Abstract

High-content biological microscopy targets high-resolution imaging across large fields-of-view, often achieved by computational imaging approaches. Previously, we demonstrated 2D multimodal high-content microscopy via structured illumination microscopy (SIM) with resolution >2× the diffraction limit, using speckle illumination from Scotch tape. In this work, we extend the method to 3D by leveraging the fact that the speckle illumination is in fact a 3D structured pattern. We use both a coherent and an incoherent imaging model to develop algorithms for joint retrieval of the 3D super-resolved fluorescent and complex-field distributions of the sample. Our reconstructed images resolve features beyond the physical diffraction-limit set by the system’s objective and demonstrate 3D multimodal imaging with 0.6×0.6×6 μm 3 resolution over a volume of 314×500×24 μm 3.

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

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2019 (1)

2018 (4)

2017 (6)

2016 (2)

2015 (7)

A. Orth, M. J. Tomaszewski, R. N. Ghosh, and E. Schonbrun, “Gigapixel multispectral microscopy,” Optica 2, 654–662 (2015).
[Crossref]

L. Tian, Z. Liu, L. Yeh, M. Chen, J. Zhong, and L. Waller, “Computational illumination for high-speed in vitro Fourier ptychographic microscopy,” Optica 2, 904–911 (2015).
[Crossref]

L. Tian and L. Waller, “3D intensity and phase imaging from light field measurements in an LED array microscope,” Optica 2, 104–111 (2015).
[Crossref]

H. Yilmaz, E. G. V. Putten, J. Bertolotti, A. Lagendijk, W. L. Vos, and A. P. Mosk, “Speckle correlation resolution enhancement of wide-field fluorescence imaging,” Optica 2, 424–429 (2015).
[Crossref]

A. Jost, E. Tolstik, P. Feldmann, K. Wicker, A. Sentenac, and R. Heintzmann, “Optical sectioning and high resolution in single-slice structured illumination microscopy by thick slice blind-SIM reconstruction,” PLoS ONE 10, e0132174 (2015).
[Crossref] [PubMed]

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349, aab3500 (2015).
[Crossref]

L.-H. Yeh, J. Dong, J. Zhong, L. Tian, M. Chen, G. Tang, M. Soltanolkotabi, and L. Waller, “Experimental robustness of Fourier ptychography phase retrieval algorithms,” Opt. Express 23, 33213–33238 (2015).
[Crossref]

2014 (6)

2013 (7)

S. Pang, C. Han, J. Erath, A. Rodriguez, and C. Yang, “Wide field-of-view Talbot grid-based microscopy for multicolor fluorescence imaging,” Opt. Express 21, 14555–14565 (2013).
[Crossref] [PubMed]

A. Orth and K. Crozier, “Gigapixel fluorescence microscopy with a water immersion microlens array,” Opt. Express 21, 2361–2368 (2013).
[Crossref] [PubMed]

A. Greenbaum, W. Luo, B. Khademhosseinieh, T.-W. Su, A. F. Coskun, and A. Ozcan, “Increased space-bandwidth product in pixel super-resolved lensfree on-chip microscopy,” Scientific reports 3: 1717 (2013).
[Crossref]

G. Zheng, R. Horstmeyer, and C. Yang, “Wide-field, high-resolution Fourier ptychographic microscopy,” Nat. Photon. 7, 739–745 (2013).
[Crossref]

R. Ayuk, H. Giovannini, A. Jost, E. Mudry, J. Girard, T. Mangeat, N. Sandeau, R. Heintzmann, K. Wicker, K. Belkebir, and A. Sentenac, “Structured illumination fluorescence microscopy with distorted excitations using a filtered blind-SIM algorithm,” Opt. Lett. 38, 4723–4726 (2013).
[Crossref] [PubMed]

J. Min, J. Jang, D. Keum, S.-W. Ryu, C. Choi, K.-H. Jeong, and J. C. Ye, “Fluorescent microscopy beyond diffraction limits using speckle illumination and joint support recovery,” Scientific Reports 3, 2075:1–6 (2013).
[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,” Scientific Reports 3, 1116 (2013).
[Crossref] [PubMed]

