Hostname: page-component-f554764f5-246sw Total loading time: 0 Render date: 2025-04-09T16:14:25.998Z Has data issue: false hasContentIssue false
  • English
  • Français

Short-wavelength cone-opponent retinal ganglion cells in mammals

Published online by Cambridge University Press:  23 April 2014

DAVID W. MARSHAK  and
STEPHEN L. MILLS
DAVID W. MARSHAK*
Affiliation:
Department of Neurobiology and Anatomy, University of Texas Medical School, Houston, Texas Department of Ophthalmology and Visual Science, University of Texas Medical School, Houston, Texas
STEPHEN L. MILLS
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas Medical School, Houston, Texas
Get access Rights & Permissions [Opens in a new window]

Abstract

In all of the mammalian species studied to date, the short-wavelength-sensitive (S) cones and the S-cone bipolar cells that receive their input are very similar, but the retinal ganglion cells that receive synapses from the S-cone bipolar cells appear to be quite different. Here, we review the literature on mammalian retinal ganglion cells that respond selectively to stimulation of S-cones and respond with opposite polarity to longer wavelength stimuli. There are at least three basic mechanisms to generate these color-opponent responses, including: (1) opponency is generated in the outer plexiform layer by horizontal cells and is conveyed to the ganglion cells via S-cone bipolar cells, (2) inputs from bipolar cells with different cone inputs and opposite response polarity converge directly on the ganglion cells, and (3) inputs from S-cone bipolar cells are inverted by S-cone amacrine cells. These are not mutually exclusive; some mammalian ganglion cells that respond selectively to S-cone stimulation seem to utilize at least two of them. Based on these findings, we suggest that the small bistratified ganglion cells described in primates are not the ancestral type, as proposed previously. Instead, the known types of ganglion cells in this pathway evolved from monostratified ancestral types and became bistratified in some mammalian lineages.

Keywords

Color visionBlueEvolutionPrimateNeuronal types
Type
Review Articles
Information
Visual Neuroscience , Volume 31 , Issue 2: Short Wavelength-Sensitive Cones and the Processing of Their Signals , March 2014 , pp. 165 - 175
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Breuninger, T., Puller, C., Haverkamp, S. & Euler, T. (2011). Chromatic bipolar cell pathways in the mouse retina. The Journal of Neuroscience 31, 6504–6517.Google Scholar
Caldwell, J.H. & Daw, N.W. (1978). New properties of rabbit retinal ganglion cells. The Journal of Physiology 276, 257–276.CrossRefGoogle ScholarPubMed
Calkins, D.J., Tsukamoto, Y. & Sterling, P. (1998). Microcircuitry and mosaic of a blue-yellow ganglion cell in the primate retina. The Journal of Neuroscience 18, 3373–3385.Google Scholar
Chang, L., Breuninger, T. & Euler, T. (2013). Chromatic coding from cone-type unselective circuits in the mouse retina. Neuron 77, 559–571.Google Scholar
Chen, S. & Li, W. (2012). A color-coding amacrine cell may provide a blue-off signal in a mammalian retina. Nature Neuroscience 15, 954–956.CrossRefGoogle Scholar
Chichilnisky, E.J. & Baylor, D.A. (1999). Receptive-field microstructure of blue-yellow ganglion cells in primate retina. Nature Neuroscience 2, 889–893.Google Scholar
Cleland, B.G. & Levick, W.R. (1974). Properties of rarely encountered types of ganglion cells in the cat’s retina and an overall classification. The Journal of Physiology 240, 457–492.Google Scholar
