Abstract

Correction of the eye’s monochromatic aberrations using adaptive optics (AO) can improve the resolution of in vivo mouse retinal images [Biss et al., Opt. Lett. 32(6), 659 (2007) and Alt et al., Proc. SPIE 7550, 755019 (2010)], but previous attempts have been limited by poor spot quality in the Shack-Hartmann wavefront sensor (SHWS). Recent advances in mouse eye wavefront sensing using an adjustable focus beacon with an annular beam profile have improved the wavefront sensor spot quality [Geng et al., Biomed. Opt. Express 2(4), 717 (2011)], and we have incorporated them into a fluorescence adaptive optics scanning laser ophthalmoscope (AOSLO). The performance of the instrument was tested on the living mouse eye, and images of multiple retinal structures, including the photoreceptor mosaic, nerve fiber bundles, fine capillaries and fluorescently labeled ganglion cells were obtained. The in vivo transverse and axial resolutions of the fluorescence channel of the AOSLO were estimated from the full width half maximum (FWHM) of the line and point spread functions (LSF and PSF), and were found to be better than 0.79 μm ± 0.03 μm (STD)(45% wider than the diffraction limit) and 10.8 μm ± 0.7 μm (STD)(two times the diffraction limit), respectively. The axial positional accuracy was estimated to be 0.36 μm. This resolution and positional accuracy has allowed us to classify many ganglion cell types, such as bistratified ganglion cells, in vivo.

© 2012 OSA

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2011 (8)

C. K. S. Leung, R. N. Weinreb, Z. W. Li, S. Liu, J. D. Lindsey, N. Choi, L. Liu, C. Y. L. Cheung, C. Ye, K. L. Qiu, L. J. Chen, W. H. Yung, J. G. Crowston, M. L. Pu, K. F. So, C. P. Pang, and D. S. C. Lam, “Long-term in vivo imaging and measurement of dendritic shrinkage of retinal ganglion cells,” Invest. Ophthalmol. Vis. Sci.52(3), 1539–1547 (2011).
[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. Express2(4), 717–738 (2011).
[CrossRef] [PubMed]

A. Dubra and Y. Sulai, “Reflective afocal broadband adaptive optics scanning ophthalmoscope,” Biomed. Opt. Express2(6), 1757–1768 (2011).
[CrossRef] [PubMed]

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. Express2(7), 1864–1876 (2011).
[CrossRef] [PubMed]

J. Tam, P. Tiruveedhula, and A. Roorda, “Characterization of single-file flow through human retinal parafoveal capillaries using an adaptive optics scanning laser ophthalmoscope,” Biomed. Opt. Express2(4), 781–793 (2011).
[CrossRef] [PubMed]

Z. Y. Zhong, H. X. Song, T. Y. P. Chui, B. L. Petrig, and S. A. Burns, “Noninvasive measurements and analysis of blood velocity profiles in human retinal vessels,” Invest. Ophthalmol. Vis. Sci.52(7), 4151–4157 (2011).
[CrossRef] [PubMed]

P. Charbel Issa, M. S. Singh, D. M. Lipinski, N. V. Chong, F. C. Delori, A. R. Barnard, and R. E. Maclaren, “Optimization of in vivo confocal autofluorescence imaging of the ocular fundus in mice and its application to models of human retinal degeneration,” Invest. Ophthalmol. Vis. Sci.53, iovs.11-8767 (2011).
[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. Express2(1), 139–148 (2011).
[CrossRef] [PubMed]

2010 (3)

I. J. Kim, Y. F. Zhang, M. Meister, and J. R. Sanes, “Laminar restriction of retinal ganglion cell dendrites and axons: subtype-specific developmental patterns revealed with transgenic markers,” J. Neurosci.30(4), 1452–1462 (2010).
[CrossRef] [PubMed]

C. Alt, D. P. Biss, N. Tajouri, T. C. Jakobs, and C. P. Lin, “An adaptive-optics scanning laser ophthalmoscope for imaging murine retinal microstructure,” Proc. SPIE7550, 755019 (2010).
[CrossRef]

J. Tam, J. A. Martin, and A. Roorda, “Noninvasive visualization and analysis of parafoveal capillaries in humans,” Invest. Ophthalmol. Vis. Sci.51(3), 1691–1698 (2010).
[CrossRef] [PubMed]

2009 (4)

A. Gómez-Vieyra, A. Dubra, D. Malacara-Hernández, and D. R. Williams, “First-order design of off-axis reflective ophthalmic adaptive optics systems using afocal telescopes,” Opt. Express17(21), 18906–18919 (2009).
[CrossRef] [PubMed]

Y. Geng, K. P. Greenberg, R. Wolfe, D. C. Gray, J. J. Hunter, A. Dubra, J. G. Flannery, D. R. Williams, and J. Porter, “In vivo imaging of microscopic structures in the rat retina,” Invest. Ophthalmol. Vis. Sci.50(12), 5872–5879 (2009).
[CrossRef] [PubMed]

