Abstract

Using light-sheet microscopy combined with digital Fourier methods we probe the dynamics of colloidal samples and DNA molecules. This combination, referred to as selective-plane illumination differential dynamic microscopy (SPIDDM), has the benefit of optical sectioning to study, with minimal photobleaching, thick samples allowing us to measure the diffusivity of colloidal particles at high volume fractions. Further, SPIDDM exploits the inherent spatially-varying thickness of Gaussian light-sheets. Where the excitation sheet is most focused, we capture high spatial frequency dynamics as the signal-to-background is high. In thicker regions, we capture the slower dynamics as diffusion out of the sheet takes longer.

© 2016 Optical Society of America

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2016 (4)

D. Germain, M. Leocmach, and T. Gibaud, “Differential dynamic microscopy to characterize Brownian motion and bacteria motility,” Am. J. Phys. 84(3), 202–210 (2016).
[Crossref]

F. Giavazzi, C. Haro-Pérez, and R. Cerbino, “Simultaneous characterization of rotational and translational diffusion of optically anisotropic particles by optical microscopy,” J. Phys. Condens. Matter 28(19), 195201 (2016).
[Crossref] [PubMed]

T. Sentjabrskaja, E. Zaccarelli, C. De Michele, F. Sciortino, P. Tartaglia, T. Voigtmann, S. U. Egelhaaf, and M. Laurati, “Anomalous dynamics of intruders in a crowded environment of mobile obstacles,” Nat. Commun. 7, 11133 (2016).
[Crossref] [PubMed]

A. V. Bayles, T. M. Squires, and M. E. Helgeson, “Dark-field differential dynamic microscopy,” Soft Matter 12(8), 2440–2452 (2016).
[Crossref] [PubMed]

2015 (7)

C. D. Chapman, S. Gorczyca, and R. M. Robertson-Anderson, “Crowding induces complex ergodic diffusion and dynamic elongation of large DNA molecules,” Biophys. J. 108(5), 1220–1228 (2015).
[Crossref] [PubMed]

J. D. C. Jacob, K. He, S. T. Retterer, R. Krishnamoorti, and J. C. Conrad, “Diffusive dynamics of nanoparticles in ultra-confined media,” Soft Matter 11(38), 7515–7524 (2015).
[Crossref] [PubMed]

M. S. Safari, M. A. Vorontsova, R. Poling-Skutvik, P. G. Vekilov, and J. C. Conrad, “Differential dynamic microscopy of weakly scattering and polydisperse protein-rich clusters,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 92(4), 042712 (2015).
[Crossref] [PubMed]

C. Manzo and M. F. Garcia-Parajo, “A review of progress in single particle tracking: from methods to biophysical insights,” Rep. Prog. Phys. 78(12), 124601 (2015).
[Crossref] [PubMed]

E. H. K. Stelzer, “Light-sheet fluorescence microscopy for quantitative biology,” Nat. Methods 12(1), 23–26 (2015).
[Crossref] [PubMed]

L. Gao, “Extend the field of view of selective plan illumination microscopy by tiling the excitation light sheet,” Opt. Express 23(5), 6102–6111 (2015).
[Crossref] [PubMed]

R. McGorty, H. Liu, D. Kamiyama, Z. Dong, S. Guo, and B. Huang, “Open-top selective plane illumination microscope for conventionally mounted specimens,” Opt. Express 23(12), 16142–16153 (2015).
[Crossref] [PubMed]

2014 (3)

K. M. Dean and R. Fiolka, “Uniform and scalable light-sheets generated by extended focusing,” Opt. Express 22(21), 26141–26152 (2014).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

F. Giavazzi and R. Cerbino, “Digital Fourier microscopy for soft matter dynamics,” J. Opt. 16(8), 083001 (2014).
[Crossref]

2013 (2)

