Abstract

Noninvasive label-free imaging of biological systems raises demand not only for high-speed three-dimensional prescreening of morphology over a wide-field of view but also it seeks to extract the microscopic functional and molecular details within. Capitalizing on the unique advantages brought out by different nonlinear optical effects, a multimodal nonlinear optical microscope can be a powerful tool for bioimaging. Bringing together the intensity-dependent contrast mechanisms via second harmonic generation, third harmonic generation and four-wave mixing for structural-sensitive imaging, and single-beam/single-pulse coherent anti-Stokes Raman scattering technique for chemical sensitive imaging in the finger-print region, we have developed a simple and nearly alignment-free multimodal nonlinear optical microscope that is based on a single wide-band Ti:Sapphire femtosecond pulse laser source. Successful imaging tests have been realized on two exemplary biological samples, a canine femur bone and collagen fibrils harvested from a rat tail. Since the ultra-broad band-width femtosecond laser is a suitable source for performing high-resolution optical coherence tomography, a wide-field optical coherence tomography arm can be easily incorporated into the presented multimodal microscope making it a versatile optical imaging tool for noninvasive label-free bioimaging.

© 2015 Optical Society of America

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References

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2015 (1)

Z. Wang, W. Zheng, C.-Y. S. Hsu, and Z. Huang, “Epi-detected quadruple-modal nonlinear optical microscopy for label-free imaging of the tooth,” Appl. Phys. Lett. 106(3), 033701 (2015).
[Crossref]

2014 (3)

2013 (1)

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

2012 (2)

T. T. Nguyen, C. Gobinet, J. Feru, S. B. Pasco, M. Manfait, and O. Piot, “Characterization of type I and IV collagens by Raman microspectroscopy: Identification of spectral markers of the dermo-epidermal junction,” Spectroscopy: Int. J. 27(5–6), 421–427 (2012).

C. Krafft, B. Dietzek, M. Schmitt, and J. Popp, “Raman and coherent anti-Stokes Raman scattering microspectroscopy for biomedical applications,” J. Biomed. Opt. 17(4), 040801 (2012).
[Crossref] [PubMed]

2011 (6)

S. Yue, M. N. Slipchenko, and J.-X. Cheng, “Multimodal Nonlinear Optical Microscopy,” Laser Photon. Rev. 5(4), 496–512 (2011).
[Crossref] [PubMed]

R. Shahar, C. Lukas, S. Papo, J. W. C. Dunlop, and R. Weinkamer, “Characterization of the spatial arrangement of secondary osteons in the diaphysis of equine and canine long bones,” Anat. Rec. (Hoboken) 294(7), 1093–1102 (2011).
[Crossref] [PubMed]

C. Gullekson, L. Lucas, K. Hewitt, and L. Kreplak, “Surface-sensitive Raman spectroscopy of collagen I fibrils,” Biophys. J. 100(7), 1837–1845 (2011).
[Crossref] [PubMed]

Y. Goulam Houssen, I. Gusachenko, M. C. Schanne-Klein, and J. M. Allain, “Monitoring micrometer-scale collagen organization in rat-tail tendon upon mechanical strain using second harmonic microscopy,” J. Biomech. 44(11), 2047–2052 (2011).
[Crossref] [PubMed]

A. Masic, L. Bertinetti, R. Schuetz, L. Galvis, N. Timofeeva, J. W. C. Dunlop, J. Seto, M. A. Hartmann, and P. Fratzl, “Observations of multiscale, stress-induced changes of collagen orientation in tendon by polarized Raman spectroscopy,” Biomacromolecules 12(11), 3989–3996 (2011).
[Crossref] [PubMed]

V. Raghunathan, Y. Han, O. Korth, N.-H. Ge, and E. O. Potma, “Rapid vibrational imaging with sum frequency generation microscopy,” Opt. Lett. 36(19), 3891–3893 (2011).
[Crossref] [PubMed]

2010 (6)

O. Katz, J. M. Levitt, E. Grinvald, and Y. Silberberg, “Single-beam coherent Raman spectroscopy and microscopy via spectral notch shaping,” Opt. Express 18(22), 22693–22701 (2010).
[Crossref] [PubMed]

M. Raghavan, N. D. Sahar, R. H. Wilson, M.-A. Mycek, N. Pleshko, D. H. Kohn, and M. D. Morris, “Quantitative polarized Raman spectroscopy in highly turbid bone tissue,” J. Biomed. Opt. 15(3), 037001 (2010).
[Crossref] [PubMed]

M. G. Glogowska, M. Komorowska, J. Hanuza, M. Ptak, and M. Kobielarz, “Structural alteration of collagen fibers– spectroscopic and mechanical studies,” Acta Bioeng. Biomech. 12(4), 55–62 (2010).

