Abstract

Progress is needed in developing animal models of photoreceptor degeneration and evaluating such models with longitudinal, noninvasive techniques. We employ confocal scanning laser ophthalmoscopy, optical coherence tomography (OCT) and high-resolution retinal imaging to noninvasively observe the retina of non-human primates with induced photoreceptor degeneration. Photoreceptors were imaged at the single-cell scale in three modalities of adaptive optics scanning light ophthalmoscopy: traditional confocal reflectance, indicative of waveguiding; a non-confocal offset aperture technique visualizing scattered light; and two-photon excited fluorescence, the time-varying signal of which, at 730 nm excitation, is representative of visual cycle function. Assessment of photoreceptor structure and function using these imaging modalities revealed a reduction in retinoid production in cone photoreceptor outer segments while inner segments appeared to remain present. Histology of one retina confirmed loss of outer segments and the presence of intact inner segments. This unique combination of imaging modalities can provide essential, clinically-relevant information on both the structural integrity and function of photoreceptors to not only validate models of photoreceptor degeneration but potentially evaluate the efficacy of future cell and gene-based therapies for vision restoration.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2018 (1)

E. J. Patterson, A. Kalitzeos, M. Kasilian, J. C. Gardner, J. Neitz, A. J. Hardcastle, M. Neitz, J. Carroll, and M. Michaelides, “Residual cone structure in patients with X-linked cone opsin mutations,” Invest. Ophthalmol. Vis. Sci. 59(10), 4238–4248 (2018).
[Crossref] [PubMed]

2017 (2)

R. Sharma, C. Schwarz, J. J. Hunter, G. Palczewska, K. Palczewski, and D. R. Williams, “Formation and clearance of all-trans-retinol in rods investigated in the living primate eye with two-photon ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci. 58(1), 604–613 (2017).
[Crossref] [PubMed]

E. A. Rossi, C. E. Granger, R. Sharma, Q. Yang, K. Saito, C. Schwarz, S. Walters, K. Nozato, J. Zhang, T. Kawakami, W. Fischer, L. R. Latchney, J. J. Hunter, M. M. Chung, and D. R. Williams, “Imaging individual neurons in the retinal ganglion cell layer of the living eye,” Proc. Natl. Acad. Sci. U.S.A. 114(3), 586–591 (2017).
[Crossref] [PubMed]

2016 (8)

M. Karali, M. Persico, M. Mutarelli, A. Carissimo, M. Pizzo, V. Singh Marwah, C. Ambrosio, M. Pinelli, D. Carrella, S. Ferrari, D. Ponzin, V. Nigro, D. di Bernardo, and S. Banfi, “High-resolution analysis of the human retina miRNome reveals isomiR variations and novel microRNAs,” Nucleic Acids Res. 44(4), 1525–1540 (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]

D. Hillmann, H. Spahr, C. Pfäffle, H. Sudkamp, G. Franke, and G. Hüttmann, “In vivo optical imaging of physiological responses to photostimulation in human photoreceptors,” Proc. Natl. Acad. Sci. U.S.A. 113(46), 13138–13143 (2016).
[Crossref] [PubMed]

L. W. Sun, R. D. Johnson, C. S. Langlo, R. F. Cooper, M. M. Razeen, M. C. Russillo, A. Dubra, T. B. Connor, D. P. Han, M. E. Pennesi, C. N. Kay, D. V. Weinberg, K. E. Stepien, and J. Carroll, “Assessing photoreceptor structure in retinitis pigmentosa and Usher syndrome,” Invest. Ophthalmol. Vis. Sci. 57(6), 2428–2442 (2016).
[Crossref] [PubMed]

C. S. Langlo, E. J. Patterson, B. P. Higgins, P. Summerfelt, M. M. Razeen, L. R. Erker, M. Parker, F. T. Collison, G. A. Fishman, C. N. Kay, J. Zhang, R. G. Weleber, P. Yang, D. J. Wilson, M. E. Pennesi, B. L. Lam, J. Chiang, J. D. Chulay, A. Dubra, W. W. Hauswirth, and J. Carroll, “Residual foveal cone structure in CNGB3-associated achromatopsia,” Invest. Ophthalmol. Vis. Sci. 57(10), 3984–3995 (2016).
[Crossref] [PubMed]

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]

D. Scoles, J. A. Flatter, R. F. Cooper, C. S. Langlo, S. Robison, M. Neitz, D. V. Weinberg, M. E. Pennesi, D. P. Han, A. Dubra, and J. Carroll, “Assessing photoreceptor structure associated with ellipsoid zone disruptions visualized with optical coherence tomography,” Retina 36(1), 91–103 (2016).
[Crossref] [PubMed]

C. Schwarz, R. Sharma, W. S. Fischer, M. Chung, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “Safety assessment in macaques of light exposures for functional two-photon ophthalmoscopy in humans,” Biomed. Opt. Express 7(12), 5148–5169 (2016).
[Crossref] [PubMed]

2015 (7)

Q. Yang, L. Yin, K. Nozato, J. Zhang, K. Saito, W. H. Merigan, D. R. Williams, and E. A. Rossi, “Calibration-free sinusoidal rectification and uniform retinal irradiance in scanning light ophthalmoscopy,” Opt. Lett. 40(1), 85–88 (2015).
[Crossref] [PubMed]

A. Guevara-Torres, D. R. Williams, and J. B. Schallek, “Imaging translucent cell bodies in the living mouse retina without contrast agents,” Biomed. Opt. Express 6(6), 2106–2119 (2015).
[Crossref] [PubMed]

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

J. Jacob, M. Paques, V. Krivosic, B. Dupas, A. Couturier, C. Kulcsar, R. Tadayoni, P. Massin, and A. Gaudric, “Meaning of visualizing retinal cone mosaic on adaptive optics images,” Am. J. Ophthalmol. 159(1), 118–123 (2015).
[Crossref] [PubMed]

J. C. Horton, A. B. Parker, J. V. Botelho, and J. L. Duncan, “Spontaneous regeneration of human photoreceptor outer segments,” Sci. Rep. 5, 12364 (2015).

