Abstract

We report the implementation of fast Interferometric Second Harmonic Generation (I-SHG) microscopy to study the polarity of non-centrosymmetric structures in biological tissues. Using a sample quartz plate, we calibrate the spatially varying phase shift introduced by the laser scanning system. Compensating this phase shift allows us to retrieve the correct phase distribution in periodically poled lithium niobate, used as a model sample. Finally, we used fast interferometric second harmonic generation microscopy to acquire phase images in tendon. Our results show that the method exposed here, using a laser scanning system, allows to recover the polarity of collagen fibrils, similarly to standard I-SHG (using a sample scanning system), but with an imaging time about 40 times shorter.

© 2016 Optical Society of America

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    [Crossref]

2015 (3)

S. Bancelin, B. Lynch, C. Bonod-Bidaud, G. Ducourthial, S. Psilodimitrakopoulos, P. Dokládal, J.-M. Allain, M.-C. Schanne-Klein, and F. Ruggiero, “Ex vivo multiscale quantitation of skin biomechanics in wild-type and genetically-modified mice using multiphoton microscopy,” Sci. Rep. 5, 17635 (2015).
[Crossref] [PubMed]

M.-A. Houle, C.-A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Légaré, “Analysis of forward and backward Second Harmonic Generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref] [PubMed]

C.-A. Couture, S. Bancelin, J. Van der Kolk, K. Popov, M. Rivard, K. Légaré, G. Martel, H. Richard, C. Brown, S. Laverty, L. Ramunno, and F. Légaré, “Impact of collagen fibrils polarity on second harmonic generation microscopy,” Biophys. J. 109(12), 2501–2510 (2015).
[Crossref] [PubMed]

2014 (2)

M. Rivard, K. Popov, C.-A. Couture, M. Laliberté, A. Bertrand-Grenier, F. Martin, H. Pépin, C. P. Pfeffer, C. Brown, L. Ramunno, and F. Légaré, “Imaging the noncentrosymmetric structural organization of tendon with Interferometric Second Harmonic Generation microscopy,” J. Biophotonics 7(8), 638–646 (2014).
[Crossref] [PubMed]

S. Bancelin, C. Aimé, I. Gusachenko, L. Kowalczuk, G. Latour, T. Coradin, and M.-C. Schanne-Klein, “Determination of collagen fibril size via absolute measurements of second-harmonic generation signals,” Nat. Commun. 5, 4920 (2014).
[Crossref] [PubMed]

2013 (2)

M. Rivard, C.-A. Couture, A. K. Miri, M. Laliberté, A. Bertrand-Grenier, L. Mongeau, and F. Légaré, “Imaging the bipolarity of myosin filaments with Interferometric Second Harmonic Generation microscopy,” Biomed. Opt. Express 4(10), 2078–2086 (2013).
[Crossref] [PubMed]

Y. Han, V. Raghunathan, R. R. Feng, H. Maekawa, C. Y. Chung, Y. Feng, E. O. Potma, and N. H. Ge, “Mapping molecular orientation with phase sensitive vibrationally resonant sum-frequency generation microscopy,” J. Phys. Chem. B 117(20), 6149–6156 (2013).
[Crossref] [PubMed]

2012 (3)

G. Latour, I. Gusachenko, L. Kowalczuk, I. Lamarre, and M.-C. Schanne-Klein, “In vivo structural imaging of the cornea by polarization-resolved second harmonic microscopy,” Biomed. Opt. Express 3(1), 1–15 (2012).
[Crossref] [PubMed]

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, “Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure,” Nat. Protoc. 7(4), 654–669 (2012).
[Crossref] [PubMed]

I. Gusachenko, V. Tran, Y. Goulam Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-resolved second-harmonic generation in tendon upon mechanical stretching,” Biophys. J. 102(9), 2220–2229 (2012).
[Crossref] [PubMed]

2011 (2)

A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
[Crossref] [PubMed]

M. Rivard, M. Laliberté, A. Bertrand-Grenier, C. Harnagea, C. P. Pfeffer, M. Vallières, Y. St-Pierre, A. Pignolet, M. A. El Khakani, and F. Légaré, “The structural origin of second harmonic generation in fascia,” Biomed. Opt. Express 2(1), 26–36 (2011).
[Crossref] [PubMed]

2010 (4)

2009 (1)

A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the second-order hyperpolarizability of the collagen triple helix and determination of its physical origin,” J. Phys. Chem. B 113(40), 13437–13445 (2009).
[Crossref] [PubMed]

2008 (3)

R. LaComb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, “Phase matching considerations in second harmonic generation from tissues: effects on emission directionality, conversion efficiency and observed morphology,” Opt. Commun. 281(7), 1823–1832 (2008).
[Crossref] [PubMed]

A. C. Kwan, D. A. Dombeck, and W. W. Webb, “Polarized microtubule arrays in apical dendrites and axons,” Proc. Natl. Acad. Sci. U.S.A. 105(32), 11370–11375 (2008).
[Crossref] [PubMed]

J. C. Mansfield, C. P. Winlove, J. Moger, and S. J. Matcher, “Collagen fiber arrangement in normal and diseased cartilage studied by polarization sensitive nonlinear microscopy,” J. Biomed. Opt. 13(4), 044020 (2008).
[Crossref] [PubMed]

2007 (2)

2006 (2)

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006).
[Crossref] [PubMed]

J. A. Palero, H. S. de Bruijn, A. van der Ploeg-van den Heuvel, H. J. Sterenborg, and H. C. Gerritsen, “In vivo nonlinear spectral imaging in mouse skin,” Opt. Express 14(10), 4395–4402 (2006).
[Crossref] [PubMed]

