Abstract

Two-photon ophthalmoscopy has potential for in vivo assessment of function of normal and diseased retina. However, light safety of the sub-100 fs laser typically used is a major concern and safety standards are not well established. To test the feasibility of safe in vivo two-photon excitation fluorescence (TPEF) imaging of photoreceptors in humans, we examined the effects of ultrashort pulsed light and the required light levels with a variety of clinical and high resolution imaging methods in macaques. The only measure that revealed a significant effect due to exposure to pulsed light within existing safety standards was infrared autofluorescence (IRAF) intensity. No other structural or functional alterations were detected by other imaging techniques for any of the exposures. Photoreceptors and retinal pigment epithelium appeared normal in adaptive optics images. No effect of repeated exposures on TPEF time course was detected, suggesting that visual cycle function was maintained. If IRAF reduction is hazardous, it is the only hurdle to applying two-photon retinal imaging in humans. To date, no harmful effects of IRAF reduction have been detected.

© 2016 Optical Society of America

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2016 (3)

R. Sharma, D. R. Williams, G. Palczewska, K. Palczewski, and J. J. Hunter, “Two-Photon Autofluorescence Imaging Reveals Cellular Structures Throughout the Retina of the Living Primate Eye,” Invest. Ophthalmol. Vis. Sci. 57(2), 632–646 (2016).
[Crossref] [PubMed]

R. Sharma, C. Schwarz, D. R. Williams, G. Palczewska, K. Palczewski, and J. J. Hunter, “In Vivo Two-Photon Fluorescence Kinetics of Primate Rods and Cones,” Invest. Ophthalmol. Vis. Sci. 57(2), 647–657 (2016).
[Crossref] [PubMed]

J. Zhang, R. Sabarinathan, T. Bubel, D. R. Williams, and J. J. Hunter, “Action spectrum for photochemical retinal pigment epithelium (RPE) disruption in an in vivo monkey model,” Proc. SPIE 9706, 1–6 (2016).

2015 (1)

A. Roorda and J. L. Duncan, “Adaptive optics ophthalmoscopy,” Annu Rev Vis Sci 1(1), 19–50 (2015).
[Crossref] [PubMed]

2014 (8)

Q. Yang, J. Zhang, K. Nozato, K. Saito, D. R. Williams, A. Roorda, and E. A. Rossi, “Closed-loop optical stabilization and digital image registration in adaptive optics scanning light ophthalmoscopy,” Biomed. Opt. Express 5(9), 3174–3191 (2014).
[Crossref] [PubMed]

B. D. Masella, D. R. Williams, W. S. Fischer, E. A. Rossi, and J. J. Hunter, “Long-term reduction in infrared autofluorescence caused by infrared light below the maximum permissible exposure,” Invest. Ophthalmol. Vis. Sci. 55(6), 3929–3938 (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]

G. M. Pocock, J. W. Oliver, C. S. Specht, J. S. Estep, G. D. Noojin, K. Schuster, and B. A. Rockwell, “High-resolution in vivo imaging of regimes of laser damage to the primate retina,” J. Ophthalmol. 2014, 516854 (2014).
[Crossref] [PubMed]

B. D. Masella, J. J. Hunter, and D. R. Williams, “Rod photopigment kinetics after photodisruption of the retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 55(11), 7535–7544 (2014).
[Crossref] [PubMed]

P. D. Kiser, M. Golczak, and K. Palczewski, “Chemistry of the retinoid (visual) cycle,” Chem. Rev. 114(1), 194–232 (2014).
[Crossref] [PubMed]

R. N. Weinreb, T. Aung, and F. A. Medeiros, “The Pathophysiology and Treatment of Glaucoma: a Review,” JAMA 311(18), 1901–1911 (2014).
[Crossref] [PubMed]

B. D. Masella, J. J. Hunter, and D. R. Williams, “New wrinkles in retinal densitometry,” Invest. Ophthalmol. Vis. Sci. 55(11), 7525–7534 (2014).
[Crossref] [PubMed]

2012 (2)

P. D. Kiser, M. Golczak, A. Maeda, and K. Palczewski, “Key enzymes of the retinoid (visual) cycle in vertebrate retina,” Biochim. Biophys. Acta – Mol. Cell Biol. Lipids 1821(1), 137–151 (2012).
[Crossref]

J. J. Hunter, J. I. W. Morgan, W. H. Merigan, D. H. Sliney, J. R. Sparrow, and D. R. Williams, “The susceptibility of the retina to photochemical damage from visible light,” Prog. Retin. Eye Res. 31(1), 28–42 (2012).
[Crossref] [PubMed]

2011 (4)

2010 (5)

C. W. Shuttleworth, “Use of NAD(P)H and flavoprotein autofluorescence transients to probe neuron and astrocyte responses to synaptic activation,” Neurochem. Int. 56(3), 379–386 (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]

E. E. Sutter, “Noninvasive Testing Methods: Multifocal Electrophysiology,” Encycl. Eye. 3, 142–160 (2010).

B. A. Rockwell, R. J. Thomas, and A. Vogel, “Ultrashort laser pulse retinal damage mechanisms and their impact on thresholds,” Med. Laser Appl. 25(2), 84–92 (2010).
[Crossref]

A. Dubra and Z. Harvey, “Registration of 2D images from fast scanning ophthalmic instruments,” Lect. Notes Comput. Sci. 6204, 60–71 (2010).
[Crossref]

2009 (3)

