Abstract

The structure and organization of the chicken retina has been investigated with an adaptive optics multiphoton imaging microscope in a backward configuration. Non-stained flat-mounted retinal tissues were imaged at different depths, from the retinal nerve fiber layer to the outer segment, by detecting the intrinsic nonlinear fluorescent signal. From the stacks of images corresponding to the different retinal layers, volume renderings of the entire retina were reconstructed. The density of photoreceptors and ganglion cells layer were directly estimated from the images as a function of the retinal eccentricity. The maximum anatomical resolving power at different retinal eccentricities was also calculated. This technique could be used for a better characterization of retinal alterations during myopia development, and may be useful for visualization of retinal pathologies and intoxication during pharmacological studies.

© 2011 OSA

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2011

J. M. Bueno, E. J. Gualda, and P. Artal, “Analysis of corneal stroma organization with wavefront optimized nonlinear microscopy,” Cornea 30(6), 692–701 (2011).
[CrossRef] [PubMed]

2010

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

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

Y. A. Kram, S. Mantey, and J. C. Corbo, “Avian cone photoreceptors tile the retina as five independent, self-organizing mosaics,” PLoS ONE 5(2), e8992 (2010).
[CrossRef] [PubMed]

2009

J. J. Mancuso, A. M. Larson, T. G. Wensel, and P. Saggau, “Multiphoton adaptation of a commercial low-cost confocal microscope for live tissue imaging,” J. Biomed. Opt. 14(3), 034048 (2009).
[CrossRef] [PubMed]

E. Diedrich and F. Schaeffel, “Spatial resolution, contrast sensitivity, and sensitivity to defocus of chicken retinal ganglion cells in vitro,” Vis. Neurosci. 26(5-6), 467–476 (2009).
[CrossRef] [PubMed]

J. J. Hunter, M. C. W. Campbell, M. L. Kisilak, and E. L. Irving, “Blur on the retina due to higher-order aberrations: comparison of eye growth models to experimental data,” J. Vis. 9(6), 12, 1–20 (2009).
[CrossRef] [PubMed]

S. Mar, M. C. Martinez-Garcia, J. T. Blanco-Mezquita, R. M. Torres, and J. Merayo-Lloves, “Measurement of correlation between transmission and scattering during wound healing in hen corneas,” J. Mod. Opt. 56(8), 1014–1021 (2009).
[CrossRef]

2008

C. Boote, S. Hayes, S. Jones, A. J. Quantock, P. M. Hocking, C. F. Inglehearn, M. Ali, and K. M. Meek, “Collagen organization in the chicken cornea and structural alterations in the retinopathy, globe enlarged (rge) phenotype--an X-ray diffraction study,” J. Struct. Biol. 161(1), 1–8 (2008).
[CrossRef] [PubMed]

C. J. Wolsley, K. J. Saunders, G. Silvestri, and R. S. Anderson, “Investigation of changes in the myopic retina using multifocal electroretinograms, optical coherence tomography and peripheral resolution acuity,” Vision Res. 48(14), 1554–1561 (2008).
[CrossRef] [PubMed]

M. L. Kisilak, J. J. Hunter, L. Huang, M. C. W. Campbell, and E. L. Irving, “In chicks wearing high powered negative lenses, spherical refraction is compensated and oblique astigmatism is induced,” J. Mod. Opt. 55(4), 611–623 (2008).
[CrossRef]

B. G. Wang, A. Eitner, J. Lindenau, and K. J. Halbhuber, “High-resolution two-photon excitation microscopy of ocular tissues in porcine eye,” Lasers Surg. Med. 40(4), 247–256 (2008).
[CrossRef] [PubMed]

2007

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

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

M. L. Rahman, M. Aoyama, and S. Sugita, “Number and density of retinal photoreceptor cells with emphasis on oil droplet distribution in the Mallard Duck (Anas platyrhynchos var. domesticus),” J. Anim. Sci. 78(6), 639–649 (2007).
[CrossRef]

M. L. Rahman, M. Aoyama, and S. Sugita, “Topography of retinal photoreceptor cells in the Jungle Crow (Corvus macrorhynchos) with emphasis on the distribution of oil droplets,” Ornitholog. Sci. 6(1), 29–38 (2007).
[CrossRef]

2006

M. M. Ghim and W. Hodos, “Spatial contrast sensitivity of birds,” J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 192(5), 523–534 (2006).
[CrossRef] [PubMed]

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

N. S. Hart, T. J. Lisney, and S. P. Collin, “Cone photoreceptor oil droplet pigmentation is affected by ambient light intensity,” J. Exp. Biol. 209(23), 4776–4787 (2006).
[CrossRef] [PubMed]

M. S. Wai, D. E. Lorke, L. S. Kung, and D. T. Yew, “Morphogenesis of the different types of photoreceptors of the chicken (Gallus domesticus) retina and the effect of amblyopia in neonatal chicken,” Microsc. Res. Tech. 69(2), 99–107 (2006).
[CrossRef] [PubMed]

M. C. Martínez-García, J. Merayo-Llovés, T. Blanco-Mezquita, and S. Mar-Sardaña, “Wound healing following refractive surgery in hens,” Exp. Eye Res. 83(4), 728–735 (2006).
[CrossRef] [PubMed]

2005

R. M. Torres, J. Merayo-Lloves, J. T. Blanco-Mezquita, C. P. Günther, G. Rodríguez, R. Gutiérez, and C. Martínez-García, “Experimental model of laser in situ keratomileusis in hens,” J. Refract. Surg. 21(4), 392–398 (2005).
[PubMed]

C. H. 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

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

J. Naito and Y. Chen, “Morphological features of chick retinal ganglion cells,” Anat. Sci. Int. 79(4), 213–225 (2004).
[CrossRef] [PubMed]

W. C. Fowler, D. H. Chang, B. C. Roberts, E. L. Zarovnaya, and A. D. Proia, “A new paradigm for corneal wound healing research: the white leghorn chicken (Gallus gallus domesticus),” Curr. Eye Res. 28(4), 241–250 (2004).
[CrossRef] [PubMed]

