Influence of birefringence on polarization resolved nonlinear microscopy and collagen SHG structural imaging

doi:10.1364/OE.18.014859

Influence of birefringence on polarization resolved nonlinear microscopy and collagen SHG structural imaging

Sophie Brasselet, Dora Aït-Belkacem, Alicja Gasecka, Fabiana Munhoz, Sophie Brustlein, and S. Brasselet »View Author Affiliations

Optics Express, Vol. 18, Issue 14, pp. 14859-14870 (2010)
http://dx.doi.org/10.1364/OE.18.014859

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Abstract

We analyze the influence of the anisotropy of molecular and biological samples on polarization resolved nonlinear microscopy imaging. We show in particular the detrimental influence of birefringence on Second Harmonic Generation (SHG) and Two-Photon Excited Fluorescence (TPEF) polarization resolved microscopy imaging, which, if not accounted for, can lead to an erroneous determination of the sample properties and thus to a misinterpretation of the read-out information. We propose a method to measure this birefringence and account for this effect in nonlinear polarization resolved experiments.

OCIS Codes
(190.1900) Nonlinear optics : Diagnostic applications of nonlinear optics
(180.4315) Microscopy : Nonlinear microscopy

ToC Category:
Microscopy

History
Original Manuscript: May 3, 2010
Manuscript Accepted: May 26, 2010
Published: June 28, 2010

Virtual Issues
Vol. 5, Iss. 11 Virtual Journal for Biomedical Optics

Citation
Sophie Brasselet, Dora Aït-Belkacem, Alicja Gasecka, Fabiana Munhoz, Sophie Brustlein, and S. Brasselet, "Influence of birefringence on polarization resolved nonlinear microscopy and collagen SHG structural imaging," Opt. Express 18, 14859-14870 (2010)
http://www.opticsinfobase.org/oe/abstract.cfm?URI=oe-18-14-14859

