Abstract

We report that combining interferometry with Second Harmonic Generation (SHG) microscopy provides valuable information about the relative orientation of noncentrosymmetric structures composing tissues. This is confirmed through the imaging of rat medial gastrocnemius muscle. The inteferometric Second Harmonic Generation (ISHG) images reveal that each side of the myosin filaments composing the A band of the sarcomere generates π phase shifted SHG signal which implies that the myosin proteins at each end of the filaments are oriented in opposite directions. This highlights the bipolar structural organization of the myosin filaments and shows that muscles can be considered as a periodically poled biological structure.

© 2013 OSA

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2013 (1)

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J Biophotonics6(2), 129–142 (2013).
[CrossRef] [PubMed]

2012 (4)

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

I. Gusachenko, V. Tran, Y. G. Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-Resolved Second-Harmonic Generation in Tendon upon Mechanical Stretching,” Biophys. J.102(9), 2220–2229 (2012).
[CrossRef] [PubMed]

C. P. Brown, M.-A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater.5(1), 62–70 (2012).
[CrossRef] [PubMed]

D. G. Winters, D. R. Smith, P. Schlup, and R. A. Bartels, “Measurement of orientation and susceptibility ratios using a polarization-resolved second-harmonic generation holographic microscope,” Biomed. Opt. Express3(9), 2004–2011 (2012).
[CrossRef] [PubMed]

2011 (2)

2010 (4)

2009 (2)

N. Prent, C. Greenhalgh, R. Cisek, A. Major, J. Aus Der Au, S. Elmore, J. H. G. M. Van Beek, B. Stewart, J. A. Squier, and V. Barzda, “Second harmonic generation microscopy reveals contraction dynamics in muscle cells,” La Physique Au Canada65, 129–131 (2009).

G. Recher, D. Rouède, P. Richard, A. Simon, J.-J. Bellanger, and F. Tiaho, “Three distinct sarcomeric patterns of skeletal muscle revealed by SHG and TPEF microscopy,” Opt. Express17(22), 19763–19777 (2009).
[CrossRef] [PubMed]

2008 (3)

C. Odin, T. Guilbert, A. Alkilani, O. P. Boryskina, V. Fleury, and Y. Le Grand, “Collagen and myosin characterization by orientation field second harmonic microscopy,” Opt. Express16(20), 16151–16165 (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]

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]

2007 (4)

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]

C. Greenhalgh, N. Prent, C. Green, R. Cisek, A. Major, B. Stewart, and V. Barzda, “Influence of semicrystalline order on the second-harmonic generation efficiency in the anisotropic bands of myocytes,” Appl. Opt.46(10), 1852–1859 (2007).
[CrossRef] [PubMed]

F. Tiaho, G. Recher, and D. Rouède, “Estimation of helical angles of myosin and collagen by second harmonic generation imaging microscopy,” Opt. Express15(19), 12286–12295 (2007).
[CrossRef] [PubMed]

2006 (2)

R. Craig and J. L. Woodhead, “Structure and function of myosin filaments,” Curr. Opin. Struct. Biol.16(2), 204–212 (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]

2005 (1)

Y. Jeon, H. Min, D. Kim, and M. Oh-e, “Determination of the Crystalline x-Axis of Quartz by Second-Harmonic Phase Measurement,” J. Korean Phys. Soc.46, S159–S162 (2005).

2004 (3)

2003 (1)

2000 (1)

P. Rechsteiner, J. Hulliger, and M. Flörsheimer, “Phase-Sensitive Second Harmonic Microscopy Reveals Bipolar Twinning of Markov-Type Molecular Crystals,” Chem. Mater.12(11), 3296–3300 (2000).
[CrossRef]

1996 (2)

R. Stolle, G. Marowsky, E. Schwarzberg, and G. Berkovic, “Phase measurements in nonlinear optics,” Appl. Phys. B63, 491–498 (1996).

