Abstract

We present IsoSense, a wavefront sensing method that mitigates sample dependency in image-based sensorless adaptive optics applications in microscopy. Our method employs structured illumination to create additional high spatial frequencies in the image through custom illumination patterns. This improves the reliability of image quality metric calculations and enables sensorless wavefront measurement even in samples with sparse spatial frequency content. We demonstrate the feasibility of IsoSense for aberration correction in a deformable-mirror-based structured illumination super-resolution fluorescence microscope.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2018 (5)

T. DuBose, D. Nankivil, F. LaRocca, G. Waterman, K. Hagan, J. Polans, B. Keller, D. Tran-Viet, L. Vajzovic, A. N. Kuo, C. A. Toth, J. A. Izatt, and S. Farsiu, “Handheld adaptive optics scanning laser ophthalmoscope,” Optica 5, 1027–1036 (2018).
[Crossref]

H. J. B. Marroux, A. P. Fidler, D. M. Neumark, and S. R. Leone, “Multidimensional spectroscopy with attosecond extreme ultraviolet and shaped near-infrared pulses,” Sci. Adv. 4, eaau3783 (2018).
[Crossref]

J. Antonello, X. Hao, E. S. Allgeyer, J. Bewersdorf, J. Rittscher, and M. J. Booth, “Sensorless adaptive optics for isoSTED nanoscopy,” Proc. SPIE 10502, 1050206 (2018).
[Crossref]

M. J. Mlodzianoski, P. J. Cheng-Hathaway, S. M. Bemiller, T. J. McCray, S. Liu, D. A. Miller, B. T. Lamb, G. E. Landreth, and F. Huang, “Active PSF shaping and adaptive optics enable volumetric localization microscopy through brain sections,” Nat. Methods 15, 583–586 (2018).
[Crossref]

T.-L. Liu, S. Upadhyayula, D. E. Milkie, V. Singh, K. Wang, I. A. Swinburne, K. R. Mosaliganti, Z. M. Collins, T. W. Hiscock, J. Shea, A. Q. Kohrman, T. N. Medwig, D. Dambournet, R. Forster, B. Cunniff, Y. Ruan, H. Yashiro, S. Scholpp, E. M. Meyerowitz, D. Hockemeyer, D. G. Drubin, B. L. Martin, D. Q. Matus, M. Koyama, S. G. Megason, T. Kirchhausen, and E. Betzig, “Observing the cell in its native state: Imaging subcellular dynamics in multicellular organisms,” Science 360, eaaq1392 (2018).
[Crossref]

2017 (4)

2016 (2)

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

M. Müller, V. Mönkemöller, S. Hennig, W. Hübner, and T. Huser, “Open-source image reconstruction of super-resolution structured illumination microscopy data in ImageJ,” Nat. Commun. 7, 10980 (2016).
[Crossref]

2015 (3)

2014 (1)

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

2013 (1)

2012 (2)

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. USA 109, 7175–7180 (2012).
[Crossref]

M. Arigovindan, J. W. Sedat, and D. A. Agard, “Effect of depth dependent spherical aberrations in 3D structured illumination microscopy,” Opt. Express 20, 6527–6541 (2012).
[Crossref]

2010 (2)

P. J. Keller, A. D. Schmidt, A. Santella, K. Khairy, Z. Bao, J. Wittbrodt, and E. H. Stelzer, “Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy,” Nat. Methods 7, 637–642 (2010).
[Crossref]

P. Kner, L. Winoto, D. A. Agar, and J. W. Sedat, “Closed loop adaptive optics for microscopy without a wavefront sensor,” Proc. SPIE 7570, 75709 (2010).
[Crossref]

2008 (4)

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

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, 1332–1336 (2008).
[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. Stofanko, S. Y. Kwon, and P. Badenhorst, “A misexpression screen to identify regulators of Drosophila larval hemocyte development,” Genetics 180, 253–267 (2008).
[Crossref]

2007 (2)

2005 (1)

2000 (1)

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]

1976 (1)

Adie, S. G.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. USA 109, 7175–7180 (2012).
[Crossref]

Agar, D. A.