J. Wallman and J. Winawer, “Homeostasis of eye growth and the question of myopia,” Neuron 43(4), 447–468 (2004).
[CrossRef] [PubMed]

2002

S. H. 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]

2001

N. S. Hart, “The visual ecology of avian photoreceptors,” Prog. Retin. Eye Res. 20(5), 675–703 (2001).
[CrossRef] [PubMed]

2000

A. J. Fischer and T. A. Reh, “Identification of a proliferating marginal zone of retinal progenitors in postnatal chickens,” Dev. Biol. 220(2), 197–210 (2000).
[CrossRef] [PubMed]

1999

Y. Chen and J. Naito, “A quantitative analysis of cells in the ganglion cell layer of the chick retina,” Brain Behav. Evol. 53(2), 75–86 (1999).
[CrossRef] [PubMed]

L. Galli-Resta, E. Novelli, Z. Kryger, G. H. Jacobs, and B. E. Reese, “Modelling the mosaic organization of rod and cone photoreceptors with a minimal-spacing rule,” Eur. J. Neurosci. 11(4), 1461–1469 (1999).
[CrossRef] [PubMed]

M. J. Chandler, P. J. Smith, D. A. Samuelson, and E. O. MacKay, “Photoreceptor density of the domestic pig retina,” Vet. Ophthalmol. 2(3), 179–184 (1999).
[CrossRef] [PubMed]

1998

K. L. Schmid and C. F. Wildsoet, “Assessment of visual acuity and contrast sensitivity in the chick using an optokinetic nystagmus paradigm,” Vision Res. 38(17), 2629–2634 (1998).
[CrossRef] [PubMed]

1997

S. Y. Kim, N. Ondhia, D. Vidgen, L. Malaval, M. Ringuette, and V. I. Kalnins, “Spatiotemporal distribution of SPARC/osteonectin in developing and mature chicken retina,” Exp. Eye Res. 65(5), 681–689 (1997).
[CrossRef] [PubMed]

Y. Guo, P. P. Ho, H. Savage, D. Harris, P. Sacks, S. Schantz, F. Liu, N. Zhadin, and R. R. Alfano, “Second-harmonic tomography of tissues,” Opt. Lett. 22(17), 1323–1325 (1997).
[CrossRef] [PubMed]

1996

A. K. Goodchild, K. K. Ghosh, and P. R. Martin, “Comparison of photoreceptor spatial density and ganglion cell morphology in the retina of human, macaque monkey, cat, and the marmoset Callithrix jacchus,” J. Comp. Neurol. 366(1), 55–75 (1996).
[CrossRef] [PubMed]

D. Troilo, M. Xiong, J. C. Crowley, and B. L. Finlay, “Factors controlling the dendritic arborization of retinal ganglion cells,” Vis. Neurosci. 13(04), 721–733 (1996).
[CrossRef] [PubMed]

1994

M. Bartmann and F. Schaeffel, “A simple mechanism for emmetropization without cues from accommodation or colour,” Vision Res. 34(7), 873–876 (1994).
[CrossRef] [PubMed]

1992

C. A. Curcio and K. R. Sloan, “Packing geometry of human cone photoreceptors: variation with eccentricity and evidence for local anisotropy,” Vis. Neurosci. 9(02), 169–180 (1992).
[CrossRef] [PubMed]

1991

F. Schaeffel, B. Rohrer, E. Zrenner, and T. Lemmer, “Diurnal control of rod function in the chicken,” Vis. Neurosci. 6(06), 641–653 (1991).
[CrossRef] [PubMed]

V. Porciatti, W. Hodos, G. Signorini, and F. Bramanti, “Electroretinographic changes in aged pigeons,” Vision Res. 31(4), 661–668 (1991).
[CrossRef] [PubMed]

1990

C. A. Curcio, K. R. Sloan, R. E. Kalina, and A. E. Hendrickson, “Human photoreceptor topography,” J. Comp. Neurol. 292(4), 497–523 (1990).
[CrossRef] [PubMed]

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

R. N. Weinreb, A. W. Dreher, A. Coleman, H. Quigley, B. Shaw, and K. Reiter, “Histopathologic validation of Fourier-ellipsometry measurements of retinal nerve fiber layer thickness,” Arch. Ophthalmol. 108(4), 557–560 (1990).
[PubMed]

1989

1988

F. Schaeffel and H. C. Howland, “Visual optics in normal and ametropic chickens,” Clin. Vis. Sci. 3, 83–89 (1988).

C. F. Wildsoet and J. D. Pettigrew, “Experimental myopia and anomalous eye growth-patterns unaffected by optic-nerve section in chickens: evidence for local-control of eye growth,” Clin. Vis. Sci. 3, 99–107 (1988).

F. Schaeffel, A. Glasser, and H. C. Howland, “Accommodation, refractive error and eye growth in chickens,” Vision Res. 28(5), 639–657 (1988).
[CrossRef] [PubMed]

1987

J. Wallman and J. I. Adams, “Developmental aspects of experimental myopia in chicks: susceptibility, recovery and relation to emmetropization,” Vision Res. 27(7), 1139–1163 (1987).
[CrossRef] [PubMed]

N. J. Coletta and D. R. Williams, “Psychophysical estimate of extrafoveal cone spacing,” J. Opt. Soc. Am. A 4(8), 1503–1513 (1987).
[CrossRef] [PubMed]

C. Straznicky and M. Chehade, “The formation of the area centralis of the retinal ganglion cell layer in the chick,” Development 100(3), 411–420 (1987).
[PubMed]

1986

F. Schaeffel, H. C. Howland, and L. Farkas, “Natural accommodation in the growing chicken,” Vision Res. 26(12), 1977–1993 (1986).
[CrossRef] [PubMed]

1985

L. Reymond, “Spatial visual acuity of the eagle Aquila audax: a behavioural, optical and anatomical investigation,” Vision Res. 25(10), 1477–1491 (1985).
[CrossRef] [PubMed]

