Abstract

Comparing the SHG image formation for thin sections of tail tendon fascia and skeletal muscle fascia, we demonstrate that the forward (F) and backward (B) SHG images are vastly different. In addition, despite the different arrangement of the collagen Type I fibrillar architecture forming these two fascias, their ratios of forward over backward signal (F/B) are nearly equal. SHG images of thick tissue blocks of the fascia-muscle unit show only backward features, as opposed to SHG images of tissue blocks of the fascia-tendon unit. These images are an amalgamation of forward and backward features due to the backscattering of forward components within tendon. These forward features disappear when this tissue block is immersed in glycerol as backscattering is hereby suppressed.

© 2007 Optical Society of America

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K. Svoboda and R. Yasuda, "Principles of two-photon excitation microscopy and its applications to neuroscience," Neuron. 50,823-839 (2006).
[CrossRef] [PubMed]

K. W. Dunn and P. A. Young, "Principles of multiphoton microscopy," Nephron Exp Nephrol. 103, 33-40 (2006).
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S. Zhuo, J. Chen, T. Luo, and D. Zou, "Multimode nonlinear optical imaging of the dermis in ex vivo human skin based on the combination of multichannel mode and Lambda mode," Opt. Express 14,7810-7820 (2006).
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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. 90,693-703 (2006).
[CrossRef]

T. A. Theodossiou, C. Thrasivoulou, C. Ekwobi, and D. L. Becker, "Second harmonic generation confocal microscopy of collagen type I from rat tendon cryosection," Biophys. J. 91,4665-4677 (2006).
[CrossRef] [PubMed]

P. P. Provenzano and R. Jr. Vanderby, "Collagen fibril morphology and organization: implications for force transmission in ligaments and tendon," Matrix Biol. 25,71-84 (2006).
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D. Débarre, W. Suppato, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, "Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy," Nat. Meth. 3,47-53 (2006).
[CrossRef]

2005 (4)

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Coté, C. P. Lin, and X. S. Xie, "Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy," Proc. Natl. Acad. Sci. USA 102,16807-16812 (2005).
[CrossRef] [PubMed]

B. Chan, C. Amann, A. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. Kochevar, and R. Redmond, "Photochemical repair of Achilles tendon rupture in a rat model," J. Surg. Res. 124,274-279 (2005).
[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]

F. Helmchen and W. Denk, "Deep tissue two-photon microscopy," Nat. Meth. 2,932-940 (2005).
[CrossRef]

2004 (3)

2003 (5)

A. T. Yeh, B. Choi, J. S. Nelson, and B. J. Tromberg, "Reversible dissociation of collagen in tissues," J. Invest. Dermatol. 121,1332-1335 (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. 9,796-800 (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. USA 100,7075-7080 (2003).
[CrossRef] [PubMed]

C. Stociek, O. Garaschuk, K. Holthoff, and A. Konnerth, "In vivo two-photon calcium imaging of neuronal networks," Proc. Natl. Acad. Sci. USA 100,7319-7324 (2003).
[CrossRef]

P. J. Campagnola and L. M. Loew, "Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms," Nat. Biotechnol. 21, 1356-1360 (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. USA 99,11014-11019 (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. 82,493-508 (2002).
[CrossRef]

2001 (2)

L. Moreaux, O. Sandre, S. Charpak, M. Blanchard-Desce, and J. Mertz, "Coherent scattering in multi-harmonic light microscopy," Biophys. J. 80,1568-1574 (2001).
[CrossRef] [PubMed]

J. Mertz and L. Moreaux, "Second-harmonic generation by focused excitation of inhomogeneously distributed scatterers," Opt. Comm. 196, 325-330 (2001).
[CrossRef]

2000 (1)

1998 (2)

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

G. Marquez, L. V. Wang, S.-P. Lin, J. A. Schwartz, and S. L. Thomsen, "Anisotropy in the absorption and scattering spectra of chicken breast tissue," App. Opt. 37,798-804 (1998).
[CrossRef]

1995 (1)

I. S. Saidi, S. L. Jacques, and F. K. Tittel, "Mie and Rayleigh modeling of visible-light scattering in neonatal skin," App. Opt. 34,7410-7418 (1995).
[CrossRef]

1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, "Two-photon laser scanning microscopy," Science 248,73-76 (1990).
[CrossRef] [PubMed]

1980 (1)

N. B. Grover and S. Shoshan, "Three-dimensional organization of collagen fibres in tendon," Tissue cell. 12,523-528 (1980).
[CrossRef] [PubMed]

1979 (1)

S. Roth and I. Freund, "Second harmonic generation in collagen," J. Chem. Phys. 70,1637-1643 (1979).
[CrossRef]

Amann, C.

