Abstract

Multifocal plane microscopy allows for capturing images at different focal planes simultaneously. Using a proprietary prism which splits the emitted light into paths of different lengths, images at 8 different focal depths were obtained, covering a volume of 50x50x4 µm3. The position of single emitters was retrieved using a phasor-based approach across the different imaging planes, with better than 10 nm precision in the axial direction. We validated the accuracy of this approach by tracking fluorescent beads in 3D to calculate water viscosity. The fast acquisition rate (>100 fps) also enabled us to follow the capturing of 0.2 µm fluorescent beads into an optical trap.

© 2020 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2020 (3)

Y. Chen, S. Zhu, W. Kan, F. Chen, L. Zhang, B. Ding, and Z. Shen, “Rapid determination of fluorescent molecular orientation in leakage radiation microscopy,” Results Phys. 16, 102938 (2020).
[Crossref]

A. Huang, D. Chen, H. Li, D. Tang, B. Yu, J. Li, and J. Qu, “Three-dimensional tracking of multiple particles in large depth of field using dual-objective bifocal plane imaging,” Chin. Opt. Lett. 18(7), 071701 (2020).
[Crossref]

E. Nehme, D. Freedman, R. Gordon, B. Ferdman, L. E. Weiss, O. Alalouf, T. Naor, R. Orange, T. Michaeli, and Y. Shechtman, “DeepSTORM3D: dense 3D localization microscopy and PSF design by deep learning,” Nat. Methods 17(7), 734–740 (2020).
[Crossref]

2019 (3)

X. Wang, H. Yi, I. Gdor, M. Hereld, and N. F. Scherer, “Nanoscale Resolution 3D Snapshot Particle Tracking by Multifocal Microscopy,” Nano Lett. 19(10), 6781–6787 (2019).
[Crossref]

Y. Li, Y.-L. Wu, P. Hoess, M. Mund, and J. Ries, “Depth-dependent PSF calibration and aberration correction for 3D single-molecule localization,” Biomed. Opt. Express 10(6), 2708 (2019).
[Crossref]

C.-H. Lu, W.-C. Tang, Y.-T. Liu, S.-W. Chang, F. C. M. Wu, C.-Y. Chen, Y.-C. Tsai, S.-M. Yang, C.-W. Kuo, Y. Okada, Y.-K. Hwu, P. Chen, and B.-C. Chen, “Lightsheet localization microscopy enables fast, large-scale, and three-dimensional super-resolution imaging,” Commun. Biol. 2(1), 177 (2019).
[Crossref]

2018 (6)

G. Vicidomini, P. Bianchini, and A. Diaspro, “STED super-resolved microscopy,” Nat. Methods 15(3), 173–182 (2018).
[Crossref]

G. Eelen, C. Dubois, A. R. Cantelmo, J. Goveia, U. Brüning, M. DeRan, G. Jarugumilli, J. van Rijssel, G. Saladino, F. Comitani, A. Zecchin, S. Rocha, R. Chen, H. Huang, S. Vandekeere, J. Kalucka, C. Lange, F. Morales-Rodriguez, B. Cruys, L. Treps, L. Ramer, S. Vinckier, K. Brepoels, S. Wyns, J. Souffreau, L. Schoonjans, W. H. Lamers, Y. Wu, J. Haustraete, J. Hofkens, S. Liekens, R. Cubbon, B. Ghesquiére, M. Dewerchin, F. L. Gervasio, X. Li, J. D. van Buul, X. Wu, and P. Carmeliet, “Role of glutamine synthetase in angiogenesis beyond glutamine synthesis,” Nature 561(7721), 63–69 (2018).
[Crossref]

A. Descloux, K. S. Grußmayer, E. Bostan, T. Lukes, A. Bouwens, A. Sharipov, S. Geissbuehler, A.-L. Mahul-Mellier, H. A. Lashuel, M. Leutenegger, and T. Lasser, “Combined multi-plane phase retrieval and super-resolution optical fluctuation imaging for 4D cell microscopy,” Nat. Photonics 12(3), 165–172 (2018).
[Crossref]