P. Kner, L. Winoto, D. A. Agar, and J. W. Sedat, “Closed loop adaptive optics for microscopy without a wavefront sensor,” Proc. SPIE 7570, 75709 (2010).
[Crossref]

Agard, D. A.

M. Arigovindan, J. W. Sedat, and D. A. Agard, “Effect of depth dependent spherical aberrations in 3D structured illumination microscopy,” Opt. Express 20, 6527–6541 (2012).
[Crossref]

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, 1332–1336 (2008).
[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]

Ahmad, A.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. USA 109, 7175–7180 (2012).
[Crossref]

Allgeyer, E. S.

J. Antonello, X. Hao, E. S. Allgeyer, J. Bewersdorf, J. Rittscher, and M. J. Booth, “Sensorless adaptive optics for isoSTED nanoscopy,” Proc. SPIE 10502, 1050206 (2018).
[Crossref]

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

Antonello, J.

J. Antonello, X. Hao, E. S. Allgeyer, J. Bewersdorf, J. Rittscher, and M. J. Booth, “Sensorless adaptive optics for isoSTED nanoscopy,” Proc. SPIE 10502, 1050206 (2018).
[Crossref]

J. Antonello, “Optimisation-based wavefront sensorless adaptive optics for microscopy,” Ph.D. thesis (Delft University of Technology, 2014).

Arigovindan, M.

Badenhorst, P.

M. Stofanko, S. Y. Kwon, and P. Badenhorst, “A misexpression screen to identify regulators of Drosophila larval hemocyte development,” Genetics 180, 253–267 (2008).
[Crossref]

Ball, G.

J. Demmerle, C. Innocent, A. J. North, G. Ball, M. Müller, E. Miron, A. Matsuda, I. M. Dobbie, Y. Markaki, and L. Schermelleh, “Strategic and practical guidelines for successful structured illumination microscopy,” Nat. Protoc. 12, 988–1010 (2017).
[Crossref]

Bao, Z.

P. J. Keller, A. D. Schmidt, A. Santella, K. Khairy, Z. Bao, J. Wittbrodt, and E. H. Stelzer, “Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy,” Nat. Methods 7, 637–642 (2010).
[Crossref]

Barnstedt, O.

Bembenek, J. N.

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

Bemiller, S. M.

M. J. Mlodzianoski, P. J. Cheng-Hathaway, S. M. Bemiller, T. J. McCray, S. Liu, D. A. Miller, B. T. Lamb, G. E. Landreth, and F. Huang, “Active PSF shaping and adaptive optics enable volumetric localization microscopy through brain sections,” Nat. Methods 15, 583–586 (2018).
[Crossref]

Betzig, E.

T.-L. Liu, S. Upadhyayula, D. E. Milkie, V. Singh, K. Wang, I. A. Swinburne, K. R. Mosaliganti, Z. M. Collins, T. W. Hiscock, J. Shea, A. Q. Kohrman, T. N. Medwig, D. Dambournet, R. Forster, B. Cunniff, Y. Ruan, H. Yashiro, S. Scholpp, E. M. Meyerowitz, D. Hockemeyer, D. G. Drubin, B. L. Martin, D. Q. Matus, M. Koyama, S. G. Megason, T. Kirchhausen, and E. Betzig, “Observing the cell in its native state: Imaging subcellular dynamics in multicellular organisms,” Science 360, eaaq1392 (2018).
[Crossref]

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

Bewersdorf, J.

J. Antonello, X. Hao, E. S. Allgeyer, J. Bewersdorf, J. Rittscher, and M. J. Booth, “Sensorless adaptive optics for isoSTED nanoscopy,” Proc. SPIE 10502, 1050206 (2018).
[Crossref]

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

D. Burke, B. Patton, F. Huang, J. Bewersdorf, and M. J. Booth, “Adaptive optics correction of specimen-induced aberrations in single-molecule switching microscopy,” Optica 2, 177–185 (2015).
[Crossref]

Böhme, R.

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

Booth, M.

Booth, M. J.

