Abstract

Two-photon microscopy allows visualization of subcellular structures in the living animal retina. In previously reported experiments it was necessary to apply a contact lens to each subject. Extending this technology to larger animals would require fitting a custom contact lens to each animal and cumbersome placement of the living animal head on microscope stage. Here we demonstrate a new device, periscope, for coupling light energy into mouse eye and capturing emitted fluorescence. Using this periscope we obtained images of the RPE and their subcellular organelles, retinosomes, with larger field of view than previously reported. This periscope provides an interface with a commercial microscope, does not require contact lens and its design could be modified to image retina in larger animals.

© 2015 Optical Society of America

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2015 (1)

Y. Du, M. Cramer, C. A. Lee, J. Tang, A. Muthusamy, D. A. Antonetti, H. Jin, K. Palczewski, and T. S. Kern, “Adrenergic and serotonin receptors affect retinal superoxide generation in diabetic mice: relationship to capillary degeneration and permeability,” FASEB J. 29(5), 2194–2204 (2015).
[Crossref] [PubMed]

2014 (5)

R. H. Douglas and G. Jeffery, “The spectral transmission of ocular media suggests ultraviolet sensitivity is widespread among mammals,” Proc. Biol. Sci. 281(1780), 20132995 (2014).
[Crossref] [PubMed]

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref] [PubMed]

G. Palczewska, M. Golczak, D. R. Williams, J. J. Hunter, and K. Palczewski, “Endogenous Fluorophores Enable Two-Photon Imaging of the Primate Eye,” Invest. Ophthalmol. Vis. Sci. 55(7), 4438–4447 (2014).
[Crossref] [PubMed]

G. Palczewska, F. Vinberg, P. Stremplewski, M. P. Bircher, D. Salom, K. Komar, J. Zhang, M. Cascella, M. Wojtkowski, V. J. Kefalov, and K. Palczewski, “Human infrared vision is triggered by two-photon chromophore isomerization,” Proc. Natl. Acad. Sci. U.S.A. 111(50), E5445–E5454 (2014).
[Crossref] [PubMed]

A. Maeda, G. Palczewska, M. Golczak, H. Kohno, Z. Dong, T. Maeda, and K. Palczewski, “Two-photon microscopy reveals early rod photoreceptor cell damage in light-exposed mutant mice,” Proc. Natl. Acad. Sci. U.S.A. 111(14), E1428–E1437 (2014).
[Crossref] [PubMed]

2013 (2)

Y. Miura, G. Huettmann, R. Orzekowsky-Schroeder, P. Steven, M. Szaszák, N. Koop, and R. Brinkmann, “Two-Photon Microscopy and Fluorescence Lifetime Imaging of Retinal Pigment Epithelial Cells Under Oxidative Stress,” Invest. Ophthalmol. Vis. Sci. 54(5), 3366–3377 (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]

2011 (4)

2010 (4)

D. Pestov, Y. Andegeko, V. Lozovoy, and M. Dantus, “Photobleaching and photoenhancement of endogenous fluorescence observed in two-photon microscopy with broadband laser sources,” J. Opt. 12(8), 084006 (2010).
[Crossref]

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]

J. M. Bueno, E. J. Gualda, and P. Artal, “Adaptive optics multiphoton microscopy to study ex vivo ocular tissues,” J. Biomed. Opt. 15(6), 066004 (2010).
[Crossref] [PubMed]

E. J. Gualda, J. M. Bueno, and P. Artal, “Wavefront optimized nonlinear microscopy of ex vivo human retinas,” J. Biomed. Opt. 15(2), 026007 (2010).
[Crossref] [PubMed]

2008 (1)

O. La Schiazza and J. F. Bille, “High-speed two-photon excited autofluorescence imaging of ex vivo human retinal pigment epithelial cells toward age-related macular degeneration diagnostic,” J. Biomed. Opt. 13(6), 064008 (2008).
[Crossref] [PubMed]

2007 (2)

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]

F. C. Delori, R. H. Webb, D. H. Sliney, and American National Standards Institute, “Maximum permissible exposures for ocular safety (ANSI 2000), with emphasis on ophthalmic devices,” J. Opt. Soc. Am. A 24(5), 1250–1265 (2007).
[Crossref] [PubMed]

2006 (5)

G. McConnell, “Improving the penetration depth in multiphoton excitation laser scanning microscopy,” J. Biomed. Opt. 11(5), 054020 (2006).
[Crossref] [PubMed]

E. G. de la Cera, G. Rodríguez, L. Llorente, F. Schaeffel, and S. Marcos, “Optical aberrations in the mouse eye,” Vision Res. 46(16), 2546–2553 (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]

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]

B. G. Wang, K. Koenig, I. Riemann, R. Krieg, and K. J. Halbhuber, “Intraocular multiphoton microscopy with subcellular spatial resolution by infrared femtosecond lasers,” Histochem. Cell Biol. 126(4), 507–515 (2006).
[Crossref] [PubMed]

2005 (1)

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[Crossref] [PubMed]

2004 (1)

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]

1998 (1)

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]

1997 (1)

R. Drabent, K. Bryl, B. Smyk, and K. Ulbrych, “Retinyl palmitate in water environment,” J. Photochem. Photobiol. B 37(3), 254–260 (1997).
[Crossref]

1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-Photon Laser Scanning Fluorescence Microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

1962 (1)

E. A. Boettner and J. R. Wolter, “Transmission of the Ocular Media,” Invest. Ophthalmol. 1(6), 776–783 (1962).

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]

Ahmad, K.