J. Q. Xu, B. A. Harder, P. Uman, and R. Craig, “Myosin Filament Structure in Vertebrate Smooth Muscle,” J. Cell Biol.134(1), 53–66 (1996).
[CrossRef] [PubMed]

1986 (1)

I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J.50(4), 693–712 (1986).
[CrossRef] [PubMed]

1982 (1)

T. D. Pollard, “Structure and Polymerization of Acanthamoeba Myosin-II Filaments,” J. Cell Biol.95(3), 816–825 (1982).
[CrossRef] [PubMed]

1963 (1)

S. G. Page and H. E. Huxley, “Filament Lengths in Striated Muscle,” J. Cell Biol.19(2), 369–390 (1963).
[CrossRef] [PubMed]

Alkilani, A.

Allain, J.-M.

I. Gusachenko, V. Tran, Y. G. Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-Resolved Second-Harmonic Generation in Tendon upon Mechanical Stretching,” Biophys. J.102(9), 2220–2229 (2012).
[CrossRef] [PubMed]

Aus Der Au, J.

N. Prent, C. Greenhalgh, R. Cisek, A. Major, J. Aus Der Au, S. Elmore, J. H. G. M. Van Beek, B. Stewart, J. A. Squier, and V. Barzda, “Second harmonic generation microscopy reveals contraction dynamics in muscle cells,” La Physique Au Canada65, 129–131 (2009).

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]

Bartels, R. A.

Barzda, V.

N. Prent, C. Greenhalgh, R. Cisek, A. Major, J. Aus Der Au, S. Elmore, J. H. G. M. Van Beek, B. Stewart, J. A. Squier, and V. Barzda, “Second harmonic generation microscopy reveals contraction dynamics in muscle cells,” La Physique Au Canada65, 129–131 (2009).

C. Greenhalgh, N. Prent, C. Green, R. Cisek, A. Major, B. Stewart, and V. Barzda, “Influence of semicrystalline order on the second-harmonic generation efficiency in the anisotropic bands of myocytes,” Appl. Opt.46(10), 1852–1859 (2007).
[CrossRef] [PubMed]

Beaurepaire, E.

Bellanger, J.-J.

Berkovic, G.

R. Stolle, G. Marowsky, E. Schwarzberg, and G. Berkovic, “Phase measurements in nonlinear optics,” Appl. Phys. B63, 491–498 (1996).

Bertrand-Grenier, A.

Boryskina, O. P.

Boulesteix, T.

Brown, C. P.

C. P. Brown, M.-A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater.5(1), 62–70 (2012).
[CrossRef] [PubMed]

Campagnola, P. J.

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

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]

Celliers, P. M.

Chen, M.

C. P. Brown, M.-A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater.5(1), 62–70 (2012).
[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, X.

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

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]

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

Cicchi, R.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J Biophotonics6(2), 129–142 (2013).
[CrossRef] [PubMed]

Cisek, R.

N. Prent, C. Greenhalgh, R. Cisek, A. Major, J. Aus Der Au, S. Elmore, J. H. G. M. Van Beek, B. Stewart, J. A. Squier, and V. Barzda, “Second harmonic generation microscopy reveals contraction dynamics in muscle cells,” La Physique Au Canada65, 129–131 (2009).

C. Greenhalgh, N. Prent, C. Green, R. Cisek, A. Major, B. Stewart, and V. Barzda, “Influence of semicrystalline order on the second-harmonic generation efficiency in the anisotropic bands of myocytes,” Appl. Opt.46(10), 1852–1859 (2007).
[CrossRef] [PubMed]

Craig, R.

R. Craig and J. L. Woodhead, “Structure and function of myosin filaments,” Curr. Opin. Struct. Biol.16(2), 204–212 (2006).
[CrossRef] [PubMed]

J. Q. Xu, B. A. Harder, P. Uman, and R. Craig, “Myosin Filament Structure in Vertebrate Smooth Muscle,” J. Cell Biol.134(1), 53–66 (1996).
[CrossRef] [PubMed]

Depeursinge, C.

Deutsch, M.

I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J.50(4), 693–712 (1986).
[CrossRef] [PubMed]

Dietzek, B.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J Biophotonics6(2), 129–142 (2013).
[CrossRef] [PubMed]

El Khakani, M. A.