J. I. W. Morgan, J. J. Hunter, W. H. Merigan, and D. R. Williams, “The reduction of retinal autofluorescence caused by light exposure,” Invest. Ophthalmol. Vis. Sci. 50(12), 6015–6022 (2009).
[Crossref] [PubMed]

J. I. W. Morgan, A. Dubra, R. Wolfe, W. H. Merigan, and D. R. Williams, “In vivo autofluorescence imaging of the human and macaque retinal pigment epithelial cell mosaic,” Invest. Ophthalmol. Vis. Sci. 50(3), 1350–1359 (2009).
[Crossref] [PubMed]

K. Tsunoda, G. Hanazono, K. Inomata, Y. Kazato, W. Suzuki, and M. Tanifuji, “Origins of retinal intrinsic signals: a series of experiments on retinas of macaque monkeys,” Jpn. J. Ophthalmol. 53(4), 297–314 (2009).
[Crossref] [PubMed]

2008 (2)

K. Grieve and A. Roorda, “Intrinsic signals from human cone photoreceptors,” Invest. Ophthalmol. Vis. Sci. 49(2), 713–719 (2008).
[Crossref] [PubMed]

J. I. W. Morgan, J. J. Hunter, B. Masella, R. Wolfe, D. C. Gray, W. H. Merigan, F. C. Delori, and D. R. Williams, “Light-induced retinal changes observed with high-resolution autofluorescence imaging of the retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 49(8), 3715–3729 (2008).
[Crossref] [PubMed]

2007 (4)

2006 (3)

P. Ala-Laurila, A. V. Kolesnikov, R. K. Crouch, E. Tsina, S. A. Shukolyukov, V. I. Govardovskii, Y. Koutalos, B. Wiggert, M. E. Estevez, and M. C. Cornwall, “Visual cycle: Dependence of retinol production and removal on photoproduct decay and cell morphology,” J. Gen. Physiol. 128(2), 153–169 (2006).
[Crossref] [PubMed]

K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50(6), 823–839 (2006).
[Crossref] [PubMed]

C. N. Keilhauer and F. C. Delori, “Near-infrared autofluorescence imaging of the fundus: visualization of ocular melanin,” Invest. Ophthalmol. Vis. Sci. 47(8), 3556–3564 (2006).
[Crossref] [PubMed]

2005 (3)

C. Chen, E. Tsina, M. C. Cornwall, R. K. Crouch, S. Vijayaraghavan, and Y. Koutalos, “Reduction of all-trans retinal to all-trans retinol in the outer segments of frog and mouse rod photoreceptors,” Biophys. J. 88(3), 2278–2287 (2005).
[Crossref] [PubMed]

C. P. Cain, R. J. Thomas, G. D. Noojin, D. J. Stolarski, P. K. Kennedy, G. D. Buffington, and B. A. Rockwell, “Sub-50-fs laser retinal damage thresholds in primate eyes with group velocity dispersion, self-focusing and low-density plasmas,” Graefes Arch. Clin. Exp. Ophthalmol. 243(2), 101–112 (2005).
[Crossref] [PubMed]

A. Diaspro, G. Chirico, and M. Collini, “Two-photon fluorescence excitation and related techniques in biological microscopy,” Q. Rev. Biophys. 38(2), 97–166 (2005).
[Crossref] [PubMed]

2004 (5)

V. C. Greenstein, K. Holopigian, W. Seiple, R. E. Carr, and D. C. Hood, “Atypical multifocal ERG responses in patients with diseases affecting the photoreceptors,” Vision Res. 44(25), 2867–2874 (2004).
[Crossref] [PubMed]

E. Tsina, C. Chen, Y. Koutalos, P. Ala-Laurila, M. Tsacopoulos, B. Wiggert, R. K. Crouch, and M. C. Cornwall, “Physiological and microfluorometric studies of reduction and clearance of retinal in bleached rod photoreceptors,” J. Gen. Physiol. 124(4), 429–443 (2004).
[Crossref] [PubMed]

T. D. Lamb and E. N. Pugh., “Dark adaptation and the retinoid cycle of vision,” Prog. Retin. Eye Res. 23(3), 307–380 (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]

O. A. R. Mahroo and T. D. Lamb, “Recovery of the human photopic electroretinogram after bleaching exposures: estimation of pigment regeneration kinetics,” J. Physiol. 554(2), 417–437 (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]

D. A. Thompson and A. Gal, “Vitamin A metabolism in the retinal pigment epithelium: genes, mutations, and diseases,” Prog. Retin. Eye Res. 22(5), 683–703 (2003).
[Crossref] [PubMed]

2002 (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).
[Crossref] [PubMed]

A. Vogel, G. Huttmann, G. Paltauf, and J. Noack, “Femtosecond-laser-produced low-density plasmas in transparent biological media: A tool for the creation of chemical, thermal and thermomechanical effects below the optical breakdown threshold,” SPIE Photonics West 4633, 23–37 (2002).

A. Vogel, J. Noack, G. Huettmann, and G. Paltauf, “Low-density plasmas below the optical breakdown threshold: potential hazard for multiphoton microscopy, and a tool for the manipulation of intracellular events,” SPIE Photonics West 4620, 202–216 (2002).

2001 (3)

P. Kayatz, G. Thumann, T. T. Luther, J. F. Jordan, K. U. Bartz-Schmidt, P. J. Esser, and U. Schraermeyer, “Oxidation causes melanin fluorescence,” Invest. Ophthalmol. Vis. Sci. 42(1), 241–246 (2001).
[PubMed]

C. Keller, C. Grimm, A. Wenzel, F. Hafezi, and C. Remé, “Protective effect of halothane anesthesia on retinal light damage: inhibition of metabolic rhodopsin regeneration,” Invest. Ophthalmol. Vis. Sci. 42(2), 476–480 (2001).
[PubMed]

M. Boulton, M. Rózanowska, and B. Rózanowski, “Retinal photodamage,” J. Photochem. Photobiol. Bol. Biol. 64, 144–161 (2001).

