Abstract

A nonlinear optical (NLO) microscopy system integrating stimulated Raman scattering (SRS), two-photon excited fluorescence (TPEF) and second-harmonic generation (SHG) was developed to image fresh mouse retinas. The morphological and functional details of various retinal layers were revealed by the endogenous NLO signals. Particularly, high resolution label-free imaging of retinal neurons and nerve fibers in the ganglion cell and nerve fiber layers was achieved by capturing endogenous SRS and TPEF signals. In addition, the spectral and temporal analysis of TPEF images allowed visualization of different fluorescent components in the retinal pigment epithelium (RPE). Fluorophores with short TPEF lifetime, such as A2E, can be differentiated from other long-lifetime components in the RPE. The NLO imaging method would provide important information for investigation of retinal ganglion cell degeneration and holds the potential to study the biochemical processes of visual cycle in the RPE.

© 2015 Optical Society of America

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2013 (5)

S. K. Teh, W. Zheng, S. Li, D. Li, Y. Zeng, Y. Yang, and J. Y. Qu, “Multimodal nonlinear optical microscopy improves the accuracy of early diagnosis of squamous intraepithelial neoplasia,” J. Biomed. Opt. 18(3), 036001 (2013).
[Crossref] [PubMed]

Y. Zeng, B. Yan, Q. Sun, S. K. Teh, W. Zhang, Z. Wen, and J. Y. Qu, “Label-free in vivo imaging of human leukocytes using two-photon excited endogenous fluorescence,” J. Biomed. Opt. 18(4), 040504 (2013).
[Crossref] [PubMed]

X. S. Xie, D. Fu, C. W. Freudiger, X. Zhang, and G. Holtom, “Hyperspectral imaging with stimulated Raman scattering by chirped femtosecond lasers,” J. Phys. Chem. B. 117, 4634–4640 (2013).

K. T. Janssen, C. E. Mac Nair, J. A. Dietz, C. L. Schlamp, and R. W. Nickells, “Nuclear atrophy of retinal ganglion cells precedes the bax-dependent stage of apoptosis,” Invest. Ophthalmol. Vis. Sci. 54(3), 1805–1815 (2013).
[Crossref] [PubMed]

R. Sharma, L. Yin, Y. Geng, W. H. Merigan, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “In vivo two-photon imaging of the mouse retina,” Biomed. Opt. Express 4(8), 1285–1293 (2013).
[Crossref] [PubMed]

2012 (2)

O. Masihzadeh, T. C. Lei, D. A. Ammar, M. Y. Kahook, and E. A. Gibson, “A multiphoton microscope platform for imaging the mouse eye,” Mol. Vis. 18, 1840–1848 (2012).
[PubMed]

E. Prokofyeva and E. Zrenner, “Epidemiology of major eye diseases leading to blindness in Europe: a literature review,” Ophthalmic Res. 47(4), 171–188 (2012).
[Crossref] [PubMed]

2011 (6)

2010 (4)

S. Lu, W. Min, S. Chong, G. R. Holtom, and X. S. Xie, “Label-free imaging of heme proteins with two-photon excited photothermal lens microscopy,” Appl. Phys. Lett. 96(11), 113701 (2010).
[Crossref]

W. Zheng, D. Li, and J. Y. Qu, “Monitoring changes of cellular metabolism and microviscosity in vitro based on time-resolved endogenous fluorescence and its anisotropy decay dynamics,” J. Biomed. Opt. 15(3), 037013 (2010).
[Crossref] [PubMed]

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]

G. Palczewska, T. Maeda, Y. Imanishi, W. Sun, Y. Chen, D. R. Williams, D. W. Piston, A. Maeda, and K. Palczewski, “Noninvasive multiphoton fluorescence microscopy resolves retinol and retinal condensation products in mouse eyes,” Nat. Med. 16(12), 1444–1449 (2010).
[Crossref] [PubMed]

2009 (1)

D. Chorvat and A. Chorvatova, “Multi-wavelength fluorescence lifetime spectroscopy: a new approach to the study of endogenous fluorescence in living cells and tissues,” Laser Phys. Lett. 6(3), 175–193 (2009).
[Crossref]

2008 (4)

C. K. Leung, J. D. Lindsey, J. G. Crowston, W. K. Ju, Q. Liu, D. U. Bartsch, and R. N. Weinreb, “In vivo imaging of murine retinal ganglion cells,” J. Neurosci. Methods 168(2), 475–478 (2008).
[Crossref] [PubMed]

D. Li, W. Zheng, and J. Y. Qu, “Time-resolved spectroscopic imaging reveals the fundamentals of cellular NADH fluorescence,” Opt. Lett. 33(20), 2365–2367 (2008).
[Crossref] [PubMed]

D. Fu, T. E. Matthews, T. Ye, I. R. Piletic, and W. S. Warren, “Label-free in vivo optical imaging of microvasculature and oxygenation level,” J. Biomed. Opt. 13(4), 040503 (2008).
[Crossref] [PubMed]

