Abstract

We demonstrate multimodal label-free nonlinear optical microscopy in human skin enabled by a fiber-based two-color ultrafast source. Energetic femtosecond pulses at 775 nm and 1250 nm are simultaneously generated by an Er-fiber laser source employing frequency doubling and self-phase modulation enabled spectral selection. The integrated nonlinear optical microscope driven by such a two-color femtosecond source enables the excitation of endogenous two-photon excitation fluorescence, second-harmonic generation, and third-harmonic generation in human skin. Such a 3-channel imaging platform constitutes a powerful tool for clinical application and optical virtual skin biopsy.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2019 (1)

H.-Y. Chung, W. Liu, Q. Cao, R. Greinert, F. X. Kärtner, and G. Q. Chang, “Tunable, ultrafast fiber-laser between 1.15 and 1.35 µm for harmonic generation microscopy in human skin,” IEEE J. Sel. Topics in Quantum Elec. 25(1), 6800708 (2019).

2018 (2)

2017 (5)

J.-Y. Huang, L.-Z. Guo, J.-Z. Wang, T.-C. Li, H.-J. Lee, P.-K. Chiu, L.-H. Peng, and T.-M. Liu, “Fiber-based 1150-nm femtosecond laser source for the minimally invasive harmonic generation microscopy,” J. Biomed. Opt. 22(3), 036008 (2017).
[Crossref] [PubMed]

W. Liu, S.-H. Chia, H.-Y. Chung, R. Greinert, F. X. Kärtner, and G. Chang, “Energetic ultrafast fiber laser sources tunable in 1030-1215 nm for deep tissue multi-photon microscopy,” Opt. Express 25(6), 6822–6831 (2017).
[Crossref] [PubMed]

H.-Y. Chung, W. Liu, Q. Cao, F. X. Kärtner, and G. Chang, “Er-fiber laser enabled, energy scalable femtosecond source tunable from 1.3 to 1.7 µm,” Opt. Express 25(14), 15760–15771 (2017).
[Crossref] [PubMed]

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[Crossref] [PubMed]

J. Xu, D. Kang, Y. Zeng, S. Zhuo, X. Zhu, L. Jiang, J. Chen, and J. Lin, “Multiphoton microscopy for label-free identification of intramural metastasis in human esophageal squamous cell carcinoma,” Biomed. Opt. Express 8(7), 3360–3368 (2017).
[Crossref] [PubMed]

2016 (5)

2015 (2)

M. Weinigel, H. G. Breunig, A. Uchugonova, and K. König, “Multipurpose nonlinear optical imaging system for in vivo and ex vivo multimodal histology,” J. Med. Imaging (Bellingham) 2(1), 016003 (2015).
[Crossref] [PubMed]

R. P. Judy, J. J. Keating, E. M. DeJesus, J. X. Jiang, O. T. Okusanya, S. Nie, D. E. Holt, S. P. Arlauckas, P. S. Low, E. J. Delikatny, and S. Singhal, “Quantification of tumor fluorescence during intraoperative optical cancer imaging,” Sci. Rep. 5(1), 16208 (2015).
[Crossref] [PubMed]

2014 (3)

M. E. Darvin, H. Richter, Y. J. Zhu, M. C. Meinke, F. Knorr, S. A. Gonchukov, K. König, and J. Lademann, “Comparison of in vivo and ex vivo laser scanning microscopy and multiphoton tomography application for human and porcine skin imaging,” Quantum Electron. 44(7), 646–651 (2014).
[Crossref]

J. R. W. Conway, N. O. Carragher, and P. Timpson, “Developments in preclinical cancer imaging: innovating the discovery of therapeutics,” Nat. Rev. Cancer 14(5), 314–328 (2014).
[Crossref] [PubMed]

L. A. Sordillo, Y. Pu, S. Pratavieira, Y. Budansky, and R. R. Alfano, “Deep optical imaging of tissue using the second and third near-infrared spectral windows,” J. Biomed. Opt. 19(5), 056004 (2014).
[Crossref] [PubMed]

2013 (3)

C. Xu and F. W. Wise, “Recent advances in fiber lasers for nonlinear microscopy,” Nat. Photonics 7(11), 875–882 (2013).
[Crossref] [PubMed]