2012 (4)

2011 (1)

2010 (1)

2009 (3)

2008 (4)

M. Guizar-Sicairos, S. T. Thurman, and J. R. Fienup, “Efficient subpixel image registration algorithms,” Opt. Lett. 33, 156–158 (2008).
[Crossref] [PubMed]

M. G. L. 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] [PubMed]

M. Debailleul, B. Simon, V. Georges, O. Haeberlé, and V. Lauer, “Holographic microscopy and diffractive microtomography of transparent samples,” Meas. Sci. Technol. 19, 074009 (2008).
[Crossref]

M. H. Kim, Y. Park, D. Seo, Y. J. Lim, D.-I. Kim, C. W. Kim, and W. H. Kim, “Virtual microscopy as a practical alternative to conventional microscopyin pathology education,” Basic Appl. Pathol. 1, 46–48 (2008).
[Crossref]

2007 (2)

V. Laketa, J. C. Simpson, S. Bechtel, S. Wiemann, and R. Pepperkok, “High-content microscopy identifies new neurite outgrowth regulators,” Mol. Biol. Cell 18, 242–252 (2007).
[Crossref]

V. Starkuviene and R. Pepperkok, “The potential of high-content high-throughput microscopy in drug discovery,” Br. J. Pharmacol 152, 62–71 (2007).
[Crossref] [PubMed]

2006 (6)

A. Trounson, “The production and directed differentiation of human embryonic stem cells,” Endocr. Rev. 27(2), 208–219 (2006).
[Crossref] [PubMed]

R. Pepperkok and J. Ellenberg, “High-throughput fluorescence microscopy for systems biology,” Nat. Rev. Mol. Cell Biol. 7, 690–696 (2006).
[Crossref] [PubMed]

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

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nature Methods 3, 793–795 (2006).
[Crossref] [PubMed]

Y. Park, G. Popescu, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Diffraction phase and fluorescence microscopy,” Opt. Express 14, 8263–8268 (2006).
[Crossref] [PubMed]

R. Heintzmann and P. A. Benedetti, “High-resolution image reconstruction in fluorescence microscopy with patterned excitation,” Appl. Opt. 45, 5037–5045 (2006).
[Crossref] [PubMed]

2005 (3)

J. García, Z. Zalevsky, and D. Fixler, “Synthetic aperture superresolution by speckle pattern projection,” Opt. Express 13, 6075–6078 (2005).
[Crossref]

M. G. L. Gustafsson, “Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution,” PNAS 102, 13081–13086 (2005).
[Crossref] [PubMed]

J. C. Yarrow, G. Totsukawa, G. T. Charras, and T. J. Mitchison, “Screening for cell migration inhibitors via automated microscopy reveals a Rho-kinase Inhibitor,” Chem. Biol. 12, 385–395 (2005).
[Crossref] [PubMed]

2004 (3)

B. Mccullough, X. Ying, T. Monticello, and M. Bonnefoi, “Digital microscopy imaging and new approaches in toxicologic pathology,” Toxicol Pathol. 32, 49–58 (2004).
[Crossref] [PubMed]

U. S. Eggert, A. A. Kiger, C. Richter, Z. E. Perlman, N. Perrimon, T. J. Mitchison, and C. M. Field, “Parallel chemical genetic and genome-wide RNAi screens identify cytokinesis inhibitors and targets,” PLoS Biol. 2, e379 (2004).
[Crossref] [PubMed]

S.-H. Jiang and J. G. Walker, “Experimental confirmation of non-scanning fluorescence confocal microscopy using speckle illumination,” Opt. Commun. 238, 1–12 (2004).
[Crossref]

2003 (1)

2002 (1)

V. Lauer, “New approach to optical diffraction tomography yielding a vector equation of diffraction tomography and a novel tomographic microscope,” J. Microscopy 205, 165–176 (2002).
[Crossref]

2001 (2)

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Supplementary Material (2)

NameDescription
» Visualization 1       Through focus visualization for 3D phase reconstruction of HT29 cells
» Visualization 2       Through focus visualization for 3D fluorescence reconstruction of HT29 cells from speckle illumination