J. I. 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]

M. D. Fischer, G. Huber, S. C. Beck, N. Tanimoto, R. Muehlfriedel, E. Fahl, C. Grimm, A. Wenzel, C. E. Remé, S. A. van de Pavert, J. Wijnholds, M. Pacal, R. Bremner, and M. W. Seeliger, “Noninvasive, in vivo assessment of mouse retinal structure using optical coherence tomography,” PLoS ONE4(10), e7507 (2009).
[CrossRef] [PubMed]

2008 (6)

H. Murata, M. Aihara, Y. N. Chen, T. Ota, J. Numaga, and M. Araie, “Imaging mouse retinal ganglion cells and their loss in vivo by a fundus camera in the normal and ischemia-reperfusion model,” Invest. Ophthalmol. Vis. Sci.49(12), 5546–5552 (2008).
[CrossRef] [PubMed]

M. K. Walsh and H. A. Quigley, “In vivo time-lapse fluorescence imaging of individual retinal ganglion cells in mice,” J. Neurosci. Methods169(1), 214–221 (2008).
[CrossRef] [PubMed]

D. C. Gray, R. Wolfe, B. P. Gee, D. Scoles, Y. Geng, B. D. Masella, A. Dubra, S. Luque, D. R. Williams, and W. H. Merigan, “In vivo imaging of the fine structure of rhodamine-labeled macaque retinal ganglion cells,” Invest. Ophthalmol. Vis. Sci.49(1), 467–473 (2008).
[CrossRef] [PubMed]

A. Dhingra, P. Sulaiman, Y. Xu, M. E. Fina, R. W. Veh, and N. Vardi, “Probing neurochemical structure and function of retinal ON bipolar cells with a transgenic mouse,” J. Comp. Neurol.510(5), 484–496 (2008).
[CrossRef] [PubMed]

S. A. Burns, Z. Zhangyi, T. Y. P. Chui, H. Song, A. E. Elsner, and V. E. Malinovsky, “Imaging the inner retina using adaptive optics,” nvest. Ophthalmol. Vis. Sci.49, 4512–9999 (2008).

Z. Y. Zhong, B. L. Petrig, X. F. Qi, and S. A. Burns, “In vivo measurement of erythrocyte velocity and retinal blood flow using adaptive optics scanning laser ophthalmoscopy,” Opt. Express16(17), 12746–12756 (2008).
[PubMed]

2007 (6)

K. P. Greenberg, S. F. Geller, D. V. Schaffer, and J. G. Flannery, “Targeted transgene expression in muller glia of normal and diseased retinas using lentiviral vectors,” Invest. Ophthalmol. Vis. Sci.48(4), 1844–1852 (2007).
[CrossRef] [PubMed]

D. P. Biss, D. Sumorok, S. A. Burns, R. H. Webb, Y. Zhou, T. G. Bifano, D. Côté, I. Veilleux, P. Zamiri, and C. P. Lin, “In vivo fluorescent imaging of the mouse retina using adaptive optics,” Opt. Lett.32(6), 659–661 (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. A24(5), 1250–1265 (2007).
[CrossRef] [PubMed]

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A. Maass, P. L. von Leithner, V. Luong, L. Guo, T. E. Salt, F. W. Fitzke, and M. F. Cordeiro, “Assessment of rat and mouse RGC apoptosis imaging in vivo with different scanning laser ophthalmoscopes,” Curr. Eye Res.32(10), 851–861 (2007).
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O. P. Kocaoglu, S. R. Uhlhorn, E. Hernandez, R. A. Juarez, R. Will, J. M. Parel, and F. Manns, “Simultaneous fundus imaging and optical coherence tomography of the mouse retina,” Invest. Ophthalmol. Vis. Sci.48(3), 1283–1289 (2007).
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2006 (7)

V. J. Srinivasan, T. H. Ko, M. Wojtkowski, M. Carvalho, A. Clermont, S. E. Bursell, Q. H. Song, J. Lem, J. S. Duker, J. S. Schuman, and J. G. Fujimoto, “Noninvasive volumetric imaging and morphometry of the rodent retina with high-speed, ultrahigh-resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.47(12), 5522–5528 (2006).
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M. Paques, M. Simonutti, M. J. Roux, S. Picaud, E. Levavasseur, C. Bellman, and J.-A. Sahel, “High resolution fundus imaging by confocal scanning laser ophthalmoscopy in the mouse,” Vision Res.46(8-9), 1336–1345 (2006).
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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. Express14(16), 7144–7158 (2006).
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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).
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K. P. Greenberg, E. S. Lee, D. V. Schaffer, and J. G. Flannery, “Gene delivery to the retina using lentiviral vectors,” Adv. Exp. Med. Biol.572, 255–266 (2006).
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T. Higashide, I. Kawaguchi, S. Ohkubo, H. Takeda, and K. Sugiyama, “In vivo imaging and counting of rat retinal ganglion cells using a scanning laser ophthalmoscope,” Invest. Ophthalmol. Vis. Sci.47(7), 2943–2950 (2006).
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J. Coombs, D. van der List, G. Y. Wang, and L. M. Chalupa, “Morphological properties of mouse retinal ganglion cells,” Neuroscience140(1), 123–136 (2006).
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2005 (5)

