Functional Imaging of Cone Photoreceptors

Color pervades our visual sensory world, yet our understanding of the neural basis of color perception, starting with the retina and on through the multiple cortical areas that subserve vision, is still incomplete. The L, M, and S cone photoreceptors, being the cellular entry point for trichromatic vision in humans and primates, have been studied in a variety of ways to reveal their relative numbers, their spatial arrangement, and their anatomical connectivity. We review work in these species that has linked mapped cone mosaics directly to functional properties such as single neuron responses in the retina and color percepts arising from cone-targeted microstimulation. Technical issues that constrain access to single cone photoreceptors for functional studies are also considered.

[1]  P. Gouras,et al.  Functional properties of ganglion cells of the rhesus monkey retina. , 1975, The Journal of physiology.

[2]  D. L. Adams,et al.  A Precise Retinotopic Map of Primate Striate Cortex Generated from the Representation of Angioscotomas , 2003, The Journal of Neuroscience.

[3]  D. L. Adams,et al.  Shadows Cast by Retinal Blood Vessels Mapped in Primary Visual Cortex , 2002, Science.

[4]  S. McKee,et al.  Spatial configurations for visual hyperacuity , 1977, Vision Research.

[5]  Ramkumar Sabesan Studying cone-by-cone contributions to color vision , 2014 .

[6]  D. Baylor,et al.  Spectral sensitivity of cones of the monkey Macaca fascicularis. , 1987, The Journal of physiology.

[7]  G. H. Jacobs,et al.  Functional consequences of the relative numbers of L and M cones. , 2000, Journal of the Optical Society of America. A, Optics, image science, and vision.

[8]  Pablo Artal,et al.  Directional imaging of the retinal cone mosaic. , 2004, Optics letters.

[9]  Austin Roorda,et al.  Design of an integrated hardware interface for AOSLO image capture and cone-targeted stimulus delivery , 2010, Optics express.

[10]  Austin Roorda,et al.  Retinally stabilized cone-targeted stimulus delivery. , 2007, Optics express.

[11]  A. Stockman,et al.  The spectral sensitivities of the middle- and long-wavelength-sensitive cones derived from measurements in observers of known genotype , 2000, Vision Research.

[12]  J. Mollon,et al.  Microspectrophotometric demonstration of four classes of photoreceptor in an old world primate, Macaca fascicularis. , 1980, The Journal of physiology.

[13]  Austin Roorda,et al.  Noninvasive visualization and analysis of parafoveal capillaries in humans. , 2010, Investigative ophthalmology & visual science.

[14]  J. Coppens,et al.  History of ocular straylight measurement: A review. , 2013, Zeitschrift fur medizinische Physik.

[15]  Light capture by human cones. , 1989, The Journal of physiology.

[16]  R. Tuma,et al.  Investigation of the source of the blue field entoptic phenomenon. , 1989, Investigative ophthalmology & visual science.

[17]  R. Marc,et al.  Chromatic organization of primate cones. , 1977, Science.

[18]  Paul R. Martin,et al.  Immunocytochemical characterization and spatial distribution of midget bipolar cells in the macaque monkey retina , 1994, Vision Research.

[19]  Wallace B. Thoreson,et al.  Lateral interactions in the outer retina , 2012, Progress in Retinal and Eye Research.

[20]  W. Rushton Review Lecture. Pigments and signals in colour vision , 1972 .

[21]  Tos T. J. M Berendschot,et al.  Fundus reflectance—historical and present ideas , 2003, Progress in Retinal and Eye Research.

[22]  B. G. Hertz,et al.  Eye movements in paralyzed cats induced by drugs and sympathetic stimulation , 1979, Vision Research.

[23]  George Smith,et al.  Chromatic dispersions of the ocular media of human eyes. , 2005, Journal of the Optical Society of America. A, Optics, image science, and vision.

[24]  B. Selig,et al.  Angioscotoma detection with fundus-oriented perimetry A study with dark and bright stimuli of different sizes , 1999, Vision Research.

[25]  R A Applegate,et al.  Parametric representation of Stiles-Crawford functions: normal variation of peak location and directionality. , 1993, Journal of the Optical Society of America. A, Optics and image science.

[26]  S. Schein,et al.  Density profile of blue-sensitive cones along the horizontal meridian of macaque retina. , 1985, Investigative ophthalmology & visual science.

[27]  C. M. Cicerone,et al.  The relative numbers of long-wavelength-sensitive to middle-wavelength-sensitive cones in the human fovea centralis , 1989, Vision Research.

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

[29]  D. Baylor,et al.  Spectral sensitivity of human cone photoreceptors , 1987, Nature.