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Figures (6)

Fig. 1
Fig. 1 3D multimodal structured illumination microscopy (SIM) with laterally translating Scotch tape as the patterning element. The coherent arm (Sensor-C1 and Sensor-C2) simultaneously captures images with different defocus at the laser illumination wavelength (λex = 532 nm), used for both 3D phase retrieval and speckle trajectory calibration. The incoherent (fluorescence) arm (Sensor-F) captures low-resolution raw fluorescence acquisitions at the emission wavelength (λem = 605 nm) for 3D fluorescence super-resolution reconstruction. OBJ: objective, DM: dichroic mirror, SF: spectral filter, ND-F: neutral-density filter.
Fig. 2
Fig. 2 3D coherent and incoherent transfer function (TF) analysis of the SIM imaging process. The 3D (a) coherent and (b) incoherent TFs of the detection system are auto correlated with the 3D Fourier support of the (c) illumination speckle field and (d)illumination intensity, respectively, resulting in the effective Fourier support of 3D (e) coherent and (f) incoherent SIM. In (e) and (f), we display decomposition of the auto-correlation in two steps: ① tracing the illumination support in one orientation and ② replicating this trace in the azimuthal direction.
Fig. 3
Fig. 3 3D multi-slice model: (a) coherent and (b) incoherent imaging models for the interaction between the sample and the speckle field as light propagates through the sample.
Fig. 4
Fig. 4 3D multimodal (fluorescence and phase) SIM reconstruction compared to widefield fluorescence and coherent intensity images for 700 nm fluorescent microspheres. Resolution beyond the system’s diffraction limit is achieved in both the (a) coherent and (b) fluorescent arms.
Fig. 5
Fig. 5 Reconstructed 3D multimodal (fluorescence and phase) large-FOV for mixed 2 μm, 4μm fluorescent and 3 μm non-fluorescent polystyrene microspheres. Zoom-ins for two ROIs show fluorescence and phase at different depths.
Fig. 6
Fig. 6 Reconstructed 3D multimodal (fluorescence and phase) large-FOV imaging for HT-29 cells (See Visualization 1 and Visualization 2). Zoom-ins for two ROIs show fluorescence and phase at different depths. The blue arrows in two ROIs indicate two-layer cell clusters that come in and out of focus. The orange arrows indicate intracellular components, including higher-phase-contrast lipid vesicles at z = −5.1 μm, nucleolus at z = 0, as well as the cell nucleus and cell-cell membrane contacts.

Tables (3)

Tables Icon

Table 1 Summary of spatial frequency bandwidths

Tables Icon

Algorithm 1 3D coherent imaging reconstruction

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Algorithm 2 3D fluorescence imaging reconstruction

Equations (23)