J. Antonello, X. Hao, E. S. Allgeyer, J. Bewersdorf, J. Rittscher, and M. J. Booth, “Sensorless adaptive optics for isoSTED nanoscopy,” Proc. SPIE 10502, 1050206 (2018).
[Crossref]

M. Žurauskas, O. Barnstedt, M. Frade-Rodriguez, S. Waddell, and M. J. Booth, “Rapid adaptive remote focusing microscope for sensing of volumetric neural activity,” Biomed. Opt. Express 8, 4369–4379 (2017).
[Crossref]

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

D. Burke, B. Patton, F. Huang, J. Bewersdorf, and M. J. Booth, “Adaptive optics correction of specimen-induced aberrations in single-molecule switching microscopy,” Optica 2, 177–185 (2015).
[Crossref]

S. A. Rahman and M. J. Booth, “Direct wavefront sensing in adaptive optical microscopy using backscattered light,” Appl. Opt. 52, 5523–5532 (2013).
[Crossref]

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

M. J. Booth, “Wavefront sensorless adaptive optics for large aberrations,” Opt. Lett. 32, 5–7 (2007).
[Crossref]

D. Débarre, M. J. Booth, and T. Wilson, “Image based adaptive optics through optimisation of low spatial frequencies,” Opt. Express 15, 8176–8190 (2007).
[Crossref]

Boppart, S. A.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. USA 109, 7175–7180 (2012).
[Crossref]

Botcherby, E. J.

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, 1332–1336 (2008).
[Crossref]

Burke, D.

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]

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P. Kner, L. Winoto, D. A. Agar, and J. W. Sedat, “Closed loop adaptive optics for microscopy without a wavefront sensor,” Proc. SPIE 7570, 75709 (2010).
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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, 1332–1336 (2008).
[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]

Seydoux, G.

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

Shanqiu, C.

Shao, L.

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

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, 1332–1336 (2008).
[Crossref]

Shea, J.

T.-L. Liu, S. Upadhyayula, D. E. Milkie, V. Singh, K. Wang, I. A. Swinburne, K. R. Mosaliganti, Z. M. Collins, T. W. Hiscock, J. Shea, A. Q. Kohrman, T. N. Medwig, D. Dambournet, R. Forster, B. Cunniff, Y. Ruan, H. Yashiro, S. Scholpp, E. M. Meyerowitz, D. Hockemeyer, D. G. Drubin, B. L. Martin, D. Q. Matus, M. Koyama, S. G. Megason, T. Kirchhausen, and E. Betzig, “Observing the cell in its native state: Imaging subcellular dynamics in multicellular organisms,” Science 360, eaaq1392 (2018).
[Crossref]

Shechtman, Y.

Shen, P.

Shuai, W.

Singh, V.

T.-L. Liu, S. Upadhyayula, D. E. Milkie, V. Singh, K. Wang, I. A. Swinburne, K. R. Mosaliganti, Z. M. Collins, T. W. Hiscock, J. Shea, A. Q. Kohrman, T. N. Medwig, D. Dambournet, R. Forster, B. Cunniff, Y. Ruan, H. Yashiro, S. Scholpp, E. M. Meyerowitz, D. Hockemeyer, D. G. Drubin, B. L. Martin, D. Q. Matus, M. Koyama, S. G. Megason, T. Kirchhausen, and E. Betzig, “Observing the cell in its native state: Imaging subcellular dynamics in multicellular organisms,” Science 360, eaaq1392 (2018).
[Crossref]

Sirinakis, G.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

Stelzer, E. H.

P. J. Keller, A. D. Schmidt, A. Santella, K. Khairy, Z. Bao, J. Wittbrodt, and E. H. Stelzer, “Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy,” Nat. Methods 7, 637–642 (2010).
[Crossref]

Stofanko, M.

M. Stofanko, S. Y. Kwon, and P. Badenhorst, “A misexpression screen to identify regulators of Drosophila larval hemocyte development,” Genetics 180, 253–267 (2008).
[Crossref]

Sun, H.-B.

Swinburne, I. A.