[30]  A. Roorda,et al.  Direct and noninvasive assessment of parafoveal capillary leukocyte velocity. , 2005, Ophthalmology.

[31]  J. Mollon,et al.  Human visual pigments: microspectrophotometric results from the eyes of seven persons , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

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

[33]  M. Rolfs Microsaccades: Small steps on a long way , 2009, Vision Research.

[34]  Joel Pokorny,et al.  Foveal cone detection statistics in color-normals and dichromats , 1991, Vision Research.

[35]  G H Jacobs,et al.  Electroretinogram flicker photometry and its applications. , 1996, Journal of the Optical Society of America. A, Optics, image science, and vision.

[36]  Jonathan W Peirce,et al.  Residual eye-movements in macaque and their effects on visual responses of neurons , 2002, Visual Neuroscience.

[37]  David Williams,et al.  A visual nonlinearity fed by single cones , 1992, Vision Research.

[38]  R Srebro,et al.  Spectral Sensitivity of Color Mechanisms: Derivation from Fluctuations of Color Appearance near Threshold , 1965, Science.

[39]  J. Pokorny,et al.  The effect of background luminance on cone sensitivity functions. , 1989, Investigative ophthalmology & visual science.

[40]  Lawrence C. Sincich,et al.  Resolving Single Cone Inputs to Visual Receptive Fields , 2009, Nature Neuroscience.

[41]  D. Dacey The mosaic of midget ganglion cells in the human retina , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  David Williams,et al.  Different sensations from cones with the same photopigment. , 2005, Journal of vision.

[43]  Thomas Euler,et al.  Retinal bipolar cells: elementary building blocks of vision , 2014, Nature Reviews Neuroscience.

[44]  B. Boycott,et al.  Cortical magnification factor and the ganglion cell density of the primate retina , 1989, Nature.

[45]  David R. Williams,et al.  Punctate sensitivity of the blue-sensitive mechanism , 1981, Vision Research.

[46]  P Lennie,et al.  Distinctive characteristics of subclasses of red–green P-cells in LGN of macaque , 1998, Visual Neuroscience.

[47]  D. Baylor,et al.  Visual transduction in cones of the monkey Macaca fascicularis. , 1990, The Journal of physiology.

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

[49]  Heidi Hofer,et al.  Trichromatic reconstruction from the interleaved cone mosaic: Bayesian model and the color appearance of small spots. , 2008, Journal of vision.

[50]  David J. Calkins,et al.  Absence of spectrally specific lateral inputs to midget ganglion cells in primate retina , 1996, Nature.

[51]  Hiroshi Imamura,et al.  The source of moving particles in parafoveal capillaries detected by adaptive optics scanning laser ophthalmoscopy. , 2012, Investigative ophthalmology & visual science.

[52]  Jacob Cohen,et al.  Weighted kappa: Nominal scale agreement provision for scaled disagreement or partial credit. , 1968 .

[53]  P Artal,et al.  Dynamics of the eye's wave aberration. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.

[54]  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.

[55]  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.

[56]  M. Campbell,et al.  The optical transverse chromatic aberration on the fovea of the human eye , 1990, Vision Research.

[57]  Austin Roorda,et al.  Adaptive optics for studying visual function: a comprehensive review. , 2011, Journal of vision.

[58]  B. Vohnsen Directional sensitivity of the retina: A layered scattering model of outer-segment photoreceptor pigments. , 2014, Biomedical optics express.

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

[60]  Graeme R. Cole,et al.  Computation of cone contrasts for color vision research , 1992 .

[61]  R. Shapley,et al.  Space and Time Maps of Cone Photoreceptor Signals in Macaque Lateral Geniculate Nucleus , 2002, The Journal of Neuroscience.

[62]  K. Yau,et al.  Light responses of primate and other mammalian cones , 2014, Proceedings of the National Academy of Sciences.

[63]  Jessica I. Wolfing,et al.  Retinal microscotomas revealed with adaptive-optics microflashes. , 2006, Investigative ophthalmology & visual science.

[64]  C. M. Cicerone,et al.  The ratio of L cones to M cones in the human parafoveal retina , 1992, Vision Research.

[65]  Paul R. Martin,et al.  Retinal connectivity and primate vision , 2010, Progress in Retinal and Eye Research.

[66]  V. Perry,et al.  The topography of magnocellular projecting ganglion cells (M-ganglion cells) in the primate retina , 1991, Neuroscience.

[67]  W. B. Marks,et al.  Visual Pigments of Single Primate Cones , 1964, Science.

[68]  D. Baylor,et al.  Spectral sensitivity of primate photoreceptors , 1988, Visual Neuroscience.