K. S. Bruce, W. M. Harmening, B. R. Langston, W. S. Tuten, A. Roorda, and L. C. Sincich, “Normal perceptual sensitivity arising from weakly reflective cone photoreceptors,” Invest. Ophthalmol. Vis. Sci. 56(8), 4431–4438 (2015).
[Crossref] [PubMed]

Q. Wang, W. S. Tuten, B. J. Lujan, J. Holland, P. S. Bernstein, S. D. Schwartz, J. L. Duncan, and A. Roorda, “Adaptive optics microperimetry and OCT images show preserved function and recovery of cone visibility in macular telangiectasia type 2 retinal lesions,” Invest. Ophthalmol. Vis. Sci. 56(2), 778–786 (2015).
[Crossref] [PubMed]

2014 (9)

D. Scoles, Y. N. Sulai, C. S. Langlo, G. A. Fishman, C. A. Curcio, J. Carroll, and A. Dubra, “In Vivo Imaging of Human Cone Photoreceptor Inner Segments,” Invest. Ophthalmol. Vis. Sci. 55(7), 4244–4251 (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]

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]

W. M. Harmening, W. S. Tuten, A. Roorda, and L. C. Sincich, “Mapping the perceptual grain of the human retina,” J. Neurosci. 34(16), 5667–5677 (2014).
[Crossref] [PubMed]

V. Busskamp, J. Krol, D. Nelidova, J. Daum, T. Szikra, B. Tsuda, J. Jüttner, K. Farrow, B. G. Scherf, C. P. Alvarez, C. Genoud, V. Sothilingam, N. Tanimoto, M. Stadler, M. Seeliger, M. Stoffel, W. Filipowicz, and B. Roska, “miRNAs 182 and 183 are necessary to maintain adult cone photoreceptor outer segments and visual function,” Neuron 83(3), 586–600 (2014).
[Crossref] [PubMed]

R. S. Jonnal, O. P. Kocaoglu, R. J. Zawadzki, S.-H. Lee, J. S. Werner, and D. T. Miller, “The cellular origins of the outer retinal bands in optical coherence tomography images,” Invest. Ophthalmol. Vis. Sci. 55(12), 7904–7918 (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).
[Crossref] [PubMed]

J. A. Flatter, R. F. Cooper, M. J. Dubow, A. Pinhas, R. S. Singh, R. Kapur, N. Shah, R. D. Walsh, S. H. Hong, D. V. Weinberg, K. E. Stepien, W. J. Wirostko, S. Robison, A. Dubra, R. B. Rosen, T. B. J. Connor, and J. Carroll, “Outer retinal structure after closed-globe blunt ocular trauma,” Retina 34(10), 2133–2146 (2014).
[Crossref] [PubMed]

Y. N. Sulai, D. Scoles, Z. Harvey, and A. Dubra, “Visualization of retinal vascular structure and perfusion with a nonconfocal adaptive optics scanning light ophthalmoscope,” J. Opt. Soc. Am. A 31(3), 569–579 (2014).
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2013 (3)

2012 (3)

T. Y. P. Chui, D. A. Vannasdale, and S. A. Burns, “The use of forward scatter to improve retinal vascular imaging with an adaptive optics scanning laser ophthalmoscope,” Biomed. Opt. Express 3(10), 2537–2549 (2012).
[Crossref] [PubMed]

W. S. Tuten, P. Tiruveedhula, and A. Roorda, “Adaptive optics scanning laser ophthalmoscope-based microperimetry,” Optom. Vis. Sci. 89(5), 563–574 (2012).
[Crossref] [PubMed]

P. Bedggood and A. Metha, “Variability in bleach kinetics and amount of photopigment between individual foveal cones,” Invest. Ophthalmol. Vis. Sci. 53(7), 3673–3681 (2012).
[Crossref] [PubMed]

2011 (2)

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]

L. H. Vandenberghe, P. Bell, A. M. Maguire, C. N. Cearley, R. Xiao, R. Calcedo, L. Wang, M. J. Castle, A. C. Maguire, R. Grant, J. H. Wolfe, J. M. Wilson, and J. Bennett, “Dosage thresholds for AAV2 and AAV8 photoreceptor gene therapy in monkey,” Science Translational Medicine 3, 88ra54 (2011).

2010 (1)

V. Busskamp, J. Duebel, D. Balya, M. Fradot, T. J. Viney, S. Siegert, A. C. Groner, E. Cabuy, V. Forster, M. Seeliger, M. Biel, P. Humphries, M. Paques, S. Mohand-Said, D. Trono, K. Deisseroth, J. A. Sahel, S. Picaud, and B. Roska, “Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa,” Science 329(5990), 413–417 (2010).
[Crossref] [PubMed]

2009 (2)

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]

J. Rha, B. Schroeder, P. Godara, and J. Carroll, “Variable optical activation of human cone photoreceptors visualized using a short coherence light source,” Opt. Lett. 34(24), 3782–3784 (2009).
[Crossref] [PubMed]

2008 (1)

K. Grieve and A. Roorda, “Intrinsic signals from human cone photoreceptors,” Invest. Ophthalmol. Vis. Sci. 49(2), 713–719 (2008).
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2007 (1)

F. M. Penha, M. Maia, M. Eid Farah, A. H. Príncipe, E. H. Freymüller, A. Maia, O. Magalhães, and R. L. Smith, “Effects of subretinal injections of indocyanine green, trypan blue, and glucose in rabbit eyes,” Ophthalmology 114(5), 899–908 (2007).
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2006 (4)

2005 (2)

H. Hofer, J. Carroll, J. Neitz, M. Neitz, and D. R. Williams, “Organization of the human trichromatic cone mosaic,” J. Neurosci. 25(42), 9669–9679 (2005).
[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]

2004 (1)

K. A. Kasischke, H. D. Vishwasrao, P. J. Fisher, W. R. Zipfel, and W. W. Webb, “Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis,” Science 305(5680), 99–103 (2004).
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2003 (2)

A. Pallikaris, D. R. Williams, and H. Hofer, “The reflectance of single cones in the living human eye,” Invest. Ophthalmol. Vis. Sci. 44(10), 4580–4592 (2003).
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D. C. Hood, J. G. Odel, C. S. Chen, and B. J. Winn, “The multifocal electroretinogram,” J. Neuroophthalmol. 23(3), 225–235 (2003).
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2002 (2)

S. Huang, A. A. Heikal, and W. W. Webb, “Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein,” Biophys. J. 82(5), 2811–2825 (2002).
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A. Roorda, F. Romero-Borja, W. Donnelly Iii, H. Queener, T. Hebert, and M. Campbell, “Adaptive optics scanning laser ophthalmoscopy,” Opt. Express 10(9), 405–412 (2002).
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1999 (1)

A. Roorda and D. R. Williams, “The arrangement of the three cone classes in the living human eye,” Nature 397(6719), 520–522 (1999).
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1997 (1)

1995 (1)

M. R. Hee, J. A. Izatt, E. A. Swanson, D. Huang, J. S. Schuman, C. P. Lin, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography of the human retina,” Arch. Ophthalmol. 113(3), 325–332 (1995).
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1993 (1)

1992 (1)

E. E. Sutter and D. Tran, “The field topography of ERG components in man-I. The photopic luminance response,” Vision Res. 32(3), 433–446 (1992).
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1991 (1)

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

1986 (1)

D. H. Anderson, C. J. Guérin, P. A. Erickson, W. H. Stern, and S. K. Fisher, “Morphological recovery in the reattached retina,” Invest. Ophthalmol. Vis. Sci. 27(2), 168–183 (1986).
[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).
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1978 (1)

R. R. Birge, J. A. Bennett, B. M. Pierce, and T. M. Thomas, “Two-photon spectroscopy of the visual chromophores. Evidence for a lowest excited 1Ag–like. pi.pi.* state in all-trans-retinol (vitamin A),” J. Am. Chem. Soc. 100(5), 1533–1539 (1978).
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1973 (1)

P. Lipton, “Effects of membrane depolarization on nicotinamide nucleotide fluorescence in brain slices,” Biochem. J. 136(4), 999–1009 (1973).
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Ahamd, K.