J.-H. Kong, D. R. Fish, R. L. Rockhill, and R. H. Masland, “Diversity of ganglion cells in the mouse retina: unsupervised morphological classification and its limits,” J. Comp. Neurol.489(3), 293–310 (2005).
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Y. Han and S. C. Massey, “Electrical synapses in retinal ON cone bipolar cells: subtype-specific expression of connexins,” Proc. Natl. Acad. Sci. U.S.A.102(37), 13313–13318 (2005).
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R. T. Libby, M. G. Anderson, I. H. Pang, Z. H. Robinson, O. V. Savinova, I. M. Cosma, A. Snow, L. A. Wilson, R. S. Smith, A. F. Clark, and S. W. John, “Inherited glaucoma in DBA/2J mice: pertinent disease features for studying the neurodegeneration,” Vis. Neurosci.22(05), 637–648 (2005).
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B. Chang, N. L. Hawes, R. E. Hurd, J. Wang, D. Howell, M. T. Davisson, T. H. Roderick, S. Nusinowitz, and J. R. Heckenlively, “Mouse models of ocular diseases,” Vis. Neurosci.22(05), 587–593 (2005).
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M. W. Seeliger, S. C. Beck, N. Pereyra-Muñoz, S. Dangel, J. Y. Tsai, U. F. Luhmann, S. A. van de Pavert, J. Wijnholds, M. Samardzija, A. Wenzel, E. Zrenner, K. Narfström, E. Fahl, N. Tanimoto, N. Acar, and F. Tonagel, “In vivo confocal imaging of the retina in animal models using scanning laser ophthalmoscopy,” Vision Res.45(28), 3512–3519 (2005).
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2004 (5)

H. Levkovitch-Verbin, “Animal models of optic nerve diseases,” Eye (Lond.)18(11), 1066–1074 (2004).
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C. Schmucker and F. Schaeffel, “A paraxial schematic eye model for the growing C57BL/6 mouse,” Vision Res.44(16), 1857–1867 (2004).
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T. C. Badea and J. Nathans, “Quantitative analysis of neuronal morphologies in the mouse retina visualized by using a genetically directed reporter,” J. Comp. Neurol.480(4), 331–351 (2004).
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F. Chan, A. Bradley, T. G. Wensel, and J. H. Wilson, “Knock-in human rhodopsin-GFP fusions as mouse models for human disease and targets for gene therapy,” Proc. Natl. Acad. Sci. U.S.A.101(24), 9109–9114 (2004).
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F. Rolling, “Recombinant AAV-mediated gene transfer to the retina: gene therapy perspectives,” Gene Ther.11(Suppl 1), S26–S32 (2004).
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2003 (3)

J. Tejedor and P. de la Villa, “Refractive changes induced by form deprivation in the mouse eye,” Invest. Ophthalmol. Vis. Sci.44(1), 32–36 (2003).
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L. Wang, J. Dong, G. Cull, B. Fortune, and G. A. Cioffi, “Varicosities of intraretinal ganglion cell axons in human and nonhuman primates,” Invest. Ophthalmol. Vis. Sci.44(1), 2–9 (2003).
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M. Paques, R. Tadayoni, R. Sercombe, P. Laurent, O. Genevois, A. Gaudric, and E. Vicaut, “Structural and hemodynamic analysis of the mouse retinal microcirculation,” Invest. Ophthalmol. Vis. Sci.44(11), 4960–4967 (2003).
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2002 (3)

G. J. Chader, “Animal models in research on retinal degenerations: past progress and future hope,” Vision Res.42(4), 393–399 (2002).
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W. Sun, N. Li, and S. He, “Large-scale morphological survey of mouse retinal ganglion cells,” J. Comp. Neurol.451(2), 115–126 (2002).
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S. Thanos, L. Indorf, and R. Naskar, “In vivo FM: using conventional fluorescence microscopy to monitor retinal neuronal death in vivo,” Trends Neurosci.25(9), 441–444 (2002).
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2000 (2)

S. Haverkamp and H. Wässle, “Immunocytochemical analysis of the mouse retina,” J. Comp. Neurol.424(1), 1–23 (2000).
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G. Feng, R. H. Mellor, M. Bernstein, C. Keller-Peck, Q. T. Nguyen, M. Wallace, J. M. Nerbonne, J. W. Lichtman, and J. R. Sanes, “Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP,” Neuron28(1), 41–51 (2000).
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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).
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1997 (2)

J. Liang, D. R. Williams, and D. T. Miller, “Supernormal vision and high-resolution retinal imaging through adaptive optics,” J. Opt. Soc. Am. A14(11), 2884–2892 (1997).
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1994 (1)

Q. Wang, B. E. Klein, R. Klein, and S. E. Moss, “Refractive status in the Beaver Dam Eye Study,” Invest. Ophthalmol. Vis. Sci.35(13), 4344–4347 (1994).
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1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science248(4951), 73–76 (1990).
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1986 (1)

R. A. Cuthbertson and T. E. Mandel, “Anatomy of the mouse retina. Endothelial cell-pericyte ratio and capillary distribution,” Invest. Ophthalmol. Vis. Sci.27(11), 1659–1664 (1986).
[PubMed]

1960 (1)

A. Sorsby, M. Sheridan, G. A. Leary, and B. Benjamin, “Vision, visual acuity, and ocular refraction of young men: findings in a sample of 1,033 subjects,” BMJ1(5183), 1394–1398 (1960).
[CrossRef] [PubMed]

Acar, N.

