Abstract

Polarization-resolved third-harmonic generation (P-THG) is a sensitive probe of material anisotropy and molecular ordering. Despite its promises, this property has little been used in biological tissues due to the lack of measurement schemes compatible with dynamic samples. We report here on the development of a fast P-THG microscope where excitation polarization is switched between line scans using an electro-optic modulator, providing temporal resolution in the 10 ms range for the polarimetric measurement. We demonstrate novel applications enabled by this approach, associated with Fourier-based analysis: probing molecular order in deforming lipid structures undergoing phase transition; revealing crystallinity of flowing particles in the zebrafish embryo’s inner ear; and detecting birefringence in vivo. These results establish that P-THG is ideally suited for probing lipid organization and mineralization in dynamic biological environments.

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

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References

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2018 (1)

S. You, H. Tu, E. J. Chaney, Y. Sun, Y. Zhao, A. J. Bower, Y. Z. Liu, M. Marjanovic, S. Sinha, Y. Pu, and S. A. Boppart, Nat. Commun. 9, 2125 (2018).
[Crossref]

2017 (2)

2016 (2)

B. Weigelin, G. J. Bakker, and P. Friedl, J. Cell Sci. 129, 245 (2016).
[Crossref]

M. Samim, S. Krouglov, and V. Barzda, Phys. Rev. A 93, 033839(2016).
[Crossref]

2014 (3)

G. Bautista, S. G. Pfisterer, M. J. Huttunen, S. Ranjan, K. Kanerva, E. Ikonen, and M. Kauranen, Biophys. J. 107, 2230 (2014).
[Crossref]

G. J. Tserevelakis, E. V. Megalou, G. Filippidis, B. Petanidou, C. Fotakis, and N. Tavernarakis, PLoS One 9e84431 (2014).
[Crossref]

E. L. Dewalt, S. Z. Sullivan, P. D. Schmitt, R. D. Muir, and G. J. Simpson, Anal. Chem. 86, 8448 (2014).
[Crossref]

2013 (1)

M. Zimmerley, P. Mahou, D. Débarre, M.-C. Schanne-Klein, and E. Beaurepaire, Phys. Rev. X 3, 011002 (2013).
[Crossref]

2011 (2)

D. Wu, J. B. Freund, S. E. Fraser, and J. Vermot, Dev. Cell 20, 271 (2011).
[Crossref]

M. J. Farrar, F. W. Wise, J. R. Fetcho, and C. B. Schaffer, Biophys. J. 100, 1362 (2011).
[Crossref]

2010 (2)

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, Science 329, 967 (2010).
[Crossref]

N. Olivier, F. Aptel, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, Opt. Express 18, 5028 (2010).
[Crossref]

2006 (2)

R. S. Pillai, M. Oh-e, H. Yokoyama, G. J. Brakenhoff, and M. Müller, Opt. Express 14, 12976 (2006).
[Crossref]

D. Débarre, W. Supatto, A.-M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, Nat. Methods 3, 47 (2006).
[Crossref]

2005 (1)

G. J. Hermann, L. K. Schroeder, C. A. Hieb, A. M. Kershner, B. M. Rabbitts, P. Fonarev, B. D. Grant, and J. R. Priess, Mol. Biol. Cell 16, 3273 (2005).
[Crossref]

2004 (1)

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, Biophys. J. 86, 3914 (2004).
[Crossref]

2003 (2)

J. Cheng, S. Pautot, D. Weitz, and X. Xie, Proc. Natl. Acad. Sci. USA 100, 9826 (2003).
[Crossref]

D. Oron, E. Tal, and Y. Silberberg, Opt. Lett. 28, 2315 (2003).
[Crossref]

2002 (1)

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, Biophys. J. 82, 3330 (2002).
[Crossref]

1997 (1)

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, Appl. Phys. Lett. 70, 922 (1997).
[Crossref]

1965 (1)

A. D. Bangham, M. M. Standish, and J. C. Watkins, J. Mol. Biol. 13, 238 (1965).
[Crossref]

Aptel, F.