K. J. A. Martens, A. N. Bader, S. Baas, B. Rieger, and J. Hohlbein, “Phasor based single-molecule localization microscopy in 3D (pSMLM-3D): An algorithm for MHz localization rates using standard CPUs,” The J. Chem. Phys. 148(12), 123311 (2018).
[Crossref]

W. Liu, K. C. Toussaint, C. Okoro, D. Zhu, Y. Chen, C. Kuang, and X. Liu, “Breaking the Axial Diffraction Limit: A Guide to Axial Super-Resolution Fluorescence Microscopy,” Laser Photonics Rev. 12(8), 1700333 (2018).
[Crossref]

T. Kudo, S.-J. Yang, and H. Masuhara, “A Single Large Assembly with Dynamically Fluctuating Swarms of Gold Nanoparticles Formed by Trapping Laser,” Nano Lett. 18(9), 5846–5853 (2018).
[Crossref]

2017 (6)

G. Sancataldo, L. Scipioni, T. Ravasenga, L. Lanzanó, A. Diaspro, A. Barberis, and M. Duocastella, “Three-dimensional multiple-particle tracking with nanometric precision over tunable axial ranges,” Optica 4(3), 367 (2017).
[Crossref]

F. C. Hendriks, F. Meirer, A. V. Kubarev, Z. Ristanović, M. B. J. Roeffaers, E. T. C. Vogt, P. C. A. Bruijnincx, and B. M. Weckhuysen, “Single-Molecule Fluorescence Microscopy Reveals Local Diffusion Coefficients in the Pore Network of an Individual Catalyst Particle,” J. Am. Chem. Soc. 139(39), 13632–13635 (2017).
[Crossref]

S. Abrahamsson, H. Blom, A. Agostinho, D. C. Jans, A. Jost, M. Müller, L. Nilsson, K. Bernhem, T. J. Lambert, R. Heintzmann, and H. Brismar, “Multifocus structured illumination microscopy for fast volumetric super-resolution imaging,” Biomed. Opt. Express 8(9), 4135 (2017).
[Crossref]

P. R. Nicovich, D. M. Owen, and K. Gaus, “Turning single-molecule localization microscopy into a quantitative bioanalytical tool,” Nat. Protoc. 12(3), 453–460 (2017).
[Crossref]

D. Wöll and C. Flors, “Super-resolution Fluorescence Imaging for Materials Science,” Small Methods 1(10), 1700191 (2017).
[Crossref]

S. Shashkova and M. Leake, “Single-molecule fluorescence microscopy review: shedding new light on old problems,” Biosci. Rep. 37(4), BSR20170031 (2017).
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2016 (3)

2015 (5)

S. Abrahamsson, M. McQuilken, S. B. Mehta, A. Verma, J. Larsch, R. Ilic, R. Heintzmann, C. I. Bargmann, A. S. Gladfelter, and R. Oldenbourg, “MultiFocus Polarization Microscope (MF-PolScope) for 3D polarization imaging of up to 25 focal planes simultaneously,” Opt. Express 23(6), 7734 (2015).
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Y. Shechtman, L. E. Weiss, A. S. Backer, S. J. Sahl, and W. E. Moerner, “Precise Three-Dimensional Scan-Free Multiple-Particle Tracking over Large Axial Ranges with Tetrapod Point Spread Functions,” Nano Lett. 15(6), 4194–4199 (2015).
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W. E. Moerner, Y. Shechtman, and Q. Wang, “Single-molecule spectroscopy and imaging over the decades,” Faraday Discuss. 184, 9–36 (2015).
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J. Tam and D. Merino, “Stochastic optical reconstruction microscopy (STORM) in comparison with stimulated emission depletion (STED) and other imaging methods,” J. Neurochem. 135(4), 643–658 (2015).
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L. Gardini, M. Capitanio, and F. S. Pavone, “3D tracking of single nanoparticles and quantum dots in living cells by out-of-focus imaging with diffraction pattern recognition,” Sci. Rep. 5(1), 16088 (2015).
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2014 (6)

