Abstract

Light-sheet microscopy (LSM) is a powerful imaging technique that uses a planar illumination oriented orthogonally to the detection axis. Two-photon (2P) LSM is a variant of LSM that exploits the 2P absorption effect for sample excitation. The light polarization state plays a significant, and often overlooked, role in 2P absorption processes. The scope of this work is to test whether using different polarization states for excitation light can affect the detected signal levels in 2P LSM imaging of typical biological samples with a spatially unordered dye population. Supported by a theoretical model, we compared the fluorescence signals obtained using different polarization states with various fluorophores (fluorescein, EGFP and GCaMP6s) and different samples (liquid solution and fixed or living zebrafish larvae). In all conditions, in agreement with our theoretical expectations, linear polarization oriented parallel to the detection plane provided the largest signal levels, while perpendicularly-oriented polarization gave low fluorescence signal with the biological samples, but a large signal for the fluorescein solution. Finally, circular polarization generally provided lower signal levels. These results highlight the importance of controlling the light polarization state in 2P LSM of biological samples. Furthermore, this characterization represents a useful guide to choose the best light polarization state when maximization of signal levels is needed, e.g. in high-speed 2P LSM.

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

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2020 (2)

P. Ricci, G. Sancataldo, V. Gavryusev, A. Franceschini, M. C. Müllenbroich, L. Silvestri, and F. S. Pavone, “Fast multi-directional DSLM for confocal detection without striping artifacts,” Biomed. Opt. Express 11(6), 3111–3124 (2020).
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[Crossref]

2019 (2)

G. Sancataldo, V. Gavryusev, G. de Vito, L. Turrini, M. Locatelli, C. Fornetto, N. Tiso, F. Vanzi, L. Silvestri, and F. S. Pavone, “Flexible Multi-Beam Light-Sheet Fluorescence Microscope for Live Imaging Without Striping Artifacts,” Front. Neuroanat. 13, 7 (2019).
[Crossref]

V. Gavryusev, G. Sancataldo, P. Ricci, A. Montalbano, C. Fornetto, L. Turrini, A. Laurino, L. Pesce, G. de Vito, N. Tiso, F. Vanzi, L. Silvestri, and F. S. Pavone, “Dual-beam confocal light-sheet microscopy via flexible acousto-optic deflector,” J. Biomed. Opt. 24(10), 106504 (2019).
[Crossref]

2018 (2)

T. A. Nguyen, H. L. Puhl, A. K. Pham, and S. S. Vogel, “Auto-FPFA: An Automated Microscope for Characterizing Genetically Encoded Biosensors,” Sci. Rep. 8(1), 7374 (2018).
[Crossref]

M. C. Müllenbroich, L. Turrini, L. Silvestri, T. Alterini, A. Gheisari, N. Tiso, F. Vanzi, L. Sacconi, and F. S. Pavone, “Bessel Beam Illumination Reduces Random and Systematic Errors in Quantitative Functional Studies Using Light-Sheet Microscopy,” Front. Cell. Neurosci. 12, 315 (2018).
[Crossref]

2017 (5)

I. Micu, C. Brideau, L. Lu, and P. K. Stys, “Effects of laser polarization on responses of the fluorescent Ca2+ indicator X-Rhod-1 in neurons and myelin,” Neurophotonics 4(2), 025002 (2017).
[Crossref]

G. de Vito, V. Cappello, I. Tonazzini, M. Cecchini, and V. Piazza, “RP-CARS reveals molecular spatial order anomalies in myelin of an animal model of Krabbe disease,” J. Biophotonics 10(3), 385–393 (2017).
[Crossref]

C. Vinegoni, P. Fumene Feruglio, C. Brand, S. Lee, A. E. Nibbs, S. Stapleton, S. Shah, I. Gryczynski, T. Reiner, R. Mazitschek, and R. Weissleder, “Measurement of drug-target engagement in live cells by two-photon fluorescence anisotropy imaging,” Nat. Protoc. 12(7), 1472–1497 (2017).
[Crossref]

L. Turrini, C. Fornetto, G. Marchetto, M. C. Müllenbroich, N. Tiso, A. Vettori, F. Resta, A. Masi, G. Mannaioni, F. S. Pavone, and F. Vanzi, “Optical mapping of neuronal activity during seizures in zebrafish,” Sci. Rep. 7(1), 3025 (2017).
[Crossref]

A. Kuznetsova, P. B. Brockhoff, and R. H. B. Christensen, “lmerTest Package: Tests in Linear Mixed Effects Models,” J. Stat. Soft. 82, 13 (2017).
[Crossref]