Alexander, N. S.

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref] [PubMed]

Andegeko, Y.

D. Pestov, Y. Andegeko, V. Lozovoy, and M. Dantus, “Photobleaching and photoenhancement of endogenous fluorescence observed in two-photon microscopy with broadband laser sources,” J. Opt. 12(8), 084006 (2010).
[Crossref]

Antonetti, D. A.

Y. Du, M. Cramer, C. A. Lee, J. Tang, A. Muthusamy, D. A. Antonetti, H. Jin, K. Palczewski, and T. S. Kern, “Adrenergic and serotonin receptors affect retinal superoxide generation in diabetic mice: relationship to capillary degeneration and permeability,” FASEB J. 29(5), 2194–2204 (2015).
[Crossref] [PubMed]

Artal, P.

J. M. Bueno, A. Giakoumaki, E. J. Gualda, F. Schaeffel, and P. Artal, “Analysis of the chicken retina with an adaptive optics multiphoton microscope,” Biomed. Opt. Express 2(6), 1637–1648 (2011).
[Crossref] [PubMed]

J. M. Bueno, E. J. Gualda, and P. Artal, “Adaptive optics multiphoton microscopy to study ex vivo ocular tissues,” J. Biomed. Opt. 15(6), 066004 (2010).
[Crossref] [PubMed]

E. J. Gualda, J. M. Bueno, and P. Artal, “Wavefront optimized nonlinear microscopy of ex vivo human retinas,” J. Biomed. Opt. 15(2), 026007 (2010).
[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]

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]

Bille, J. F.

O. La Schiazza and J. F. Bille, “High-speed two-photon excited autofluorescence imaging of ex vivo human retinal pigment epithelial cells toward age-related macular degeneration diagnostic,” J. Biomed. Opt. 13(6), 064008 (2008).
[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]

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]

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]

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]

Bircher, M. P.

G. Palczewska, F. Vinberg, P. Stremplewski, M. P. Bircher, D. Salom, K. Komar, J. Zhang, M. Cascella, M. Wojtkowski, V. J. Kefalov, and K. Palczewski, “Human infrared vision is triggered by two-photon chromophore isomerization,” Proc. Natl. Acad. Sci. U.S.A. 111(50), E5445–E5454 (2014).
[Crossref] [PubMed]

Boettner, E. A.

E. A. Boettner and J. R. Wolter, “Transmission of the Ocular Media,” Invest. Ophthalmol. 1(6), 776–783 (1962).

Brinkmann, R.

Y. Miura, G. Huettmann, R. Orzekowsky-Schroeder, P. Steven, M. Szaszák, N. Koop, and R. Brinkmann, “Two-Photon Microscopy and Fluorescence Lifetime Imaging of Retinal Pigment Epithelial Cells Under Oxidative Stress,” Invest. Ophthalmol. Vis. Sci. 54(5), 3366–3377 (2013).
[Crossref] [PubMed]

Bryl, K.

R. Drabent, K. Bryl, B. Smyk, and K. Ulbrych, “Retinyl palmitate in water environment,” J. Photochem. Photobiol. B 37(3), 254–260 (1997).
[Crossref]

Bueno, J. M.

J. M. Bueno, A. Giakoumaki, E. J. Gualda, F. Schaeffel, and P. Artal, “Analysis of the chicken retina with an adaptive optics multiphoton microscope,” Biomed. Opt. Express 2(6), 1637–1648 (2011).
[Crossref] [PubMed]

J. M. Bueno, E. J. Gualda, and P. Artal, “Adaptive optics multiphoton microscopy to study ex vivo ocular tissues,” J. Biomed. Opt. 15(6), 066004 (2010).
[Crossref] [PubMed]

E. J. Gualda, J. M. Bueno, and P. Artal, “Wavefront optimized nonlinear microscopy of ex vivo human retinas,” J. Biomed. Opt. 15(2), 026007 (2010).
[Crossref] [PubMed]

Cascella, M.

G. Palczewska, F. Vinberg, P. Stremplewski, M. P. Bircher, D. Salom, K. Komar, J. Zhang, M. Cascella, M. Wojtkowski, V. J. Kefalov, and K. Palczewski, “Human infrared vision is triggered by two-photon chromophore isomerization,” Proc. Natl. Acad. Sci. U.S.A. 111(50), E5445–E5454 (2014).
[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]

Cramer, M.