2000 (1)

J. C. Saari, “Biochemistry of Visual Pigment Regeneration: the Friedenwald Lecture,” Invest. Ophthalmol. Vis. Sci. 41(2), 337–348 (2000).
[PubMed]

1997 (1)

1996 (1)

G. J. Brakenhoff, M. Müller, and R. I. Ghauharali, “Analysis of efficiency of two-photon versus single-photon absorption of fluorescence generation in biological objects,” J. Microsc. 183(2), 140–144 (1996).
[Crossref] [PubMed]

1995 (4)

F. C. Delori, C. K. Dorey, G. Staurenghi, O. Arend, D. G. Goger, and J. J. Weiter, “In vivo fluorescence of the ocular fundus exhibits retinal pigment epithelium lipofuscin characteristics,” Invest. Ophthalmol. Vis. Sci. 36(3), 718–729 (1995).
[PubMed]

A. C. Bird, “Retinal photoreceptor dystrophies LI. Edward Jackson Memorial Lecture,” Am. J. Ophthalmol. 119(5), 543–562 (1995).
[Crossref] [PubMed]

P. K. Kennedy, “A First-Order Model for Computation of Laser-Induced Breakdown Thresholds in Ocular and Aqueous Media: Part I - Theory,” IEEE J. Quantum Electron. 31(12), 2241–2249 (1995).
[Crossref]

P. K. Kennedy, S. A. Boppart, D. X. Hammer, B. A. Rockwell, G. D. Noojin, and W. P. Roach, “A First-Order Model for Computation of Laser-Induced Breakdown Thresholds in Ocular and Aqueous Media: II - Comparison to Experiment,” IEEE J. Quantum Electron. 31(12), 2250–2257 (1995).
[Crossref]

1993 (2)

1992 (1)

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]

1987 (1)

D. A. Baylor, B. J. Nunn, and J. L. Schnapf, “Spectral sensitivity of cones of the monkey Macaca fascicularis,” J. Physiol. 390(1), 145–160 (1987).
[Crossref] [PubMed]

1985 (1)

M. W. Kaplan, “Distribution and axial diffusion of retinol in bleached rod outer segments of frogs (Rana pipiens),” Exp. Eye Res. 40(5), 721–729 (1985).
[Crossref] [PubMed]

1975 (1)

J. H. Marburger, “Self-focusing: Theory,” Prog. Quantum Electron. 4, 35–110 (1975).
[Crossref]

1969 (1)

P. A. Liebman, “Microspectrophotometry of retinal cells,” Ann. N. Y. Acad. Sci. 157(1 Data Extracti), 250–264 (1969).
[Crossref]

1965 (1)

L. V. Keldysh, “Ionization in the field of a strong electromagnetic wave,” Sov. Phys. JETP 20, 1307–1314 (1965).

1962 (1)

E. A. Boettner and J. R. Wolter, “Transmission of the ocular media,” Invest. Ophthalmol. Vis. Sci. 1, 776–783 (1962).

1956 (1)

W. A. H. Rushton, “The difference spectrum and the photosensitivity of rhodopsin in the living human eye,” J. Physiol. 134(1), 11–29 (1956).
[Crossref] [PubMed]

1931 (1)

M. Göppert-Mayer, “Ueber Elementrarakte mit zwei Quantenspruengen,” Ann. Phys. 114, 273 (1931).

1929 (1)

M. Göppert, “Über die Wahrscheinlichkeit des Zusammenwirkens zweier Lichtquanten in einem Elementarakt,” Naturwissenschaften 17, 932 (1929).
[Crossref]

Ala-Laurila, P.

P. Ala-Laurila, A. V. Kolesnikov, R. K. Crouch, E. Tsina, S. A. Shukolyukov, V. I. Govardovskii, Y. Koutalos, B. Wiggert, M. E. Estevez, and M. C. Cornwall, “Visual cycle: Dependence of retinol production and removal on photoproduct decay and cell morphology,” J. Gen. Physiol. 128(2), 153–169 (2006).
[Crossref] [PubMed]

E. Tsina, C. Chen, Y. Koutalos, P. Ala-Laurila, M. Tsacopoulos, B. Wiggert, R. K. Crouch, and M. C. Cornwall, “Physiological and microfluorometric studies of reduction and clearance of retinal in bleached rod photoreceptors,” J. Gen. Physiol. 124(4), 429–443 (2004).
[Crossref] [PubMed]

Arend, O.

F. C. Delori, C. K. Dorey, G. Staurenghi, O. Arend, D. G. Goger, and J. J. Weiter, “In vivo fluorescence of the ocular fundus exhibits retinal pigment epithelium lipofuscin characteristics,” Invest. Ophthalmol. Vis. Sci. 36(3), 718–729 (1995).
[PubMed]

Aung, T.

R. N. Weinreb, T. Aung, and F. A. Medeiros, “The Pathophysiology and Treatment of Glaucoma: a Review,” JAMA 311(18), 1901–1911 (2014).
[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]

Bartz-Schmidt, K. U.

P. Kayatz, G. Thumann, T. T. Luther, J. F. Jordan, K. U. Bartz-Schmidt, P. J. Esser, and U. Schraermeyer, “Oxidation causes melanin fluorescence,” Invest. Ophthalmol. Vis. Sci. 42(1), 241–246 (2001).
[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]

Baylor, D. A.