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References

J. Gannaway and C. J. R. Sheppard, “Second harmonic imaging in the scanning optical microscope,” Opt. Quantum Electron. 10, 435–439 (1978). [CrossRef]
I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J. 50, 693–712 (1986). [CrossRef] [PubMed]
M. Fl¨orsheimer, C. Radüge, H. Salmen, M. Bösch, R. Terbrack, and H. Fuchs, “In-situ imaging of Langmuir monolayers by second-harmonic microscopy,” Thin Solid Films 284, 659–662 (1996). [CrossRef]
L. Moreaux, O. Sandrea, and J. Mertz, “Membrane Imaging by Second Harmonic Generation Microscopy,” J. Opt. Soc. Am. B 17, 1685–1689 (2000). [CrossRef]
P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “3-Dimesional High-Resolution Second Harmonic Generation Imaging of Endogenous Structural Proteins in Biological Tissues,” Biophys J. 81, 493–508 (2002). [CrossRef]
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, 7081 (2003). [CrossRef] [PubMed]
M. Strupler, M. Hernest, C. Fligny, J. L. Martin, P.-L. Tharaux, and M. C. Schanne-Klein, “Second Harmonic Microscopy to Quantify Renal Interstitial Fibrosis and Arterial Remodeling,” J. Biomed. Opt. 13, 054041 (2008). [CrossRef] [PubMed]
O. Nadiarnykh, R. LaComb, M. Brewer, and P. J. Campagnola, “Second Harmonic Generation Imaging Microscopy of Ovarian Cancer,” Biophys. J. 94, 4504–4514 (2008). [PubMed]
S. W. Teng, H. Y. Tan, J. L. Peng, H. H. Lin, K. H. Kim, W. Lo, Y. Sun, W. C. Lin, S. J. Lin, S. H. Jee, P. T. C. So, and C.Y. Dong, “Multiphoton autofluorescence and second-harmonic generation (SHG) imaging of ex-vivo porcine eye,” Invest. Ophthalmol. Vis. Sci. 47, 1216–1224 (2006). [CrossRef] [PubMed]
E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben,“Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162, 500–508 (2008). [CrossRef] [PubMed]
D. Axelrod, “Carbocyanine dye orientation in red cell membrane studied by microscopic fluorescence polarization,” Biophys. J. 26, 557–573 (1979). [CrossRef] [PubMed]
J. Borejdo and S. Burlacu, “Measuring Orientation of Actin Filaments within a Cell: orientation of Actin in Intestinal Microvilli,” Biophys. J. 65, 300–309 (1993). [CrossRef] [PubMed]
M. Flörsheimer, M. Bösch, C. Brillert, M. Wierschem, and H. Fuchs, “Second-harmonic microscopy - a quantitative probe for molecular surface order,” Adv. Mater. 9, 1061-1065 (1997). [CrossRef]
C. Anceau, S. Brasselet, and J. Zyss, ”Local orientational distribution of molecular monolayers probed by nonlinear microscopy,” Chem. Phys. Lett. 411, 98–102 (2005). [CrossRef]
P. Stoller, B.M. Kim, A. M. Rubenchik, K. M. Reiser, and L. B. Da Silva, “Polarization-dependent optical second harmonic imaging of a rat-tail tendon,” J. Biomed. Opt. 7, 205–214 (2000). [CrossRef]
P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-Modulated Second Harmonic Generation in Collagen,” Biophys. J. 82, 3330–3342 (2002). [CrossRef] [PubMed]
T. Yasui, K. Sasaki, Y. Tohno, and T. Araki, “Tomographic imaging of collagen fiber orientation in human tissue using depth-resolved polarimetry of second-harmonic-generation,” Opt. Quantum Electron. 37, 1397–1408 (2005). [CrossRef]
R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting Second-Harmonic Generation Images of Collagen I Fibrils,” Biophys. J. 88, 1377-1386 (2005). [CrossRef]
S. Yen, W. L. Chen, H. Y. Wu, F. C. Li, W. Lo, S. J. Lin, S. H. Jee, Y. F. Chen, P. T. C. So, and C. Y. Dong, “Collagen Thermal denaturation study with high resolution second harmonic generation imaging and polarization optical microscopy,” Biophys. J. 91, 2620–2625 (2006). [CrossRef]
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S. Psilodimitrakopoulos, S. I. C. O. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, “In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy,” J. Biomed. Opt. 14, 014001 (2009). [CrossRef] [PubMed]
A. Gasecka, T.-J. Han, C. Favard, B. R. Cho, and S. Brasselet, “Quantitative imaging of molecular order in lipid membranes using two-photon fuorescence polarimetry,” Biophys. J. 97, 2854–2862 (2009). [CrossRef] [PubMed]
A. Gasecka, L.-Q. Dieu, D. Bruehviler, and S. Brasselet, “Probing molecular order in zeolite L inclusion compounds using two-photon fluorescence polarimetric microscoy,” J. Phys. Chem. B 114, 4192–4198 (2010). [CrossRef] [PubMed]
V. Le Floc’h, S. Brasselet, J.-F. Roch, and J. Zyss, “Monitoring of orientation in molecular ensembles by polarization sensitive nonlinear microscopy,” J. Phys. Chem. B 107, 12403–12410 (2003). [CrossRef]
S. Brasselet, V. Le Floc’h, F. Treussart, J.-F. Roch, J. Zyss, E. Botzung-Appert, and A. Ibanez, “In situ diagnostics of the crystalline nature of single organic nanocrystals by nonlinear microscopy,” Phys. Rev. Lett. 92, 207401–204405 (2004). [CrossRef] [PubMed]
K. Komorowska, S. Brasselet, J. Zyss, L. Pourlsen, M. Jazdzyk, H. J. Egelhaaf, J. Gierschner, and M. Hanack, “Nanometric scale investigation of the nonlinear efficiency of perhydrotriphynylene inclusion compounds,” Chem. Phys. 318, 12–20 (2005). [CrossRef]
S. Brasselet, and J. Zyss, “Nonlinear polarimetry of molecular crystals down to the nanoscale,” C. R. Physique 8, 165–179 (2007). [CrossRef]
P. Sch¨on, F. Munhoz, A. Gasecka, S. Brustlein, and S. Brasselet, “Polarization distortion effects in polarimetric two-photon microscopy,” Opt. Express 16, 20891–20901 (2008). [CrossRef] [PubMed]
B. Richards, and E. Wolf, “Electromagnetic Diffraction in Optical Systems. II. Structure of the Image Field in an Aplanatic System, ” Proc. R. Soc. London Ser. A. 253, 358–379 (1959). [CrossRef]
E. Y. S. Yew, and C. R. J. Sheppard, “Effects of axial field components on second harmonic generation microscopy, ” Opt. Express 14, 1167–1174 (2006). [CrossRef] [PubMed]
N. Sandeau, L. L. Xuan, D. Chauvat, C. Zhou, J. F. Roch, and S. Brasselet, “ Defocused imaging of second harmonic generation from a single nanocrystal,” Opt. Express 15, 16051–16060 (2007). [CrossRef] [PubMed]
P. Schön, M. Behrndt, D. Ait-Belkacem, H. Rigneault, and S. Brasselet, “Polarization and Phase Pulse Shaping applied to Structural Contrast in Nonlinear Microscopy Imaging,” Phys. Rev. A 81, 013809 (2010). [CrossRef]
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C. E. Bigelow, and T. H. Foster, “Confocal fluorescence polarization microscopy in turbid media: Effects of scattering-induced depolarisation,” J. Opt. Soc. Am. A 23, 2932 (2006). [CrossRef]
I. Ledoux, C. Lepers, A. Prigaud, J. Badan, and J. Zyss, “Linear and nonlinear optical properties of N-4-nitrophenyl L-prolinol single crystals,” Opt. Commun. 80, 149–154 (1990). [CrossRef]
F. P. Bolin, L. E. Preuss, R. C. Taylor, and R. J. Ference, “Refractive index of some mammalian tissues using a fiber optic cladding method,” Appl. Opt. 28, 2297–2303 (1989). [CrossRef] [PubMed]
D. T. Poh, “Examination of refractive index of human epidermis in-vitro and in-vivo.,” Proc. Inter. Conf. Lasers. 96, 118–125 (1996).

