Abstract

Fascia tissue is rich in collagen type I proteins and can be imaged by second harmonic generation (SHG) microscopy. While identifying the overall alignment of the collagen fibrils is evident from those images, the tridimensional structural origin for the observation of SHG signal is more complex than it apparently seems. Those images reveal that the noncentrosymmetric (piezoelectric) structures are distributed heterogeneously on spatial dimensions inferior to the resolution provided by the nonlinear optical microscope (sub-micron). Using piezoresponse force microscopy (PFM), we show that an individual collagen fibril has a noncentrosymmetric structural organization. Fibrils are found to be arranged in nano-domains where the anisotropic axis is preserved along the fibrillar axis, while across the collagen sheets, the phase of the second order nonlinear susceptibility is changing by 180 degrees between adjacent nano-domains. This complex architecture of noncentrosymmetric nano-domains governs the coherent addition of 2ω light within the focal volume and the observed features in the SHG images taken in fascia.

© 2010 OSA

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  35. J. Hulliger, “Connective tissue polarity unraveled by a Markov-chain mechanism of collagen fibril segment self-assembly,” Biophys. J. 84(6), 3501–3507 (2003).
    [CrossRef] [PubMed]
  36. I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum frequency vibrational spectroscopy: the molecular origins of the optical second-order nonlinearity of collagen,” Biophys. J. 93(12), 4433–4444 (2007).
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2010 (3)

A. F. Pegoraro, A. D. Slepkov, A. Ridsdale, J. P. Pezacki, and A. Stolow, “Single laser source for multimodal coherent anti-Stokes Raman scattering microscopy,” Appl. Opt. 49(25), F10–F17 (2010).
[CrossRef] [PubMed]

C. Harnagea, M. Vallières, C. P. Pfeffer, D. Wu, B. R. Olsen, A. Pignolet, F. Légaré, and A. Gruverman, “Two-dimensional nanoscale structural and functional imaging in individual collagen type I fibrils,” Biophys. J. 98(12), 3070–3077 (2010).
[CrossRef] [PubMed]

A. Kholkin, N. Amdursky, I. Bdikin, E. Gazit, and G. Rosenman, “Strong piezoelectricity in bioinspired peptide nanotubes,” ACS Nano 4(2), 610–614 (2010).
[CrossRef] [PubMed]

2009 (4)

M. Minary-Jolandan and M.-F. Yu, “Uncovering Nanoscale Electromechanical Heterogeneity in the Subfibrillar Structure of Collagen Fibrils Responsible for the Piezoelectricity of Bone,” ACS Nano 3(7), 1859–1863 (2009).
[CrossRef] [PubMed]

P. Nandakumar, A. Kovalev, and A. Volkmer, “Vibrational imaging based on stimulated Raman scattering microscopy,” N. J. Phys. 11(3), 033026 (2009).
[CrossRef]

S.-W. Chu, S.-P. Tai, T.-M. Liu, C.-K. Sun, and C. H. Lin, “Selective imaging in second-harmonic-generation microscopy with anisotropic radiation,” J. Biomed. Opt. 14(1), 010504 (2009).
[CrossRef] [PubMed]

R. A. Rao, M. R. Mehta, S. Leithem, and K. C. Toussaint., “Quantitative analysis of forward and backward second-harmonic images of collagen fibers using Fourier transform second-harmonic-generation microscopy,” Opt. Lett. 34(24), 3779–3781 (2009).
[CrossRef] [PubMed]

2008 (6)

K. E. Kadler, A. Hill, and E. G. Canty-Laird, “Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators,” Curr. Opin. Cell Biol. 20(5), 495–501 (2008).
[CrossRef] [PubMed]

P. Bianchini and A. Diaspro, “Three-dimensional (3D) backward and forward second harmonic generation (SHG) microscopy of biological tissues,” J Biophotonics 1(6), 443–450 (2008).
[CrossRef] [PubMed]

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]

C. W. Freudiger, W. Min, B. G. Saar, S. Lu, G. R. Holtom, C. He, J. C. Tsai, J. X. Kang, and X. S. Xie, “Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy,” Science 322(5909), 1857–1861 (2008).
[CrossRef] [PubMed]

W. H. Stoothoff, B. J. Bacskai, and B. T. Hyman, “Monitoring tau-tubulin interactions utilizing second harmonic generation in living neurons,” J. Biomed. Opt. 13(6), 064039 (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 (3)

O. Nadiarnykh, R. B. Lacomb, P. J. Campagnola, and W. A. Mohler, “Coherent and incoherent SHG in fibrillar cellulose matrices,” Opt. Express 15(6), 3348–3360 (2007).
[CrossRef] [PubMed]

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

I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum frequency vibrational spectroscopy: the molecular origins of the optical second-order nonlinearity of collagen,” Biophys. J. 93(12), 4433–4444 (2007).
[CrossRef] [PubMed]

2006 (4)

C. Harnagea, A. Pignolet, M. Alexe, and D. Hesse, “Higher-order electromechanical response of thin films by contact resonance piezoresponse force microscopy,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 53(12), 2309–2322 (2006).
[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 cryosections,” Biophys. J. 91(12), 4665–4677 (2006).
[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]

D. Débarre, W. Supatto, 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. Methods 3(1), 47–53 (2006).
[CrossRef] [PubMed]

2005 (5)

H. Wang, Y. Fu, P. Zickmund, R. Shi, and J. X. Cheng, “Coherent anti-stokes Raman scattering imaging of axonal myelin in live spinal tissues,” Biophys. J. 89(1), 581–591 (2005).
[CrossRef] [PubMed]

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, 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. U.S.A. 102(46), 16807–16812 (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(2), 1377–1386 (2005).
[CrossRef] [PubMed]

A. T. Yeh, M. J. Hammer-Wilson, D. C. Van Sickle, H. P. Benton, A. Zoumi, B. J. Tromberg, and G. M. Peavy, “Nonlinear optical microscopy of articular cartilage,” Osteoarthritis Cartilage 13(4), 345–352 (2005).
[CrossRef] [PubMed]

