Abstract

Wide-field fluorescent microscopy (WFFM) is widely employed in biomedical studies, due to its inherent advantages in high-speed imaging of biological dynamics noninvasively and specifically. However, WFFM suffers from the loss of axial resolution and the poor resistance to light scattering in deep tissue imaging. Here we propose a novel WFFM which has the capability in optical sectioning and volumetric imaging. We perform speckle illumination with a digital-micromirror-device for optical sectioning and employ an electrically tunable lens for defocusing modulation so as to quickly switch the image planes. We demonstrate its applications in multi-plane, wide-field imaging of biological dynamics in both zebrafish brains and mouse brains in vivo.

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

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References

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    [Crossref]
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2019 (1)

J. Fan, J. Suo, J. Wu, H. Xie, Y. Shen, F. Chen, G. Wang, L. Cao, G. Jin, Q. He, T. Li, G. Luan, L. Kong, Z. Zheng, and Q. Dai, “Video-rate imaging of biological dynamics at centimetre scale and micrometre resolution,” Nat. Photonics 13, 809–816 (2019).
[Crossref]

2018 (3)

P. Zhou, S. L. Resendez, J. Rodriguez-Romaguera, J. C. Jimenez, S. Q. Neufeld, A. Giovannucci, J. Friedrich, E. A. Pnevmatikakis, G. D. Stuber, R. Hen, M. A. Kheirbek, B. L. Sabatini, R. E. Kass, and L. Paninski, “Efficient and accurate extraction of in vivo calcium signals from microendoscopic video data,” eLife 7, e28728 (2018).
[Crossref]

E. Yoshida, S.-I. Terada, Y. H. Tanaka, K. Kobayashi, M. Ohkura, J. Nakai, and M. Matsuzaki, “In vivo wide-field calcium imaging of mouse thalamocortical synapses with an 8 K ultra-high-definition camera,” Sci. Rep. 8(1), 8324 (2018).
[Crossref]

W. Yang, L. Carrillo-Reid, Y. Bando, D. S. Peterka, and R. Yuste, “Simultaneous two-photon imaging and two-photon optogenetics of cortical circuits in three dimensions,” eLife 7, e32671 (2018).
[Crossref]

2017 (2)

J. H. Park, L. Kong, Y. Zhou, and M. Cui, “Large-field-of-view imaging by multi-pupil adaptive optics,” Nat. Methods 14(6), 581–583 (2017).
[Crossref]

D. H. Kim, J. Kim, J. C. Marques, A. Grama, D. G. C. Hildebrand, W. Gu, J. M. Li, and D. N. Robson, “Pan-neuronal calcium imaging with cellular resolution in freely swimming zebrafish,” Nat. Methods 14(11), 1107–1114 (2017).
[Crossref]

2015 (2)

M. A. Lauterbach, E. Ronzitti, J. R. Sternberg, C. Wyart, and V. Emiliani, “Fast Calcium Imaging with Optical Sectioning via HiLo Microscopy,” PLoS One 10(12), e0143681 (2015).
[Crossref]

T. Hinsdale, B. H. Malik, C. Olsovsky, J. A. Jo, and K. C. Maitland, “Volumetric structured illumination microscopy enabled by a tunable-focus lens,” Opt. Lett. 40(21), 4943–4946 (2015).
[Crossref]

2014 (2)

D. Dan, B. Yao, and L. J. S. B. Ming, “Structured illumination microscopy for super-resolution and optical sectioning,” Sci. Bull. 59(12), 1291–1307 (2014).
[Crossref]

M. Duocastella, G. Vicidomini, and A. Diaspro, “Simultaneous multiplane confocal microscopy using acoustic tunable lenses,” Opt. Express 22(16), 19293–19301 (2014).
[Crossref]

2013 (1)

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref]

2012 (2)

T. N. Ford, D. Lim, and J. Mertz, “Fast optically sectioned fluorescence HiLo endomicroscopy,” J. Biomed. Opt. 17(2), 021105 (2012).
[Crossref]

A. Florence, G. Sabine, B. Sylvie, R. M. Johannes, V. Jean-Claude, A. Mireille, M. Mathieu, D. Antoine, G. Isabelle, and V. D. S. Boudewijn, “Specific in vivo staining of astrocytes in the whole brain after intravenous injection of sulforhodamine dyes,” PLoS One 7(4), e35169 (2012).
[Crossref]