W. Zheng, Y. Wu, D. Li, and J. Y. Qu, “Autofluorescence of epithelial tissue: single-photon versus two-photon excitation,” J. Biomed. Opt. 13(5), 054010 (2008).
[Crossref] [PubMed]

2007 (3)

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

L. Pérez De Sevilla Müller, J. Shelley, and R. Weiler, “Displaced amacrine cells of the mouse retina,” J. Comp. Neurol. 505(2), 177–189 (2007).
[Crossref] [PubMed]

M. Han, G. Giese, S. Schmitz-Valckenberg, A. Bindewald-Wittich, F. G. Holz, J. Yu, J. F. Bille, and M. H. Niemz, “Age-related structural abnormalities in the human retina-choroid complex revealed by two-photon excited autofluorescence imaging,” J. Biomed. Opt. 12(2), 024012 (2007).
[Crossref] [PubMed]

2006 (4)

M. Han, A. Bindewald-Wittich, F. G. Holz, G. Giese, M. H. Niemz, S. Snyder, H. Sun, J. Yu, M. Agopov, O. La Schiazza, and J. F. Bille, “Two-photon excited autofluorescence imaging of human retinal pigment epithelial cells,” J. Biomed. Opt. 11(1), 010501 (2006).
[Crossref] [PubMed]

J. Coombs, D. van der List, G. Y. Wang, and L. M. Chalupa, “Morphological properties of mouse retinal ganglion cells,” Neuroscience 140(1), 123–136 (2006).
[Crossref] [PubMed]

A. Bindewald-Wittich, M. Han, S. Schmitz-Valckenberg, S. R. Snyder, G. Giese, J. F. Bille, and F. G. Holz, “Two-Photon-Excited Fluorescence Imaging of Human RPE Cells with a Femtosecond Ti:Sapphire Laser,” Invest. Ophthalmol. Vis. Sci. 47(10), 4553–4557 (2006).
[Crossref] [PubMed]

Y. Wu and J. Y. Qu, “Autofluorescence spectroscopy of epithelial tissues,” J. Biomed. Opt. 11(5), 054023 (2006).
[Crossref] [PubMed]

2005 (2)

O. Strauss, “The retinal pigment epithelium in visual function,” Physiol. Rev. 85(3), 845–881 (2005).
[Crossref] [PubMed]

J. R. Sparrow and M. Boulton, “RPE lipofuscin and its role in retinal pathobiology,” Exp. Eye Res. 80(5), 595–606 (2005).
[Crossref] [PubMed]

2004 (4)

B. J. Klevering, A. Maugeri, A. Wagner, S. L. Go, C. Vink, F. P. Cremers, and C. B. Hoyng, “Three families displaying the combination of Stargardt’s disease with cone-rod dystrophy or retinitis pigmentosa,” Ophthalmology 111(3), 546–553 (2004).
[Crossref] [PubMed]

R. A. Radu, N. L. Mata, A. Bagla, and G. H. Travis, “Light exposure stimulates formation of A2E oxiranes in a mouse model of Stargardt’s macular degeneration,” Proc. Natl. Acad. Sci. USA 101(16), 5928–5933 (2004).
[Crossref] [PubMed]

H. P. Scholl, N. H. Chong, A. G. Robson, G. E. Holder, A. T. Moore, and A. C. Bird, “Fundus autofluorescence in patients with leber congenital amaurosis,” Invest. Ophthalmol. Vis. Sci. 45(8), 2747–2752 (2004).
[Crossref] [PubMed]

Y. Imanishi, M. L. Batten, D. W. Piston, W. Baehr, and K. Palczewski, “Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye,” J. Cell Biol. 164(3), 373–383 (2004).
[Crossref] [PubMed]

2003 (2)

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

J. R. Sparrow, N. Fishkin, J. Zhou, B. Cai, Y. P. Jang, S. Krane, Y. Itagaki, and K. Nakanishi, “A2E, a byproduct of the visual cycle,” Vision Res. 43(28), 2983–2990 (2003).
[Crossref] [PubMed]

2002 (3)

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 99(17), 11014–11019 (2002).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

T. Nagai, K. Ibata, E. S. Park, M. Kubota, K. Mikoshiba, and A. Miyawaki, “A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications,” Nat. Biotechnol. 20(1), 87–90 (2002).
[Crossref] [PubMed]

2001 (4)

A. I. den Hollander, J. R. Heckenlively, L. I. van den Born, Y. J. de Kok, S. D. van der Velde-Visser, U. Kellner, B. Jurklies, M. J. van Schooneveld, A. Blankenagel, K. Rohrschneider, B. Wissinger, J. R. Cruysberg, A. F. Deutman, H. G. Brunner, E. Apfelstedt-Sylla, C. B. Hoyng, and F. P. Cremers, “Leber congenital amaurosis and retinitis pigmentosa with Coats-like exudative vasculopathy are associated with mutations in the crumbs homologue 1 (CRB1) gene,” Am. J. Hum. Genet. 69(1), 198–203 (2001).
[Crossref] [PubMed]