Cohen, E. & Sterling, P. (1990 a). Convergence and divergence of cones onto bipolar cells in the central area of cat retina. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 330, 323–328.Google Scholar
Cohen, E. & Sterling, P. (1990 b). Demonstration of cell types among cone bipolar neurons of cat retina. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 330, 305–321.Google ScholarPubMed
Crook, J.D., Davenport, C.M., Peterson, B.B., Packer, O.S., Detwiler, P.B. & Dacey, D.M. (2009). Parallel ON and OFF cone bipolar inputs establish spatially coextensive receptive field structure of blue-yellow ganglion cells in primate retina. The Journal of Neuroscience 29, 8372–8387.Google Scholar
Crook, J.D., Manookin, M.B., Packer, O.S. & Dacey, D.M. (2011). Horizontal cell feedback without cone type-selective inhibition mediates “red-green” color opponency in midget ganglion cells of the primate retina. The Journal of Neuroscience 31, 1762–1772.CrossRefGoogle ScholarPubMed
Crook, J.D., Peterson, B.B., Packer, O.S., Robinson, F.R., Gamlin, P.D., Troy, J.B. & Dacey, D.M. (2008). The smooth monostratified ganglion cell: Evidence for spatial diversity in the Y-cell pathway to the lateral geniculate nucleus and superior colliculus in the macaque monkey. The Journal of Neuroscience 28, 12654–12671.CrossRefGoogle Scholar
Dacey, D.M. (1993). Morphology of a small-field bistratified ganglion cell type in the macaque and human retina. Visual Neuroscience 10, 1081–1098.CrossRefGoogle ScholarPubMed
Dacey, D.M. (2000). Parallel pathways for spectral coding in primate retina. Annual Review of Neuroscience 23, 743–775.Google Scholar
Dacey, D.M. & Lee, B.B. (1994). The ‘blue-on’ opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature 367, 731–735.Google Scholar
Dacey, D.M., Liao, H.W., Peterson, B.B., Robinson, F.R., Smith, V.C., Pokorny, J., Yau, K.W. & Gamlin, P.D. (2005). Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433, 749–754.Google Scholar
Dacey, D.M. & Packer, O.S. (2003). Colour coding in the primate retina: diverse cell types and cone-specific circuitry. Current Opinion in Neurobiology 13, 421–427.CrossRefGoogle ScholarPubMed
Dacey, D.M., Peterson, B.B., Robinson, F.R. & Gamlin, P.D. (2003). Fireworks in the primate retina: In vitro photodynamics reveals diverse LGN-projecting ganglion cell types. Neuron 37, 15–27.Google Scholar
Dacey, D.M., Crook, J.D., Manookin, M.B. & Packer, O.S. (2011). Absence of synaptic inhibition associated with S-cone on excitatory input to the small bistratified, blue-yellow opponent ganglion cell of the macaque monkey retina. Association for Research in Vision and Ophthalmology Annual Meeting, Fort Lauderdale, FL.Google Scholar
de Monasterio, F.M. (1978 a). Center and surround mechanisms of opponent-color X and Y ganglion cells of retina of macaques. Journal of Neurophysiology 41, 1418–1434.Google Scholar
de Monasterio, F.M. (1978 b). Properties of concentrically organized X and Y ganglion cells of macaque retina. Journal of Neurophysiology 41, 1394–1417.CrossRefGoogle ScholarPubMed
de Monasterio, F.M. & Gouras, P. (1975). Functional properties of ganglion cells of the rhesus monkey retina. The Journal of Physiology 251, 167–195.CrossRefGoogle ScholarPubMed
de Monasterio, F.M., Gouras, P. & Tolhurst, D.J. (1975). Trichromatic colour opponency in ganglion cells of the rhesus monkey retina. The Journal of Physiology 251, 197–216.Google Scholar
Dowling, J.E. (2012). The Retina: An Approachable Part of the Brain. Cambridge, MAHarvard University Press.CrossRefGoogle Scholar
Ekesten, B. & Gouras, P. (2005). Cone and rod inputs to murine retinal ganglion cells: evidence of cone opsin specific channels. Visual Neuroscience 22, 893–903.Google Scholar