1984

V. Budnik, J. Mpodozis, F. J. Varela, and H. R. Maturana, “Regional specialization of the quail retina: ganglion cell density and oil droplet distribution,” Neurosci. Lett. 51(1), 145–150 (1984).
[CrossRef] [PubMed]

1982

J. I. Yellott., “Spectral analysis of spatial sampling by photoreceptors: topological disorder prevents aliasing,” Vision Res. 22(9), 1205–1210 (1982).
[CrossRef] [PubMed]

1981

D. Ehrlich, “Regional specialization of the chick retina as revealed by the size and density of neurons in the ganglion cell layer,” J. Comp. Neurol. 195(4), 643–657 (1981).
[CrossRef] [PubMed]

R. Over and D. Moore, “Spatial acuity of the chicken,” Brain Res. 211(2), 424–426 (1981).
[CrossRef] [PubMed]

1977

J. K. Bowmaker, “The visual pigments, oil droplets and spectral sensitivity of the pigeon,” Vision Res. 17(10), 1129–1138 (1977).
[CrossRef] [PubMed]

1971

R. L. Trelstad and A. J. Coulombre, “Morphogenesis of the collagenous stroma in the chick cornea,” J. Cell Biol. 50(3), 840–858 (1971).
[CrossRef] [PubMed]

1969

R. L. Binggeli and W. J. Paule, “The pigeon retina: quantitative aspects of the optic nerve and ganglion cell layer,” J. Comp. Neurol. 137(1), 1–18 (1969).
[CrossRef] [PubMed]

1918

G. Davis Buckner, R. H. Wilkins, and J. H. Kastle, “The normal growth of White Leghorn chickens,” Am. J. Physiol. 47, 393–398 (1918).

Adams, J. I.

J. Wallman and J. I. Adams, “Developmental aspects of experimental myopia in chicks: susceptibility, recovery and relation to emmetropization,” Vision Res. 27(7), 1139–1163 (1987).
[CrossRef] [PubMed]

Agopov, M.

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

Alfano, R. R.

Ali, M.

C. Boote, S. Hayes, S. Jones, A. J. Quantock, P. M. Hocking, C. F. Inglehearn, M. Ali, and K. M. Meek, “Collagen organization in the chicken cornea and structural alterations in the retinopathy, globe enlarged (rge) phenotype--an X-ray diffraction study,” J. Struct. Biol. 161(1), 1–8 (2008).
[CrossRef] [PubMed]

Anderson, R. S.

C. J. Wolsley, K. J. Saunders, G. Silvestri, and R. S. Anderson, “Investigation of changes in the myopic retina using multifocal electroretinograms, optical coherence tomography and peripheral resolution acuity,” Vision Res. 48(14), 1554–1561 (2008).
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Aoyama, M.

M. L. Rahman, M. Aoyama, and S. Sugita, “Number and density of retinal photoreceptor cells with emphasis on oil droplet distribution in the Mallard Duck (Anas platyrhynchos var. domesticus),” J. Anim. Sci. 78(6), 639–649 (2007).
[CrossRef]

M. L. Rahman, M. Aoyama, and S. Sugita, “Topography of retinal photoreceptor cells in the Jungle Crow (Corvus macrorhynchos) with emphasis on the distribution of oil droplets,” Ornitholog. Sci. 6(1), 29–38 (2007).
[CrossRef]

Artal, P.

J. M. Bueno, E. J. Gualda, and P. Artal, “Analysis of corneal stroma organization with wavefront optimized nonlinear microscopy,” Cornea 30(6), 692–701 (2011).
[CrossRef] [PubMed]

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

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

P. Artal and R. Navarro, “High-resolution imaging of the living human fovea: measurement of the intercenter cone distance by speckle interferometry,” Opt. Lett. 14(20), 1098–1100 (1989).
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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).
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Barrie, D. L.

J. G. Sivak, D. L. Barrie, and J. A. Weerheim, “Bilateral experimental myopia in chicks,” Optom. Vis. Sci. 66(12), 854–858 (1989).
[CrossRef] [PubMed]

Bartmann, M.

M. Bartmann and F. Schaeffel, “A simple mechanism for emmetropization without cues from accommodation or colour,” Vision Res. 34(7), 873–876 (1994).
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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]

Becker, W.

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

Bergmann, A.

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

Bille, J. F.

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

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

Bindewald-Wittich, A.

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

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

Binggeli, R. L.

R. L. Binggeli and W. J. Paule, “The pigeon retina: quantitative aspects of the optic nerve and ganglion cell layer,” J. Comp. Neurol. 137(1), 1–18 (1969).
[CrossRef] [PubMed]

Birckner, E.

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

Blanco-Mezquita, J. T.

S. Mar, M. C. Martinez-Garcia, J. T. Blanco-Mezquita, R. M. Torres, and J. Merayo-Lloves, “Measurement of correlation between transmission and scattering during wound healing in hen corneas,” J. Mod. Opt. 56(8), 1014–1021 (2009).
[CrossRef]

R. M. Torres, J. Merayo-Lloves, J. T. Blanco-Mezquita, C. P. Günther, G. Rodríguez, R. Gutiérez, and C. Martínez-García, “Experimental model of laser in situ keratomileusis in hens,” J. Refract. Surg. 21(4), 392–398 (2005).
[PubMed]

Blanco-Mezquita, T.

M. C. Martínez-García, J. Merayo-Llovés, T. Blanco-Mezquita, and S. Mar-Sardaña, “Wound healing following refractive surgery in hens,” Exp. Eye Res. 83(4), 728–735 (2006).
[CrossRef] [PubMed]

Boote, C.

C. Boote, S. Hayes, S. Jones, A. J. Quantock, P. M. Hocking, C. F. Inglehearn, M. Ali, and K. M. Meek, “Collagen organization in the chicken cornea and structural alterations in the retinopathy, globe enlarged (rge) phenotype--an X-ray diffraction study,” J. Struct. Biol. 161(1), 1–8 (2008).
[CrossRef] [PubMed]

Bowmaker, J. K.