2004 (1)

2003 (5)

P. Stoller, P. M. Celliers, K. M. Reiser, and A. M. Rubenchik, “Quantitative second-harmonic generation microscopy in collagen,” Appl. Opt. 42(25), 5209–5219 (2003).
[Crossref] [PubMed]

D. A. Dombeck, K. A. Kasischke, H. D. Vishwasrao, M. Ingelsson, B. T. Hyman, and W. W. Webb, “Uniform polarity microtubule assemblies imaged in native brain tissue by second-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7081–7086 (2003).
[Crossref] [PubMed]

A. T. Yeh, B. Choi, J. S. Nelson, and B. J. Tromberg, “Reversible dissociation of collagen in tissues,” J. Invest. Dermatol. 121(6), 1332–1335 (2003).
[Crossref] [PubMed]

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003).
[Crossref] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[Crossref] [PubMed]

2002 (2)

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 99(17), 11014–11019 (2002).
[Crossref] [PubMed]

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J. 82(1), 493–508 (2002).
[Crossref] [PubMed]

2000 (2)

A. K. Dunn, V. P. Wallace, M. Coleno, M. W. Berns, and B. J. Tromberg, “Influence of optical properties on two-photon fluorescence imaging in turbid samples,” Appl. Opt. 39(7), 1194–1201 (2000).
[Crossref] [PubMed]

P. Rechsteiner, J. Hulliger, and M. Flörsheimer, “Phase-sensitive second harmonic microscopy reveals bipolar twinning of markov type molecular crystals,” Chem. Mater. 12(11), 3296–3300 (2000).
[Crossref]

1998 (1)

V. E. Centonze and J. G. White, “Multiphoton excitation provides optical sections from deeper within scattering specimens than confocal imaging,” Biophys. J. 75(4), 2015–2024 (1998).
[Crossref] [PubMed]

1996 (1)

R. Stolle, G. Marowsky, E. Schwarzberg, and G. Berkovic, “Phase measurements in nonlinear optics,” Appl. Phys. B 63(5), 491–498 (1996).
[Crossref]

1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

1986 (1)

1979 (1)

S. Roth and I. Freund, “Second harmonic generation in collagen,” J. Chem. Phys. 70(4), 1637 (1979).
[Crossref]

Aimé, C.

S. Bancelin, C. Aimé, I. Gusachenko, L. Kowalczuk, G. Latour, T. Coradin, and M.-C. Schanne-Klein, “Determination of collagen fibril size via absolute measurements of second-harmonic generation signals,” Nat. Commun. 5, 4920 (2014).
[Crossref] [PubMed]

Allain, J.-M.

S. Bancelin, B. Lynch, C. Bonod-Bidaud, G. Ducourthial, S. Psilodimitrakopoulos, P. Dokládal, J.-M. Allain, M.-C. Schanne-Klein, and F. Ruggiero, “Ex vivo multiscale quantitation of skin biomechanics in wild-type and genetically-modified mice using multiphoton microscopy,” Sci. Rep. 5, 17635 (2015).
[Crossref] [PubMed]

I. Gusachenko, V. Tran, Y. Goulam Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-resolved second-harmonic generation in tendon upon mechanical stretching,” Biophys. J. 102(9), 2220–2229 (2012).
[Crossref] [PubMed]

Auger, E.

M.-A. Houle, C.-A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Légaré, “Analysis of forward and backward Second Harmonic Generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref] [PubMed]

Bancelin, S.

M.-A. Houle, C.-A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Légaré, “Analysis of forward and backward Second Harmonic Generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref] [PubMed]

C.-A. Couture, S. Bancelin, J. Van der Kolk, K. Popov, M. Rivard, K. Légaré, G. Martel, H. Richard, C. Brown, S. Laverty, L. Ramunno, and F. Légaré, “Impact of collagen fibrils polarity on second harmonic generation microscopy,” Biophys. J. 109(12), 2501–2510 (2015).
[Crossref] [PubMed]

S. Bancelin, B. Lynch, C. Bonod-Bidaud, G. Ducourthial, S. Psilodimitrakopoulos, P. Dokládal, J.-M. Allain, M.-C. Schanne-Klein, and F. Ruggiero, “Ex vivo multiscale quantitation of skin biomechanics in wild-type and genetically-modified mice using multiphoton microscopy,” Sci. Rep. 5, 17635 (2015).
[Crossref] [PubMed]

S. Bancelin, C. Aimé, I. Gusachenko, L. Kowalczuk, G. Latour, T. Coradin, and M.-C. Schanne-Klein, “Determination of collagen fibril size via absolute measurements of second-harmonic generation signals,” Nat. Commun. 5, 4920 (2014).
[Crossref] [PubMed]

Bartels, R. A.

Barzda, V.

A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
[Crossref] [PubMed]

Beaurepaire, 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, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[Crossref] [PubMed]

Benichou, E.

A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the second-order hyperpolarizability of the collagen triple helix and determination of its physical origin,” J. Phys. Chem. B 113(40), 13437–13445 (2009).
[Crossref] [PubMed]

Berkovic, G.

R. Stolle, G. Marowsky, E. Schwarzberg, and G. Berkovic, “Phase measurements in nonlinear optics,” Appl. Phys. B 63(5), 491–498 (1996).
[Crossref]

Berns, M. W.

Bertrand-Grenier, A.

Bonod-Bidaud, C.