2016 (1)

Z. Lavagnino, G. Sancataldo, M. d’Amora, P. Follert, D. De Pietri Tonelli, A. Diaspro, and F. Cella Zanacchi, “4D (x-y-z-t) imaging of thick biological samples by means of Two-Photon inverted Selective Plane Illumination Microscopy (2PE-iSPIM),” Sci. Rep. 6(1), 23923 (2016).
[Crossref]

2015 (1)

S. Wolf, W. Supatto, G. Debrégeas, P. Mahou, S. G. Kruglik, J.-M. Sintes, E. Beaurepaire, and R. Candelier, “Whole-brain functional imaging with two-photon light-sheet microscopy,” Nat. Methods 12(5), 379–380 (2015).
[Crossref]

2014 (1)

N. Vladimirov, Y. Mu, T. Kawashima, D. V. Bennett, C.-T. Yang, L. L. Looger, P. J. Keller, J. Freeman, and M. B. Ahrens, “Light-sheet functional imaging in fictively behaving zebrafish,” Nat. Methods 11(9), 883–884 (2014).
[Crossref]

2013 (3)

A. Kress, X. Wang, H. Ranchon, J. Savatier, H. Rigneault, P. Ferrand, and S. Brasselet, “Mapping the Local Organization of Cell Membranes Using Excitation-Polarization-Resolved Confocal Fluorescence Microscopy,” Biophys. J. 105(1), 127–136 (2013).
[Crossref]

K. Wang, N. G. Horton, and C. Xu, “Going Deep: Brain Imaging with Multi-Photon Microscopy,” Opt. Photonics News 24(11), 32–39 (2013).
[Crossref]

Z. Lavagnino, F. C. Zanacchi, E. Ronzitti, and A. Diaspro, “Two-photon excitation selective plane illumination microscopy (2PE-SPIM) of highly scattering samples: characterization and application,” Opt. Express 21(5), 5998–6008 (2013).
[Crossref]

2011 (5)

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

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]

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]

S. Brasselet, “Polarization-resolved nonlinear microscopy: application to structural molecular and biological imaging,” Adv. Opt. Photonics 3(3), 205 (2011).
[Crossref]

C. Lorenzo, C. Frongia, R. Jorand, J. Fehrenbach, P. Weiss, A. Maandhui, G. Gay, B. Ducommun, and V. Lobjois, “Live cell division dynamics monitoring in 3D large spheroid tumor models using light sheet microscopy,” Cell Div. 6(1), 22 (2011).
[Crossref]

2010 (5)

M. Zimmerley, R. Younger, T. Valenton, D. C. Oertel, J. L. Ward, and E. O. Potma, “Molecular Orientation in Dry and Hydrated Cellulose Fibers: A Coherent Anti-Stokes Raman Scattering Microscopy Study,” J. Phys. Chem. B 114(31), 10200–10208 (2010).
[Crossref]

V. Nucciotti, C. Stringari, L. Sacconi, F. Vanzi, L. Fusi, M. Linari, G. Piazzesi, V. Lombardi, and F. S. Pavone, “Probing myosin structural conformation in vivo by second-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U. S. A. 107(17), 7763–7768 (2010).
[Crossref]

A. Anantharam, B. Onoa, R. H. Edwards, R. W. Holz, and D. Axelrod, “Localized topological changes of the plasma membrane upon exocytosis visualized by polarized TIRFM,” J. Cell Biol. 188(3), 415–428 (2010).
[Crossref]

J. Palero, S. I. C. O. Santos, D. Artigas, and P. Loza-Alvarez, “A simple scanless two-photon fluorescence microscope using selective plane illumination,” Opt. Express 18(8), 8491–8498 (2010).
[Crossref]

A. Nag and D. Goswami, “Polarization induced control of single and two-photon fluorescence,” J. Chem. Phys. 132(15), 154508 (2010).
[Crossref]

2009 (3)

G. Steinbach, I. Pomozi, O. Zsiros, L. Menczel, and G. Garab, “Imaging anisotropy using differential polarization laser scanning confocal microscopy,” Acta Histochem. 111(4), 317–326 (2009).
[Crossref]

A. Gasecka, T.-J. Han, C. Favard, B. R. Cho, and S. Brasselet, “Quantitative Imaging of Molecular Order in Lipid Membranes Using Two-Photon Fluorescence Polarimetry,” Biophys. J. 97(10), 2854–2862 (2009).
[Crossref]

H. Mojzisova, J. Olesiak, M. Zielinski, K. Matczyszyn, D. Chauvat, and J. Zyss, “Polarization-Sensitive Two-Photon Microscopy Study of the Organization of Liquid-Crystalline DNA,” Biophys. J. 97(8), 2348–2357 (2009).
[Crossref]