M. W. Seeliger, S. C. Beck, N. Pereyra-Muñoz, S. Dangel, J. Y. Tsai, U. F. Luhmann, S. A. van de Pavert, J. Wijnholds, M. Samardzija, A. Wenzel, E. Zrenner, K. Narfström, E. Fahl, N. Tanimoto, N. Acar, and F. Tonagel, “In vivo confocal imaging of the retina in animal models using scanning laser ophthalmoscopy,” Vision Res.45(28), 3512–3519 (2005).
[CrossRef] [PubMed]

Ahamd, K.

Ahmad, K.

Aihara, M.

H. Murata, M. Aihara, Y. N. Chen, T. Ota, J. Numaga, and M. Araie, “Imaging mouse retinal ganglion cells and their loss in vivo by a fundus camera in the normal and ischemia-reperfusion model,” Invest. Ophthalmol. Vis. Sci.49(12), 5546–5552 (2008).
[CrossRef] [PubMed]

Alt, C.

C. Alt, D. P. Biss, N. Tajouri, T. C. Jakobs, and C. P. Lin, “An adaptive-optics scanning laser ophthalmoscope for imaging murine retinal microstructure,” Proc. SPIE7550, 755019 (2010).
[CrossRef]

Anderson, M. G.

R. T. Libby, M. G. Anderson, I. H. Pang, Z. H. Robinson, O. V. Savinova, I. M. Cosma, A. Snow, L. A. Wilson, R. S. Smith, A. F. Clark, and S. W. John, “Inherited glaucoma in DBA/2J mice: pertinent disease features for studying the neurodegeneration,” Vis. Neurosci.22(05), 637–648 (2005).
[CrossRef] [PubMed]

Araie, M.

H. Murata, M. Aihara, Y. N. Chen, T. Ota, J. Numaga, and M. Araie, “Imaging mouse retinal ganglion cells and their loss in vivo by a fundus camera in the normal and ischemia-reperfusion model,” Invest. Ophthalmol. Vis. Sci.49(12), 5546–5552 (2008).
[CrossRef] [PubMed]

Badea, T. C.

T. C. Badea and J. Nathans, “Quantitative analysis of neuronal morphologies in the mouse retina visualized by using a genetically directed reporter,” J. Comp. Neurol.480(4), 331–351 (2004).
[CrossRef] [PubMed]

Barnard, A. R.

P. Charbel Issa, M. S. Singh, D. M. Lipinski, N. V. Chong, F. C. Delori, A. R. Barnard, and R. E. Maclaren, “Optimization of in vivo confocal autofluorescence imaging of the ocular fundus in mice and its application to models of human retinal degeneration,” Invest. Ophthalmol. Vis. Sci.53, iovs.11-8767 (2011).
[PubMed]

Beck, S. C.

M. D. Fischer, G. Huber, S. C. Beck, N. Tanimoto, R. Muehlfriedel, E. Fahl, C. Grimm, A. Wenzel, C. E. Remé, S. A. van de Pavert, J. Wijnholds, M. Pacal, R. Bremner, and M. W. Seeliger, “Noninvasive, in vivo assessment of mouse retinal structure using optical coherence tomography,” PLoS ONE4(10), e7507 (2009).
[CrossRef] [PubMed]

M. W. Seeliger, S. C. Beck, N. Pereyra-Muñoz, S. Dangel, J. Y. Tsai, U. F. Luhmann, S. A. van de Pavert, J. Wijnholds, M. Samardzija, A. Wenzel, E. Zrenner, K. Narfström, E. Fahl, N. Tanimoto, N. Acar, and F. Tonagel, “In vivo confocal imaging of the retina in animal models using scanning laser ophthalmoscopy,” Vision Res.45(28), 3512–3519 (2005).
[CrossRef] [PubMed]

Bellman, C.

M. Paques, M. Simonutti, M. J. Roux, S. Picaud, E. Levavasseur, C. Bellman, and J.-A. Sahel, “High resolution fundus imaging by confocal scanning laser ophthalmoscopy in the mouse,” Vision Res.46(8-9), 1336–1345 (2006).
[CrossRef] [PubMed]

Benjamin, B.

A. Sorsby, M. Sheridan, G. A. Leary, and B. Benjamin, “Vision, visual acuity, and ocular refraction of young men: findings in a sample of 1,033 subjects,” BMJ1(5183), 1394–1398 (1960).
[CrossRef] [PubMed]

Bernstein, M.

