The organization of the cone photoreceptor mosaic measured in the living human retina

ABSTRACT The cone photoreceptors represent the initial fundamental sampling step in the acquisition of visual information. While recent advances in adaptive optics have provided increasingly precise estimates of the packing density and spacing of the cone photoreceptors in the living human retina, little is known about the local cone geometric arrangement beyond a tendency towards hexagonal packing. We analyzed the cone mosaic in data from 10 normal subjects. A technique was applied to calculate the local average cone mosaic structure which allowed us to determine the hexagonality, spacing and orientation of local regions. Using cone spacing estimates, we find the expected decrease in cone density with retinal eccentricity and higher densities along the horizontal as opposed to the vertical meridians. Orientation analysis reveals an asymmetry in the local cone spacing of the hexagonal packing, with cones having a larger local spacing along the horizontal direction. This horizontal/vertical asymmetry is altered at eccentricities larger than 2 degrees in the superior meridian and 2.5 degrees in the inferior meridian. Analysis of hexagon orientations in the central 1.4° of the retina shows a tendency for orientation to be locally coherent, with orientation patches consisting of between 35 and 240 cones.

[1]  A D Springer,et al.  Development of the primate area of high acuity, 3: Temporal relationships between pit formation, retinal elongation and cone packing , 2005, Visual Neuroscience.

[2]  Gang Huang,et al.  Lucky averaging: quality improvement of adaptive optics scanning laser ophthalmoscope images. , 2011, Optics letters.

[3]  Stephen A Burns,et al.  Wavefront-aberration sorting and correction for a dual-deformable-mirror adaptive-optics system. , 2008, Optics letters.

[4]  Stephen A Burns,et al.  Individual variations in human cone photoreceptor packing density: variations with refractive error. , 2008, Investigative ophthalmology & visual science.

[5]  Austin Roorda,et al.  Automated identification of cone photoreceptors in adaptive optics retinal images. , 2007, Journal of the Optical Society of America. A, Optics, image science, and vision.

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

[7]  A J Ahumada,et al.  Cone sampling array models. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[8]  Christopher S. Langlo,et al.  Repeatability of In Vivo Parafoveal Cone Density and Spacing Measurements , 2012, Optometry and vision science : official publication of the American Academy of Optometry.

[9]  Elise W. Dees,et al.  Variability in parafoveal cone mosaic in normal trichromatic individuals , 2011, Biomedical optics express.

[10]  Heidi Hofer,et al.  Organization of the Human Trichromatic Cone Mosaic , 2003, The Journal of Neuroscience.

[11]  T. Hebert,et al.  Adaptive optics scanning laser ophthalmoscopy. , 2002, Optics express.

[12]  Jessica I. W. Morgan,et al.  Cone photoreceptor mosaic disruption associated with Cys203Arg mutation in the M-cone opsin , 2009, Proceedings of the National Academy of Sciences.

[13]  P K Ahnelt,et al.  Iso-orientation areas in the foveal cone mosaic , 1990, Visual Neuroscience.

[14]  V. Greenstein,et al.  A study of factors affecting the human cone photoreceptor density measured by adaptive optics scanning laser ophthalmoscope. , 2013, Experimental eye research.

[15]  Cynthia A Toth,et al.  Histologic development of the human fovea from midgestation to maturity. , 2012, American journal of ophthalmology.

[16]  D. Williams,et al.  Cone spacing and the visual resolution limit. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[17]  D R Williams,et al.  Supernormal vision and high-resolution retinal imaging through adaptive optics. , 1997, Journal of the Optical Society of America. A, Optics, image science, and vision.

[18]  C. M. Cicerone,et al.  The spatial arrangement of the L and M cones in the central fovea of the living human eye , 1998, Vision Research.

[19]  P K Ahnelt,et al.  The photoreceptor mosaic , 1998, Eye.

[20]  Joseph A. Izatt,et al.  Automatic cone photoreceptor segmentation using graph theory and dynamic programming , 2013, Biomedical optics express.

[21]  P K Ahnelt,et al.  Identification of a subtype of cone photoreceptor, likely to be blue sensitive, in the human retina , 1987, The Journal of comparative neurology.

[22]  R. W. Rodieck The density recovery profile: A method for the analysis of points in the plane applicable to retinal studies , 1991, Visual Neuroscience.

[23]  W A Rushton,et al.  Red--grees sensitivity in normal vision. , 1964, Vision research.

[24]  Maureen Neitz,et al.  Adaptive optics retinal imaging reveals S-cone dystrophy in tritan color-vision deficiency. , 2007, Journal of the Optical Society of America. A, Optics, image science, and vision.

[25]  M. Lombardo,et al.  Eccentricity dependent changes of density, spacing and packing arrangement of parafoveal cones , 2013, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[26]  A. Hendrickson,et al.  A qualitative and quantitative analysis of the human fovea during development , 1986, Vision Research.