B. P. Chan, C. Amann, A. N. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. E. Kochevar, and R. W. Redmond, “Photochemical repair of Achilles tendon rupture in a rat model,” J. Surg. Res. 124(2), 274–279 (2005).
[CrossRef] [PubMed]

2004 (3)

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(6), 3914–3922 (2004).
[CrossRef] [PubMed]

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(17), 2031–2033 (2004).
[CrossRef] [PubMed]

D. Oron, D. Yelin, E. Tal, S. Raz, R. Fachima, and Y. Silberberg, “Depth-resolved structural imaging by third-harmonic generation microscopy,” J. Struct. Biol. 147(1), 3–11 (2004).
[CrossRef] [PubMed]

2003 (4)

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]

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]

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]

J. Hulliger, “Connective tissue polarity unraveled by a Markov-chain mechanism of collagen fibril segment self-assembly,” Biophys. J. 84(6), 3501–3507 (2003).
[CrossRef] [PubMed]

2002 (2)

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]

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]

2001 (2)

A. Volkmer, J.-X. Cheng, and X. Sunney Xie, “Vibrational imaging with high sensitivity via epidetected coherent anti-Stokes Raman scattering microscopy,” Phys. Rev. Lett. 87(2), 023901 (2001).
[CrossRef]

J. Mertz and L. Moreaux, “Second-harmonic generation by focused excitation of inhomogeneously distributed scatterers,” Opt. Commun. 196(1-6), 325–330 (2001).
[CrossRef]

1998 (1)

M. F. Paige, J. K. Rainey, and M. C. Goh, “Fibrous long spacing collagen ultrastructure elucidated by atomic force microscopy,” Biophys. J. 74(6), 3211–3216 (1998).
[CrossRef] [PubMed]

1996 (1)

K. E. Kadler, D. F. Holmes, J. A. Trotter, and J. A. Chapman, “Collagen fibril formation,” Biochem. J. 316(Pt 1), 1–11 (1996).
[PubMed]

1994 (1)

D. F. Holmes, M. P. Lowe, and J. A. Chapman, “Vertebrate (chick) collagen fibrils formed in vivo can exhibit a reversal in molecular polarity,” J. Mol. Biol. 235(1), 80–83 (1994).
[CrossRef] [PubMed]

1993 (1)

D. R. Baselt, J. P. Revel, and J. D. Baldeschwieler, “Subfibrillar structure of type I collagen observed by atomic force microscopy,” Biophys. J. 65(6), 2644–2655 (1993).
[CrossRef] [PubMed]

1977 (1)

D. A. D. Parry and A. S. Craig, “Quantitative electron microscope observations of the collagen fibrils in rat-tail tendon,” Biopolymers 16(5), 1015–1031 (1977).
[CrossRef] [PubMed]

1969 (1)

K. Kühn, “The structure of collagen,” Essays Biochem. 5, 59–87 (1969).
[PubMed]

Alexe, M.

C. Harnagea, A. Pignolet, M. Alexe, and D. Hesse, “Higher-order electromechanical response of thin films by contact resonance piezoresponse force microscopy,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 53(12), 2309–2322 (2006).
[CrossRef] [PubMed]

Amann, C.

B. P. Chan, C. Amann, A. N. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. E. Kochevar, and R. W. Redmond, “Photochemical repair of Achilles tendon rupture in a rat model,” J. Surg. Res. 124(2), 274–279 (2005).
[CrossRef] [PubMed]

Amdursky, N.

A. Kholkin, N. Amdursky, I. Bdikin, E. Gazit, and G. Rosenman, “Strong piezoelectricity in bioinspired peptide nanotubes,” ACS Nano 4(2), 610–614 (2010).
[CrossRef] [PubMed]

Bacskai, B. J.

W. H. Stoothoff, B. J. Bacskai, and B. T. Hyman, “Monitoring tau-tubulin interactions utilizing second harmonic generation in living neurons,” J. Biomed. Opt. 13(6), 064039 (2008).
[CrossRef] [PubMed]

Baldeschwieler, J. D.

D. R. Baselt, J. P. Revel, and J. D. Baldeschwieler, “Subfibrillar structure of type I collagen observed by atomic force microscopy,” Biophys. J. 65(6), 2644–2655 (1993).
[CrossRef] [PubMed]

Baselt, D. R.

D. R. Baselt, J. P. Revel, and J. D. Baldeschwieler, “Subfibrillar structure of type I collagen observed by atomic force microscopy,” Biophys. J. 65(6), 2644–2655 (1993).
[CrossRef] [PubMed]

Bdikin, I.

A. Kholkin, N. Amdursky, I. Bdikin, E. Gazit, and G. Rosenman, “Strong piezoelectricity in bioinspired peptide nanotubes,” ACS Nano 4(2), 610–614 (2010).
[CrossRef] [PubMed]

Beaurepaire, E.

D. Débarre, W. Supatto, 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. Methods 3(1), 47–53 (2006).
[CrossRef] [PubMed]

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(17), 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 cryosections,” Biophys. J. 91(12), 4665–4677 (2006).
[CrossRef] [PubMed]

Benton, H. P.

A. T. Yeh, M. J. Hammer-Wilson, D. C. Van Sickle, H. P. Benton, A. Zoumi, B. J. Tromberg, and G. M. Peavy, “Nonlinear optical microscopy of articular cartilage,” Osteoarthritis Cartilage 13(4), 345–352 (2005).
[CrossRef] [PubMed]

Bianchini, P.

P. Bianchini and A. Diaspro, “Three-dimensional (3D) backward and forward second harmonic generation (SHG) microscopy of biological tissues,” J Biophotonics 1(6), 443–450 (2008).
[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]

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(6), 796–801 (2003).
[CrossRef] [PubMed]

Campagnola, P. J.