D. A. Baylor, B. J. Nunn, and J. L. Schnapf, “Spectral sensitivity of cones of the monkey Macaca fascicularis,” J. Physiol. 390(1), 145–160 (1987).
[Crossref] [PubMed]

Berson, E. L.

E. L. Berson, “Retinitis pigmentosa: The Friedenwald lecture,” Invest. Ophthalmol. Vis. Sci. 34(5), 1659–1676 (1993).
[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]

Bird, A. C.

A. C. Bird, “Retinal photoreceptor dystrophies LI. Edward Jackson Memorial Lecture,” Am. J. Ophthalmol. 119(5), 543–562 (1995).
[Crossref] [PubMed]

Boettner, E. A.

E. A. Boettner and J. R. Wolter, “Transmission of the ocular media,” Invest. Ophthalmol. Vis. Sci. 1, 776–783 (1962).

Boppart, S. A.

P. K. Kennedy, S. A. Boppart, D. X. Hammer, B. A. Rockwell, G. D. Noojin, and W. P. Roach, “A First-Order Model for Computation of Laser-Induced Breakdown Thresholds in Ocular and Aqueous Media: II - Comparison to Experiment,” IEEE J. Quantum Electron. 31(12), 2250–2257 (1995).
[Crossref]

Boulton, M.

M. Boulton, M. Rózanowska, and B. Rózanowski, “Retinal photodamage,” J. Photochem. Photobiol. Bol. Biol. 64, 144–161 (2001).

Bradley, A.

Brakenhoff, G. J.

G. J. Brakenhoff, M. Müller, and R. I. Ghauharali, “Analysis of efficiency of two-photon versus single-photon absorption of fluorescence generation in biological objects,” J. Microsc. 183(2), 140–144 (1996).
[Crossref] [PubMed]

Bubel, T.

J. Zhang, R. Sabarinathan, T. Bubel, D. R. Williams, and J. J. Hunter, “Action spectrum for photochemical retinal pigment epithelium (RPE) disruption in an in vivo monkey model,” Proc. SPIE 9706, 1–6 (2016).

Buffington, G. D.

C. P. Cain, R. J. Thomas, G. D. Noojin, D. J. Stolarski, P. K. Kennedy, G. D. Buffington, and B. A. Rockwell, “Sub-50-fs laser retinal damage thresholds in primate eyes with group velocity dispersion, self-focusing and low-density plasmas,” Graefes Arch. Clin. Exp. Ophthalmol. 243(2), 101–112 (2005).
[Crossref] [PubMed]

Cain, C. P.

C. P. Cain, R. J. Thomas, G. D. Noojin, D. J. Stolarski, P. K. Kennedy, G. D. Buffington, and B. A. Rockwell, “Sub-50-fs laser retinal damage thresholds in primate eyes with group velocity dispersion, self-focusing and low-density plasmas,” Graefes Arch. Clin. Exp. Ophthalmol. 243(2), 101–112 (2005).
[Crossref] [PubMed]

B. A. Rockwell, W. P. Roach, M. E. Rogers, M. W. Mayo, C. A. Toth, C. P. Cain, and G. D. Noojin, “Nonlinear refraction in vitreous humor,” Opt. Lett. 18(21), 1792–1794 (1993).
[Crossref] [PubMed]

Carr, R. E.

V. C. Greenstein, K. Holopigian, W. Seiple, R. E. Carr, and D. C. Hood, “Atypical multifocal ERG responses in patients with diseases affecting the photoreceptors,” Vision Res. 44(25), 2867–2874 (2004).
[Crossref] [PubMed]

Carroll, J.

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, C.

C. Chen, E. Tsina, M. C. Cornwall, R. K. Crouch, S. Vijayaraghavan, and Y. Koutalos, “Reduction of all-trans retinal to all-trans retinol in the outer segments of frog and mouse rod photoreceptors,” Biophys. J. 88(3), 2278–2287 (2005).
[Crossref] [PubMed]

E. Tsina, C. Chen, Y. Koutalos, P. Ala-Laurila, M. Tsacopoulos, B. Wiggert, R. K. Crouch, and M. C. Cornwall, “Physiological and microfluorometric studies of reduction and clearance of retinal in bleached rod photoreceptors,” J. Gen. Physiol. 124(4), 429–443 (2004).
[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]

Chirico, G.

A. Diaspro, G. Chirico, and M. Collini, “Two-photon fluorescence excitation and related techniques in biological microscopy,” Q. Rev. Biophys. 38(2), 97–166 (2005).
[Crossref] [PubMed]

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]

Chung, M.

E. A. Rossi, M. Chung, A. Dubra, J. J. Hunter, W. H. Merigan, and D. R. Williams, “Imaging retinal mosaics in the living eye,” Eye (Lond.) 25(3), 301–308 (2011).
[Crossref] [PubMed]

Coello, Y.

Collini, M.

A. Diaspro, G. Chirico, and M. Collini, “Two-photon fluorescence excitation and related techniques in biological microscopy,” Q. Rev. Biophys. 38(2), 97–166 (2005).
[Crossref] [PubMed]

Cooper, R. F.

Cornwall, M. C.