Alvarez, C. P.

V. Busskamp, J. Krol, D. Nelidova, J. Daum, T. Szikra, B. Tsuda, J. Jüttner, K. Farrow, B. G. Scherf, C. P. Alvarez, C. Genoud, V. Sothilingam, N. Tanimoto, M. Stadler, M. Seeliger, M. Stoffel, W. Filipowicz, and B. Roska, “miRNAs 182 and 183 are necessary to maintain adult cone photoreceptor outer segments and visual function,” Neuron 83(3), 586–600 (2014).
[Crossref] [PubMed]

Ambrosio, C.

M. Karali, M. Persico, M. Mutarelli, A. Carissimo, M. Pizzo, V. Singh Marwah, C. Ambrosio, M. Pinelli, D. Carrella, S. Ferrari, D. Ponzin, V. Nigro, D. di Bernardo, and S. Banfi, “High-resolution analysis of the human retina miRNome reveals isomiR variations and novel microRNAs,” Nucleic Acids Res. 44(4), 1525–1540 (2016).
[Crossref] [PubMed]

Anderson, D. H.

D. H. Anderson, C. J. Guérin, P. A. Erickson, W. H. Stern, and S. K. Fisher, “Morphological recovery in the reattached retina,” Invest. Ophthalmol. Vis. Sci. 27(2), 168–183 (1986).
[PubMed]

Balya, D.

V. Busskamp, J. Duebel, D. Balya, M. Fradot, T. J. Viney, S. Siegert, A. C. Groner, E. Cabuy, V. Forster, M. Seeliger, M. Biel, P. Humphries, M. Paques, S. Mohand-Said, D. Trono, K. Deisseroth, J. A. Sahel, S. Picaud, and B. Roska, “Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa,” Science 329(5990), 413–417 (2010).
[Crossref] [PubMed]

Banfi, S.

M. Karali, M. Persico, M. Mutarelli, A. Carissimo, M. Pizzo, V. Singh Marwah, C. Ambrosio, M. Pinelli, D. Carrella, S. Ferrari, D. Ponzin, V. Nigro, D. di Bernardo, and S. Banfi, “High-resolution analysis of the human retina miRNome reveals isomiR variations and novel microRNAs,” Nucleic Acids Res. 44(4), 1525–1540 (2016).
[Crossref] [PubMed]

Bedggood, P.

P. Bedggood and A. Metha, “Variability in bleach kinetics and amount of photopigment between individual foveal cones,” Invest. Ophthalmol. Vis. Sci. 53(7), 3673–3681 (2012).
[Crossref] [PubMed]

Bell, P.

L. H. Vandenberghe, P. Bell, A. M. Maguire, C. N. Cearley, R. Xiao, R. Calcedo, L. Wang, M. J. Castle, A. C. Maguire, R. Grant, J. H. Wolfe, J. M. Wilson, and J. Bennett, “Dosage thresholds for AAV2 and AAV8 photoreceptor gene therapy in monkey,” Science Translational Medicine 3, 88ra54 (2011).

Bennett, J.

L. H. Vandenberghe, P. Bell, A. M. Maguire, C. N. Cearley, R. Xiao, R. Calcedo, L. Wang, M. J. Castle, A. C. Maguire, R. Grant, J. H. Wolfe, J. M. Wilson, and J. Bennett, “Dosage thresholds for AAV2 and AAV8 photoreceptor gene therapy in monkey,” Science Translational Medicine 3, 88ra54 (2011).

Bennett, J. A.

R. R. Birge, J. A. Bennett, B. M. Pierce, and T. M. Thomas, “Two-photon spectroscopy of the visual chromophores. Evidence for a lowest excited 1Ag–like. pi.pi.* state in all-trans-retinol (vitamin A),” J. Am. Chem. Soc. 100(5), 1533–1539 (1978).
[Crossref]

Bernstein, P. S.

Q. Wang, W. S. Tuten, B. J. Lujan, J. Holland, P. S. Bernstein, S. D. Schwartz, J. L. Duncan, and A. Roorda, “Adaptive optics microperimetry and OCT images show preserved function and recovery of cone visibility in macular telangiectasia type 2 retinal lesions,” Invest. Ophthalmol. Vis. Sci. 56(2), 778–786 (2015).
[Crossref] [PubMed]

Biel, M.

V. Busskamp, J. Duebel, D. Balya, M. Fradot, T. J. Viney, S. Siegert, A. C. Groner, E. Cabuy, V. Forster, M. Seeliger, M. Biel, P. Humphries, M. Paques, S. Mohand-Said, D. Trono, K. Deisseroth, J. A. Sahel, S. Picaud, and B. Roska, “Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa,” Science 329(5990), 413–417 (2010).
[Crossref] [PubMed]

Birge, R. R.

R. R. Birge, J. A. Bennett, B. M. Pierce, and T. M. Thomas, “Two-photon spectroscopy of the visual chromophores. Evidence for a lowest excited 1Ag–like. pi.pi.* state in all-trans-retinol (vitamin A),” J. Am. Chem. Soc. 100(5), 1533–1539 (1978).
[Crossref]

Botelho, J. V.

J. C. Horton, A. B. Parker, J. V. Botelho, and J. L. Duncan, “Spontaneous regeneration of human photoreceptor outer segments,” Sci. Rep. 5, 12364 (2015).

Bruce, K. S.

K. S. Bruce, W. M. Harmening, B. R. Langston, W. S. Tuten, A. Roorda, and L. C. Sincich, “Normal perceptual sensitivity arising from weakly reflective cone photoreceptors,” Invest. Ophthalmol. Vis. Sci. 56(8), 4431–4438 (2015).
[Crossref] [PubMed]

Burns, M. E.