Ait-Belkacem, D.
Amat-Roldan, I.
Anceau, C.
Araki, T.
Artigas, D.
Axelrod, D.
Badan, J.
Baffet, G.
Behrndt, M.
Bembi, B.
Bigelow, C. E.
Bolin, F. P.
Borejdo, J.
Bösch, M.
Brasselet, S.
Brewer, M.
Brillert, C.
Bruehviler, D.
Brustlein, S.
Burlacu, S.
Campagnola, P. J.
Celliers, P. M.
Chauvat, D.
Chen, W. L.
Chen, Y. F.
Chien, Y. H.
Cho, B. R.
Czapiga, M.
Da Silva, L. B.
Dainty, C.
Deutsch, M.
Dieu, L.-Q.
Dombeck, D. A.
Dong, C. Y.
Dong, C.Y.
Egelhaaf, H. J.
Favard, C.
Ference, R. J.
Fl¨orsheimer, M.
Fligny, C.
Flörsheimer, M.
Foster, T. H.
Freund, I.
Fuchs, H.
Gailhouste, L.
Gannaway, J.
Gasecka, A.
Gierschner, J.
Han, T.-J.
Hanack, M.
Hernest, M.
Hoppe, P. E.
Hwu, W. L.
Hyman, B. T.
Ingelsson, M.
Jazdzyk, M.
Jee, S. H.
Kasischke, K. A.
Kim, B.M.
Kim, K. H.
Komorowska, K.
LaComb, R.
Lara, D.
Le Grand, Y.
Ledoux, I.
Lepers, C.
Li, F. C.
Lin, H. H.
Lin, S. J.
Lin, W. C.
Lo, W.
Loza-Alvarez, P.
Malone, C. J.
Martin, J. L.
Mertz, J.
Millard, A. C.
Mohler, W. A.
Moreaux, L.
Munhoz, F.
Nadiarnykh, O.
Odin, C.
Peng, J. L.
Pittis, M. G.
Plotz, P.
Poh, D. T.
Pourlsen, L.
Preuss, L. E.
Prigaud, A.
Psilodimitrakopoulos, S.
Raben, N.
Radüge, C.
Ralston, E.
Recher, G.
Reiser, K. M.
Renault, A.
Richards, B.
Rigneault, H.
Roch, J. F.
Rouéde, D.
Rubenchik, A. M.
Salmen, H.
Sandeau, N.
Sandrea, O.
Santos, S. I. C. O.
Sasaki, K.
Sch¨on, P.
Schanne-Klein, M. C.
Schön, P.
Schwartz, O.
Sheppard, C. J. R.
Sheppard, C. R. J.
So, P. T. C.
Sprecher, A.
Stoller, P.
Strupler, M.
Sun, Y.
Swaim, B.
Tan, H. Y.
Taylor, R. C.
Teng, S. W.
Terasaki, M.
Terbrack, R.
Tharaux, P.-L.
Thayil, A. K. N.
Tiaho, F.
Tohno, Y.
Vishwasrao, H. D.
Webb, W. W.
Wierschem, M.
Williams, R. M.
Wolf, E.
Wu, H. Y.
Xuan, L. L.
Yasui, T.
Yen, S.
Yew, E. Y. S.
Zhou, C.
Zipfel, W. R.
Zyss, J.