Y. Tian, M. V. Kuzimenkova, M. Xie, M. Meyer, P.-O. Larsson, and I. G. Scheblykin, “Watching two conjugated polymer chains breaking each other when colliding in solution,” NPG Asia Mater 6(10), e134 (2014).
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K. Notelaers, S. Rocha, R. Paesen, N. Smisdom, B. De Clercq, J. C. Meier, J.-M. Rigo, J. Hofkens, and M. Ameloot, “Analysis of α3 GlyR single particle tracking in the cell membrane,” Biochim. Biophys. Acta, Biomembr. 1843(3), 544–553 (2014).
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S. Geissbuehler, A. Sharipov, A. Godinat, N. L. Bocchio, P. A. Sandoz, A. Huss, N. A. Jensen, S. Jakobs, J. Enderlein, F. Gisou van der Goot, E. A. Dubikovskaya, T. Lasser, and M. Leutenegger, “Live-cell multiplane three-dimensional super-resolution optical fluctuation imaging,” Nat. Commun. 5(1), 5830 (2014).
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B. Hajj, J. Wisniewski, M. El Beheiry, J. Chen, A. Revyakin, C. Wu, and M. Dahan, “Whole-cell, multicolor superresolution imaging using volumetric multifocus microscopy,” Proc. Natl. Acad. Sci. U. S. A. 111(49), 17480–17485 (2014).
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R. McGorty, J. Schnitzbauer, W. Zhang, and B. Huang, “Correction of depth-dependent aberrations in 3D single-molecule localization and super-resolution microscopy,” Opt. Lett. 39(2), 275 (2014).
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A. D. Edelstein, M. A. Tsuchida, N. Amodaj, H. Pinkard, R. D. Vale, and N. Stuurman, “Advanced methods of microscope control using µManager software,” J. Biol. Methods 1(2), 10 (2014).
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2013 (6)

P. H. J. Kouwer, M. Koepf, V. A. A. Le Sage, M. Jaspers, A. M. van Buul, Z. H. Eksteen-Akeroyd, T. Woltinge, E. Schwartz, H. J. Kitto, R. Hoogenboom, S. J. Picken, R. J. M. Nolte, E. Mendes, and A. E. Rowan, “Responsive biomimetic networks from polyisocyanopeptide hydrogels,” Nature 493(7434), 651–655 (2013).
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K.-I. Yuyama, T. Sugiyama, and H. Masuhara, “Laser Trapping and Crystallization Dynamics of l-Phenylalanine at Solution Surface,” J. Phys. Chem. Lett. 4(15), 2436–2440 (2013).
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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(1), 60–63 (2013).
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H. Kirshner, F. Aguet, D. Sage, and M. Unser, “3-D PSF fitting for fluorescence microscopy: implementation and localization application,” J. Microsc. 249(1), 13–25 (2013).
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S.-L. Liu, J. Li, Z.-L. Zhang, Z.-G. Wang, Z.-Q. Tian, G.-P. Wang, and D.-W. Pang, “Fast and High-Accuracy Localization for Three-Dimensional Single-Particle Tracking,” Sci. Rep. 3(1), 2462 (2013).
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T. Cordes and S. A. Blum, “Opportunities and challenges in single-molecule and single-particle fluorescence microscopy for mechanistic studies of chemical reactions,” Nat. Chem. 5(12), 993–999 (2013).
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2012 (3)

S. Ram, D. Kim, R. J. Ober, and E. S. Ward, “3D Single Molecule Tracking with Multifocal Plane Microscopy Reveals Rapid Intercellular Transferrin Transport at Epithelial Cell Barriers,” Biophys. J. 103(7), 1594–1603 (2012).
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K. Notelaers, N. Smisdom, S. Rocha, D. Janssen, J. C. Meier, J.-M. Rigo, J. Hofkens, and M. Ameloot, “Ensemble and single particle fluorimetric techniques in concerted action to study the diffusion and aggregation of the glycine receptor α3 isoforms in the cell plasma membrane,” Biochim. Biophys. Acta, Biomembr. 1818(12), 3131–3140 (2012).
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T. Sugiyama, K.-I. Yuyama, and H. Masuhara, “Laser trapping chemistry: from polymer assembly to amino acid crystallization,” Acc. Chem. Res. 45(11), 1946–1954 (2012).
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2011 (1)