Y. Du, M. Cramer, C. A. Lee, J. Tang, A. Muthusamy, D. A. Antonetti, H. Jin, K. Palczewski, and T. S. Kern, “Adrenergic and serotonin receptors affect retinal superoxide generation in diabetic mice: relationship to capillary degeneration and permeability,” FASEB J. 29(5), 2194–2204 (2015).
[Crossref] [PubMed]

Curcio, C. A.

Dantus, M.

D. Pestov, Y. Andegeko, V. Lozovoy, and M. Dantus, “Photobleaching and photoenhancement of endogenous fluorescence observed in two-photon microscopy with broadband laser sources,” J. Opt. 12(8), 084006 (2010).
[Crossref]

de la Cera, E. G.

E. G. de la Cera, G. Rodríguez, L. Llorente, F. Schaeffel, and S. Marcos, “Optical aberrations in the mouse eye,” Vision Res. 46(16), 2546–2553 (2006).
[Crossref] [PubMed]

Delori, F. C.

Denk, W.

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[Crossref] [PubMed]

W. Denk, J. H. Strickler, and W. W. Webb, “Two-Photon Laser Scanning Fluorescence Microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Dong, Z.

A. Maeda, G. Palczewska, M. Golczak, H. Kohno, Z. Dong, T. Maeda, and K. Palczewski, “Two-photon microscopy reveals early rod photoreceptor cell damage in light-exposed mutant mice,” Proc. Natl. Acad. Sci. U.S.A. 111(14), E1428–E1437 (2014).
[Crossref] [PubMed]

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
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R. H. Douglas and G. Jeffery, “The spectral transmission of ocular media suggests ultraviolet sensitivity is widespread among mammals,” Proc. Biol. Sci. 281(1780), 20132995 (2014).
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Dubra, A.

Geng, Y.

Giakoumaki, A.

Giese, G.

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).
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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).
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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).
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G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
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G. Palczewska, M. Golczak, D. R. Williams, J. J. Hunter, and K. Palczewski, “Endogenous Fluorophores Enable Two-Photon Imaging of the Primate Eye,” Invest. Ophthalmol. Vis. Sci. 55(7), 4438–4447 (2014).
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A. Maeda, G. Palczewska, M. Golczak, H. Kohno, Z. Dong, T. Maeda, and K. Palczewski, “Two-photon microscopy reveals early rod photoreceptor cell damage in light-exposed mutant mice,” Proc. Natl. Acad. Sci. U.S.A. 111(14), E1428–E1437 (2014).
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J. M. Bueno, A. Giakoumaki, E. J. Gualda, F. Schaeffel, and P. Artal, “Analysis of the chicken retina with an adaptive optics multiphoton microscope,” Biomed. Opt. Express 2(6), 1637–1648 (2011).
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B. G. Wang, K. Koenig, I. Riemann, R. Krieg, and K. J. Halbhuber, “Intraocular multiphoton microscopy with subcellular spatial resolution by infrared femtosecond lasers,” Histochem. Cell Biol. 126(4), 507–515 (2006).
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Han, M.

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).
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F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
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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]

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]

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]

Huettmann, G.

Y. Miura, G. Huettmann, R. Orzekowsky-Schroeder, P. Steven, M. Szaszák, N. Koop, and R. Brinkmann, “Two-Photon Microscopy and Fluorescence Lifetime Imaging of Retinal Pigment Epithelial Cells Under Oxidative Stress,” Invest. Ophthalmol. Vis. Sci. 54(5), 3366–3377 (2013).
[Crossref] [PubMed]

Hunter, J. J.

G. Palczewska, M. Golczak, D. R. Williams, J. J. Hunter, and K. Palczewski, “Endogenous Fluorophores Enable Two-Photon Imaging of the Primate Eye,” Invest. Ophthalmol. Vis. Sci. 55(7), 4438–4447 (2014).
[Crossref] [PubMed]

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[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]

J. J. Hunter, B. Masella, A. Dubra, R. Sharma, L. Yin, W. H. Merigan, G. Palczewska, K. Palczewski, and D. R. Williams, “Images of photoreceptors in living primate eyes using adaptive optics two-photon ophthalmoscopy,” Biomed. Opt. Express 2(1), 139–148 (2011).
[Crossref] [PubMed]

Imanishi, 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]

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]

Jeffery, G.

R. H. Douglas and G. Jeffery, “The spectral transmission of ocular media suggests ultraviolet sensitivity is widespread among mammals,” Proc. Biol. Sci. 281(1780), 20132995 (2014).
[Crossref] [PubMed]

Jeon, C. J.

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]

Jin, H.

Y. Du, M. Cramer, C. A. Lee, J. Tang, A. Muthusamy, D. A. Antonetti, H. Jin, K. Palczewski, and T. S. Kern, “Adrenergic and serotonin receptors affect retinal superoxide generation in diabetic mice: relationship to capillary degeneration and permeability,” FASEB J. 29(5), 2194–2204 (2015).
[Crossref] [PubMed]

Kefalov, V. J.