J. K. Bowmaker, “The visual pigments, oil droplets and spectral sensitivity of the pigeon,” Vision Res. 17(10), 1129–1138 (1977).
[CrossRef] [PubMed]

Bramanti, F.

V. Porciatti, W. Hodos, G. Signorini, and F. Bramanti, “Electroretinographic changes in aged pigeons,” Vision Res. 31(4), 661–668 (1991).
[CrossRef] [PubMed]

Budnik, V.

V. Budnik, J. Mpodozis, F. J. Varela, and H. R. Maturana, “Regional specialization of the quail retina: ganglion cell density and oil droplet distribution,” Neurosci. Lett. 51(1), 145–150 (1984).
[CrossRef] [PubMed]

Bueno, J. M.

J. M. Bueno, E. J. Gualda, and P. Artal, “Analysis of corneal stroma organization with wavefront optimized nonlinear microscopy,” Cornea 30(6), 692–701 (2011).
[CrossRef] [PubMed]

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

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

Campbell, M. C. W.

J. J. Hunter, M. C. W. Campbell, M. L. Kisilak, and E. L. Irving, “Blur on the retina due to higher-order aberrations: comparison of eye growth models to experimental data,” J. Vis. 9(6), 12, 1–20 (2009).
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M. L. Kisilak, J. J. Hunter, L. Huang, M. C. W. Campbell, and E. L. Irving, “In chicks wearing high powered negative lenses, spherical refraction is compensated and oblique astigmatism is induced,” J. Mod. Opt. 55(4), 611–623 (2008).
[CrossRef]

Chandler, M. J.

M. J. Chandler, P. J. Smith, D. A. Samuelson, and E. O. MacKay, “Photoreceptor density of the domestic pig retina,” Vet. Ophthalmol. 2(3), 179–184 (1999).
[CrossRef] [PubMed]

Chang, D. H.

W. C. Fowler, D. H. Chang, B. C. Roberts, E. L. Zarovnaya, and A. D. Proia, “A new paradigm for corneal wound healing research: the white leghorn chicken (Gallus gallus domesticus),” Curr. Eye Res. 28(4), 241–250 (2004).
[CrossRef] [PubMed]

Chehade, M.

C. Straznicky and M. Chehade, “The formation of the area centralis of the retinal ganglion cell layer in the chick,” Development 100(3), 411–420 (1987).
[PubMed]

Chen, C. H.

C. H. 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, Y.

J. Naito and Y. Chen, “Morphological features of chick retinal ganglion cells,” Anat. Sci. Int. 79(4), 213–225 (2004).
[CrossRef] [PubMed]

Y. Chen and J. Naito, “A quantitative analysis of cells in the ganglion cell layer of the chick retina,” Brain Behav. Evol. 53(2), 75–86 (1999).
[CrossRef] [PubMed]

Coleman, A.

R. N. Weinreb, A. W. Dreher, A. Coleman, H. Quigley, B. Shaw, and K. Reiter, “Histopathologic validation of Fourier-ellipsometry measurements of retinal nerve fiber layer thickness,” Arch. Ophthalmol. 108(4), 557–560 (1990).
[PubMed]

Coletta, N. J.

Collin, S. P.

N. S. Hart, T. J. Lisney, and S. P. Collin, “Cone photoreceptor oil droplet pigmentation is affected by ambient light intensity,” J. Exp. Biol. 209(23), 4776–4787 (2006).
[CrossRef] [PubMed]

Corbo, J. C.

Y. A. Kram, S. Mantey, and J. C. Corbo, “Avian cone photoreceptors tile the retina as five independent, self-organizing mosaics,” PLoS ONE 5(2), e8992 (2010).
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Cornwall, M. C.

C. H. 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]

Coulombre, A. J.

R. L. Trelstad and A. J. Coulombre, “Morphogenesis of the collagenous stroma in the chick cornea,” J. Cell Biol. 50(3), 840–858 (1971).
[CrossRef] [PubMed]

Crouch, R. K.

C. H. 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]

Crowley, J. C.

D. Troilo, M. Xiong, J. C. Crowley, and B. L. Finlay, “Factors controlling the dendritic arborization of retinal ganglion cells,” Vis. Neurosci. 13(04), 721–733 (1996).
[CrossRef] [PubMed]

Curcio, C. A.

C. A. Curcio and K. R. Sloan, “Packing geometry of human cone photoreceptors: variation with eccentricity and evidence for local anisotropy,” Vis. Neurosci. 9(02), 169–180 (1992).
[CrossRef] [PubMed]

C. A. Curcio, K. R. Sloan, R. E. Kalina, and A. E. Hendrickson, “Human photoreceptor topography,” J. Comp. Neurol. 292(4), 497–523 (1990).
[CrossRef] [PubMed]

Davis Buckner, G.

G. Davis Buckner, R. H. Wilkins, and J. H. Kastle, “The normal growth of White Leghorn chickens,” Am. J. Physiol. 47, 393–398 (1918).

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]

Diedrich, E.

E. Diedrich and F. Schaeffel, “Spatial resolution, contrast sensitivity, and sensitivity to defocus of chicken retinal ganglion cells in vitro,” Vis. Neurosci. 26(5-6), 467–476 (2009).
[CrossRef] [PubMed]

Dreher, A. W.

R. N. Weinreb, A. W. Dreher, A. Coleman, H. Quigley, B. Shaw, and K. Reiter, “Histopathologic validation of Fourier-ellipsometry measurements of retinal nerve fiber layer thickness,” Arch. Ophthalmol. 108(4), 557–560 (1990).
[PubMed]

Ehrlich, D.

D. Ehrlich, “Regional specialization of the chick retina as revealed by the size and density of neurons in the ganglion cell layer,” J. Comp. Neurol. 195(4), 643–657 (1981).
[CrossRef] [PubMed]

Eitner, A.

B. G. Wang, A. Eitner, J. Lindenau, and K. J. Halbhuber, “High-resolution two-photon excitation microscopy of ocular tissues in porcine eye,” Lasers Surg. Med. 40(4), 247–256 (2008).
[CrossRef] [PubMed]

Farkas, L.

