Abstract

Scanning microscopes are important research tools for investigating 3D specimens. Modern beam shaping techniques can be combined with suitably designed data processing algorithms to improve instrument versatility and imaging performance. Here we introduce image scanning microscopy with freely programmable excitation and detection pupils and investigate point spread function (PSF) designs for parallel 3D information acquisition. The volumetric data is collected in a single 2D scan without the requirement of physical refocus. By sculpturing the excitation and detection PSFs into helical shapes of opposing handedness, we are able to capture sample information in a volume whose axial extension measures more than four times the z resolution. In a more generalized approach, jointly optimized phase masks are used in both pupils to shape the PSFs. As an exemplary case, we study the use of beam-splitting phase masks for the parallel scanning in multiple planes. The image reconstruction algorithm optimally integrates this information according to the various signal-to-noise ratios. Generalized PSF engineering scanning systems provide resolution improvement relative to confocal microscopy while accelerating data collection. We analyze the opportunities, trade-offs, and limitations of the approach.

© 2017 Optical Society of America

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Corrections

15 November 2017: A correction was made to the funding section.


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2017 (1)

M. Castello, G. Tortarolo, M. Buttafava, A. Tosi, C. Sheppard, A. Diaspro, and G. Vicidomini, “Image scanning microscopy using a SPAD detector array (Conference Presentation),” Proc. SPIE 10071, 1007101 (2017).
[Crossref]

2016 (2)

2015 (3)

2014 (2)

Y. Shechtman, S. J. Sahl, A. S. Backer, and W. E. Moerner, “Optimal point spread function design for 3D imaging,” Phys. Rev. Lett. 113, 133902 (2014).
[Crossref]

M. Ingaramo, A. G. York, E. Hoogendoorn, M. Postma, H. Shroff, and G. H. Patterson, “Richardson-Lucy deconvolution as a general tool for combining images with complementary strengths,” Chem. Phys. Chem. 15, 794–800 (2014).
[Crossref]

2013 (7)

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

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, and H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Methods 10, 1122–1126 (2013).
[Crossref]

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. D. Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2013).
[Crossref]

J. H. Clegg and M. A. A. Neil, “Double pass, common path method for arbitrary polarization control using a ferroelectric liquid crystal spatial light modulator,” Opt. Lett. 38, 1043–1045 (2013).
[Crossref]

A. Jesacher, C. Roider, and M. Ritsch-Marte, “Enhancing diffractive multi-plane microscopy using colored illumination,” Opt. Express 21, 11150–11161 (2013).
[Crossref]

C. J. R. Sheppard, S. B. Mehta, and R. Heintzmann, “Superresolution by image scanning microscopy using pixel reassignment,” Opt. Lett. 38, 2889–2892 (2013).
[Crossref]

G. M. R. De Luca, R. M. P. Breedijk, R. A. J. Brandt, C. H. C. Zeelenberg, B. E. de Jong, W. Timmermans, L. N. Azar, R. A. Hoebe, S. Stallinga, and E. M. M. Manders, “Re-scan confocal microscopy: scanning twice for better resolution,” Biomed. Opt. Express 4, 2644–2656 (2013).
[Crossref]

2012 (3)

A. Agrawal, S. Quirin, G. Grover, and R. Piestun, “Limits of 3D dipole localization and orientation estimation for single-molecule imaging: towards Green’s tensor engineering,” Opt. Express 20, 26667–26680 (2012).
[Crossref]

M. Temerinac-Ott, O. Ronneberger, P. Ochs, W. Driever, T. Brox, and H. Burkhardt, “Multiview deblurring for 3-D images from light-sheet-based fluorescence microscopy,” IEEE Trans. on Image Process. 21, 1863–1873 (2012).
[Crossref]

M. P. Backlund, M. D. Lew, A. S. Backer, S. J. Sahl, G. Grover, A. Agrawal, R. Piestun, and W. E. Moerner, “Simultaneous, accurate measurement of the 3D position and orientation of single molecules,” Proc. Natl. Acad. Sci. USA 109, 19087–19092 (2012).
[Crossref]

2010 (3)

2009 (1)

2008 (2)

2007 (2)

M. J. Booth, “Adaptive optics in microscopy,” Philos. Trans. R. Soc. A 365, 2829–2843 (2007).
[Crossref]

C. Maurer, A. Jesacher, S. Fürhapter, S. Bernet, and M. Ritsch-Marte, “Tailoring of arbitrary optical vector beams,” New J. Phys. 9, 78 (2007).
[Crossref]

2006 (2)

E. J. Botcherby, R. Juškaitis, and T. Wilson, “Scanning two photon fluorescence microscopy with extended depth of field,” Opt. Commun. 268, 253–260 (2006).
[Crossref]