Bakker, G. J.

B. Weigelin, G. J. Bakker, and P. Friedl, J. Cell Sci. 129, 245 (2016).
[Crossref]

Balla, N. K.

Bangham, A. D.

A. D. Bangham, M. M. Standish, and J. C. Watkins, J. Mol. Biol. 13, 238 (1965).
[Crossref]

Barad, Y.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, Appl. Phys. Lett. 70, 922 (1997).
[Crossref]

Barzda, V.

L. Kontenis, M. Samim, S. Krouglov, and V. Barzda, Opt. Express 25, 13174 (2017).
[Crossref]

M. Samim, S. Krouglov, and V. Barzda, Phys. Rev. A 93, 033839(2016).
[Crossref]

Bautista, G.

G. Bautista, S. G. Pfisterer, M. J. Huttunen, S. Ranjan, K. Kanerva, E. Ikonen, and M. Kauranen, Biophys. J. 107, 2230 (2014).
[Crossref]

Beaurepaire, E.

M. Zimmerley, P. Mahou, D. Débarre, M.-C. Schanne-Klein, and E. Beaurepaire, Phys. Rev. X 3, 011002 (2013).
[Crossref]

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, Science 329, 967 (2010).
[Crossref]

N. Olivier, F. Aptel, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, Opt. Express 18, 5028 (2010).
[Crossref]

D. Débarre, W. Supatto, A.-M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, Nat. Methods 3, 47 (2006).
[Crossref]

Boppart, S. A.

S. You, H. Tu, E. J. Chaney, Y. Sun, Y. Zhao, A. J. Bower, Y. Z. Liu, M. Marjanovic, S. Sinha, Y. Pu, and S. A. Boppart, Nat. Commun. 9, 2125 (2018).
[Crossref]

Bourgine, P.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, Science 329, 967 (2010).
[Crossref]

Bower, A. J.

S. You, H. Tu, E. J. Chaney, Y. Sun, Y. Zhao, A. J. Bower, Y. Z. Liu, M. Marjanovic, S. Sinha, Y. Pu, and S. A. Boppart, Nat. Commun. 9, 2125 (2018).
[Crossref]

Boyd, R. W.

R. W. Boyd, Nonlinear Optics (2008).

Brakenhoff, G. J.

Brasselet, S.

Celliers, P. M.

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, Biophys. J. 82, 3330 (2002).
[Crossref]

Chaney, E. J.

S. You, H. Tu, E. J. Chaney, Y. Sun, Y. Zhao, A. J. Bower, Y. Z. Liu, M. Marjanovic, S. Sinha, Y. Pu, and S. A. Boppart, Nat. Commun. 9, 2125 (2018).
[Crossref]

Chen, S. Y.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, Biophys. J. 86, 3914 (2004).
[Crossref]

Chen, Y. C.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, Biophys. J. 86, 3914 (2004).
[Crossref]

Cheng, J.

J. Cheng, S. Pautot, D. Weitz, and X. Xie, Proc. Natl. Acad. Sci. USA 100, 9826 (2003).
[Crossref]

Chern, G. W.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, Biophys. J. 86, 3914 (2004).
[Crossref]

Chu, S. W.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, Biophys. J. 86, 3914 (2004).
[Crossref]

Combettes, L.

D. Débarre, W. Supatto, A.-M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, Nat. Methods 3, 47 (2006).
[Crossref]

Débarre, D.

M. Zimmerley, P. Mahou, D. Débarre, M.-C. Schanne-Klein, and E. Beaurepaire, Phys. Rev. X 3, 011002 (2013).
[Crossref]

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, Science 329, 967 (2010).
[Crossref]

D. Débarre, W. Supatto, A.-M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, Nat. Methods 3, 47 (2006).
[Crossref]

Dewalt, E. L.