P. Zhang, R. J. Zawadzki, M. Goswami, P. T. Nguyen, V. Yarov-Yarovoy, M. E. Burns, and E. N. Pugh, “In vivo optophysiology reveals that G-protein activation triggers osmotic swelling and increased light scattering of rod photoreceptors,” Proceedings of the National Academy of Sciences (2017).
[Crossref]

Burns, S. A.

Busskamp, V.

V. Busskamp, J. Krol, D. Nelidova, J. Daum, T. Szikra, B. Tsuda, J. Jüttner, K. Farrow, B. G. Scherf, C. P. Alvarez, C. Genoud, V. Sothilingam, N. Tanimoto, M. Stadler, M. Seeliger, M. Stoffel, W. Filipowicz, and B. Roska, “miRNAs 182 and 183 are necessary to maintain adult cone photoreceptor outer segments and visual function,” Neuron 83(3), 586–600 (2014).
[Crossref] [PubMed]

V. Busskamp, J. Duebel, D. Balya, M. Fradot, T. J. Viney, S. Siegert, A. C. Groner, E. Cabuy, V. Forster, M. Seeliger, M. Biel, P. Humphries, M. Paques, S. Mohand-Said, D. Trono, K. Deisseroth, J. A. Sahel, S. Picaud, and B. Roska, “Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa,” Science 329(5990), 413–417 (2010).
[Crossref] [PubMed]

Cabuy, E.

V. Busskamp, J. Duebel, D. Balya, M. Fradot, T. J. Viney, S. Siegert, A. C. Groner, E. Cabuy, V. Forster, M. Seeliger, M. Biel, P. Humphries, M. Paques, S. Mohand-Said, D. Trono, K. Deisseroth, J. A. Sahel, S. Picaud, and B. Roska, “Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa,” Science 329(5990), 413–417 (2010).
[Crossref] [PubMed]

Calcedo, R.

L. H. Vandenberghe, P. Bell, A. M. Maguire, C. N. Cearley, R. Xiao, R. Calcedo, L. Wang, M. J. Castle, A. C. Maguire, R. Grant, J. H. Wolfe, J. M. Wilson, and J. Bennett, “Dosage thresholds for AAV2 and AAV8 photoreceptor gene therapy in monkey,” Science Translational Medicine 3, 88ra54 (2011).

Campbell, M.

Carissimo, A.

M. Karali, M. Persico, M. Mutarelli, A. Carissimo, M. Pizzo, V. Singh Marwah, C. Ambrosio, M. Pinelli, D. Carrella, S. Ferrari, D. Ponzin, V. Nigro, D. di Bernardo, and S. Banfi, “High-resolution analysis of the human retina miRNome reveals isomiR variations and novel microRNAs,” Nucleic Acids Res. 44(4), 1525–1540 (2016).
[Crossref] [PubMed]

Carrella, D.

M. Karali, M. Persico, M. Mutarelli, A. Carissimo, M. Pizzo, V. Singh Marwah, C. Ambrosio, M. Pinelli, D. Carrella, S. Ferrari, D. Ponzin, V. Nigro, D. di Bernardo, and S. Banfi, “High-resolution analysis of the human retina miRNome reveals isomiR variations and novel microRNAs,” Nucleic Acids Res. 44(4), 1525–1540 (2016).
[Crossref] [PubMed]

Carroll, J.

E. J. Patterson, A. Kalitzeos, M. Kasilian, J. C. Gardner, J. Neitz, A. J. Hardcastle, M. Neitz, J. Carroll, and M. Michaelides, “Residual cone structure in patients with X-linked cone opsin mutations,” Invest. Ophthalmol. Vis. Sci. 59(10), 4238–4248 (2018).
[Crossref] [PubMed]

D. Scoles, J. A. Flatter, R. F. Cooper, C. S. Langlo, S. Robison, M. Neitz, D. V. Weinberg, M. E. Pennesi, D. P. Han, A. Dubra, and J. Carroll, “Assessing photoreceptor structure associated with ellipsoid zone disruptions visualized with optical coherence tomography,” Retina 36(1), 91–103 (2016).
[Crossref] [PubMed]

L. W. Sun, R. D. Johnson, C. S. Langlo, R. F. Cooper, M. M. Razeen, M. C. Russillo, A. Dubra, T. B. Connor, D. P. Han, M. E. Pennesi, C. N. Kay, D. V. Weinberg, K. E. Stepien, and J. Carroll, “Assessing photoreceptor structure in retinitis pigmentosa and Usher syndrome,” Invest. Ophthalmol. Vis. Sci. 57(6), 2428–2442 (2016).
[Crossref] [PubMed]

C. S. Langlo, E. J. Patterson, B. P. Higgins, P. Summerfelt, M. M. Razeen, L. R. Erker, M. Parker, F. T. Collison, G. A. Fishman, C. N. Kay, J. Zhang, R. G. Weleber, P. Yang, D. J. Wilson, M. E. Pennesi, B. L. Lam, J. Chiang, J. D. Chulay, A. Dubra, W. W. Hauswirth, and J. Carroll, “Residual foveal cone structure in CNGB3-associated achromatopsia,” Invest. Ophthalmol. Vis. Sci. 57(10), 3984–3995 (2016).
[Crossref] [PubMed]

D. Scoles, Y. N. Sulai, C. S. Langlo, G. A. Fishman, C. A. Curcio, J. Carroll, and A. Dubra, “In Vivo Imaging of Human Cone Photoreceptor Inner Segments,” Invest. Ophthalmol. Vis. Sci. 55(7), 4244–4251 (2014).
[Crossref] [PubMed]

J. A. Flatter, R. F. Cooper, M. J. Dubow, A. Pinhas, R. S. Singh, R. Kapur, N. Shah, R. D. Walsh, S. H. Hong, D. V. Weinberg, K. E. Stepien, W. J. Wirostko, S. Robison, A. Dubra, R. B. Rosen, T. B. J. Connor, and J. Carroll, “Outer retinal structure after closed-globe blunt ocular trauma,” Retina 34(10), 2133–2146 (2014).
[Crossref] [PubMed]

J. Rha, B. Schroeder, P. Godara, and J. Carroll, “Variable optical activation of human cone photoreceptors visualized using a short coherence light source,” Opt. Lett. 34(24), 3782–3784 (2009).
[Crossref] [PubMed]

H. Hofer, J. Carroll, J. Neitz, M. Neitz, and D. R. Williams, “Organization of the human trichromatic cone mosaic,” J. Neurosci. 25(42), 9669–9679 (2005).
[Crossref] [PubMed]

Castle, M. J.