B. Chan, C. Amann, A. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. Kochevar, and R. Redmond, "Photochemical repair of Achilles tendon rupture in a rat model," J. Surg. Res. 124,274-279 (2005).
[CrossRef] [PubMed]

Beaurepaire, E.

D. Débarre, W. Suppato, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, "Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy," Nat. Meth. 3,47-53 (2006).
[CrossRef]

T. Boulesteix, E. Beaurepaire, M.-P. Sauviat, and M.-C. Schanne-Klein, "Second-harmonic microscopy of unstained living cardiac myocytes: measurements of sarcomere length with 20-nm accuracy," Opt. Lett. 29,2031-2033 (2004).
[CrossRef] [PubMed]

Becker, D. L.

T. A. Theodossiou, C. Thrasivoulou, C. Ekwobi, and D. L. Becker, "Second harmonic generation confocal microscopy of collagen type I from rat tendon cryosection," Biophys. J. 91,4665-4677 (2006).
[CrossRef] [PubMed]

Blanchard-Desce, M.

L. Moreaux, O. Sandre, S. Charpak, M. Blanchard-Desce, and J. Mertz, "Coherent scattering in multi-harmonic light microscopy," Biophys. J. 80,1568-1574 (2001).
[CrossRef] [PubMed]

L. Moreaux, O. Sandre, M. Blanchard-Desce, and J. Mertz, "Membrane imaging by simultaneous second-harmonic generation and two-photon microscopy," Opt. Lett. 25,320-322 (2000).
[CrossRef]

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. 9,796-800 (2003).
[CrossRef] [PubMed]

Boulesteix, T.

Brown, E.

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. 9,796-800 (2003).
[CrossRef] [PubMed]

Campagnola, P. J.

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. 90,693-703 (2006).
[CrossRef]

P. J. Campagnola and L. M. Loew, "Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms," Nat. Biotechnol. 21, 1356-1360 (2003).
[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. 82,493-508 (2002).
[CrossRef]

Centonze, V. E.

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

Chan, B.

B. Chan, C. Amann, A. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. Kochevar, and R. Redmond, "Photochemical repair of Achilles tendon rupture in a rat model," J. Surg. Res. 124,274-279 (2005).
[CrossRef] [PubMed]

Charpak, S.

L. Moreaux, O. Sandre, S. Charpak, M. Blanchard-Desce, and J. Mertz, "Coherent scattering in multi-harmonic light microscopy," Biophys. J. 80,1568-1574 (2001).
[CrossRef] [PubMed]

Chen, J.

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, "Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy," Biophys. J. 86,3914-3922 (2004).
[CrossRef] [PubMed]

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, "Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy," Biophys. J. 86,3914-3922 (2004).
[CrossRef] [PubMed]

Chen, Z.

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, "Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy," Biophys. J. 86,3914-3922 (2004).
[CrossRef] [PubMed]

Choi, B.

A. T. Yeh, B. Choi, J. S. Nelson, and B. J. Tromberg, "Reversible dissociation of collagen in tissues," J. Invest. Dermatol. 121,1332-1335 (2003).
[CrossRef] [PubMed]

Christie, 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. USA 100,7075-7080 (2003).
[CrossRef] [PubMed]

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, "Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy," Biophys. J. 86,3914-3922 (2004).
[CrossRef] [PubMed]

Combettes, L.

D. Débarre, W. Suppato, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, "Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy," Nat. Meth. 3,47-53 (2006).
[CrossRef]

Coté, D.

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Coté, C. P. Lin, and X. S. Xie, "Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy," Proc. Natl. Acad. Sci. USA 102,16807-16812 (2005).
[CrossRef] [PubMed]

Débarre, D.

D. Débarre, W. Suppato, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, "Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy," Nat. Meth. 3,47-53 (2006).
[CrossRef]

Denk, W.