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f l , 1 ( r ) = C { p c ( r r l ) h Δ s l , λ ex ( r ) } ,
g l , m ( r ) = f l , m ( r ) t m ( r ) , m = 1 , , M , f l , m + 1 ( r ) = g l , m ( r ) h Δ z m , λ ex ( r ) , m = 1 , , M 1.
I c , l z ( r ) = | G l ( r ) h c ( r ) h z , λ ex ( r ) | 2 , l = 1 , , N img , z = z c 1 , z c 2 ,
minimize t 1 , , t M , p c , h c e c ( t 1 , t M , p c , h c ) = l , z e c , l z ( t 1 , , t M , p c , h c ) where e c , l z ( t 1 , , t M , p c , h c ) = r | I c , l z ( r ) | G l ( r ) h c ( r ) h z , λ ex ( r ) | | 2 .
I f , l ( r ) = m = 1 M [ o m ( r ) | f l , m ( r ) | 2 ] | h f , z m , l ( r ) | 2 , l = 1 , , N img ,
minimize o 1 , , o M , p c , h f e f ( o 1 , o M , p c , h f ) = l e f , l ( o 1 , , o M , p c , h f ) where e f , l ( o 1 , , o M , p c , h f ) = r | I f , l ( r ) m = 1 M [ o m ( r ) | f l , m ( r ) | 2 ] | h f , z m , l ( r ) | 2 | 2 ,
Δ s l = ( n 1 ) s , for l = 12 2 ( n 1 ) + 1 , , 12 2 n , where n = 1 , , 9 ,
f l , 1 = H Δ s l , λ ex Q S l p c , g l , m = diag ( f l , m ) t m , m = 1 , , M , f l , m + 1 = H Δ z m , λ ex g l , m , m = 1 , , M 1 , G l = H Δ z M , l , λ ex g l , M ,
H z , λ = F 1 diag ( h ˜ z , λ ) F ,
I c , l z = | H c H z , λ ex G l | 2 , I f , l = m = 1 M K z m , l diag ( | f l , m | 2 ) o m ,
K z m , l = F 1 diag ( F | F 1 diag ( h ˜ z m , l , λ em ) h ˜ f | 2 ) F
e c , l z ( t 1 , , t M , p c , h ˜ c ) = e c , l z T e c , l z = I c , l z | H c H z , λ ex G l | 2 2 , e f , l ( o 1 , , o M , p c , h ˜ f ) = e f , l T e f , l = I f , l m = 1 M K z m , l diag ( | f l , m | 2 ) o m 2 2 ,
t m e c , l z = ( e c , l z g l , m g l , m t m ) = diag ( f l , m ¯ ) ( e c , l z g l , m ) = diag ( f l , m ¯ ) v l , m ,
v l , M = ( e c , l z g l , M ) = H Δ z M , l , λ ex H z , λ ex H c diag ( H c H z , λ e x G l | H c H z , λ e x G l | ) e c , l z v l , m = ( e c , l z g l , m + 1 g l , m + 1 g l , m ) = H Δ z m , λ ex diag ( t m + 1 ¯ ) v l , m + 1 , m = 1 , , M 1 ,
p c e c , l z = ( e c , l z g l , 1 g l , 1 p c ) = S l Q H Δ s l , λ ex diag ( t 1 ¯ ) v l , 1 .
h ˜ c e c , l z = ( e c , l z h ˜ c ) = diag ( F G l ¯ ) diag ( h ˜ z , λ ex ¯ ) F diag ( H c H z , λ ex G l | H c H z , λ ex G l | ) e c , l z
o m e f , l = ( e f , l o m ) = 2 diag ( | f l , m | 2 ) K z m , l e f , l , m = 1 , , M
p c e f , l = m = 1 M ( e f , l f l , m f l , m p c ) = 2 m = 1 M ( f l , m p c ) diag ( f l , m ) diag ( o m ) K z m , l e f , l ,
( f l , m p c ) = ( f l , m g l , m 1 g l , m 1 g l , m 2 t s g l , 2 g l , 1 g l , 1 p c ) = S l Q H Δ s , λ ex [ diag ( t 1 ¯ ) H Δ z 1 , λ ex ] [ diag ( t m 1 ¯ ) H Δ z m 1 , λ ex ] .
h ˜ f e f , l = 2 m = 1 M diag ( h ˜ z m , l , λ em ¯ ) F diag ( F 1 diag ( h ˜ z m , l , λ em ) h ˜ f ) F 1 diag ( F diag ( | f l , m | 2 ) o m ¯ ) F e f , l
p c initial ( r ) = l = 1 N img I c , l , z = 0 ( r + r l ) / N img .
o m initial ( r ) = n = 1 9 ( I f , l ( r ) I f , l ( r ) l ( n ) ) ( | f m , l ( r ) | 2 | f m , l ( r ) | 2   l ( n ) ) l ( n ) ,
Δ | f m , l ( r ) | 2 Δ I f , l ( r ) l ( n ) = m = 1 M o m ( r ) Δ | f m , l ( r ) | 2 Δ | f m , l ( r ) | 2   l ( n ) h f , z m , l ( r r ) d r m = 1 M o m ( r ) Δ | f m , l ( r ) | 2   l ( n ) 2 δ m , m δ ( r r ) h f , z m , l ( r r ) d r Δ | f m , l ( r ) | 2   l ( n ) 2 o m ( r ) ,

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