L. H. Vandenberghe, P. Bell, A. M. Maguire, C. N. Cearley, R. Xiao, R. Calcedo, L. Wang, M. J. Castle, A. C. Maguire, R. Grant, J. H. Wolfe, J. M. Wilson, and J. Bennett, “Dosage thresholds for AAV2 and AAV8 photoreceptor gene therapy in monkey,” Science Translational Medicine 3, 88ra54 (2011).

Cearley, C. N.

L. H. Vandenberghe, P. Bell, A. M. Maguire, C. N. Cearley, R. Xiao, R. Calcedo, L. Wang, M. J. Castle, A. C. Maguire, R. Grant, J. H. Wolfe, J. M. Wilson, and J. Bennett, “Dosage thresholds for AAV2 and AAV8 photoreceptor gene therapy in monkey,” Science Translational Medicine 3, 88ra54 (2011).

Cense, B.

Chang, W.

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

Chen, C. S.

D. C. Hood, J. G. Odel, C. S. Chen, and B. J. Winn, “The multifocal electroretinogram,” J. Neuroophthalmol. 23(3), 225–235 (2003).
[Crossref] [PubMed]

Chiang, J.

C. S. Langlo, E. J. Patterson, B. P. Higgins, P. Summerfelt, M. M. Razeen, L. R. Erker, M. Parker, F. T. Collison, G. A. Fishman, C. N. Kay, J. Zhang, R. G. Weleber, P. Yang, D. J. Wilson, M. E. Pennesi, B. L. Lam, J. Chiang, J. D. Chulay, A. Dubra, W. W. Hauswirth, and J. Carroll, “Residual foveal cone structure in CNGB3-associated achromatopsia,” Invest. Ophthalmol. Vis. Sci. 57(10), 3984–3995 (2016).
[Crossref] [PubMed]

Chui, T. Y. P.

Chulay, J. D.

C. S. Langlo, E. J. Patterson, B. P. Higgins, P. Summerfelt, M. M. Razeen, L. R. Erker, M. Parker, F. T. Collison, G. A. Fishman, C. N. Kay, J. Zhang, R. G. Weleber, P. Yang, D. J. Wilson, M. E. Pennesi, B. L. Lam, J. Chiang, J. D. Chulay, A. Dubra, W. W. Hauswirth, and J. Carroll, “Residual foveal cone structure in CNGB3-associated achromatopsia,” Invest. Ophthalmol. Vis. Sci. 57(10), 3984–3995 (2016).
[Crossref] [PubMed]

Chung, M.

Chung, M. M.

E. A. Rossi, C. E. Granger, R. Sharma, Q. Yang, K. Saito, C. Schwarz, S. Walters, K. Nozato, J. Zhang, T. Kawakami, W. Fischer, L. R. Latchney, J. J. Hunter, M. M. Chung, and D. R. Williams, “Imaging individual neurons in the retinal ganglion cell layer of the living eye,” Proc. Natl. Acad. Sci. U.S.A. 114(3), 586–591 (2017).
[Crossref] [PubMed]

E. A. Rossi, P. Rangel-Fonseca, K. Parkins, W. Fischer, L. R. Latchney, M. A. Folwell, D. R. Williams, A. Dubra, and M. M. Chung, “In vivo imaging of retinal pigment epithelium cells in age related macular degeneration,” Biomed. Opt. Express 4(11), 2527–2539 (2013).
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Collison, F. T.

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J. A. Flatter, R. F. Cooper, M. J. Dubow, A. Pinhas, R. S. Singh, R. Kapur, N. Shah, R. D. Walsh, S. H. Hong, D. V. Weinberg, K. E. Stepien, W. J. Wirostko, S. Robison, A. Dubra, R. B. Rosen, T. B. J. Connor, and J. Carroll, “Outer retinal structure after closed-globe blunt ocular trauma,” Retina 34(10), 2133–2146 (2014).
[Crossref] [PubMed]

Walters, S.

E. A. Rossi, C. E. Granger, R. Sharma, Q. Yang, K. Saito, C. Schwarz, S. Walters, K. Nozato, J. Zhang, T. Kawakami, W. Fischer, L. R. Latchney, J. J. Hunter, M. M. Chung, and D. R. Williams, “Imaging individual neurons in the retinal ganglion cell layer of the living eye,” Proc. Natl. Acad. Sci. U.S.A. 114(3), 586–591 (2017).
[Crossref] [PubMed]

Wang, L.

L. H. Vandenberghe, P. Bell, A. M. Maguire, C. N. Cearley, R. Xiao, R. Calcedo, L. Wang, M. J. Castle, A. C. Maguire, R. Grant, J. H. Wolfe, J. M. Wilson, and J. Bennett, “Dosage thresholds for AAV2 and AAV8 photoreceptor gene therapy in monkey,” Science Translational Medicine 3, 88ra54 (2011).

Wang, Q.

Q. Wang, W. S. Tuten, B. J. Lujan, J. Holland, P. S. Bernstein, S. D. Schwartz, J. L. Duncan, and A. Roorda, “Adaptive optics microperimetry and OCT images show preserved function and recovery of cone visibility in macular telangiectasia type 2 retinal lesions,” Invest. Ophthalmol. Vis. Sci. 56(2), 778–786 (2015).
[Crossref] [PubMed]

Webb, W. W.

K. A. Kasischke, H. D. Vishwasrao, P. J. Fisher, W. R. Zipfel, and W. W. Webb, “Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis,” Science 305(5680), 99–103 (2004).
[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]

Weinberg, D. V.

D. Scoles, J. A. Flatter, R. F. Cooper, C. S. Langlo, S. Robison, M. Neitz, D. V. Weinberg, M. E. Pennesi, D. P. Han, A. Dubra, and J. Carroll, “Assessing photoreceptor structure associated with ellipsoid zone disruptions visualized with optical coherence tomography,” Retina 36(1), 91–103 (2016).
[Crossref] [PubMed]

L. W. Sun, R. D. Johnson, C. S. Langlo, R. F. Cooper, M. M. Razeen, M. C. Russillo, A. Dubra, T. B. Connor, D. P. Han, M. E. Pennesi, C. N. Kay, D. V. Weinberg, K. E. Stepien, and J. Carroll, “Assessing photoreceptor structure in retinitis pigmentosa and Usher syndrome,” Invest. Ophthalmol. Vis. Sci. 57(6), 2428–2442 (2016).
[Crossref] [PubMed]

J. A. Flatter, R. F. Cooper, M. J. Dubow, A. Pinhas, R. S. Singh, R. Kapur, N. Shah, R. D. Walsh, S. H. Hong, D. V. Weinberg, K. E. Stepien, W. J. Wirostko, S. Robison, A. Dubra, R. B. Rosen, T. B. J. Connor, and J. Carroll, “Outer retinal structure after closed-globe blunt ocular trauma,” Retina 34(10), 2133–2146 (2014).
[Crossref] [PubMed]

Weleber, R. G.