2011 (4)

B. F. Grewe, F. F. Voigt, M. V. Hoff, and F. Helmchen, “Fast two-layer two-photon imaging of neuronal cell populations using an electrically tunable lens,” Biomed. Opt. Express 2(7), 2035–2046 (2011).
[Crossref]

D. Lim, T. N. Ford, K. K. Chu, and J. Mertz, “Optically sectioned in vivo imaging with speckle illumination HiLo microscopy,” J. Biomed. Opt. 16(1), 016014 (2011).
[Crossref]

J. Mertz, “Optical sectioning microscopy with planar or structured illumination,” Nat. Methods 8(10), 811–819 (2011).
[Crossref]

P. A. Santi, “Light Sheet Fluorescence Microscopy: A Review,” J. Histochem. Cytochem. 59(2), 129–138 (2011).
[Crossref]

2009 (1)

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[Crossref]

2008 (1)

2006 (1)

S. A. Khan and N. A. Riza, “Demonstration of a no-moving-parts axial scanning confocal microscope using liquid crystal optics,” Opt. Commun. 265(2), 461–467 (2006).
[Crossref]

2003 (2)

D. Dudley, W. M. Duncan, and J. Slaughter, “Emerging digital micromirror device (DMD) applications,” Proc. SPIE 4985, 14 (2003).
[Crossref]

M. Böhmer and J. Enderlein, “Orientation imaging of single molecules by wide-field epifluorescence microscopy,” J. Opt. Soc. Am. B 20(3), 554–559 (2003).
[Crossref]

2002 (1)

J. R. Swedlow and M. Platani, “Live Cell Imaging Using Wide-Field Microscopy and Deconvolution,” Cell Struct. Funct. 27(5), 335–341 (2002).
[Crossref]

2000 (3)

J. T. Frohn, H. F. Knapp, and A. Stemmer, “True optical resolution beyond the Rayleigh limit achieved by standing wave illumination,” Proc. Natl. Acad. Sci. U. S. A. 97(13), 7232–7236 (2000).
[Crossref]

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

M. A. Neil, A. Squire, R. Juskaitis, P. I. Bastiaens, and T. Wilson, “Wide-field optically sectioning fluorescence microscopy with laser illumination,” J. Microsc. 197(1), 1–4 (2000).
[Crossref]

1998 (2)

M. A. A. Neil, R. Juškaitis, and T. Wilson, “Real time 3D fluorescence microscopy by two beam interference illumination,” Opt. Commun. 153(1–3), 1–4 (1998).
[Crossref]

Verveer, Hanley, Verbeek, van Vliet, and Jovin, “Theory of confocal fluorescence imaging in the programmable array microscope (PAM),” J. Microsc. 189(3), 192–198 (1998).
[Crossref]

1997 (2)

M. A. A. Neil, R. Juškaitis, and T. Wilson, “Method of obtaining optical sectioning by using structured light in a conventional microscope,” Opt. Lett. 22(24), 1905–1907 (1997).
[Crossref]

D. W. Zaidel, M. M. Esiri, and P. J. Harrison, “Size, shape, and orientation of neurons in the left and right hippocampus: investigation of normal asymmetries and alterations in schizophrenia,” Am. J. Psychiatry 154(6), 812–818 (1997).
[Crossref]

1981 (1)

H. R. Maricq, “Wide-field capillary microscopy,” Arthritis Rheum. 24(9), 1159–1165 (1981).
[Crossref]

1969 (1)

P. Stokseth, “Properties of a defocused optical system,” J. Opt. 59(10), 1314–1321 (1969).
[Crossref]

Antoine, D.

A. Florence, G. Sabine, B. Sylvie, R. M. Johannes, V. Jean-Claude, A. Mireille, M. Mathieu, D. Antoine, G. Isabelle, and V. D. S. Boudewijn, “Specific in vivo staining of astrocytes in the whole brain after intravenous injection of sulforhodamine dyes,” PLoS One 7(4), e35169 (2012).
[Crossref]

Bando, Y.

