N.

Chaudhari, S. N.

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]

Chen, D. C.

Chen, N.

Clark, C. G.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7, 205–209 (2013).
[Crossref]

Crest, J.

Davidson, M. W.

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

Debarre, D.

Denk, W.

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2, 932–940 (2005).
[Crossref]

Diaz Leon, J. J.

M. Kissel, M. Reinig, O. Azucena, J. J. Diaz Leon, and J. Kubby, “Development and testing of an AO-structured illumination microscope,” Proc. SPIE 8978, 89780G (2014).
[Crossref]

Dillon, D.

Esterowitz, D.

M. Rajadhyaksha, M. Grossman, D. Esterowitz, R. H. Webb, and R. R. Anderson, “In vivo confocal scanning laser microscopy of human skin: melanin provides strong contrast,” J. Invest. Dermatol. 104, 946–952 (1995).
[Crossref]

Fernandez, B.

Fienup, J. R.

S. A. Shroff, J. R. Fienup, and D. R. Williams, “OTF compensation in structured illumination superresolution images,” Proc. SPIE 7094, 709402 (2008).

Fragola, A.

M. Pedrazzani, V. Loriette, P. Tchenio, S. Benrezzak, D. Nutarelli, and A. Fragola, “Sensorless adaptive optics implementation in widefield optical sectioning microscopy inside in vivo Drosophila brain,” J. Biomed. Opt. 21, 036006 (2016).
[Crossref]

P. Vermeulen, E. Muro, T. Pons, V. Loriette, and A. Fragola, “Adaptive optics for fluorescence widefield microscopy using spectrally independent guide star and markers,” J. Biomed. Opt. 16, 076019 (2011).
[Crossref]

Fraser, S. E.

Fu, M.

Gao, P.

Garcia, D.

Gavel, D.

Godshalk, S. E.

M. R. Reinig, S. W. Novak, X. Tao, L. A. Bentolila, D. G. Roberts, A. MacKenzie-Graham, S. E. Godshalk, M. A. Raven, D. W. Knowles, and J. Kubby, “Enhancing image quality in cleared tissue with adaptive optics,” J. Biomed. Opt. 21, 121508 (2016).
[Crossref]

Golubovskaya, I. N.

M. G. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94, 4957–4970 (2008).
[Crossref]

Gong, W.

Grossman, M.

M. Rajadhyaksha, M. Grossman, D. Esterowitz, R. H. Webb, and R. R. Anderson, “In vivo confocal scanning laser microscopy of human skin: melanin provides strong contrast,” J. Invest. Dermatol. 104, 946–952 (1995).
[Crossref]

Gustafsson, M. G.

M. G. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94, 4957–4970 (2008).
[Crossref]

Gustafsson, M. G. L.

M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy: widefield fluorescence imaging with theoretically unlimited resolution,” Proc. Natl. Acad. Sci. USA 102, 13081–13086 (2005).
[Crossref]

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

M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Doubling the lateral resolution of wide-field fluorescence microscopy using structured illumination,” Proc. SPIE 3919, 141–150 (2000).

Hagen, G. M.

Hardy, J. W.

J. W. Hardy, Adaptive Optics for Astronomical Telescopes (Oxford University, 1998).

Heintzmann, R.

Hell, S. W.

Helmchen, F.

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2, 932–940 (2005).
[Crossref]

Hess, H. F.

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

Hirosawa, K.

Q. Song, K. Isobe, K. Hirosawa, K. Midorikawa, and F. Kannari, “2D simultaneous spatial and temporal focusing multiphoton microscopy for fast volume imaging with improved sectioning ability,” Proc. SPIE 9329, 93292N (2015).

Holland, D. B.

Horton, N. G.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7, 205–209 (2013).
[Crossref]

Isobe, K.

Q. Song, K. Isobe, K. Hirosawa, K. Midorikawa, and F. Kannari, “2D simultaneous spatial and temporal focusing multiphoton microscopy for fast volume imaging with improved sectioning ability,” Proc. SPIE 9329, 93292N (2015).

Jones, S. M.

Jordi, A.

Ju skaitis, R.

Juskaitis, R.

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. USA 99, 5788–5792 (2002).
[Crossref]

Kam, Z.