P. Ala-Laurila, A. V. Kolesnikov, R. K. Crouch, E. Tsina, S. A. Shukolyukov, V. I. Govardovskii, Y. Koutalos, B. Wiggert, M. E. Estevez, and M. C. Cornwall, “Visual cycle: Dependence of retinol production and removal on photoproduct decay and cell morphology,” J. Gen. Physiol. 128(2), 153–169 (2006).
[Crossref] [PubMed]

C. Chen, E. Tsina, M. C. Cornwall, R. K. Crouch, S. Vijayaraghavan, and Y. Koutalos, “Reduction of all-trans retinal to all-trans retinol in the outer segments of frog and mouse rod photoreceptors,” Biophys. J. 88(3), 2278–2287 (2005).
[Crossref] [PubMed]

E. Tsina, C. Chen, Y. Koutalos, P. Ala-Laurila, M. Tsacopoulos, B. Wiggert, R. K. Crouch, and M. C. Cornwall, “Physiological and microfluorometric studies of reduction and clearance of retinal in bleached rod photoreceptors,” J. Gen. Physiol. 124(4), 429–443 (2004).
[Crossref] [PubMed]

Crouch, R. K.

P. Ala-Laurila, A. V. Kolesnikov, R. K. Crouch, E. Tsina, S. A. Shukolyukov, V. I. Govardovskii, Y. Koutalos, B. Wiggert, M. E. Estevez, and M. C. Cornwall, “Visual cycle: Dependence of retinol production and removal on photoproduct decay and cell morphology,” J. Gen. Physiol. 128(2), 153–169 (2006).
[Crossref] [PubMed]

C. Chen, E. Tsina, M. C. Cornwall, R. K. Crouch, S. Vijayaraghavan, and Y. Koutalos, “Reduction of all-trans retinal to all-trans retinol in the outer segments of frog and mouse rod photoreceptors,” Biophys. J. 88(3), 2278–2287 (2005).
[Crossref] [PubMed]

E. Tsina, C. Chen, Y. Koutalos, P. Ala-Laurila, M. Tsacopoulos, B. Wiggert, R. K. Crouch, and M. C. Cornwall, “Physiological and microfluorometric studies of reduction and clearance of retinal in bleached rod photoreceptors,” J. Gen. Physiol. 124(4), 429–443 (2004).
[Crossref] [PubMed]

Dantus, M.

Delori, F. C.

J. I. W. Morgan, J. J. Hunter, B. Masella, R. Wolfe, D. C. Gray, W. H. Merigan, F. C. Delori, and D. R. Williams, “Light-induced retinal changes observed with high-resolution autofluorescence imaging of the retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 49(8), 3715–3729 (2008).
[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]

C. N. Keilhauer and F. C. Delori, “Near-infrared autofluorescence imaging of the fundus: visualization of ocular melanin,” Invest. Ophthalmol. Vis. Sci. 47(8), 3556–3564 (2006).
[Crossref] [PubMed]

F. C. Delori, C. K. Dorey, G. Staurenghi, O. Arend, D. G. Goger, and J. J. Weiter, “In vivo fluorescence of the ocular fundus exhibits retinal pigment epithelium lipofuscin characteristics,” Invest. Ophthalmol. Vis. Sci. 36(3), 718–729 (1995).
[PubMed]

Denk, W.

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Diaspro, A.

A. Diaspro, G. Chirico, and M. Collini, “Two-photon fluorescence excitation and related techniques in biological microscopy,” Q. Rev. Biophys. 38(2), 97–166 (2005).
[Crossref] [PubMed]

Dorey, C. K.

F. C. Delori, C. K. Dorey, G. Staurenghi, O. Arend, D. G. Goger, and J. J. Weiter, “In vivo fluorescence of the ocular fundus exhibits retinal pigment epithelium lipofuscin characteristics,” Invest. Ophthalmol. Vis. Sci. 36(3), 718–729 (1995).
[PubMed]

Dubis, A. M.

Dubra, A.

A. Dubra, Y. Sulai, J. L. Norris, R. F. Cooper, A. M. Dubis, D. R. Williams, and J. Carroll, “Noninvasive imaging of the human rod photoreceptor mosaic using a confocal adaptive optics scanning ophthalmoscope,” Biomed. Opt. Express 2(7), 1864–1876 (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]

E. A. Rossi, M. Chung, A. Dubra, J. J. Hunter, W. H. Merigan, and D. R. Williams, “Imaging retinal mosaics in the living eye,” Eye (Lond.) 25(3), 301–308 (2011).
[Crossref] [PubMed]

A. Dubra and Z. Harvey, “Registration of 2D images from fast scanning ophthalmic instruments,” Lect. Notes Comput. Sci. 6204, 60–71 (2010).
[Crossref]

J. I. W. Morgan, A. Dubra, R. Wolfe, W. H. Merigan, and D. R. Williams, “In vivo autofluorescence imaging of the human and macaque retinal pigment epithelial cell mosaic,” Invest. Ophthalmol. Vis. Sci. 50(3), 1350–1359 (2009).
[Crossref] [PubMed]

Duncan, J. L.

A. Roorda and J. L. Duncan, “Adaptive optics ophthalmoscopy,” Annu Rev Vis Sci 1(1), 19–50 (2015).
[Crossref] [PubMed]

Esser, P. J.

P. Kayatz, G. Thumann, T. T. Luther, J. F. Jordan, K. U. Bartz-Schmidt, P. J. Esser, and U. Schraermeyer, “Oxidation causes melanin fluorescence,” Invest. Ophthalmol. Vis. Sci. 42(1), 241–246 (2001).
[PubMed]

Estep, J. S.

G. M. Pocock, J. W. Oliver, C. S. Specht, J. S. Estep, G. D. Noojin, K. Schuster, and B. A. Rockwell, “High-resolution in vivo imaging of regimes of laser damage to the primate retina,” J. Ophthalmol. 2014, 516854 (2014).
[Crossref] [PubMed]

Estevez, M. E.