F. Munhoz, H. Rigneault, and S. Brasselet, “High order symmetry structural properties of vibrational resonances using multiple-field polarization coherent anti-Stokes Raman spectroscopy microscopy,” Phys. Rev. Lett. 105(12), 123903 (2010).
[Crossref] [PubMed]

R. S. Lim, A. Kratzer, N. P. Barry, S. Miyazaki-Anzai, M. Miyazaki, W. W. Mantulin, M. Levi, E. O. Potma, and B. J. Tromberg, “Multimodal CARS microscopy determination of the impact of diet on macrophage infiltration and lipid accumulation on plaque formation in ApoE-deficient mice,” J. Lipid Res. 51(7), 1729–1737 (2010).
[Crossref] [PubMed]

T. T. Le, S. Yue, and J. X. Cheng, “Shedding new light on lipid biology with CARS microscopy,” J. Lipid Res. 51, 3091–3102 (2010).
[Crossref] [PubMed]

2009 (5)

A. Conovaloff, H. W. Wang, J. X. Cheng, and A. Panitch, “Imaging growth of neurites in conditioned hydrogel by coherent anti-stokes Raman scattering microscopy,” Organogenesis 5(4), 231–237 (2009).
[Crossref] [PubMed]

M. N. Slipchenko, T. T. Le, H. Chen, and J. X. Cheng, “High-speed vibrational imaging and spectral analysis of lipid bodies by compound Raman microscopy,” J. Phys. Chem. B 113(21), 7681–7686 (2009).
[Crossref] [PubMed]

W. Min, S. Lu, M. Rueckel, G. R. Holtom, and X. S. Xie, “Near-Degenerate Four-Wave-Mixing Microscopy,” Nano Lett. 9(6), 2423–2426 (2009).
[Crossref] [PubMed]

W. Langbein, I. Rocha-Mendoza, and P. Borri, “Single source coherent anti-Stokes Raman microspectroscopy using spectral focusing,” Appl. Phys. Lett. 95(8), 081109 (2009).
[Crossref]

A. F. Pegoraro, A. Ridsdale, D. J. Moffatt, Y. Jia, J. P. Pezacki, and A. Stolow, “Optimally chirped multimodal CARS microscopy based on a single Ti:sapphire oscillator,” Opt. Express 17(4), 2984–2996 (2009).
[Crossref] [PubMed]

2008 (2)

J. T. Holopainen, P. A. J. Brama, E. Halmesmäki, T. Harjula, J. Tuukkanen, P. R. van Weeren, H. J. Helminen, and M. M. Hyttinen, “Changes in subchondral bone mineral density and collagen matrix organization in growing horses,” Bone 43(6), 1108–1114 (2008).
[Crossref] [PubMed]

C. L. Evans and X. S. Xie, “Coherent anti-Stokes Raman scattering microscopy: chemically selective imaging for biology and medicine,” Annu. Rev. Anal. Chem. 1(1), 883–909 (2008).
[Crossref]

2007 (1)

2006 (3)

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]

H. Peterlik, P. Roschger, K. Klaushofer, and P. Fratzl, “From brittle to ductile fracture of bone,” Nat. Mater. 5(1), 52–55 (2006).
[Crossref] [PubMed]

J. P. R. O. Orgel, T. C. Irving, A. Miller, and T. J. Wess, “Microfibrillar structure of type I collagen in situ,” Proc. Natl. Acad. Sci. U.S.A. 103(24), 9001–9005 (2006).
[Crossref] [PubMed]

2005 (1)

T. J. Wess, “Collagen fibril form and function,” Adv. Protein Chem. 70, 341–374 (2005).
[Crossref] [PubMed]

2004 (4)

J.-X. Cheng and X. S. Xie, “Coherent anti-Stokes Raman scattering microscopy: instrumentation, theory, and applications,” J. Phys. Chem. B 108(3), 827–840 (2004).
[Crossref]

D. L. Marks and S. A. Boppart, “Nonlinear Interferometric Vibrational Imaging,” Phys. Rev. Lett. 92(12), 123905 (2004).
[Crossref] [PubMed]

C. Vinegoni, J. Bredfeldt, D. Marks, and S. Boppart, “Nonlinear optical contrast enhancement for optical coherence tomography,” Opt. Express 12(2), 331–341 (2004).
[Crossref] [PubMed]

Y. Jiang, I. Tomov, Y. Wang, and Z. Chen, “Second-harmonic optical coherence tomography,” Opt. Lett. 29(10), 1090–1092 (2004).
[Crossref] [PubMed]

2003 (5)

A. F. Fercher, W. Drexler, C. K. Hitzenberger, and T. Lasser, “Optical coherence tomography - principles and applications,” Rep. Prog. Phys. 66(2), 239–303 (2003).
[Crossref]

N. Dudovich, D. Oron, and Y. Silberberg, “Single-pulse coherent anti-Stokes Raman spectroscopy in the fingerprint spectral region,” J. Chem. Phys. 118(20), 9208–9215 (2003).
[Crossref]

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: Multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

M. Venturoni, T. Gutsmann, G. E. Fantner, J. H. Kindt, and P. K. Hansma, “Investigations into the polymorphism of rat tail tendon fibrils using atomic force microscopy,” Biochem. Biophys. Res. Commun. 303(2), 508–513 (2003).
[Crossref] [PubMed]

P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21(11), 1356–1360 (2003).
[Crossref] [PubMed]

2002 (1)

N. Dudovich, D. Oron, and Y. Silberberg, “Single-pulse coherently controlled nonlinear Raman spectroscopy and microscopy,” Nature 418(6897), 512–514 (2002).
[Crossref] [PubMed]

1999 (1)

1991 (1)

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[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]

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]

Allain, J. M.