W. Yang, L. Carrillo-Reid, Y. Bando, D. S. Peterka, and R. Yuste, “Simultaneous two-photon imaging and two-photon optogenetics of cortical circuits in three dimensions,” eLife 7, e32671 (2018).
[Crossref]

Bartoo, A. C.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[Crossref]

Bastiaens, P. I.

M. A. Neil, A. Squire, R. Juskaitis, P. I. Bastiaens, and T. Wilson, “Wide-field optically sectioning fluorescence microscopy with laser illumination,” J. Microsc. 197(1), 1–4 (2000).
[Crossref]

Böhmer, M.

Boudewijn, V. D. S.

A. Florence, G. Sabine, B. Sylvie, R. M. Johannes, V. Jean-Claude, A. Mireille, M. Mathieu, D. Antoine, G. Isabelle, and V. D. S. Boudewijn, “Specific in vivo staining of astrocytes in the whole brain after intravenous injection of sulforhodamine dyes,” PLoS One 7(4), e35169 (2012).
[Crossref]

Bozinovic, N.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[Crossref]

N. Bozinovic, C. Ventalon, T. Ford, and J. Mertz, “Fluorescence endomicroscopy with structured illumination,” Opt. Express 16(11), 8016–8025 (2008).
[Crossref]

Cao, L.

J. Fan, J. Suo, J. Wu, H. Xie, Y. Shen, F. Chen, G. Wang, L. Cao, G. Jin, Q. He, T. Li, G. Luan, L. Kong, Z. Zheng, and Q. Dai, “Video-rate imaging of biological dynamics at centimetre scale and micrometre resolution,” Nat. Photonics 13, 809–816 (2019).
[Crossref]

Carrillo-Reid, L.

W. Yang, L. Carrillo-Reid, Y. Bando, D. S. Peterka, and R. Yuste, “Simultaneous two-photon imaging and two-photon optogenetics of cortical circuits in three dimensions,” eLife 7, e32671 (2018).
[Crossref]

Chen, F.

J. Fan, J. Suo, J. Wu, H. Xie, Y. Shen, F. Chen, G. Wang, L. Cao, G. Jin, Q. He, T. Li, G. Luan, L. Kong, Z. Zheng, and Q. Dai, “Video-rate imaging of biological dynamics at centimetre scale and micrometre resolution,” Nat. Photonics 13, 809–816 (2019).
[Crossref]

Chu, K. K.

D. Lim, T. N. Ford, K. K. Chu, and J. Mertz, “Optically sectioned in vivo imaging with speckle illumination HiLo microscopy,” J. Biomed. Opt. 16(1), 016014 (2011).
[Crossref]

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[Crossref]

Cui, M.

J. H. Park, L. Kong, Y. Zhou, and M. Cui, “Large-field-of-view imaging by multi-pupil adaptive optics,” Nat. Methods 14(6), 581–583 (2017).
[Crossref]

Dai, Q.

J. Fan, J. Suo, J. Wu, H. Xie, Y. Shen, F. Chen, G. Wang, L. Cao, G. Jin, Q. He, T. Li, G. Luan, L. Kong, Z. Zheng, and Q. Dai, “Video-rate imaging of biological dynamics at centimetre scale and micrometre resolution,” Nat. Photonics 13, 809–816 (2019).
[Crossref]

Dan, D.

D. Dan, B. Yao, and L. J. S. B. Ming, “Structured illumination microscopy for super-resolution and optical sectioning,” Sci. Bull. 59(12), 1291–1307 (2014).
[Crossref]

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref]

Diaspro, A.

Dudley, D.

D. Dudley, W. M. Duncan, and J. Slaughter, “Emerging digital micromirror device (DMD) applications,” Proc. SPIE 4985, 14 (2003).
[Crossref]

Duncan, W. M.

D. Dudley, W. M. Duncan, and J. Slaughter, “Emerging digital micromirror device (DMD) applications,” Proc. SPIE 4985, 14 (2003).
[Crossref]

Duocastella, M.

Emiliani, V.

M. A. Lauterbach, E. Ronzitti, J. R. Sternberg, C. Wyart, and V. Emiliani, “Fast Calcium Imaging with Optical Sectioning via HiLo Microscopy,” PLoS One 10(12), e0143681 (2015).
[Crossref]

Enderlein, J.