S. Bancelin, B. Lynch, C. Bonod-Bidaud, G. Ducourthial, S. Psilodimitrakopoulos, P. Dokládal, J.-M. Allain, M.-C. Schanne-Klein, and F. Ruggiero, “Ex vivo multiscale quantitation of skin biomechanics in wild-type and genetically-modified mice using multiphoton microscopy,” Sci. Rep. 5, 17635 (2015).
[Crossref] [PubMed]

Boucher, Y.

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003).
[Crossref] [PubMed]

Bourgine, P.

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M. Rivard, K. Popov, C.-A. Couture, M. Laliberté, A. Bertrand-Grenier, F. Martin, H. Pépin, C. P. Pfeffer, C. Brown, L. Ramunno, and F. Légaré, “Imaging the noncentrosymmetric structural organization of tendon with Interferometric Second Harmonic Generation microscopy,” J. Biophotonics 7(8), 638–646 (2014).
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E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003).
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P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J. 82(1), 493–508 (2002).
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Y. Han, V. Raghunathan, R. R. Feng, H. Maekawa, C. Y. Chung, Y. Feng, E. O. Potma, and N. H. Ge, “Mapping molecular orientation with phase sensitive vibrationally resonant sum-frequency generation microscopy,” J. Phys. Chem. B 117(20), 6149–6156 (2013).
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Coradin, T.

S. Bancelin, C. Aimé, I. Gusachenko, L. Kowalczuk, G. Latour, T. Coradin, and M.-C. Schanne-Klein, “Determination of collagen fibril size via absolute measurements of second-harmonic generation signals,” Nat. Commun. 5, 4920 (2014).
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M.-A. Houle, C.-A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Légaré, “Analysis of forward and backward Second Harmonic Generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
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C.-A. Couture, S. Bancelin, J. Van der Kolk, K. Popov, M. Rivard, K. Légaré, G. Martel, H. Richard, C. Brown, S. Laverty, L. Ramunno, and F. Légaré, “Impact of collagen fibrils polarity on second harmonic generation microscopy,” Biophys. J. 109(12), 2501–2510 (2015).
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M. Rivard, C.-A. Couture, A. K. Miri, M. Laliberté, A. Bertrand-Grenier, L. Mongeau, and F. Légaré, “Imaging the bipolarity of myosin filaments with Interferometric Second Harmonic Generation microscopy,” Biomed. Opt. Express 4(10), 2078–2086 (2013).
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D. A. Dombeck, K. A. Kasischke, H. D. Vishwasrao, M. Ingelsson, B. T. Hyman, and W. W. Webb, “Uniform polarity microtubule assemblies imaged in native brain tissue by second-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7081–7086 (2003).
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El Khakani, M. A.

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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, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
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Goulam Houssen, Y.

I. Gusachenko, V. Tran, Y. Goulam Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-resolved second-harmonic generation in tendon upon mechanical stretching,” Biophys. J. 102(9), 2220–2229 (2012).
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G. Latour, I. Gusachenko, L. Kowalczuk, I. Lamarre, and M.-C. Schanne-Klein, “In vivo structural imaging of the cornea by polarization-resolved second harmonic microscopy,” Biomed. Opt. Express 3(1), 1–15 (2012).
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A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the second-order hyperpolarizability of the collagen triple helix and determination of its physical origin,” J. Phys. Chem. B 113(40), 13437–13445 (2009).
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Y. Han, V. Raghunathan, R. R. Feng, H. Maekawa, C. Y. Chung, Y. Feng, E. O. Potma, and N. H. Ge, “Mapping molecular orientation with phase sensitive vibrationally resonant sum-frequency generation microscopy,” J. Phys. Chem. B 117(20), 6149–6156 (2013).
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Hoppe, P. E.

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J. 82(1), 493–508 (2002).
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M.-A. Houle, C.-A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Légaré, “Analysis of forward and backward Second Harmonic Generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
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Hulliger, J.

P. Rechsteiner, J. Hulliger, and M. Flörsheimer, “Phase-sensitive second harmonic microscopy reveals bipolar twinning of markov type molecular crystals,” Chem. Mater. 12(11), 3296–3300 (2000).
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D. A. Dombeck, K. A. Kasischke, H. D. Vishwasrao, M. Ingelsson, B. T. Hyman, and W. W. Webb, “Uniform polarity microtubule assemblies imaged in native brain tissue by second-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7081–7086 (2003).
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W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
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Ingelsson, M.

D. A. Dombeck, K. A. Kasischke, H. D. Vishwasrao, M. Ingelsson, B. T. Hyman, and W. W. Webb, “Uniform polarity microtubule assemblies imaged in native brain tissue by second-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7081–7086 (2003).
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Jain, R. K.

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003).
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Kaneshiro, J.

Kasischke, K. A.

D. A. Dombeck, K. A. Kasischke, H. D. Vishwasrao, M. Ingelsson, B. T. Hyman, and W. W. Webb, “Uniform polarity microtubule assemblies imaged in native brain tissue by second-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7081–7086 (2003).
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S. Bancelin, C. Aimé, I. Gusachenko, L. Kowalczuk, G. Latour, T. Coradin, and M.-C. Schanne-Klein, “Determination of collagen fibril size via absolute measurements of second-harmonic generation signals,” Nat. Commun. 5, 4920 (2014).
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G. Latour, I. Gusachenko, L. Kowalczuk, I. Lamarre, and M.-C. Schanne-Klein, “In vivo structural imaging of the cornea by polarization-resolved second harmonic microscopy,” Biomed. Opt. Express 3(1), 1–15 (2012).
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A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
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A. C. Kwan, D. A. Dombeck, and W. W. Webb, “Polarized microtubule arrays in apical dendrites and axons,” Proc. Natl. Acad. Sci. U.S.A. 105(32), 11370–11375 (2008).
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R. LaComb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, “Phase matching considerations in second harmonic generation from tissues: effects on emission directionality, conversion efficiency and observed morphology,” Opt. Commun. 281(7), 1823–1832 (2008).
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Laliberté, M.