Adv. Mater.

M. Flörsheimer, M. Bösch, C. Brillert, M. Wierschem, and H. Fuchs, “Second-harmonic microscopy - a quantitative probe for molecular surface order,” Adv. Mater. 9, 1061-1065 (1997). [CrossRef]

Appl. Opt.

Biophys J.

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “3-Dimesional High-Resolution Second Harmonic Generation Imaging of Endogenous Structural Proteins in Biological Tissues,” Biophys J. 81, 493–508 (2002). [CrossRef]

Biophys. J.

O. Nadiarnykh, R. LaComb, M. Brewer, and P. J. Campagnola, “Second Harmonic Generation Imaging Microscopy of Ovarian Cancer,” Biophys. J. 94, 4504–4514 (2008). [PubMed]
I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J. 50, 693–712 (1986). [CrossRef] [PubMed]
D. Axelrod, “Carbocyanine dye orientation in red cell membrane studied by microscopic fluorescence polarization,” Biophys. J. 26, 557–573 (1979). [CrossRef] [PubMed]
J. Borejdo and S. Burlacu, “Measuring Orientation of Actin Filaments within a Cell: orientation of Actin in Intestinal Microvilli,” Biophys. J. 65, 300–309 (1993). [CrossRef] [PubMed]
P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-Modulated Second Harmonic Generation in Collagen,” Biophys. J. 82, 3330–3342 (2002). [CrossRef] [PubMed]
R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting Second-Harmonic Generation Images of Collagen I Fibrils,” Biophys. J. 88, 1377-1386 (2005). [CrossRef]
S. Yen, W. L. Chen, H. Y. Wu, F. C. Li, W. Lo, S. J. Lin, S. H. Jee, Y. F. Chen, P. T. C. So, and C. Y. Dong, “Collagen Thermal denaturation study with high resolution second harmonic generation imaging and polarization optical microscopy,” Biophys. J. 91, 2620–2625 (2006). [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 fuorescence polarimetry,” Biophys. J. 97, 2854–2862 (2009). [CrossRef] [PubMed]

C. R. Physique

S. Brasselet, and J. Zyss, “Nonlinear polarimetry of molecular crystals down to the nanoscale,” C. R. Physique 8, 165–179 (2007). [CrossRef]

Chem. Phys.

K. Komorowska, S. Brasselet, J. Zyss, L. Pourlsen, M. Jazdzyk, H. J. Egelhaaf, J. Gierschner, and M. Hanack, “Nanometric scale investigation of the nonlinear efficiency of perhydrotriphynylene inclusion compounds,” Chem. Phys. 318, 12–20 (2005). [CrossRef]

Chem. Phys. Lett.

C. Anceau, S. Brasselet, and J. Zyss, ”Local orientational distribution of molecular monolayers probed by nonlinear microscopy,” Chem. Phys. Lett. 411, 98–102 (2005). [CrossRef]

Invest. Ophthalmol. Vis. Sci.