Elmore, S.

N. Prent, C. Greenhalgh, R. Cisek, A. Major, J. Aus Der Au, S. Elmore, J. H. G. M. Van Beek, B. Stewart, J. A. Squier, and V. Barzda, “Second harmonic generation microscopy reveals contraction dynamics in muscle cells,” La Physique Au Canada65, 129–131 (2009).

Fink, R. H. A.

S. Schürmann, F. von Wegner, R. H. A. Fink, O. Friedrich, and M. Vogel, “Second Harmonic Generation Microscopy Probes Different States of Motor Protein Interaction in Myofibrils,” Biophys. J.99(6), 1842–1851 (2010).
[CrossRef] [PubMed]

Fleury, V.

Flörsheimer, M.

P. Rechsteiner, J. Hulliger, and M. Flörsheimer, “Phase-Sensitive Second Harmonic Microscopy Reveals Bipolar Twinning of Markov-Type Molecular Crystals,” Chem. Mater.12(11), 3296–3300 (2000).
[CrossRef]

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]

Freund, I.

I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J.50(4), 693–712 (1986).
[CrossRef] [PubMed]

Friedrich, O.

S. Schürmann, F. von Wegner, R. H. A. Fink, O. Friedrich, and M. Vogel, “Second Harmonic Generation Microscopy Probes Different States of Motor Protein Interaction in Myofibrils,” Biophys. J.99(6), 1842–1851 (2010).
[CrossRef] [PubMed]

Fukui, T.

Gill, H. S.

C. P. Brown, M.-A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater.5(1), 62–70 (2012).
[CrossRef] [PubMed]

Green, C.

Greenhalgh, C.

N. Prent, C. Greenhalgh, R. Cisek, A. Major, J. Aus Der Au, S. Elmore, J. H. G. M. Van Beek, B. Stewart, J. A. Squier, and V. Barzda, “Second harmonic generation microscopy reveals contraction dynamics in muscle cells,” La Physique Au Canada65, 129–131 (2009).

C. Greenhalgh, N. Prent, C. Green, R. Cisek, A. Major, B. Stewart, and V. Barzda, “Influence of semicrystalline order on the second-harmonic generation efficiency in the anisotropic bands of myocytes,” Appl. Opt.46(10), 1852–1859 (2007).
[CrossRef] [PubMed]

Guilbert, T.

Gusachenko, I.

I. Gusachenko, V. Tran, Y. G. Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-Resolved Second-Harmonic Generation in Tendon upon Mechanical Stretching,” Biophys. J.102(9), 2220–2229 (2012).
[CrossRef] [PubMed]

Harder, B. A.

J. Q. Xu, B. A. Harder, P. Uman, and R. Craig, “Myosin Filament Structure in Vertebrate Smooth Muscle,” J. Cell Biol.134(1), 53–66 (1996).
[CrossRef] [PubMed]

Harnagea, C.

Houle, M.-A.

C. P. Brown, M.-A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater.5(1), 62–70 (2012).
[CrossRef] [PubMed]

Houssen, Y. G.

I. Gusachenko, V. Tran, Y. G. Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-Resolved Second-Harmonic Generation in Tendon upon Mechanical Stretching,” Biophys. J.102(9), 2220–2229 (2012).
[CrossRef] [PubMed]

Hulliger, J.

P. Rechsteiner, J. Hulliger, and M. Flörsheimer, “Phase-Sensitive Second Harmonic Microscopy Reveals Bipolar Twinning of Markov-Type Molecular Crystals,” Chem. Mater.12(11), 3296–3300 (2000).
[CrossRef]

Huxley, H. E.

S. G. Page and H. E. Huxley, “Filament Lengths in Striated Muscle,” J. Cell Biol.19(2), 369–390 (1963).
[CrossRef] [PubMed]

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]

Jeon, Y.

Y. Jeon, H. Min, D. Kim, and M. Oh-e, “Determination of the Crystalline x-Axis of Quartz by Second-Harmonic Phase Measurement,” J. Korean Phys. Soc.46, S159–S162 (2005).