2010 (3)

M. Badieirostami, M. D. Lew, M. A. Thompson, and W. E. Moerner, “Three-dimensional localization precision of the double-helix point spread function versus astigmatism and biplane,” Appl. Phys. Lett. 97(16), 161103 (2010).
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M. A. Thompson, M. D. Lew, M. Badieirostami, and W. E. Moerner, “Localizing and Tracking Single Nanoscale Emitters in Three Dimensions with High Spatiotemporal Resolution Using a Double-Helix Point Spread Function,” Nano Lett. 10(1), 211–218 (2010).
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X. Michalet, “Mean square displacement analysis of single-particle trajectories with localization error: Brownian motion in an isotropic medium,” Phys. Rev. E 82(4), 041914 (2010).
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2009 (5)

S. Ram, P. Prabhat, E. S. Ward, and R. J. Ober, “Improved single particle localization accuracy with dual objective multifocal plane microscopy,” Opt. Express 17(8), 6881 (2009).
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S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U. S. A. 106(9), 2995–2999 (2009).
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S. Rocha, J. A. Hutchison, K. Peneva, A. Herrmann, K. Müllen, M. Skjøt, C. I. Jørgensen, A. Svendsen, F. C. De Schryver, J. Hofkens, and H. Uji-i, “Linking Phospholipase Mobility to Activity by Single-Molecule Wide-Field Microscopy,” ChemPhysChem 10(1), 151–161 (2009).
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D. Wöll, E. Braeken, A. Deres, F. C. De Schryver, H. Uji-i, and J. Hofkens, “Polymers and single molecule fluorescence spectroscopy, what can we learn?” Chem. Soc. Rev. 38(2), 313–328 (2009).
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B. Huang, M. Bates, and X. Zhuang, “Super-resolution fluorescence microscopy,” Annu. Rev. Biochem. 78(1), 993–1016 (2009).
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2008 (7)

D. Wöll, H. Uji-i, T. Schnitzler, J.-I. Hotta, P. Dedecker, A. Herrmann, F. C. De Schryver, K. Müllen, and J. Hofkens, “Radical Polymerization Tracked by Single Molecule Spectroscopy,” Angew. Chem. Int. Ed. 47(4), 783–787 (2008).
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C. M. Brown, R. B. Dalal, B. Hebert, M. A. Digman, A. R. Horwitz, and E. Gratton, “Raster image correlation spectroscopy (RICS) for measuring fast protein dynamics and concentrations with a commercial laser scanning confocal microscope,” J. Microsc. 229(1), 78–91 (2008).
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R. Cerbino and V. Trappe, “Differential Dynamic Microscopy: Probing Wave Vector Dependent Dynamics with a Microscope,” Phys. Rev. Lett. 100(18), 188102 (2008).
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B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
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M. F. Juette, T. J. Gould, M. D. Lessard, M. J. Mlodzianoski, B. S. Nagpure, B. T. Bennett, S. T. Hess, and J. Bewersdorf, “Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples,” Nat. Methods 5(6), 527–529 (2008).
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S. Ram, P. Prabhat, J. Chao, E. S. Ward, and R. J. Ober, “High accuracy 3D quantum dot tracking with multifocal plane microscopy for the study of fast intracellular dynamics in live cells,” Biophys. J. 95(12), 6025–6043 (2008).
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A. Sergé, N. Bertaux, H. Rigneault, and D. Marguet, “Dynamic multiple-target tracing to probe spatiotemporal cartography of cell membranes,” Nat. Methods 5(8), 687–694 (2008).
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2007 (2)