F. Helmchen and W. Denk, "Deep tissue two-photon microscopy," Nat. Meth. 2,932-940 (2005).
[CrossRef]

W. Denk, J. H. Strickler, and W. W. Webb, "Two-photon laser scanning microscopy," Science 248,73-76 (1990).
[CrossRef] [PubMed]

diTomaso, E.

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. 9,796-800 (2003).
[CrossRef] [PubMed]

Dunn, K. W.

K. W. Dunn and P. A. Young, "Principles of multiphoton microscopy," Nephron Exp Nephrol. 103, 33-40 (2006).
[CrossRef]

Ekwobi, C.

T. A. Theodossiou, C. Thrasivoulou, C. Ekwobi, and D. L. Becker, "Second harmonic generation confocal microscopy of collagen type I from rat tendon cryosection," Biophys. J. 91,4665-4677 (2006).
[CrossRef] [PubMed]

Evans, C. L.

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Coté, C. P. Lin, and X. S. Xie, "Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy," Proc. Natl. Acad. Sci. USA 102,16807-16812 (2005).
[CrossRef] [PubMed]

Fabre, A.

D. Débarre, W. Suppato, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, "Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy," Nat. Meth. 3,47-53 (2006).
[CrossRef]

Freund, I.

S. Roth and I. Freund, "Second harmonic generation in collagen," J. Chem. Phys. 70,1637-1643 (1979).
[CrossRef]

Garaschuk, O.

C. Stociek, O. Garaschuk, K. Holthoff, and A. Konnerth, "In vivo two-photon calcium imaging of neuronal networks," Proc. Natl. Acad. Sci. USA 100,7319-7324 (2003).
[CrossRef]

Grover, N. B.

N. B. Grover and S. Shoshan, "Three-dimensional organization of collagen fibres in tendon," Tissue cell. 12,523-528 (1980).
[CrossRef] [PubMed]

Helmchen, F.

F. Helmchen and W. Denk, "Deep tissue two-photon microscopy," Nat. Meth. 2,932-940 (2005).
[CrossRef]

Holthoff, K.

C. Stociek, O. Garaschuk, K. Holthoff, and A. Konnerth, "In vivo two-photon calcium imaging of neuronal networks," Proc. Natl. Acad. Sci. USA 100,7319-7324 (2003).
[CrossRef]

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. 82,493-508 (2002).
[CrossRef]

Hyman, B. T.

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. USA 100,7075-7080 (2003).
[CrossRef] [PubMed]

Jacques, S. L.

I. S. Saidi, S. L. Jacques, and F. K. Tittel, "Mie and Rayleigh modeling of visible-light scattering in neonatal skin," App. Opt. 34,7410-7418 (1995).
[CrossRef]

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. 9,796-800 (2003).
[CrossRef] [PubMed]

Jiang, Y.

Jr, R.

P. P. Provenzano and R. Jr. Vanderby, "Collagen fibril morphology and organization: implications for force transmission in ligaments and tendon," Matrix Biol. 25,71-84 (2006).
[CrossRef]

Kochevar, I.

B. Chan, C. Amann, A. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. Kochevar, and R. Redmond, "Photochemical repair of Achilles tendon rupture in a rat model," J. Surg. Res. 124,274-279 (2005).
[CrossRef] [PubMed]

Konnerth, A.

C. Stociek, O. Garaschuk, K. Holthoff, and A. Konnerth, "In vivo two-photon calcium imaging of neuronal networks," Proc. Natl. Acad. Sci. USA 100,7319-7324 (2003).
[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, "Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy," Biophys. J. 86,3914-3922 (2004).
[CrossRef] [PubMed]

Lin, C. P.

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Coté, C. P. Lin, and X. S. Xie, "Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy," Proc. Natl. Acad. Sci. USA 102,16807-16812 (2005).
[CrossRef] [PubMed]

Lin, S.-P.

G. Marquez, L. V. Wang, S.-P. Lin, J. A. Schwartz, and S. L. Thomsen, "Anisotropy in the absorption and scattering spectra of chicken breast tissue," App. Opt. 37,798-804 (1998).
[CrossRef]

Loew, L. M.