Kaneshiro, J.

Kapsokalyvas, D.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J Biophotonics6(2), 129–142 (2013).
[CrossRef] [PubMed]

Kim, D.

Y. Jeon, H. Min, D. Kim, and M. Oh-e, “Determination of the Crystalline x-Axis of Quartz by Second-Harmonic Phase Measurement,” J. Korean Phys. Soc.46, S159–S162 (2005).

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]

Laiho, L. H.

Laliberté, M.

Le Grand, Y.

Légaré, F.

C. P. Brown, M.-A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater.5(1), 62–70 (2012).
[CrossRef] [PubMed]

M. Rivard, M. Laliberté, A. Bertrand-Grenier, C. Harnagea, C. P. Pfeffer, M. Vallières, Y. St-Pierre, A. Pignolet, M. A. El Khakani, and F. Légaré, “The structural origin of second harmonic generation in fascia,” Biomed. Opt. Express2(1), 26–36 (2011).
[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]

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]

Magistretti, P.

Major, A.

N. Prent, C. Greenhalgh, R. Cisek, A. Major, J. Aus Der Au, S. Elmore, J. H. G. M. Van Beek, B. Stewart, J. A. Squier, and V. Barzda, “Second harmonic generation microscopy reveals contraction dynamics in muscle cells,” La Physique Au Canada65, 129–131 (2009).

C. Greenhalgh, N. Prent, C. Green, R. Cisek, A. Major, B. Stewart, and V. Barzda, “Influence of semicrystalline order on the second-harmonic generation efficiency in the anisotropic bands of myocytes,” Appl. Opt.46(10), 1852–1859 (2007).
[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]

Marowsky, G.

R. Stolle, G. Marowsky, E. Schwarzberg, and G. Berkovic, “Phase measurements in nonlinear optics,” Appl. Phys. B63, 491–498 (1996).

Marquet, P.

Masihzadeh, O.

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]

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]

Min, H.

Y. Jeon, H. Min, D. Kim, and M. Oh-e, “Determination of the Crystalline x-Axis of Quartz by Second-Harmonic Phase Measurement,” J. Korean Phys. Soc.46, S159–S162 (2005).

Moger, J.

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

Mohler, W. A.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the Myosin-Based Source for Second-Harmonic Generation from Muscle Sarcomeres,” Biophys. J.90(2), 693–703 (2006).
[CrossRef] [PubMed]

Moratal, C.

Nadiarynkh, O.

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

Odin, C.

Oh-e, M.

Y. Jeon, H. Min, D. Kim, and M. Oh-e, “Determination of the Crystalline x-Axis of Quartz by Second-Harmonic Phase Measurement,” J. Korean Phys. Soc.46, S159–S162 (2005).

Olsen, B. R.

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]

Page, S. G.

S. G. Page and H. E. Huxley, “Filament Lengths in Striated Muscle,” J. Cell Biol.19(2), 369–390 (1963).
[CrossRef] [PubMed]

Pavone, F. S.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J Biophotonics6(2), 129–142 (2013).
[CrossRef] [PubMed]

Pfeffer, C. P.

Pignolet, A.

Plotnikov, S.

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

Plotnikov, S. V.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the Myosin-Based Source for Second-Harmonic Generation from Muscle Sarcomeres,” Biophys. J.90(2), 693–703 (2006).
[CrossRef] [PubMed]

Pollard, T. D.

T. D. Pollard, “Structure and Polymerization of Acanthamoeba Myosin-II Filaments,” J. Cell Biol.95(3), 816–825 (1982).
[CrossRef] [PubMed]

Popp, J.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J Biophotonics6(2), 129–142 (2013).
[CrossRef] [PubMed]

Prent, N.

N. Prent, C. Greenhalgh, R. Cisek, A. Major, J. Aus Der Au, S. Elmore, J. H. G. M. Van Beek, B. Stewart, J. A. Squier, and V. Barzda, “Second harmonic generation microscopy reveals contraction dynamics in muscle cells,” La Physique Au Canada65, 129–131 (2009).