Y.-H. Liao, S.-Y. Chen, S.-Y. Chou, P.-H. Wang, M.-R. Tsai, and C.-K. Sun, “Determination of chronological aging parameters in epidermal keratinocytes by in vivo harmonic generation microscopy,” Biomed. Opt. Express 4(1), 77–88 (2013).
[Crossref] [PubMed]

M. Balu, A. Mazhar, C. K. Hayakawa, R. Mittal, T. B. Krasieva, K. König, V. Venugopalan, and B. J. Tromberg, “In vivo multiphoton NADH fluorescence reveals depth-dependent keratinocyte metabolism in human skin,” Biophys. J. 104(1), 258–267 (2013).
[Crossref] [PubMed]

2012 (4)

H. A. El Madani, E. Tancrède-Bohin, A. Bensussan, A. Colonna, A. Dupuy, M. Bagot, and A.-M. Pena, “In vivo multiphoton imaging of human skin: assessment of topical corticosteroid-induced epidermis atrophy and depigmentation,” J. Biomed. Opt. 17(2), 026009 (2012).
[Crossref] [PubMed]

B. Weigelin, G.-J. Bakker, and P. Friedl, “Intravital third harmonic generation microscopy of collective melanoma cell invasion: Principles of interface guidance and microvesicle dynamics,” Intravital 1(1), 32–43 (2012).
[Crossref] [PubMed]

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]

Y. Liu, H. Tu, and S. A. Boppart, “Wave-breaking-extended fiber supercontinuum generation for high compression ratio transform-limited pulse compression,” Opt. Lett. 37(12), 2172–2174 (2012).
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2011 (5)

M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods 8(5), 393–399 (2011).
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C. Thrasivoulou, G. Virich, T. Krenacs, I. Korom, and D. L. Becker, “Optical delineation of human malignant melanoma using second harmonic imaging of collagen,” Biomed. Opt. Express 2(5), 1282–1295 (2011).
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M.-R. Tsai, S.-Y. Chen, D.-B. Shieh, P.-J. Lou, and C.-K. Sun, “In vivo optical virtual biopsy of human oral mucosa with harmonic generation microscopy,” Biomed. Opt. Express 2(8), 2317–2328 (2011).
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P. Campagnola, “Second harmonic generation imaging microscopy: applications to diseases diagnostics,” Anal. Chem. 83(9), 3224–3231 (2011).
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S. Witte, A. Negrean, J. C. Lodder, C. P. J. de Kock, G. Testa Silva, H. D. Mansvelder, and M. Louise Groot, “Label-free live brain imaging and targeted patching with third-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A. 108(15), 5970–5975 (2011).
[Crossref] [PubMed]

2010 (4)

F. Aptel, N. Olivier, A. Deniset-Besseau, J.-M. Legeais, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, “Multimodal nonlinear imaging of the human cornea,” Invest. Ophthalmol. Vis. Sci. 51(5), 2459–2465 (2010).
[Crossref] [PubMed]

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer 10(1), 94 (2010).
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H. G. Breunig, H. Studier, and K. König, “Multiphoton excitation characteristics of cellular fluorophores of human skin in vivo,” Opt. Express 18(8), 7857–7871 (2010).
[Crossref] [PubMed]

S.-Y. Chen, S.-U. Chen, H.-Y. Wu, W.-J. Lee, Y.-H. Liao, and C.-K. Sun, “In vivo virtual biopsy of human skin by using noninvasive higher harmonic generation microscopy,” IEEE J. Sel. Topics in Quantum Elec. 16(3), 478–492 (2010).
[Crossref]

2009 (5)

2008 (4)

C.-S. Hsieh, S.-U. Chen, Y.-W. Lee, Y.-S. Yang, and C.-K. Sun, “Higher harmonic generation microscopy of in vitro cultured mammal oocytes and embryos,” Opt. Express 16(15), 11574–11588 (2008).
[PubMed]