Famiglietti, E.V. (2008). Wide-field cone bipolar cells and the blue-ON pathway to color-coded ganglion cells in rabbit retina. Visual Neuroscience 25, 53–66.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (2009). Bistratified ganglion cells of rabbit retina: Neural architecture for contrast-independent visual responses. Visual Neuroscience 26, 195–213.Google Scholar
Famiglietti, E.V. Jr. (1981). Functional architecture of cone bipolar cells in mammalian retina. Vision Research 21, 1559–1563.Google Scholar
Field, G.D., Gauthier, J.L., Sher, A., Greschner, M., Machado, T.A., Jepson, L.H., Shlens, J., Gunning, D.E., Mathieson, K., Dabrowski, W., Paninski, L., Litke, A.M. & Chichilnisky, E.J. (2010). Functional connectivity in the retina at the resolution of photoreceptors. Nature 467, 673–677.Google Scholar
Field, G.D., Greschner, M., Gauthier, J.L., Rangel, C., Shlens, J., Sher, A., Marshak, D.W., Litke, A.M. & Chichilnisky, E.J. (2009). High-sensitivity rod photoreceptor input to the blue-yellow color opponent pathway in macaque retina. Nature Neuroscience 12, 1159–1164.CrossRefGoogle Scholar
Field, G.D., Sher, A., Gauthier, J.L., Greschner, M., Shlens, J., Litke, A.M. & Chichilnisky, E.J. (2007). Spatial properties and functional organization of small bistratified ganglion cells in primate retina. The Journal of Neuroscience 27, 13261–13272.Google Scholar
Ghosh, F., Bruun, A. & Ehinger, B. (1999). Graft-host connections in long-term full-thickness embryonic rabbit retinal transplants. Investigative Ophthalmology & Visual Science 40, 126–132.Google ScholarPubMed
Ghosh, K.K., Martin, P.R. & Grunert, U. (1997). Morphological analysis of the blue cone pathway in the retina of a New World monkey, the marmoset Callithrix jacchus. The Journal of Comparative Neurology 379, 211–225.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Gouras, P. (1968). Identification of cone mechanisms in monkey ganglion cells. The Journal of Physiology 199, 533–547.Google Scholar
Gouras, P. & Eggers, H. (1982). Ganglion cells mediating the signals of blue sensitive cones in primate retina detect white-yellow borders independently of brightness. Vision Research 22, 675–679.Google Scholar
Greschner, M., Shlens, J., Bakolitsa, C., Field, G.D., Gauthier, J.L., Jepson, L.H., Sher, A., Litke, A.M. & Chichilnisky, E.J. (2011). Correlated firing among major ganglion cell types in primate retina. The Journal of Physiology 589, 75–86.Google Scholar
Grunert, U., Jusuf, P.R., Lee, S.C. & Nguyen, D.T. (2011). Bipolar input to melanopsin containing ganglion cells in primate retina. Visual Neuroscience 28, 39–50.CrossRefGoogle ScholarPubMed
Guenther, E. & Zrenner, E. (1993). The spectral sensitivity of dark- and light-adapted cat retinal ganglion cells. The Journal of Neuroscience 13, 1543–1550.Google Scholar
Haverkamp, S., Wassle, H., Duebel, J., Kuner, T., Augustine, G.J., Feng, G. & Euler, T. (2005). The primordial, blue-cone color system of the mouse retina. The Journal of Neuroscience 25, 5438–5445.Google Scholar
Hemmi, J.M., James, A. & Taylor, W.R. (2002). Color opponent retinal ganglion cells in the tammar wallaby retina. Journal of Vision 2, 608–617.Google Scholar
Hong, Y.K., Kim, I.J. & Sanes, J.R. (2011). Stereotyped axonal arbors of retinal ganglion cell subsets in the mouse superior colliculus. The Journal of Comparative Neurology 519, 1691–1711.CrossRefGoogle ScholarPubMed
Hoshi, H. & Mills, S.L. (2009). Components and properties of the G3 ganglion cell circuit in the rabbit retina. The Journal of Comparative Neurology 513, 69–82.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1960). Receptive fields of optic nerve fibres in the spider monkey. The Journal of Physiology 154, 572–580.Google Scholar