F. Schaeffel, H. C. Howland, and L. Farkas, “Natural accommodation in the growing chicken,” Vision Res. 26(12), 1977–1993 (1986).
[CrossRef] [PubMed]

Finlay, B. L.

D. Troilo, M. Xiong, J. C. Crowley, and B. L. Finlay, “Factors controlling the dendritic arborization of retinal ganglion cells,” Vis. Neurosci. 13(04), 721–733 (1996).
[CrossRef] [PubMed]

Fischer, A. J.

A. J. Fischer and T. A. Reh, “Identification of a proliferating marginal zone of retinal progenitors in postnatal chickens,” Dev. Biol. 220(2), 197–210 (2000).
[CrossRef] [PubMed]

Fowler, W. C.

W. C. Fowler, D. H. Chang, B. C. Roberts, E. L. Zarovnaya, and A. D. Proia, “A new paradigm for corneal wound healing research: the white leghorn chicken (Gallus gallus domesticus),” Curr. Eye Res. 28(4), 241–250 (2004).
[CrossRef] [PubMed]

Galli-Resta, L.

L. Galli-Resta, E. Novelli, Z. Kryger, G. H. Jacobs, and B. E. Reese, “Modelling the mosaic organization of rod and cone photoreceptors with a minimal-spacing rule,” Eur. J. Neurosci. 11(4), 1461–1469 (1999).
[CrossRef] [PubMed]

Ghim, M. M.

M. M. Ghim and W. Hodos, “Spatial contrast sensitivity of birds,” J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 192(5), 523–534 (2006).
[CrossRef] [PubMed]

Ghosh, K. K.

A. K. Goodchild, K. K. Ghosh, and P. R. Martin, “Comparison of photoreceptor spatial density and ganglion cell morphology in the retina of human, macaque monkey, cat, and the marmoset Callithrix jacchus,” J. Comp. Neurol. 366(1), 55–75 (1996).
[CrossRef] [PubMed]

Giese, G.

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

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

Glasser, A.

F. Schaeffel, A. Glasser, and H. C. Howland, “Accommodation, refractive error and eye growth in chickens,” Vision Res. 28(5), 639–657 (1988).
[CrossRef] [PubMed]

Goodchild, A. K.

A. K. Goodchild, K. K. Ghosh, and P. R. Martin, “Comparison of photoreceptor spatial density and ganglion cell morphology in the retina of human, macaque monkey, cat, and the marmoset Callithrix jacchus,” J. Comp. Neurol. 366(1), 55–75 (1996).
[CrossRef] [PubMed]

Gualda, E. J.

J. M. Bueno, E. J. Gualda, and P. Artal, “Analysis of corneal stroma organization with wavefront optimized nonlinear microscopy,” Cornea 30(6), 692–701 (2011).
[CrossRef] [PubMed]

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

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

Günther, C. P.

R. M. Torres, J. Merayo-Lloves, J. T. Blanco-Mezquita, C. P. Günther, G. Rodríguez, R. Gutiérez, and C. Martínez-García, “Experimental model of laser in situ keratomileusis in hens,” J. Refract. Surg. 21(4), 392–398 (2005).
[PubMed]

Guo, Y.

Gutiérez, R.

R. M. Torres, J. Merayo-Lloves, J. T. Blanco-Mezquita, C. P. Günther, G. Rodríguez, R. Gutiérez, and C. Martínez-García, “Experimental model of laser in situ keratomileusis in hens,” J. Refract. Surg. 21(4), 392–398 (2005).
[PubMed]

Halbhuber, K. J.

B. G. Wang, A. Eitner, J. Lindenau, and K. J. Halbhuber, “High-resolution two-photon excitation microscopy of ocular tissues in porcine eye,” Lasers Surg. Med. 40(4), 247–256 (2008).
[CrossRef] [PubMed]

Hammer, M.

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

Han, M.

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

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

Harris, D.

Hart, N. S.

N. S. Hart, T. J. Lisney, and S. P. Collin, “Cone photoreceptor oil droplet pigmentation is affected by ambient light intensity,” J. Exp. Biol. 209(23), 4776–4787 (2006).
[CrossRef] [PubMed]

N. S. Hart, “The visual ecology of avian photoreceptors,” Prog. Retin. Eye Res. 20(5), 675–703 (2001).
[CrossRef] [PubMed]

Hayes, S.

C. Boote, S. Hayes, S. Jones, A. J. Quantock, P. M. Hocking, C. F. Inglehearn, M. Ali, and K. M. Meek, “Collagen organization in the chicken cornea and structural alterations in the retinopathy, globe enlarged (rge) phenotype--an X-ray diffraction study,” J. Struct. Biol. 161(1), 1–8 (2008).
[CrossRef] [PubMed]

Heikal, A. A.

S. H. 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]

Hendrickson, A. E.

C. A. Curcio, K. R. Sloan, R. E. Kalina, and A. E. Hendrickson, “Human photoreceptor topography,” J. Comp. Neurol. 292(4), 497–523 (1990).
[CrossRef] [PubMed]

Ho, P. P.

Hocking, P. M.

C. Boote, S. Hayes, S. Jones, A. J. Quantock, P. M. Hocking, C. F. Inglehearn, M. Ali, and K. M. Meek, “Collagen organization in the chicken cornea and structural alterations in the retinopathy, globe enlarged (rge) phenotype--an X-ray diffraction study,” J. Struct. Biol. 161(1), 1–8 (2008).
[CrossRef] [PubMed]

Hodos, W.

M. M. Ghim and W. Hodos, “Spatial contrast sensitivity of birds,” J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 192(5), 523–534 (2006).
[CrossRef] [PubMed]

V. Porciatti, W. Hodos, G. Signorini, and F. Bramanti, “Electroretinographic changes in aged pigeons,” Vision Res. 31(4), 661–668 (1991).
[CrossRef] [PubMed]

Holz, F. G.

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

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

Straznicky, C.