E. L. Dewalt, S. Z. Sullivan, P. D. Schmitt, R. D. Muir, and G. J. Simpson, Anal. Chem. 86, 8448 (2014).
[Crossref]

Duloquin, L.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, Science 329, 967 (2010).
[Crossref]

Eisenberg, H.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, Appl. Phys. Lett. 70, 922 (1997).
[Crossref]

Fabre, A.

D. Débarre, W. Supatto, A.-M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, Nat. Methods 3, 47 (2006).
[Crossref]

Farrar, M. J.

M. J. Farrar, F. W. Wise, J. R. Fetcho, and C. B. Schaffer, Biophys. J. 100, 1362 (2011).
[Crossref]

Faure, E.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, Science 329, 967 (2010).
[Crossref]

Fetcho, J. R.

M. J. Farrar, F. W. Wise, J. R. Fetcho, and C. B. Schaffer, Biophys. J. 100, 1362 (2011).
[Crossref]

Filippidis, G.

G. J. Tserevelakis, E. V. Megalou, G. Filippidis, B. Petanidou, C. Fotakis, and N. Tavernarakis, PLoS One 9e84431 (2014).
[Crossref]

Fonarev, P.

G. J. Hermann, L. K. Schroeder, C. A. Hieb, A. M. Kershner, B. M. Rabbitts, P. Fonarev, B. D. Grant, and J. R. Priess, Mol. Biol. Cell 16, 3273 (2005).
[Crossref]

Fotakis, C.

G. J. Tserevelakis, E. V. Megalou, G. Filippidis, B. Petanidou, C. Fotakis, and N. Tavernarakis, PLoS One 9e84431 (2014).
[Crossref]

Fraser, S. E.

D. Wu, J. B. Freund, S. E. Fraser, and J. Vermot, Dev. Cell 20, 271 (2011).
[Crossref]

Freund, J. B.

D. Wu, J. B. Freund, S. E. Fraser, and J. Vermot, Dev. Cell 20, 271 (2011).
[Crossref]

Friedl, P.

B. Weigelin, G. J. Bakker, and P. Friedl, J. Cell Sci. 129, 245 (2016).
[Crossref]

Grant, B. D.

G. J. Hermann, L. K. Schroeder, C. A. Hieb, A. M. Kershner, B. M. Rabbitts, P. Fonarev, B. D. Grant, and J. R. Priess, Mol. Biol. Cell 16, 3273 (2005).
[Crossref]

Hermann, G. J.

G. J. Hermann, L. K. Schroeder, C. A. Hieb, A. M. Kershner, B. M. Rabbitts, P. Fonarev, B. D. Grant, and J. R. Priess, Mol. Biol. Cell 16, 3273 (2005).
[Crossref]

Hieb, C. A.

G. J. Hermann, L. K. Schroeder, C. A. Hieb, A. M. Kershner, B. M. Rabbitts, P. Fonarev, B. D. Grant, and J. R. Priess, Mol. Biol. Cell 16, 3273 (2005).
[Crossref]

Hofer, M.

Horowitz, M.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, Appl. Phys. Lett. 70, 922 (1997).
[Crossref]

Huttunen, M. J.

G. Bautista, S. G. Pfisterer, M. J. Huttunen, S. Ranjan, K. Kanerva, E. Ikonen, and M. Kauranen, Biophys. J. 107, 2230 (2014).
[Crossref]

Ikonen, E.

G. Bautista, S. G. Pfisterer, M. J. Huttunen, S. Ranjan, K. Kanerva, E. Ikonen, and M. Kauranen, Biophys. J. 107, 2230 (2014).
[Crossref]

Kanerva, K.

G. Bautista, S. G. Pfisterer, M. J. Huttunen, S. Ranjan, K. Kanerva, E. Ikonen, and M. Kauranen, Biophys. J. 107, 2230 (2014).
[Crossref]

Kauranen, M.

G. Bautista, S. G. Pfisterer, M. J. Huttunen, S. Ranjan, K. Kanerva, E. Ikonen, and M. Kauranen, Biophys. J. 107, 2230 (2014).
[Crossref]

Kershner, A. M.