G. Indebetouw and W. Zhong, “Scanning holographic microscopy of three-dimensional fluorescent specimens,” J. Opt. Soc. Am. A 23, 1699–1707 (2006).
[Crossref]

2004 (1)

A. Greengard, Y. Y. Schechner, and R. Piestun, “Depth from rotating point spread functions,” Proc. SPIE 5557, 91–97 (2004).
[Crossref]

2002 (2)

2001 (1)

R. Heintzmann, Q. Hanley, D. Arndt-Jovin, and T. Jovin, “A dual path programmable array microscope (PAM): simultaneous acquisition of conjugate and non-conjugate images,” J. Microsc. 204, 119–135 (2001).
[Crossref]

2000 (3)

R. Heintzmann, G. Kreth, and C. Cremer, “Reconstruction of axial tomographic high resolution data from confocal fluorescence microscopy: a method for improving 3D FISH images,” Anal. Cell. Pathol. 20, 7–15 (2000).
[Crossref]

J. Campos, J. C. Escalera, C. J. Sheppard, and M. J. Yzuel, “Axially invariant pupil filters,” J. Mod. Opt. 47, 57–68 (2000).
[Crossref]

M. A. A. Neil, R. Juškaitis, T. Wilson, Z. J. Laczik, and V. Sarafis, “Optimized pupil-plane filters for confocal microscope point-spread function engineering,” Opt. Lett. 25, 245–247 (2000).
[Crossref]

1999 (1)

1995 (1)

M. Martínez-Corral, P. Andres, J. Ojeda-Castaneda, and G. Saavedra, “Tunable axial superresolution by annular binary filters. Application to confocal microscopy,” Opt. Commun. 119, 491–498 (1995).
[Crossref]

1994 (4)

1988 (1)

C. J. R. Sheppard, “Super-resolution in confocal imaging,” Optik 80, 53–54 (1988).

1986 (1)

1985 (2)

1982 (1)

L. A. Shepp and Y. Vardi, “Maximum likelihood reconstruction for emission tomography,” IEEE Trans. Med. Imaging 1, 113–122 (1982).
[Crossref]

1979 (1)

1977 (2)

A. P. Dempster, N. M. Laird, and D. B. Rubin, “Maximum likelihood from incomplete data via the EM algorithm,” Journal of the Royal Statistical Society Series B 39, 1–38 (1977).

C. J. R. Sheppard and A. Choudhury, “Image formation in the scanning microscope,” J. Mod. Opt. 24, 1051–1073 (1977).
[Crossref]

1974 (1)

L. B. Lucy, “An iterative technique for the rectification of observed distributions,” Astron. J. 79, 745–754 (1974).
[Crossref]

1972 (1)

1964 (1)

1960 (1)

1952 (1)

G. T. di Francia, “Nuovo pupille superresolventi,” Atti Fond. Giorgio Ronchi 7, 366–372 (1952).

Abrahamsson, S.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. D. Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2013).
[Crossref]

Agard, D. A.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. D. Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2013).
[Crossref]

Agrawal, A.

M. P. Backlund, M. D. Lew, A. S. Backer, S. J. Sahl, G. Grover, A. Agrawal, R. Piestun, and W. E. Moerner, “Simultaneous, accurate measurement of the 3D position and orientation of single molecules,” Proc. Natl. Acad. Sci. USA 109, 19087–19092 (2012).
[Crossref]

A. Agrawal, S. Quirin, G. Grover, and R. Piestun, “Limits of 3D dipole localization and orientation estimation for single-molecule imaging: towards Green’s tensor engineering,” Opt. Express 20, 26667–26680 (2012).
[Crossref]

Andres, P.

M. Martínez-Corral, P. Andres, J. Ojeda-Castaneda, and G. Saavedra, “Tunable axial superresolution by annular binary filters. Application to confocal microscopy,” Opt. Commun. 119, 491–498 (1995).
[Crossref]

Anhut, T.

J. Huff, W. Bathe, R. Netz, T. Anhut, and K. Weisshart, “The Airyscan detector from ZEISS: confocal imaging with improved signal-to-noise ratio and super-resolution,” Nat. Methods 12, 1–19 (2015).

Araya, R.

V. Nikolenko, B. O. Watson, R. Araya, A. Woodruff, D. S. Peterka, and R. Yuste, “SLM Microscopy: scanless two-photon imaging and photostimulation using spatial light modulators,” Front. Neural Circuits2 (2008).

Arndt-Jovin, D.

R. Heintzmann, Q. Hanley, D. Arndt-Jovin, and T. Jovin, “A dual path programmable array microscope (PAM): simultaneous acquisition of conjugate and non-conjugate images,” J. Microsc. 204, 119–135 (2001).
[Crossref]

Azar, L. N.

Azuma, T.

Backer, A. S.