Y. Goulam Houssen, I. Gusachenko, M. C. Schanne-Klein, and J. M. Allain, “Monitoring micrometer-scale collagen organization in rat-tail tendon upon mechanical strain using second harmonic microscopy,” J. Biomech. 44(11), 2047–2052 (2011).
[Crossref] [PubMed]

Andreana, M.

M. Andreana and A. Stolow, “Multimodal nonlinear optical microscopy – from biology to geophotonics,” Opt. Photonics News 25(3), 42–49 (2014).
[Crossref]

Barry, N. P.

R. S. Lim, A. Kratzer, N. P. Barry, S. Miyazaki-Anzai, M. Miyazaki, W. W. Mantulin, M. Levi, E. O. Potma, and B. J. Tromberg, “Multimodal CARS microscopy determination of the impact of diet on macrophage infiltration and lipid accumulation on plaque formation in ApoE-deficient mice,” J. Lipid Res. 51(7), 1729–1737 (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]

Bertinetti, L.

A. Masic, L. Bertinetti, R. Schuetz, L. Galvis, N. Timofeeva, J. W. C. Dunlop, J. Seto, M. A. Hartmann, and P. Fratzl, “Observations of multiscale, stress-induced changes of collagen orientation in tendon by polarized Raman spectroscopy,” Biomacromolecules 12(11), 3989–3996 (2011).
[Crossref] [PubMed]

Boppart, S.

Boppart, S. A.

D. L. Marks and S. A. Boppart, “Nonlinear Interferometric Vibrational Imaging,” Phys. Rev. Lett. 92(12), 123905 (2004).
[Crossref] [PubMed]

Borri, P.

W. Langbein, I. Rocha-Mendoza, and P. Borri, “Single source coherent anti-Stokes Raman microspectroscopy using spectral focusing,” Appl. Phys. Lett. 95(8), 081109 (2009).
[Crossref]

Brama, P. A. J.

J. T. Holopainen, P. A. J. Brama, E. Halmesmäki, T. Harjula, J. Tuukkanen, P. R. van Weeren, H. J. Helminen, and M. M. Hyttinen, “Changes in subchondral bone mineral density and collagen matrix organization in growing horses,” Bone 43(6), 1108–1114 (2008).
[Crossref] [PubMed]

Brasselet, S.

F. Munhoz, H. Rigneault, and S. Brasselet, “High order symmetry structural properties of vibrational resonances using multiple-field polarization coherent anti-Stokes Raman spectroscopy microscopy,” Phys. Rev. Lett. 105(12), 123903 (2010).
[Crossref] [PubMed]

Bredfeldt, J.

Campagnola, P. J.

P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21(11), 1356–1360 (2003).
[Crossref] [PubMed]

Chang, W.

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Miyazaki-Anzai, S.

R. S. Lim, A. Kratzer, N. P. Barry, S. Miyazaki-Anzai, M. Miyazaki, W. W. Mantulin, M. Levi, E. O. Potma, and B. J. Tromberg, “Multimodal CARS microscopy determination of the impact of diet on macrophage infiltration and lipid accumulation on plaque formation in ApoE-deficient mice,” J. Lipid Res. 51(7), 1729–1737 (2010).
[Crossref] [PubMed]

Moffatt, D. J.

Morris, M. D.

M. Raghavan, N. D. Sahar, R. H. Wilson, M.-A. Mycek, N. Pleshko, D. H. Kohn, and M. D. Morris, “Quantitative polarized Raman spectroscopy in highly turbid bone tissue,” J. Biomed. Opt. 15(3), 037001 (2010).
[Crossref] [PubMed]

Munhoz, F.

F. Munhoz, H. Rigneault, and S. Brasselet, “High order symmetry structural properties of vibrational resonances using multiple-field polarization coherent anti-Stokes Raman spectroscopy microscopy,” Phys. Rev. Lett. 105(12), 123903 (2010).
[Crossref] [PubMed]

Mycek, M.-A.

M. Raghavan, N. D. Sahar, R. H. Wilson, M.-A. Mycek, N. Pleshko, D. H. Kohn, and M. D. Morris, “Quantitative polarized Raman spectroscopy in highly turbid bone tissue,” J. Biomed. Opt. 15(3), 037001 (2010).
[Crossref] [PubMed]

Nguyen, T. T.

T. T. Nguyen, C. Gobinet, J. Feru, S. B. Pasco, M. Manfait, and O. Piot, “Characterization of type I and IV collagens by Raman microspectroscopy: Identification of spectral markers of the dermo-epidermal junction,” Spectroscopy: Int. J. 27(5–6), 421–427 (2012).

Orgel, J. P. R. O.

J. P. R. O. Orgel, T. C. Irving, A. Miller, and T. J. Wess, “Microfibrillar structure of type I collagen in situ,” Proc. Natl. Acad. Sci. U.S.A. 103(24), 9001–9005 (2006).
[Crossref] [PubMed]

Oron, D.