M. L. Katz and T. M. Redmond, “Effect of Rpe65 knockout on accumulation of lipofuscin fluorophores in the retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 42(12), 3023–3030 (2001).
[PubMed]

F. C. Delori, D. G. Goger, and C. K. Dorey, “Age-related accumulation and spatial distribution of lipofuscin in RPE of normal subjects,” Invest. Ophthalmol. Vis. Sci. 42(8), 1855–1866 (2001).
[PubMed]

F. G. Holz, C. Bellman, S. Staudt, F. Schütt, and H. E. Völcker, “Fundus autofluorescence and development of geographic atrophy in age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 42(5), 1051–1056 (2001).
[PubMed]

2000 (1)

G. Feng, R. H. Mellor, M. Bernstein, C. Keller-Peck, Q. T. Nguyen, M. Wallace, J. M. Nerbonne, J. W. Lichtman, and J. R. Sanes, “Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP,” Neuron 28(1), 41–51 (2000).
[Crossref] [PubMed]

1999 (1)

J. Weng, N. L. Mata, S. M. Azarian, R. T. Tzekov, D. G. Birch, and G. H. Travis, “Insights into the Function of Rim Protein in Photoreceptors and Etiology of Stargardt’s Disease from the Phenotype in abcr Knockout Mice,” Cell 98(1), 13–23 (1999).
[Crossref] [PubMed]

1998 (2)

C. J. Jeon, E. Strettoi, and R. H. Masland, “The major cell populations of the mouse retina,” J. Neurosci. 18(21), 8936–8946 (1998).
[PubMed]

A. Marquardt, H. Stöhr, L. A. Passmore, F. Krämer, A. Rivera, and B. H. Weber, “Mutations in a novel gene, VMD2, encoding a protein of unknown properties cause juvenile-onset vitelliform macular dystrophy (Best’s disease),” Hum. Mol. Genet. 7(9), 1517–1525 (1998).
[Crossref] [PubMed]

1997 (1)

U. Solbach, C. Keilhauer, H. Knabben, and S. Wolf, “Imaging of retinal autofluorescence in patients with age-related macular degeneration,” Retina 17(5), 385–389 (1997).
[Crossref] [PubMed]

1996 (1)

J. P. Dunn, S. W. Noorily, M. Petri, D. Finkelstein, J. T. Rosenbaum, and D. A. Jabs, “Antiphospholipid antibodies and retinal vascular disease,” Lupus 5(4), 313–322 (1996).
[Crossref] [PubMed]

1995 (1)

D. W. Piston, B. R. Masters, and W. W. Webb, “Three-dimensionally resolved NAD(P)H cellular metabolic redox imaging of the in situ cornea with two-photon excitation laser scanning microscopy,” J. Microsc. 178(1), 20–27 (1995).
[Crossref] [PubMed]

1990 (1)

C. S. von Bartheld, D. E. Cunningham, and E. W. Rubel, “Neuronal tracing with DiI: decalcification, cryosectioning, and photoconversion for light and electron microscopic analysis,” J. Histochem. Cytochem. 38(5), 725–733 (1990).
[Crossref] [PubMed]

1988 (1)

G. E. Eldred and M. L. Katz, “Fluorophores of the human retinal pigment epithelium: separation and spectral characterization,” Exp. Eye Res. 47(1), 71–86 (1988).
[Crossref] [PubMed]

1986 (2)

M. L. Katz, C. M. Drea, and W. G. Robison., “Relationship between dietary retinol and lipofuscin in the retinal pigment epithelium,” Mech. Ageing Dev. 35(3), 291–305 (1986).
[Crossref] [PubMed]

T. Voigt, “Cholinergic amacrine cells in the rat retina,” J. Comp. Neurol. 248(1), 19–35 (1986).
[Crossref] [PubMed]

1984 (2)

L. Feeney-Burns, E. S. Hilderbrand, and S. Eldridge, “Aging human RPE: morphometric analysis of macular, equatorial, and peripheral cells,” Invest. Ophthalmol. Vis. Sci. 25(2), 195–200 (1984).
[PubMed]

V. H. Perry, R. J. Morris, and G. Raisman, “Is Thy-1 expressed only by ganglion cells and their axons in the retina and optic nerve?” J. Neurocytol. 13(5), 809–824 (1984).
[Crossref] [PubMed]

Agar, N. Y.

M. Ji, D. A. Orringer, C. W. Freudiger, S. Ramkissoon, X. Liu, D. Lau, A. J. Golby, I. Norton, M. Hayashi, N. Y. Agar, G. S. Young, C. Spino, S. Santagata, S. Camelo-Piragua, K. L. Ligon, O. Sagher, and X. S. Xie, “Rapid, label-free detection of brain tumors with stimulated Raman scattering microscopy,” Sci. Transl. Med.5,201ra119 (2013).