Jepson, L.H., Hottowy, P., Mathieson, K., Gunning, D.E., Dabrowski, W., Litke, A.M. & Chichilnisky, E.J. (2013). Focal electrical stimulation of major ganglion cell types in the primate retina for the design of visual prostheses. The Journal of Neuroscience 33, 7194–7205.Google Scholar
Jusuf, P.R., Lee, S.C., Hannibal, J. & Grunert, U. (2007). Characterization and synaptic connectivity of melanopsin-containing ganglion cells in the primate retina. The European Journal of Neuroscience 26, 2906–2921.Google Scholar
Klug, K., Herr, S., Ngo, I.T., Sterling, P. & Schein, S. (2003). Macaque retina contains an S-cone OFF midget pathway. The Journal of Neuroscience 23, 9881–9887.CrossRefGoogle ScholarPubMed
Koilkonda, R.D., Hauswirth, W.W. & Guy, J. (2009). Efficient expression of self-complementary AAV in ganglion cells of the ex vivo primate retina. Molecular Vision 15, 2796–2802.Google ScholarPubMed
Kolb, H., Goede, P., Roberts, S., McDermott, R. & Gouras, P. (1992). Uniqueness of the S-cone pedicle in the human retina and consequences for color processing. The Journal of Comparative Neurology 386, 443–460.Google Scholar
Kolb, H., Linberg, K.A. & Fisher, S.K. (1992). Neurons of the human retina: a Golgi study. The Journal of Comparative Neurology 318, 147–187.Google Scholar
Li, W. & DeVries, S.H. (2006). Bipolar cell pathways for color and luminance vision in a dichromatic mammalian retina. Nature Neuroscience 9, 669–675.Google Scholar
Light, A.C., Zhu, Y., Shi, J., Saszik, S., Lindstrom, S., Davidson, L., Li, X., Chiodo, V.A., Hauswirth, W.W., Li, W. & DeVries, S.H. (2012). Organizational motifs for ground squirrel cone bipolar cells. The Journal of Comparative Neurology 520, 2864–2887.Google Scholar
Linberg, K.A., Suemune, S. & Fisher, S.K. (1996). Retinal neurons of the California ground squirrel, Spermophilus beecheyi: A Golgi study. The Journal of Comparative Neurology 365, 173–216.3.0.CO;2-2>CrossRefGoogle ScholarPubMed
Liu, P.C. & Chiao, C.C. (2007). Morphologic identification of the OFF-type blue cone bipolar cell in the rabbit retina. Investigative Ophthalmology & Visual Science 48, 3388–3395.Google Scholar
MacNeil, M.A. & Gaul, P.A. (2008). Biocytin wide-field bipolar cells in rabbit retina selectively contact blue cones. The Journal of Comparative Neurology 506, 6–15.Google Scholar
Marc, R.E., Kalloniatis, M. & Jones, B.W. (2005). Excitation mapping with the organic cation AGB2+. Vision Research 45, 3454–3468.Google Scholar
Marshak, D. (1997). Secretoneurin-IR amacrine cells of the macaque retina. Investigative Ophthalmology & Visual Science 38, S50.Google Scholar
Marshak, D.W., Aldrich, L.B., Del Valle, J. & Yamada, T. (1990). Localization of immunoreactive cholecystokinin precursor to amacrine cells and bipolar cells of the macaque monkey retina. The Journal of Neuroscience 10, 3045–3055.CrossRefGoogle ScholarPubMed
Michael, C.R. (1968). Receptive fields of single optic nerve fibers in a mammal with an all-cone retina. 3. Opponent color units. Journal of Neurophysiology 31, 268–282.Google Scholar
Mills, S.L. & Tian, L.-M. (2012). The morphology and physiology of blue/green ganglion cells in the rabbit retina. Association for Research in Vision and Ophthalmology Annual Meeting, Ft. Lauderdale, FL.Google Scholar
Moritoh, S., Komatsu, Y., Yamamori, T. & Koizumi, A. (2013). Diversity of retinal ganglion cells identified by transient GFP transfection in organotypic tissue culture of adult marmoset monkey retina. PLoS One 8, e54667.Google Scholar
Packer, O.S., Verweij, J., Li, P.H., Schnapf, J.L. & Dacey, D.M. (2010). Blue-yellow opponency in primate S cone photoreceptors. The Journal of Neuroscience 30, 568–572.Google Scholar