C. S. Langlo, E. J. Patterson, B. P. Higgins, P. Summerfelt, M. M. Razeen, L. R. Erker, M. Parker, F. T. Collison, G. A. Fishman, C. N. Kay, J. Zhang, R. G. Weleber, P. Yang, D. J. Wilson, M. E. Pennesi, B. L. Lam, J. Chiang, J. D. Chulay, A. Dubra, W. W. Hauswirth, and J. Carroll, “Residual foveal cone structure in CNGB3-associated achromatopsia,” Invest. Ophthalmol. Vis. Sci. 57(10), 3984–3995 (2016).
[Crossref] [PubMed]

Werner, J. S.

R. S. Jonnal, O. P. Kocaoglu, R. J. Zawadzki, S.-H. Lee, J. S. Werner, and D. T. Miller, “The cellular origins of the outer retinal bands in optical coherence tomography images,” Invest. Ophthalmol. Vis. Sci. 55(12), 7904–7918 (2014).
[Crossref] [PubMed]

Y. Zhang, B. Cense, J. Rha, R. S. Jonnal, W. Gao, R. J. Zawadzki, J. S. Werner, S. Jones, S. Olivier, and D. T. Miller, “High-speed volumetric imaging of cone photoreceptors with adaptive optics spectral-domain optical coherence tomography,” Opt. Express 14(10), 4380–4394 (2006).
[Crossref] [PubMed]

Williams, D. R.

E. A. Rossi, C. E. Granger, R. Sharma, Q. Yang, K. Saito, C. Schwarz, S. Walters, K. Nozato, J. Zhang, T. Kawakami, W. Fischer, L. R. Latchney, J. J. Hunter, M. M. Chung, and D. R. Williams, “Imaging individual neurons in the retinal ganglion cell layer of the living eye,” Proc. Natl. Acad. Sci. U.S.A. 114(3), 586–591 (2017).
[Crossref] [PubMed]

R. Sharma, C. Schwarz, J. J. Hunter, G. Palczewska, K. Palczewski, and D. R. Williams, “Formation and clearance of all-trans-retinol in rods investigated in the living primate eye with two-photon ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci. 58(1), 604–613 (2017).
[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]

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]

C. Schwarz, R. Sharma, W. S. Fischer, M. Chung, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “Safety assessment in macaques of light exposures for functional two-photon ophthalmoscopy in humans,” Biomed. Opt. Express 7(12), 5148–5169 (2016).
[Crossref] [PubMed]

A. Guevara-Torres, D. R. Williams, and J. B. Schallek, “Imaging translucent cell bodies in the living mouse retina without contrast agents,” Biomed. Opt. Express 6(6), 2106–2119 (2015).
[Crossref] [PubMed]

Q. Yang, L. Yin, K. Nozato, J. Zhang, K. Saito, W. H. Merigan, D. R. Williams, and E. A. Rossi, “Calibration-free sinusoidal rectification and uniform retinal irradiance in scanning light ophthalmoscopy,” Opt. Lett. 40(1), 85–88 (2015).
[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]

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]

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]

E. A. Rossi, P. Rangel-Fonseca, K. Parkins, W. Fischer, L. R. Latchney, M. A. Folwell, D. R. Williams, A. Dubra, and M. M. Chung, “In vivo imaging of retinal pigment epithelium cells in age related macular degeneration,” Biomed. Opt. Express 4(11), 2527–2539 (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]

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).
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D. C. Gray, W. Merigan, J. I. Wolfing, B. P. Gee, J. Porter, A. Dubra, T. H. Twietmeyer, K. Ahamd, R. Tumbar, F. Reinholz, and D. R. Williams, “In vivo fluorescence imaging of primate retinal ganglion cells and retinal pigment epithelial cells,” Opt. Express 14(16), 7144–7158 (2006).
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H. Hofer, J. Carroll, J. Neitz, M. Neitz, and D. R. Williams, “Organization of the human trichromatic cone mosaic,” J. Neurosci. 25(42), 9669–9679 (2005).
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A. Pallikaris, D. R. Williams, and H. Hofer, “The reflectance of single cones in the living human eye,” Invest. Ophthalmol. Vis. Sci. 44(10), 4580–4592 (2003).
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A. Roorda and D. R. Williams, “The arrangement of the three cone classes in the living human eye,” Nature 397(6719), 520–522 (1999).
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J. Liang, D. R. Williams, and D. T. Miller, “Supernormal vision and high-resolution retinal imaging through adaptive optics,” J. Opt. Soc. Am. A 14(11), 2884–2892 (1997).
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Wilson, D. J.

C. S. Langlo, E. J. Patterson, B. P. Higgins, P. Summerfelt, M. M. Razeen, L. R. Erker, M. Parker, F. T. Collison, G. A. Fishman, C. N. Kay, J. Zhang, R. G. Weleber, P. Yang, D. J. Wilson, M. E. Pennesi, B. L. Lam, J. Chiang, J. D. Chulay, A. Dubra, W. W. Hauswirth, and J. Carroll, “Residual foveal cone structure in CNGB3-associated achromatopsia,” Invest. Ophthalmol. Vis. Sci. 57(10), 3984–3995 (2016).
[Crossref] [PubMed]

Wilson, J. M.

L. H. Vandenberghe, P. Bell, A. M. Maguire, C. N. Cearley, R. Xiao, R. Calcedo, L. Wang, M. J. Castle, A. C. Maguire, R. Grant, J. H. Wolfe, J. M. Wilson, and J. Bennett, “Dosage thresholds for AAV2 and AAV8 photoreceptor gene therapy in monkey,” Science Translational Medicine 3, 88ra54 (2011).

Winn, B. J.

D. C. Hood, J. G. Odel, C. S. Chen, and B. J. Winn, “The multifocal electroretinogram,” J. Neuroophthalmol. 23(3), 225–235 (2003).
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J. A. Flatter, R. F. Cooper, M. J. Dubow, A. Pinhas, R. S. Singh, R. Kapur, N. Shah, R. D. Walsh, S. H. Hong, D. V. Weinberg, K. E. Stepien, W. J. Wirostko, S. Robison, A. Dubra, R. B. Rosen, T. B. J. Connor, and J. Carroll, “Outer retinal structure after closed-globe blunt ocular trauma,” Retina 34(10), 2133–2146 (2014).
[Crossref] [PubMed]

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L. H. Vandenberghe, P. Bell, A. M. Maguire, C. N. Cearley, R. Xiao, R. Calcedo, L. Wang, M. J. Castle, A. C. Maguire, R. Grant, J. H. Wolfe, J. M. Wilson, and J. Bennett, “Dosage thresholds for AAV2 and AAV8 photoreceptor gene therapy in monkey,” Science Translational Medicine 3, 88ra54 (2011).