N. Dudovich, D. Oron, and Y. Silberberg, “Single-pulse coherent anti-Stokes Raman spectroscopy in the fingerprint spectral region,” J. Chem. Phys. 118(20), 9208–9215 (2003).
[Crossref]

N. Dudovich, D. Oron, and Y. Silberberg, “Single-pulse coherently controlled nonlinear Raman spectroscopy and microscopy,” Nature 418(6897), 512–514 (2002).
[Crossref] [PubMed]

Panitch, A.

A. Conovaloff, H. W. Wang, J. X. Cheng, and A. Panitch, “Imaging growth of neurites in conditioned hydrogel by coherent anti-stokes Raman scattering microscopy,” Organogenesis 5(4), 231–237 (2009).
[Crossref] [PubMed]

Papo, S.

R. Shahar, C. Lukas, S. Papo, J. W. C. Dunlop, and R. Weinkamer, “Characterization of the spatial arrangement of secondary osteons in the diaphysis of equine and canine long bones,” Anat. Rec. (Hoboken) 294(7), 1093–1102 (2011).
[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]

Pasco, S. B.

T. T. Nguyen, C. Gobinet, J. Feru, S. B. Pasco, M. Manfait, and O. Piot, “Characterization of type I and IV collagens by Raman microspectroscopy: Identification of spectral markers of the dermo-epidermal junction,” Spectroscopy: Int. J. 27(5–6), 421–427 (2012).

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]

Peterlik, H.

H. Peterlik, P. Roschger, K. Klaushofer, and P. Fratzl, “From brittle to ductile fracture of bone,” Nat. Mater. 5(1), 52–55 (2006).
[Crossref] [PubMed]

Pezacki, J. P.

Piot, O.

T. T. Nguyen, C. Gobinet, J. Feru, S. B. Pasco, M. Manfait, and O. Piot, “Characterization of type I and IV collagens by Raman microspectroscopy: Identification of spectral markers of the dermo-epidermal junction,” Spectroscopy: Int. J. 27(5–6), 421–427 (2012).

Pleshko, N.

M. Raghavan, N. D. Sahar, R. H. Wilson, M.-A. Mycek, N. Pleshko, D. H. Kohn, and M. D. Morris, “Quantitative polarized Raman spectroscopy in highly turbid bone tissue,” J. Biomed. Opt. 15(3), 037001 (2010).
[Crossref] [PubMed]

Popp, J.

C. Krafft, B. Dietzek, M. Schmitt, and J. Popp, “Raman and coherent anti-Stokes Raman scattering microspectroscopy for biomedical applications,” J. Biomed. Opt. 17(4), 040801 (2012).
[Crossref] [PubMed]

Potma, E. O.

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

V. Raghunathan, Y. Han, O. Korth, N.-H. Ge, and E. O. Potma, “Rapid vibrational imaging with sum frequency generation microscopy,” Opt. Lett. 36(19), 3891–3893 (2011).
[Crossref] [PubMed]

R. S. Lim, A. Kratzer, N. P. Barry, S. Miyazaki-Anzai, M. Miyazaki, W. W. Mantulin, M. Levi, E. O. Potma, and B. J. Tromberg, “Multimodal CARS microscopy determination of the impact of diet on macrophage infiltration and lipid accumulation on plaque formation in ApoE-deficient mice,” J. Lipid Res. 51(7), 1729–1737 (2010).
[Crossref] [PubMed]

Považay, B.

Ptak, M.

M. G. Glogowska, M. Komorowska, J. Hanuza, M. Ptak, and M. Kobielarz, “Structural alteration of collagen fibers– spectroscopic and mechanical studies,” Acta Bioeng. Biomech. 12(4), 55–62 (2010).

Puliafito, C. A.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

Raghavan, M.

M. Raghavan, N. D. Sahar, R. H. Wilson, M.-A. Mycek, N. Pleshko, D. H. Kohn, and M. D. Morris, “Quantitative polarized Raman spectroscopy in highly turbid bone tissue,” J. Biomed. Opt. 15(3), 037001 (2010).
[Crossref] [PubMed]

Raghunathan, V.

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

V. Raghunathan, Y. Han, O. Korth, N.-H. Ge, and E. O. Potma, “Rapid vibrational imaging with sum frequency generation microscopy,” Opt. Lett. 36(19), 3891–3893 (2011).
[Crossref] [PubMed]

Ridsdale, A.

Rigneault, H.

F. Munhoz, H. Rigneault, and S. Brasselet, “High order symmetry structural properties of vibrational resonances using multiple-field polarization coherent anti-Stokes Raman spectroscopy microscopy,” Phys. Rev. Lett. 105(12), 123903 (2010).
[Crossref] [PubMed]

Rocha-Mendoza, I.

W. Langbein, I. Rocha-Mendoza, and P. Borri, “Single source coherent anti-Stokes Raman microspectroscopy using spectral focusing,” Appl. Phys. Lett. 95(8), 081109 (2009).
[Crossref]

Roschger, P.

H. Peterlik, P. Roschger, K. Klaushofer, and P. Fratzl, “From brittle to ductile fracture of bone,” Nat. Mater. 5(1), 52–55 (2006).
[Crossref] [PubMed]

Rueckel, M.

W. Min, S. Lu, M. Rueckel, G. R. Holtom, and X. S. Xie, “Near-Degenerate Four-Wave-Mixing Microscopy,” Nano Lett. 9(6), 2423–2426 (2009).
[Crossref] [PubMed]

Sahar, N. D.