Y. Shechtman, S. J. Sahl, A. S. Backer, and W. E. Moerner, “Optimal point spread function design for 3D imaging,” Phys. Rev. Lett. 113, 133902 (2014).
[Crossref]

M. P. Backlund, M. D. Lew, A. S. Backer, S. J. Sahl, G. Grover, A. Agrawal, R. Piestun, and W. E. Moerner, “Simultaneous, accurate measurement of the 3D position and orientation of single molecules,” Proc. Natl. Acad. Sci. USA 109, 19087–19092 (2012).
[Crossref]

Backlund, M. P.

M. P. Backlund, M. D. Lew, A. S. Backer, S. J. Sahl, G. Grover, A. Agrawal, R. Piestun, and W. E. Moerner, “Simultaneous, accurate measurement of the 3D position and orientation of single molecules,” Proc. Natl. Acad. Sci. USA 109, 19087–19092 (2012).
[Crossref]

Bargmann, C. I.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. D. Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2013).
[Crossref]

Bathe, W.

J. Huff, W. Bathe, R. Netz, T. Anhut, and K. Weisshart, “The Airyscan detector from ZEISS: confocal imaging with improved signal-to-noise ratio and super-resolution,” Nat. Methods 12, 1–19 (2015).

Bernet, S.

Blahut, R. E.

R. E. Blahut, Theory of Remote Image Formation (Cambridge University, 2004).

Blanchard, P. M.

Booth, M. J.

M. J. Booth, “Adaptive optics in microscopy,” Philos. Trans. R. Soc. A 365, 2829–2843 (2007).
[Crossref]

Botcherby, E. J.

E. J. Botcherby, R. Juškaitis, and T. Wilson, “Scanning two photon fluorescence microscopy with extended depth of field,” Opt. Commun. 268, 253–260 (2006).
[Crossref]

Brandt, R. A. J.

Breedijk, R. M. P.

Brox, T.

M. Temerinac-Ott, O. Ronneberger, P. Ochs, W. Driever, T. Brox, and H. Burkhardt, “Multiview deblurring for 3-D images from light-sheet-based fluorescence microscopy,” IEEE Trans. on Image Process. 21, 1863–1873 (2012).
[Crossref]

Burkhardt, H.

M. Temerinac-Ott, O. Ronneberger, P. Ochs, W. Driever, T. Brox, and H. Burkhardt, “Multiview deblurring for 3-D images from light-sheet-based fluorescence microscopy,” IEEE Trans. on Image Process. 21, 1863–1873 (2012).
[Crossref]

Buttafava, M.

M. Castello, G. Tortarolo, M. Buttafava, A. Tosi, C. Sheppard, A. Diaspro, and G. Vicidomini, “Image scanning microscopy using a SPAD detector array (Conference Presentation),” Proc. SPIE 10071, 1007101 (2017).
[Crossref]

Caballero, M. T.

Campos, J.

J. Campos, J. C. Escalera, C. J. Sheppard, and M. J. Yzuel, “Axially invariant pupil filters,” J. Mod. Opt. 47, 57–68 (2000).
[Crossref]

Castello, M.

M. Castello, G. Tortarolo, M. Buttafava, A. Tosi, C. Sheppard, A. Diaspro, and G. Vicidomini, “Image scanning microscopy using a SPAD detector array (Conference Presentation),” Proc. SPIE 10071, 1007101 (2017).
[Crossref]

Cathey, W. T.

Chandris, P.

A. G. York, P. Chandris, D. Dalle Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, and H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Methods 10, 1122–1126 (2013).
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Supplementary Material (6)

NameDescription
» Supplement 1       supplementary text document
» Visualization 1       data shows detector position (red spot) on camera and projections of the corresponding 3D PSFs.
» Visualization 2       data shows detector position (red spot) on camera and projections of the corresponding 3D PSFs.
» Visualization 3       data shows detector position (red spot) on camera and projections of the corresponding 3D PSFs.
» Visualization 4       data shows detector position (red spot) on camera and projections of the corresponding 3D PSFs.
» Visualization 5       data shows detector position (red spot) on camera and projections of the corresponding 3D PSFs.

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Figures (9)

Fig. 1.
Fig. 1.

Sketch of the eISM microscope. A single LCoS SLM (here shown as transmissive device for clarity) is used to display individual diffractive patterns ( P ex and P det ) for shaping the excitation and detection PSFs independently. The inset in the lower right corner shows the light path unfolded to visualize the image formation described in Eq. (1). H ex and H det are the excitation and detection optical transfer functions, respectively, and ρ is the fluorophore density of the object. The abbreviation “FT” denotes the optical Fourier transform performed by a lens.

Fig. 2.
Fig. 2.