P. Kner, J. W. Sedat, D. A. Agard, and Z. Kam, “High-resolution widefield microscopy with adaptive optics for spherical aberration correction and motionless focusing,” J. Microsc. 237, 136–147 (2010).
[Crossref]

Kannari, F.

Q. Song, K. Isobe, K. Hirosawa, K. Midorikawa, and F. Kannari, “2D simultaneous spatial and temporal focusing multiphoton microscopy for fast volume imaging with improved sectioning ability,” Proc. SPIE 9329, 93292N (2015).

Kipreos, E. T.

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]

Kissel, M.

M. Kissel, M. Reinig, O. Azucena, J. J. Diaz Leon, and J. Kubby, “Development and testing of an AO-structured illumination microscope,” Proc. SPIE 8978, 89780G (2014).
[Crossref]

X. Tao, A. Norton, M. Kissel, O. Azucena, and J. Kubby, “Adaptive optical two-photon microscopy using auto fluorescent guide stars,” Opt. Lett. 38, 5075–5078 (2013).
[Crossref]

Kner, P.

K. F. Tehrani, J. Xu, Y. Zhang, P. Shen, and P. Kner, “Adaptive optics stochastic optical reconstruction microscopy (AO-STORM) using a genetic algorithm,” Opt. Express 23, 13677–13692 (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]

P. Kner, J. W. Sedat, D. A. Agard, and Z. Kam, “High-resolution widefield microscopy with adaptive optics for spherical aberration correction and motionless focusing,” J. Microsc. 237, 136–147 (2010).
[Crossref]

O. Azucena, J. Crest, J. Cao, W. Sullivan, P. Kner, D. Gavel, D. Dillon, S. Olivier, and J. Kubby, “Wavefront aberration measurements and corrections through thick tissue using fluorescent microsphere reference beacons,” Opt. Express 18, 17521–17532 (2010).
[Crossref]

Knowles, D. W.

M. R. Reinig, S. W. Novak, X. Tao, L. A. Bentolila, D. G. Roberts, A. MacKenzie-Graham, S. E. Godshalk, M. A. Raven, D. W. Knowles, and J. Kubby, “Enhancing image quality in cleared tissue with adaptive optics,” J. Biomed. Opt. 21, 121508 (2016).
[Crossref]

Kobat, D.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7, 205–209 (2013).
[Crossref]

Kotadia, S.

Krizek, P.

Kubby, J.

M. R. Reinig, S. W. Novak, X. Tao, L. A. Bentolila, D. G. Roberts, A. MacKenzie-Graham, S. E. Godshalk, M. A. Raven, D. W. Knowles, and J. Kubby, “Enhancing image quality in cleared tissue with adaptive optics,” J. Biomed. Opt. 21, 121508 (2016).
[Crossref]

M. Kissel, M. Reinig, O. Azucena, J. J. Diaz Leon, and J. Kubby, “Development and testing of an AO-structured illumination microscope,” Proc. SPIE 8978, 89780G (2014).
[Crossref]

X. Tao, A. Norton, M. Kissel, O. Azucena, and J. Kubby, “Adaptive optical two-photon microscopy using auto fluorescent guide stars,” Opt. Lett. 38, 5075–5078 (2013).
[Crossref]

X. Tao, J. Crest, S. Kotadia, O. Azucena, D. C. Chen, B. Sullivan, and J. Kubby, “Live imaging using adaptive optics with fluorescent protein guide-stars,” Opt. Express 20, 15969–15982 (2012).
[Crossref]

X. Tao, B. Fernandez, O. Azucena, M. Fu, D. Garcia, Y. Zuo, D. C. Chen, and J. Kubby, “Adaptive optics confocal microscopy using direct wavefront sensing,” Opt. Lett. 36, 1062–1064 (2011).
[Crossref]

O. Azucena, J. Crest, S. Kotadia, W. Sullivan, X. Tao, M. Reinig, D. Gavel, S. Olivier, and J. Kubby, “Adaptive optics widefield microscopy using direct wavefront sensing,” Opt. Lett. 36, 825–827 (2011).
[Crossref]

O. Azucena, J. Crest, J. Cao, W. Sullivan, P. Kner, D. Gavel, D. Dillon, S. Olivier, and J. Kubby, “Wavefront aberration measurements and corrections through thick tissue using fluorescent microsphere reference beacons,” Opt. Express 18, 17521–17532 (2010).
[Crossref]

Kubby, J. A.