[69]  Paul R. Martin,et al.  Chromatic sensitivity of ganglion cells in the peripheral primate retina , 2001, Nature.

[70]  B. Boycott,et al.  Parasol (Pα) ganglion-cells of the primate fovea: Immunocytochemical staining with antibodies against GABAA-receptors , 1993, Vision Research.

[71]  Martin J. How,et al.  A Different Form of Color Vision in Mantis Shrimp , 2014, Science.

[72]  Keith Mathieson,et al.  Retinal Representation of the Elementary Visual Signal , 2014, Neuron.

[73]  Timothy A. Machado,et al.  Functional connectivity in the retina at the resolution of photoreceptors , 2010, Nature.

[74]  Peter Lennie,et al.  Coding of color and form in the geniculostriate visual pathway (invited review). , 2005, Journal of the Optical Society of America. A, Optics, image science, and vision.

[75]  B. Vohnsen,et al.  Guided light and diffraction model of human-eye photoreceptors. , 2005, Journal of the Optical Society of America. A, Optics, image science, and vision.

[76]  David R. Williams,et al.  Serial spatial filters in vision , 1993, Vision Research.

[77]  P. Rakić,et al.  Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[78]  Donald T. Miller,et al.  Imaging outer segment renewal in living human cone photoreceptors. , 2010, Optics express.

[79]  Darren E. Koenig,et al.  Do color appearance judgments interfere with detection of small threshold stimuli? , 2012, Journal of the Optical Society of America. A, Optics, image science, and vision.

[80]  Austin Roorda,et al.  Adaptive Optics Scanning Laser Ophthalmoscope-Based Microperimetry , 2011, Optometry and vision science : official publication of the American Academy of Optometry.

[81]  Peter Sterling,et al.  Electrical Coupling between Mammalian Cones , 2002, Current Biology.

[82]  J Nathans,et al.  Spectral sensitivities of human cone visual pigments determined in vivo and in vitro. , 2000, Methods in enzymology.

[83]  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.

[84]  Drew Williams,et al.  Photopigment transmittance imaging of the primate photoreceptor mosaic , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[85]  David Williams Imaging single cells in the living retina , 2011, Vision Research.

[86]  Paul R. Martin,et al.  Contribution of chromatic aberrations to color signals in the primate visual system. , 2006, Journal of vision.

[87]  Susana Marcos,et al.  Investigating sources of variability of monochromatic and transverse chromatic aberrations across eyes , 2001, Vision Research.

[88]  B. B. Lee,et al.  Receptive fields of primate retinal ganglion cells studied with a novel technique , 1998, Visual Neuroscience.

[89]  Jay Neitz,et al.  Topography of long- and middle-wavelength sensitive cone opsin gene expression in human and Old World monkey retina , 2006, Visual Neuroscience.

[90]  Michael Pircher,et al.  Retinal cone mosaic imaged with transverse scanning optical coherence tomography. , 2006, Optics letters.

[91]  Paul R. Martin,et al.  Specificity of M and L Cone Inputs to Receptive Fields in the Parvocellular Pathway: Random Wiring with Functional Bias , 2006, The Journal of Neuroscience.

[92]  L N Thibos,et al.  Statistical distribution of foveal transverse chromatic aberration, pupil centration, and angle psi in a population of young adult eyes. , 1995, Journal of the Optical Society of America. A, Optics, image science, and vision.

[93]  John S. Werner,et al.  Spatial summation in human cone mechanisms from 0° to 20° in the superior retina , 2000 .

[94]  Austin Roorda,et al.  Mapping the Perceptual Grain of the Human Retina , 2014, The Journal of Neuroscience.

[95]  J. Odom,et al.  Distribution of carbonic anhydrase among human photoreceptors. , 1990, Investigative ophthalmology & visual science.

[96]  Jay M. Enoch,et al.  Vertebrate photoreceptor optics , 1981 .

[97]  J. Pokorny,et al.  Responses of macaque ganglion cells to the relative phase of heterochromatically modulated lights. , 1992, The Journal of physiology.

[98]  A. Elsner,et al.  Angioscotometry with the scanning laser ophthalmoscope. Comparison of the effect of different wavelengths. , 1996, Investigative ophthalmology & visual science.

[99]  N. Drasdo,et al.  The length of Henle fibers in the human retina and a model of ganglion receptive field density in the visual field , 2007, Vision Research.

[100]  D. Snodderly,et al.  Neural-vascular relationships in central retina of macaque monkeys (Macaca fascicularis) , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[101]  J. L. Schnapf,et al.  Electrical coupling between red and green cones in primate retina , 2004, Nature Neuroscience.