G. Palczewska, F. Vinberg, P. Stremplewski, M. P. Bircher, D. Salom, K. Komar, J. Zhang, M. Cascella, M. Wojtkowski, V. J. Kefalov, and K. Palczewski, “Human infrared vision is triggered by two-photon chromophore isomerization,” Proc. Natl. Acad. Sci. U.S.A. 111(50), E5445–E5454 (2014).
[Crossref] [PubMed]

Kern, T. S.

Y. Du, M. Cramer, C. A. Lee, J. Tang, A. Muthusamy, D. A. Antonetti, H. Jin, K. Palczewski, and T. S. Kern, “Adrenergic and serotonin receptors affect retinal superoxide generation in diabetic mice: relationship to capillary degeneration and permeability,” FASEB J. 29(5), 2194–2204 (2015).
[Crossref] [PubMed]

Keyser, K.

Koenig, K.

B. G. Wang, K. Koenig, I. Riemann, R. Krieg, and K. J. Halbhuber, “Intraocular multiphoton microscopy with subcellular spatial resolution by infrared femtosecond lasers,” Histochem. Cell Biol. 126(4), 507–515 (2006).
[Crossref] [PubMed]

Kohno, H.

A. Maeda, G. Palczewska, M. Golczak, H. Kohno, Z. Dong, T. Maeda, and K. Palczewski, “Two-photon microscopy reveals early rod photoreceptor cell damage in light-exposed mutant mice,” Proc. Natl. Acad. Sci. U.S.A. 111(14), E1428–E1437 (2014).
[Crossref] [PubMed]

Komar, K.

G. Palczewska, F. Vinberg, P. Stremplewski, M. P. Bircher, D. Salom, K. Komar, J. Zhang, M. Cascella, M. Wojtkowski, V. J. Kefalov, and K. Palczewski, “Human infrared vision is triggered by two-photon chromophore isomerization,” Proc. Natl. Acad. Sci. U.S.A. 111(50), E5445–E5454 (2014).
[Crossref] [PubMed]

Koop, N.

Y. Miura, G. Huettmann, R. Orzekowsky-Schroeder, P. Steven, M. Szaszák, N. Koop, and R. Brinkmann, “Two-Photon Microscopy and Fluorescence Lifetime Imaging of Retinal Pigment Epithelial Cells Under Oxidative Stress,” Invest. Ophthalmol. Vis. Sci. 54(5), 3366–3377 (2013).
[Crossref] [PubMed]

Krieg, R.

B. G. Wang, K. Koenig, I. Riemann, R. Krieg, and K. J. Halbhuber, “Intraocular multiphoton microscopy with subcellular spatial resolution by infrared femtosecond lasers,” Histochem. Cell Biol. 126(4), 507–515 (2006).
[Crossref] [PubMed]

La Schiazza, O.

O. La Schiazza and J. F. Bille, “High-speed two-photon excited autofluorescence imaging of ex vivo human retinal pigment epithelial cells toward age-related macular degeneration diagnostic,” J. Biomed. Opt. 13(6), 064008 (2008).
[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]

Lee, C. A.

Y. Du, M. Cramer, C. A. Lee, J. Tang, A. Muthusamy, D. A. Antonetti, H. Jin, K. Palczewski, and T. S. Kern, “Adrenergic and serotonin receptors affect retinal superoxide generation in diabetic mice: relationship to capillary degeneration and permeability,” FASEB J. 29(5), 2194–2204 (2015).
[Crossref] [PubMed]

Li, Y. C.

Libby, R. T.

Llorente, L.

E. G. de la Cera, G. Rodríguez, L. Llorente, F. Schaeffel, and S. Marcos, “Optical aberrations in the mouse eye,” Vision Res. 46(16), 2546–2553 (2006).
[Crossref] [PubMed]

Lozovoy, V.

D. Pestov, Y. Andegeko, V. Lozovoy, and M. Dantus, “Photobleaching and photoenhancement of endogenous fluorescence observed in two-photon microscopy with broadband laser sources,” J. Opt. 12(8), 084006 (2010).
[Crossref]

Lu, R. W.

Maeda, A.

A. Maeda, G. Palczewska, M. Golczak, H. Kohno, Z. Dong, T. Maeda, and K. Palczewski, “Two-photon microscopy reveals early rod photoreceptor cell damage in light-exposed mutant mice,” Proc. Natl. Acad. Sci. U.S.A. 111(14), E1428–E1437 (2014).
[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]

Maeda, T.

A. Maeda, G. Palczewska, M. Golczak, H. Kohno, Z. Dong, T. Maeda, and K. Palczewski, “Two-photon microscopy reveals early rod photoreceptor cell damage in light-exposed mutant mice,” Proc. Natl. Acad. Sci. U.S.A. 111(14), E1428–E1437 (2014).
[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]

Marcos, S.