D. Träutlein, F. Adler, K. Moutzouris, A. Jeromin, A. Leitenstorfer, and E. Ferrando-May, “Highly versatile confocal microscopy system based on a tunable femtosecond Er:fiber source,” J. Biophotonics 1(1), 53–61 (2008).
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J. Paoli, M. Smedh, A.-M. Wennberg, and M. B. Ericson, “Multiphoton laser scanning microscopy on non-melanoma skin cancer: morphologic features for future non-invasive diagnostics,” J. Invest. Dermatol. 128(5), 1248–1255 (2008).
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T. Hompland, A. Erikson, M. Lindgren, T. Lindmo, and C. de Lange Davies, “Second-harmonic generation in collagen as a potential cancer diagnostic parameter,” J. Biomed. Opt. 13(5), 054050 (2008).
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2007 (3)

R. Cicchi, D. Massi, S. Sestini, P. Carli, V. De Giorgi, T. Lotti, and F. S. Pavone, “Multidimensional non-linear laser imaging of basal cell carcinoma,” Opt. Express 15(16), 10135–10148 (2007).
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K. König, A. Ehlers, I. Riemann, S. Schenkl, R. Bückle, and M. Kaatz, “Clinical two-photon microendoscopy,” Microsc. Res. Tech. 70(5), 398–402 (2007).
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M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
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2006 (5)

K. König, A. Ehlers, F. Stracke, and I. Riemann, “In vivo drug screening in human skin using femtosecond laser multiphoton tomography,” Skin Pharmacol. Physiol. 19(2), 78–88 (2006).
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P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006).
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S.-J. Lin, S.-H. Jee, C.-J. Kuo, R.-J. Wu, W.-C. Lin, J.-S. Chen, Y.-H. Liao, C.-J. Hsu, T.-F. Tsai, Y.-F. Chen, and C.-Y. Dong, “Discrimination of basal cell carcinoma from normal dermal stroma by quantitative multiphoton imaging,” Opt. Lett. 31(18), 2756–2758 (2006).
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J. R. Unruh, E. S. Price, R. G. Molla, L. Stehno-Bittel, C. K. Johnson, and R. Hui, “Two-photon microscopy with wavelength switchable fiber laser excitation,” Opt. Express 14(21), 9825–9831 (2006).
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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]

2005 (1)

2004 (1)

C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, “Higher harmonic generation microscopy for developmental biology,” J. Struct. Biol. 147(1), 19–30 (2004).
[Crossref] [PubMed]

2003 (5)

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]

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), 796–800 (2003).
[Crossref] [PubMed]

C.-K. Sun, C.-C. Chen, S.-W. Chu, T.-H. Tsai, Y.-C. Chen, and B.-L. Lin, “Multiharmonic-generation biopsy of skin,” Opt. Lett. 28(24), 2488–2490 (2003).
[Crossref] [PubMed]

K. König and I. Riemann, “High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution,” J. Biomed. Opt. 8(3), 432–439 (2003).
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P. S. Tsai, B. Friedman, A. I. Ifarraguerri, B. D. Thompson, V. Lev-Ram, C. B. Schaffer, Q. Xiong, R. Y. Tsien, J. A. Squier, and D. Kleinfeld, “All-optical histology using ultrashort laser pulses,” Neuron 39(1), 27–41 (2003).
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2002 (2)

S. Huang, A. A. Heikal, and W. W. Webb, “Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein,” Biophys. J. 82(5), 2811–2825 (2002).
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S.-W. Chu, I. H. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, “Nonlinear bio-photonic crystal effects revealed with multimodal nonlinear microscopy,” J. Microsc. 208(Pt 3), 190–200 (2002).
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2001 (2)

2000 (1)

R. D. Schaller, J. C. Johnson, and R. J. Saykally, “Nonlinear chemical imaging microscopy: near-field third harmonic generation imaging of human red blood cells,” Anal. Chem. 72(21), 5361–5364 (2000).
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1999 (1)

1998 (2)

M. Müller, J. Squier, K. R. Wilson, and G. J. Brakenhoff, “3D Microscopy of transparent objects using third-harmonic generation,” J. Microsc. 191(3), 266–274 (1998).
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J. Squier, M. Müller, G. Brakenhoff, and K. R. Wilson, “Third harmonic generation microscopy,” Opt. Express 3(9), 315–324 (1998).
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1997 (1)

B. R. Masters, P. T. C. So, and E. Gratton, “Multiphoton excitation fluorescence microscopy and spectroscopy of in vivo human skin,” Biophys. J. 72(6), 2405–2412 (1997).
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1996 (2)