P. Prabhat, Z. Gan, J. Chao, S. Ram, C. Vaccaro, S. Gibbons, R. J. Ober, and E. S. Ward, “Elucidation of intracellular recycling pathways leading to exocytosis of the Fc receptor, FcRn, by using multifocal plane microscopy,” Proc. Natl. Acad. Sci. 104(14), 5889–5894 (2007).
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E. Toprak, H. Balci, B. H. Blehm, and P. R. Selvin, “Three-Dimensional Particle Tracking via Bifocal Imaging,” Nano Lett. 7(7), 2043–2045 (2007).
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2005 (1)

M. A. Digman, C. M. Brown, P. Sengupta, P. W. Wiseman, A. R. Horwitz, and E. Gratton, “Measuring Fast Dynamics in Solutions and Cells with a Laser Scanning Microscope,” Biophys. J. 89(2), 1317–1327 (2005).
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2000 (2)

A. J. Levine and T. C. Lubensky, “One- and Two-Particle Microrheology,” Phys. Rev. Lett. 85(8), 1774–1777 (2000).
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J. C. Crocker, M. T. Valentine, E. R. Weeks, T. Gisler, P. D. Kaplan, A. G. Yodh, and D. A. Weitz, “Two-Point Microrheology of Inhomogeneous Soft Materials,” Phys. Rev. Lett. 85(4), 888–891 (2000).
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1997 (2)

A. Ashkin, “Optical trapping and manipulation of neutral particles using lasers,” Proc. Natl. Acad. Sci. 94(10), 4853–4860 (1997).
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1996 (1)

J. C. Crocker and D. G. Grier, “Methods of Digital Video Microscopy for Colloidal Studies,” J. Colloid Interface Sci. 179(1), 298–310 (1996).
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1993 (1)

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1992 (1)

A. Ashkin, “Forces of a single-beam gradient laser trap on a dielectric sphere in the ray optics regime,” Biophys. J. 61(2), 569–582 (1992).
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1987 (1)

A. Ashkin, J. M. Dziedzic, and T. Yamane, “Optical trapping and manipulation of single cells using infrared laser beams,” Nature 330(6150), 769–771 (1987).
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1986 (1)

1976 (1)

D. Axelrod, D. Koppel, J. Schlessinger, E. Elson, and W. Webb, “Mobility measurement by analysis of fluorescence photobleaching recovery kinetics,” Biophys. J. 16(9), 1055–1069 (1976).
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1972 (1)

D. Magde, E. Elson, and W. W. Webb, “Thermodynamic Fluctuations in a Reacting System–Measurement by Fluorescence Correlation Spectroscopy,” Phys. Rev. Lett. 29(11), 705–708 (1972).
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1971 (1)

H. C. Berg, “How to Track Bacteria,” Rev. Sci. Instrum. 42(6), 868–871 (1971).
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1969 (1)

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1957 (1)

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1905 (1)

A. Einstein, “über die von der molekularkinetischen Theorie der Wärme geforderte Bewegung von in ruhenden Flüssigkeiten suspendierten Teilchen,” Ann. Phys. 322(8), 549–560 (1905).
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H. Kirshner, F. Aguet, D. Sage, and M. Unser, “3-D PSF fitting for fluorescence microscopy: implementation and localization application,” J. Microsc. 249(1), 13–25 (2013).
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E. Nehme, D. Freedman, R. Gordon, B. Ferdman, L. E. Weiss, O. Alalouf, T. Naor, R. Orange, T. Michaeli, and Y. Shechtman, “DeepSTORM3D: dense 3D localization microscopy and PSF design by deep learning,” Nat. Methods 17(7), 734–740 (2020).
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Ameloot, M.