K. He, F. Babaye Khorasani, S. T. Retterer, D. K. Thomas, J. C. Conrad, and R. Krishnamoorti, “Diffusive dynamics of nanoparticles in arrays of nanoposts,” ACS Nano 7(6), 5122–5130 (2013).
[Crossref] [PubMed]

P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10(7), 598–599 (2013).
[Crossref] [PubMed]

2012 (6)

J. Huisken, “Slicing embryos gently with laser light sheets,” BioEssays 34(5), 406–411 (2012).
[Crossref] [PubMed]

R. Tomer, K. Khairy, F. Amat, and P. J. Keller, “Quantitative high-speed imaging of entire developing embryos with simultaneous multiview light-sheet microscopy,” Nat. Methods 9(7), 755–763 (2012).
[Crossref] [PubMed]

R. Wang, L. Lei, Y. Wang, A. J. Levine, and G. Popescu, “Dispersion-relation fluorescence spectroscopy,” Phys. Rev. Lett. 109(18), 188104 (2012).
[Crossref] [PubMed]

P. J. Lu, F. Giavazzi, T. E. Angelini, E. Zaccarelli, F. Jargstorff, A. B. Schofield, J. N. Wilking, M. B. Romanowsky, D. A. Weitz, and R. Cerbino, “Characterizing concentrated, multiply scattering, and actively driven fluorescent systems with confocal differential dynamic microscopy,” Phys. Rev. Lett. 108(21), 218103 (2012).
[Crossref] [PubMed]

K. He, M. Spannuth, J. C. Conrad, and R. Krishnamoorti, “Diffusive dynamics of nanoparticles in aqueous dispersions,” Soft Matter 8(47), 11933–11938 (2012).
[Crossref]

M. Reufer, V. A. Martinez, P. Schurtenberger, and W. C. K. Poon, “Differential dynamic microscopy for anisotropic colloidal dynamics,” Langmuir 28(10), 4618–4624 (2012).
[Crossref] [PubMed]

2011 (6)

L. G. Wilson, V. A. Martinez, J. Schwarz-Linek, J. Tailleur, G. Bryant, P. N. Pusey, and W. C. K. Poon, “Differential dynamic microscopy of bacterial motility,” Phys. Rev. Lett. 106(1), 018101 (2011).
[Crossref] [PubMed]

T. V. Truong, W. Supatto, D. S. Koos, J. M. Choi, and S. E. Fraser, “Deep and fast live imaging with two-photon scanned light-sheet microscopy,” Nat. Methods 8(9), 757–760 (2011).
[Crossref] [PubMed]

T. Kalwarczyk, N. Ziȩbacz, A. Bielejewska, E. Zaboklicka, K. Koynov, J. Szymański, A. Wilk, A. Patkowski, J. Gapiński, H.-J. Butt, and R. Hołyst, “Comparative analysis of viscosity of complex liquids and cytoplasm of mammalian cells at the nanoscale,” Nano Lett. 11(5), 2157–2163 (2011).
[Crossref] [PubMed]

J. Capoulade, M. Wachsmuth, L. Hufnagel, and M. Knop, “Quantitative fluorescence imaging of protein diffusion and interaction in living cells,” Nat. Biotechnol. 29(9), 835–839 (2011).
[Crossref] [PubMed]

E. L. Elson, “Fluorescence correlation spectroscopy: past, present, future,” Biophys. J. 101(12), 2855–2870 (2011).
[Crossref] [PubMed]

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[Crossref] [PubMed]

2010 (2)

T. Wohland, X. Shi, J. Sankaran, and E. H. K. Stelzer, “Single Plane Illumination Fluorescence Correlation Spectroscopy (SPIM-FCS) probes inhomogeneous three-dimensional environments,” Opt. Express 18(10), 10627–10641 (2010).
[Crossref] [PubMed]

J. G. Ritter, R. Veith, A. Veenendaal, J. P. Siebrasse, and U. Kubitscheck, “Light sheet microscopy for single molecule tracking in living tissue,” PLoS One 5(7), e11639 (2010).
[Crossref] [PubMed]