[102]  Stephen A. Burns,et al.  A new approach to the study of ocular chromatic aberrations , 1999, Vision Research.

[103]  Barry B. Lee,et al.  Horizontal Cells of the Primate Retina: Cone Specificity Without Spectral Opponency , 1996, Science.

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

[105]  David Williams,et al.  Noninvasive imaging of the human rod photoreceptor mosaic using a confocal adaptive optics scanning ophthalmoscope , 2011, Biomedical optics express.

[106]  W. Stiles,et al.  The Luminous Efficiency of Rays Entering the Eye Pupil at Different Points , 1933 .

[107]  Omer P. Kocaoglu,et al.  The cellular origins of the outer retinal bands in optical coherence tomography images. , 2014, Investigative ophthalmology & visual science.

[108]  A. Bradley,et al.  Theory and measurement of ocular chromatic aberration , 1990, Vision Research.

[109]  H. Kolb,et al.  Midget ganglion cells of the parafovea of the human retina: A Study by electron microscopy and serial section reconstructions , 1991, The Journal of comparative neurology.

[110]  M E Wilson,et al.  Invariant features of spatial summation with changing locus in the visual field , 1970, The Journal of physiology.

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

[112]  Ivar Lie,et al.  Visual detection and resolution as a function of retinal locus , 1980, Vision Research.

[113]  J. Neitz,et al.  Flicker-photometric electroretinogram estimates of L:M cone photoreceptor ratio in men with photopigment spectra derived from genetics. , 2000, Journal of the Optical Society of America. A, Optics, image science, and vision.

[114]  Donald T. Miller,et al.  Measuring retinal contributions to the optical Stiles-Crawford effect with optical coherence tomography. , 2008, Optics express.

[115]  Austin Roorda,et al.  Pulsatility of parafoveal capillary leukocytes. , 2009, Experimental eye research.

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

[117]  R. W. Rodieck The First Steps in Seeing , 1998 .

[118]  Lawrence C. Sincich,et al.  Measurement and correction of transverse chromatic offsets for multi-wavelength retinal microscopy in the living eye , 2012, Biomedical optics express.

[119]  K Miyamoto,et al.  Visualization and quantitative analysis of leukocyte dynamics in retinal microcirculation of rats. , 1996, Investigative ophthalmology & visual science.

[120]  C. Cicerone,et al.  L and M cone relative numerosity and red-green opponency from fovea to midperiphery in the human retina. , 2000, Journal of the Optical Society of America. A, Optics, image science, and vision.

[121]  J. Bowmaker,et al.  Visual pigments of rods and cones in a human retina. , 1980, The Journal of physiology.

[122]  D. Baylor,et al.  Receptive-field microstructure of blue-yellow ganglion cells in primate retina , 1999, Nature Neuroscience.

[123]  Joel Pokorny,et al.  Foveal cone thresholds , 1989, Vision Research.

[124]  D. Dacey,et al.  Distinct synaptic mechanisms create parallel S-ON and S-OFF color opponent pathways in the primate retina , 2013, Visual Neuroscience.

[125]  Hendrik P N Scholl,et al.  Cone selective adaptation influences L- and M-cone driven signals in electroretinography and psychophysics. , 2003, Journal of vision.

[126]  John Krauskopf,et al.  Color appearance of small stimuli and the spatial distribution of color receptors , 1964 .

[127]  William S Tuten,et al.  Normal Perceptual Sensitivity Arising From Weakly Reflective Cone Photoreceptors. , 2015, Investigative ophthalmology & visual science.

[128]  R. Hess,et al.  Human peripheral spatial resolution for achromatic and chromatic stimuli: limits imposed by optical and retinal factors. , 1991, The Journal of physiology.

[129]  G. M. Morris,et al.  Images of cone photoreceptors in the living human eye , 1996, Vision Research.

[130]  J. Verweij,et al.  L and M Cone Contributions to the Midget and Parasol Ganglion Cell Receptive Fields of Macaque Monkey Retina , 2004, The Journal of Neuroscience.

[131]  Michael S. Landy,et al.  The Design of Chromatically Opponent Receptive Fields , 1991 .

[132]  U. Grünert,et al.  Synaptic connectivity in the midget‐parvocellular pathway of primate central retina , 2006, The Journal of comparative neurology.

[133]  Austin Roorda,et al.  Characterization of single-file flow through human retinal parafoveal capillaries using an adaptive optics scanning laser ophthalmoscope , 2011, Biomedical optics express.

[134]  Jay Neitz,et al.  Estimates of L:M cone ratio from ERG flicker photometry and genetics. , 2002, Journal of vision.