G. Feng, R. H. Mellor, M. Bernstein, C. Keller-Peck, Q. T. Nguyen, M. Wallace, J. M. Nerbonne, J. W. Lichtman, and J. R. Sanes, “Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP,” Neuron28(1), 41–51 (2000).
[CrossRef] [PubMed]

Bifano, T. G.

Biss, D. P.

C. Alt, D. P. Biss, N. Tajouri, T. C. Jakobs, and C. P. Lin, “An adaptive-optics scanning laser ophthalmoscope for imaging murine retinal microstructure,” Proc. SPIE7550, 755019 (2010).
[CrossRef]

D. P. Biss, D. Sumorok, S. A. Burns, R. H. Webb, Y. Zhou, T. G. Bifano, D. Côté, I. Veilleux, P. Zamiri, and C. P. Lin, “In vivo fluorescent imaging of the mouse retina using adaptive optics,” Opt. Lett.32(6), 659–661 (2007).
[CrossRef] [PubMed]

Bradley, A.

F. Chan, A. Bradley, T. G. Wensel, and J. H. Wilson, “Knock-in human rhodopsin-GFP fusions as mouse models for human disease and targets for gene therapy,” Proc. Natl. Acad. Sci. U.S.A.101(24), 9109–9114 (2004).
[CrossRef] [PubMed]

Bremner, R.

M. D. Fischer, G. Huber, S. C. Beck, N. Tanimoto, R. Muehlfriedel, E. Fahl, C. Grimm, A. Wenzel, C. E. Remé, S. A. van de Pavert, J. Wijnholds, M. Pacal, R. Bremner, and M. W. Seeliger, “Noninvasive, in vivo assessment of mouse retinal structure using optical coherence tomography,” PLoS ONE4(10), e7507 (2009).
[CrossRef] [PubMed]

Burns, S. A.

Z. Y. Zhong, H. X. Song, T. Y. P. Chui, B. L. Petrig, and S. A. Burns, “Noninvasive measurements and analysis of blood velocity profiles in human retinal vessels,” Invest. Ophthalmol. Vis. Sci.52(7), 4151–4157 (2011).
[CrossRef] [PubMed]

Z. Y. Zhong, B. L. Petrig, X. F. Qi, and S. A. Burns, “In vivo measurement of erythrocyte velocity and retinal blood flow using adaptive optics scanning laser ophthalmoscopy,” Opt. Express16(17), 12746–12756 (2008).
[PubMed]

S. A. Burns, Z. Zhangyi, T. Y. P. Chui, H. Song, A. E. Elsner, and V. E. Malinovsky, “Imaging the inner retina using adaptive optics,” nvest. Ophthalmol. Vis. Sci.49, 4512–9999 (2008).

D. P. Biss, D. Sumorok, S. A. Burns, R. H. Webb, Y. Zhou, T. G. Bifano, D. Côté, I. Veilleux, P. Zamiri, and C. P. Lin, “In vivo fluorescent imaging of the mouse retina using adaptive optics,” Opt. Lett.32(6), 659–661 (2007).
[CrossRef] [PubMed]

Bursell, S. E.

V. J. Srinivasan, T. H. Ko, M. Wojtkowski, M. Carvalho, A. Clermont, S. E. Bursell, Q. H. Song, J. Lem, J. S. Duker, J. S. Schuman, and J. G. Fujimoto, “Noninvasive volumetric imaging and morphometry of the rodent retina with high-speed, ultrahigh-resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.47(12), 5522–5528 (2006).
[CrossRef] [PubMed]

Carroll, J.

Carvalho, M.

V. J. Srinivasan, T. H. Ko, M. Wojtkowski, M. Carvalho, A. Clermont, S. E. Bursell, Q. H. Song, J. Lem, J. S. Duker, J. S. Schuman, and J. G. Fujimoto, “Noninvasive volumetric imaging and morphometry of the rodent retina with high-speed, ultrahigh-resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.47(12), 5522–5528 (2006).
[CrossRef] [PubMed]

Chader, G. J.

G. J. Chader, “Animal models in research on retinal degenerations: past progress and future hope,” Vision Res.42(4), 393–399 (2002).
[CrossRef] [PubMed]

Chalupa, L. M.

J. Coombs, D. van der List, G. Y. Wang, and L. M. Chalupa, “Morphological properties of mouse retinal ganglion cells,” Neuroscience140(1), 123–136 (2006).
[CrossRef] [PubMed]

Chan, F.

F. Chan, A. Bradley, T. G. Wensel, and J. H. Wilson, “Knock-in human rhodopsin-GFP fusions as mouse models for human disease and targets for gene therapy,” Proc. Natl. Acad. Sci. U.S.A.101(24), 9109–9114 (2004).
[CrossRef] [PubMed]

Chang, B.

B. Chang, N. L. Hawes, R. E. Hurd, J. Wang, D. Howell, M. T. Davisson, T. H. Roderick, S. Nusinowitz, and J. R. Heckenlively, “Mouse models of ocular diseases,” Vis. Neurosci.22(05), 587–593 (2005).
[CrossRef] [PubMed]

Charbel Issa, P.