Lamarre, I.

Latour, G.

S. Bancelin, C. Aimé, I. Gusachenko, L. Kowalczuk, G. Latour, T. Coradin, and M.-C. Schanne-Klein, “Determination of collagen fibril size via absolute measurements of second-harmonic generation signals,” Nat. Commun. 5, 4920 (2014).
[Crossref] [PubMed]

G. Latour, I. Gusachenko, L. Kowalczuk, I. Lamarre, and M.-C. Schanne-Klein, “In vivo structural imaging of the cornea by polarization-resolved second harmonic microscopy,” Biomed. Opt. Express 3(1), 1–15 (2012).
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C.-A. Couture, S. Bancelin, J. Van der Kolk, K. Popov, M. Rivard, K. Légaré, G. Martel, H. Richard, C. Brown, S. Laverty, L. Ramunno, and F. Légaré, “Impact of collagen fibrils polarity on second harmonic generation microscopy,” Biophys. J. 109(12), 2501–2510 (2015).
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Légaré, F.

C.-A. Couture, S. Bancelin, J. Van der Kolk, K. Popov, M. Rivard, K. Légaré, G. Martel, H. Richard, C. Brown, S. Laverty, L. Ramunno, and F. Légaré, “Impact of collagen fibrils polarity on second harmonic generation microscopy,” Biophys. J. 109(12), 2501–2510 (2015).
[Crossref] [PubMed]

M.-A. Houle, C.-A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Légaré, “Analysis of forward and backward Second Harmonic Generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
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M. Rivard, K. Popov, C.-A. Couture, M. Laliberté, A. Bertrand-Grenier, F. Martin, H. Pépin, C. P. Pfeffer, C. Brown, L. Ramunno, and F. Légaré, “Imaging the noncentrosymmetric structural organization of tendon with Interferometric Second Harmonic Generation microscopy,” J. Biophotonics 7(8), 638–646 (2014).
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M. Rivard, C.-A. Couture, A. K. Miri, M. Laliberté, A. Bertrand-Grenier, L. Mongeau, and F. Légaré, “Imaging the bipolarity of myosin filaments with Interferometric Second Harmonic Generation microscopy,” Biomed. Opt. Express 4(10), 2078–2086 (2013).
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C.-A. Couture, S. Bancelin, J. Van der Kolk, K. Popov, M. Rivard, K. Légaré, G. Martel, H. Richard, C. Brown, S. Laverty, L. Ramunno, and F. Légaré, “Impact of collagen fibrils polarity on second harmonic generation microscopy,” Biophys. J. 109(12), 2501–2510 (2015).
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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, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
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S. Bancelin, B. Lynch, C. Bonod-Bidaud, G. Ducourthial, S. Psilodimitrakopoulos, P. Dokládal, J.-M. Allain, M.-C. Schanne-Klein, and F. Ruggiero, “Ex vivo multiscale quantitation of skin biomechanics in wild-type and genetically-modified mice using multiphoton microscopy,” Sci. Rep. 5, 17635 (2015).
[Crossref] [PubMed]

Maekawa, H.

Y. Han, V. Raghunathan, R. R. Feng, H. Maekawa, C. Y. Chung, Y. Feng, E. O. Potma, and N. H. Ge, “Mapping molecular orientation with phase sensitive vibrationally resonant sum-frequency generation microscopy,” J. Phys. Chem. B 117(20), 6149–6156 (2013).
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Malone, C. J.

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J. 82(1), 493–508 (2002).
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J. C. Mansfield, C. P. Winlove, J. Moger, and S. J. Matcher, “Collagen fiber arrangement in normal and diseased cartilage studied by polarization sensitive nonlinear microscopy,” J. Biomed. Opt. 13(4), 044020 (2008).
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C.-A. Couture, S. Bancelin, J. Van der Kolk, K. Popov, M. Rivard, K. Légaré, G. Martel, H. Richard, C. Brown, S. Laverty, L. Ramunno, and F. Légaré, “Impact of collagen fibrils polarity on second harmonic generation microscopy,” Biophys. J. 109(12), 2501–2510 (2015).
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M. Rivard, K. Popov, C.-A. Couture, M. Laliberté, A. Bertrand-Grenier, F. Martin, H. Pépin, C. P. Pfeffer, C. Brown, L. Ramunno, and F. Légaré, “Imaging the noncentrosymmetric structural organization of tendon with Interferometric Second Harmonic Generation microscopy,” J. Biophotonics 7(8), 638–646 (2014).
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Matcher, S. J.

J. C. Mansfield, C. P. Winlove, J. Moger, and S. J. Matcher, “Collagen fiber arrangement in normal and diseased cartilage studied by polarization sensitive nonlinear microscopy,” J. Biomed. Opt. 13(4), 044020 (2008).
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E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003).
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S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006).
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P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J. 82(1), 493–508 (2002).
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Moger, J.

J. C. Mansfield, C. P. Winlove, J. Moger, and S. J. Matcher, “Collagen fiber arrangement in normal and diseased cartilage studied by polarization sensitive nonlinear microscopy,” J. Biomed. Opt. 13(4), 044020 (2008).
[Crossref] [PubMed]

Mohler, W. A.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006).
[Crossref] [PubMed]

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J. 82(1), 493–508 (2002).
[Crossref] [PubMed]

Mongeau, L.