2009 (3)

Z. Zhang, N. Xu, D. T. N. Chen, P. Yunker, A. M. Alsayed, K. B. Aptowicz, P. Habdas, A. J. Liu, S. R. Nagel, and A. G. Yodh, “Thermal vestige of the zero-temperature jamming transition,” Nature 459(7244), 230–233 (2009).
[Crossref] [PubMed]

F. Giavazzi, D. Brogioli, V. Trappe, T. Bellini, and R. Cerbino, “Scattering information obtained by optical microscopy: differential dynamic microscopy and beyond,” Phys. Rev. E 80(3 Pt 1), 031403 (2009).
[Crossref] [PubMed]

Y. Gao and M. L. Kilfoil, “Accurate detection and complete tracking of large populations of features in three dimensions,” Opt. Express 17(6), 4685–4704 (2009).
[Crossref] [PubMed]

2008 (4)

C. P. Brangwynne, G. H. Koenderink, F. C. MacKintosh, and D. A. Weitz, “Cytoplasmic diffusion: molecular motors mix it up,” J. Cell Biol. 183(4), 583–587 (2008).
[Crossref] [PubMed]

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. K. Stelzer, “Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

T. F. Holekamp, D. Turaga, and T. E. Holy, “Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy,” Neuron 57(5), 661–672 (2008).
[Crossref] [PubMed]

R. Cerbino and V. Trappe, “Differential dynamic microscopy: probing wave vector dependent dynamics with a microscope,” Phys. Rev. Lett. 100(18), 188102 (2008).
[Crossref] [PubMed]

2007 (2)

2006 (4)

R. M. Robertson, S. Laib, and D. E. Smith, “Diffusion of isolated DNA molecules: dependence on length and topology,” Proc. Natl. Acad. Sci. U.S.A. 103(19), 7310–7314 (2006).
[Crossref] [PubMed]

D. L. Kolin, D. Ronis, and P. W. Wiseman, “k-Space image correlation spectroscopy: a method for accurate transport measurements independent of fluorophore photophysics,” Biophys. J. 91(8), 3061–3075 (2006).
[Crossref] [PubMed]

F. Croccolo, D. Brogioli, A. Vailati, M. Giglio, and D. S. Cannell, “Use of dynamic Schlieren interferometry to study fluctuations during free diffusion,” Appl. Opt. 45(10), 2166–2173 (2006).
[Crossref] [PubMed]

S. Laib, R. M. Robertson, and D. E. Smith, “Preparation and characterization of a set of linear DNA molecules for polymer physics and rheology studies,” Macromolecules 39(12), 4115–4119 (2006).
[Crossref]

2004 (1)

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

2000 (1)

W. K. Kegel and A. Blaaderen, “Direct observation of dynamical heterogeneities in colloidal hard-sphere suspensions,” Science 287(5451), 290–293 (2000).
[Crossref] [PubMed]

1995 (1)

T. G. Mason and D. A. Weitz, “Optical measurements of frequency-dependent linear viscoelastic moduli of complex fluids,” Phys. Rev. Lett. 74(7), 1250–1253 (1995).
[Crossref] [PubMed]

1992 (1)

D. N. Petsev and N. D. Denkov, “Diffusion of charged colloidal particles at low volume fraction: Theoretical model and light scattering experiments,” J. Colloid Interface Sci. 149(2), 329–344 (1992).
[Crossref]

1985 (1)

S. H. Chen and J. S. Huang, “Dynamic slowing-down and nonexponential decay of the density correlation function in dense microemulsions,” Phys. Rev. Lett. 55(18), 1888–1891 (1985).
[Crossref] [PubMed]

Alsayed, A. M.