P. Charbel Issa, M. S. Singh, D. M. Lipinski, N. V. Chong, F. C. Delori, A. R. Barnard, and R. E. Maclaren, “Optimization of in vivo confocal autofluorescence imaging of the ocular fundus in mice and its application to models of human retinal degeneration,” Invest. Ophthalmol. Vis. Sci.53, iovs.11-8767 (2011).
[PubMed]

Chen, L. J.

C. K. S. Leung, R. N. Weinreb, Z. W. Li, S. Liu, J. D. Lindsey, N. Choi, L. Liu, C. Y. L. Cheung, C. Ye, K. L. Qiu, L. J. Chen, W. H. Yung, J. G. Crowston, M. L. Pu, K. F. So, C. P. Pang, and D. S. C. Lam, “Long-term in vivo imaging and measurement of dendritic shrinkage of retinal ganglion cells,” Invest. Ophthalmol. Vis. Sci.52(3), 1539–1547 (2011).
[CrossRef] [PubMed]

Chen, Y. N.

H. Murata, M. Aihara, Y. N. Chen, T. Ota, J. Numaga, and M. Araie, “Imaging mouse retinal ganglion cells and their loss in vivo by a fundus camera in the normal and ischemia-reperfusion model,” Invest. Ophthalmol. Vis. Sci.49(12), 5546–5552 (2008).
[CrossRef] [PubMed]

Cheung, C. Y. L.

C. K. S. Leung, R. N. Weinreb, Z. W. Li, S. Liu, J. D. Lindsey, N. Choi, L. Liu, C. Y. L. Cheung, C. Ye, K. L. Qiu, L. J. Chen, W. H. Yung, J. G. Crowston, M. L. Pu, K. F. So, C. P. Pang, and D. S. C. Lam, “Long-term in vivo imaging and measurement of dendritic shrinkage of retinal ganglion cells,” Invest. Ophthalmol. Vis. Sci.52(3), 1539–1547 (2011).
[CrossRef] [PubMed]

Choi, N.

C. K. S. Leung, R. N. Weinreb, Z. W. Li, S. Liu, J. D. Lindsey, N. Choi, L. Liu, C. Y. L. Cheung, C. Ye, K. L. Qiu, L. J. Chen, W. H. Yung, J. G. Crowston, M. L. Pu, K. F. So, C. P. Pang, and D. S. C. Lam, “Long-term in vivo imaging and measurement of dendritic shrinkage of retinal ganglion cells,” Invest. Ophthalmol. Vis. Sci.52(3), 1539–1547 (2011).
[CrossRef] [PubMed]

Chong, N. V.

P. Charbel Issa, M. S. Singh, D. M. Lipinski, N. V. Chong, F. C. Delori, A. R. Barnard, and R. E. Maclaren, “Optimization of in vivo confocal autofluorescence imaging of the ocular fundus in mice and its application to models of human retinal degeneration,” Invest. Ophthalmol. Vis. Sci.53, iovs.11-8767 (2011).
[PubMed]

Chui, T. Y. P.

Z. Y. Zhong, H. X. Song, T. Y. P. Chui, B. L. Petrig, and S. A. Burns, “Noninvasive measurements and analysis of blood velocity profiles in human retinal vessels,” Invest. Ophthalmol. Vis. Sci.52(7), 4151–4157 (2011).
[CrossRef] [PubMed]

S. A. Burns, Z. Zhangyi, T. Y. P. Chui, H. Song, A. E. Elsner, and V. E. Malinovsky, “Imaging the inner retina using adaptive optics,” nvest. Ophthalmol. Vis. Sci.49, 4512–9999 (2008).

Cioffi, G. A.

L. Wang, J. Dong, G. Cull, B. Fortune, and G. A. Cioffi, “Varicosities of intraretinal ganglion cell axons in human and nonhuman primates,” Invest. Ophthalmol. Vis. Sci.44(1), 2–9 (2003).
[CrossRef] [PubMed]

Clark, A. F.

R. T. Libby, M. G. Anderson, I. H. Pang, Z. H. Robinson, O. V. Savinova, I. M. Cosma, A. Snow, L. A. Wilson, R. S. Smith, A. F. Clark, and S. W. John, “Inherited glaucoma in DBA/2J mice: pertinent disease features for studying the neurodegeneration,” Vis. Neurosci.22(05), 637–648 (2005).
[CrossRef] [PubMed]

Clermont, A.

V. J. Srinivasan, T. H. Ko, M. Wojtkowski, M. Carvalho, A. Clermont, S. E. Bursell, Q. H. Song, J. Lem, J. S. Duker, J. S. Schuman, and J. G. Fujimoto, “Noninvasive volumetric imaging and morphometry of the rodent retina with high-speed, ultrahigh-resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.47(12), 5522–5528 (2006).
[CrossRef] [PubMed]

Coombs, J.

J. Coombs, D. van der List, G. Y. Wang, and L. M. Chalupa, “Morphological properties of mouse retinal ganglion cells,” Neuroscience140(1), 123–136 (2006).
[CrossRef] [PubMed]

Cooper, R. F.

Cordeiro, M. F.