M. Raghavan, N. D. Sahar, R. H. Wilson, M.-A. Mycek, N. Pleshko, D. H. Kohn, and M. D. Morris, “Quantitative polarized Raman spectroscopy in highly turbid bone tissue,” J. Biomed. Opt. 15(3), 037001 (2010).
[Crossref] [PubMed]

Schanne-Klein, M. C.

Y. Goulam Houssen, I. Gusachenko, M. C. Schanne-Klein, and J. M. Allain, “Monitoring micrometer-scale collagen organization in rat-tail tendon upon mechanical strain using second harmonic microscopy,” J. Biomech. 44(11), 2047–2052 (2011).
[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]

Schmitt, M.

C. Krafft, B. Dietzek, M. Schmitt, and J. Popp, “Raman and coherent anti-Stokes Raman scattering microspectroscopy for biomedical applications,” J. Biomed. Opt. 17(4), 040801 (2012).
[Crossref] [PubMed]

Schuetz, R.

A. Masic, L. Bertinetti, R. Schuetz, L. Galvis, N. Timofeeva, J. W. C. Dunlop, J. Seto, M. A. Hartmann, and P. Fratzl, “Observations of multiscale, stress-induced changes of collagen orientation in tendon by polarized Raman spectroscopy,” Biomacromolecules 12(11), 3989–3996 (2011).
[Crossref] [PubMed]

Schuman, J. S.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

Seto, J.

A. Masic, L. Bertinetti, R. Schuetz, L. Galvis, N. Timofeeva, J. W. C. Dunlop, J. Seto, M. A. Hartmann, and P. Fratzl, “Observations of multiscale, stress-induced changes of collagen orientation in tendon by polarized Raman spectroscopy,” Biomacromolecules 12(11), 3989–3996 (2011).
[Crossref] [PubMed]

Shahar, R.

R. Shahar, C. Lukas, S. Papo, J. W. C. Dunlop, and R. Weinkamer, “Characterization of the spatial arrangement of secondary osteons in the diaphysis of equine and canine long bones,” Anat. Rec. (Hoboken) 294(7), 1093–1102 (2011).
[Crossref] [PubMed]

Silberberg, Y.

Slipchenko, M. N.

S. Yue, M. N. Slipchenko, and J.-X. Cheng, “Multimodal Nonlinear Optical Microscopy,” Laser Photon. Rev. 5(4), 496–512 (2011).
[Crossref] [PubMed]

M. N. Slipchenko, T. T. Le, H. Chen, and J. X. Cheng, “High-speed vibrational imaging and spectral analysis of lipid bodies by compound Raman microscopy,” J. Phys. Chem. B 113(21), 7681–7686 (2009).
[Crossref] [PubMed]

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]

Stinson, W. G.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

Stolow, A.

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]

Swanson, E. A.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

Teh, S.

Timofeeva, N.

A. Masic, L. Bertinetti, R. Schuetz, L. Galvis, N. Timofeeva, J. W. C. Dunlop, J. Seto, M. A. Hartmann, and P. Fratzl, “Observations of multiscale, stress-induced changes of collagen orientation in tendon by polarized Raman spectroscopy,” Biomacromolecules 12(11), 3989–3996 (2011).
[Crossref] [PubMed]

Tomov, I.

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]

Tromberg, B. J.

R. S. Lim, A. Kratzer, N. P. Barry, S. Miyazaki-Anzai, M. Miyazaki, W. W. Mantulin, M. Levi, E. O. Potma, and B. J. Tromberg, “Multimodal CARS microscopy determination of the impact of diet on macrophage infiltration and lipid accumulation on plaque formation in ApoE-deficient mice,” J. Lipid Res. 51(7), 1729–1737 (2010).
[Crossref] [PubMed]

Tuukkanen, J.

J. T. Holopainen, P. A. J. Brama, E. Halmesmäki, T. Harjula, J. Tuukkanen, P. R. van Weeren, H. J. Helminen, and M. M. Hyttinen, “Changes in subchondral bone mineral density and collagen matrix organization in growing horses,” Bone 43(6), 1108–1114 (2008).
[Crossref] [PubMed]

Unterhuber, A.

van Weeren, P. R.

J. T. Holopainen, P. A. J. Brama, E. Halmesmäki, T. Harjula, J. Tuukkanen, P. R. van Weeren, H. J. Helminen, and M. M. Hyttinen, “Changes in subchondral bone mineral density and collagen matrix organization in growing horses,” Bone 43(6), 1108–1114 (2008).
[Crossref] [PubMed]

Venturoni, M.

M. Venturoni, T. Gutsmann, G. E. Fantner, J. H. Kindt, and P. K. Hansma, “Investigations into the polymorphism of rat tail tendon fibrils using atomic force microscopy,” Biochem. Biophys. Res. Commun. 303(2), 508–513 (2003).
[Crossref] [PubMed]

Vinegoni, C.

Wang, H. W.

A. Conovaloff, H. W. Wang, J. X. Cheng, and A. Panitch, “Imaging growth of neurites in conditioned hydrogel by coherent anti-stokes Raman scattering microscopy,” Organogenesis 5(4), 231–237 (2009).
[Crossref] [PubMed]

Wang, Y.