2008 (1)

J. Hohlbein and C. G. Hübner, “Three-dimensional orientation determination of the emission dipoles of single molecules: The shot-noise limit,” J. Chem. Phys. 129(9), 094703 (2008).
[Crossref]

2004 (1)

J. Huisken, J. Swoger, F. D. 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]

2003 (1)

F. Maderspacher and C. Nüsslein-Volhard, “Formation of the adult pigment pattern in zebrafish requires leopard and obelix dependent cell interactions,” Development 130(15), 3447–3457 (2003).
[Crossref]

2000 (1)

C. L. Asbury, J. L. Uy, and G. van den Engh, “Polarization of scatter and fluorescence signals in flow cytometry,” Cytometry 40(2), 88–101 (2000).
[Crossref]

1999 (1)

D. Magde, G. E. Rojas, and P. G. Seybold, “Solvent Dependence of the Fluorescence Lifetimes of Xanthene Dyes,” Photochem. Photobiol. 70(5), 737–744 (1999).
[Crossref]

1997 (1)

R. Swaminathan, C. P. Hoang, and A. S. Verkman, “Photobleaching recovery and anisotropy decay of green fluorescent protein GFP-S65T in solution and cells: cytoplasmic viscosity probed by green fluorescent protein translational and rotational diffusion,” Biophys. J. 72(4), 1900–1907 (1997).
[Crossref]

1996 (1)

B. R. Sorensen and M. A. Shea, “Calcium binding decreases the stokes radius of calmodulin and mutants R74A, R90A, and R90G,” Biophys. J. 71(6), 3407–3420 (1996).
[Crossref]

1987 (1)

1984 (1)

1931 (1)

M. Göppert-Mayer, “Über Elementarakte mit zwei Quantensprüngen,” Ann. Phys. 401(3), 273–294 (1931).
[Crossref]

1902 (1)

H. Siedentopf and R. Zsigmondy, “Visualisation and determination of size of ultra microscopic particles, with special use of Goldrubin glasses,” Ann. Phys. 315(1), 1–39 (1902).
[Crossref]

Ahrens, M. B.

N. Vladimirov, Y. Mu, T. Kawashima, D. V. Bennett, C.-T. Yang, L. L. Looger, P. J. Keller, J. Freeman, and M. B. Ahrens, “Light-sheet functional imaging in fictively behaving zebrafish,” Nat. Methods 11(9), 883–884 (2014).
[Crossref]

Alterini, T.

M. C. Müllenbroich, L. Turrini, L. Silvestri, T. Alterini, A. Gheisari, N. Tiso, F. Vanzi, L. Sacconi, and F. S. Pavone, “Bessel Beam Illumination Reduces Random and Systematic Errors in Quantitative Functional Studies Using Light-Sheet Microscopy,” Front. Cell. Neurosci. 12, 315 (2018).
[Crossref]

Amat-Roldan, I.

S. Psilodimitrakopoulos, V. Petegnief, G. Soria, I. Amat-Roldan, D. Artigas, A. M. Planas, and P. Loza-Alvarez, “Polarization second harmonic generation (PSHG) imaging of neurons: estimating the effective orientation of the SHG source in axons,” in Multiphoton Microscopy in the Biomedical Sciences X (International Society for Optics and Photonics, 2010), Vol. 7569, p. 75692W.

Anantharam, A.

A. Anantharam, B. Onoa, R. H. Edwards, R. W. Holz, and D. Axelrod, “Localized topological changes of the plasma membrane upon exocytosis visualized by polarized TIRFM,” J. Cell Biol. 188(3), 415–428 (2010).
[Crossref]

Artigas, D.

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M. C. Müllenbroich, L. Turrini, L. Silvestri, T. Alterini, A. Gheisari, N. Tiso, F. Vanzi, L. Sacconi, and F. S. Pavone, “Bessel Beam Illumination Reduces Random and Systematic Errors in Quantitative Functional Studies Using Light-Sheet Microscopy,” Front. Cell. Neurosci. 12, 315 (2018).
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G. de Vito, C. Fornetto, P. Ricci, C. Müllenbroich, G. Sancataldo, L. Turrini, G. Mazzamuto, N. Tiso, L. Sacconi, D. Fanelli, L. Silvestri, F. Vanzi, and F. S. Pavone, “Two-photon high-speed light-sheet volumetric imaging of brain activity during sleep in zebrafish larvae,” in Neural Imaging and Sensing 2020 (International Society for Optics and Photonics, 2020), Vol. 11226, p. 1122604.