A. Maass, P. L. von Leithner, V. Luong, L. Guo, T. E. Salt, F. W. Fitzke, and M. F. Cordeiro, “Assessment of rat and mouse RGC apoptosis imaging in vivo with different scanning laser ophthalmoscopes,” Curr. Eye Res.32(10), 851–861 (2007).
[CrossRef] [PubMed]

Cosma, I. M.

R. T. Libby, M. G. Anderson, I. H. Pang, Z. H. Robinson, O. V. Savinova, I. M. Cosma, A. Snow, L. A. Wilson, R. S. Smith, A. F. Clark, and S. W. John, “Inherited glaucoma in DBA/2J mice: pertinent disease features for studying the neurodegeneration,” Vis. Neurosci.22(05), 637–648 (2005).
[CrossRef] [PubMed]

Côté, D.

Crowston, J. G.

C. K. S. Leung, R. N. Weinreb, Z. W. Li, S. Liu, J. D. Lindsey, N. Choi, L. Liu, C. Y. L. Cheung, C. Ye, K. L. Qiu, L. J. Chen, W. H. Yung, J. G. Crowston, M. L. Pu, K. F. So, C. P. Pang, and D. S. C. Lam, “Long-term in vivo imaging and measurement of dendritic shrinkage of retinal ganglion cells,” Invest. Ophthalmol. Vis. Sci.52(3), 1539–1547 (2011).
[CrossRef] [PubMed]

Cull, G.

L. Wang, J. Dong, G. Cull, B. Fortune, and G. A. Cioffi, “Varicosities of intraretinal ganglion cell axons in human and nonhuman primates,” Invest. Ophthalmol. Vis. Sci.44(1), 2–9 (2003).
[CrossRef] [PubMed]

Cuthbertson, R. A.

R. A. Cuthbertson and T. E. Mandel, “Anatomy of the mouse retina. Endothelial cell-pericyte ratio and capillary distribution,” Invest. Ophthalmol. Vis. Sci.27(11), 1659–1664 (1986).
[PubMed]

Dangel, S.

M. W. Seeliger, S. C. Beck, N. Pereyra-Muñoz, S. Dangel, J. Y. Tsai, U. F. Luhmann, S. A. van de Pavert, J. Wijnholds, M. Samardzija, A. Wenzel, E. Zrenner, K. Narfström, E. Fahl, N. Tanimoto, N. Acar, and F. Tonagel, “In vivo confocal imaging of the retina in animal models using scanning laser ophthalmoscopy,” Vision Res.45(28), 3512–3519 (2005).
[CrossRef] [PubMed]

Davisson, M. T.

B. Chang, N. L. Hawes, R. E. Hurd, J. Wang, D. Howell, M. T. Davisson, T. H. Roderick, S. Nusinowitz, and J. R. Heckenlively, “Mouse models of ocular diseases,” Vis. Neurosci.22(05), 587–593 (2005).
[CrossRef] [PubMed]

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]

de la Villa, P.

J. Tejedor and P. de la Villa, “Refractive changes induced by form deprivation in the mouse eye,” Invest. Ophthalmol. Vis. Sci.44(1), 32–36 (2003).
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Delori, F. C.

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Y. Geng, K. P. Greenberg, R. Wolfe, D. C. Gray, J. J. Hunter, A. Dubra, J. G. Flannery, D. R. Williams, and J. Porter, “In vivo imaging of microscopic structures in the rat retina,” Invest. Ophthalmol. Vis. Sci.50(12), 5872–5879 (2009).
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Figures (15)

Fig. 1
Fig. 1

Schematic of the mouse eye fluorescence AOSLO. LD: fiber coupled laser diode. SLD: fiber coupled Super Luminescent Diode. PMT: photomultiplier tube. SHWS: Shack-Hartmann wavefront sensor. F: band pass filter. 90/10: 90/10 beam splitter. HS: horizontal scanner. VS: vertical scanner. M1-9: Concave spherical mirrors.

Fig. 2
Fig. 2

Spot diagrams for 27 configurations evaluated at the retinal plane, over a 3° × 3° FOV for a vergence range of 60 D in the mouse AOSLO optical design. Configurations are grouped by vergences, and all configurations are diffraction limited for 450 nm of wavelength. The radius of Airy disk (Black circle) is 0.59 µm.

Fig. 3
Fig. 3

Spot diagrams for the 4 pupil planes of the mouse AOSLO at 450 nm over a 3° × 3° FOV, for an on-axis point object at the SHWS pupil plane. Different scanning configurations are coded by color. Black circle represents the Airy disk.

Fig. 4
Fig. 4

Typical SHWS spot patterns before the spots are focused on the wavefront sensing source or AO correction (a), and after AO correction (b). The spots are brighter and sharper after AO correction. These SHWS spot patterns are taken at a scanning field of 5° × 5°. Each wavefront sensor spot is sampled by 16 × 16 pixels on the CCD camera. The width of both images is approximately 465 pixels.