Wang, Z.

Z. Wang, W. Zheng, C.-Y. S. Hsu, and Z. Huang, “Epi-detected quadruple-modal nonlinear optical microscopy for label-free imaging of the tooth,” Appl. Phys. Lett. 106(3), 033701 (2015).
[Crossref]

J. Lin, S. Teh, W. Zheng, Z. Wang, and Z. Huang, “Multimodal nonlinear optical microscopic imaging provides new insights into acetowhitening mechanisms in live mammalian cells without labeling,” Biomed. Opt. Express 5(9), 3116–3122 (2014).
[Crossref] [PubMed]

Webb, W. W.

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: Multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

Weinkamer, R.

R. Shahar, C. Lukas, S. Papo, J. W. C. Dunlop, and R. Weinkamer, “Characterization of the spatial arrangement of secondary osteons in the diaphysis of equine and canine long bones,” Anat. Rec. (Hoboken) 294(7), 1093–1102 (2011).
[Crossref] [PubMed]

Werkmeister, R.

Wess, T. J.

J. P. R. O. Orgel, T. C. Irving, A. Miller, and T. J. Wess, “Microfibrillar structure of type I collagen in situ,” Proc. Natl. Acad. Sci. U.S.A. 103(24), 9001–9005 (2006).
[Crossref] [PubMed]

T. J. Wess, “Collagen fibril form and function,” Adv. Protein Chem. 70, 341–374 (2005).
[Crossref] [PubMed]

Williams, R. M.

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: Multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

Wilson, R. H.

M. Raghavan, N. D. Sahar, R. H. Wilson, M.-A. Mycek, N. Pleshko, D. H. Kohn, and M. D. Morris, “Quantitative polarized Raman spectroscopy in highly turbid bone tissue,” J. Biomed. Opt. 15(3), 037001 (2010).
[Crossref] [PubMed]

Wong, S. T. C.

Xie, X. S.

W. Min, S. Lu, M. Rueckel, G. R. Holtom, and X. S. Xie, “Near-Degenerate Four-Wave-Mixing Microscopy,” Nano Lett. 9(6), 2423–2426 (2009).
[Crossref] [PubMed]

C. L. Evans and X. S. Xie, “Coherent anti-Stokes Raman scattering microscopy: chemically selective imaging for biology and medicine,” Annu. Rev. Anal. Chem. 1(1), 883–909 (2008).
[Crossref]

C. L. Evans, X. Xu, S. Kesari, X. S. Xie, S. T. C. Wong, and G. S. Young, “Chemically-selective imaging of brain structures with CARS microscopy,” Opt. Express 15(19), 12076–12087 (2007).
[Crossref] [PubMed]

J.-X. Cheng and X. S. Xie, “Coherent anti-Stokes Raman scattering microscopy: instrumentation, theory, and applications,” J. Phys. Chem. B 108(3), 827–840 (2004).
[Crossref]

Xu, X.

Yelin, D.

Young, G. S.

Yue, S.

S. Yue, M. N. Slipchenko, and J.-X. Cheng, “Multimodal Nonlinear Optical Microscopy,” Laser Photon. Rev. 5(4), 496–512 (2011).
[Crossref] [PubMed]

T. T. Le, S. Yue, and J. X. Cheng, “Shedding new light on lipid biology with CARS microscopy,” J. Lipid Res. 51, 3091–3102 (2010).
[Crossref] [PubMed]

Zheng, W.

Z. Wang, W. Zheng, C.-Y. S. Hsu, and Z. Huang, “Epi-detected quadruple-modal nonlinear optical microscopy for label-free imaging of the tooth,” Appl. Phys. Lett. 106(3), 033701 (2015).
[Crossref]

J. Lin, S. Teh, W. Zheng, Z. Wang, and Z. Huang, “Multimodal nonlinear optical microscopic imaging provides new insights into acetowhitening mechanisms in live mammalian cells without labeling,” Biomed. Opt. Express 5(9), 3116–3122 (2014).
[Crossref] [PubMed]

Zipfel, W. R.

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: Multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

Acta Bioeng. Biomech. (1)

M. G. Glogowska, M. Komorowska, J. Hanuza, M. Ptak, and M. Kobielarz, “Structural alteration of collagen fibers– spectroscopic and mechanical studies,” Acta Bioeng. Biomech. 12(4), 55–62 (2010).

Adv. Protein Chem. (1)

T. J. Wess, “Collagen fibril form and function,” Adv. Protein Chem. 70, 341–374 (2005).
[Crossref] [PubMed]

Anat. Rec. (Hoboken) (1)

R. Shahar, C. Lukas, S. Papo, J. W. C. Dunlop, and R. Weinkamer, “Characterization of the spatial arrangement of secondary osteons in the diaphysis of equine and canine long bones,” Anat. Rec. (Hoboken) 294(7), 1093–1102 (2011).
[Crossref] [PubMed]

Annu. Rev. Anal. Chem. (1)

C. L. Evans and X. S. Xie, “Coherent anti-Stokes Raman scattering microscopy: chemically selective imaging for biology and medicine,” Annu. Rev. Anal. Chem. 1(1), 883–909 (2008).
[Crossref]