J. A. Kubby, Adaptive Optics for Biological Imaging (CRC Press, 2013).

Liebling, M.

Lind-Wasser, O. W.

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

Lippincott-Schwartz, J.

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

Loriette, V.

M. Pedrazzani, V. Loriette, P. Tchenio, S. Benrezzak, D. Nutarelli, and A. Fragola, “Sensorless adaptive optics implementation in widefield optical sectioning microscopy inside in vivo Drosophila brain,” J. Biomed. Opt. 21, 036006 (2016).
[Crossref]

P. Vermeulen, E. Muro, T. Pons, V. Loriette, and A. Fragola, “Adaptive optics for fluorescence widefield microscopy using spectrally independent guide star and markers,” J. Biomed. Opt. 16, 076019 (2011).
[Crossref]

Loza-Alvarez, P.

MacKenzie-Graham, A.

M. R. Reinig, S. W. Novak, X. Tao, L. A. Bentolila, D. G. Roberts, A. MacKenzie-Graham, S. E. Godshalk, M. A. Raven, D. W. Knowles, and J. Kubby, “Enhancing image quality in cleared tissue with adaptive optics,” J. Biomed. Opt. 21, 121508 (2016).
[Crossref]

Masson, A.

Mertz, J.

J. Mertz, “Optical sectioning microscopy with planar or structured illumination,” Nat. Methods 8, 811–819 (2011).
[Crossref]

Midorikawa, K.

Q. Song, K. Isobe, K. Hirosawa, K. Midorikawa, and F. Kannari, “2D simultaneous spatial and temporal focusing multiphoton microscopy for fast volume imaging with improved sectioning ability,” Proc. SPIE 9329, 93292N (2015).

Muro, E.

P. Vermeulen, E. Muro, T. Pons, V. Loriette, and A. Fragola, “Adaptive optics for fluorescence widefield microscopy using spectrally independent guide star and markers,” J. Biomed. Opt. 16, 076019 (2011).
[Crossref]

Neil, M. A. A.

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. USA 99, 5788–5792 (2002).
[Crossref]

M. A. A. Neil, R. Ju skaitis, and T. Wilson, “Method of obtaining optical sectioning by using structured light in a conventional microscope,” Opt. Lett. 22, 1905–1907 (1997).
[Crossref]

Nienhaus, U.

Nieto, M.

Norton, A.

Novak, S. W.

M. R. Reinig, S. W. Novak, X. Tao, L. A. Bentolila, D. G. Roberts, A. MacKenzie-Graham, S. E. Godshalk, M. A. Raven, D. W. Knowles, and J. Kubby, “Enhancing image quality in cleared tissue with adaptive optics,” J. Biomed. Opt. 21, 121508 (2016).
[Crossref]

Nutarelli, D.

M. Pedrazzani, V. Loriette, P. Tchenio, S. Benrezzak, D. Nutarelli, and A. Fragola, “Sensorless adaptive optics implementation in widefield optical sectioning microscopy inside in vivo Drosophila brain,” J. Biomed. Opt. 21, 036006 (2016).
[Crossref]

A. Masson, M. Pedrazzani, S. Benrezzak, P. Tchenio, T. Preat, and D. Nutarelli, “Micromirror structured illumination microscope for high-speed in vivo drosophila brain imaging,” Opt. Express 22, 1243–1256 (2014).
[Crossref]

Olarte, O. E.

Olenych, S.

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

Olivier, S.

Olivier, S. S.

Osten, W.

Patterson, G. H.

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

Pedrazzani, M.

M. Pedrazzani, V. Loriette, P. Tchenio, S. Benrezzak, D. Nutarelli, and A. Fragola, “Sensorless adaptive optics implementation in widefield optical sectioning microscopy inside in vivo Drosophila brain,” J. Biomed. Opt. 21, 036006 (2016).
[Crossref]

A. Masson, M. Pedrazzani, S. Benrezzak, P. Tchenio, T. Preat, and D. Nutarelli, “Micromirror structured illumination microscope for high-speed in vivo drosophila brain imaging,” Opt. Express 22, 1243–1256 (2014).
[Crossref]

Pedrini, G.