Z. Zhang, N. Xu, D. T. N. Chen, P. Yunker, A. M. Alsayed, K. B. Aptowicz, P. Habdas, A. J. Liu, S. R. Nagel, and A. G. Yodh, “Thermal vestige of the zero-temperature jamming transition,” Nature 459(7244), 230–233 (2009).
[Crossref] [PubMed]

Amat, F.

R. Tomer, K. Khairy, F. Amat, and P. J. Keller, “Quantitative high-speed imaging of entire developing embryos with simultaneous multiview light-sheet microscopy,” Nat. Methods 9(7), 755–763 (2012).
[Crossref] [PubMed]

Amodaj, N.

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).
[Crossref] [PubMed]

Angelini, T. E.

P. J. Lu, F. Giavazzi, T. E. Angelini, E. Zaccarelli, F. Jargstorff, A. B. Schofield, J. N. Wilking, M. B. Romanowsky, D. A. Weitz, and R. Cerbino, “Characterizing concentrated, multiply scattering, and actively driven fluorescent systems with confocal differential dynamic microscopy,” Phys. Rev. Lett. 108(21), 218103 (2012).
[Crossref] [PubMed]

Aptowicz, K. B.

Z. Zhang, N. Xu, D. T. N. Chen, P. Yunker, A. M. Alsayed, K. B. Aptowicz, P. Habdas, A. J. Liu, S. R. Nagel, and A. G. Yodh, “Thermal vestige of the zero-temperature jamming transition,” Nature 459(7244), 230–233 (2009).
[Crossref] [PubMed]

Babaye Khorasani, F.

K. He, F. Babaye Khorasani, S. T. Retterer, D. K. Thomas, J. C. Conrad, and R. Krishnamoorti, “Diffusive dynamics of nanoparticles in arrays of nanoposts,” ACS Nano 7(6), 5122–5130 (2013).
[Crossref] [PubMed]

Bayles, A. V.

A. V. Bayles, T. M. Squires, and M. E. Helgeson, “Dark-field differential dynamic microscopy,” Soft Matter 12(8), 2440–2452 (2016).
[Crossref] [PubMed]

Bellini, T.

F. Giavazzi, D. Brogioli, V. Trappe, T. Bellini, and R. Cerbino, “Scattering information obtained by optical microscopy: differential dynamic microscopy and beyond,” Phys. Rev. E 80(3 Pt 1), 031403 (2009).
[Crossref] [PubMed]

Betzig, E.

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K. He, F. Babaye Khorasani, S. T. Retterer, D. K. Thomas, J. C. Conrad, and R. Krishnamoorti, “Diffusive dynamics of nanoparticles in arrays of nanoposts,” ACS Nano 7(6), 5122–5130 (2013).
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Figures (7)