[27]  P. Lennie,et al.  Packing arrangement of the three cone classes in primate retina , 2001, Vision Research.

[28]  A. Springer New role for the primate fovea: A retinal excavation determines photoreceptor deployment and shape , 1999, Visual Neuroscience.

[29]  Kaccie Y. Li,et al.  Intersubject variability of foveal cone photoreceptor density in relation to eye length. , 2010, Investigative ophthalmology & visual science.

[30]  Bing Wu,et al.  Automated analysis of differential interference contrast microscopy images of the foveal cone mosaic. , 2008, Journal of the Optical Society of America. A, Optics, image science, and vision.

[31]  P Artal,et al.  Coherent imaging of the cone mosaic in the living human eye. , 1996, Journal of the Optical Society of America. A, Optics, image science, and vision.

[32]  David Williams,et al.  The arrangement of the three cone classes in the living human eye , 1999, Nature.

[33]  A. Roorda,et al.  Observation of cone and rod photoreceptors in normal subjects and patients using a new generation adaptive optics scanning laser ophthalmoscope , 2011, Biomedical optics express.

[34]  John S Werner,et al.  In vivo imaging of the photoreceptor mosaic in retinal dystrophies and correlations with visual function. , 2006, Investigative ophthalmology & visual science.

[35]  Susana Marcos,et al.  Foveal cone spacing and cone photopigment density difference: Objective measurements in the same subjects , 1997, Vision Research.

[36]  Adam M. Dubis,et al.  Adaptation of the central retina for high acuity vision: Cones, the fovea and the avascular zone , 2013, Progress in Retinal and Eye Research.

[37]  Christopher S. Langlo,et al.  Automatic detection of modal spacing (Yellott's ring) in adaptive optics scanning light ophthalmoscope images , 2013, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[38]  Daniel X Hammer,et al.  Adaptive optics scanning laser ophthalmoscope with integrated wide-field retinal imaging and tracking. , 2010, Journal of the Optical Society of America. A, Optics, image science, and vision.

[39]  John S Werner,et al.  Photoreceptor counting and montaging of en-face retinal images from an adaptive optics fundus camera. , 2007, Journal of the Optical Society of America. A, Optics, image science, and vision.

[40]  S A Burns,et al.  Cone spacing and waveguide properties from cone directionality measurements. , 1999, Journal of the Optical Society of America. A, Optics, image science, and vision.

[41]  A. Hendrickson,et al.  The morphological development of the human fovea. , 1984, Ophthalmology.

[42]  C. Curcio,et al.  Variability in Human Cone Topography Assessed by Adaptive Optics Scanning Laser Ophthalmoscopy. , 2015, American journal of ophthalmology.

[43]  J. Mollon,et al.  THE ARRANGEMENT OF L AND M CONES IN HUMAN AND A PRIMATE RETINA , 2003 .

[44]  J. Mollon,et al.  The spatial arrangement of cones in the primate fovea , 1992, Nature.

[45]  E. Rossi,et al.  The relationship between visual resolution and cone spacing in the human fovea , 2009, Nature Neuroscience.

[46]  Christine A. Curcio,et al.  The spatial resolution capacity of human foveal retina , 1989, Vision Research.

[47]  F. M. de Monasterio,et al.  Regularity and Structure of the Spatial Pattern of Blue Cones of Macaque Retina , 1985 .

[48]  David Williams Topography of the foveal cone mosaic in the living human eye , 1988, Vision Research.

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

[50]  Ann E Elsner,et al.  In vivo adaptive optics microvascular imaging in diabetic patients without clinically severe diabetic retinopathy. , 2014, Biomedical optics express.

[51]  A D Springer,et al.  Development of the primate area of high acuity. 1. Use of finite element analysis models to identify mechanical variables affecting pit formation , 2004, Visual Neuroscience.

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

[53]  M. Stirpe,et al.  INTEROCULAR SYMMETRY OF PARAFOVEAL PHOTORECEPTOR CONE DENSITY DISTRIBUTION , 2013, Retina.

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

[55]  A. Milam,et al.  Distribution and morphology of human cone photoreceptors stained with anti‐blue opsin , 1991, The Journal of comparative neurology.

[56]  Toco Y P Chui,et al.  Variation of cone photoreceptor packing density with retinal eccentricity and age. , 2011, Investigative ophthalmology & visual science.

[57]  Isabelle Bloch,et al.  Automatic Photoreceptor Detection in In-Vivo Adaptive Optics Retinal Images: Statistical Validation , 2012, ICIAR.

[58]  Toco Y P Chui,et al.  Adaptive-optics imaging of human cone photoreceptor distribution. , 2008, Journal of the Optical Society of America. A, Optics, image science, and vision.

[59]  J. Provis,et al.  Evidence of photoreceptor migration during early foveal development: A quantitative analysis of human fetal retinae , 1992, Visual Neuroscience.