Moratal, C.

Nadiarnykh, O.

R. LaComb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, “Phase matching considerations in second harmonic generation from tissues: effects on emission directionality, conversion efficiency and observed morphology,” Opt. Commun. 281(7), 1823–1832 (2008).
[Crossref] [PubMed]

Nadiarynkh, O.

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, “Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure,” Nat. Protoc. 7(4), 654–669 (2012).
[Crossref] [PubMed]

Nelson, J. S.

A. T. Yeh, B. Choi, J. S. Nelson, and B. J. Tromberg, “Reversible dissociation of collagen in tissues,” J. Invest. Dermatol. 121(6), 1332–1335 (2003).
[Crossref] [PubMed]

Nikitin, A. Y.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[Crossref] [PubMed]

Olivier, 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, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[Crossref] [PubMed]

Olsen, B. R.

F. Légaré, C. Pfeffer, and B. R. Olsen, “The role of backscattering in SHG tissue imaging,” Biophys. J. 93(4), 1312–1320 (2007).
[Crossref] [PubMed]

Palero, J. A.

Pépin, H.

M. Rivard, K. Popov, C.-A. Couture, M. Laliberté, A. Bertrand-Grenier, F. Martin, H. Pépin, C. P. Pfeffer, C. Brown, L. Ramunno, and F. Légaré, “Imaging the noncentrosymmetric structural organization of tendon with Interferometric Second Harmonic Generation microscopy,” J. Biophotonics 7(8), 638–646 (2014).
[Crossref] [PubMed]

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, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[Crossref] [PubMed]

Pfeffer, C.

F. Légaré, C. Pfeffer, and B. R. Olsen, “The role of backscattering in SHG tissue imaging,” Biophys. J. 93(4), 1312–1320 (2007).
[Crossref] [PubMed]

Pfeffer, C. P.

M. Rivard, K. Popov, C.-A. Couture, M. Laliberté, A. Bertrand-Grenier, F. Martin, H. Pépin, C. P. Pfeffer, C. Brown, L. Ramunno, and F. Légaré, “Imaging the noncentrosymmetric structural organization of tendon with Interferometric Second Harmonic Generation microscopy,” J. Biophotonics 7(8), 638–646 (2014).
[Crossref] [PubMed]

M. Rivard, M. Laliberté, A. Bertrand-Grenier, C. Harnagea, C. P. Pfeffer, M. Vallières, Y. St-Pierre, A. Pignolet, M. A. El Khakani, and F. Légaré, “The structural origin of second harmonic generation in fascia,” Biomed. Opt. Express 2(1), 26–36 (2011).
[Crossref] [PubMed]

Pignolet, A.

Plotnikov, S.

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, “Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure,” Nat. Protoc. 7(4), 654–669 (2012).
[Crossref] [PubMed]

Plotnikov, S. V.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006).
[Crossref] [PubMed]

Pluen, A.

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003).
[Crossref] [PubMed]

Popov, K.

C.-A. Couture, S. Bancelin, J. Van der Kolk, K. Popov, M. Rivard, K. Légaré, G. Martel, H. Richard, C. Brown, S. Laverty, L. Ramunno, and F. Légaré, “Impact of collagen fibrils polarity on second harmonic generation microscopy,” Biophys. J. 109(12), 2501–2510 (2015).
[Crossref] [PubMed]

M.-A. Houle, C.-A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Légaré, “Analysis of forward and backward Second Harmonic Generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref] [PubMed]

M. Rivard, K. Popov, C.-A. Couture, M. Laliberté, A. Bertrand-Grenier, F. Martin, H. Pépin, C. P. Pfeffer, C. Brown, L. Ramunno, and F. Légaré, “Imaging the noncentrosymmetric structural organization of tendon with Interferometric Second Harmonic Generation microscopy,” J. Biophotonics 7(8), 638–646 (2014).
[Crossref] [PubMed]

Potma, E. O.

Y. Han, V. Raghunathan, R. R. Feng, H. Maekawa, C. Y. Chung, Y. Feng, E. O. Potma, and N. H. Ge, “Mapping molecular orientation with phase sensitive vibrationally resonant sum-frequency generation microscopy,” J. Phys. Chem. B 117(20), 6149–6156 (2013).
[Crossref] [PubMed]

Prent, N.

A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
[Crossref] [PubMed]

Psilodimitrakopoulos, S.

S. Bancelin, B. Lynch, C. Bonod-Bidaud, G. Ducourthial, S. Psilodimitrakopoulos, P. Dokládal, J.-M. Allain, M.-C. Schanne-Klein, and F. Ruggiero, “Ex vivo multiscale quantitation of skin biomechanics in wild-type and genetically-modified mice using multiphoton microscopy,” Sci. Rep. 5, 17635 (2015).
[Crossref] [PubMed]

Raghunathan, V.

Y. Han, V. Raghunathan, R. R. Feng, H. Maekawa, C. Y. Chung, Y. Feng, E. O. Potma, and N. H. Ge, “Mapping molecular orientation with phase sensitive vibrationally resonant sum-frequency generation microscopy,” J. Phys. Chem. B 117(20), 6149–6156 (2013).
[Crossref] [PubMed]

Ramunno, L.