A. Hariharan, M. E. Fermann, M. L. Stock, D. J. Harter, and J. Squier, “Alexandrite-pumped alexandrite regenerative amplifier for femtosecond pulse amplification,” Opt. Lett. 21(2), 128–130 (1996).
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A. Hariharan, D. J. Harter, T. S. Sosnowski, S. Kane, D. Du, T. B. Norris, and J. Squier, “Injection of ultrafast regenerative amplifiers with low energy femtosecond pulses from an Er-doped fiber laser,” Opt. Commun. 132(5-6), 469–473 (1996).
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1995 (1)

K. Tamura, Y. Kimura, and M. Nakazawa, “Femtosecond pulse generation over 82 nm wavelength span from passively mode locked erbium-doped fiber laser,” Electron. Lett. 31(13), 1062–1063 (1995).
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1981 (1)

R. R. Anderson and J. A. Parrish, “The optics of human skin,” J. Invest. Dermatol. 77(1), 13–19 (1981).
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1978 (1)

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1961 (1)

P. A. Franken, A. E. Hill, C. W. Peters, and G. Weinreich, “Generation of optical harmonics,” Phys. Rev. Lett. 7(4), 118–119 (1961).
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D. Träutlein, F. Adler, K. Moutzouris, A. Jeromin, A. Leitenstorfer, and E. Ferrando-May, “Highly versatile confocal microscopy system based on a tunable femtosecond Er:fiber source,” J. Biophotonics 1(1), 53–61 (2008).
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Alfano, R. R.

L. A. Sordillo, Y. Pu, S. Pratavieira, Y. Budansky, and R. R. Alfano, “Deep optical imaging of tissue using the second and third near-infrared spectral windows,” J. Biomed. Opt. 19(5), 056004 (2014).
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Anderson, R. R.

R. R. Anderson and J. A. Parrish, “The optics of human skin,” J. Invest. Dermatol. 77(1), 13–19 (1981).
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Aptel, F.

F. Aptel, N. Olivier, A. Deniset-Besseau, J.-M. Legeais, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, “Multimodal nonlinear imaging of the human cornea,” Invest. Ophthalmol. Vis. Sci. 51(5), 2459–2465 (2010).
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Araki, T.

Arlauckas, S. P.

R. P. Judy, J. J. Keating, E. M. DeJesus, J. X. Jiang, O. T. Okusanya, S. Nie, D. E. Holt, S. P. Arlauckas, P. S. Low, E. J. Delikatny, and S. Singhal, “Quantification of tumor fluorescence during intraoperative optical cancer imaging,” Sci. Rep. 5(1), 16208 (2015).
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Baayen, J. C.

Bagot, M.

H. A. El Madani, E. Tancrède-Bohin, A. Bensussan, A. Colonna, A. Dupuy, M. Bagot, and A.-M. Pena, “In vivo multiphoton imaging of human skin: assessment of topical corticosteroid-induced epidermis atrophy and depigmentation,” J. Biomed. Opt. 17(2), 026009 (2012).
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Bakker, G.-J.

B. Weigelin, G.-J. Bakker, and P. Friedl, “Third harmonic generation microscopy of cells and tissue organization,” J. Cell Sci. 129(2), 245–255 (2016).
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B. Weigelin, G.-J. Bakker, and P. Friedl, “Intravital third harmonic generation microscopy of collective melanoma cell invasion: Principles of interface guidance and microvesicle dynamics,” Intravital 1(1), 32–43 (2012).
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Balu, M.

M. Balu, A. Mazhar, C. K. Hayakawa, R. Mittal, T. B. Krasieva, K. König, V. Venugopalan, and B. J. Tromberg, “In vivo multiphoton NADH fluorescence reveals depth-dependent keratinocyte metabolism in human skin,” Biophys. J. 104(1), 258–267 (2013).
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Bardeen, C. J.

K. M. Hanson and C. J. Bardeen, “Application of nonlinear optical microscopy for imaging skin,” Photochem. Photobiol. 85(1), 33–44 (2009).
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Barille, R.

Batista, A.

A. Batista, H. G. Breunig, A. Uchugonova, A. M. Morgado, and K. König, “Two-photon spectral fluorescence lifetime and second-harmonic generation imaging of the porcine cornea with a 12-femtosecond laser microscope,” J. Biomed. Opt. 21(3), 036002 (2016).
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Beaurepaire, E.