Appl. Phys. Lett. (2)

Z. Wang, W. Zheng, C.-Y. S. Hsu, and Z. Huang, “Epi-detected quadruple-modal nonlinear optical microscopy for label-free imaging of the tooth,” Appl. Phys. Lett. 106(3), 033701 (2015).
[Crossref]

W. Langbein, I. Rocha-Mendoza, and P. Borri, “Single source coherent anti-Stokes Raman microspectroscopy using spectral focusing,” Appl. Phys. Lett. 95(8), 081109 (2009).
[Crossref]

Biochem. Biophys. Res. Commun. (1)

M. Venturoni, T. Gutsmann, G. E. Fantner, J. H. Kindt, and P. K. Hansma, “Investigations into the polymorphism of rat tail tendon fibrils using atomic force microscopy,” Biochem. Biophys. Res. Commun. 303(2), 508–513 (2003).
[Crossref] [PubMed]

Biomacromolecules (1)

A. Masic, L. Bertinetti, R. Schuetz, L. Galvis, N. Timofeeva, J. W. C. Dunlop, J. Seto, M. A. Hartmann, and P. Fratzl, “Observations of multiscale, stress-induced changes of collagen orientation in tendon by polarized Raman spectroscopy,” Biomacromolecules 12(11), 3989–3996 (2011).
[Crossref] [PubMed]

Biomed. Opt. Express (1)

Biophys. J. (2)

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

C. Gullekson, L. Lucas, K. Hewitt, and L. Kreplak, “Surface-sensitive Raman spectroscopy of collagen I fibrils,” Biophys. J. 100(7), 1837–1845 (2011).
[Crossref] [PubMed]

Biopolymers (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]

Bone (1)

J. T. Holopainen, P. A. J. Brama, E. Halmesmäki, T. Harjula, J. Tuukkanen, P. R. van Weeren, H. J. Helminen, and M. M. Hyttinen, “Changes in subchondral bone mineral density and collagen matrix organization in growing horses,” Bone 43(6), 1108–1114 (2008).
[Crossref] [PubMed]

J. Biomech. (1)

Y. Goulam Houssen, I. Gusachenko, M. C. Schanne-Klein, and J. M. Allain, “Monitoring micrometer-scale collagen organization in rat-tail tendon upon mechanical strain using second harmonic microscopy,” J. Biomech. 44(11), 2047–2052 (2011).
[Crossref] [PubMed]

J. Biomed. Opt. (2)

M. Raghavan, N. D. Sahar, R. H. Wilson, M.-A. Mycek, N. Pleshko, D. H. Kohn, and M. D. Morris, “Quantitative polarized Raman spectroscopy in highly turbid bone tissue,” J. Biomed. Opt. 15(3), 037001 (2010).
[Crossref] [PubMed]

C. Krafft, B. Dietzek, M. Schmitt, and J. Popp, “Raman and coherent anti-Stokes Raman scattering microspectroscopy for biomedical applications,” J. Biomed. Opt. 17(4), 040801 (2012).
[Crossref] [PubMed]

J. Chem. Phys. (1)

N. Dudovich, D. Oron, and Y. Silberberg, “Single-pulse coherent anti-Stokes Raman spectroscopy in the fingerprint spectral region,” J. Chem. Phys. 118(20), 9208–9215 (2003).
[Crossref]

J. Lipid Res. (2)

R. S. Lim, A. Kratzer, N. P. Barry, S. Miyazaki-Anzai, M. Miyazaki, W. W. Mantulin, M. Levi, E. O. Potma, and B. J. Tromberg, “Multimodal CARS microscopy determination of the impact of diet on macrophage infiltration and lipid accumulation on plaque formation in ApoE-deficient mice,” J. Lipid Res. 51(7), 1729–1737 (2010).
[Crossref] [PubMed]

T. T. Le, S. Yue, and J. X. Cheng, “Shedding new light on lipid biology with CARS microscopy,” J. Lipid Res. 51, 3091–3102 (2010).
[Crossref] [PubMed]

J. Phys. Chem. B (3)

J.-X. Cheng and X. S. Xie, “Coherent anti-Stokes Raman scattering microscopy: instrumentation, theory, and applications,” J. Phys. Chem. B 108(3), 827–840 (2004).
[Crossref]

M. N. Slipchenko, T. T. Le, H. Chen, and J. X. Cheng, “High-speed vibrational imaging and spectral analysis of lipid bodies by compound Raman microscopy,” J. Phys. Chem. B 113(21), 7681–7686 (2009).
[Crossref] [PubMed]

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

Laser Photon. Rev. (1)

S. Yue, M. N. Slipchenko, and J.-X. Cheng, “Multimodal Nonlinear Optical Microscopy,” Laser Photon. Rev. 5(4), 496–512 (2011).
[Crossref] [PubMed]

Nano Lett. (1)

W. Min, S. Lu, M. Rueckel, G. R. Holtom, and X. S. Xie, “Near-Degenerate Four-Wave-Mixing Microscopy,” Nano Lett. 9(6), 2423–2426 (2009).
[Crossref] [PubMed]

Nat. Biotechnol. (2)

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: Multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

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Figures (8)