Esiri, M. M.

D. W. Zaidel, M. M. Esiri, and P. J. Harrison, “Size, shape, and orientation of neurons in the left and right hippocampus: investigation of normal asymmetries and alterations in schizophrenia,” Am. J. Psychiatry 154(6), 812–818 (1997).
[Crossref]

Fan, J.

J. Fan, J. Suo, J. Wu, H. Xie, Y. Shen, F. Chen, G. Wang, L. Cao, G. Jin, Q. He, T. Li, G. Luan, L. Kong, Z. Zheng, and Q. Dai, “Video-rate imaging of biological dynamics at centimetre scale and micrometre resolution,” Nat. Photonics 13, 809–816 (2019).
[Crossref]

Florence, A.

A. Florence, G. Sabine, B. Sylvie, R. M. Johannes, V. Jean-Claude, A. Mireille, M. Mathieu, D. Antoine, G. Isabelle, and V. D. S. Boudewijn, “Specific in vivo staining of astrocytes in the whole brain after intravenous injection of sulforhodamine dyes,” PLoS One 7(4), e35169 (2012).
[Crossref]

Ford, T.

Ford, T. N.

T. N. Ford, D. Lim, and J. Mertz, “Fast optically sectioned fluorescence HiLo endomicroscopy,” J. Biomed. Opt. 17(2), 021105 (2012).
[Crossref]

D. Lim, T. N. Ford, K. K. Chu, and J. Mertz, “Optically sectioned in vivo imaging with speckle illumination HiLo microscopy,” J. Biomed. Opt. 16(1), 016014 (2011).
[Crossref]

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J. Biomed. Opt. 14(3), 030502 (2009).
[Crossref]

Friedrich, J.

P. Zhou, S. L. Resendez, J. Rodriguez-Romaguera, J. C. Jimenez, S. Q. Neufeld, A. Giovannucci, J. Friedrich, E. A. Pnevmatikakis, G. D. Stuber, R. Hen, M. A. Kheirbek, B. L. Sabatini, R. E. Kass, and L. Paninski, “Efficient and accurate extraction of in vivo calcium signals from microendoscopic video data,” eLife 7, e28728 (2018).
[Crossref]

Frohn, J. T.

J. T. Frohn, H. F. Knapp, and A. Stemmer, “True optical resolution beyond the Rayleigh limit achieved by standing wave illumination,” Proc. Natl. Acad. Sci. U. S. A. 97(13), 7232–7236 (2000).
[Crossref]

Gao, P.

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref]

Giovannucci, A.

P. Zhou, S. L. Resendez, J. Rodriguez-Romaguera, J. C. Jimenez, S. Q. Neufeld, A. Giovannucci, J. Friedrich, E. A. Pnevmatikakis, G. D. Stuber, R. Hen, M. A. Kheirbek, B. L. Sabatini, R. E. Kass, and L. Paninski, “Efficient and accurate extraction of in vivo calcium signals from microendoscopic video data,” eLife 7, e28728 (2018).
[Crossref]

Grama, A.

D. H. Kim, J. Kim, J. C. Marques, A. Grama, D. G. C. Hildebrand, W. Gu, J. M. Li, and D. N. Robson, “Pan-neuronal calcium imaging with cellular resolution in freely swimming zebrafish,” Nat. Methods 14(11), 1107–1114 (2017).
[Crossref]

Grewe, B. F.

Gu, W.

D. H. Kim, J. Kim, J. C. Marques, A. Grama, D. G. C. Hildebrand, W. Gu, J. M. Li, and D. N. Robson, “Pan-neuronal calcium imaging with cellular resolution in freely swimming zebrafish,” Nat. Methods 14(11), 1107–1114 (2017).
[Crossref]

Gustafsson, M. G.

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

Hanley,

Verveer, Hanley, Verbeek, van Vliet, and Jovin, “Theory of confocal fluorescence imaging in the programmable array microscope (PAM),” J. Microsc. 189(3), 192–198 (1998).
[Crossref]

Harrison, P. J.

D. W. Zaidel, M. M. Esiri, and P. J. Harrison, “Size, shape, and orientation of neurons in the left and right hippocampus: investigation of normal asymmetries and alterations in schizophrenia,” Am. J. Psychiatry 154(6), 812–818 (1997).
[Crossref]

He, Q.