F. Aptel, N. Olivier, A. Deniset-Besseau, J.-M. Legeais, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, “Multimodal nonlinear imaging of the human cornea,” Invest. Ophthalmol. Vis. Sci. 51(5), 2459–2465 (2010).
[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).
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Becker, D. L.

Bensussan, A.

H. A. El Madani, E. Tancrède-Bohin, A. Bensussan, A. Colonna, A. Dupuy, M. Bagot, and A.-M. Pena, “In vivo multiphoton imaging of human skin: assessment of topical corticosteroid-induced epidermis atrophy and depigmentation,” J. Biomed. Opt. 17(2), 026009 (2012).
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Boppart, S. A.

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), 796–800 (2003).
[Crossref] [PubMed]

Brakenhoff, G.

Brakenhoff, G. J.

M. Müller, J. Squier, K. R. Wilson, and G. J. Brakenhoff, “3D Microscopy of transparent objects using third-harmonic generation,” J. Microsc. 191(3), 266–274 (1998).
[Crossref] [PubMed]

Breunig, H. G.

A. Batista, H. G. Breunig, A. Uchugonova, A. M. Morgado, and K. König, “Two-photon spectral fluorescence lifetime and second-harmonic generation imaging of the porcine cornea with a 12-femtosecond laser microscope,” J. Biomed. Opt. 21(3), 036002 (2016).
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M. Weinigel, H. G. Breunig, A. Uchugonova, and K. König, “Multipurpose nonlinear optical imaging system for in vivo and ex vivo multimodal histology,” J. Med. Imaging (Bellingham) 2(1), 016003 (2015).
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H. G. Breunig, H. Studier, and K. König, “Multiphoton excitation characteristics of cellular fluorophores of human skin in vivo,” Opt. Express 18(8), 7857–7871 (2010).
[Crossref] [PubMed]

Brewer, M. A.

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer 10(1), 94 (2010).
[Crossref] [PubMed]

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), 796–800 (2003).
[Crossref] [PubMed]

Bückle, R.

K. König, A. Ehlers, I. Riemann, S. Schenkl, R. Bückle, and M. Kaatz, “Clinical two-photon microendoscopy,” Microsc. Res. Tech. 70(5), 398–402 (2007).
[Crossref] [PubMed]

Budansky, Y.

L. A. Sordillo, Y. Pu, S. Pratavieira, Y. Budansky, and R. R. Alfano, “Deep optical imaging of tissue using the second and third near-infrared spectral windows,” J. Biomed. Opt. 19(5), 056004 (2014).
[Crossref] [PubMed]

Buhman, K. K.

Campagnola, P.

P. Campagnola, “Second harmonic generation imaging microscopy: applications to diseases diagnostics,” Anal. Chem. 83(9), 3224–3231 (2011).
[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]

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer 10(1), 94 (2010).
[Crossref] [PubMed]

Campbell, J. M.

P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006).
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Canioni, L.

Cao, Q.

Carli, P.

Carragher, N. O.

J. R. W. Conway, N. O. Carragher, and P. Timpson, “Developments in preclinical cancer imaging: innovating the discovery of therapeutics,” Nat. Rev. Cancer 14(5), 314–328 (2014).
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Chang, G.

Chang, G. Q.

H.-Y. Chung, W. Liu, Q. Cao, R. Greinert, F. X. Kärtner, and G. Q. Chang, “Tunable, ultrafast fiber-laser between 1.15 and 1.35 µm for harmonic generation microscopy in human skin,” IEEE J. Sel. Topics in Quantum Elec. 25(1), 6800708 (2019).

Charan, K.

Chen, C.-C.

Chen, H.

Chen, I. H.

S.-W. Chu, I. H. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, “Nonlinear bio-photonic crystal effects revealed with multimodal nonlinear microscopy,” J. Microsc. 208(Pt 3), 190–200 (2002).
[Crossref] [PubMed]

Chen, I.-H.

Chen, J.

Chen, J.-S.

Chen, P.-C.

Chen, S.-U.