C. Straznicky and M. Chehade, “The formation of the area centralis of the retinal ganglion cell layer in the chick,” Development 100(3), 411–420 (1987).
[PubMed]

Strickler, J. H.

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

Sugita, S.

M. L. Rahman, M. Aoyama, and S. Sugita, “Topography of retinal photoreceptor cells in the Jungle Crow (Corvus macrorhynchos) with emphasis on the distribution of oil droplets,” Ornitholog. Sci. 6(1), 29–38 (2007).
[CrossRef]

M. L. Rahman, M. Aoyama, and S. Sugita, “Number and density of retinal photoreceptor cells with emphasis on oil droplet distribution in the Mallard Duck (Anas platyrhynchos var. domesticus),” J. Anim. Sci. 78(6), 639–649 (2007).
[CrossRef]

Sun, H.

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

Torres, R. M.

S. Mar, M. C. Martinez-Garcia, J. T. Blanco-Mezquita, R. M. Torres, and J. Merayo-Lloves, “Measurement of correlation between transmission and scattering during wound healing in hen corneas,” J. Mod. Opt. 56(8), 1014–1021 (2009).
[CrossRef]

R. M. Torres, J. Merayo-Lloves, J. T. Blanco-Mezquita, C. P. Günther, G. Rodríguez, R. Gutiérez, and C. Martínez-García, “Experimental model of laser in situ keratomileusis in hens,” J. Refract. Surg. 21(4), 392–398 (2005).
[PubMed]

Trelstad, R. L.

R. L. Trelstad and A. J. Coulombre, “Morphogenesis of the collagenous stroma in the chick cornea,” J. Cell Biol. 50(3), 840–858 (1971).
[CrossRef] [PubMed]

Troilo, D.

D. Troilo, M. Xiong, J. C. Crowley, and B. L. Finlay, “Factors controlling the dendritic arborization of retinal ganglion cells,” Vis. Neurosci. 13(04), 721–733 (1996).
[CrossRef] [PubMed]

Tsina, E.

C. H. 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]

Varela, F. J.

V. Budnik, J. Mpodozis, F. J. Varela, and H. R. Maturana, “Regional specialization of the quail retina: ganglion cell density and oil droplet distribution,” Neurosci. Lett. 51(1), 145–150 (1984).
[CrossRef] [PubMed]

Vidgen, D.

S. Y. Kim, N. Ondhia, D. Vidgen, L. Malaval, M. Ringuette, and V. I. Kalnins, “Spatiotemporal distribution of SPARC/osteonectin in developing and mature chicken retina,” Exp. Eye Res. 65(5), 681–689 (1997).
[CrossRef] [PubMed]

Vijayaraghavan, S.

C. H. 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]

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M. S. Wai, D. E. Lorke, L. S. Kung, and D. T. Yew, “Morphogenesis of the different types of photoreceptors of the chicken (Gallus domesticus) retina and the effect of amblyopia in neonatal chicken,” Microsc. Res. Tech. 69(2), 99–107 (2006).
[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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B. G. Wang, A. Eitner, J. Lindenau, and K. J. Halbhuber, “High-resolution two-photon excitation microscopy of ocular tissues in porcine eye,” Lasers Surg. Med. 40(4), 247–256 (2008).
[CrossRef] [PubMed]

Webb, W. W.

S. H. 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]

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

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J. G. Sivak, D. L. Barrie, and J. A. Weerheim, “Bilateral experimental myopia in chicks,” Optom. Vis. Sci. 66(12), 854–858 (1989).
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R. N. Weinreb, A. W. Dreher, A. Coleman, H. Quigley, B. Shaw, and K. Reiter, “Histopathologic validation of Fourier-ellipsometry measurements of retinal nerve fiber layer thickness,” Arch. Ophthalmol. 108(4), 557–560 (1990).
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J. J. Mancuso, A. M. Larson, T. G. Wensel, and P. Saggau, “Multiphoton adaptation of a commercial low-cost confocal microscope for live tissue imaging,” J. Biomed. Opt. 14(3), 034048 (2009).
[CrossRef] [PubMed]

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K. L. Schmid and C. F. Wildsoet, “Assessment of visual acuity and contrast sensitivity in the chick using an optokinetic nystagmus paradigm,” Vision Res. 38(17), 2629–2634 (1998).
[CrossRef] [PubMed]

C. F. Wildsoet and J. D. Pettigrew, “Experimental myopia and anomalous eye growth-patterns unaffected by optic-nerve section in chickens: evidence for local-control of eye growth,” Clin. Vis. Sci. 3, 99–107 (1988).

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G. Davis Buckner, R. H. Wilkins, and J. H. Kastle, “The normal growth of White Leghorn chickens,” Am. J. Physiol. 47, 393–398 (1918).

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Winawer, J.

J. Wallman and J. Winawer, “Homeostasis of eye growth and the question of myopia,” Neuron 43(4), 447–468 (2004).
[CrossRef] [PubMed]

Wolsley, C. J.

C. J. Wolsley, K. J. Saunders, G. Silvestri, and R. S. Anderson, “Investigation of changes in the myopic retina using multifocal electroretinograms, optical coherence tomography and peripheral resolution acuity,” Vision Res. 48(14), 1554–1561 (2008).
[CrossRef] [PubMed]

Xiong, M.

D. Troilo, M. Xiong, J. C. Crowley, and B. L. Finlay, “Factors controlling the dendritic arborization of retinal ganglion cells,” Vis. Neurosci. 13(04), 721–733 (1996).
[CrossRef] [PubMed]

Yellott, J. I.

J. I. Yellott., “Spectral analysis of spatial sampling by photoreceptors: topological disorder prevents aliasing,” Vision Res. 22(9), 1205–1210 (1982).
[CrossRef] [PubMed]

Yew, D. T.

M. S. Wai, D. E. Lorke, L. S. Kung, and D. T. Yew, “Morphogenesis of the different types of photoreceptors of the chicken (Gallus domesticus) retina and the effect of amblyopia in neonatal chicken,” Microsc. Res. Tech. 69(2), 99–107 (2006).
[CrossRef] [PubMed]

Yu, J. Y.