M.-A. Houle, C.-A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Légaré, “Analysis of forward and backward Second Harmonic Generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref] [PubMed]

C.-A. Couture, S. Bancelin, J. Van der Kolk, K. Popov, M. Rivard, K. Légaré, G. Martel, H. Richard, C. Brown, S. Laverty, L. Ramunno, and F. Légaré, “Impact of collagen fibrils polarity on second harmonic generation microscopy,” Biophys. J. 109(12), 2501–2510 (2015).
[Crossref] [PubMed]

M. Rivard, K. Popov, C.-A. Couture, M. Laliberté, A. Bertrand-Grenier, F. Martin, H. Pépin, C. P. Pfeffer, C. Brown, L. Ramunno, and F. Légaré, “Imaging the noncentrosymmetric structural organization of tendon with Interferometric Second Harmonic Generation microscopy,” J. Biophotonics 7(8), 638–646 (2014).
[Crossref] [PubMed]

Recher, G.

Rechsteiner, P.

P. Rechsteiner, J. Hulliger, and M. Flörsheimer, “Phase-sensitive second harmonic microscopy reveals bipolar twinning of markov type molecular crystals,” Chem. Mater. 12(11), 3296–3300 (2000).
[Crossref]

Reiser, K. M.

Richard, H.

C.-A. Couture, S. Bancelin, J. Van der Kolk, K. Popov, M. Rivard, K. Légaré, G. Martel, H. Richard, C. Brown, S. Laverty, L. Ramunno, and F. Légaré, “Impact of collagen fibrils polarity on second harmonic generation microscopy,” Biophys. J. 109(12), 2501–2510 (2015).
[Crossref] [PubMed]

Rivard, M.

C.-A. Couture, S. Bancelin, J. Van der Kolk, K. Popov, M. Rivard, K. Légaré, G. Martel, H. Richard, C. Brown, S. Laverty, L. Ramunno, and F. Légaré, “Impact of collagen fibrils polarity on second harmonic generation microscopy,” Biophys. J. 109(12), 2501–2510 (2015).
[Crossref] [PubMed]

M. Rivard, K. Popov, C.-A. Couture, M. Laliberté, A. Bertrand-Grenier, F. Martin, H. Pépin, C. P. Pfeffer, C. Brown, L. Ramunno, and F. Légaré, “Imaging the noncentrosymmetric structural organization of tendon with Interferometric Second Harmonic Generation microscopy,” J. Biophotonics 7(8), 638–646 (2014).
[Crossref] [PubMed]

M. Rivard, C.-A. Couture, A. K. Miri, M. Laliberté, A. Bertrand-Grenier, L. Mongeau, and F. Légaré, “Imaging the bipolarity of myosin filaments with Interferometric Second Harmonic Generation microscopy,” Biomed. Opt. Express 4(10), 2078–2086 (2013).
[Crossref] [PubMed]

M. Rivard, M. Laliberté, A. Bertrand-Grenier, C. Harnagea, C. P. Pfeffer, M. Vallières, Y. St-Pierre, A. Pignolet, M. A. El Khakani, and F. Légaré, “The structural origin of second harmonic generation in fascia,” Biomed. Opt. Express 2(1), 26–36 (2011).
[Crossref] [PubMed]

Roth, S.

S. Roth and I. Freund, “Second harmonic generation in collagen,” J. Chem. Phys. 70(4), 1637 (1979).
[Crossref]

Rouède, D.

Rubenchik, A. M.

Ruggiero, F.

S. Bancelin, B. Lynch, C. Bonod-Bidaud, G. Ducourthial, S. Psilodimitrakopoulos, P. Dokládal, J.-M. Allain, M.-C. Schanne-Klein, and F. Ruggiero, “Ex vivo multiscale quantitation of skin biomechanics in wild-type and genetically-modified mice using multiphoton microscopy,” Sci. Rep. 5, 17635 (2015).
[Crossref] [PubMed]

Sandkuijl, D.

A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
[Crossref] [PubMed]

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, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[Crossref] [PubMed]

Savy, T.

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, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[Crossref] [PubMed]

Schanne-Klein, M.-C.

S. Bancelin, B. Lynch, C. Bonod-Bidaud, G. Ducourthial, S. Psilodimitrakopoulos, P. Dokládal, J.-M. Allain, M.-C. Schanne-Klein, and F. Ruggiero, “Ex vivo multiscale quantitation of skin biomechanics in wild-type and genetically-modified mice using multiphoton microscopy,” Sci. Rep. 5, 17635 (2015).
[Crossref] [PubMed]

S. Bancelin, C. Aimé, I. Gusachenko, L. Kowalczuk, G. Latour, T. Coradin, and M.-C. Schanne-Klein, “Determination of collagen fibril size via absolute measurements of second-harmonic generation signals,” Nat. Commun. 5, 4920 (2014).
[Crossref] [PubMed]

I. Gusachenko, V. Tran, Y. Goulam Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-resolved second-harmonic generation in tendon upon mechanical stretching,” Biophys. J. 102(9), 2220–2229 (2012).
[Crossref] [PubMed]

G. Latour, I. Gusachenko, L. Kowalczuk, I. Lamarre, and M.-C. Schanne-Klein, “In vivo structural imaging of the cornea by polarization-resolved second harmonic microscopy,” Biomed. Opt. Express 3(1), 1–15 (2012).
[Crossref] [PubMed]

A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the second-order hyperpolarizability of the collagen triple helix and determination of its physical origin,” J. Phys. Chem. B 113(40), 13437–13445 (2009).
[Crossref] [PubMed]

Schlup, P.

Schwarzberg, E.

R. Stolle, G. Marowsky, E. Schwarzberg, and G. Berkovic, “Phase measurements in nonlinear optics,” Appl. Phys. B 63(5), 491–498 (1996).
[Crossref]

Seed, B.

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003).
[Crossref] [PubMed]

Shaffer, E.

So, P.

Solinas, X.