Platt, B. C.

B. C. Platt and R. Shack, “History and principles of Shack–Hartmann wavefront sensing,” J. Refractive Surg. 17, S573–S577 (2001).

Pons, T.

P. Vermeulen, E. Muro, T. Pons, V. Loriette, and A. Fragola, “Adaptive optics for fluorescence widefield microscopy using spectrally independent guide star and markers,” J. Biomed. Opt. 16, 076019 (2011).
[Crossref]

Porcar-Guezenec, R.

Porter, J.

J. Porter, Adaptive Optics for Vision Science: Principles, Practices, Design, and Applications (Wiley-Interscience, 2006).

Preat, T.

Raaka, I.

Rajadhyaksha, M.

M. Rajadhyaksha, M. Grossman, D. Esterowitz, R. H. Webb, and R. R. Anderson, “In vivo confocal scanning laser microscopy of human skin: melanin provides strong contrast,” J. Invest. Dermatol. 104, 946–952 (1995).
[Crossref]

Raven, M. A.

M. R. Reinig, S. W. Novak, X. Tao, L. A. Bentolila, D. G. Roberts, A. MacKenzie-Graham, S. E. Godshalk, M. A. Raven, D. W. Knowles, and J. Kubby, “Enhancing image quality in cleared tissue with adaptive optics,” J. Biomed. Opt. 21, 121508 (2016).
[Crossref]

Reinig, M.

M. Kissel, M. Reinig, O. Azucena, J. J. Diaz Leon, and J. Kubby, “Development and testing of an AO-structured illumination microscope,” Proc. SPIE 8978, 89780G (2014).
[Crossref]

O. Azucena, J. Crest, S. Kotadia, W. Sullivan, X. Tao, M. Reinig, D. Gavel, S. Olivier, and J. Kubby, “Adaptive optics widefield microscopy using direct wavefront sensing,” Opt. Lett. 36, 825–827 (2011).
[Crossref]

Reinig, M. R.

M. R. Reinig, S. W. Novak, X. Tao, L. A. Bentolila, D. G. Roberts, A. MacKenzie-Graham, S. E. Godshalk, M. A. Raven, D. W. Knowles, and J. Kubby, “Enhancing image quality in cleared tissue with adaptive optics,” J. Biomed. Opt. 21, 121508 (2016).
[Crossref]

Rieger, B.

Roberts, D. G.

M. R. Reinig, S. W. Novak, X. Tao, L. A. Bentolila, D. G. Roberts, A. MacKenzie-Graham, S. E. Godshalk, M. A. Raven, D. W. Knowles, and J. Kubby, “Enhancing image quality in cleared tissue with adaptive optics,” J. Biomed. Opt. 21, 121508 (2016).
[Crossref]

Schaffer, C. B.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7, 205–209 (2013).
[Crossref]

Sedat, J. W.

P. Kner, J. W. Sedat, D. A. Agard, and Z. Kam, “High-resolution widefield microscopy with adaptive optics for spherical aberration correction and motionless focusing,” J. Microsc. 237, 136–147 (2010).
[Crossref]

M. G. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94, 4957–4970 (2008).
[Crossref]

M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Doubling the lateral resolution of wide-field fluorescence microscopy using structured illumination,” Proc. SPIE 3919, 141–150 (2000).

Shack, R.

B. C. Platt and R. Shack, “History and principles of Shack–Hartmann wavefront sensing,” J. Refractive Surg. 17, S573–S577 (2001).

Shao, L.

M. G. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94, 4957–4970 (2008).
[Crossref]

Shen, P.

Sheppard, C. J. R.

Shroff, S. A.

S. A. Shroff, J. R. Fienup, and D. R. Williams, “OTF compensation in structured illumination superresolution images,” Proc. SPIE 7094, 709402 (2008).

Si, K.

Silva, D. A.

Song, Q.

Q. Song, K. Isobe, K. Hirosawa, K. Midorikawa, and F. Kannari, “2D simultaneous spatial and temporal focusing multiphoton microscopy for fast volume imaging with improved sectioning ability,” Proc. SPIE 9329, 93292N (2015).