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

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

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W. C. Fowler, D. H. Chang, B. C. Roberts, E. L. Zarovnaya, and A. D. Proia, “A new paradigm for corneal wound healing research: the white leghorn chicken (Gallus gallus domesticus),” Curr. Eye Res. 28(4), 241–250 (2004).
[CrossRef] [PubMed]

Zhadin, N.

Zrenner, E.

F. Schaeffel, B. Rohrer, E. Zrenner, and T. Lemmer, “Diurnal control of rod function in the chicken,” Vis. Neurosci. 6(06), 641–653 (1991).
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Am. J. Physiol.

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R. N. Weinreb, A. W. Dreher, A. Coleman, H. Quigley, B. Shaw, and K. Reiter, “Histopathologic validation of Fourier-ellipsometry measurements of retinal nerve fiber layer thickness,” Arch. Ophthalmol. 108(4), 557–560 (1990).
[PubMed]

Biophys. J.

C. H. 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]

S. H. 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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F. Schaeffel and H. C. Howland, “Visual optics in normal and ametropic chickens,” Clin. Vis. Sci. 3, 83–89 (1988).

Cornea

J. M. Bueno, E. J. Gualda, and P. Artal, “Analysis of corneal stroma organization with wavefront optimized nonlinear microscopy,” Cornea 30(6), 692–701 (2011).
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Curr. Eye Res.

W. C. Fowler, D. H. Chang, B. C. Roberts, E. L. Zarovnaya, and A. D. Proia, “A new paradigm for corneal wound healing research: the white leghorn chicken (Gallus gallus domesticus),” Curr. Eye Res. 28(4), 241–250 (2004).
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Dev. Biol.

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Development

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[PubMed]

Eur. J. Neurosci.

L. Galli-Resta, E. Novelli, Z. Kryger, G. H. Jacobs, and B. E. Reese, “Modelling the mosaic organization of rod and cone photoreceptors with a minimal-spacing rule,” Eur. J. Neurosci. 11(4), 1461–1469 (1999).
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Exp. Eye Res.

S. Y. Kim, N. Ondhia, D. Vidgen, L. Malaval, M. Ringuette, and V. I. Kalnins, “Spatiotemporal distribution of SPARC/osteonectin in developing and mature chicken retina,” Exp. Eye Res. 65(5), 681–689 (1997).
[CrossRef] [PubMed]

M. C. Martínez-García, J. Merayo-Llovés, T. Blanco-Mezquita, and S. Mar-Sardaña, “Wound healing following refractive surgery in hens,” Exp. Eye Res. 83(4), 728–735 (2006).
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J. Anim. Sci.

M. L. Rahman, M. Aoyama, and S. Sugita, “Number and density of retinal photoreceptor cells with emphasis on oil droplet distribution in the Mallard Duck (Anas platyrhynchos var. domesticus),” J. Anim. Sci. 78(6), 639–649 (2007).
[CrossRef]

J. Biomed. Opt.

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

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

J. J. Mancuso, A. M. Larson, T. G. Wensel, and P. Saggau, “Multiphoton adaptation of a commercial low-cost confocal microscope for live tissue imaging,” J. Biomed. Opt. 14(3), 034048 (2009).
[CrossRef] [PubMed]

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

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

J. Cell Biol.

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R. L. Binggeli and W. J. Paule, “The pigeon retina: quantitative aspects of the optic nerve and ganglion cell layer,” J. Comp. Neurol. 137(1), 1–18 (1969).
[CrossRef] [PubMed]

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[CrossRef] [PubMed]

J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol.

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J. Mod. Opt.

S. Mar, M. C. Martinez-Garcia, J. T. Blanco-Mezquita, R. M. Torres, and J. Merayo-Lloves, “Measurement of correlation between transmission and scattering during wound healing in hen corneas,” J. Mod. Opt. 56(8), 1014–1021 (2009).
[CrossRef]

M. L. Kisilak, J. J. Hunter, L. Huang, M. C. W. Campbell, and E. L. Irving, “In chicks wearing high powered negative lenses, spherical refraction is compensated and oblique astigmatism is induced,” J. Mod. Opt. 55(4), 611–623 (2008).
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R. M. Torres, J. Merayo-Lloves, J. T. Blanco-Mezquita, C. P. Günther, G. Rodríguez, R. Gutiérez, and C. Martínez-García, “Experimental model of laser in situ keratomileusis in hens,” J. Refract. Surg. 21(4), 392–398 (2005).
[PubMed]

J. Struct. Biol.

C. Boote, S. Hayes, S. Jones, A. J. Quantock, P. M. Hocking, C. F. Inglehearn, M. Ali, and K. M. Meek, “Collagen organization in the chicken cornea and structural alterations in the retinopathy, globe enlarged (rge) phenotype--an X-ray diffraction study,” J. Struct. Biol. 161(1), 1–8 (2008).
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J. Vis.

J. J. Hunter, M. C. W. Campbell, M. L. Kisilak, and E. L. Irving, “Blur on the retina due to higher-order aberrations: comparison of eye growth models to experimental data,” J. Vis. 9(6), 12, 1–20 (2009).
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Lasers Surg. Med.

B. G. Wang, A. Eitner, J. Lindenau, and K. J. Halbhuber, “High-resolution two-photon excitation microscopy of ocular tissues in porcine eye,” Lasers Surg. Med. 40(4), 247–256 (2008).
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Microsc. Res. Tech.

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

M. S. Wai, D. E. Lorke, L. S. Kung, and D. T. Yew, “Morphogenesis of the different types of photoreceptors of the chicken (Gallus domesticus) retina and the effect of amblyopia in neonatal chicken,” Microsc. Res. Tech. 69(2), 99–107 (2006).
[CrossRef] [PubMed]

Neuron

J. Wallman and J. Winawer, “Homeostasis of eye growth and the question of myopia,” Neuron 43(4), 447–468 (2004).
[CrossRef] [PubMed]

Neurosci. Lett.