P. Ala-Laurila, A. V. Kolesnikov, R. K. Crouch, E. Tsina, S. A. Shukolyukov, V. I. Govardovskii, Y. Koutalos, B. Wiggert, M. E. Estevez, and M. C. Cornwall, “Visual cycle: Dependence of retinol production and removal on photoproduct decay and cell morphology,” J. Gen. Physiol. 128(2), 153–169 (2006).
[Crossref] [PubMed]

Fischer, W. S.

B. D. Masella, D. R. Williams, W. S. Fischer, E. A. Rossi, and J. J. Hunter, “Long-term reduction in infrared autofluorescence caused by infrared light below the maximum permissible exposure,” Invest. Ophthalmol. Vis. Sci. 55(6), 3929–3938 (2014).
[Crossref] [PubMed]

Gal, A.

D. A. Thompson and A. Gal, “Vitamin A metabolism in the retinal pigment epithelium: genes, mutations, and diseases,” Prog. Retin. Eye Res. 22(5), 683–703 (2003).
[Crossref] [PubMed]

Ghauharali, R. I.

G. J. Brakenhoff, M. Müller, and R. I. Ghauharali, “Analysis of efficiency of two-photon versus single-photon absorption of fluorescence generation in biological objects,” J. Microsc. 183(2), 140–144 (1996).
[Crossref] [PubMed]

Glickman, R. D.

R. D. Glickman, “Ultraviolet phototoxicity to the retina,” Eye Contact Lens 37(4), 196–205 (2011).
[Crossref] [PubMed]

Goger, D. G.

F. C. Delori, C. K. Dorey, G. Staurenghi, O. Arend, D. G. Goger, and J. J. Weiter, “In vivo fluorescence of the ocular fundus exhibits retinal pigment epithelium lipofuscin characteristics,” Invest. Ophthalmol. Vis. Sci. 36(3), 718–729 (1995).
[PubMed]

Golczak, M.

P. D. Kiser, M. Golczak, and K. Palczewski, “Chemistry of the retinoid (visual) cycle,” Chem. Rev. 114(1), 194–232 (2014).
[Crossref] [PubMed]

P. D. Kiser, M. Golczak, A. Maeda, and K. Palczewski, “Key enzymes of the retinoid (visual) cycle in vertebrate retina,” Biochim. Biophys. Acta – Mol. Cell Biol. Lipids 1821(1), 137–151 (2012).
[Crossref]

G. H. Travis, M. Golczak, A. R. Moise, and K. Palczewski, “Diseases caused by defects in the visual cycle: retinoids as potential therapeutic agents,” Annu. Rev. Pharmacol. Toxicol. 47(1), 469–512 (2007).
[Crossref] [PubMed]

Göppert, M.

M. Göppert, “Über die Wahrscheinlichkeit des Zusammenwirkens zweier Lichtquanten in einem Elementarakt,” Naturwissenschaften 17, 932 (1929).
[Crossref]

Göppert-Mayer, M.

M. Göppert-Mayer, “Ueber Elementrarakte mit zwei Quantenspruengen,” Ann. Phys. 114, 273 (1931).

Govardovskii, V. I.

P. Ala-Laurila, A. V. Kolesnikov, R. K. Crouch, E. Tsina, S. A. Shukolyukov, V. I. Govardovskii, Y. Koutalos, B. Wiggert, M. E. Estevez, and M. C. Cornwall, “Visual cycle: Dependence of retinol production and removal on photoproduct decay and cell morphology,” J. Gen. Physiol. 128(2), 153–169 (2006).
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A. Vogel, J. Noack, G. Huettmann, and G. Paltauf, “Low-density plasmas below the optical breakdown threshold: potential hazard for multiphoton microscopy, and a tool for the manipulation of intracellular events,” SPIE Photonics West 4620, 202–216 (2002).

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Q. Yang, J. Zhang, K. Nozato, K. Saito, D. R. Williams, A. Roorda, and E. A. Rossi, “Closed-loop optical stabilization and digital image registration in adaptive optics scanning light ophthalmoscopy,” Biomed. Opt. Express 5(9), 3174–3191 (2014).
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B. D. Masella, D. R. Williams, W. S. Fischer, E. A. Rossi, and J. J. Hunter, “Long-term reduction in infrared autofluorescence caused by infrared light below the maximum permissible exposure,” Invest. Ophthalmol. Vis. Sci. 55(6), 3929–3938 (2014).
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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).
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G. M. Pocock, J. W. Oliver, C. S. Specht, J. S. Estep, G. D. Noojin, K. Schuster, and B. A. Rockwell, “High-resolution in vivo imaging of regimes of laser damage to the primate retina,” J. Ophthalmol. 2014, 516854 (2014).
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R. Sharma, C. Schwarz, D. R. Williams, G. Palczewska, K. Palczewski, and J. J. Hunter, “In Vivo Two-Photon Fluorescence Kinetics of Primate Rods and Cones,” Invest. Ophthalmol. Vis. Sci. 57(2), 647–657 (2016).
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R. Sharma, C. Schwarz, D. R. Williams, G. Palczewska, K. Palczewski, and J. J. Hunter, “In Vivo Two-Photon Fluorescence Kinetics of Primate Rods and Cones,” Invest. Ophthalmol. Vis. Sci. 57(2), 647–657 (2016).
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R. Sharma, D. R. Williams, G. Palczewska, K. Palczewski, and J. J. Hunter, “Two-Photon Autofluorescence Imaging Reveals Cellular Structures Throughout the Retina of the Living Primate Eye,” Invest. Ophthalmol. Vis. Sci. 57(2), 632–646 (2016).
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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).
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P. Ala-Laurila, A. V. Kolesnikov, R. K. Crouch, E. Tsina, S. A. Shukolyukov, V. I. Govardovskii, Y. Koutalos, B. Wiggert, M. E. Estevez, and M. C. Cornwall, “Visual cycle: Dependence of retinol production and removal on photoproduct decay and cell morphology,” J. Gen. Physiol. 128(2), 153–169 (2006).
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G. M. Pocock, J. W. Oliver, C. S. Specht, J. S. Estep, G. D. Noojin, K. Schuster, and B. A. Rockwell, “High-resolution in vivo imaging of regimes of laser damage to the primate retina,” J. Ophthalmol. 2014, 516854 (2014).
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Thomas, R. J.