K. Notelaers, S. Rocha, R. Paesen, N. Smisdom, B. De Clercq, J. C. Meier, J.-M. Rigo, J. Hofkens, and M. Ameloot, “Analysis of α3 GlyR single particle tracking in the cell membrane,” Biochim. Biophys. Acta, Biomembr. 1843(3), 544–553 (2014).
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K. Notelaers, N. Smisdom, S. Rocha, D. Janssen, J. C. Meier, J.-M. Rigo, J. Hofkens, and M. Ameloot, “Ensemble and single particle fluorimetric techniques in concerted action to study the diffusion and aggregation of the glycine receptor α3 isoforms in the cell plasma membrane,” Biochim. Biophys. Acta, Biomembr. 1818(12), 3131–3140 (2012).
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A. D. Edelstein, M. A. Tsuchida, N. Amodaj, H. Pinkard, R. D. Vale, and N. Stuurman, “Advanced methods of microscope control using µManager software,” J. Biol. Methods 1(2), 10 (2014).
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H. C. Berg, “How to Track Bacteria,” Rev. Sci. Instrum. 42(6), 868–871 (1971).
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Supplementary Material (1)

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Figures (6)

Fig. 1.
Fig. 1. Schematic of the multiplane wide-field microscope. The trapping laser, the cylindrical lens, and the proprietary prism are the three main components that differ from conventional wide-field microscopes. The inserted diagram shows the extended, interleaved, and equal camera configurations which can be obtained by modifying the relative alignment of the two cameras. $\delta z$ is the focal distance between two consecutive planes of one camera, d is the lateral distance between two consecutive images on the camera and is determined by the prism geometry, n is the refractive index of the prism and ML is the in-plane magnification. At the bottom: images of 2 beads in the 8 planes acquired simultaneously using the extended configuration showing how the multiplane setup allows for simultaneous 3D imaging.
Fig. 2.
Fig. 2. Plane calibration: A and B shows one of the image planes for two different z-slices in focus (A) and out of focus (B). C and D shows the image intensity gradient corresponding to A and B, respectively. The maximum of the image intensity gradient obtained (C, D) is then plotted in E as a function of z position. E shows the maximum image intensity gradient as a function of z (dots) for all image planes. The solid line indicates the Gaussian function fit which we used to determine the position of the plane and calculate the distance between them.
Fig. 3.
Fig. 3. A) Tracking traces of individual particles for unidirectional motor-induced motion. The shadow on the plot shows $\pm$3 times the mean standard deviation representing a 99.7% confidence level. The solid bold line represents the real trace from the piezo stage. B) Tracking of helical motion induced by the piezo stage using extended configuration. The helix is 400 nm diameter, 1 µm per turn, and 50 nm step-size in z. The different home-built algorithms used codes to generate defined motion paths with the stage (linear, elliptical, 1D or 2D motion) were written in Java and adapted for micro-manager and are freely available at https://github.com/BorisLouis/MMScript.
Fig. 4.
Fig. 4. Comparison between phasor and astigmatism approach. A) PSF of a single emitter in 3D. B) ellipticity(z) curves for the different imaging planes. C) Axial precision for the two tested approaches as a function of the number of photons detected. For both approaches, the axial precision was calculated using a 1D stepwise motion (see the previous section).
Fig. 5.
Fig. 5. 3D single-particle tracking A) A representative example of an experimental 3D diffusion single trace for a 1 µm bead in water. The color indicates time in second. B) 3D MSD vs lag time for 0.2, 0.5, and 1 µm diameter PS fluorescent particles with the corresponding fitting for short lag times (dashed lines). C) 3D diffusion coefficient dependence on the bead diameter.
Fig. 6.
Fig. 6. Tracking fluorescent particles as they come to the trapping site. (A-B) Exemplary time-color-coded trace at 36 mW (A) and 240 mW (B). The trapping site was localized approximately at position (5,5). Locally average radial speed is noted in the inset. In both cases, the speed increases when approaching the trap. (C-D) 3D traces of all the trapping events acquired from 45 independent movies at 36 mW (C) and 240 mW (D). (E) Distribution of radial speed for the different trapping laser powers used (36, 60, 120 and 240 mW). (F) Plot of the trapping probability as a function of the trapping laser power after objective, the red solid line is a linear fit, R$^2$ = 0.98.

Equations (2)

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M S D ( τ ) = 2 n D n τ
D = k B T 6 π η r 0