Fig. 1
Fig. 1 Schematic energy level diagram for the multi-photon processes; (a) second harmonic generation, (b) third harmonic generation, (c) a combination of resonant and nonresonant coherent anti-Stokes Raman scattering, and (d) purely nonresonant electronic four wave mixing which contributes to a broad-band background signal in the spectral domain or an ultrashort temporal component at zero in the time-domain. By applying a narrow band-width pump and probe (green), and a broad band-width stokes photons (red), there are three cases of the four wave mixing signal generation, namely, the resonant excitation of one vibrational level with frequency Ω along with a large number of nonresonant levels represented by the dashed lines in (c) and only nonresonant contribution in (d). The four wave mixing process presented in (d) is purely nonresonant in nature as no real vibrational level has been addressed by the three incident laser fields. A combination of processes represented in (c) and (d) contribute to the total four wave mixing signal in the experiments and hence the total signal has a very small resonant contribution as compared to the large nonresonant signal.
Fig. 2
Fig. 2 Single pulse CARS scheme explained. (a) Simulated traces of Gaussian femtosecond (fs) laser pulses in wavelength and the time domain compared for the pulses as they are vis-à-vis shaped using a notch filter. The effect of a narrow notch feature in the spectral domain results into a picosecond delayed component in the pulse in the time-domain. (b) Schematic energy level picture of the broad-band pump and stokes pulses coherently exciting vibrational modes with frequencies Ωi which are frequency-resolved using a narrow probe. (c-d) Actual experimental results on toluene showing the strong Raman vibrational bands coherently excited and spectrally resolved using the single pulse CARS scheme. The notch-shaped laser pulse spectra for three different angular positions of the notch filter are shown in the upper panel of (c) and the corresponding FWM spectra are shown in the lower panel of (c) along with that for the notch location for which there are no resonant features in detected spectral window (black dashed curve). (d) Normalized difference FWM spectra showing the spectrally resolved CARS features at the expected frequencies. These features move with the excitation notch location (the peaks are connected by dashed lines for a reference). For the probe notch location at 772 nm, the CARS features appear at 716, 727 and 706 nm which correspond to Raman frequencies of ~1010 cm−1, 793 cm−1 and 1202 cm−1, respectively.
Fig. 3
Fig. 3 Layout of the multimodal nonlinear optical microscopy setup used for simultaneous second harmonic generation (SHG), third harmonic generation (THG), resonant coherent anti-Stokes Raman scattering (CARS), and four wave mixing (FWM) micro-spectroscopic imaging of biological samples. The forward propagation light scattered through the sample is spectrally selected by various dichroic mirrors (DM), short-pass filters (SPF) or band-pass filters (BPF) before it is detected at the corresponding photomultiplier tube (PMT). The resonant detection of a CARS signal is achieved by a pair of notch filters (NF), one tunable excitation notch and one fixed detection notch. The spectrally resolved and time-integrated light is detected using a spectrometer and PMTs, respectively. This experimental system is capable of producing simultaneous two photon excited fluorescence (TPEF) micrographs in the epi-direction.
Fig. 4
Fig. 4 (a) As recorded spectra (upper panel) of the forward propagating four wave mixing generated light from the canine femur bone sample shown for two positions of the excitation notch location such that for one there is just the nonresonant background FWM signal (lower curve) and for the other there is a resonant CARS feature superimposed on the nonresonant background in the observation window of the spectrometer, and the normalized difference FWM spectrum (lower panel) revealing the resonant CARS feature at a frequency of ~960 cm−1. (b) Microscope generated real images of the bone sample set for simultaneous SHG, THG, FWM and the resonant CARS imaging at frequency 960 cm−1 as marked in the corresponding images. The results in each modality have been drawn with a single color, i.e., CARS in red, SHG in blue, THG in gray and FWM in coral, between the minimum (color black) and the maximum (color white). The scanned area is 250μm × 250μm with 1μm pixel size. The black dot near the top edge in the images (as marked in the THG image) is the Haversian canal in the bone which provides a good landmark for imaging around it. Scale bar is 50μm. The interlinking of atleast four Osteons can be identified in the images which have been marked with dashed lines in the THG image.
Fig. 5
Fig. 5 SHG and THG contrast images of canine femur bone sample taken over an scan area of 250µm × 250µm recorded at various depth positions (z) of the focal plane inside the sample relative to its first position (z = 0 for the left most image).
Fig. 6
Fig. 6 Nonlinear optical images of a rat tail tendon taken simultaneously using the resonant CARS for collagen imaging at ~1260 cm−1, FWM, SHG and THG imaging modalities of the custom-built MNLOM platform. The scale bar is 50μm. For estimating the areal density of the collagen fibrils, a square area (dashed in yellow) of length 50μm is chosen within the SHG image of the sample.
Fig. 7
Fig. 7 Wide-field prescreening of the canine femur bone obtained using SD-OCT setup described in [43] covering 8.4mm × 4.4mm area of the sample surface: enface view summed up over all depth information (top) and cross-sectional slice (bottom) of size 1024 pixels × 512 pixels.
Fig. 8
Fig. 8 Wide field SD-OCT images of the rat tail tendon taken using custom-built SD-OCT setup described in [43] for the front view (a) and top view (b). A total 4.2mm × 1.1mm area of the sample surface was covered.

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