T.-L. Liu, S. Upadhyayula, D. E. Milkie, V. Singh, K. Wang, I. A. Swinburne, K. R. Mosaliganti, Z. M. Collins, T. W. Hiscock, J. Shea, A. Q. Kohrman, T. N. Medwig, D. Dambournet, R. Forster, B. Cunniff, Y. Ruan, H. Yashiro, S. Scholpp, E. M. Meyerowitz, D. Hockemeyer, D. G. Drubin, B. L. Martin, D. Q. Matus, M. Koyama, S. G. Megason, T. Kirchhausen, and E. Betzig, “Observing the cell in its native state: Imaging subcellular dynamics in multicellular organisms,” Science 360, eaaq1392 (2018).
[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]

Toomre, D.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

Toth, C. A.

Tran-Viet, D.

Tulu, U. S.

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

Upadhyayula, S.

T.-L. Liu, S. Upadhyayula, D. E. Milkie, V. Singh, K. Wang, I. A. Swinburne, K. R. Mosaliganti, Z. M. Collins, T. W. Hiscock, J. Shea, A. Q. Kohrman, T. N. Medwig, D. Dambournet, R. Forster, B. Cunniff, Y. Ruan, H. Yashiro, S. Scholpp, E. M. Meyerowitz, D. Hockemeyer, D. G. Drubin, B. L. Martin, D. Q. Matus, M. Koyama, S. G. Megason, T. Kirchhausen, and E. Betzig, “Observing the cell in its native state: Imaging subcellular dynamics in multicellular organisms,” Science 360, eaaq1392 (2018).
[Crossref]

Vajzovic, L.

Valles, A.

R. M. Parton, A. Valles, I. Dobbie, and I. Davis, “Pushing the limits of live cell imaging in Drosophila,” in Live Cell Imaging: A Laboratory Manual, R. Goldman, D. Spector, and J. Swedlow, eds., 2nd ed., (Cold Spring Harbor Laboratory, 2010).

Waddell, S.

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, J. T.

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

Wang, K.

T.-L. Liu, S. Upadhyayula, D. E. Milkie, V. Singh, K. Wang, I. A. Swinburne, K. R. Mosaliganti, Z. M. Collins, T. W. Hiscock, J. Shea, A. Q. Kohrman, T. N. Medwig, D. Dambournet, R. Forster, B. Cunniff, Y. Ruan, H. Yashiro, S. Scholpp, E. M. Meyerowitz, D. Hockemeyer, D. G. Drubin, B. L. Martin, D. Q. Matus, M. Koyama, S. G. Megason, T. Kirchhausen, and E. Betzig, “Observing the cell in its native state: Imaging subcellular dynamics in multicellular organisms,” Science 360, eaaq1392 (2018).
[Crossref]

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

Waterman, G.

Wenjing, L.

Wilson, T.

Winoto, L.

P. Kner, L. Winoto, D. A. Agar, and J. W. Sedat, “Closed loop adaptive optics for microscopy without a wavefront sensor,” Proc. SPIE 7570, 75709 (2010).
[Crossref]

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, 1332–1336 (2008).
[Crossref]

Wittbrodt, J.

P. J. Keller, A. D. Schmidt, A. Santella, K. Khairy, Z. Bao, J. Wittbrodt, and E. H. Stelzer, “Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy,” Nat. Methods 7, 637–642 (2010).
[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]

Wu, X. S.

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

Xu, B.

Xu, J.

Yang, P.

Yashiro, H.

T.-L. Liu, S. Upadhyayula, D. E. Milkie, V. Singh, K. Wang, I. A. Swinburne, K. R. Mosaliganti, Z. M. Collins, T. W. Hiscock, J. Shea, A. Q. Kohrman, T. N. Medwig, D. Dambournet, R. Forster, B. Cunniff, Y. Ruan, H. Yashiro, S. Scholpp, E. M. Meyerowitz, D. Hockemeyer, D. G. Drubin, B. L. Martin, D. Q. Matus, M. Koyama, S. G. Megason, T. Kirchhausen, and E. Betzig, “Observing the cell in its native state: Imaging subcellular dynamics in multicellular organisms,” Science 360, eaaq1392 (2018).
[Crossref]

Zhang, Y.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[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]

Žurauskas, M.