S. W. Teng, H. Y. Tan, J. L. Peng, H. H. Lin, K. H. Kim, W. Lo, Y. Sun, W. C. Lin, S. J. Lin, S. H. Jee, P. T. C. So, and C.Y. Dong, “Multiphoton autofluorescence and second-harmonic generation (SHG) imaging of ex-vivo porcine eye,” Invest. Ophthalmol. Vis. Sci. 47, 1216–1224 (2006). [CrossRef] [PubMed]

J. Biomed. Opt.

P. Stoller, B.M. Kim, A. M. Rubenchik, K. M. Reiser, and L. B. Da Silva, “Polarization-dependent optical second harmonic imaging of a rat-tail tendon,” J. Biomed. Opt. 7, 205–214 (2000). [CrossRef]
S. Psilodimitrakopoulos, S. I. C. O. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, “In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy,” J. Biomed. Opt. 14, 014001 (2009). [CrossRef] [PubMed]
M. Strupler, M. Hernest, C. Fligny, J. L. Martin, P.-L. Tharaux, and M. C. Schanne-Klein, “Second Harmonic Microscopy to Quantify Renal Interstitial Fibrosis and Arterial Remodeling,” J. Biomed. Opt. 13, 054041 (2008). [CrossRef] [PubMed]

J. Microsc.

C. Odin, Y. Le Grand, A. Renault, L. Gailhouste, and G. Baffet, “Orientation fields of nonlinear biological fibrils by second harmonic generation microscopy,” J. Microsc. 229, 32–38 (2008). [CrossRef] [PubMed]

J. Opt. Soc. Am. A

C. E. Bigelow, and T. H. Foster, “Confocal fluorescence polarization microscopy in turbid media: Effects of scattering-induced depolarisation,” J. Opt. Soc. Am. A 23, 2932 (2006). [CrossRef]

J. Opt. Soc. Am. B

L. Moreaux, O. Sandrea, and J. Mertz, “Membrane Imaging by Second Harmonic Generation Microscopy,” J. Opt. Soc. Am. B 17, 1685–1689 (2000). [CrossRef]

J. Phys. Chem. B

A. Gasecka, L.-Q. Dieu, D. Bruehviler, and S. Brasselet, “Probing molecular order in zeolite L inclusion compounds using two-photon fluorescence polarimetric microscoy,” J. Phys. Chem. B 114, 4192–4198 (2010). [CrossRef] [PubMed]
V. Le Floc’h, S. Brasselet, J.-F. Roch, and J. Zyss, “Monitoring of orientation in molecular ensembles by polarization sensitive nonlinear microscopy,” J. Phys. Chem. B 107, 12403–12410 (2003). [CrossRef]

J. Struct. Biol.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben,“Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162, 500–508 (2008). [CrossRef] [PubMed]

Opt. Commun.

I. Ledoux, C. Lepers, A. Prigaud, J. Badan, and J. Zyss, “Linear and nonlinear optical properties of N-4-nitrophenyl L-prolinol single crystals,” Opt. Commun. 80, 149–154 (1990). [CrossRef]

Opt. Express

Opt. Quantum Electron.

T. Yasui, K. Sasaki, Y. Tohno, and T. Araki, “Tomographic imaging of collagen fiber orientation in human tissue using depth-resolved polarimetry of second-harmonic-generation,” Opt. Quantum Electron. 37, 1397–1408 (2005). [CrossRef]
J. Gannaway and C. J. R. Sheppard, “Second harmonic imaging in the scanning optical microscope,” Opt. Quantum Electron. 10, 435–439 (1978). [CrossRef]

Phys. Rev. A

P. Schön, M. Behrndt, D. Ait-Belkacem, H. Rigneault, and S. Brasselet, “Polarization and Phase Pulse Shaping applied to Structural Contrast in Nonlinear Microscopy Imaging,” Phys. Rev. A 81, 013809 (2010). [CrossRef]

Phys. Rev. Lett.