C. Greenhalgh, N. Prent, C. Green, R. Cisek, A. Major, B. Stewart, and V. Barzda, “Influence of semicrystalline order on the second-harmonic generation efficiency in the anisotropic bands of myocytes,” Appl. Opt.46(10), 1852–1859 (2007).
[CrossRef] [PubMed]

Price, A. J.

C. P. Brown, M.-A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater.5(1), 62–70 (2012).
[CrossRef] [PubMed]

Recher, G.

Rechsteiner, P.

P. Rechsteiner, J. Hulliger, and M. Flörsheimer, “Phase-Sensitive Second Harmonic Microscopy Reveals Bipolar Twinning of Markov-Type Molecular Crystals,” Chem. Mater.12(11), 3296–3300 (2000).
[CrossRef]

Reiser, K. M.

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]

Richard, P.

Rivard, M.

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]

Rouède, D.

Rubenchik, A. M.

Sauviat, M.-P.

Schanne-Klein, M.-C.

I. Gusachenko, V. Tran, Y. G. Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-Resolved Second-Harmonic Generation in Tendon upon Mechanical Stretching,” Biophys. J.102(9), 2220–2229 (2012).
[CrossRef] [PubMed]

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]

Schaub, E.

Schlup, P.

Schürmann, S.

S. Schürmann, F. von Wegner, R. H. A. Fink, O. Friedrich, and M. Vogel, “Second Harmonic Generation Microscopy Probes Different States of Motor Protein Interaction in Myofibrils,” Biophys. J.99(6), 1842–1851 (2010).
[CrossRef] [PubMed]

Schwarzberg, E.

R. Stolle, G. Marowsky, E. Schwarzberg, and G. Berkovic, “Phase measurements in nonlinear optics,” Appl. Phys. B63, 491–498 (1996).

Shaffer, E.

Simon, A.

Smith, D. R.

So, P. T. C.

Sprecher, A.

I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J.50(4), 693–712 (1986).
[CrossRef] [PubMed]

Squier, J. A.

N. Prent, C. Greenhalgh, R. Cisek, A. Major, J. Aus Der Au, S. Elmore, J. H. G. M. Van Beek, B. Stewart, J. A. Squier, and V. Barzda, “Second harmonic generation microscopy reveals contraction dynamics in muscle cells,” La Physique Au Canada65, 129–131 (2009).

Stewart, B.

N. Prent, C. Greenhalgh, R. Cisek, A. Major, J. Aus Der Au, S. Elmore, J. H. G. M. Van Beek, B. Stewart, J. A. Squier, and V. Barzda, “Second harmonic generation microscopy reveals contraction dynamics in muscle cells,” La Physique Au Canada65, 129–131 (2009).

C. Greenhalgh, N. Prent, C. Green, R. Cisek, A. Major, B. Stewart, and V. Barzda, “Influence of semicrystalline order on the second-harmonic generation efficiency in the anisotropic bands of myocytes,” Appl. Opt.46(10), 1852–1859 (2007).
[CrossRef] [PubMed]

Stolle, R.

R. Stolle, G. Marowsky, E. Schwarzberg, and G. Berkovic, “Phase measurements in nonlinear optics,” Appl. Phys. B63, 491–498 (1996).

Stoller, P.

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]

St-Pierre, Y.

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

Tiaho, F.

Tran, V.

I. Gusachenko, V. Tran, Y. G. Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-Resolved Second-Harmonic Generation in Tendon upon Mechanical Stretching,” Biophys. J.102(9), 2220–2229 (2012).
[CrossRef] [PubMed]

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

Uesu, Y.

Uman, P.

J. Q. Xu, B. A. Harder, P. Uman, and R. Craig, “Myosin Filament Structure in Vertebrate Smooth Muscle,” J. Cell Biol.134(1), 53–66 (1996).
[CrossRef] [PubMed]

Vallières, M.

Van Beek, J. H. G. M.