Sougrat, R.

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

Srinivas, S.

Stallinga, S.

Stelzer, E. H. K.

E. H. K. Stelzer, “Light-sheet fluorescence microscopy for quantitative biology,” Nat. Methods 12, 23–26 (2014).
[Crossref]

Sullivan, B.

Sullivan, W.

Tao, X.

Tchenio, P.

M. Pedrazzani, V. Loriette, P. Tchenio, S. Benrezzak, D. Nutarelli, and A. Fragola, “Sensorless adaptive optics implementation in widefield optical sectioning microscopy inside in vivo Drosophila brain,” J. Biomed. Opt. 21, 036006 (2016).
[Crossref]

A. Masson, M. Pedrazzani, S. Benrezzak, P. Tchenio, T. Preat, and D. Nutarelli, “Micromirror structured illumination microscope for high-speed in vivo drosophila brain imaging,” Opt. Express 22, 1243–1256 (2014).
[Crossref]

Tehrani, K. F.

Thomas, B.

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]

Trinh, L. A.

Trivedi, V.

Truong, T. V.

Vermeulen, P.

P. Vermeulen, E. Muro, T. Pons, V. Loriette, and A. Fragola, “Adaptive optics for fluorescence widefield microscopy using spectrally independent guide star and markers,” J. Biomed. Opt. 16, 076019 (2011).
[Crossref]

Wang, C. J. R.

M. G. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94, 4957–4970 (2008).
[Crossref]

Wang, K.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7, 205–209 (2013).
[Crossref]

Watanabe, T.

Webb, R. H.

M. Rajadhyaksha, M. Grossman, D. Esterowitz, R. H. Webb, and R. R. Anderson, “In vivo confocal scanning laser microscopy of human skin: melanin provides strong contrast,” J. Invest. Dermatol. 104, 946–952 (1995).
[Crossref]

Wichmann, J.

Williams, D. R.

S. A. Shroff, J. R. Fienup, and D. R. Williams, “OTF compensation in structured illumination superresolution images,” Proc. SPIE 7094, 709402 (2008).

Wilson, T.

Wise, F. W.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7, 205–209 (2013).
[Crossref]

Wolstenholme, A.

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]

Xavier, L.

Xu, C.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7, 205–209 (2013).
[Crossref]

Xu, J.

Zhang, Y.

Zuo, Y.

Biomed. Opt. Express (2)

Biophys. J. (1)

M. G. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94, 4957–4970 (2008).
[Crossref]

J. Biomed. Opt. (4)

P. Vermeulen, E. Muro, T. Pons, V. Loriette, and A. Fragola, “Adaptive optics for fluorescence widefield microscopy using spectrally independent guide star and markers,” J. Biomed. Opt. 16, 076019 (2011).
[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]

M. Pedrazzani, V. Loriette, P. Tchenio, S. Benrezzak, D. Nutarelli, and A. Fragola, “Sensorless adaptive optics implementation in widefield optical sectioning microscopy inside in vivo Drosophila brain,” J. Biomed. Opt. 21, 036006 (2016).
[Crossref]

M. R. Reinig, S. W. Novak, X. Tao, L. A. Bentolila, D. G. Roberts, A. MacKenzie-Graham, S. E. Godshalk, M. A. Raven, D. W. Knowles, and J. Kubby, “Enhancing image quality in cleared tissue with adaptive optics,” J. Biomed. Opt. 21, 121508 (2016).
[Crossref]

J. Invest. Dermatol. (1)

M. Rajadhyaksha, M. Grossman, D. Esterowitz, R. H. Webb, and R. R. Anderson, “In vivo confocal scanning laser microscopy of human skin: melanin provides strong contrast,” J. Invest. Dermatol. 104, 946–952 (1995).
[Crossref]

J. Microsc. (2)

P. Kner, J. W. Sedat, D. A. Agard, and Z. Kam, “High-resolution widefield microscopy with adaptive optics for spherical aberration correction and motionless focusing,” J. Microsc. 237, 136–147 (2010).
[Crossref]

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

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

J. Refractive Surg. (1)

B. C. Platt and R. Shack, “History and principles of Shack–Hartmann wavefront sensing,” J. Refractive Surg. 17, S573–S577 (2001).