E. G. de la Cera, G. Rodríguez, L. Llorente, F. Schaeffel, and S. Marcos, “Optical aberrations in the mouse eye,” Vision Res. 46(16), 2546–2553 (2006).
[Crossref] [PubMed]

Masella, B.

Masland, R. H.

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]

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G. McConnell, “Improving the penetration depth in multiphoton excitation laser scanning microscopy,” J. Biomed. Opt. 11(5), 054020 (2006).
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Merigan, W. H.

Miura, Y.

Y. Miura, G. Huettmann, R. Orzekowsky-Schroeder, P. Steven, M. Szaszák, N. Koop, and R. Brinkmann, “Two-Photon Microscopy and Fluorescence Lifetime Imaging of Retinal Pigment Epithelial Cells Under Oxidative Stress,” Invest. Ophthalmol. Vis. Sci. 54(5), 3366–3377 (2013).
[Crossref] [PubMed]

Muthusamy, A.

Y. Du, M. Cramer, C. A. Lee, J. Tang, A. Muthusamy, D. A. Antonetti, H. Jin, K. Palczewski, and T. S. Kern, “Adrenergic and serotonin receptors affect retinal superoxide generation in diabetic mice: relationship to capillary degeneration and permeability,” FASEB J. 29(5), 2194–2204 (2015).
[Crossref] [PubMed]

Niemz, M. H.

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]

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]

Orzekowsky-Schroeder, R.

Y. Miura, G. Huettmann, R. Orzekowsky-Schroeder, P. Steven, M. Szaszák, N. Koop, and R. Brinkmann, “Two-Photon Microscopy and Fluorescence Lifetime Imaging of Retinal Pigment Epithelial Cells Under Oxidative Stress,” Invest. Ophthalmol. Vis. Sci. 54(5), 3366–3377 (2013).
[Crossref] [PubMed]

Palczewska, G.

G. Palczewska, F. Vinberg, P. Stremplewski, M. P. Bircher, D. Salom, K. Komar, J. Zhang, M. Cascella, M. Wojtkowski, V. J. Kefalov, and K. Palczewski, “Human infrared vision is triggered by two-photon chromophore isomerization,” Proc. Natl. Acad. Sci. U.S.A. 111(50), E5445–E5454 (2014).
[Crossref] [PubMed]

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref] [PubMed]

G. Palczewska, M. Golczak, D. R. Williams, J. J. Hunter, and K. Palczewski, “Endogenous Fluorophores Enable Two-Photon Imaging of the Primate Eye,” Invest. Ophthalmol. Vis. Sci. 55(7), 4438–4447 (2014).
[Crossref] [PubMed]

A. Maeda, G. Palczewska, M. Golczak, H. Kohno, Z. Dong, T. Maeda, and K. Palczewski, “Two-photon microscopy reveals early rod photoreceptor cell damage in light-exposed mutant mice,” Proc. Natl. Acad. Sci. U.S.A. 111(14), E1428–E1437 (2014).
[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]

J. J. Hunter, B. Masella, A. Dubra, R. Sharma, L. Yin, W. H. Merigan, G. Palczewska, K. Palczewski, and D. R. Williams, “Images of photoreceptors in living primate eyes using adaptive optics two-photon ophthalmoscopy,” Biomed. Opt. Express 2(1), 139–148 (2011).
[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]

Palczewski, K.

Y. Du, M. Cramer, C. A. Lee, J. Tang, A. Muthusamy, D. A. Antonetti, H. Jin, K. Palczewski, and T. S. Kern, “Adrenergic and serotonin receptors affect retinal superoxide generation in diabetic mice: relationship to capillary degeneration and permeability,” FASEB J. 29(5), 2194–2204 (2015).
[Crossref] [PubMed]

A. Maeda, G. Palczewska, M. Golczak, H. Kohno, Z. Dong, T. Maeda, and K. Palczewski, “Two-photon microscopy reveals early rod photoreceptor cell damage in light-exposed mutant mice,” Proc. Natl. Acad. Sci. U.S.A. 111(14), E1428–E1437 (2014).
[Crossref] [PubMed]

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref] [PubMed]

G. Palczewska, M. Golczak, D. R. Williams, J. J. Hunter, and K. Palczewski, “Endogenous Fluorophores Enable Two-Photon Imaging of the Primate Eye,” Invest. Ophthalmol. Vis. Sci. 55(7), 4438–4447 (2014).
[Crossref] [PubMed]

G. Palczewska, F. Vinberg, P. Stremplewski, M. P. Bircher, D. Salom, K. Komar, J. Zhang, M. Cascella, M. Wojtkowski, V. J. Kefalov, and K. Palczewski, “Human infrared vision is triggered by two-photon chromophore isomerization,” Proc. Natl. Acad. Sci. U.S.A. 111(50), E5445–E5454 (2014).
[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]

J. J. Hunter, B. Masella, A. Dubra, R. Sharma, L. Yin, W. H. Merigan, G. Palczewska, K. Palczewski, and D. R. Williams, “Images of photoreceptors in living primate eyes using adaptive optics two-photon ophthalmoscopy,” Biomed. Opt. Express 2(1), 139–148 (2011).
[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]

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]

Pestov, D.