P. J. Campagnola and L. M. Loew, "Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms," Nat. Biotechnol. 21, 1356-1360 (2003).
[CrossRef] [PubMed]

Luo, T.

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. 82,493-508 (2002).
[CrossRef]

Marquez, G.

G. Marquez, L. V. Wang, S.-P. Lin, J. A. Schwartz, and S. L. Thomsen, "Anisotropy in the absorption and scattering spectra of chicken breast tissue," App. Opt. 37,798-804 (1998).
[CrossRef]

McKee, T.

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. 9,796-800 (2003).
[CrossRef] [PubMed]

Mertz, J.

J. Mertz and L. Moreaux, "Second-harmonic generation by focused excitation of inhomogeneously distributed scatterers," Opt. Comm. 196, 325-330 (2001).
[CrossRef]

L. Moreaux, O. Sandre, S. Charpak, M. Blanchard-Desce, and J. Mertz, "Coherent scattering in multi-harmonic light microscopy," Biophys. J. 80,1568-1574 (2001).
[CrossRef] [PubMed]

L. Moreaux, O. Sandre, M. Blanchard-Desce, and J. Mertz, "Membrane imaging by simultaneous second-harmonic generation and two-photon microscopy," Opt. Lett. 25,320-322 (2000).
[CrossRef]

Millard, A. C.

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. 90,693-703 (2006).
[CrossRef]

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. 82,493-508 (2002).
[CrossRef]

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. 90,693-703 (2006).
[CrossRef]

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. 82,493-508 (2002).
[CrossRef]

Moreaux, L.

L. Moreaux, O. Sandre, S. Charpak, M. Blanchard-Desce, and J. Mertz, "Coherent scattering in multi-harmonic light microscopy," Biophys. J. 80,1568-1574 (2001).
[CrossRef] [PubMed]

J. Mertz and L. Moreaux, "Second-harmonic generation by focused excitation of inhomogeneously distributed scatterers," Opt. Comm. 196, 325-330 (2001).
[CrossRef]

L. Moreaux, O. Sandre, M. Blanchard-Desce, and J. Mertz, "Membrane imaging by simultaneous second-harmonic generation and two-photon microscopy," Opt. Lett. 25,320-322 (2000).
[CrossRef]

Nelson, J. S.

A. T. Yeh, B. Choi, J. S. Nelson, and B. J. Tromberg, "Reversible dissociation of collagen in tissues," J. Invest. Dermatol. 121,1332-1335 (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. USA 100,7075-7080 (2003).
[CrossRef] [PubMed]

Pena, A. M.

D. Débarre, W. Suppato, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, "Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy," Nat. Meth. 3,47-53 (2006).
[CrossRef]

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. 90,693-703 (2006).
[CrossRef]

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. 9,796-800 (2003).
[CrossRef] [PubMed]

Potma, E. O.

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Coté, C. P. Lin, and X. S. Xie, "Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy," Proc. Natl. Acad. Sci. USA 102,16807-16812 (2005).
[CrossRef] [PubMed]

Provenzano, P. P.

P. P. Provenzano and R. Jr. Vanderby, "Collagen fibril morphology and organization: implications for force transmission in ligaments and tendon," Matrix Biol. 25,71-84 (2006).
[CrossRef]

Puoris’haag, M.

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Coté, C. P. Lin, and X. S. Xie, "Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy," Proc. Natl. Acad. Sci. USA 102,16807-16812 (2005).
[CrossRef] [PubMed]

Redmond, R.

B. Chan, C. Amann, A. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. Kochevar, and R. Redmond, "Photochemical repair of Achilles tendon rupture in a rat model," J. Surg. Res. 124,274-279 (2005).
[CrossRef] [PubMed]

Roth, S.

S. Roth and I. Freund, "Second harmonic generation in collagen," J. Chem. Phys. 70,1637-1643 (1979).
[CrossRef]

Saidi, I. S.

I. S. Saidi, S. L. Jacques, and F. K. Tittel, "Mie and Rayleigh modeling of visible-light scattering in neonatal skin," App. Opt. 34,7410-7418 (1995).
[CrossRef]

Sandre, O.