N. Prent, C. Greenhalgh, R. Cisek, A. Major, J. Aus Der Au, S. Elmore, J. H. G. M. Van Beek, B. Stewart, J. A. Squier, and V. Barzda, “Second harmonic generation microscopy reveals contraction dynamics in muscle cells,” La Physique Au Canada65, 129–131 (2009).

Vogel, M.

S. Schürmann, F. von Wegner, R. H. A. Fink, O. Friedrich, and M. Vogel, “Second Harmonic Generation Microscopy Probes Different States of Motor Protein Interaction in Myofibrils,” Biophys. J.99(6), 1842–1851 (2010).
[CrossRef] [PubMed]

Vogler, N.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J Biophotonics6(2), 129–142 (2013).
[CrossRef] [PubMed]

von Wegner, F.

S. Schürmann, F. von Wegner, R. H. A. Fink, O. Friedrich, and M. Vogel, “Second Harmonic Generation Microscopy Probes Different States of Motor Protein Interaction in Myofibrils,” Biophys. J.99(6), 1842–1851 (2010).
[CrossRef] [PubMed]

Wang, 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]

Winlove, C. P.

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

Winters, D. G.

Woodhead, J. L.

R. Craig and J. L. Woodhead, “Structure and function of myosin filaments,” Curr. Opin. Struct. Biol.16(2), 204–212 (2006).
[CrossRef] [PubMed]

Xu, J. Q.

J. Q. Xu, B. A. Harder, P. Uman, and R. Craig, “Myosin Filament Structure in Vertebrate Smooth Muscle,” J. Cell Biol.134(1), 53–66 (1996).
[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]

Yazdanfar, S.

Appl. Opt. (2)

Appl. Phys. B (1)

R. Stolle, G. Marowsky, E. Schwarzberg, and G. Berkovic, “Phase measurements in nonlinear optics,” Appl. Phys. B63, 491–498 (1996).

Biomed. Opt. Express (3)

Biophys. J. (7)

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]

S. Schürmann, F. von Wegner, R. H. A. Fink, O. Friedrich, and M. Vogel, “Second Harmonic Generation Microscopy Probes Different States of Motor Protein Interaction in Myofibrils,” Biophys. J.99(6), 1842–1851 (2010).
[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]

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. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J.50(4), 693–712 (1986).
[CrossRef] [PubMed]

I. Gusachenko, V. Tran, Y. G. Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-Resolved Second-Harmonic Generation in Tendon upon Mechanical Stretching,” Biophys. J.102(9), 2220–2229 (2012).
[CrossRef] [PubMed]

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]

Chem. Mater. (1)

P. Rechsteiner, J. Hulliger, and M. Flörsheimer, “Phase-Sensitive Second Harmonic Microscopy Reveals Bipolar Twinning of Markov-Type Molecular Crystals,” Chem. Mater.12(11), 3296–3300 (2000).
[CrossRef]

Curr. Opin. Struct. Biol. (1)

R. Craig and J. L. Woodhead, “Structure and function of myosin filaments,” Curr. Opin. Struct. Biol.16(2), 204–212 (2006).
[CrossRef] [PubMed]

J Biophotonics (1)

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J Biophotonics6(2), 129–142 (2013).
[CrossRef] [PubMed]

J. Biomed. Opt. (2)

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]

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. Cell Biol. (3)

S. G. Page and H. E. Huxley, “Filament Lengths in Striated Muscle,” J. Cell Biol.19(2), 369–390 (1963).
[CrossRef] [PubMed]

T. D. Pollard, “Structure and Polymerization of Acanthamoeba Myosin-II Filaments,” J. Cell Biol.95(3), 816–825 (1982).
[CrossRef] [PubMed]

J. Q. Xu, B. A. Harder, P. Uman, and R. Craig, “Myosin Filament Structure in Vertebrate Smooth Muscle,” J. Cell Biol.134(1), 53–66 (1996).
[CrossRef] [PubMed]

J. Korean Phys. Soc. (1)

Y. Jeon, H. Min, D. Kim, and M. Oh-e, “Determination of the Crystalline x-Axis of Quartz by Second-Harmonic Phase Measurement,” J. Korean Phys. Soc.46, S159–S162 (2005).