Agopov, M.

M. Han, A. Bindewald-Wittich, F. G. Holz, G. Giese, M. H. Niemz, S. Snyder, H. Sun, J. Yu, M. Agopov, O. La Schiazza, and J. F. Bille, “Two-photon excited autofluorescence imaging of human retinal pigment epithelial cells,” J. Biomed. Opt. 11(1), 010501 (2006).
[Crossref] [PubMed]

Ammar, D. A.

O. Masihzadeh, T. C. Lei, D. A. Ammar, M. Y. Kahook, and E. A. Gibson, “A multiphoton microscope platform for imaging the mouse eye,” Mol. Vis. 18, 1840–1848 (2012).
[PubMed]

A. W. Johnson, D. A. Ammar, and M. Y. Kahook, “Two-photon imaging of the mouse eye,” Invest. Ophthalmol. Vis. Sci. 52(7), 4098–4105 (2011).
[Crossref] [PubMed]

Apfelstedt-Sylla, E.

A. I. den Hollander, J. R. Heckenlively, L. I. van den Born, Y. J. de Kok, S. D. van der Velde-Visser, U. Kellner, B. Jurklies, M. J. van Schooneveld, A. Blankenagel, K. Rohrschneider, B. Wissinger, J. R. Cruysberg, A. F. Deutman, H. G. Brunner, E. Apfelstedt-Sylla, C. B. Hoyng, and F. P. Cremers, “Leber congenital amaurosis and retinitis pigmentosa with Coats-like exudative vasculopathy are associated with mutations in the crumbs homologue 1 (CRB1) gene,” Am. J. Hum. Genet. 69(1), 198–203 (2001).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

Azarian, S. M.

J. Weng, N. L. Mata, S. M. Azarian, R. T. Tzekov, D. G. Birch, and G. H. Travis, “Insights into the Function of Rim Protein in Photoreceptors and Etiology of Stargardt’s Disease from the Phenotype in abcr Knockout Mice,” Cell 98(1), 13–23 (1999).
[Crossref] [PubMed]

Baehr, W.

Y. Imanishi, M. L. Batten, D. W. Piston, W. Baehr, and K. Palczewski, “Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye,” J. Cell Biol. 164(3), 373–383 (2004).
[Crossref] [PubMed]

Bagla, A.

R. A. Radu, N. L. Mata, A. Bagla, and G. H. Travis, “Light exposure stimulates formation of A2E oxiranes in a mouse model of Stargardt’s macular degeneration,” Proc. Natl. Acad. Sci. USA 101(16), 5928–5933 (2004).
[Crossref] [PubMed]

Bartsch, D. U.

C. K. Leung, J. D. Lindsey, J. G. Crowston, W. K. Ju, Q. Liu, D. U. Bartsch, and R. N. Weinreb, “In vivo imaging of murine retinal ganglion cells,” J. Neurosci. Methods 168(2), 475–478 (2008).
[Crossref] [PubMed]

Batten, M. L.

Y. Imanishi, M. L. Batten, D. W. Piston, W. Baehr, and K. Palczewski, “Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye,” J. Cell Biol. 164(3), 373–383 (2004).
[Crossref] [PubMed]

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]

Becker, W.

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

Bellman, C.

F. G. Holz, C. Bellman, S. Staudt, F. Schütt, and H. E. Völcker, “Fundus autofluorescence and development of geographic atrophy in age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 42(5), 1051–1056 (2001).
[PubMed]

Bergmann, A.

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

Bernstein, M.

G. Feng, R. H. Mellor, M. Bernstein, C. Keller-Peck, Q. T. Nguyen, M. Wallace, J. M. Nerbonne, J. W. Lichtman, and J. R. Sanes, “Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP,” Neuron 28(1), 41–51 (2000).
[Crossref] [PubMed]

Bille, J. F.

M. Han, G. Giese, S. Schmitz-Valckenberg, A. Bindewald-Wittich, F. G. Holz, J. Yu, J. F. Bille, and M. H. Niemz, “Age-related structural abnormalities in the human retina-choroid complex revealed by two-photon excited autofluorescence imaging,” J. Biomed. Opt. 12(2), 024012 (2007).
[Crossref] [PubMed]

A. Bindewald-Wittich, M. Han, S. Schmitz-Valckenberg, S. R. Snyder, G. Giese, J. F. Bille, and F. G. Holz, “Two-Photon-Excited Fluorescence Imaging of Human RPE Cells with a Femtosecond Ti:Sapphire Laser,” Invest. Ophthalmol. Vis. Sci. 47(10), 4553–4557 (2006).
[Crossref] [PubMed]

M. Han, A. Bindewald-Wittich, F. G. Holz, G. Giese, M. H. Niemz, S. Snyder, H. Sun, J. Yu, M. Agopov, O. La Schiazza, and J. F. Bille, “Two-photon excited autofluorescence imaging of human retinal pigment epithelial cells,” J. Biomed. Opt. 11(1), 010501 (2006).
[Crossref] [PubMed]

Bindewald-Wittich, A.