L. Moreaux, O. Sandre, S. Charpak, M. Blanchard-Desce, and J. Mertz, "Coherent scattering in multi-harmonic light microscopy," Biophys. J. 80,1568-1574 (2001).
[CrossRef] [PubMed]

L. Moreaux, O. Sandre, M. Blanchard-Desce, and J. Mertz, "Membrane imaging by simultaneous second-harmonic generation and two-photon microscopy," Opt. Lett. 25,320-322 (2000).
[CrossRef]

Sauviat, M.-P.

Schanne-Klein, M.-C.

D. Débarre, W. Suppato, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, "Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy," Nat. Meth. 3,47-53 (2006).
[CrossRef]

T. Boulesteix, E. Beaurepaire, M.-P. Sauviat, and M.-C. Schanne-Klein, "Second-harmonic microscopy of unstained living cardiac myocytes: measurements of sarcomere length with 20-nm accuracy," Opt. Lett. 29,2031-2033 (2004).
[CrossRef] [PubMed]

Schwartz, J. A.

G. Marquez, L. V. Wang, S.-P. Lin, J. A. Schwartz, and S. L. Thomsen, "Anisotropy in the absorption and scattering spectra of chicken breast tissue," App. Opt. 37,798-804 (1998).
[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. 9,796-800 (2003).
[CrossRef] [PubMed]

Shoshan, S.

N. B. Grover and S. Shoshan, "Three-dimensional organization of collagen fibres in tendon," Tissue cell. 12,523-528 (1980).
[CrossRef] [PubMed]

Smink, D.

B. Chan, C. Amann, A. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. Kochevar, and R. Redmond, "Photochemical repair of Achilles tendon rupture in a rat model," J. Surg. Res. 124,274-279 (2005).
[CrossRef] [PubMed]

Stociek, C.

C. Stociek, O. Garaschuk, K. Holthoff, and A. Konnerth, "In vivo two-photon calcium imaging of neuronal networks," Proc. Natl. Acad. Sci. USA 100,7319-7324 (2003).
[CrossRef]

Strickler, J. H.

W. Denk, J. H. Strickler, and W. W. Webb, "Two-photon laser scanning microscopy," Science 248,73-76 (1990).
[CrossRef] [PubMed]

Sun, C.-K.

S.-W. Chu, S.-Y. Chen, G.-W. Chern, T. H. Tsai, Y. C. Chen, B.-L. Lin, and C.-K. Sun, "Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy," Biophys. J. 86,3914-3922 (2004).
[CrossRef] [PubMed]

Suppato, W.

D. Débarre, W. Suppato, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, "Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy," Nat. Meth. 3,47-53 (2006).
[CrossRef]

Svoboda, K.

K. Svoboda and R. Yasuda, "Principles of two-photon excitation microscopy and its applications to neuroscience," Neuron. 50,823-839 (2006).
[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. 82,493-508 (2002).
[CrossRef]

Theodossiou, T. A.

T. A. Theodossiou, C. Thrasivoulou, C. Ekwobi, and D. L. Becker, "Second harmonic generation confocal microscopy of collagen type I from rat tendon cryosection," Biophys. J. 91,4665-4677 (2006).
[CrossRef] [PubMed]

Thomsen, S. L.

G. Marquez, L. V. Wang, S.-P. Lin, J. A. Schwartz, and S. L. Thomsen, "Anisotropy in the absorption and scattering spectra of chicken breast tissue," App. Opt. 37,798-804 (1998).
[CrossRef]

Thrasivoulou, C.

T. A. Theodossiou, C. Thrasivoulou, C. Ekwobi, and D. L. Becker, "Second harmonic generation confocal microscopy of collagen type I from rat tendon cryosection," Biophys. J. 91,4665-4677 (2006).
[CrossRef] [PubMed]

Title, C.

B. Chan, C. Amann, A. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. Kochevar, and R. Redmond, "Photochemical repair of Achilles tendon rupture in a rat model," J. Surg. Res. 124,274-279 (2005).
[CrossRef] [PubMed]

Tittel, F. K.

I. S. Saidi, S. L. Jacques, and F. K. Tittel, "Mie and Rayleigh modeling of visible-light scattering in neonatal skin," App. Opt. 34,7410-7418 (1995).
[CrossRef]

Tomov, I.

Tordjmann, T.