D. Pestov, Y. Andegeko, V. Lozovoy, and M. Dantus, “Photobleaching and photoenhancement of endogenous fluorescence observed in two-photon microscopy with broadband laser sources,” J. Opt. 12(8), 084006 (2010).
[Crossref]

Piston, D. W.

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]

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]

Riemann, I.

B. G. Wang, K. Koenig, I. Riemann, R. Krieg, and K. J. Halbhuber, “Intraocular multiphoton microscopy with subcellular spatial resolution by infrared femtosecond lasers,” Histochem. Cell Biol. 126(4), 507–515 (2006).
[Crossref] [PubMed]

Rodríguez, G.

E. G. de la Cera, G. Rodríguez, L. Llorente, F. Schaeffel, and S. Marcos, “Optical aberrations in the mouse eye,” Vision Res. 46(16), 2546–2553 (2006).
[Crossref] [PubMed]

Salom, D.

G. Palczewska, F. Vinberg, P. Stremplewski, M. P. Bircher, D. Salom, K. Komar, J. Zhang, M. Cascella, M. Wojtkowski, V. J. Kefalov, and K. Palczewski, “Human infrared vision is triggered by two-photon chromophore isomerization,” Proc. Natl. Acad. Sci. U.S.A. 111(50), E5445–E5454 (2014).
[Crossref] [PubMed]

Schaeffel, F.

J. M. Bueno, A. Giakoumaki, E. J. Gualda, F. Schaeffel, and P. Artal, “Analysis of the chicken retina with an adaptive optics multiphoton microscope,” Biomed. Opt. Express 2(6), 1637–1648 (2011).
[Crossref] [PubMed]

E. G. de la Cera, G. Rodríguez, L. Llorente, F. Schaeffel, and S. Marcos, “Optical aberrations in the mouse eye,” Vision Res. 46(16), 2546–2553 (2006).
[Crossref] [PubMed]

Schery, L. A.

Schmitz-Valckenberg, S.

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]

Sharma, R.

Sliney, D. H.

Smyk, B.

R. Drabent, K. Bryl, B. Smyk, and K. Ulbrych, “Retinyl palmitate in water environment,” J. Photochem. Photobiol. B 37(3), 254–260 (1997).
[Crossref]

Snyder, S.

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]

Snyder, S. R.

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]

Steven, P.

Y. Miura, G. Huettmann, R. Orzekowsky-Schroeder, P. Steven, M. Szaszák, N. Koop, and R. Brinkmann, “Two-Photon Microscopy and Fluorescence Lifetime Imaging of Retinal Pigment Epithelial Cells Under Oxidative Stress,” Invest. Ophthalmol. Vis. Sci. 54(5), 3366–3377 (2013).
[Crossref] [PubMed]

Strang, C.

Stremplewski, P.

G. Palczewska, F. Vinberg, P. Stremplewski, M. P. Bircher, D. Salom, K. Komar, J. Zhang, M. Cascella, M. Wojtkowski, V. J. Kefalov, and K. Palczewski, “Human infrared vision is triggered by two-photon chromophore isomerization,” Proc. Natl. Acad. Sci. U.S.A. 111(50), E5445–E5454 (2014).
[Crossref] [PubMed]

Strettoi, E.

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]

Strickler, J. H.

W. Denk, J. H. Strickler, and W. W. Webb, “Two-Photon Laser Scanning Fluorescence Microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Sun, H.

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]

Sun, W.

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]

Szaszák, M.

Y. Miura, G. Huettmann, R. Orzekowsky-Schroeder, P. Steven, M. Szaszák, N. Koop, and R. Brinkmann, “Two-Photon Microscopy and Fluorescence Lifetime Imaging of Retinal Pigment Epithelial Cells Under Oxidative Stress,” Invest. Ophthalmol. Vis. Sci. 54(5), 3366–3377 (2013).
[Crossref] [PubMed]

Tang, J.

Y. Du, M. Cramer, C. A. Lee, J. Tang, A. Muthusamy, D. A. Antonetti, H. Jin, K. Palczewski, and T. S. Kern, “Adrenergic and serotonin receptors affect retinal superoxide generation in diabetic mice: relationship to capillary degeneration and permeability,” FASEB J. 29(5), 2194–2204 (2015).
[Crossref] [PubMed]

Ulbrych, K.

R. Drabent, K. Bryl, B. Smyk, and K. Ulbrych, “Retinyl palmitate in water environment,” J. Photochem. Photobiol. B 37(3), 254–260 (1997).
[Crossref]

Vinberg, F.