M. Han, G. Giese, S. Schmitz-Valckenberg, A. Bindewald-Wittich, F. G. Holz, J. Yu, J. F. Bille, and M. H. Niemz, “Age-related structural abnormalities in the human retina-choroid complex revealed by two-photon excited autofluorescence imaging,” J. Biomed. Opt. 12(2), 024012 (2007).
[Crossref] [PubMed]

A. Bindewald-Wittich, M. Han, S. Schmitz-Valckenberg, S. R. Snyder, G. Giese, J. F. Bille, and F. G. Holz, “Two-Photon-Excited Fluorescence Imaging of Human RPE Cells with a Femtosecond Ti:Sapphire Laser,” Invest. Ophthalmol. Vis. Sci. 47(10), 4553–4557 (2006).
[Crossref] [PubMed]

M. Han, A. Bindewald-Wittich, F. G. Holz, G. Giese, M. H. Niemz, S. Snyder, H. Sun, J. Yu, M. Agopov, O. La Schiazza, and J. F. Bille, “Two-photon excited autofluorescence imaging of human retinal pigment epithelial cells,” J. Biomed. Opt. 11(1), 010501 (2006).
[Crossref] [PubMed]

Birch, D. G.

J. Weng, N. L. Mata, S. M. Azarian, R. T. Tzekov, D. G. Birch, and G. H. Travis, “Insights into the Function of Rim Protein in Photoreceptors and Etiology of Stargardt’s Disease from the Phenotype in abcr Knockout Mice,” Cell 98(1), 13–23 (1999).
[Crossref] [PubMed]

Birckner, E.

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

Bird, A. C.

H. P. Scholl, N. H. Chong, A. G. Robson, G. E. Holder, A. T. Moore, and A. C. Bird, “Fundus autofluorescence in patients with leber congenital amaurosis,” Invest. Ophthalmol. Vis. Sci. 45(8), 2747–2752 (2004).
[Crossref] [PubMed]

Blankenagel, A.

A. I. den Hollander, J. R. Heckenlively, L. I. van den Born, Y. J. de Kok, S. D. van der Velde-Visser, U. Kellner, B. Jurklies, M. J. van Schooneveld, A. Blankenagel, K. Rohrschneider, B. Wissinger, J. R. Cruysberg, A. F. Deutman, H. G. Brunner, E. Apfelstedt-Sylla, C. B. Hoyng, and F. P. Cremers, “Leber congenital amaurosis and retinitis pigmentosa with Coats-like exudative vasculopathy are associated with mutations in the crumbs homologue 1 (CRB1) gene,” Am. J. Hum. Genet. 69(1), 198–203 (2001).
[Crossref] [PubMed]

Boulton, M.

J. R. Sparrow and M. Boulton, “RPE lipofuscin and its role in retinal pathobiology,” Exp. Eye Res. 80(5), 595–606 (2005).
[Crossref] [PubMed]

Brunner, H. G.

A. I. den Hollander, J. R. Heckenlively, L. I. van den Born, Y. J. de Kok, S. D. van der Velde-Visser, U. Kellner, B. Jurklies, M. J. van Schooneveld, A. Blankenagel, K. Rohrschneider, B. Wissinger, J. R. Cruysberg, A. F. Deutman, H. G. Brunner, E. Apfelstedt-Sylla, C. B. Hoyng, and F. P. Cremers, “Leber congenital amaurosis and retinitis pigmentosa with Coats-like exudative vasculopathy are associated with mutations in the crumbs homologue 1 (CRB1) gene,” Am. J. Hum. Genet. 69(1), 198–203 (2001).
[Crossref] [PubMed]

Cai, B.

J. R. Sparrow, N. Fishkin, J. Zhou, B. Cai, Y. P. Jang, S. Krane, Y. Itagaki, and K. Nakanishi, “A2E, a byproduct of the visual cycle,” Vision Res. 43(28), 2983–2990 (2003).
[Crossref] [PubMed]

Camelo-Piragua, S.

M. Ji, D. A. Orringer, C. W. Freudiger, S. Ramkissoon, X. Liu, D. Lau, A. J. Golby, I. Norton, M. Hayashi, N. Y. Agar, G. S. Young, C. Spino, S. Santagata, S. Camelo-Piragua, K. L. Ligon, O. Sagher, and X. S. Xie, “Rapid, label-free detection of brain tumors with stimulated Raman scattering microscopy,” Sci. Transl. Med.5,201ra119 (2013).

Chalupa, L. M.

J. Coombs, D. van der List, G. Y. Wang, and L. M. Chalupa, “Morphological properties of mouse retinal ganglion cells,” Neuroscience 140(1), 123–136 (2006).
[Crossref] [PubMed]

Chen, Y.

