Analysis of the chicken retina with an adaptive optics multiphoton microscope

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.

[1]  William Hodos,et al.  Spatial contrast sensitivity of birds , 2006, Journal of Comparative Physiology A.

[2]  F. Schaeffel,et al.  Diurnal control of rod function in the chicken , 1991, Visual Neuroscience.

[3]  B. Finlay,et al.  Factors controlling the dendritic arborization of retinal ganglion cells , 1996, Visual Neuroscience.

[4]  D. Yew,et al.  Morphogenesis of the different types of photoreceptors of the chicken (Gallus domesticus) retina and the effect of amblyopia in neonatal chicken , 2006, Microscopy research and technique.

[5]  Lawrence K. Cormack,et al.  An Introduction to the Visual System: References , 1996 .

[6]  C. Curcio,et al.  Packing geometry of human cone photoreceptors: variation with eccentricity and evidence for local anisotropy. , 1992, Visual neuroscience.

[7]  Steffen Schmitz-Valckenberg,et al.  Age-related structural abnormalities in the human retina-choroid complex revealed by two-photon excited autofluorescence imaging. , 2007, Journal of biomedical optics.

[8]  R. Over,et al.  Spatial acuity of the chicken , 1981, Brain Research.

[9]  J. Merayo-Lloves,et al.  Wound healing following refractive surgery in hens. , 2006, Experimental eye research.

[10]  J. Merayo-Lloves,et al.  Experimental model of laser in situ keratomileusis in hens. , 2005, Journal of refractive surgery.

[11]  J. Yellott Spectral analysis of spatial sampling by photoreceptors: Topological disorder prevents aliasing , 1982, Vision Research.

[12]  Jumpei Naito,et al.  Morphological features of chick retinal ganglion cells , 2004, Anatomical science international.

[13]  D. Ehrlich Regional specialization of the chick retina as revealed by the size and density of neurons in the ganglion cell layer , 1981, The Journal of comparative neurology.

[14]  A. Hendrickson,et al.  Human photoreceptor topography , 1990, The Journal of comparative neurology.

[15]  N J Coletta,et al.  Psychophysical estimate of extrafoveal cone spacing. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[16]  Annett Eitner,et al.  High‐resolution two‐photon excitation microscopy of ocular tissues in porcine eye , 2008, Lasers in surgery and medicine.

[17]  R. Weinreb,et al.  Histopathologic validation of Fourier-ellipsometry measurements of retinal nerve fiber layer thickness. , 1990, Archives of ophthalmology.

[18]  J. Merayo-Lloves,et al.  Measurement of correlation between transmission and scattering during wound healing in hen corneas , 2009 .

[19]  D. Chang,et al.  A new paradigm for corneal wound healing research: The white leghorn chicken (Gallus gallus domesticus) , 2004, Current eye research.

[20]  W. Denk,et al.  Two-photon laser scanning fluorescence microscopy. , 1990, Science.

[21]  H. Maturana,et al.  Regional specialization of the quail retina: Ganglion cell density and oil droplet distribution , 1984, Neuroscience Letters.

[22]  J. Pettigrew,et al.  Experimental myopia and anamalous eye growth patterns unaffected by optic nerve section in chickens: Evidence for local control of eye growth , 1988 .

[23]  R. Anderson,et al.  Investigation of changes in the myopic retina using multifocal electroretinograms, optical coherence tomography and peripheral resolution acuity , 2008, Vision Research.

[24]  G. H. Jacobs,et al.  Modelling the mosaic organization of rod and cone photoreceptors with a minimal‐spacing rule , 1999, The European journal of neuroscience.

[25]  R. Binggeli,et al.  The pigeon retina: Quantitative aspects of the optic nerve and ganglion cell layer , 1969, The Journal of comparative neurology.

[26]  Frank Schaeffel,et al.  Spatial resolution, contrast sensitivity, and sensitivity to defocus of chicken retinal ganglion cells in vitro , 2009, Visual Neuroscience.

[27]  L. Malaval,et al.  Spatiotemporal distribution of SPARC/osteonectin in developing and mature chicken retina. , 1997, Experimental eye research.

[28]  Pablo Artal,et al.  Wavefront optimized nonlinear microscopy of ex vivo human retinas. , 2010, Journal of biomedical optics.

[29]  Adrian Glasser,et al.  Accommodation, refractive error and eye growth in chickens , 1988, Vision Research.

[30]  Watt W Webb,et al.  Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein. , 2002, Biophysical journal.

[31]  Howard C. Howland,et al.  Natural accommodation in the growing chicken , 1986, Vision Research.

[32]  Adam M. Larson,et al.  Multiphoton adaptation of a commercial low-cost confocal microscope for live tissue imaging. , 2009, Journal of biomedical optics.