G. Palczewska, F. Vinberg, P. Stremplewski, M. P. Bircher, D. Salom, K. Komar, J. Zhang, M. Cascella, M. Wojtkowski, V. J. Kefalov, and K. Palczewski, “Human infrared vision is triggered by two-photon chromophore isomerization,” Proc. Natl. Acad. Sci. U.S.A. 111(50), E5445–E5454 (2014).
[Crossref] [PubMed]

Wang, B. G.

B. G. Wang, K. Koenig, I. Riemann, R. Krieg, and K. J. Halbhuber, “Intraocular multiphoton microscopy with subcellular spatial resolution by infrared femtosecond lasers,” Histochem. Cell Biol. 126(4), 507–515 (2006).
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Webb, W. W.

W. Denk, J. H. Strickler, and W. W. Webb, “Two-Photon Laser Scanning Fluorescence Microscopy,” Science 248(4951), 73–76 (1990).
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Williams, D. R.

G. Palczewska, M. Golczak, D. R. Williams, J. J. Hunter, and K. Palczewski, “Endogenous Fluorophores Enable Two-Photon Imaging of the Primate Eye,” Invest. Ophthalmol. Vis. Sci. 55(7), 4438–4447 (2014).
[Crossref] [PubMed]

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
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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]

Y. Geng, L. A. Schery, R. Sharma, A. Dubra, K. Ahmad, R. T. Libby, and D. R. Williams, “Optical properties of the mouse eye,” Biomed. Opt. Express 2(4), 717–738 (2011).
[Crossref] [PubMed]

J. J. Hunter, B. Masella, A. Dubra, R. Sharma, L. Yin, W. H. Merigan, G. Palczewska, K. Palczewski, and D. R. Williams, “Images of photoreceptors in living primate eyes using adaptive optics two-photon ophthalmoscopy,” Biomed. Opt. Express 2(1), 139–148 (2011).
[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]

Wojtkowski, M.

G. Palczewska, F. Vinberg, P. Stremplewski, M. P. Bircher, D. Salom, K. Komar, J. Zhang, M. Cascella, M. Wojtkowski, V. J. Kefalov, and K. Palczewski, “Human infrared vision is triggered by two-photon chromophore isomerization,” Proc. Natl. Acad. Sci. U.S.A. 111(50), E5445–E5454 (2014).
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E. A. Boettner and J. R. Wolter, “Transmission of the Ocular Media,” Invest. Ophthalmol. 1(6), 776–783 (1962).

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Ye, T.

Yin, L.

Yu, J.

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]

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]

Zhang, J.

G. Palczewska, F. Vinberg, P. Stremplewski, M. P. Bircher, D. Salom, K. Komar, J. Zhang, M. Cascella, M. Wojtkowski, V. J. Kefalov, and K. Palczewski, “Human infrared vision is triggered by two-photon chromophore isomerization,” Proc. Natl. Acad. Sci. U.S.A. 111(50), E5445–E5454 (2014).
[Crossref] [PubMed]

Biomed. Opt. Express (5)

FASEB J. (1)

Y. Du, M. Cramer, C. A. Lee, J. Tang, A. Muthusamy, D. A. Antonetti, H. Jin, K. Palczewski, and T. S. Kern, “Adrenergic and serotonin receptors affect retinal superoxide generation in diabetic mice: relationship to capillary degeneration and permeability,” FASEB J. 29(5), 2194–2204 (2015).
[Crossref] [PubMed]

Histochem. Cell Biol. (1)

B. G. Wang, K. Koenig, I. Riemann, R. Krieg, and K. J. Halbhuber, “Intraocular multiphoton microscopy with subcellular spatial resolution by infrared femtosecond lasers,” Histochem. Cell Biol. 126(4), 507–515 (2006).
[Crossref] [PubMed]

Invest. Ophthalmol. (1)

E. A. Boettner and J. R. Wolter, “Transmission of the Ocular Media,” Invest. Ophthalmol. 1(6), 776–783 (1962).

Invest. Ophthalmol. Vis. Sci. (3)

G. Palczewska, M. Golczak, D. R. Williams, J. J. Hunter, and K. Palczewski, “Endogenous Fluorophores Enable Two-Photon Imaging of the Primate Eye,” Invest. Ophthalmol. Vis. Sci. 55(7), 4438–4447 (2014).
[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. Miura, G. Huettmann, R. Orzekowsky-Schroeder, P. Steven, M. Szaszák, N. Koop, and R. Brinkmann, “Two-Photon Microscopy and Fluorescence Lifetime Imaging of Retinal Pigment Epithelial Cells Under Oxidative Stress,” Invest. Ophthalmol. Vis. Sci. 54(5), 3366–3377 (2013).
[Crossref] [PubMed]

J. Biomed. Opt. (6)

G. McConnell, “Improving the penetration depth in multiphoton excitation laser scanning microscopy,” J. Biomed. Opt. 11(5), 054020 (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]