Nat. Methods (3)

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2, 932–940 (2005).
[Crossref]

E. H. K. Stelzer, “Light-sheet fluorescence microscopy for quantitative biology,” Nat. Methods 12, 23–26 (2014).
[Crossref]

J. Mertz, “Optical sectioning microscopy with planar or structured illumination,” Nat. Methods 8, 811–819 (2011).
[Crossref]

Nat. Photonics (1)

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7, 205–209 (2013).
[Crossref]

Opt. Express (8)

D. Debarre, E. J. Botcherby, M. J. Booth, and T. Wilson, “Adaptive optics for structured illumination microscopy,” Opt. Express 16, 9290–9305 (2008).
[Crossref]

K. F. Tehrani, J. Xu, Y. Zhang, P. Shen, and P. Kner, “Adaptive optics stochastic optical reconstruction microscopy (AO-STORM) using a genetic algorithm,” Opt. Express 23, 13677–13692 (2015).
[Crossref]

O. Azucena, J. Crest, J. Cao, W. Sullivan, P. Kner, D. Gavel, D. Dillon, S. Olivier, and J. Kubby, “Wavefront aberration measurements and corrections through thick tissue using fluorescent microsphere reference beacons,” Opt. Express 18, 17521–17532 (2010).
[Crossref]

X. Tao, J. Crest, S. Kotadia, O. Azucena, D. C. Chen, B. Sullivan, and J. Kubby, “Live imaging using adaptive optics with fluorescent protein guide-stars,” Opt. Express 20, 15969–15982 (2012).
[Crossref]

A. Masson, M. Pedrazzani, S. Benrezzak, P. Tchenio, T. Preat, and D. Nutarelli, “Micromirror structured illumination microscope for high-speed in vivo drosophila brain imaging,” Opt. Express 22, 1243–1256 (2014).
[Crossref]

N. Chakrova, R. Heintzmann, B. Rieger, and S. Stallinga, “Studying different illumination patterns for resolution improvement in fluorescence microscopy,” Opt. Express 23, 31367–31383 (2015).
[Crossref]

M. Booth, “Wave front sensor-less adaptive optics: a model-based approach using sphere packings,” Opt. Express 14, 1339–1352 (2006).
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P. Krizek, I. Raaka, and G. M. Hagen, “Flexible structured illumination microscope with a programmable illumination array,” Opt. Express 20, 24585–24599 (2012).
[Crossref]

Opt. Lett. (9)

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

X. Tao, A. Norton, M. Kissel, O. Azucena, and J. Kubby, “Adaptive optical two-photon microscopy using auto fluorescent guide stars,” Opt. Lett. 38, 5075–5078 (2013).
[Crossref]

O. Azucena, J. Crest, S. Kotadia, W. Sullivan, X. Tao, M. Reinig, D. Gavel, S. Olivier, and J. Kubby, “Adaptive optics widefield microscopy using direct wavefront sensing,” Opt. Lett. 36, 825–827 (2011).
[Crossref]

X. Tao, B. Fernandez, O. Azucena, M. Fu, D. Garcia, Y. Zuo, D. C. Chen, and J. Kubby, “Adaptive optics confocal microscopy using direct wavefront sensing,” Opt. Lett. 36, 1062–1064 (2011).
[Crossref]

D. Debarre, E. J. Botcherby, T. Watanabe, S. Srinivas, M. J. Booth, and T. Wilson, “Image-based adaptive optics for two-photon microscopy,” Opt. Lett. 34, 2495–2497 (2009).
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P. Gao and U. Nienhaus, “Confocal laser scanning microscopy with spatiotemporal structured illumination,” Opt. Lett. 41, 1193–1196 (2016).
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M. A. A. Neil, R. Ju skaitis, and T. Wilson, “Method of obtaining optical sectioning by using structured light in a conventional microscope,” Opt. Lett. 22, 1905–1907 (1997).
[Crossref]

P. Gao, G. Pedrini, and W. Osten, “Structured illumination for resolution enhancement and autofocusing in digital holographic microscopy,” Opt. Lett. 38, 1328–1330 (2013).
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W. Gong, K. Si, N. Chen, and C. J. R. Sheppard, “Improved spatial resolution in fluorescence focal modulation microscopy,” Opt. Lett. 34, 3508–3510 (2009).
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Proc. Natl. Acad. Sci. USA (2)

M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy: widefield fluorescence imaging with theoretically unlimited resolution,” Proc. Natl. Acad. Sci. USA 102, 13081–13086 (2005).
[Crossref]

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. USA 99, 5788–5792 (2002).
[Crossref]

Proc. SPIE (4)

M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Doubling the lateral resolution of wide-field fluorescence microscopy using structured illumination,” Proc. SPIE 3919, 141–150 (2000).