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]

O. Nadiarnykh, R. B. Lacomb, P. J. Campagnola, and W. A. Mohler, “Coherent and incoherent SHG in fibrillar cellulose matrices,” Opt. Express 15(6), 3348–3360 (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]

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]

Canty-Laird, E. G.

K. E. Kadler, A. Hill, and E. G. Canty-Laird, “Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators,” Curr. Opin. Cell Biol. 20(5), 495–501 (2008).
[CrossRef] [PubMed]

Celliers, P. M.

Chan, B. P.

B. P. Chan, C. Amann, A. N. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. E. Kochevar, and R. W. Redmond, “Photochemical repair of Achilles tendon rupture in a rat model,” J. Surg. Res. 124(2), 274–279 (2005).
[CrossRef] [PubMed]

Chapman, J. A.

K. E. Kadler, D. F. Holmes, J. A. Trotter, and J. A. Chapman, “Collagen fibril formation,” Biochem. J. 316(Pt 1), 1–11 (1996).
[PubMed]

D. F. Holmes, M. P. Lowe, and J. A. Chapman, “Vertebrate (chick) collagen fibrils formed in vivo can exhibit a reversal in molecular polarity,” J. Mol. Biol. 235(1), 80–83 (1994).
[CrossRef] [PubMed]

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(6), 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(6), 3914–3922 (2004).
[CrossRef] [PubMed]

Cheng, J. X.

H. Wang, Y. Fu, P. Zickmund, R. Shi, and J. X. Cheng, “Coherent anti-stokes Raman scattering imaging of axonal myelin in live spinal tissues,” Biophys. J. 89(1), 581–591 (2005).
[CrossRef] [PubMed]

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A. Volkmer, J.-X. Cheng, and X. Sunney Xie, “Vibrational imaging with high sensitivity via epidetected coherent anti-Stokes Raman scattering microscopy,” Phys. Rev. Lett. 87(2), 023901 (2001).
[CrossRef]

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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(6), 3914–3922 (2004).
[CrossRef] [PubMed]

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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).
[CrossRef] [PubMed]

Chu, S.-W.

S.-W. Chu, S.-P. Tai, T.-M. Liu, C.-K. Sun, and C. H. Lin, “Selective imaging in second-harmonic-generation microscopy with anisotropic radiation,” J. Biomed. Opt. 14(1), 010504 (2009).
[CrossRef] [PubMed]

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(6), 3914–3922 (2004).
[CrossRef] [PubMed]

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D. Débarre, W. Supatto, 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. Methods 3(1), 47–53 (2006).
[CrossRef] [PubMed]

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C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, 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. U.S.A. 102(46), 16807–16812 (2005).
[CrossRef] [PubMed]

Craig, A. S.

D. A. D. Parry and A. S. Craig, “Quantitative electron microscope observations of the collagen fibrils in rat-tail tendon,” Biopolymers 16(5), 1015–1031 (1977).
[CrossRef] [PubMed]

Débarre, D.

D. Débarre, W. Supatto, 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. Methods 3(1), 47–53 (2006).
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P. Bianchini and A. Diaspro, “Three-dimensional (3D) backward and forward second harmonic generation (SHG) microscopy of biological tissues,” J Biophotonics 1(6), 443–450 (2008).
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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(6), 796–801 (2003).
[CrossRef] [PubMed]

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T. A. Theodossiou, C. Thrasivoulou, C. Ekwobi, and D. L. Becker, “Second harmonic generation confocal microscopy of collagen type I from rat tendon cryosections,” Biophys. J. 91(12), 4665–4677 (2006).
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C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, 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. U.S.A. 102(46), 16807–16812 (2005).
[CrossRef] [PubMed]

Fabre, A.

D. Débarre, W. Supatto, 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. Methods 3(1), 47–53 (2006).
[CrossRef] [PubMed]

Fachima, R.

D. Oron, D. Yelin, E. Tal, S. Raz, R. Fachima, and Y. Silberberg, “Depth-resolved structural imaging by third-harmonic generation microscopy,” J. Struct. Biol. 147(1), 3–11 (2004).
[CrossRef] [PubMed]

Frank, C. W.

I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum frequency vibrational spectroscopy: the molecular origins of the optical second-order nonlinearity of collagen,” Biophys. J. 93(12), 4433–4444 (2007).
[CrossRef] [PubMed]

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C. W. Freudiger, W. Min, B. G. Saar, S. Lu, G. R. Holtom, C. He, J. C. Tsai, J. X. Kang, and X. S. Xie, “Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy,” Science 322(5909), 1857–1861 (2008).
[CrossRef] [PubMed]

Fu, Y.

H. Wang, Y. Fu, P. Zickmund, R. Shi, and J. X. Cheng, “Coherent anti-stokes Raman scattering imaging of axonal myelin in live spinal tissues,” Biophys. J. 89(1), 581–591 (2005).
[CrossRef] [PubMed]

Gazit, E.

A. Kholkin, N. Amdursky, I. Bdikin, E. Gazit, and G. Rosenman, “Strong piezoelectricity in bioinspired peptide nanotubes,” ACS Nano 4(2), 610–614 (2010).
[CrossRef] [PubMed]

Goh, M. C.

M. F. Paige, J. K. Rainey, and M. C. Goh, “Fibrous long spacing collagen ultrastructure elucidated by atomic force microscopy,” Biophys. J. 74(6), 3211–3216 (1998).
[CrossRef] [PubMed]

Gruverman, A.

C. Harnagea, M. Vallières, C. P. Pfeffer, D. Wu, B. R. Olsen, A. Pignolet, F. Légaré, and A. Gruverman, “Two-dimensional nanoscale structural and functional imaging in individual collagen type I fibrils,” Biophys. J. 98(12), 3070–3077 (2010).
[CrossRef] [PubMed]

Hammer-Wilson, M. J.