Appl. Opt. (2)

Biomed. Opt. Express (1)

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]

Cell (1)

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

Genetics (1)

M. Stofanko, S. Y. Kwon, and P. Badenhorst, “A misexpression screen to identify regulators of Drosophila larval hemocyte development,” Genetics 180, 253–267 (2008).
[Crossref]

J. Biomed. Opt. (1)

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]

J. Microsc. (1)

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. (1)

Nat. Commun. (1)

M. Müller, V. Mönkemöller, S. Hennig, W. Hübner, and T. Huser, “Open-source image reconstruction of super-resolution structured illumination microscopy data in ImageJ,” Nat. Commun. 7, 10980 (2016).
[Crossref]

Nat. Methods (2)

M. J. Mlodzianoski, P. J. Cheng-Hathaway, S. M. Bemiller, T. J. McCray, S. Liu, D. A. Miller, B. T. Lamb, G. E. Landreth, and F. Huang, “Active PSF shaping and adaptive optics enable volumetric localization microscopy through brain sections,” Nat. Methods 15, 583–586 (2018).
[Crossref]

P. J. Keller, A. D. Schmidt, A. Santella, K. Khairy, Z. Bao, J. Wittbrodt, and E. H. Stelzer, “Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy,” Nat. Methods 7, 637–642 (2010).
[Crossref]

Nat. Protoc. (1)

J. Demmerle, C. Innocent, A. J. North, G. Ball, M. Müller, E. Miron, A. Matsuda, I. M. Dobbie, Y. Markaki, and L. Schermelleh, “Strategic and practical guidelines for successful structured illumination microscopy,” Nat. Protoc. 12, 988–1010 (2017).
[Crossref]

Opt. Express (6)

Opt. Lett. (1)

Optica (2)

Proc. Natl. Acad. Sci. USA (1)

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. USA 109, 7175–7180 (2012).
[Crossref]

Proc. SPIE (2)

J. Antonello, X. Hao, E. S. Allgeyer, J. Bewersdorf, J. Rittscher, and M. J. Booth, “Sensorless adaptive optics for isoSTED nanoscopy,” Proc. SPIE 10502, 1050206 (2018).
[Crossref]

P. Kner, L. Winoto, D. A. Agar, and J. W. Sedat, “Closed loop adaptive optics for microscopy without a wavefront sensor,” Proc. SPIE 7570, 75709 (2010).
[Crossref]

Sci. Adv. (1)

H. J. B. Marroux, A. P. Fidler, D. M. Neumark, and S. R. Leone, “Multidimensional spectroscopy with attosecond extreme ultraviolet and shaped near-infrared pulses,” Sci. Adv. 4, eaau3783 (2018).
[Crossref]

Science (3)

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, 1332–1336 (2008).
[Crossref]

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

T.-L. Liu, S. Upadhyayula, D. E. Milkie, V. Singh, K. Wang, I. A. Swinburne, K. R. Mosaliganti, Z. M. Collins, T. W. Hiscock, J. Shea, A. Q. Kohrman, T. N. Medwig, D. Dambournet, R. Forster, B. Cunniff, Y. Ruan, H. Yashiro, S. Scholpp, E. M. Meyerowitz, D. Hockemeyer, D. G. Drubin, B. L. Martin, D. Q. Matus, M. Koyama, S. G. Megason, T. Kirchhausen, and E. Betzig, “Observing the cell in its native state: Imaging subcellular dynamics in multicellular organisms,” Science 360, eaaq1392 (2018).
[Crossref]

Other (4)

R. M. Parton, A. Valles, I. Dobbie, and I. Davis, “Pushing the limits of live cell imaging in Drosophila,” in Live Cell Imaging: A Laboratory Manual, R. Goldman, D. Spector, and J. Swedlow, eds., 2nd ed., (Cold Spring Harbor Laboratory, 2010).

M. D. Pritt and D. C. Ghiglia, Two-Dimensional Phase Unwrapping: Theory, Algorithms, and Software (Wiley, 1998).

J. Antonello, “Optimisation-based wavefront sensorless adaptive optics for microscopy,” Ph.D. thesis (Delft University of Technology, 2014).