V. Budnik, J. Mpodozis, F. J. Varela, and H. R. Maturana, “Regional specialization of the quail retina: ganglion cell density and oil droplet distribution,” Neurosci. Lett. 51(1), 145–150 (1984).
[CrossRef] [PubMed]

Opt. Lett.

Optom. Vis. Sci.

J. G. Sivak, D. L. Barrie, and J. A. Weerheim, “Bilateral experimental myopia in chicks,” Optom. Vis. Sci. 66(12), 854–858 (1989).
[CrossRef] [PubMed]

Ornitholog. Sci.

M. L. Rahman, M. Aoyama, and S. Sugita, “Topography of retinal photoreceptor cells in the Jungle Crow (Corvus macrorhynchos) with emphasis on the distribution of oil droplets,” Ornitholog. Sci. 6(1), 29–38 (2007).
[CrossRef]

PLoS ONE

Y. A. Kram, S. Mantey, and J. C. Corbo, “Avian cone photoreceptors tile the retina as five independent, self-organizing mosaics,” PLoS ONE 5(2), e8992 (2010).
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N. S. Hart, “The visual ecology of avian photoreceptors,” Prog. Retin. Eye Res. 20(5), 675–703 (2001).
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Science

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
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M. J. Chandler, P. J. Smith, D. A. Samuelson, and E. O. MacKay, “Photoreceptor density of the domestic pig retina,” Vet. Ophthalmol. 2(3), 179–184 (1999).
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Vis. Neurosci.

E. Diedrich and F. Schaeffel, “Spatial resolution, contrast sensitivity, and sensitivity to defocus of chicken retinal ganglion cells in vitro,” Vis. Neurosci. 26(5-6), 467–476 (2009).
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D. Troilo, M. Xiong, J. C. Crowley, and B. L. Finlay, “Factors controlling the dendritic arborization of retinal ganglion cells,” Vis. Neurosci. 13(04), 721–733 (1996).
[CrossRef] [PubMed]

F. Schaeffel, B. Rohrer, E. Zrenner, and T. Lemmer, “Diurnal control of rod function in the chicken,” Vis. Neurosci. 6(06), 641–653 (1991).
[CrossRef] [PubMed]

C. A. Curcio and K. R. Sloan, “Packing geometry of human cone photoreceptors: variation with eccentricity and evidence for local anisotropy,” Vis. Neurosci. 9(02), 169–180 (1992).
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J. I. Yellott., “Spectral analysis of spatial sampling by photoreceptors: topological disorder prevents aliasing,” Vision Res. 22(9), 1205–1210 (1982).
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[CrossRef] [PubMed]

F. Schaeffel, A. Glasser, and H. C. Howland, “Accommodation, refractive error and eye growth in chickens,” Vision Res. 28(5), 639–657 (1988).
[CrossRef] [PubMed]

J. Wallman and J. I. Adams, “Developmental aspects of experimental myopia in chicks: susceptibility, recovery and relation to emmetropization,” Vision Res. 27(7), 1139–1163 (1987).
[CrossRef] [PubMed]

C. J. Wolsley, K. J. Saunders, G. Silvestri, and R. S. Anderson, “Investigation of changes in the myopic retina using multifocal electroretinograms, optical coherence tomography and peripheral resolution acuity,” Vision Res. 48(14), 1554–1561 (2008).
[CrossRef] [PubMed]

Other

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Figures (9)

Fig. 1
Fig. 1

Adaptive optics multiphoton microscope. AO module, adaptive optics module (Hartmann-Shack wavefront sensor and deformable mirror); PMT, photomultiplier tube.

Fig. 2
Fig. 2

Microscopy images of different chicken retinal layers acquired with a bright-field microscope and a 20x objective. Nerve fibers (a), ganglion cells (b), inner nuclear layer (c), and photoreceptors (oil droplets, see text) (d). Scale bar: 50 µm.

Fig. 3
Fig. 3

(a) Histological transversal section of a fixed and stained chicken retina. (b)-(g) TPEF images of the different retinal layers acquired with a 20x objective: nerve fibers (b), ganglion cells (c), inner plexiform layer (d), inner nuclear layer (e), outer nuclear layer (f), and photoreceptors (oil droplets, see text) (g). Images correspond to a retinal eccentricity of about 30 deg. TPEF signal is exclusively due to the local endogenous fluorescence (autofluorescence). Scale bar: 50 µm.

Fig. 4
Fig. 4

TPEF in chicken retinal tissues. (a) The same transversal XZ section of a chicken retina as in Fig. 3a. (b)-(g) TPEF images acquired with a 100x objective for the same retinal area as in Fig. 3; (b) ganglion cells; (c and d) inner nuclear layer; (e) outer plexiform layer; (f) outer nuclear layer and (g) photoreceptors. Scale bar: 25 μm.

Fig. 5
Fig. 5

(a, b) Reconstructed volume renderings of the chicken central retina: top (a) and bottom (b) views. Diagonal cross-section (c) and transversal tomography (d) computed from (a). A different false color has been chosen for a better visualization.

Fig. 6
Fig. 6

TPEF images of the ganglion cells and photoreceptors of a chicken retina for different retinal eccentricities (12° (left), 50° (middle) and 85° (right). Ganglion cells (upper panels); photoreceptors (bottom panels). Scale bar: 50 μm.

Fig. 7
Fig. 7

Photoreceptor density values (cells/mm2) as a function of retinal eccentricity. The black line fitted to the data gives a significant linear decrease with increasing retinal eccentricity (p< 0.0001). Linear fit: y = −175x + 20675.

Fig. 8
Fig. 8

Averaged density values (cells/mm2) for photoreceptors (red symbols) and ganglion cells (blue symbols) as a function of retinal eccentricity.

Fig. 9
Fig. 9

Values of maximum anatomical resolving power (c/deg) in the chick retina as a function of retinal eccentricity computed using Eq. (1). An example of an image corresponding to the Fourier transform of a photoreceptor mosaic is shown on the left. Linear fit: y = −0.03x + 7.15.

Equations (1)

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

MARP = PND 57.3 D cone 3 ,

Metrics