S.-Y. Chen, S.-U. Chen, H.-Y. Wu, W.-J. Lee, Y.-H. Liao, and C.-K. Sun, “In vivo virtual biopsy of human skin by using noninvasive higher harmonic generation microscopy,” IEEE J. Sel. Topics in Quantum Elec. 16(3), 478–492 (2010).
[Crossref]

C.-S. Hsieh, S.-U. Chen, Y.-W. Lee, Y.-S. Yang, and C.-K. Sun, “Higher harmonic generation microscopy of in vitro cultured mammal oocytes and embryos,” Opt. Express 16(15), 11574–11588 (2008).
[PubMed]

Chen, S.-Y.

Y.-H. Liao, S.-Y. Chen, S.-Y. Chou, P.-H. Wang, M.-R. Tsai, and C.-K. Sun, “Determination of chronological aging parameters in epidermal keratinocytes by in vivo harmonic generation microscopy,” Biomed. Opt. Express 4(1), 77–88 (2013).
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M.-R. Tsai, S.-Y. Chen, D.-B. Shieh, P.-J. Lou, and C.-K. Sun, “In vivo optical virtual biopsy of human oral mucosa with harmonic generation microscopy,” Biomed. Opt. Express 2(8), 2317–2328 (2011).
[Crossref] [PubMed]

S.-Y. Chen, S.-U. Chen, H.-Y. Wu, W.-J. Lee, Y.-H. Liao, and C.-K. Sun, “In vivo virtual biopsy of human skin by using noninvasive higher harmonic generation microscopy,” IEEE J. Sel. Topics in Quantum Elec. 16(3), 478–492 (2010).
[Crossref]

S.-Y. Chen, H.-Y. Wu, and C.-K. Sun, “In vivo harmonic generation biopsy of human skin,” J. Biomed. Opt. 14(6), 060505 (2009).
[Crossref] [PubMed]

C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, “Higher harmonic generation microscopy for developmental biology,” J. Struct. Biol. 147(1), 19–30 (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.

Chen, Y.-F.

Cheng, J. X.

Cheng, P.-C.

S.-W. Chu, I. H. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, “Nonlinear bio-photonic crystal effects revealed with multimodal nonlinear microscopy,” J. Microsc. 208(Pt 3), 190–200 (2002).
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Cheng, Y.-T.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
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Chia, S.-H.

Chiu, P.-K.

J.-Y. Huang, L.-Z. Guo, J.-Z. Wang, T.-C. Li, H.-J. Lee, P.-K. Chiu, L.-H. Peng, and T.-M. Liu, “Fiber-based 1150-nm femtosecond laser source for the minimally invasive harmonic generation microscopy,” J. Biomed. Opt. 22(3), 036008 (2017).
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Chou, S.-Y.

Christie, R.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
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Chu, S.-W.

C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, “Higher harmonic generation microscopy for developmental biology,” J. Struct. Biol. 147(1), 19–30 (2004).
[Crossref] [PubMed]

C.-K. Sun, C.-C. Chen, S.-W. Chu, T.-H. Tsai, Y.-C. Chen, and B.-L. Lin, “Multiharmonic-generation biopsy of skin,” Opt. Lett. 28(24), 2488–2490 (2003).
[Crossref] [PubMed]

S.-W. Chu, I. H. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, “Nonlinear bio-photonic crystal effects revealed with multimodal nonlinear microscopy,” J. Microsc. 208(Pt 3), 190–200 (2002).
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S.-W. Chu, I.-H. Chen, T.-M. Liu, P.-C. Chen, C.-K. Sun, and B.-L. Lin, “Multimodal nonlinear spectral microscopy based on a femtosecond Cr:forsterite laser,” Opt. Lett. 26(23), 1909–1911 (2001).
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Chung, H.-Y.

Cicchi, R.

Colonna, A.

H. A. El Madani, E. Tancrède-Bohin, A. Bensussan, A. Colonna, A. Dupuy, M. Bagot, and A.-M. Pena, “In vivo multiphoton imaging of human skin: assessment of topical corticosteroid-induced epidermis atrophy and depigmentation,” J. Biomed. Opt. 17(2), 026009 (2012).
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Combettes, L.

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]

Conway, J. R. W.