G. Palczewska, T. Maeda, Y. Imanishi, W. Sun, Y. Chen, D. R. Williams, D. W. Piston, A. Maeda, and K. Palczewski, “Noninvasive multiphoton fluorescence microscopy resolves retinol and retinal condensation products in mouse eyes,” Nat. Med. 16(12), 1444–1449 (2010).
[Crossref] [PubMed]

Chong, N. H.

H. P. Scholl, N. H. Chong, A. G. Robson, G. E. Holder, A. T. Moore, and A. C. Bird, “Fundus autofluorescence in patients with leber congenital amaurosis,” Invest. Ophthalmol. Vis. Sci. 45(8), 2747–2752 (2004).
[Crossref] [PubMed]

Chong, S.

S. Lu, W. Min, S. Chong, G. R. Holtom, and X. S. Xie, “Label-free imaging of heme proteins with two-photon excited photothermal lens microscopy,” Appl. Phys. Lett. 96(11), 113701 (2010).
[Crossref]

Chorvat, D.

D. Chorvat and A. Chorvatova, “Multi-wavelength fluorescence lifetime spectroscopy: a new approach to the study of endogenous fluorescence in living cells and tissues,” Laser Phys. Lett. 6(3), 175–193 (2009).
[Crossref]

Chorvatova, A.

D. Chorvat and A. Chorvatova, “Multi-wavelength fluorescence lifetime spectroscopy: a new approach to the study of endogenous fluorescence in living cells and tissues,” Laser Phys. Lett. 6(3), 175–193 (2009).
[Crossref]

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).
[Crossref] [PubMed]

Coombs, J.

J. Coombs, D. van der List, G. Y. Wang, and L. M. Chalupa, “Morphological properties of mouse retinal ganglion cells,” Neuroscience 140(1), 123–136 (2006).
[Crossref] [PubMed]

Cremers, F. P.

B. J. Klevering, A. Maugeri, A. Wagner, S. L. Go, C. Vink, F. P. Cremers, and C. B. Hoyng, “Three families displaying the combination of Stargardt’s disease with cone-rod dystrophy or retinitis pigmentosa,” Ophthalmology 111(3), 546–553 (2004).
[Crossref] [PubMed]

A. I. den Hollander, J. R. Heckenlively, L. I. van den Born, Y. J. de Kok, S. D. van der Velde-Visser, U. Kellner, B. Jurklies, M. J. van Schooneveld, A. Blankenagel, K. Rohrschneider, B. Wissinger, J. R. Cruysberg, A. F. Deutman, H. G. Brunner, E. Apfelstedt-Sylla, C. B. Hoyng, and F. P. Cremers, “Leber congenital amaurosis and retinitis pigmentosa with Coats-like exudative vasculopathy are associated with mutations in the crumbs homologue 1 (CRB1) gene,” Am. J. Hum. Genet. 69(1), 198–203 (2001).
[Crossref] [PubMed]

Crowston, J. G.

C. K. Leung, J. D. Lindsey, J. G. Crowston, W. K. Ju, Q. Liu, D. U. Bartsch, and R. N. Weinreb, “In vivo imaging of murine retinal ganglion cells,” J. Neurosci. Methods 168(2), 475–478 (2008).
[Crossref] [PubMed]

Cruysberg, J. R.

A. I. den Hollander, J. R. Heckenlively, L. I. van den Born, Y. J. de Kok, S. D. van der Velde-Visser, U. Kellner, B. Jurklies, M. J. van Schooneveld, A. Blankenagel, K. Rohrschneider, B. Wissinger, J. R. Cruysberg, A. F. Deutman, H. G. Brunner, E. Apfelstedt-Sylla, C. B. Hoyng, and F. P. Cremers, “Leber congenital amaurosis and retinitis pigmentosa with Coats-like exudative vasculopathy are associated with mutations in the crumbs homologue 1 (CRB1) gene,” Am. J. Hum. Genet. 69(1), 198–203 (2001).
[Crossref] [PubMed]

Cunningham, D. E.

C. S. von Bartheld, D. E. Cunningham, and E. W. Rubel, “Neuronal tracing with DiI: decalcification, cryosectioning, and photoconversion for light and electron microscopic analysis,” J. Histochem. Cytochem. 38(5), 725–733 (1990).
[Crossref] [PubMed]

de Kok, Y. J.

A. I. den Hollander, J. R. Heckenlively, L. I. van den Born, Y. J. de Kok, S. D. van der Velde-Visser, U. Kellner, B. Jurklies, M. J. van Schooneveld, A. Blankenagel, K. Rohrschneider, B. Wissinger, J. R. Cruysberg, A. F. Deutman, H. G. Brunner, E. Apfelstedt-Sylla, C. B. Hoyng, and F. P. Cremers, “Leber congenital amaurosis and retinitis pigmentosa with Coats-like exudative vasculopathy are associated with mutations in the crumbs homologue 1 (CRB1) gene,” Am. J. Hum. Genet. 69(1), 198–203 (2001).
[Crossref] [PubMed]

Delori, F. C.