A. T. Yeh, M. J. Hammer-Wilson, D. C. Van Sickle, H. P. Benton, A. Zoumi, B. J. Tromberg, and G. M. Peavy, “Nonlinear optical microscopy of articular cartilage,” Osteoarthritis Cartilage 13(4), 345–352 (2005).
[CrossRef] [PubMed]

Harnagea, C.

C. Harnagea, M. Vallières, C. P. Pfeffer, D. Wu, B. R. Olsen, A. Pignolet, F. Légaré, and A. Gruverman, “Two-dimensional nanoscale structural and functional imaging in individual collagen type I fibrils,” Biophys. J. 98(12), 3070–3077 (2010).
[CrossRef] [PubMed]

C. Harnagea, A. Pignolet, M. Alexe, and D. Hesse, “Higher-order electromechanical response of thin films by contact resonance piezoresponse force microscopy,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 53(12), 2309–2322 (2006).
[CrossRef] [PubMed]

He, C.

C. W. Freudiger, W. Min, B. G. Saar, S. Lu, G. R. Holtom, C. He, J. C. Tsai, J. X. Kang, and X. S. Xie, “Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy,” Science 322(5909), 1857–1861 (2008).
[CrossRef] [PubMed]

Hesse, D.

C. Harnagea, A. Pignolet, M. Alexe, and D. Hesse, “Higher-order electromechanical response of thin films by contact resonance piezoresponse force microscopy,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 53(12), 2309–2322 (2006).
[CrossRef] [PubMed]

Hill, A.

K. E. Kadler, A. Hill, and E. G. Canty-Laird, “Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators,” Curr. Opin. Cell Biol. 20(5), 495–501 (2008).
[CrossRef] [PubMed]

Holmes, D. F.

K. E. Kadler, D. F. Holmes, J. A. Trotter, and J. A. Chapman, “Collagen fibril formation,” Biochem. J. 316(Pt 1), 1–11 (1996).
[PubMed]

D. F. Holmes, M. P. Lowe, and J. A. Chapman, “Vertebrate (chick) collagen fibrils formed in vivo can exhibit a reversal in molecular polarity,” J. Mol. Biol. 235(1), 80–83 (1994).
[CrossRef] [PubMed]

Holtom, G. R.

C. W. Freudiger, W. Min, B. G. Saar, S. Lu, G. R. Holtom, C. He, J. C. Tsai, J. X. Kang, and X. S. Xie, “Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy,” Science 322(5909), 1857–1861 (2008).
[CrossRef] [PubMed]

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).
[CrossRef] [PubMed]

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J. Hulliger, “Connective tissue polarity unraveled by a Markov-chain mechanism of collagen fibril segment self-assembly,” Biophys. J. 84(6), 3501–3507 (2003).
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Hyman, B. T.

W. H. Stoothoff, B. J. Bacskai, and B. T. Hyman, “Monitoring tau-tubulin interactions utilizing second harmonic generation in living neurons,” J. Biomed. Opt. 13(6), 064039 (2008).
[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]

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).
[CrossRef] [PubMed]

Kadler, K. E.

K. E. Kadler, A. Hill, and E. G. Canty-Laird, “Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators,” Curr. Opin. Cell Biol. 20(5), 495–501 (2008).
[CrossRef] [PubMed]

K. E. Kadler, D. F. Holmes, J. A. Trotter, and J. A. Chapman, “Collagen fibril formation,” Biochem. J. 316(Pt 1), 1–11 (1996).
[PubMed]

Kang, J. X.

C. W. Freudiger, W. Min, B. G. Saar, S. Lu, G. R. Holtom, C. He, J. C. Tsai, J. X. Kang, and X. S. Xie, “Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy,” Science 322(5909), 1857–1861 (2008).
[CrossRef] [PubMed]

Kholkin, A.

A. Kholkin, N. Amdursky, I. Bdikin, E. Gazit, and G. Rosenman, “Strong piezoelectricity in bioinspired peptide nanotubes,” ACS Nano 4(2), 610–614 (2010).
[CrossRef] [PubMed]

Knoesen, A.

I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum frequency vibrational spectroscopy: the molecular origins of the optical second-order nonlinearity of collagen,” Biophys. J. 93(12), 4433–4444 (2007).
[CrossRef] [PubMed]

Kochevar, I. E.

B. P. Chan, C. Amann, A. N. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. E. Kochevar, and R. W. Redmond, “Photochemical repair of Achilles tendon rupture in a rat model,” J. Surg. Res. 124(2), 274–279 (2005).
[CrossRef] [PubMed]

Kovalev, A.

P. Nandakumar, A. Kovalev, and A. Volkmer, “Vibrational imaging based on stimulated Raman scattering microscopy,” N. J. Phys. 11(3), 033026 (2009).
[CrossRef]

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K. Kühn, “The structure of collagen,” Essays Biochem. 5, 59–87 (1969).
[PubMed]

Lacomb, R.

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]

Lacomb, R. B.

Légaré, F.

C. Harnagea, M. Vallières, C. P. Pfeffer, D. Wu, B. R. Olsen, A. Pignolet, F. Légaré, and A. Gruverman, “Two-dimensional nanoscale structural and functional imaging in individual collagen type I fibrils,” Biophys. J. 98(12), 3070–3077 (2010).
[CrossRef] [PubMed]

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

Leithem, S.

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(6), 3914–3922 (2004).
[CrossRef] [PubMed]

Lin, C. H.

S.-W. Chu, S.-P. Tai, T.-M. Liu, C.-K. Sun, and C. H. Lin, “Selective imaging in second-harmonic-generation microscopy with anisotropic radiation,” J. Biomed. Opt. 14(1), 010504 (2009).
[CrossRef] [PubMed]

Lin, C. P.

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, 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. U.S.A. 102(46), 16807–16812 (2005).
[CrossRef] [PubMed]

Liu, T.-M.