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, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[Crossref] [PubMed]

Sterenborg, H. J.

Stolle, R.

R. Stolle, G. Marowsky, E. Schwarzberg, and G. Berkovic, “Phase measurements in nonlinear optics,” Appl. Phys. B 63(5), 491–498 (1996).
[Crossref]

Stoller, P.

St-Pierre, Y.

Strickler, J. H.

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Terasaki, M.

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J. 82(1), 493–508 (2002).
[Crossref] [PubMed]

Tiaho, F.

Townsend, S. S.

R. LaComb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, “Phase matching considerations in second harmonic generation from tissues: effects on emission directionality, conversion efficiency and observed morphology,” Opt. Commun. 281(7), 1823–1832 (2008).
[Crossref] [PubMed]

Tran, V.

I. Gusachenko, V. Tran, Y. Goulam Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-resolved second-harmonic generation in tendon upon mechanical stretching,” Biophys. J. 102(9), 2220–2229 (2012).
[Crossref] [PubMed]

Tromberg, B. J.

A. T. Yeh, B. Choi, J. S. Nelson, and B. J. Tromberg, “Reversible dissociation of collagen in tissues,” J. Invest. Dermatol. 121(6), 1332–1335 (2003).
[Crossref] [PubMed]

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 99(17), 11014–11019 (2002).
[Crossref] [PubMed]

A. K. Dunn, V. P. Wallace, M. Coleno, M. W. Berns, and B. J. Tromberg, “Influence of optical properties on two-photon fluorescence imaging in turbid samples,” Appl. Opt. 39(7), 1194–1201 (2000).
[Crossref] [PubMed]

Tuer, A. E.

A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
[Crossref] [PubMed]

Uesu, Y.

Vallières, M.

Van der Kolk, J.

C.-A. Couture, S. Bancelin, J. Van der Kolk, K. Popov, M. Rivard, K. Légaré, G. Martel, H. Richard, C. Brown, S. Laverty, L. Ramunno, and F. Légaré, “Impact of collagen fibrils polarity on second harmonic generation microscopy,” Biophys. J. 109(12), 2501–2510 (2015).
[Crossref] [PubMed]

M.-A. Houle, C.-A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Légaré, “Analysis of forward and backward Second Harmonic Generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
[Crossref] [PubMed]

van der Ploeg-van den Heuvel, A.

Veilleux, I.

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, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science 329(5994), 967–971 (2010).
[Crossref] [PubMed]

Vishwasrao, H. D.

D. A. Dombeck, K. A. Kasischke, H. D. Vishwasrao, M. Ingelsson, B. T. Hyman, and W. W. Webb, “Uniform polarity microtubule assemblies imaged in native brain tissue by second-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7081–7086 (2003).
[Crossref] [PubMed]

Wallace, V. P.

Webb, W. W.

A. C. Kwan, D. A. Dombeck, and W. W. Webb, “Polarized microtubule arrays in apical dendrites and axons,” Proc. Natl. Acad. Sci. U.S.A. 105(32), 11370–11375 (2008).
[Crossref] [PubMed]

D. A. Dombeck, K. A. Kasischke, H. D. Vishwasrao, M. Ingelsson, B. T. Hyman, and W. W. Webb, “Uniform polarity microtubule assemblies imaged in native brain tissue by second-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7081–7086 (2003).
[Crossref] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[Crossref] [PubMed]

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

White, J. G.

V. E. Centonze and J. G. White, “Multiphoton excitation provides optical sections from deeper within scattering specimens than confocal imaging,” Biophys. J. 75(4), 2015–2024 (1998).
[Crossref] [PubMed]

Williams, R. M.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[Crossref] [PubMed]

Wilson, B. C.

A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
[Crossref] [PubMed]

Winlove, C. P.

J. C. Mansfield, C. P. Winlove, J. Moger, and S. J. Matcher, “Collagen fiber arrangement in normal and diseased cartilage studied by polarization sensitive nonlinear microscopy,” J. Biomed. Opt. 13(4), 044020 (2008).
[Crossref] [PubMed]

Yasufuku, K.

A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
[Crossref] [PubMed]

Yazdanfar, S.

Yeh, A.

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 99(17), 11014–11019 (2002).
[Crossref] [PubMed]

Yeh, A. T.

A. T. Yeh, B. Choi, J. S. Nelson, and B. J. Tromberg, “Reversible dissociation of collagen in tissues,” J. Invest. Dermatol. 121(6), 1332–1335 (2003).
[Crossref] [PubMed]

Zipfel, W. R.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[Crossref] [PubMed]

Zoumi, A.

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 99(17), 11014–11019 (2002).
[Crossref] [PubMed]

Appl. Opt. (2)

Appl. Phys. B (1)

R. Stolle, G. Marowsky, E. Schwarzberg, and G. Berkovic, “Phase measurements in nonlinear optics,” Appl. Phys. B 63(5), 491–498 (1996).
[Crossref]

Biomed. Opt. Express (3)

Biophys. J. (6)

F. Légaré, C. Pfeffer, and B. R. Olsen, “The role of backscattering in SHG tissue imaging,” Biophys. J. 93(4), 1312–1320 (2007).
[Crossref] [PubMed]

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006).
[Crossref] [PubMed]

I. Gusachenko, V. Tran, Y. Goulam Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-resolved second-harmonic generation in tendon upon mechanical stretching,” Biophys. J. 102(9), 2220–2229 (2012).
[Crossref] [PubMed]

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J. 82(1), 493–508 (2002).
[Crossref] [PubMed]