F. C. Delori, D. G. Goger, and C. K. Dorey, “Age-related accumulation and spatial distribution of lipofuscin in RPE of normal subjects,” Invest. Ophthalmol. Vis. Sci. 42(8), 1855–1866 (2001).
[PubMed]

den Hollander, A. I.

A. I. den Hollander, J. R. Heckenlively, L. I. van den Born, Y. J. de Kok, S. D. van der Velde-Visser, U. Kellner, B. Jurklies, M. J. van Schooneveld, A. Blankenagel, K. Rohrschneider, B. Wissinger, J. R. Cruysberg, A. F. Deutman, H. G. Brunner, E. Apfelstedt-Sylla, C. B. Hoyng, and F. P. Cremers, “Leber congenital amaurosis and retinitis pigmentosa with Coats-like exudative vasculopathy are associated with mutations in the crumbs homologue 1 (CRB1) gene,” Am. J. Hum. Genet. 69(1), 198–203 (2001).
[Crossref] [PubMed]

Deniset-Besseau, A.

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]

Deutman, A. F.

A. I. den Hollander, J. R. Heckenlively, L. I. van den Born, Y. J. de Kok, S. D. van der Velde-Visser, U. Kellner, B. Jurklies, M. J. van Schooneveld, A. Blankenagel, K. Rohrschneider, B. Wissinger, J. R. Cruysberg, A. F. Deutman, H. G. Brunner, E. Apfelstedt-Sylla, C. B. Hoyng, and F. P. Cremers, “Leber congenital amaurosis and retinitis pigmentosa with Coats-like exudative vasculopathy are associated with mutations in the crumbs homologue 1 (CRB1) gene,” Am. J. Hum. Genet. 69(1), 198–203 (2001).
[Crossref] [PubMed]

Dietz, J. A.

K. T. Janssen, C. E. Mac Nair, J. A. Dietz, C. L. Schlamp, and R. W. Nickells, “Nuclear atrophy of retinal ganglion cells precedes the bax-dependent stage of apoptosis,” Invest. Ophthalmol. Vis. Sci. 54(3), 1805–1815 (2013).
[Crossref] [PubMed]

Dorey, C. K.

F. C. Delori, D. G. Goger, and C. K. Dorey, “Age-related accumulation and spatial distribution of lipofuscin in RPE of normal subjects,” Invest. Ophthalmol. Vis. Sci. 42(8), 1855–1866 (2001).
[PubMed]

Drea, C. M.

M. L. Katz, C. M. Drea, and W. G. Robison., “Relationship between dietary retinol and lipofuscin in the retinal pigment epithelium,” Mech. Ageing Dev. 35(3), 291–305 (1986).
[Crossref] [PubMed]

Dunn, J. P.

J. P. Dunn, S. W. Noorily, M. Petri, D. Finkelstein, J. T. Rosenbaum, and D. A. Jabs, “Antiphospholipid antibodies and retinal vascular disease,” Lupus 5(4), 313–322 (1996).
[Crossref] [PubMed]

Eldred, G. E.

G. E. Eldred and M. L. Katz, “Fluorophores of the human retinal pigment epithelium: separation and spectral characterization,” Exp. Eye Res. 47(1), 71–86 (1988).
[Crossref] [PubMed]

Eldridge, S.

L. Feeney-Burns, E. S. Hilderbrand, and S. Eldridge, “Aging human RPE: morphometric analysis of macular, equatorial, and peripheral cells,” Invest. Ophthalmol. Vis. Sci. 25(2), 195–200 (1984).
[PubMed]

Feeney-Burns, L.

L. Feeney-Burns, E. S. Hilderbrand, and S. Eldridge, “Aging human RPE: morphometric analysis of macular, equatorial, and peripheral cells,” Invest. Ophthalmol. Vis. Sci. 25(2), 195–200 (1984).
[PubMed]

Feng, G.

G. Feng, R. H. Mellor, M. Bernstein, C. Keller-Peck, Q. T. Nguyen, M. Wallace, J. M. Nerbonne, J. W. Lichtman, and J. R. Sanes, “Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP,” Neuron 28(1), 41–51 (2000).
[Crossref] [PubMed]

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S. Lu, W. Min, S. Chong, G. R. Holtom, and X. S. Xie, “Label-free imaging of heme proteins with two-photon excited photothermal lens microscopy,” Appl. Phys. Lett. 96(11), 113701 (2010).
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J. P. Dunn, S. W. Noorily, M. Petri, D. Finkelstein, J. T. Rosenbaum, and D. A. Jabs, “Antiphospholipid antibodies and retinal vascular disease,” Lupus 5(4), 313–322 (1996).
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J. R. Sparrow, N. Fishkin, J. Zhou, B. Cai, Y. P. Jang, S. Krane, Y. Itagaki, and K. Nakanishi, “A2E, a byproduct of the visual cycle,” Vision Res. 43(28), 2983–2990 (2003).
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O. Masihzadeh, T. C. Lei, D. A. Ammar, M. Y. Kahook, and E. A. Gibson, “A multiphoton microscope platform for imaging the mouse eye,” Mol. Vis. 18, 1840–1848 (2012).
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V. H. Perry, R. J. Morris, and G. Raisman, “Is Thy-1 expressed only by ganglion cells and their axons in the retina and optic nerve?” J. Neurocytol. 13(5), 809–824 (1984).
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Sanes, J. R.