S.-W. Chu, S.-P. Tai, T.-M. Liu, C.-K. Sun, and C. H. Lin, “Selective imaging in second-harmonic-generation microscopy with anisotropic radiation,” J. Biomed. Opt. 14(1), 010504 (2009).
[CrossRef] [PubMed]

Lowe, M. P.

D. F. Holmes, M. P. Lowe, and J. A. Chapman, “Vertebrate (chick) collagen fibrils formed in vivo can exhibit a reversal in molecular polarity,” J. Mol. Biol. 235(1), 80–83 (1994).
[CrossRef] [PubMed]

Lu, S.

C. W. Freudiger, W. Min, B. G. Saar, S. Lu, G. R. Holtom, C. He, J. C. Tsai, J. X. Kang, and X. S. Xie, “Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy,” Science 322(5909), 1857–1861 (2008).
[CrossRef] [PubMed]

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).
[CrossRef] [PubMed]

Mansfield, J. C.

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]

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).
[CrossRef] [PubMed]

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(6), 796–801 (2003).
[CrossRef] [PubMed]

Mehta, M. R.

Mertz, J.

J. Mertz and L. Moreaux, “Second-harmonic generation by focused excitation of inhomogeneously distributed scatterers,” Opt. Commun. 196(1-6), 325–330 (2001).
[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(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]

Min, W.

C. W. Freudiger, W. Min, B. G. Saar, S. Lu, G. R. Holtom, C. He, J. C. Tsai, J. X. Kang, and X. S. Xie, “Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy,” Science 322(5909), 1857–1861 (2008).
[CrossRef] [PubMed]

Minary-Jolandan, M.

M. Minary-Jolandan and M.-F. Yu, “Uncovering Nanoscale Electromechanical Heterogeneity in the Subfibrillar Structure of Collagen Fibrils Responsible for the Piezoelectricity of Bone,” ACS Nano 3(7), 1859–1863 (2009).
[CrossRef] [PubMed]

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.

O. Nadiarnykh, R. B. Lacomb, P. J. Campagnola, and W. A. Mohler, “Coherent and incoherent SHG in fibrillar cellulose matrices,” Opt. Express 15(6), 3348–3360 (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]

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]

Moreaux, L.

J. Mertz and L. Moreaux, “Second-harmonic generation by focused excitation of inhomogeneously distributed scatterers,” Opt. Commun. 196(1-6), 325–330 (2001).
[CrossRef]

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]

O. Nadiarnykh, R. B. Lacomb, P. J. Campagnola, and W. A. Mohler, “Coherent and incoherent SHG in fibrillar cellulose matrices,” Opt. Express 15(6), 3348–3360 (2007).
[CrossRef] [PubMed]

Nandakumar, P.

P. Nandakumar, A. Kovalev, and A. Volkmer, “Vibrational imaging based on stimulated Raman scattering microscopy,” N. J. Phys. 11(3), 033026 (2009).
[CrossRef]

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]

Olsen, B. R.

C. Harnagea, M. Vallières, C. P. Pfeffer, D. Wu, B. R. Olsen, A. Pignolet, F. Légaré, and A. Gruverman, “Two-dimensional nanoscale structural and functional imaging in individual collagen type I fibrils,” Biophys. J. 98(12), 3070–3077 (2010).
[CrossRef] [PubMed]

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

Oron, D.

D. Oron, D. Yelin, E. Tal, S. Raz, R. Fachima, and Y. Silberberg, “Depth-resolved structural imaging by third-harmonic generation microscopy,” J. Struct. Biol. 147(1), 3–11 (2004).
[CrossRef] [PubMed]

Paige, M. F.

M. F. Paige, J. K. Rainey, and M. C. Goh, “Fibrous long spacing collagen ultrastructure elucidated by atomic force microscopy,” Biophys. J. 74(6), 3211–3216 (1998).
[CrossRef] [PubMed]

Parry, D. A. D.

D. A. D. Parry and A. S. Craig, “Quantitative electron microscope observations of the collagen fibrils in rat-tail tendon,” Biopolymers 16(5), 1015–1031 (1977).
[CrossRef] [PubMed]

Peavy, G. M.

A. T. Yeh, M. J. Hammer-Wilson, D. C. Van Sickle, H. P. Benton, A. Zoumi, B. J. Tromberg, and G. M. Peavy, “Nonlinear optical microscopy of articular cartilage,” Osteoarthritis Cartilage 13(4), 345–352 (2005).
[CrossRef] [PubMed]

Pegoraro, A. F.

Pena, A. M.

D. Débarre, W. Supatto, 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. Methods 3(1), 47–53 (2006).
[CrossRef] [PubMed]

Pezacki, J. P.

Pfeffer, C. P.

C. Harnagea, M. Vallières, C. P. Pfeffer, D. Wu, B. R. Olsen, A. Pignolet, F. Légaré, and A. Gruverman, “Two-dimensional nanoscale structural and functional imaging in individual collagen type I fibrils,” Biophys. J. 98(12), 3070–3077 (2010).
[CrossRef] [PubMed]

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

Pignolet, A.

C. Harnagea, M. Vallières, C. P. Pfeffer, D. Wu, B. R. Olsen, A. Pignolet, F. Légaré, and A. Gruverman, “Two-dimensional nanoscale structural and functional imaging in individual collagen type I fibrils,” Biophys. J. 98(12), 3070–3077 (2010).
[CrossRef] [PubMed]

C. Harnagea, A. Pignolet, M. Alexe, and D. Hesse, “Higher-order electromechanical response of thin films by contact resonance piezoresponse force microscopy,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 53(12), 2309–2322 (2006).
[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]

Potma, E. O.

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, 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. U.S.A. 102(46), 16807–16812 (2005).
[CrossRef] [PubMed]

Puoris’haag, M.

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, 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. U.S.A. 102(46), 16807–16812 (2005).
[CrossRef] [PubMed]

Rainey, J. K.