D. Débarre, W. Suppato, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, "Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy," Nat. Meth. 3,47-53 (2006).
[CrossRef]

Tromberg, B. J.

A. T. Yeh, B. Choi, J. S. Nelson, and B. J. Tromberg, "Reversible dissociation of collagen in tissues," J. Invest. Dermatol. 121,1332-1335 (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. USA 99,11014-11019 (2002).
[CrossRef] [PubMed]

Tsai, T. H.

S.-W. Chu, S.-Y. Chen, G.-W. Chern, T. H. Tsai, Y. C. Chen, B.-L. Lin, and C.-K. Sun, "Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy," Biophys. J. 86,3914-3922 (2004).
[CrossRef] [PubMed]

Wang, L. V.

G. Marquez, L. V. Wang, S.-P. Lin, J. A. Schwartz, and S. L. Thomsen, "Anisotropy in the absorption and scattering spectra of chicken breast tissue," App. Opt. 37,798-804 (1998).
[CrossRef]

Wang, Y.

Webb, W. W.

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]

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. USA 100,7075-7080 (2003).
[CrossRef] [PubMed]

W. Denk, J. H. Strickler, and W. W. Webb, "Two-photon laser scanning microscopy," Science 248,73-76 (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. 75,2015-2024 (1998).
[CrossRef] [PubMed]

Williams, R. M.

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]

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. USA 100,7075-7080 (2003).
[CrossRef] [PubMed]

Xie, X. S.

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Coté, C. P. Lin, and X. S. Xie, "Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy," Proc. Natl. Acad. Sci. USA 102,16807-16812 (2005).
[CrossRef] [PubMed]

Yaroslavsky, A.

B. Chan, C. Amann, A. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. Kochevar, and R. Redmond, "Photochemical repair of Achilles tendon rupture in a rat model," J. Surg. Res. 124,274-279 (2005).
[CrossRef] [PubMed]

Yasuda, R.

K. Svoboda and R. Yasuda, "Principles of two-photon excitation microscopy and its applications to neuroscience," Neuron. 50,823-839 (2006).
[CrossRef] [PubMed]

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. USA 99,11014-11019 (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. 121,1332-1335 (2003).
[CrossRef] [PubMed]

Young, P. A.

K. W. Dunn and P. A. Young, "Principles of multiphoton microscopy," Nephron Exp Nephrol. 103, 33-40 (2006).
[CrossRef]

Zarins, B.

B. Chan, C. Amann, A. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. Kochevar, and R. Redmond, "Photochemical repair of Achilles tendon rupture in a rat model," J. Surg. Res. 124,274-279 (2005).
[CrossRef] [PubMed]

Zhuo, S.

Zipfel, W. R.

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]

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. USA 100,7075-7080 (2003).
[CrossRef] [PubMed]

Zou, D.

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. USA 99,11014-11019 (2002).
[CrossRef] [PubMed]

App. Opt. (2)

G. Marquez, L. V. Wang, S.-P. Lin, J. A. Schwartz, and S. L. Thomsen, "Anisotropy in the absorption and scattering spectra of chicken breast tissue," App. Opt. 37,798-804 (1998).
[CrossRef]

I. S. Saidi, S. L. Jacques, and F. K. Tittel, "Mie and Rayleigh modeling of visible-light scattering in neonatal skin," App. Opt. 34,7410-7418 (1995).
[CrossRef]

Biophys. J. (7)

L. Moreaux, O. Sandre, S. Charpak, M. Blanchard-Desce, and J. Mertz, "Coherent scattering in multi-harmonic light microscopy," Biophys. J. 80,1568-1574 (2001).
[CrossRef] [PubMed]

T. A. Theodossiou, C. Thrasivoulou, C. Ekwobi, and D. L. Becker, "Second harmonic generation confocal microscopy of collagen type I from rat tendon cryosection," Biophys. J. 91,4665-4677 (2006).
[CrossRef] [PubMed]

V. E. Centonze and J. G. White, "Multiphoton excitation provides optical sections from deeper within scattering specimens than confocal imaging," Biophys. J. 75,2015-2024 (1998).
[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.-W. Chu, S.-Y. Chen, G.-W. Chern, T. H. Tsai, Y. C. Chen, B.-L. Lin, and C.-K. Sun, "Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy," Biophys. J. 86,3914-3922 (2004).
[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. 90,693-703 (2006).
[CrossRef]