J. Mech. Behav. Biomed. Mater. (1)

C. P. Brown, M.-A. Houle, M. Chen, A. J. Price, F. Légaré, and H. S. Gill, “Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy,” J. Mech. Behav. Biomed. Mater.5(1), 62–70 (2012).
[CrossRef] [PubMed]

J. Opt. Soc. Am. B (1)

La Physique Au Canada (1)

N. Prent, C. Greenhalgh, R. Cisek, A. Major, J. Aus Der Au, S. Elmore, J. H. G. M. Van Beek, B. Stewart, J. A. Squier, and V. Barzda, “Second harmonic generation microscopy reveals contraction dynamics in muscle cells,” La Physique Au Canada65, 129–131 (2009).

Nat. Protoc. (1)

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

Opt. Express (5)

Opt. Lett. (2)

Other (3)

M. Rivard, K. Popov, C.-A. Couture, M. Laliberté, A. Bertrand-Grenier, F. Martin, H. Pépin, C. P. Pfeffer, C. Brown, L. Ramunno, and F. Légaré, “Imaging the noncentrosymmetric structural organization of tendon with Interferometric Second Harmonic Generation microscopy,” J. Biophotonics, DOI: (2013).
[CrossRef]

A. G. Engel, Myology, 3rd edition (McGraw-Hill Professional, 2004), Chap. 7.

R. W. Boyd, Nonlinear optics, 3rd edition (Academic Press, 2008), Chap. 1.

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Figures (5)

Fig. 1
Fig. 1

(a) The experimental setup can take interferometric or standard SHG images. (b) The reference quartz SHG interferes with the SHG of a sample quartz. The SHG signal intensity depends of the glass window angle. (c) Rotating the 350 µm thick reference quartz by 180° along the light propagation axis flips its χ(2) and inverts the interference.

Fig. 2
Fig. 2

(a) Forward SHG image of muscle sarcomeres (65 X 20 μm). (b-d) Forward raw ISHG images of the same area taken at φref = (b) 105°, (c) 285° and (d) 465°. (e-f) Treated ISHG images obtained by subtracting image (b) to image (c) to obtain image (e) and by subtracting image (c) to image (d) to obtain image (f). As expected, image (e), to which we attribute φref = 105°, is the opposite of image (f), φref = 285°. The contrast is enhanced in calculated ISHG images.

Fig. 3
Fig. 3

(a) Image of Fig. 2(e) rotated by 90° with a black and white contrast. An area in a domain is delimited in yellow and a profile crossing multiple domains is drawn in blue. (b) The average interferometric contrast in a single χ(2) domain, delimited in yellow in (a), in function of φref. As expected from Eq. (2), it has a sinusoidal shape. (c) The interferometric contrast along a profile crossing multiple sarcomeres, shown in blue in (a), in function of φref. The phase of the SHG generated by each χ(2) domain in the tissue is very well defined with a maximum at either φref = 105° or 285°. The image shown in (c) is in fact a surface made of sinusoidal curves, such as the one shown in (b), with a phase that flips by exactly 180° when encountering a new χ(2) domain while moving along the blue profile drawn in (a).

Fig. 4
Fig. 4

(a) Image of the SHG phase φexp interpolated from ISHG measurements (65 X 20 μm). (b) Histogram of the distribution of pixels from image (a) in function of their SHG phase φexp with Gaussian curve fits on the peaks.

Fig. 5
Fig. 5

(a) A schematic representation of three consecutive sarcomeres. (b) SHG (black) and ISHG (green and red) signals along the profile drawn in (c). To better explain the results, the schematic representation (a) was scaled to match the curve presented in (b). ISHG microscopy can clearly distinguish the χ(2) inversion (separate red and green peaks) while SHG microscopy does not (single peak). These results also highlight the bipolar structural organization of the myosin filaments.

Equations (2)

Equations on this page are rendered with MathJax. Learn more.

I( φ ref )= I ref + I exp +2 I ref I exp cos( φ exp φ ref )
I( φ ref )I( φ ref +π )=4 I ref I exp cos( φ exp φ ref )

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