B. A. Rockwell, R. J. Thomas, and A. Vogel, “Ultrashort laser pulse retinal damage mechanisms and their impact on thresholds,” Med. Laser Appl. 25(2), 84–92 (2010).
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C. P. Cain, R. J. Thomas, G. D. Noojin, D. J. Stolarski, P. K. Kennedy, G. D. Buffington, and B. A. Rockwell, “Sub-50-fs laser retinal damage thresholds in primate eyes with group velocity dispersion, self-focusing and low-density plasmas,” Graefes Arch. Clin. Exp. Ophthalmol. 243(2), 101–112 (2005).
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E. Tsina, C. Chen, Y. Koutalos, P. Ala-Laurila, M. Tsacopoulos, B. Wiggert, R. K. Crouch, and M. C. Cornwall, “Physiological and microfluorometric studies of reduction and clearance of retinal in bleached rod photoreceptors,” J. Gen. Physiol. 124(4), 429–443 (2004).
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B. A. Rockwell, R. J. Thomas, and A. Vogel, “Ultrashort laser pulse retinal damage mechanisms and their impact on thresholds,” Med. Laser Appl. 25(2), 84–92 (2010).
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A. Vogel, G. Huttmann, G. Paltauf, and J. Noack, “Femtosecond-laser-produced low-density plasmas in transparent biological media: A tool for the creation of chemical, thermal and thermomechanical effects below the optical breakdown threshold,” SPIE Photonics West 4633, 23–37 (2002).

A. Vogel, J. Noack, G. Huettmann, and G. Paltauf, “Low-density plasmas below the optical breakdown threshold: potential hazard for multiphoton microscopy, and a tool for the manipulation of intracellular events,” SPIE Photonics West 4620, 202–216 (2002).

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Webb, W. W.

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[PubMed]

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C. Keller, C. Grimm, A. Wenzel, F. Hafezi, and C. Remé, “Protective effect of halothane anesthesia on retinal light damage: inhibition of metabolic rhodopsin regeneration,” Invest. Ophthalmol. Vis. Sci. 42(2), 476–480 (2001).
[PubMed]

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P. Ala-Laurila, A. V. Kolesnikov, R. K. Crouch, E. Tsina, S. A. Shukolyukov, V. I. Govardovskii, Y. Koutalos, B. Wiggert, M. E. Estevez, and M. C. Cornwall, “Visual cycle: Dependence of retinol production and removal on photoproduct decay and cell morphology,” J. Gen. Physiol. 128(2), 153–169 (2006).
[Crossref] [PubMed]

E. Tsina, C. Chen, Y. Koutalos, P. Ala-Laurila, M. Tsacopoulos, B. Wiggert, R. K. Crouch, and M. C. Cornwall, “Physiological and microfluorometric studies of reduction and clearance of retinal in bleached rod photoreceptors,” J. Gen. Physiol. 124(4), 429–443 (2004).
[Crossref] [PubMed]

Williams, D. R.

R. Sharma, D. R. Williams, G. Palczewska, K. Palczewski, and J. J. Hunter, “Two-Photon Autofluorescence Imaging Reveals Cellular Structures Throughout the Retina of the Living Primate Eye,” Invest. Ophthalmol. Vis. Sci. 57(2), 632–646 (2016).
[Crossref] [PubMed]

R. Sharma, C. Schwarz, D. R. Williams, G. Palczewska, K. Palczewski, and J. J. Hunter, “In Vivo Two-Photon Fluorescence Kinetics of Primate Rods and Cones,” Invest. Ophthalmol. Vis. Sci. 57(2), 647–657 (2016).
[Crossref] [PubMed]

J. Zhang, R. Sabarinathan, T. Bubel, D. R. Williams, and J. J. Hunter, “Action spectrum for photochemical retinal pigment epithelium (RPE) disruption in an in vivo monkey model,” Proc. SPIE 9706, 1–6 (2016).