Wolfe, R.

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]

Wolfing, J. I.

Xiao, R.

L. H. Vandenberghe, P. Bell, A. M. Maguire, C. N. Cearley, R. Xiao, R. Calcedo, L. Wang, M. J. Castle, A. C. Maguire, R. Grant, J. H. Wolfe, J. M. Wilson, and J. Bennett, “Dosage thresholds for AAV2 and AAV8 photoreceptor gene therapy in monkey,” Science Translational Medicine 3, 88ra54 (2011).

Yang, P.

C. S. Langlo, E. J. Patterson, B. P. Higgins, P. Summerfelt, M. M. Razeen, L. R. Erker, M. Parker, F. T. Collison, G. A. Fishman, C. N. Kay, J. Zhang, R. G. Weleber, P. Yang, D. J. Wilson, M. E. Pennesi, B. L. Lam, J. Chiang, J. D. Chulay, A. Dubra, W. W. Hauswirth, and J. Carroll, “Residual foveal cone structure in CNGB3-associated achromatopsia,” Invest. Ophthalmol. Vis. Sci. 57(10), 3984–3995 (2016).
[Crossref] [PubMed]

Yang, Q.

E. A. Rossi, C. E. Granger, R. Sharma, Q. Yang, K. Saito, C. Schwarz, S. Walters, K. Nozato, J. Zhang, T. Kawakami, W. Fischer, L. R. Latchney, J. J. Hunter, M. M. Chung, and D. R. Williams, “Imaging individual neurons in the retinal ganglion cell layer of the living eye,” Proc. Natl. Acad. Sci. U.S.A. 114(3), 586–591 (2017).
[Crossref] [PubMed]

Q. Yang, L. Yin, K. Nozato, J. Zhang, K. Saito, W. H. Merigan, D. R. Williams, and E. A. Rossi, “Calibration-free sinusoidal rectification and uniform retinal irradiance in scanning light ophthalmoscopy,” Opt. Lett. 40(1), 85–88 (2015).
[Crossref] [PubMed]

Yarov-Yarovoy, V.

P. Zhang, R. J. Zawadzki, M. Goswami, P. T. Nguyen, V. Yarov-Yarovoy, M. E. Burns, and E. N. Pugh, “In vivo optophysiology reveals that G-protein activation triggers osmotic swelling and increased light scattering of rod photoreceptors,” Proceedings of the National Academy of Sciences (2017).
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Yin, L.

Zawadzki, R. J.

R. S. Jonnal, O. P. Kocaoglu, R. J. Zawadzki, S.-H. Lee, J. S. Werner, and D. T. Miller, “The cellular origins of the outer retinal bands in optical coherence tomography images,” Invest. Ophthalmol. Vis. Sci. 55(12), 7904–7918 (2014).
[Crossref] [PubMed]

Y. Zhang, B. Cense, J. Rha, R. S. Jonnal, W. Gao, R. J. Zawadzki, J. S. Werner, S. Jones, S. Olivier, and D. T. Miller, “High-speed volumetric imaging of cone photoreceptors with adaptive optics spectral-domain optical coherence tomography,” Opt. Express 14(10), 4380–4394 (2006).
[Crossref] [PubMed]

P. Zhang, R. J. Zawadzki, M. Goswami, P. T. Nguyen, V. Yarov-Yarovoy, M. E. Burns, and E. N. Pugh, “In vivo optophysiology reveals that G-protein activation triggers osmotic swelling and increased light scattering of rod photoreceptors,” Proceedings of the National Academy of Sciences (2017).
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Zhang, J.

E. A. Rossi, C. E. Granger, R. Sharma, Q. Yang, K. Saito, C. Schwarz, S. Walters, K. Nozato, J. Zhang, T. Kawakami, W. Fischer, L. R. Latchney, J. J. Hunter, M. M. Chung, and D. R. Williams, “Imaging individual neurons in the retinal ganglion cell layer of the living eye,” Proc. Natl. Acad. Sci. U.S.A. 114(3), 586–591 (2017).
[Crossref] [PubMed]

C. S. Langlo, E. J. Patterson, B. P. Higgins, P. Summerfelt, M. M. Razeen, L. R. Erker, M. Parker, F. T. Collison, G. A. Fishman, C. N. Kay, J. Zhang, R. G. Weleber, P. Yang, D. J. Wilson, M. E. Pennesi, B. L. Lam, J. Chiang, J. D. Chulay, A. Dubra, W. W. Hauswirth, and J. Carroll, “Residual foveal cone structure in CNGB3-associated achromatopsia,” Invest. Ophthalmol. Vis. Sci. 57(10), 3984–3995 (2016).
[Crossref] [PubMed]

Q. Yang, L. Yin, K. Nozato, J. Zhang, K. Saito, W. H. Merigan, D. R. Williams, and E. A. Rossi, “Calibration-free sinusoidal rectification and uniform retinal irradiance in scanning light ophthalmoscopy,” Opt. Lett. 40(1), 85–88 (2015).
[Crossref] [PubMed]

Zhang, P.

P. Zhang, R. J. Zawadzki, M. Goswami, P. T. Nguyen, V. Yarov-Yarovoy, M. E. Burns, and E. N. Pugh, “In vivo optophysiology reveals that G-protein activation triggers osmotic swelling and increased light scattering of rod photoreceptors,” Proceedings of the National Academy of Sciences (2017).
[Crossref]

Zhang, Y.

Zipfel, W. R.