G. Feng, R. H. Mellor, M. Bernstein, C. Keller-Peck, Q. T. Nguyen, M. Wallace, J. M. Nerbonne, J. W. Lichtman, and J. R. Sanes, “Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP,” Neuron 28(1), 41–51 (2000).
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Am. J. Hum. Genet. (1)

A. I. den Hollander, J. R. Heckenlively, L. I. van den Born, Y. J. de Kok, S. D. van der Velde-Visser, U. Kellner, B. Jurklies, M. J. van Schooneveld, A. Blankenagel, K. Rohrschneider, B. Wissinger, J. R. Cruysberg, A. F. Deutman, H. G. Brunner, E. Apfelstedt-Sylla, C. B. Hoyng, and F. P. Cremers, “Leber congenital amaurosis and retinitis pigmentosa with Coats-like exudative vasculopathy are associated with mutations in the crumbs homologue 1 (CRB1) gene,” Am. J. Hum. Genet. 69(1), 198–203 (2001).
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Appl. Phys. Lett. (1)

S. Lu, W. Min, S. Chong, G. R. Holtom, and X. S. Xie, “Label-free imaging of heme proteins with two-photon excited photothermal lens microscopy,” Appl. Phys. Lett. 96(11), 113701 (2010).
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Biomed. Opt. Express (2)

Biophys. J. (1)

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Cell (1)

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Invest. Ophthalmol. Vis. Sci. (9)

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Figures (5)

Fig. 1
Fig. 1 Schematic diagram of multimodal NLO microscope system. BS: beam splitter; M: mirror; DM: dichroic mirror; SP: short-pass filter; FB: fiber bundle; M-PMT: Multichannel PMT array; TCSPC: time-correlated single photon counting module; Fs: filter set.
Fig. 2
Fig. 2 Representative TPEF and SRS images of different retinal layers. (a1)-(a2) TPEF and SRS images of the GCL; (b1)-(b2) IPL; (c1)-(c2) INL; (d1)-(d2) ONL; (e1)-(e2) RPE; (f1)-(f2) sclera; (g) histology image of H&E staining retinal sample; (h) TPEF spectra of each retinal layer. The field of view of (a)-(f) is 100 µm × 100 µm. Scale bar in (g): 40 µm. Depths of images: a-5 µm; b-20 µm; c-50 µm; d-70 µm; e-100 µm; f-110 µm.
Fig. 3
Fig. 3 Representative TPEF and SRS images of the NFL and the GCL in transgenic mice retinas. (a1)-(e1) TPEF images of transgenic mice retina; green: NADH in retinal neurons; orange: YFP labeled retinal neurons and optical nerve fibers; red: hemoglobin in red blood cells; (a2)-(e2) SRS images of transgenic mice retina. The field of view of all images is 100 µm × 100 µm. Arrow in (b&c): red blood cells. Arrow in (d&e): optical nerve fibers.
Fig. 4
Fig. 4 SRS and fluorescence images of transgenic mice retinas with RGCs retrograde labeled with DiI. (a1)-(c1) SRS images of the GCL; (a2)-(c2) fluorescence images of the YFP (green) and DiI (yellow) signals; (a3)-(c3) overlaid images of SRS and fluorescence; (d) TPEF lifetime of YFP and DiI signals; (e) histogram of nuclear diameter of DiI-labeled RGCs. The field of view of all images is 100 µm × 100 µm.
Fig. 5
Fig. 5 Imaging-guided spectral analysis of the RPE. (a1) TPEF spectra-coded image of RPE at 740 nm excitation; (a2) TPEF lifetime-coded image of RPE at 740 nm excitation; (b1) TPEF spectra-coded image of RPE at 780 nm excitation; (b2) TPEF lifetime-coded image of RPE at 780 nm excitation; (c1) TPEF spectra-coded image of RPE at 805 nm excitation; (c2) TPEF lifetime-coded image of RPE at 805 nm excitation; (d1) TPEF spectra of the particles in RPE at 740 nm, 760 nm and 780 nm excitation; (d2) TPEF spectra of the particle-removed background in RPE at 740 nm, 760 nm, 780 nm and 805 nm excitation. The field of view of all images is 100 µm × 100 µm.

Tables (1)

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Table 1 TPEF lifetime bi-exponential fitting parameters of fluorophores in RPE

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