M. F. Paige, J. K. Rainey, and M. C. Goh, “Fibrous long spacing collagen ultrastructure elucidated by atomic force microscopy,” Biophys. J. 74(6), 3211–3216 (1998).
[CrossRef] [PubMed]

Rao, R. A.

Raz, S.

D. Oron, D. Yelin, E. Tal, S. Raz, R. Fachima, and Y. Silberberg, “Depth-resolved structural imaging by third-harmonic generation microscopy,” J. Struct. Biol. 147(1), 3–11 (2004).
[CrossRef] [PubMed]

Redmond, R. W.

B. P. Chan, C. Amann, A. N. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. E. Kochevar, and R. W. Redmond, “Photochemical repair of Achilles tendon rupture in a rat model,” J. Surg. Res. 124(2), 274–279 (2005).
[CrossRef] [PubMed]

Reiser, K. M.

I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum frequency vibrational spectroscopy: the molecular origins of the optical second-order nonlinearity of collagen,” Biophys. J. 93(12), 4433–4444 (2007).
[CrossRef] [PubMed]

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]

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D. R. Baselt, J. P. Revel, and J. D. Baldeschwieler, “Subfibrillar structure of type I collagen observed by atomic force microscopy,” Biophys. J. 65(6), 2644–2655 (1993).
[CrossRef] [PubMed]

Ridsdale, A.

Rocha-Mendoza, I.

I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum frequency vibrational spectroscopy: the molecular origins of the optical second-order nonlinearity of collagen,” Biophys. J. 93(12), 4433–4444 (2007).
[CrossRef] [PubMed]

Rosenman, G.

A. Kholkin, N. Amdursky, I. Bdikin, E. Gazit, and G. Rosenman, “Strong piezoelectricity in bioinspired peptide nanotubes,” ACS Nano 4(2), 610–614 (2010).
[CrossRef] [PubMed]

Rubenchik, A. M.

Saar, B. G.

C. W. Freudiger, W. Min, B. G. Saar, S. Lu, G. R. Holtom, C. He, J. C. Tsai, J. X. Kang, and X. S. Xie, “Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy,” Science 322(5909), 1857–1861 (2008).
[CrossRef] [PubMed]

Sauviat, M.-P.

Schanne-Klein, M. C.

D. Débarre, W. Supatto, 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. Methods 3(1), 47–53 (2006).
[CrossRef] [PubMed]

Schanne-Klein, M.-C.

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]

Shi, R.

H. Wang, Y. Fu, P. Zickmund, R. Shi, and J. X. Cheng, “Coherent anti-stokes Raman scattering imaging of axonal myelin in live spinal tissues,” Biophys. J. 89(1), 581–591 (2005).
[CrossRef] [PubMed]

Silberberg, Y.

D. Oron, D. Yelin, E. Tal, S. Raz, R. Fachima, and Y. Silberberg, “Depth-resolved structural imaging by third-harmonic generation microscopy,” J. Struct. Biol. 147(1), 3–11 (2004).
[CrossRef] [PubMed]

Slepkov, A. D.

Smink, D.

B. P. Chan, C. Amann, A. N. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. E. Kochevar, and R. W. Redmond, “Photochemical repair of Achilles tendon rupture in a rat model,” J. Surg. Res. 124(2), 274–279 (2005).
[CrossRef] [PubMed]

Stoller, P.

Stolow, A.

Stoothoff, W. H.

W. H. Stoothoff, B. J. Bacskai, and B. T. Hyman, “Monitoring tau-tubulin interactions utilizing second harmonic generation in living neurons,” J. Biomed. Opt. 13(6), 064039 (2008).
[CrossRef] [PubMed]

Sun, C.-K.

S.-W. Chu, S.-P. Tai, T.-M. Liu, C.-K. Sun, and C. H. Lin, “Selective imaging in second-harmonic-generation microscopy with anisotropic radiation,” J. Biomed. Opt. 14(1), 010504 (2009).
[CrossRef] [PubMed]

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(6), 3914–3922 (2004).
[CrossRef] [PubMed]

Sunney Xie, X.

A. Volkmer, J.-X. Cheng, and X. Sunney Xie, “Vibrational imaging with high sensitivity via epidetected coherent anti-Stokes Raman scattering microscopy,” Phys. Rev. Lett. 87(2), 023901 (2001).
[CrossRef]

Supatto, W.

D. Débarre, W. Supatto, 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. Methods 3(1), 47–53 (2006).
[CrossRef] [PubMed]

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S.-W. Chu, S.-P. Tai, T.-M. Liu, C.-K. Sun, and C. H. Lin, “Selective imaging in second-harmonic-generation microscopy with anisotropic radiation,” J. Biomed. Opt. 14(1), 010504 (2009).
[CrossRef] [PubMed]

Tal, E.

D. Oron, D. Yelin, E. Tal, S. Raz, R. Fachima, and Y. Silberberg, “Depth-resolved structural imaging by third-harmonic generation microscopy,” J. Struct. Biol. 147(1), 3–11 (2004).
[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]

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 cryosections,” Biophys. J. 91(12), 4665–4677 (2006).
[CrossRef] [PubMed]

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 cryosections,” Biophys. J. 91(12), 4665–4677 (2006).
[CrossRef] [PubMed]

Title, C.

B. P. Chan, C. Amann, A. N. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. E. Kochevar, and R. W. Redmond, “Photochemical repair of Achilles tendon rupture in a rat model,” J. Surg. Res. 124(2), 274–279 (2005).
[CrossRef] [PubMed]

Tordjmann, T.

D. Débarre, W. Supatto, 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. Methods 3(1), 47–53 (2006).
[CrossRef] [PubMed]

Toussaint, K. C.

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]

Tromberg, B. J.