V. E. Centonze and J. G. White, “Multiphoton excitation provides optical sections from deeper within scattering specimens than confocal imaging,” Biophys. J. 75(4), 2015–2024 (1998).
[Crossref] [PubMed]

C.-A. Couture, S. Bancelin, J. Van der Kolk, K. Popov, M. Rivard, K. Légaré, G. Martel, H. Richard, C. Brown, S. Laverty, L. Ramunno, and F. Légaré, “Impact of collagen fibrils polarity on second harmonic generation microscopy,” Biophys. J. 109(12), 2501–2510 (2015).
[Crossref] [PubMed]

Chem. Mater. (1)

P. Rechsteiner, J. Hulliger, and M. Flörsheimer, “Phase-sensitive second harmonic microscopy reveals bipolar twinning of markov type molecular crystals,” Chem. Mater. 12(11), 3296–3300 (2000).
[Crossref]

J. Biomed. Opt. (1)

J. C. Mansfield, C. P. Winlove, J. Moger, and S. J. Matcher, “Collagen fiber arrangement in normal and diseased cartilage studied by polarization sensitive nonlinear microscopy,” J. Biomed. Opt. 13(4), 044020 (2008).
[Crossref] [PubMed]

J. Biophotonics (2)

M. Rivard, K. Popov, C.-A. Couture, M. Laliberté, A. Bertrand-Grenier, F. Martin, H. Pépin, C. P. Pfeffer, C. Brown, L. Ramunno, and F. Légaré, “Imaging the noncentrosymmetric structural organization of tendon with Interferometric Second Harmonic Generation microscopy,” J. Biophotonics 7(8), 638–646 (2014).
[Crossref] [PubMed]

M.-A. Houle, C.-A. Couture, S. Bancelin, J. Van der Kolk, E. Auger, C. Brown, K. Popov, L. Ramunno, and F. Légaré, “Analysis of forward and backward Second Harmonic Generation images to probe the nanoscale structure of collagen within bone and cartilage,” J. Biophotonics 8(11-12), 993–1001 (2015).
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J. Chem. Phys. (1)

S. Roth and I. Freund, “Second harmonic generation in collagen,” J. Chem. Phys. 70(4), 1637 (1979).
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J. Invest. Dermatol. (1)

A. T. Yeh, B. Choi, J. S. Nelson, and B. J. Tromberg, “Reversible dissociation of collagen in tissues,” J. Invest. Dermatol. 121(6), 1332–1335 (2003).
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J. Opt. Soc. Am. B (1)

J. Phys. Chem. B (3)

A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
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A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the second-order hyperpolarizability of the collagen triple helix and determination of its physical origin,” J. Phys. Chem. B 113(40), 13437–13445 (2009).
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Nat. Commun. (1)

S. Bancelin, C. Aimé, I. Gusachenko, L. Kowalczuk, G. Latour, T. Coradin, and M.-C. Schanne-Klein, “Determination of collagen fibril size via absolute measurements of second-harmonic generation signals,” Nat. Commun. 5, 4920 (2014).
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Nat. Med. (1)

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003).
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Nat. Protoc. (1)

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Opt. Commun. (1)

R. LaComb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, “Phase matching considerations in second harmonic generation from tissues: effects on emission directionality, conversion efficiency and observed morphology,” Opt. Commun. 281(7), 1823–1832 (2008).
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Opt. Express (4)

Opt. Lett. (2)

Proc. Natl. Acad. Sci. U.S.A. (4)

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Sci. Rep. (1)

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Science (2)

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Figures (6)

Fig. 1
Fig. 1 Experimental setup used for fast I-SHG microscopy. a) Experimental setup and b) characterization of the glass plate used to extract the relative phase.
Fig. 2
Fig. 2 Subtraction stack obtained in PPLN sample. Red and green colors stand respectively for negative and positive values after the subtraction. Therefore, red and green colors reflect the sign of the cosine term in Eq. (1) and denote π phase shifted sample phase. Scale bar: 50µm.
Fig. 3
Fig. 3 Impact of the sample scanning in phase measurement. a) Phase calibration in a sample quartz plate. b) Histogram of the relative phase measured in the sample quartz plate. c) Profile of the subtracted images, calculated along the black dashed line in (a), as a function of the distance from the center of the circular pattern, for various reference phases. d) Interferometric contrast in the field of view. Scale bars: 50µm.
Fig. 4
Fig. 4 Phase correction in PPLN. Phase a) image and b) histogram measured in PLLN sample before correction. Phase c) image and d) histogram after correction of the phase shift introduced by the microscope. Phase e) image and f) histogram measured in PPLN sample using the former sample scanning I-SHG setup. The red straight lines in d) and f) are bi-Gaussian fittings of the phase distributions used to retrieve the peaks width σ. Scale bars: 25µm.
Fig. 5
Fig. 5 Fast I-SHG imaging of a mice tail tendon. a) and b) Phase images before and after correction respectively. c) Corrected phase distribution obtained in tendon. Red straight line is the bi-Gaussian fitting used to retrieve the peaks width σ.
Fig. 6
Fig. 6 Impact of the reference phase step on the peak width determination. a) Peak width measured in tendon as a function of the reference phase step used for the image acquisition. b) Ratio of fibrils pointing in opposite direction (f ratio) as a function of the reference phase step. Black squares and red circles correspond to the first peak (centered at –π/2) and the second peak (centered at π/2) respectively. Red and black straight lines indicate the more precise value obtained with a 15° reference phase step.

Equations (2)

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I( φ ref )I( φ ref +π )=4 I ref I samp cos( φ samp φ ref )
f= N( + χ (2) ) N( + χ (2) )+N( χ (2) )

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