O. La Schiazza and J. F. Bille, “High-speed two-photon excited autofluorescence imaging of ex vivo human retinal pigment epithelial cells toward age-related macular degeneration diagnostic,” J. Biomed. Opt. 13(6), 064008 (2008).
[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]

J. M. Bueno, E. J. Gualda, and P. Artal, “Adaptive optics multiphoton microscopy to study ex vivo ocular tissues,” J. Biomed. Opt. 15(6), 066004 (2010).
[Crossref] [PubMed]

E. J. Gualda, J. M. Bueno, and P. Artal, “Wavefront optimized nonlinear microscopy of ex vivo human retinas,” J. Biomed. Opt. 15(2), 026007 (2010).
[Crossref] [PubMed]

J. Cell Biol. (1)

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]

J. Neurosci. (1)

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]

J. Opt. (1)

D. Pestov, Y. Andegeko, V. Lozovoy, and M. Dantus, “Photobleaching and photoenhancement of endogenous fluorescence observed in two-photon microscopy with broadband laser sources,” J. Opt. 12(8), 084006 (2010).
[Crossref]

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

J. Photochem. Photobiol. B (1)

R. Drabent, K. Bryl, B. Smyk, and K. Ulbrych, “Retinyl palmitate in water environment,” J. Photochem. Photobiol. B 37(3), 254–260 (1997).
[Crossref]

Nat. Med. (2)

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]

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref] [PubMed]

Nat. Methods (1)

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[Crossref] [PubMed]

Proc. Biol. Sci. (1)

R. H. Douglas and G. Jeffery, “The spectral transmission of ocular media suggests ultraviolet sensitivity is widespread among mammals,” Proc. Biol. Sci. 281(1780), 20132995 (2014).
[Crossref] [PubMed]

Proc. Natl. Acad. Sci. U.S.A. (2)

G. Palczewska, F. Vinberg, P. Stremplewski, M. P. Bircher, D. Salom, K. Komar, J. Zhang, M. Cascella, M. Wojtkowski, V. J. Kefalov, and K. Palczewski, “Human infrared vision is triggered by two-photon chromophore isomerization,” Proc. Natl. Acad. Sci. U.S.A. 111(50), E5445–E5454 (2014).
[Crossref] [PubMed]

A. Maeda, G. Palczewska, M. Golczak, H. Kohno, Z. Dong, T. Maeda, and K. Palczewski, “Two-photon microscopy reveals early rod photoreceptor cell damage in light-exposed mutant mice,” Proc. Natl. Acad. Sci. U.S.A. 111(14), E1428–E1437 (2014).
[Crossref] [PubMed]

Science (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-Photon Laser Scanning Fluorescence Microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Vision Res. (1)

E. G. de la Cera, G. Rodríguez, L. Llorente, F. Schaeffel, and S. Marcos, “Optical aberrations in the mouse eye,” Vision Res. 46(16), 2546–2553 (2006).
[Crossref] [PubMed]

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Figures (5)

Fig. 1
Fig. 1 (a) Position of the periscope in the microscope setup. DM 1 and DM 2 are dichroic mirrors, SPF is a short pass filter. (b) Schematic of the periscope and centers of the extreme rays (blue lines). L1 is an achromatic doublet with a 75 mm focal length and 25 mm diameter; L2 is an achromatic doublet with a 10 mm focal length and an 8 mm diameter. Unless otherwise specified, all dimensions shown are in millimeters.
Fig. 2
Fig. 2 (a) Calculated imaging depth adjustment range. The central position of L1 results in a collimated periscope output beam and a focal spot located 2.5 mm from eye lens. (b) Calculated FOV versus position of focal spot with respect to the cardinal plane of the eye lens.
Fig. 3
Fig. 3 Two-photon imaging of the RPE in living WT and Rpe65–/– mice. (a) Mouse eye illuminated with the newly designed periscope. (b) Image of the RPE in the WT albino mouse. (c), (d). Enlarged images of the RPE in Rpe65–/– (c) and WT (d) albino mice. Excitation wavelength: 730 nm. Mean power at the cornea: 20 mW in (c) and 25 mW in (b) and (d). Scale bars: 100 µm in (b), and 50 µm in (c) and (d). Red arrows indicate shadows from retinal vasculature.
Fig. 4
Fig. 4 Images of retinal capillaries in a live WT mouse after tail vain injection with FITC-BSA. Images were acquired with a TPM equipped with a periscope. Top row images were acquired with dispersion compensation (DC), bottom row images were procured without dispersion compensation. Excitation wavelengths are indicated in each image. Scale bars are equal to 100 µm.
Fig. 5
Fig. 5 Fluorescence emission spectrum from the RPE of a live Rpe65−/−mouse. (a) Spectrum measured with a periscope had maximum at 524 nm. (b) Deconvolution of the spectrum (black squares, red line) revealed two components (green lines), one with a maximum at 524 nm and the second, a long wavelength shoulder with a maximum at 627 nm.

Equations (2)

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M a = f L1 f L2 = 75 10
M f = f eye f obj = 2.5 10

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