[33]  Hui Sun,et al.  Two-photon excited autofluorescence imaging of human retinal pigment epithelial cells. , 2006, Journal of biomedical optics.

[34]  Yaoxing Chen,et al.  A Quantitative Analysis of Cells in the Ganglion Cell Layer of the Chick Retina , 1999, Brain, Behavior and Evolution.

[35]  D. Schweitzer,et al.  Towards metabolic mapping of the human retina , 2007, Microscopy research and technique.

[36]  Frank Schaeffel,et al.  A simple mechanism for emmetropization without cues from accommodation or colour , 1994, Vision Research.

[37]  Yiannis Koutalos,et al.  Reduction of all-trans retinal to all-trans retinol in the outer segments of frog and mouse rod photoreceptors. , 2005, Biophysical journal.

[38]  Paul R. Martin,et al.  Comparison of photoreceptor spatial density and ganglion cell morphology in the retina of human, macaque monkey, cat, and the marmoset Callithrix jacchus , 1996, The Journal of comparative neurology.

[39]  P Artal,et al.  High-resolution imaging of the living human fovea: measurement of the intercenter cone distance by speckle interferometry. , 1989, Optics letters.

[40]  Katrina L Schmid,et al.  Assessment of visual acuity and contrast sensitivity in the chick using an optokinetic nystagmus paradigm , 1998, Vision Research.

[41]  C. Straznicky,et al.  The formation of the area centralis of the retinal ganglion cell layer in the chick. , 1987, Development.

[42]  E. Irving,et al.  In chicks wearing high powered negative lenses, spherical refraction is compensated and oblique astigmatism is induced , 2008 .

[43]  S. Sugita,et al.  Number and density of retinal photoreceptor cells with emphasis on oil droplet distribution in the Mallard Duck (Anas platyrhynchos var. domesticus) , 2007 .

[44]  J. Bowmaker The visual pigments, oil droplets and spectral sensitivity of the pigeon , 1977, Vision Research.

[45]  J. Wallman,et al.  Developmental aspects of experimental myopia in chicks: Susceptibility, recovery and relation to emmetropization , 1987, Vision Research.

[46]  T. Reh,et al.  Identification of a proliferating marginal zone of retinal progenitors in postnatal chickens. , 2000, Developmental biology.

[47]  J. Corbo,et al.  Avian Cone Photoreceptors Tile the Retina as Five Independent, Self-Organizing Mosaics , 2010, PloS one.

[48]  D. Samuelson,et al.  Photoreceptor density of the domestic pig retina. , 1999, Veterinary ophthalmology.

[49]  S. Collin,et al.  Cone photoreceptor oil droplet pigmentation is affected by ambient light intensity , 2006, Journal of Experimental Biology.

[50]  P. Artal,et al.  Analysis of Corneal Stroma Organization With Wavefront Optimized Nonlinear Microscopy , 2011, Cornea.

[51]  L. Reymond Spatial visual acuity of the eagle Aquila audax: a behavioural, optical and anatomical investigation , 1985, Vision Research.

[52]  Jonathan Winawer,et al.  Homeostasis of Eye Growth and the Question of Myopia , 2012, Neuron.

[53]  N. Hart The Visual Ecology of Avian Photoreceptors , 2001, Progress in Retinal and Eye Research.

[54]  J. Sivak,et al.  Bilateral Experimental Myopia in Chicks , 1989, Optometry and vision science : official publication of the American Academy of Optometry.

[55]  A. Quantock,et al.  Collagen organization in the chicken cornea and structural alterations in the retinopathy, globe enlarged (rge) phenotype--an X-ray diffraction study. , 2008, Journal of structural biology.

[56]  S. Sugita,et al.  Topography of retinal photoreceptor cells in the Jungle Crow (Corvus macrorhynchos) with emphasis on the distribution of oil droplets , 2007 .

[57]  R. Wilkins,et al.  THE NORMAL GROWTH OF WHITE LEGHORN CHICKENS , 1918 .

[58]  Jennifer J. Hunter,et al.  Blur on the retina due to higher-order aberrations: comparison of eye growth models to experimental data. , 2009, Journal of vision.

[59]  Krzysztof Palczewski,et al.  Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye , 2004, The Journal of cell biology.

[60]  W. Hodos,et al.  Electroretinographic changes in aged pigeons , 1991, Vision Research.

[61]  R R Alfano,et al.  Second-harmonic tomography of tissues. , 1997, Optics letters.

[62]  Pablo Artal,et al.  Adaptive optics multiphoton microscopy to study ex vivo ocular tissues. , 2010, Journal of biomedical optics.

[63]  R. Trelstad,et al.  MORPHOGENESIS OF THE COLLAGENOUS STROMA IN THE CHICK CORNEA , 1971, The Journal of cell biology.