B. D. Masella, D. R. Williams, W. S. Fischer, E. A. Rossi, and J. J. Hunter, “Long-term reduction in infrared autofluorescence caused by infrared light below the maximum permissible exposure,” Invest. Ophthalmol. Vis. Sci. 55(6), 3929–3938 (2014).
[Crossref] [PubMed]

Q. Yang, J. Zhang, K. Nozato, K. Saito, D. R. Williams, A. Roorda, and E. A. Rossi, “Closed-loop optical stabilization and digital image registration in adaptive optics scanning light ophthalmoscopy,” Biomed. Opt. Express 5(9), 3174–3191 (2014).
[Crossref] [PubMed]

B. D. Masella, J. J. Hunter, and D. R. Williams, “New wrinkles in retinal densitometry,” Invest. Ophthalmol. Vis. Sci. 55(11), 7525–7534 (2014).
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B. D. Masella, J. J. Hunter, and D. R. Williams, “Rod photopigment kinetics after photodisruption of the retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 55(11), 7535–7544 (2014).
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J. J. Hunter, J. I. W. Morgan, W. H. Merigan, D. H. Sliney, J. R. Sparrow, and D. R. Williams, “The susceptibility of the retina to photochemical damage from visible light,” Prog. Retin. Eye Res. 31(1), 28–42 (2012).
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Figures (10)

Fig. 1
Fig. 1 Representative fundus images of animal 1 in blue reflectance (a, b), blue autofluorescence (c, d), infrared reflectance (e, f), and infrared autofluorescence (g, h) modes taken with the Spectralis before and after single exposures. Four locations received 20.4 J/cm2 exposures with the 730-nm pulsed laser (blue boxes); four locations received 81.7 J/cm2 (orange boxes). IRAF was reduced at the exposure sites. Scale bar: 400 µm.
Fig. 2
Fig. 2 Change in reflectance and autofluorescence intensity measured with the Heidelberg Spectralis following a 730-nm pulsed laser exposure. The only significant change caused by the 20.4 J/cm2 and 81.7 J/cm2 exposures is a significant decrease in IRAF compared to baseline (p<0.001). In week 22 (after a recovery period of 19 weeks), IRAF had partially recovered. Data are averaged across subjects and locations. Error bars represent standard errors and the dashed lines indicate the standard error from 8 control measurements.
Fig. 3
Fig. 3 IRAF fundus images of animal 1 after the 3rd exposure in week 3 (a) and in week 22 after a recovery period of 19 weeks (b). IRAF partially recovered. Refer to Fig. 1 for exposure sites. Scale bar: 400 µm.
Fig. 4
Fig. 4 Color fundus photograph (a) and fluorescein angiogram (b) of animal 1 after the third exposure in week 3. No changes were detected at the exposed locations. Refer to Fig. 1 for exposure sites. Scale bar: 400 µm.
Fig. 5
Fig. 5 Representative OCT B-scans of the same retinal location before the first exposure in week 0 (a) and after the third exposure in week 3 (b). Arrows mark the center of the 81.7 J/cm2 exposure measuring 340 µm along the shown axis. Scale bar: 100 µm.
Fig. 6
Fig. 6 Exposures with ~55 fs pulses and broadened pulses caused a similar decrease in infrared autofluorescence, implying that the decrease is unlikely to be due to a nonlinear effect.
Fig. 7
Fig. 7 Infrared reflectance images of the photoreceptor layer at two different locations (a-c and d-f) after the first exposure (a, d) and several weeks after three cumulative exposures to 81.7 J/cm2 (b, e), and images of autofluorescence from RPE cells underlying exposed locations. Scale bar: 50 µm.
Fig. 8
Fig. 8 TPEF time course with onset of the pulsed 730-nm laser following 15 min of dark adaptation at a sample location. For both exposures, 20.4 J/cm2 (a) and 81.7 J/cm2 (b), TPEF increases to a plateau. Data are well described by an exponential rise to plateau (R2>0.91). Error bars represent standard errors.
Fig. 9
Fig. 9 Time constant (a) and relative TPEF increase ΔF/F (b) versus imaging week extracted from exponential fits to the TPEF time course for low (blue) and high (orange) exposures. Stars and triangles represent different animals.
Fig. 10
Fig. 10 The red curve shows the maximum average power of the pulsed laser that is permitted versus exposure time when keeping the same parameters for imaging as used in the described experiment. The blue (20.4 J/cm2) and orange (81.7 J/cm2) squares mark the exposures that were tested in this study.

Tables (3)

Tables Icon

Table 1 Clinical and laboratory instruments employed to assess retinal status

Tables Icon

Table 2 Imaging and exposure time points of the safety study

Tables Icon

Table 3 Maximum permissible average power at the pupil and other relevant parameters

Equations (17)

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

P peak =0.94 P avg f rep τ 214 W
P cr,SF = 0.148λ 2 n n 2 1.34 MW
I cr = ( ρ cr A0.5τ ) 1/K B
A=( 2 9π )ω ( m'ω ) 3/2 e 2K Φ(z) ( 1 16 ) K
B= q 2 m'Δ ω 2 c ε 0 n 0
I cr,LDP 5.47 10 4 W μ m 2
I cr,LIB 1.73 10 5 W μ m 2
P cr,LDP 136 kW
P cr,LIB 431 kW
MP W CW,th =1.8 10 3 C A C E * A P,7 t 0.25
MP E P,th =1.8 10 3 C P C A C E * A P,7 t min 0.25
1 C M C τ ( 2.5 10 4 W 6.33 10 4 W + 5 10 5 W 7.75 10 3 W + 5 10 5 W 7.33 10 3 W + 5 10 4 W 4.42 10 3 W )0.39
1 C M C τ ( 2.5 10 4 W 6.33 10 4 W + 5 10 5 W 7.75 10 3 W + 5 10 5 W 6.16 10 3 W + 1 10 3 W 3.71 10 3 W )0.75
E 730 = C M C τ ( 1 2.5 10 4 6.33 10 3 + 5 10 5 7.75 10 3 5 10 5 t 1/4 1.84 10 2 ) 1.11 10 2 t 1/4
MP E av,1 =δ 10 7 A P,7 τ
MP E av,2 =1.8 10 3 C A A P,7 t 1/4
t max = ( 1.8 10 3 C A A P,7 P ) 4

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