G. J. Hermann, L. K. Schroeder, C. A. Hieb, A. M. Kershner, B. M. Rabbitts, P. Fonarev, B. D. Grant, and J. R. Priess, Mol. Biol. Cell 16, 3273 (2005).
[Crossref]

Kontenis, L.

Krouglov, S.

L. Kontenis, M. Samim, S. Krouglov, and V. Barzda, Opt. Express 25, 13174 (2017).
[Crossref]

M. Samim, S. Krouglov, and V. Barzda, Phys. Rev. A 93, 033839(2016).
[Crossref]

Lin, B. L.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, Biophys. J. 86, 3914 (2004).
[Crossref]

Liu, Y. Z.

S. You, H. Tu, E. J. Chaney, Y. Sun, Y. Zhao, A. J. Bower, Y. Z. Liu, M. Marjanovic, S. Sinha, Y. Pu, and S. A. Boppart, Nat. Commun. 9, 2125 (2018).
[Crossref]

Luengo-Oroz, M. A.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, Science 329, 967 (2010).
[Crossref]

Mahou, P.

M. Zimmerley, P. Mahou, D. Débarre, M.-C. Schanne-Klein, and E. Beaurepaire, Phys. Rev. X 3, 011002 (2013).
[Crossref]

Marjanovic, M.

S. You, H. Tu, E. J. Chaney, Y. Sun, Y. Zhao, A. J. Bower, Y. Z. Liu, M. Marjanovic, S. Sinha, Y. Pu, and S. A. Boppart, Nat. Commun. 9, 2125 (2018).
[Crossref]

Megalou, E. V.

G. J. Tserevelakis, E. V. Megalou, G. Filippidis, B. Petanidou, C. Fotakis, and N. Tavernarakis, PLoS One 9e84431 (2014).
[Crossref]

Muir, R. D.

E. L. Dewalt, S. Z. Sullivan, P. D. Schmitt, R. D. Muir, and G. J. Simpson, Anal. Chem. 86, 8448 (2014).
[Crossref]

Müller, M.

Oh-e, M.

Olivier, N.

N. Olivier, F. Aptel, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, Opt. Express 18, 5028 (2010).
[Crossref]

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, Science 329, 967 (2010).
[Crossref]

Oron, D.

Pautot, S.

J. Cheng, S. Pautot, D. Weitz, and X. Xie, Proc. Natl. Acad. Sci. USA 100, 9826 (2003).
[Crossref]

Pena, A.-M.

D. Débarre, W. Supatto, A.-M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, Nat. Methods 3, 47 (2006).
[Crossref]

Petanidou, B.

G. J. Tserevelakis, E. V. Megalou, G. Filippidis, B. Petanidou, C. Fotakis, and N. Tavernarakis, PLoS One 9e84431 (2014).
[Crossref]

Peyriéras, N.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, Science 329, 967 (2010).
[Crossref]

Pfisterer, S. G.

G. Bautista, S. G. Pfisterer, M. J. Huttunen, S. Ranjan, K. Kanerva, E. Ikonen, and M. Kauranen, Biophys. J. 107, 2230 (2014).
[Crossref]

Pillai, R. S.

Plamann, K.

Priess, J. R.

G. J. Hermann, L. K. Schroeder, C. A. Hieb, A. M. Kershner, B. M. Rabbitts, P. Fonarev, B. D. Grant, and J. R. Priess, Mol. Biol. Cell 16, 3273 (2005).
[Crossref]

Pu, Y.

S. You, H. Tu, E. J. Chaney, Y. Sun, Y. Zhao, A. J. Bower, Y. Z. Liu, M. Marjanovic, S. Sinha, Y. Pu, and S. A. Boppart, Nat. Commun. 9, 2125 (2018).
[Crossref]

Rabbitts, B. M.

G. J. Hermann, L. K. Schroeder, C. A. Hieb, A. M. Kershner, B. M. Rabbitts, P. Fonarev, B. D. Grant, and J. R. Priess, Mol. Biol. Cell 16, 3273 (2005).
[Crossref]

Ranjan, S.