A. T. Yeh, M. J. Hammer-Wilson, D. C. Van Sickle, H. P. Benton, A. Zoumi, B. J. Tromberg, and G. M. Peavy, “Nonlinear optical microscopy of articular cartilage,” Osteoarthritis Cartilage 13(4), 345–352 (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. U.S.A. 99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

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K. E. Kadler, D. F. Holmes, J. A. Trotter, and J. A. Chapman, “Collagen fibril formation,” Biochem. J. 316(Pt 1), 1–11 (1996).
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C. W. Freudiger, W. Min, B. G. Saar, S. Lu, G. R. Holtom, C. He, J. C. Tsai, J. X. Kang, and X. S. Xie, “Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy,” Science 322(5909), 1857–1861 (2008).
[CrossRef] [PubMed]

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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(6), 3914–3922 (2004).
[CrossRef] [PubMed]

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C. Harnagea, M. Vallières, C. P. Pfeffer, D. Wu, B. R. Olsen, A. Pignolet, F. Légaré, and A. Gruverman, “Two-dimensional nanoscale structural and functional imaging in individual collagen type I fibrils,” Biophys. J. 98(12), 3070–3077 (2010).
[CrossRef] [PubMed]

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A. T. Yeh, M. J. Hammer-Wilson, D. C. Van Sickle, H. P. Benton, A. Zoumi, B. J. Tromberg, and G. M. Peavy, “Nonlinear optical microscopy of articular cartilage,” Osteoarthritis Cartilage 13(4), 345–352 (2005).
[CrossRef] [PubMed]

Volkmer, A.

P. Nandakumar, A. Kovalev, and A. Volkmer, “Vibrational imaging based on stimulated Raman scattering microscopy,” N. J. Phys. 11(3), 033026 (2009).
[CrossRef]

A. Volkmer, J.-X. Cheng, and X. Sunney Xie, “Vibrational imaging with high sensitivity via epidetected coherent anti-Stokes Raman scattering microscopy,” Phys. Rev. Lett. 87(2), 023901 (2001).
[CrossRef]

Wang, H.

H. Wang, Y. Fu, P. Zickmund, R. Shi, and J. X. Cheng, “Coherent anti-stokes Raman scattering imaging of axonal myelin in live spinal tissues,” Biophys. J. 89(1), 581–591 (2005).
[CrossRef] [PubMed]

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I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum frequency vibrational spectroscopy: the molecular origins of the optical second-order nonlinearity of collagen,” Biophys. J. 93(12), 4433–4444 (2007).
[CrossRef] [PubMed]

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R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005).
[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]

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(2), 1377–1386 (2005).
[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).
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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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Wu, D.

C. Harnagea, M. Vallières, C. P. Pfeffer, D. Wu, B. R. Olsen, A. Pignolet, F. Légaré, and A. Gruverman, “Two-dimensional nanoscale structural and functional imaging in individual collagen type I fibrils,” Biophys. J. 98(12), 3070–3077 (2010).
[CrossRef] [PubMed]

Xie, X. S.

C. W. Freudiger, W. Min, B. G. Saar, S. Lu, G. R. Holtom, C. He, J. C. Tsai, J. X. Kang, and X. S. Xie, “Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy,” Science 322(5909), 1857–1861 (2008).
[CrossRef] [PubMed]

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, 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. U.S.A. 102(46), 16807–16812 (2005).
[CrossRef] [PubMed]

Yankelevich, D. R.

I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum frequency vibrational spectroscopy: the molecular origins of the optical second-order nonlinearity of collagen,” Biophys. J. 93(12), 4433–4444 (2007).
[CrossRef] [PubMed]

Yaroslavsky, A. N.

B. P. Chan, C. Amann, A. N. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. E. Kochevar, and R. W. Redmond, “Photochemical repair of Achilles tendon rupture in a rat model,” J. Surg. Res. 124(2), 274–279 (2005).
[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. U.S.A. 99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

Yeh, A. T.

A. T. Yeh, M. J. Hammer-Wilson, D. C. Van Sickle, H. P. Benton, A. Zoumi, B. J. Tromberg, and G. M. Peavy, “Nonlinear optical microscopy of articular cartilage,” Osteoarthritis Cartilage 13(4), 345–352 (2005).
[CrossRef] [PubMed]

Yelin, D.

D. Oron, D. Yelin, E. Tal, S. Raz, R. Fachima, and Y. Silberberg, “Depth-resolved structural imaging by third-harmonic generation microscopy,” J. Struct. Biol. 147(1), 3–11 (2004).
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Yu, M.-F.

M. Minary-Jolandan and M.-F. Yu, “Uncovering Nanoscale Electromechanical Heterogeneity in the Subfibrillar Structure of Collagen Fibrils Responsible for the Piezoelectricity of Bone,” ACS Nano 3(7), 1859–1863 (2009).
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B. P. Chan, C. Amann, A. N. Yaroslavsky, C. Title, D. Smink, B. Zarins, I. E. Kochevar, and R. W. Redmond, “Photochemical repair of Achilles tendon rupture in a rat model,” J. Surg. Res. 124(2), 274–279 (2005).
[CrossRef] [PubMed]

Zickmund, P.

H. Wang, Y. Fu, P. Zickmund, R. Shi, and J. X. Cheng, “Coherent anti-stokes Raman scattering imaging of axonal myelin in live spinal tissues,” Biophys. J. 89(1), 581–591 (2005).
[CrossRef] [PubMed]

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(2), 1377–1386 (2005).
[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]

Zoumi, A.