K. A. Kasischke, H. D. Vishwasrao, P. J. Fisher, W. R. Zipfel, and W. W. Webb, “Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis,” Science 305(5680), 99–103 (2004).
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J. Jacob, M. Paques, V. Krivosic, B. Dupas, A. Couturier, C. Kulcsar, R. Tadayoni, P. Massin, and A. Gaudric, “Meaning of visualizing retinal cone mosaic on adaptive optics images,” Am. J. Ophthalmol. 159(1), 118–123 (2015).
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C. Schwarz, R. Sharma, W. S. Fischer, M. Chung, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “Safety assessment in macaques of light exposures for functional two-photon ophthalmoscopy in humans,” Biomed. Opt. Express 7(12), 5148–5169 (2016).
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E. A. Rossi, P. Rangel-Fonseca, K. Parkins, W. Fischer, L. R. Latchney, M. A. Folwell, D. R. Williams, A. Dubra, and M. M. Chung, “In vivo imaging of retinal pigment epithelium cells in age related macular degeneration,” Biomed. Opt. Express 4(11), 2527–2539 (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]

A. Guevara-Torres, D. R. Williams, and J. B. Schallek, “Imaging translucent cell bodies in the living mouse retina without contrast agents,” Biomed. Opt. Express 6(6), 2106–2119 (2015).
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D. Scoles, Y. N. Sulai, and A. Dubra, “In vivo dark-field imaging of the retinal pigment epithelium cell mosaic,” Biomed. Opt. Express 4(9), 1710–1723 (2013).
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T. Y. P. Chui, D. A. Vannasdale, and S. A. Burns, “The use of forward scatter to improve retinal vascular imaging with an adaptive optics scanning laser ophthalmoscope,” Biomed. Opt. Express 3(10), 2537–2549 (2012).
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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).
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S. Huang, A. A. Heikal, and W. W. Webb, “Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein,” Biophys. J. 82(5), 2811–2825 (2002).
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R. S. Jonnal, O. P. Kocaoglu, R. J. Zawadzki, S.-H. Lee, J. S. Werner, and D. T. Miller, “The cellular origins of the outer retinal bands in optical coherence tomography images,” Invest. Ophthalmol. Vis. Sci. 55(12), 7904–7918 (2014).
[Crossref] [PubMed]

A. Pallikaris, D. R. Williams, and H. Hofer, “The reflectance of single cones in the living human eye,” Invest. Ophthalmol. Vis. Sci. 44(10), 4580–4592 (2003).
[Crossref] [PubMed]

D. H. Anderson, C. J. Guérin, P. A. Erickson, W. H. Stern, and S. K. Fisher, “Morphological recovery in the reattached retina,” Invest. Ophthalmol. Vis. Sci. 27(2), 168–183 (1986).
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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).
[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]

R. Sharma, C. Schwarz, J. J. Hunter, G. Palczewska, K. Palczewski, and D. R. Williams, “Formation and clearance of all-trans-retinol in rods investigated in the living primate eye with two-photon ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci. 58(1), 604–613 (2017).
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L. W. Sun, R. D. Johnson, C. S. Langlo, R. F. Cooper, M. M. Razeen, M. C. Russillo, A. Dubra, T. B. Connor, D. P. Han, M. E. Pennesi, C. N. Kay, D. V. Weinberg, K. E. Stepien, and J. Carroll, “Assessing photoreceptor structure in retinitis pigmentosa and Usher syndrome,” Invest. Ophthalmol. Vis. Sci. 57(6), 2428–2442 (2016).
[Crossref] [PubMed]

C. S. Langlo, E. J. Patterson, B. P. Higgins, P. Summerfelt, M. M. Razeen, L. R. Erker, M. Parker, F. T. Collison, G. A. Fishman, C. N. Kay, J. Zhang, R. G. Weleber, P. Yang, D. J. Wilson, M. E. Pennesi, B. L. Lam, J. Chiang, J. D. Chulay, A. Dubra, W. W. Hauswirth, and J. Carroll, “Residual foveal cone structure in CNGB3-associated achromatopsia,” Invest. Ophthalmol. Vis. Sci. 57(10), 3984–3995 (2016).
[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]

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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K. Grieve and A. Roorda, “Intrinsic signals from human cone photoreceptors,” Invest. Ophthalmol. Vis. Sci. 49(2), 713–719 (2008).
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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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K. S. Bruce, W. M. Harmening, B. R. Langston, W. S. Tuten, A. Roorda, and L. C. Sincich, “Normal perceptual sensitivity arising from weakly reflective cone photoreceptors,” Invest. Ophthalmol. Vis. Sci. 56(8), 4431–4438 (2015).
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Figures (8)

Fig. 1
Fig. 1 AOSLO detection channel configurations for (a) confocal reflectance and (b) multioffset, where the pinhole and PMT are displaced from the confocal position.
Fig. 2
Fig. 2 cSLO images of M1 prior to (a,c,e,g) and 28 weeks after (b,d,f,h) subretinal injection of virus in four modalities: IR (a,b); IRAF (c,d); BR (e,f); BAF (g,h). In (b), white arrow denotes injection site, and white dashed circle the extent of the bleb. Scale bar: 1 mm.
Fig. 3
Fig. 3 cSLO (a,c) and corresponding OCT (b,d) of affected regions within the bleb for monkey M1 (a,b) and M2 (c,d). The dotted white line in cSLO images is indicative of the position of the OCT B-scans. White arrows mark positions of disruption in both the cSLO images and corresponding OCT B-scans. Scale bar: horizontal, 200 μm; vertical, 100 μm.
Fig. 4
Fig. 4 AOSLO imaging of affected regions within the bleb of three monkeys. Images of the same location in three modalities are presented: 730 nm confocal reflectance (a,d,g), TPEF (b,e,h), and multioffset (c,f,i). Scale bar: 50 μm.
Fig. 5
Fig. 5 TPEF imaging of affected regions in two monkeys at different excitation wavelengths. Images of the same location in each monkey are presented at 730 nm excitation (a, c) and 900 nm excitation (b, d). Scale bars: 50 μm.
Fig. 6
Fig. 6 AOSLO imaging of an affected region on the inferotemporal edge of the bleb in monkey M4, in three modalities: 730 nm confocal reflectance (a), TPEF (b), and multioffset (c). The orange arrow denotes a cone photoreceptor that appears to be waveguiding (a), is bright in TPEF (b), and has low contrast in multioffset (c). The blue arrow denotes a cone photoreceptor that appears dark in reflectance (a) and TPEF (b), but has high contrast in multioffset (c). The white arrow denotes a rod that is bright in reflectance (a) and TPEF (b), but could not be visualized in multioffset (c). Scale bar: 50 μm.
Fig. 7
Fig. 7 The time course of TPEF for M2 in the same location as Fig. 4(d)-(f). Image segmentation is shown in (a), with the blue rectangle encompassing a normal region and the orange rectangle encompassing an affected region. Areas outlined in yellow are excluded from the affected region, and are plotted separately in their corresponding color in (b). Data points in (b) represent approximately 0.8 seconds of binned data of each of the regions in (a), with error bars representing standard error of the mean. Plotted lines in (b) are exponential fits to the data. Scale bar, 50 μm.
Fig. 8
Fig. 8 Two histological sections (b and c) through an affected region in monkey M1, horizontally aligned to TPEF imaging at 730 nm excitation (a). Here, lines A and B denote angle of each histological section with respect to the en face imaging. ONL, outer nuclear layer; Ch, choroid. Scale bar, 50 μm.

Tables (1)

Tables Icon

Table 1 Summary of Non-Human Primate Subretinal Injections