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S. Psilodimitrakopoulos, V. Petegnief, G. Soria, I. Amat-Roldan, D. Artigas, A. M. Planas, and P. Loza-Alvarez, “Polarization second harmonic generation (PSHG) imaging of neurons: estimating the effective orientation of the SHG source in axons,” in Multiphoton Microscopy in the Biomedical Sciences X (International Society for Optics and Photonics, 2010), Vol. 7569, p. 75692W.

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G. Steinbach, I. Pomozi, O. Zsiros, L. Menczel, and G. Garab, “Imaging anisotropy using differential polarization laser scanning confocal microscopy,” Acta Histochem. 111(4), 317–326 (2009).
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M. Zimmerley, R. Younger, T. Valenton, D. C. Oertel, J. L. Ward, and E. O. Potma, “Molecular Orientation in Dry and Hydrated Cellulose Fibers: A Coherent Anti-Stokes Raman Scattering Microscopy Study,” J. Phys. Chem. B 114(31), 10200–10208 (2010).
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S. Psilodimitrakopoulos, V. Petegnief, G. Soria, I. Amat-Roldan, D. Artigas, A. M. Planas, and P. Loza-Alvarez, “Polarization second harmonic generation (PSHG) imaging of neurons: estimating the effective orientation of the SHG source in axons,” in Multiphoton Microscopy in the Biomedical Sciences X (International Society for Optics and Photonics, 2010), Vol. 7569, p. 75692W.

Puhl, H. L.

T. A. Nguyen, H. L. Puhl, A. K. Pham, and S. S. Vogel, “Auto-FPFA: An Automated Microscope for Characterizing Genetically Encoded Biosensors,” Sci. Rep. 8(1), 7374 (2018).
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P. Ricci, G. Sancataldo, V. Gavryusev, A. Franceschini, M. C. Müllenbroich, L. Silvestri, and F. S. Pavone, “Fast multi-directional DSLM for confocal detection without striping artifacts,” Biomed. Opt. Express 11(6), 3111–3124 (2020).
[Crossref]

V. Gavryusev, G. Sancataldo, P. Ricci, A. Montalbano, C. Fornetto, L. Turrini, A. Laurino, L. Pesce, G. de Vito, N. Tiso, F. Vanzi, L. Silvestri, and F. S. Pavone, “Dual-beam confocal light-sheet microscopy via flexible acousto-optic deflector,” J. Biomed. Opt. 24(10), 106504 (2019).
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N. Vladimirov, Y. Mu, T. Kawashima, D. V. Bennett, C.-T. Yang, L. L. Looger, P. J. Keller, J. Freeman, and M. B. Ahrens, “Light-sheet functional imaging in fictively behaving zebrafish,” Nat. Methods 11(9), 883–884 (2014).
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C. Vinegoni, P. Fumene Feruglio, C. Brand, S. Lee, A. E. Nibbs, S. Stapleton, S. Shah, I. Gryczynski, T. Reiner, R. Mazitschek, and R. Weissleder, “Measurement of drug-target engagement in live cells by two-photon fluorescence anisotropy imaging,” Nat. Protoc. 12(7), 1472–1497 (2017).
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F. C. Zanacchi, Z. Lavagnino, M. Pesce, F. Difato, E. Ronzitti, and A. Diaspro, “Two-photon fluorescence excitation within a light sheet based microscopy architecture,” in Multiphoton Microscopy in the Biomedical Sciences XI (International Society for Optics and Photonics, 2011), Vol. 7903, p. 79032W.

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G. de Vito, L. Turrini, C. Fornetto, P. Ricci, C. Müllenbroich, G. Sancataldo, E. Trabalzini, G. Mazzamuto, N. Tiso, L. Sacconi, D. Fanelli, L. Silvestri, F. Vanzi, and F. S. Pavone, “Two-photon light-sheet microscopy for high-speed whole-brain functional imaging of zebrafish neuronal physiology and pathology,” in Neurophotonics (International Society for Optics and Photonics, 2020), Vol. 11360, p. 1136004.

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S. Psilodimitrakopoulos, V. Petegnief, G. Soria, I. Amat-Roldan, D. Artigas, A. M. Planas, and P. Loza-Alvarez, “Polarization second harmonic generation (PSHG) imaging of neurons: estimating the effective orientation of the SHG source in axons,” in Multiphoton Microscopy in the Biomedical Sciences X (International Society for Optics and Photonics, 2010), Vol. 7569, p. 75692W.