S. Brasselet, V. Le Floc’h, F. Treussart, J.-F. Roch, J. Zyss, E. Botzung-Appert, and A. Ibanez, “In situ diagnostics of the crystalline nature of single organic nanocrystals by nonlinear microscopy,” Phys. Rev. Lett. 92, 207401–204405 (2004). [CrossRef] [PubMed]

Proc. Inter. Conf. Lasers.

D. T. Poh, “Examination of refractive index of human epidermis in-vitro and in-vivo.,” Proc. Inter. Conf. Lasers. 96, 118–125 (1996).

Proc. Natl. Acad. Sci. U.S.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, 7081 (2003). [CrossRef] [PubMed]

Proc. R. Soc. London Ser. A.

B. Richards, and E. Wolf, “Electromagnetic Diffraction in Optical Systems. II. Structure of the Image Field in an Aplanatic System, ” Proc. R. Soc. London Ser. A. 253, 358–379 (1959). [CrossRef]

Thin Solid Films

M. Fl¨orsheimer, C. Radüge, H. Salmen, M. Bösch, R. Terbrack, and H. Fuchs, “In-situ imaging of Langmuir monolayers by second-harmonic microscopy,” Thin Solid Films 284, 659–662 (1996). [CrossRef]

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[1] J. Gannaway and C. J. R. Sheppard, “Second harmonic imaging in the scanning optical microscope,” Opt. Quantum Electron. 10, 435–439 (1978). [CrossRef]

[2] I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J. 50, 693–712 (1986). [CrossRef] [PubMed]

[3] M. Fl¨orsheimer, C. Radüge, H. Salmen, M. Bösch, R. Terbrack, and H. Fuchs, “In-situ imaging of Langmuir monolayers by second-harmonic microscopy,” Thin Solid Films 284, 659–662 (1996). [CrossRef]

[4] L. Moreaux, O. Sandrea, and J. Mertz, “Membrane Imaging by Second Harmonic Generation Microscopy,” J. Opt. Soc. Am. B 17, 1685–1689 (2000). [CrossRef]

[5] P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “3-Dimesional High-Resolution Second Harmonic Generation Imaging of Endogenous Structural Proteins in Biological Tissues,” Biophys J. 81, 493–508 (2002). [CrossRef]

[6] 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, 7081 (2003). [CrossRef] [PubMed]

[7] M. Strupler, M. Hernest, C. Fligny, J. L. Martin, P.-L. Tharaux, and M. C. Schanne-Klein, “Second Harmonic Microscopy to Quantify Renal Interstitial Fibrosis and Arterial Remodeling,” J. Biomed. Opt. 13, 054041 (2008). [CrossRef] [PubMed]

[8] O. Nadiarnykh, R. LaComb, M. Brewer, and P. J. Campagnola, “Second Harmonic Generation Imaging Microscopy of Ovarian Cancer,” Biophys. J. 94, 4504–4514 (2008). [PubMed]

[9] S. W. Teng, H. Y. Tan, J. L. Peng, H. H. Lin, K. H. Kim, W. Lo, Y. Sun, W. C. Lin, S. J. Lin, S. H. Jee, P. T. C. So, and C.Y. Dong, “Multiphoton autofluorescence and second-harmonic generation (SHG) imaging of ex-vivo porcine eye,” Invest. Ophthalmol. Vis. Sci. 47, 1216–1224 (2006). [CrossRef] [PubMed]

[10] E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben,“Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162, 500–508 (2008). [CrossRef] [PubMed]

[11] D. Axelrod, “Carbocyanine dye orientation in red cell membrane studied by microscopic fluorescence polarization,” Biophys. J. 26, 557–573 (1979). [CrossRef] [PubMed]

[12] J. Borejdo and S. Burlacu, “Measuring Orientation of Actin Filaments within a Cell: orientation of Actin in Intestinal Microvilli,” Biophys. J. 65, 300–309 (1993). [CrossRef] [PubMed]

[13] M. Flörsheimer, M. Bösch, C. Brillert, M. Wierschem, and H. Fuchs, “Second-harmonic microscopy - a quantitative probe for molecular surface order,” Adv. Mater. 9, 1061-1065 (1997). [CrossRef]

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Influence of birefringence on polarization resolved nonlinear microscopy and collagen SHG structural imaging

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