Fig. 1
Fig. 1 (a) The thickness of a Gaussian light-sheet varies along the direction of propagation, x. (b) Therefore, fluorescently-labeled particles may be localized at the light-sheet’s focus but not on either side where the sheet thickens. (c) Cartoon of light-sheet microscope showing the excitation objective (left) and the water-dipping imaging objective (bottom) imaging a sample within a tube placed in a water bath. (d) Image of 200-nm fluorescent beads showing good optical sectioning where the sheet is thinnest (left side) and higher background where the sheet thickens (right side). (e) Image showing the varying thickness of our light-sheet.
Fig. 2
Fig. 2 (a) A sequence of captured images is analyzed by subtracting each pair separated by a given lag time, Δt, taking the square of the Fourier transform, and averaging to produce the image structure function, shown in (b). (c) The radially averaged image structure function for Δt = 0.05 s. This procedure is then repeated for a range of lag times.
Fig. 3
Fig. 3 Images acquired of 200-nm fluorescent beads, φ = 10−3, with 1408 × 128 resolution are broken into eleven ROIs of 128 × 128 pixels and analyzed separately. (a) Full-field of view with two boxes highlighting different ROIs. The black box highlights the ROI (i) where the light-sheet is focused. The gray box highlights an ROI (ii) 90 µm upstream (w.r.t. the propagation of the excitation light-sheet). (b) The image structure functions, D(qt), of the two ROIs are shown (identical intensity scaling). The 2D image structure functions are shown with a lag time of 0.03 seconds. (c) The radial average of D(qt) for both ROIs is plotted as a function of wave-vector for three lag times: 0.03 s (diamonds), 0.18 s (circles) and 0.66 s (squares). (d) For both ROIs, D(qt) is plotted as a function time lag for three separate spatial frequencies: 2.09 rad/µm (circle), 5.22 rad/µm (square) and 8.36 rad/µm (diamond). Red lines are fits to Eq. (2).
Fig. 4
Fig. 4 (a) Just over half of a full 1408 × 128 field-of-view shown of fluorescent beads with volume fraction φ = 4 × 10−4. The black box highlights an ROI (i) where the light-sheet is most focused and the gray box (ii) where the light-sheet is thicker (~30 µm versus ~4.5 µm). (b) Five movies of 4000 frames each and of 1408 × 128 resolution were recorded at 300 Hz. For each ROI of 128 × 128 pixels we determined the diffusion coefficient, Dc. We plot the mean Dc as a function of the ROI (corresponding with the image above) with error bars showing the standard deviation across the five movies. Across all ROIs we found Dc = 2.28 µm2/s ± 0.03 µm2/s. The larger uncertainty in Dc for the far right ROI, which is about ± 0.1 µm2/s, is likely due to the higher background. (c) The diffusion coefficients are found by determining where τmq–2 and calculating the average Dc = τm−1q–2 over that range. The solid gray line is τm = (2.28 µm2/s)−1 q–2. The darker points correspond to ROI i and follow the τmq–2 scaling from around q ~1.5 rad/µm to q ~10 rad/µm. The gray points correspond to ROI ii and follow τmq–2 from around q ~0.6 rad/µm to q ~5.5 rad/µm.
Fig. 5
Fig. 5 Five movies, each of 4000 images, with 1408 × 128 resolution are taken of fluorescent 200-nm beads of volume fraction φ = 10−3 (representative image shown in Fig. 3(a)). Each movie is divided into eleven 128 × 128 ROIs and for each we find the range of wave-vectors, q, where τm scales as q–2. We find that where the light-sheet is thinnest (our central ROI) the expected τmq–2 scaling holds for larger q-values though it departs from the scaling, on the low-q end, at greater values than in regions where the light-sheet is thicker. Error bars depict the standard deviation of where the τmq–2 scaling fails on the low and high ends across the five different movies.
Fig. 6
Fig. 6 We varied the volume fraction by two orders of magnitude from φ = 4 × 10−4 to ~6 × 10−2. We typically recorded five movies at each volume fraction from which we could analyze multiple 128 × 128 ROIs. We include x error bars in the higher volume fractions as some uncertainty in introduced by concentrating the beads from the volume fraction supplied, φ = 2 × 10−2.
Fig. 7
Fig. 7 Labeled DNA in an aqueous buffer was analyzed with SPIDDM. (a) We recorded several movies of 4000 frames and 768 × 128 pixel resolution at 190 Hz. (b) We observe the same trend as with the colloidal suspension data. Analysis of images from the thinner regions of the light-sheet depart from the expected τq–2 scaling, on the low-q end, at greater q than regions where the light-sheet is thicker. Our data does not follow the τq–2 for as high a wave-vector (typically ~7 rad/ µm) as the data with the colloidal suspension. This is likely due to decreased signal-to-noise as the DNA molecules have fewer dyes molecules than the beads and excitation power had to be minimized to avoid photobleaching. The solid gray line shows τ = Dcq–2 for Dc = 0.72 µm2/s.

Equations (2)

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D(q,Δt)=A(q)[1g(q,Δt)]+B(q).
D(q,Δt)=A(q)[1exp {Δt/τ(q)} α(q) ]+B(q).

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