Q. Song, K. Isobe, K. Hirosawa, K. Midorikawa, and F. Kannari, “2D simultaneous spatial and temporal focusing multiphoton microscopy for fast volume imaging with improved sectioning ability,” Proc. SPIE 9329, 93292N (2015).

S. A. Shroff, J. R. Fienup, and D. R. Williams, “OTF compensation in structured illumination superresolution images,” Proc. SPIE 7094, 709402 (2008).

M. Kissel, M. Reinig, O. Azucena, J. J. Diaz Leon, and J. Kubby, “Development and testing of an AO-structured illumination microscope,” Proc. SPIE 8978, 89780G (2014).
[Crossref]

Science (1)

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

Other (3)

J. A. Kubby, Adaptive Optics for Biological Imaging (CRC Press, 2013).

J. Porter, Adaptive Optics for Vision Science: Principles, Practices, Design, and Applications (Wiley-Interscience, 2006).

J. W. Hardy, Adaptive Optics for Astronomical Telescopes (Oxford University, 1998).

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Figures (6)

Fig. 1.
Fig. 1.

Layout of the woofer–tweeter AOSIM. The DLP with 608×684 pixels (DLP3000 Texas Instruments) is placed at a conjugate plane of the objective lens focal plane. The SHW sensor consists of a lenslet array (f=24  mm) and a CCD camera (Photometrics) and is placed at a conjugate plane of the objective lens aperture plane. Blue line, 488 nm excitation light path (488 nm excitation laser from Spectra-Physics); green line, 515 nm emission path. The focal lengths of the lenses are f1=120  mm, f2=125  mm, f3=120  mm, f4=150  mm, f5=500  mm, f6=750  mm, f7=150  mm, f8=75  mm, f9=100  mm, f10=450  mm, f11=150  mm, f12=50  mm. M, mirror; SF, spatial filter; TL, trial lens (cylinder); F, filter; Di, dichroic mirror; FM, flip mirror.

Fig. 2.
Fig. 2.

Comparison of (a)–(d) widefield and (e)–(h) SIM microscope images with and without wavefront correction. The figure shows the images of nanoparticles (110 nm) after introducing trial lens in between lenses f1 and f2. (a), (e) Without AO correction; (b), (f) woofer-only correction; (c), (d) tweeter-only correction; (d), (h) both woofer and tweeter correction. The scale bar is 5 μm.

Fig. 3.
Fig. 3.

Zernike modes of the wavefront errors with and without woofer–tweeter correction. The inset is the value of the remaining Zernike modes after removing the sixth-order vertical astigmatism. The Zernike order is in Noll single-index order [43].

Fig. 4.
Fig. 4.

Comparison of 0.11 μm beads under AO widefield (black line) and AOSIM (red line), Shown as line plots of the intensity of beads in areas 1 and 2 of Figs. 2(d) and 2(h). (a) Intensity profile of two closely spaced beads. The distance between two well-resolved peaks in AOSIM is 145 nm. (b) The FWHMs of a single bead in widefield and AOSIM are 235 and 140 nm, respectively.

Fig. 5.
Fig. 5.

Images of GFP-labeled aCC/RP2 motoneurons of a Drosophila embryo. (a) Widefield without AO, (b) SIM without AO, (c) widefield with AO, (d) SIM with AO, (e) intensity plots of the line profiles in (a)–(d). The lines are along the dendrites of the aCC. The scale bar is 10 μm.

Fig. 6.
Fig. 6.

Zernike modes of the Drosophila embryo wavefront errors with and without woofer–tweeter correction [43].

Tables (1)

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Table 1. Analysis of Measured Wavefront of Figs. 2(a)2(d)a

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