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Figures (4)

Fig. 1.
Fig. 1. Schematic of the polarization-dependent effects in 2P LSM, assuming a fixed orientation of the fluorophore dipole moment. (a) If both the polarization plane (indicated by short red arrows) of the linearly-polarized excitation light (red arrow) and the transition dipole of the fluorophore (black line) are aligned with the z-axis, the fluorophore is excited, but the fluorescence light (colored distribution) is emitted predominately on the xy-plane [24]. (b) If the polarization plane of the excitation light is parallel to the y-axis while the transition dipole is perpendicular to it, then no fluorescence light is generated. (c) If both the polarization plane of the excitation light and the transition dipole are aligned with the y-axis, then the fluorescence light is emitted predominately on the xz-plane and therefore part of it (green arrow) can be collected by the detection objective (on the z-axis).
Fig. 2.
Fig. 2. (a) Schematic of the custom-made 2P LS microscope. Fs-laser: femtosecond laser. Pre Comp: pulse compressor. Int. control: intensity control assembly, composed by a half-wave plate and a Glan–Thompson prism. EOM: Electro-Optical Modulator. λ/2: half-wave plate. λ/4: quarter-wave plate. Galvos: galvanometric mirror assembly, composed by a resonant mirror and a closed-loop mirror. Red line: excitation light. Green line: fluorescence light. The dashed lines indicate vertical paths. Axis specification is consistent with Fig. 1, with the excitation and detection objectives oriented along the x-axis and the z-axis, respectively. (b) Scatter plot of the fluorescent signal generated by a fixed Tg(actin:EGFP) larva as a function of the excitation power. Parabolic fit of the data is indicated by the continuous line and its coefficient of determination is reported on the graph. (c) Scatter plot of the signal generated by a fluorescein solution excited with circularly-, vertically- or horizontally-polarized light. Each condition was tested in triplicate and each point represents a single measure. The signal value is normalized to the average of the circular polarization case. Statistically significant differences are indicated by three asterisks.
Fig. 3.
Fig. 3. Imaging of Tg(actin:EGFP) larvae in fixed condition, (a) and (c), and in living condition, (b), (d) and (e). (a), (b) Individual z-slices extracted from volumetric acquisitions of larvae representative of the respective conditions. The green ovals indicate the ROIs traced on these larvae. Scale bars: 100 µm. (c), (d) Scatter plots of the average signal measured from the ROIs as a function of the polarization condition. Each point represents an individual acquisition, the points inherent to the same animal are indicated with the same color in the respective graph. The average values for each animal and for each condition are linked with lines of the same color. In each graph the signal value is normalized to the average of the circular polarization case. Statistically significant differences are indicated by three asterisks (p-value < 0.0001). (e) Z-slices extracted from volumetric acquisitions of the same larva as in (b) in the three polarization conditions. The signal intensity is mapped as indicated in the grayscale bar on the right. Magnifications of the areas in the green squares are reported in the insets. Scale bar: 100 µm.
Fig. 4.
Fig. 4. Imaging of Tg(elavl3:H2B-GCaMP6s) larvae in fixed condition, (a) and (c), and in living condition, (b) and (d). (a) Individual z-slice extracted from the volumetric acquisitions of a representative larva. The green oval indicates the ROI measured for this larva. (b) Maximum projection of a sub-volume of the volumetric stack (70 µm along the dorso-ventral direction from the original 150 µm) of the larva. The colored ovals indicate the different ROIs. Scale bars: 100 µm. (c), (d) Scatter plots of the average signal measured from the ROIs traced on the larvae as a function of the polarization condition. The signal value is normalized to the mean of the circular polarization case. Statistically significant differences are indicated by asterisks (***: p-value < 0.0001, **: p-value = 0.0016). (c) Each point represents an individual acquisition, the points inherent to the same animal are indicated with the same color. The average values for each animal and for each condition are linked with lines of the same color. (d) Different colors indicate different ROIs, as shown in (b). For each color, each point represents an individual acquisition. The average values for each ROI and for each condition are linked with lines of the same color. The thick black line indicates the global averages for each condition.

Equations (8)

Equations on this page are rendered with MathJax. Learn more.

InphPabsnphPem
Pabsnph|μgeEexc|2n,
Pabs 1ph|μge|2Iexccos2(θ)
Pabs 2ph |μge |4Iexc 2cos4(θ),
Pem(i^)Iem(i^)|Eemi^|2|(k^×(k^×μeg))i^|2=|μegi^|2
I2ph(i^)|μegi^|2|μgeEexc|4|μegi^|2|μge|4Iexc2cos4(θ),
β=11+τ/α,
α=ηVKbT