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. 82,493-508 (2002).
[CrossRef]

J. Chem. Phys. (1)

S. Roth and I. Freund, "Second harmonic generation in collagen," J. Chem. Phys. 70,1637-1643 (1979).
[CrossRef]

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. 121,1332-1335 (2003).
[CrossRef] [PubMed]

J. Surg. Res. (1)

B. Chan, C. Amann, A. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. Kochevar, and R. Redmond, "Photochemical repair of Achilles tendon rupture in a rat model," J. Surg. Res. 124,274-279 (2005).
[CrossRef] [PubMed]

Matrix Biol. (1)

P. P. Provenzano and R. Jr. Vanderby, "Collagen fibril morphology and organization: implications for force transmission in ligaments and tendon," Matrix Biol. 25,71-84 (2006).
[CrossRef]

Nat. Biotechnol. (1)

P. J. Campagnola and L. M. Loew, "Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms," Nat. Biotechnol. 21, 1356-1360 (2003).
[CrossRef] [PubMed]

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. 9,796-800 (2003).
[CrossRef] [PubMed]

Nat. Meth. (2)

F. Helmchen and W. Denk, "Deep tissue two-photon microscopy," Nat. Meth. 2,932-940 (2005).
[CrossRef]

D. Débarre, W. Suppato, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M.-C. Schanne-Klein, and E. Beaurepaire, "Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy," Nat. Meth. 3,47-53 (2006).
[CrossRef]

Nephron Exp Nephrol. (1)

K. W. Dunn and P. A. Young, "Principles of multiphoton microscopy," Nephron Exp Nephrol. 103, 33-40 (2006).
[CrossRef]

Neuron. (1)

K. Svoboda and R. Yasuda, "Principles of two-photon excitation microscopy and its applications to neuroscience," Neuron. 50,823-839 (2006).
[CrossRef] [PubMed]

Opt. Comm. (1)

J. Mertz and L. Moreaux, "Second-harmonic generation by focused excitation of inhomogeneously distributed scatterers," Opt. Comm. 196, 325-330 (2001).
[CrossRef]

Opt. Express (1)

Opt. Lett. (3)

Proc. Natl. Acad. Sci. USA (4)

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Coté, C. P. Lin, and X. S. Xie, "Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy," Proc. Natl. Acad. Sci. USA 102,16807-16812 (2005).
[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. USA 99,11014-11019 (2002).
[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. USA 100,7075-7080 (2003).
[CrossRef] [PubMed]

C. Stociek, O. Garaschuk, K. Holthoff, and A. Konnerth, "In vivo two-photon calcium imaging of neuronal networks," Proc. Natl. Acad. Sci. USA 100,7319-7324 (2003).
[CrossRef]

Science (1)

W. Denk, J. H. Strickler, and W. W. Webb, "Two-photon laser scanning microscopy," Science 248,73-76 (1990).
[CrossRef] [PubMed]

Tissue cell. (1)

N. B. Grover and S. Shoshan, "Three-dimensional organization of collagen fibres in tendon," Tissue cell. 12,523-528 (1980).
[CrossRef] [PubMed]

Other (2)

W. S. Rasband, ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, h7ttp://rsb.info.nih.gov/ij/ (1997-2007).

R. W. Boyd, Nonlinear optics (Academic Press, London, 2003), pp. 87-99.

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Figures (3)

Fig. 1.
Fig. 1.

SHG images of thin sections (∼10 microns) of collagen arrays. (a) Forward and (b) backward fascia-muscle. (c) Forward and (d) backward fascia-tendon.

Fig. 2.
Fig. 2.

SHG images of fascia within thick tissue block. (a) Fascia-muscle, (b) Fascia-tendon.

Fig. 3.
Fig. 3.

SHG image of fascia-tendon tissue block immersed in glycerol.

Tables (1)

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Table 1. Summary of our experimental results. F/B is the ratio of forward (F) over backward signal (B) for thin tissue sections (∼10 microns thickness) of fascia. T/B is the ratio of backward signal for thick tissue (T), fascia-muscle and fascia-tendon blocks, and backward signal (B) of thin tissue sections.

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