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Supplementary Material (2)

NameDescription
» Visualization 1       Dual-plane imaging of vascular dilations in mouse cerebral cortex in vivo
» Visualization 2       Three-plane calcium imaging of Zebrafish brain in vivo

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Figures (6)

Fig. 1.
Fig. 1. Optical setup and the calibration results. (a) Experimental setup. The light from a light-emitting-diode (LED) is delivered to the digital-micromirror-device (DMD) with a total internal reflection prism (TIR). The binary pattern on the DMD is projected onto the sample plane through two sets of relay lenses, one consists of L1 (f = 100 mm) and L2 (f = 300 mm); the other one consists of L3 (f = 180 mm) and “electrically tunable lens (ETL)-objective (OBJ)” set. Fluorescence signals from the specimen is collected by the objective, reflected by the dichroic mirror (DM), and imaged onto the sCMOS camera by L4 (f = 100 mm). (b) Lateral point-spread function (PSF) determined with 0.5 µm fluorescent beads. The measured FWHM is 1.49 µm. (c) Axial PSF determined with a fluorescent sheet. The measured FWHM is 6.4 µm. (d) Field-of-view measured from a specific test target: 1.56 mm × 1.83 mm. (e) The relative field-of-view change versus the applied current.
Fig. 2.
Fig. 2. The calibration of axial positions at specific currents of ETL and the signal synchronization for image acquisition. (a) The axial displacement versus applied current of the ETL. The blue arrow indicates the direction of rising current (from 0 to 292 mA), and the yellow arrow indicates the direction of decreasing current (from 292 to 0 mA). (b) The signal synchronization for image acquisition.
Fig. 3.
Fig. 3. Dual-plane imaging of vascular dilations in mouse cerebral cortex in vivo. (a, b) Uniformly-illuminated image and optical-sectioning image of the top plane, respectively. (c, d) Uniformly-illuminated image and optical-sectioning image of the bottom plane (45 µm deeper), respectively. The insert shows the detail spatial morphology of blood vessels. (e) Dilations relative to the average diameters of blood vessels at the top and bottom planes (see also Visualization 1).
Fig. 4.
Fig. 4. Three-plane calcium imaging of zebrafish brain in vivo. (a, c, and e) Uniformly-illuminated images of the top, middle, and bottom planes, respectively. (b, d, and f) Optical-sectioning images of the corresponding planes as in a, c, and e. The inserts in (a) and (b) show the ROI in the top plane for further discussion in Fig. 5. The axial scanning range is 105 µm, with the interval between each plane being 52.5 µm (see also Visualization 2).
Fig. 5.
Fig. 5. Calcium tracing of neurons recorded in the uniformly-illuminated and optical-sectioning modes, at the top plane. (a) Fluorescent intensity dynamics in both modes, with the ROIs labeled in the inserts of Fig. 4 (a) and (b). The calcium tracing intensities of uniformly-illuminated mode are enlarged by a factor of 5. Arrows indicate the artifacts introduced by background fluorescence in the uniformly-illuminated mode. (b, c) The histogram of the $\Delta F/F$ in the uniformly-illuminated and HiLo modes, respectively, at the top plane.
Fig. 6.
Fig. 6. Calcium tracing of single neurons from HiLo images. (a-c) Estimated neuron contours at the top, middle, and bottom planes of the optical-sectioning images. (d-f) Calcium traces of single neurons at the top, middle, and bottom planes. (g) The histogram of the correlation coefficients. (h) Calcium signals from 40 example neurons at each plane.

Equations (8)

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I H i ( ρ ) = H P [ I u ( ρ ) ]
C s ( ρ ) = σ [ I s ( ρ ) ]
I d ( ρ ) = I u ( ρ ) I s ( ρ )
C ( ρ ) = σ [ I d ( ρ ) ]
B P ( k ) = exp ( | k 2 | 2 σ s 2 ) exp ( | k 2 | σ s 2 )
I L o ( ρ ) = L P [ C ( ρ ) I u ( ρ ) ]
I H i L o ( ρ ) = I H i ( ρ ) + η I L o ( ρ )
F W H M axial = 0.54 K S × N A