Fig. 5
Fig. 5

In vivo reflectance image of the NFL close to the optic disk in the mouse eye. This image was an average of 100 frames. Confocal pinhole diameter was 2.1 Airy disks. Arrows: examples of nerve fiber bundles. Arrowhead: example of capillaries. Image was contrast stretched for display purposes. Scale bar: 20 µm.

Fig. 6
Fig. 6

In vivo reflectance image montage of the NFL in the mouse eye, showing a large blood vessel in the center, capillaries, and nerve fiber bundles. This location was over 15 degrees away from the optic disk. Size of this image was 553 µm × 230 µm, or 16.3° × 6.8°. Each individual image was an average of 50 frames. Confocal pinhole diameter was 2.1 Airy disks. Scale bar: 20 µm. Image was contrast stretched for display purposes only.

Fig. 7
Fig. 7

In vivo reflectance capillary images in the mouse retina. All images are taken at the same retinal location. (a), (b), (d) Capillary images at different depths. Each image is a registered average of 50 individual frames. (c) Standard deviation/motion contrast image corresponding to the depth of image (a). Arrows and arrowhead: dark regions and microscopic bright point structures within the intermediate capillary layer. Confocal pinhole diameter was 2.1 Airy disks. All images were contrast stretched identically for display purposes. Scale bar: 20 µm.

Fig. 8
Fig. 8

(a) Photoreceptors imaged in reflectance in the mouse eye. This image is an average of 120 frames. Scale bar: 10 µm. (b) Fourier spectrum of the photoreceptor image in (a), showing a concentration of energy at a fixed radius from the origin. The partial circle indicates the spatial frequency calculated using a 1.60 µm nearest neighbor distance. Confocal pinhole diameter was 2.1 Airy disks. Image (a) was contrast stretched for display purposes.

Fig. 9
Fig. 9

In vivo fluoresence images of a ganglion cell expressing YFP. (a-c) Individual images from three of the focuses, at focus steps of 11.6 μm. Each image at an individual focus step was a registered image average of 500 frames. (d) Maximum intensity projection image generated from 5 separate in vivo images taken at focus steps of 5.8 μm. Confocal pinhole diameter was 3.9 Airy disks. All images were contrast stretched identically to preserve their relative brightness. Scale bar: 20 µm.

Fig. 10
Fig. 10

In vivo imaging of the same fluorescent ganglion cells at times separated by one month. Image shown in (a) and (b) are taken one month apart. Both images are maximum intensity projection images generated from 10 separate in vivo images at individual focuses. Each image at an individual focus is a registered average of 750 frames. Confocal pinhole diameter was 1.9 Airy disks. Images were contrast stretched identically for display purposes. Scale bar: 20 µm.

Fig. 11
Fig. 11

Characterization of the in vivo resolution using an image stack of a fluorescent ganglion cell. (a) Maximum projection image for a focus stack. (b) One individual focus from the focus stack. Transverse cross section on a typical dendrite labeled in yellow is plotted as an example in (d). (c) An individual focus image 11.6 μm shallower than the focus in (b). Arrow indicates measurement position for a typical axial cross section shown in (e). (d) and (e) are the characterization of the in vivo transverse and axial resolution, respectively. Circle data points: in vivo measurement. Solid black line: spline fit to in vivo measurement data. Solid gray line: theoretical diffraction-limited axial PSF. Scale bar: 20 µm.

Fig. 12
Fig. 12

Direct comparison of in vivo and ex vivo mouse monostratified ganglion cell. In vivo image dimensions (degree to µm conversion calculated using paraxial eye model [28]) matched very well with ex vivo image dimensions. (a) Ex vivo histological image acquired using a 40x oil immersion confocal microscope with a 1.3 NA objective. (b) In vivo image in a mouse retina taken with AO correction over a 0.49 NA. The in vivo image was a maximum intensity projection image generated from 11 in vivo images taken at different depths. Ex vivo image was a maximum intensity projection image generated from an image stack of 51 images. Confocal pinhole size was 1 Airy disk for ex vivo, and 1.9 Airy disks for in vivo imaging. Scale bar: 20 μm.

Fig. 13
Fig. 13

Direct comparison of in vivo and ex vivo mouse bistratified ganglion cells. All imaging parameters used were the same as that used for the cell imaged in Fig. 12.

Fig. 14
Fig. 14

In vivo imaging of six more monostratified ganglion cells. Shadows from large blood vessels can be seen in images of cell 2, 4 and 6. Cells 5 and 6 are taken from transgenic mice with ganglion cells expressing YFP, and all other cells are labeled with retrograde viral vector. Images are contrast stretched for display purposes. Scale bar: 20 μm.

Fig. 15
Fig. 15

In vivo imaging of three more bistratified ganglion cells. The left column shows the maximum projection image of the cell; middle and right columns shows the dendrite stratifications at 2 different focuses. All images are contrast stretched for display purposes. Scale bar: 20 μm.

Tables (3)

Tables Icon

Table 1 Comparison of the mouse eye and human eye optics parameters*

Tables Icon

Table 2 In vivo classification of a few monostratified ganglion cells

Tables Icon

Table 3 Summary of in vivo classification of a few bistratified ganglion cells

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