Imaging of a three-layered fluorescent structure in the helix-helix system. (a) The helical excitation focus (green) is produced by a helical phase mask (greyscale image) and excites the layers at approximately elliptical intersection regions (yellow). (b) Another helical phase mask in the detection arm (greyscale image) forms the detection PSF into a helix as well. The plane that is finally imaged onto the camera is the center plane of ( h ex · ρ ) h det . If the handedness of h det (red helix) is different from h ex , the images of the excited zones show a large lateral separation on the camera (red elliptic zones).

Fig. 3.
Fig. 3.

Properties of 3D PSFs h m in: (a) ISM and (b) helix-helix imaging. The PSF properties are color-coded in the five images ( NA = 0.92 · RI , with RI being the sample refractive index; circular excitation polarization and unpolarized fluorescence, but no Stokes shift assumed; λ is the wavelength in a medium with a refractive index RI).

Fig. 4.
Fig. 4.

Energy harvests for ISM (green plots) and helix-helix imaging. Dashed lines: energies contained in the pixel-specific PSFs h m , in descending order. The detector number refers to the energy contained. Solid lines: cumulative sums of dashed lines, i.e., total energy harvest of all pixels up to the number on the x axis. The harvests for ISM and helix-helix imaging converge for very large detector areas (see extended graphs in Supplement 1). The energy harvest of a confocal microscope [pinhole diameter 1 Airy unit (AU)] is also marked with a horizontal gray line.

Fig. 5.
Fig. 5.

Imaging of a three-layered fluorescent structure in beam-splitting eISM, designed to scan three z planes in parallel. (a) Three foci excite the layers at the circular intersection regions (yellow). (b) The plane recorded by the camera is the center plane of ( h ex · ρ ) h det .

Fig. 6.
Fig. 6.

Three-plane imaging: simulated properties of the 27 strongest 3D PSFs h m ( NA = 0.92 · RI ).

Fig. 7.
Fig. 7.

Energy harvests for ISM (green plots) and beam-splitting eISM for the imaging of two and three planes, respectively. Dashed lines: energies contained in PSFs h m . Solid lines: cumulative energy collected by all PSFs up to number given on the x axis.

Fig. 8.
Fig. 8.

Three-plane versus helix-helix imaging (NA 1.4) of a COS 7 cell with Alexa647-stained mitochondria. Upper box: confocal (pinhole diam. 0.8 AU), ISM, and wide-field images, Middle box: the three images are obtained in a single scan using beam-splitting phase masks (81 views were jointly deconvolved using 75 iterations). The numbers in the images indicate their z position. Lower box: helix-helix image series of the same cell (114 views jointly deconvolved in 200 iterations).

Fig. 9.
Fig. 9.

Helix-helix images of a 3D distribution of fluorescent microbeads (NA 1.25, wavelengths: ex . / em . = 640 / 660    nm , refractive index of mounting medium = 1.47 ). The two image columns on the left show different x y sections of the helix-helix image data and a sequentially taken ISM stack for comparison. The corresponding z values are stated in the images. The four rectangular images at the right show two axial cross sections (a and b) through both stacks. Their positions in the sample volume are indicated by the yellow dashed lines. The image at the upper right corner shows an exemplary wide-field image of the sample. The color scale bar applies to all images. Both the helix-helix and ISM stacks have been normalized to 255.

Equations (5)

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I WF ( x ) F { F { F { H ex ( k ) } · ρ ( x ) } · H det ( k ) } = [ ( h ex · ρ ) h det ] ( x ) .
I m ( x s , y s ) d x d y P m ( x , y ) { d x ^ d y ^ d z ^ h e x ( x ^ , y ^ , z ^ ) · ρ ( x ^ x s , y ^ y s , z ^ ) h det ( x + x ^ , y + y ^ , z ^ ) } = ( ρ * h m ) ( x s , y s , 0 ) ,
h m ( x ^ , y ^ , z ^ ) = h ex ( x ^ , y ^ , z ^ ) ( P m 2 D h det ) ( x ^ , y ^ , z ^ ) .
E n + 1 ( x ) = E n ( x ) · { 1 M m = 1 M [ ( V m ( x ) E n ( x ) * h m ( x ) + ϵ 1 ) * h m ( x ) ] + 1 } .
h ex I 0 ( x R 0 sin ( 60 ° ) , y R 0 cos ( 60 ° ) + I 0 ( x , y + R 0 , z ) + , z Δ z ) + I 0 ( x + R 0 sin ( 60 ° ) , y R 0 cos ( 60 ° ) , z + Δ z ) h det I 0 ( x R 0 sin ( 60 ° ) , y R 0 cos ( 60 ° ) S y , z Δ z ) + I 0 ( x , y + R 0 , z ) + I 0 ( x + R 0 sin ( 60 ° ) , y R 0 cos ( 60 ° ) + S y , z + Δ z ) .