J. R. W. Conway, N. O. Carragher, and P. Timpson, “Developments in preclinical cancer imaging: innovating the discovery of therapeutics,” Nat. Rev. Cancer 14(5), 314–328 (2014).
[Crossref] [PubMed]

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D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
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B. Li, M. Wang, K. Charan, M.-J. Li, and C. Xu, “Investigation of the long wavelength limit of soliton self-frequency shift in a silica fiber,” Opt. Express 26(15), 19637–19647 (2018).
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Appl. Opt. (1)

Biomed. Opt. Express (6)

M.-R. Tsai, S.-Y. Chen, D.-B. Shieh, P.-J. Lou, and C.-K. Sun, “In vivo optical virtual biopsy of human oral mucosa with harmonic generation microscopy,” Biomed. Opt. Express 2(8), 2317–2328 (2011).
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C. Thrasivoulou, G. Virich, T. Krenacs, I. Korom, and D. L. Becker, “Optical delineation of human malignant melanoma using second harmonic imaging of collagen,” Biomed. Opt. Express 2(5), 1282–1295 (2011).
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J. Xu, D. Kang, Y. Zeng, S. Zhuo, X. Zhu, L. Jiang, J. Chen, and J. Lin, “Multiphoton microscopy for label-free identification of intramural metastasis in human esophageal squamous cell carcinoma,” Biomed. Opt. Express 8(7), 3360–3368 (2017).
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N. V. Kuzmin, P. Wesseling, P. C. Hamer, D. P. Noske, G. D. Galgano, H. D. Mansvelder, J. C. Baayen, and M. L. Groot, “Third harmonic generation imaging for fast, label-free pathology of human brain tumors,” Biomed. Opt. Express 7(5), 1889–1904 (2016).
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Y.-H. Liao, S.-Y. Chen, S.-Y. Chou, P.-H. Wang, M.-R. Tsai, and C.-K. Sun, “Determination of chronological aging parameters in epidermal keratinocytes by in vivo harmonic generation microscopy,” Biomed. Opt. Express 4(1), 77–88 (2013).
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Biophys. J. (3)

S. Huang, A. A. Heikal, and W. W. Webb, “Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein,” Biophys. J. 82(5), 2811–2825 (2002).
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BMC Cancer (1)

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer 10(1), 94 (2010).
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BMC Med. (1)

P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006).
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Electron. Lett. (1)

K. Tamura, Y. Kimura, and M. Nakazawa, “Femtosecond pulse generation over 82 nm wavelength span from passively mode locked erbium-doped fiber laser,” Electron. Lett. 31(13), 1062–1063 (1995).
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IEEE J. Sel. Topics in Quantum Elec. (2)

H.-Y. Chung, W. Liu, Q. Cao, R. Greinert, F. X. Kärtner, and G. Q. Chang, “Tunable, ultrafast fiber-laser between 1.15 and 1.35 µm for harmonic generation microscopy in human skin,” IEEE J. Sel. Topics in Quantum Elec. 25(1), 6800708 (2019).

S.-Y. Chen, S.-U. Chen, H.-Y. Wu, W.-J. Lee, Y.-H. Liao, and C.-K. Sun, “In vivo virtual biopsy of human skin by using noninvasive higher harmonic generation microscopy,” IEEE J. Sel. Topics in Quantum Elec. 16(3), 478–492 (2010).
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Intravital (1)

B. Weigelin, G.-J. Bakker, and P. Friedl, “Intravital third harmonic generation microscopy of collective melanoma cell invasion: Principles of interface guidance and microvesicle dynamics,” Intravital 1(1), 32–43 (2012).
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Invest. Ophthalmol. Vis. Sci. (1)

F. Aptel, N. Olivier, A. Deniset-Besseau, J.-M. Legeais, K. Plamann, M.-C. Schanne-Klein, and E. Beaurepaire, “Multimodal nonlinear imaging of the human cornea,” Invest. Ophthalmol. Vis. Sci. 51(5), 2459–2465 (2010).
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J. Biomed. Opt. (7)