G. Bautista, S. G. Pfisterer, M. J. Huttunen, S. Ranjan, K. Kanerva, E. Ikonen, and M. Kauranen, Biophys. J. 107, 2230 (2014).
[Crossref]

Reiser, K. M.

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, Biophys. J. 82, 3330 (2002).
[Crossref]

Rubenchik, A. M.

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, Biophys. J. 82, 3330 (2002).
[Crossref]

Samim, M.

L. Kontenis, M. Samim, S. Krouglov, and V. Barzda, Opt. Express 25, 13174 (2017).
[Crossref]

M. Samim, S. Krouglov, and V. Barzda, Phys. Rev. A 93, 033839(2016).
[Crossref]

Santos, A.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, Science 329, 967 (2010).
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Supplementary Material (4)

NameDescription
» Supplement 1       Supplementary figures and protocols
» Visualization 1       Animation illustrating the EOM-based XPY acquisition of P-THG images.
» Visualization 2       P-THG imaging of a multilamellar lipid vesicle (MLV) with rotating linear polarization. The image sequence illustrates the polarization dependence of the interface signal and of the birefringence-related inner THG. . Excitation power: 60 mW...
» Visualization 3       Time-lapse THG imaging of flowing endogenous microparticles in the otolith cavity of a 24 hpf zebrafish. One forming otolith is visible as a fixed structure producing strong THG. Excitation power: 100-150 mW. Axial resolution: 2µm...

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Figures (5)

Fig. 1.
Fig. 1. Contrast mechanisms in P-THG microscopy. (a) Possibility of THG in isotropic and anisotropic materials depending on sample geometry and incident polarization. The red spot represents the beam focus. (b)–(d) Typical P-THG intensity profiles from (c) the interface or (d) the volume of an anisotropic material.
Fig. 2.
Fig. 2. EOM-based P-THG. (a) Experimental setup. (b) Sequence of scanning and EOM signals for XPY acquisition. (c)–(h) Simultaneous P-SHG and P-THG imaging of a starch granule while switching between linear polarization states (c)–(e) and horizontal/circular states (f)–(h). (e)–(h) Average of individual polarization images. (c)–(f) Polarization states shown on Poincaré sphere. Scale bar 10 μm.
Fig. 3.
Fig. 3. Probing molecular order with Fourier analysis of P-THG data. (a) THG image of multilamellar lipid vesicle (MLV) from an 18-image P-THG sequence recorded with rotating linear polarizations. See Visualization 2. Scale bar 5 μm. Also shown are examples of polarization profiles and Fourier coefficients for interface and birefringence-related THG signals. (b) FT maps of the first three Fourier coefficients. (c) Masks, P-THG modulation, and molecular angle maps extracted from the data. (d) Decrease of the interface P-THG modulation amplitude measured in MLVs undergoing phase transition under heating. Left, pixel modulation histogram for a single vesicle. Right, pooled data from eight vesicles.
Fig. 4.
Fig. 4. In vivo detection of anisotropy of flowing microparticles in the zebrafish inner ear. (a) Schematic of the otic cavity in a 22 h post fertilization (hpf) zebrafish. (b) THG image of the cavity containing otolith precursor microparticles flowing at 1–50 μm/s. Scale bar 20 μm. See Visualization 3. (c) Extraction of the microparticles mean P-THG modulation. (d) Histogram of THG modulation for endogenous otolith microparticles (blue) and injected polystyrene beads (gray). The data identify that the microparticles are made of anisotropic material.
Fig. 5.
Fig. 5. Detection of birefringence with circular-linear polarization switching. (a)–(i) One-shot measurement of the anisotropy parameter C-THG/(L-THG+ C-THG) in an oil droplet (isotropic), a three-days zebrafish otolith (birefringent) and a MLV (both types of THG signals). Scale bars 5 μm. (j) Application: in vivo detection of birefringent granules in an adult C. elegans worm. Scale bar 20 μm.

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