J. Sedat, University of California, San Francisco (UCSF) (personal communication, 2010).

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Figures (9)

Fig. 1.
Fig. 1. Image-quality-metric-based wavefront sensing. (a) Flowchart depicting classical implementation of sensorless-AO-based wavefront measurement. (b) Sample images are captured for each mode using at least three different bias values (b, a, +b). Image quality is estimated using a suitable defined metric for each image (M, Mz, M+), and a quadratic function is fitted to the measured points. The peak value of the fitted curve corresponds to estimated best correction. Inset images represent a PSF affected by various amounts of coma. (c) Typical image quality evolution as different modes are corrected in pre-set sequence. The correction order on the horizontal axis refers to events in which individual modes from the sequence are corrected.
Fig. 2.
Fig. 2. Spatial frequency content as a basis for image quality measurements. An FFT of a lawn of sub-diffraction-limit sized beads contains a good representation of all the spatial frequencies that can be transmitted by the system [(a) raw image, and (b) FFT] before correction and (c), (d) after. In many experiments, images of real samples do not contain a wide enough range of spatial frequency information for adequate pupil sampling: an image of a bovine pulmonary artery endothelial cell showing preferentially oriented actin (e) illustrates uneven information distribution in the spatial frequency space [FFT (f)].
Fig. 3.
Fig. 3. Custom illumination patterns for enhanced sampling of the OTF. (a), (b) Illustration of OTF calculation. The OTF (b) is calculated as the autocorrelation of the shifted pupil function (a). The absolute value of the OTF is numerically identical to the contrast of the image of a sine grating at the corresponding spatial frequency. In a simplified case, an object consisting of one spatial frequency (a), (b), would be affected only by aberrations affecting the OTF (e), (i) through a few limited zones in the pupil plane (f), (j). Conversely, any phase aberrations that do not affect the spatial frequencies present in an object [denoted by dark pink (f), (j), (n)] are undetectable by using image-quality-based metrics. (k)–(n) illustrate that a carefully chosen illumination pattern can help to fill the pupil with information and ensure adequate sampling of the OTF.
Fig. 4.
Fig. 4. Structured illumination for reducing sample-dependent effects on wavefront sensing accuracy. (a) Simulated illumination pattern resulting from four-beam interference. (b) Frequency content of the illumination pattern. (c) Image acquired from a fixed bovine pulmonary artery endothelial cell showing actin (Alexa 488, phalloidin), illuminated with the sensing pattern. (d) Fourier transform of (c) demonstrates increased signal at higher spatial frequencies.
Fig. 5.
Fig. 5. Interferometric wavefront sensing for mirror control. (a) A schematic showing the main components of the interferometer; (b) an interferogram captured with the interference camera; (c) FFT of (b); (d) masked and shifted high frequency carrier; (e) phase profile corresponding to the optical phase of the wavefront was then obtained after phase unwrapping.
Fig. 6.
Fig. 6. Optical setup for AO SIM imaging.
Fig. 7.
Fig. 7. SIM reconstruction of 2D bead clusters on the coverslip represents a non-aberrating object. In a well-aligned system, system flat AO correction setting (b) should provide similar image quality as when AO is bypassed (c). When the mirror is switched off (a), the membrane relaxes, significantly affecting image quality.
Fig. 8.
Fig. 8. AO correction for live SIM imaging of a macrophage expressing Jupiter::GFP (labeling microtubules). IsoSense corrected images (b) and (d) contain fewer artifacts than the images (a) and (c) that were obtained using system flat correction. The benefit of correction is much more apparent in SIM reconstructions (c) versus (d) (bottom row) than in pseudo-widefield reconstructions (a) versus (b) (top row).
Fig. 9.
Fig. 9. AO corrections for cellular imaging with SIM. (a) and (c) Widefield and reconstructed images of Jupiter::GFP expressing lamellocytes labeling microtubules, where image-quality-based wavefront sensing was performed with widefield illumination. In (b) and (d), custom illumination patterns for imaging quality sensing were used. (c) demonstrates higher quality correction along the direction corresponding with preferential fiber orientation, while (d) shows more isotropic and better overall correction. (e), (g) are the amplitude components of Fourier transforms of the widefield images, and (f), (h) are the detected phase profiles used for correction (in radians).

Equations (2)

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OTF(m)=PP*=P(rm)P*(r)d2r.
P(x,y)=sin(Ax+By)·sin(Ay+Bx).

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