J.-Y. Huang, L.-Z. Guo, J.-Z. Wang, T.-C. Li, H.-J. Lee, P.-K. Chiu, L.-H. Peng, and T.-M. Liu, “Fiber-based 1150-nm femtosecond laser source for the minimally invasive harmonic generation microscopy,” J. Biomed. Opt. 22(3), 036008 (2017).
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S.-Y. Chen, H.-Y. Wu, and C.-K. Sun, “In vivo harmonic generation biopsy of human skin,” J. Biomed. Opt. 14(6), 060505 (2009).
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K. König and I. Riemann, “High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution,” J. Biomed. Opt. 8(3), 432–439 (2003).
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D. Träutlein, F. Adler, K. Moutzouris, A. Jeromin, A. Leitenstorfer, and E. Ferrando-May, “Highly versatile confocal microscopy system based on a tunable femtosecond Er:fiber source,” J. Biophotonics 1(1), 53–61 (2008).
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J. Cell Sci. (1)

B. Weigelin, G.-J. Bakker, and P. Friedl, “Third harmonic generation microscopy of cells and tissue organization,” J. Cell Sci. 129(2), 245–255 (2016).
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J. Invest. Dermatol. (2)

J. Paoli, M. Smedh, A.-M. Wennberg, and M. B. Ericson, “Multiphoton laser scanning microscopy on non-melanoma skin cancer: morphologic features for future non-invasive diagnostics,” J. Invest. Dermatol. 128(5), 1248–1255 (2008).
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M. Weinigel, H. G. Breunig, A. Uchugonova, and K. König, “Multipurpose nonlinear optical imaging system for in vivo and ex vivo multimodal histology,” J. Med. Imaging (Bellingham) 2(1), 016003 (2015).
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J. Microsc. (2)

M. Müller, J. Squier, K. R. Wilson, and G. J. Brakenhoff, “3D Microscopy of transparent objects using third-harmonic generation,” J. Microsc. 191(3), 266–274 (1998).
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S.-W. Chu, I. H. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, “Nonlinear bio-photonic crystal effects revealed with multimodal nonlinear microscopy,” J. Microsc. 208(Pt 3), 190–200 (2002).
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J. Struct. Biol. (1)

C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, “Higher harmonic generation microscopy for developmental biology,” J. Struct. Biol. 147(1), 19–30 (2004).
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Microsc. Res. Tech. (1)

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Nat. Med. (1)

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–800 (2003).
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Nat. Methods (3)

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Figures (8)

Fig. 1
Fig. 1 Schematic setup of the multimodal microscope driven by a fiber-based ultrafast source. SPM: self-phase modulation, HWP: half-wave plate, PBS: polarization beam splitter, L: lens, MgO:PPLN: magnesium-doped periodically poled lithium niobate, M: mirror, DM: dichroic mirror, BPF: bandpass filter, PMT: photomultiplier tube.
Fig. 2
Fig. 2 (a) Input spectrum before MgO:PPLN. (b) Autocorrelation traces of the pulses at 775 nm. Red curve: measured autocorrelation trace. Black dashed curve: calculated from the transform-limited pulses allowed by the frequency-doubled spectrum (inset).
Fig. 3
Fig. 3 (a) Spectral broadening from 9-cm DSF. (b) Measured autocorrelation trace of the filtered pulses at 1250 nm (red curve) and calculated autocorrelation trace of the transform-limited pulse allowed by the filtered spectrum (black dashed curve). Inset: filtered spectrum centered at 1250 nm.
Fig. 4
Fig. 4 SHG/THG imaging of ex vivo human skin from the trunk part at different penetration depth. (a) 25 μm. (b) 30 μm. (c) 45 μm. (d) 55 μm. (e) 60 μm. (f) 65 μm. Scale bar: 50 μm.
Fig. 5
Fig. 5 SHG imaging of the fiber network in dermis of ex vivo human skin from the head part at different penetration depth. (a) 130 μm. (b) 150 μm. (c) 170 μm. Scale bar: 100 μm.
Fig. 6
Fig. 6 2PEF imaging of ex vivo human skin from the head part at different penetration depth. (a) 30 μm. (b) 40 μm. (c) 50 μm. (d) 60 μm. (e) 65 μm. (f) 70 μm. Scale bar: 50 μm.
Fig. 7
Fig. 7 Ex vivo human skin from the head part visualized by different modalities. (a-c) THG imaging excited by 1250-nm pulses. (d-f) 2PEF imaging excited by 775-nm pulses. Scale bar: 50 μm.
Fig. 8
Fig. 8 Schematic setup of the three-color configuration to generate femtosecond pulses at 775 nm, 850 nm, and 1250 nm.