A. T. Yeh, M. J. Hammer-Wilson, D. C. Van Sickle, H. P. Benton, A. Zoumi, B. J. Tromberg, and G. M. Peavy, “Nonlinear optical microscopy of articular cartilage,” Osteoarthritis Cartilage 13(4), 345–352 (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. U.S.A. 99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

ACS Nano (2)

M. Minary-Jolandan and M.-F. Yu, “Uncovering Nanoscale Electromechanical Heterogeneity in the Subfibrillar Structure of Collagen Fibrils Responsible for the Piezoelectricity of Bone,” ACS Nano 3(7), 1859–1863 (2009).
[CrossRef] [PubMed]

A. Kholkin, N. Amdursky, I. Bdikin, E. Gazit, and G. Rosenman, “Strong piezoelectricity in bioinspired peptide nanotubes,” ACS Nano 4(2), 610–614 (2010).
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Appl. Opt. (2)

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D. R. Baselt, J. P. Revel, and J. D. Baldeschwieler, “Subfibrillar structure of type I collagen observed by atomic force microscopy,” Biophys. J. 65(6), 2644–2655 (1993).
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M. F. Paige, J. K. Rainey, and M. C. Goh, “Fibrous long spacing collagen ultrastructure elucidated by atomic force microscopy,” Biophys. J. 74(6), 3211–3216 (1998).
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[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 cryosections,” Biophys. J. 91(12), 4665–4677 (2006).
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H. Wang, Y. Fu, P. Zickmund, R. Shi, and J. X. Cheng, “Coherent anti-stokes Raman scattering imaging of axonal myelin in live spinal tissues,” Biophys. J. 89(1), 581–591 (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(2), 1377–1386 (2005).
[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).
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[CrossRef] [PubMed]

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[CrossRef] [PubMed]

W. H. Stoothoff, B. J. Bacskai, and B. T. Hyman, “Monitoring tau-tubulin interactions utilizing second harmonic generation in living neurons,” J. Biomed. Opt. 13(6), 064039 (2008).
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D. Débarre, W. Supatto, 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. Methods 3(1), 47–53 (2006).
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Opt. Lett. (2)

Osteoarthritis Cartilage (1)

A. T. Yeh, M. J. Hammer-Wilson, D. C. Van Sickle, H. P. Benton, A. Zoumi, B. J. Tromberg, and G. M. Peavy, “Nonlinear optical microscopy of articular cartilage,” Osteoarthritis Cartilage 13(4), 345–352 (2005).
[CrossRef] [PubMed]

Phys. Rev. Lett. (1)

A. Volkmer, J.-X. Cheng, and X. Sunney Xie, “Vibrational imaging with high sensitivity via epidetected coherent anti-Stokes Raman scattering microscopy,” Phys. Rev. Lett. 87(2), 023901 (2001).
[CrossRef]

Proc. Natl. Acad. Sci. U.S.A. (3)

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, 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. U.S.A. 102(46), 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. U.S.A. 99(17), 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. U.S.A. 100(12), 7075–7080 (2003).
[CrossRef] [PubMed]

Science (1)

C. W. Freudiger, W. Min, B. G. Saar, S. Lu, G. R. Holtom, C. He, J. C. Tsai, J. X. Kang, and X. S. Xie, “Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy,” Science 322(5909), 1857–1861 (2008).
[CrossRef] [PubMed]

Other (1)

M. Strupler, and M.-C. Schanne-Klein, “Simulating second harmonic generation from tendon - Do we see fibrils?” in Biomedical Optics, OSA Technical Digest (CD) (Optical Society of America, 2010), paper BTuD83.

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Figures (6)

Fig. 1
Fig. 1

Experimental setup used for the SHG experiments: forward and backward SHG imaging microscopy, forward SHG microscopy with a variable collection numerical aperture (iris) and SHG under tight focusing near a quartz interface (radiation pattern measurement). H, half-wave plate; P, polarizer; D, Dichroic mirror; O1, illumination objective (0.8 NA, water); O2, collection objective (1.15 NA, water); F, filters; PMT, photomultiplier tube. In the forward direction, the detector is whether a PMT or a CCD.

Fig. 2
Fig. 2

SHG images of fascia tissue in (a) forward and (b) backward direction. Signal profiles taken along the same lines in forward and backward images (c) longitudinally and (d) transverse to the collagen sheets. Longitudinal and transverse (to the fibrillar axis) intensity profiles were taken along the yellow lines. The boundaries between the collagen sheets are clear in the backward direction.

Fig. 3
Fig. 3

SHG images of fascia tissue taken with different collection NA by varying the aperture of the collection objective with an iris. Forward signal was collected with (a) 1,15 NA, (b) 0,55 NA, (c) 0,35 NA, (d) 0,19 NA and (e) 0,07 NA. Longitudinal and transversal (to the fibrillar axis) intensity profiles taken in (a-e) along the yellow lines shown in (a) are also presented in (f) and (g). New modulations in the signal appear along those structures when the collection NA used to take the image is smaller than 0.55.

Fig. 4
Fig. 4

Experimental signal profiles when (i) the focus travels through (a) the lower and (b) the upper interface of the quartz crystal. When the NA used for collection is reduced, the SHG signal profile becomes asymmetric in Z at both interfaces. Images of the collimated radiation pattern are taken with a CCD camera while the focus is near the upper interface: (c) 6 μm in the crystal, (d) 4 μm in the crystal, (e) 2 μm in the crystal, (f) at the interface, (g) 2 μm in the air, and (h) 4 μm in the air. (j) The radial intensity profile in function of the equivalent NA (which is a measure of the angle of emission). This demonstrates that the position of the focus in the χ(2) distribution can be responsible for changes in the radiation pattern.

Fig. 5
Fig. 5

Piezoresponse force microscopy experiment on fascia. a) sample topography, 5μm scan, (b) topography, zoom of (a), and (c) piezoresponse image [of the same area as in (b)] showing the orientation of the piezoelectric tensor. The piezoelectric response in fascia has either a positive or negative value (white or a dark contrast).

Fig. 6
Fig. 6

The dependence of the PFM signal (in-plane measurements) on the angle between the cantilever and the collagen fibril axis, averaged over a 5μm of fibril length. The single collagen fibril was rotated in steps of 15 degrees. The insets illustrate two of the image sets (each composed of topography at left and PFM image at right, 5μm scans) used to construct the graph. The yellow arrows in the PFM images illustrate the detection direction.

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