Percival, K.A., Jusuf, P.R., Martin, P.R. & Grunert, U. (2009). Synaptic inputs onto small bistratified (blue-ON/yellow-OFF) ganglion cells in marmoset retina. The Journal of Comparative Neurology 517, 655–669.Google Scholar
Percival, K.A., Martin, P.R. & Grunert, U. (2011). Synaptic inputs to two types of koniocellular pathway ganglion cells in marmoset retina. The Journal of Comparative Neurology 519, 2135–2153.Google Scholar
Percival, K.A., Martin, P.R. & Grunert, U. (2013). Organisation of koniocellular-projecting ganglion cells and diffuse bipolar cells in the primate fovea. The European Journal of Neuroscience 37, 1072–1089.Google Scholar
Peterson, B.B. & Dacey, D.M. (2000). Morphology of wide-field bistratified and diffuse human retinal ganglion cells. Visual Neuroscience 17, 567–578.Google Scholar
Petrusca, D., Grivich, M.I., Sher, A., Field, G.D., Gauthier, J.L., Greschner, M., Shlens, J., Chichilnisky, E.J. & Litke, A.M. (2007). Identification and characterization of a Y-like primate retinal ganglion cell type. The Journal of Neuroscience 27, 11019–11027.Google Scholar
Puller, C. & Haverkamp, S. (2011). Bipolar cell pathways for color vision in non-primate dichromats. Visual Neuroscience 28, 51–60.Google Scholar
Puller, C., Ondreka, K. & Haverkamp, S. (2011). Bipolar cells of the ground squirrel retina. The Journal of Comparative Neurology 519, 759–774.Google Scholar
Ringo, J.L. & Wolbarsht, M.L. (1986). Spectral coding in cat retinal ganglion cell receptive fields. Journal of Neurophysiology 55, 320–330.Google Scholar
Rockhill, R.L., Daly, F.J., MacNeil, M.A., Brown, S.P. & Masland, R.H. (2002). The diversity of ganglion cells in a mammalian retina. The Journal of Neuroscience 22, 3831–3843.CrossRefGoogle Scholar
Rodieck, R.W. (1991). Which Cells Code for Color? In From Pigments to Perception, eds. Valberg, A. & Lee, B.B., pp. 83–93. New YorkPlenum Press.Google Scholar
Rowe, M.H. & Cox, J.F. (1993). Spatial receptive-field structure of cat retinal W cells. Visual Neuroscience 10, 765–779.Google Scholar
Schuurmans, R.P. & Zrenner, E. (1981). Responses of the blue sensitive cone system from the visual cortex and the arterially perfused eye in cat and monkey. Vision Research 21, 1611–1615.Google Scholar
Sher, A. & DeVries, S.H. (2012). A non-canonical pathway for mammalian blue-green color vision. Nature Neuroscience 15, 952–953.Google Scholar
Shinomori, K. & Werner, J.S. (2012). Aging of human short-wave cone pathways. Proceedings of the National Academy of Sciences of the United States of America 109, 13422–13427.Google Scholar
Siegert, S., Cabuy, E., Scherf, B.G., Kohler, H., Panda, S., Le, Y.Z., Fehling, H.J., Gaidatzis, D., Stadler, M.B. & Roska, B. (2012). Transcriptional code and disease map for adult retinal cell types. Nature Neuroscience 15, 487–495, S481–482.Google Scholar
Silveira, L.C., Lee, B.B., Yamada, E.S., Kremers, J., Hunt, D.M., Martin, P.R. & Gomes, F.L. (1999). Ganglion cells of a short-wavelength-sensitive cone pathway in New World monkeys: Morphology and physiology. Visual Neuroscience 16, 333–343.Google Scholar
Solomon, S.G., Lee, B.B., White, A.J., Ruttiger, L. & Martin, P.R. (2005). Chromatic organization of ganglion cell receptive fields in the peripheral retina. The Journal of Neuroscience 25, 4527–4539.CrossRefGoogle ScholarPubMed
Tian, N. (2008). Synaptic activity, visual experience and the maturation of retinal synaptic circuitry. The Journal of Physiology 586, 4347–4355.Google Scholar
van Hateren, J.H., Ruttiger, L., Sun, H. & Lee, B.B. (2002). Processing of natural temporal stimuli by macaque retinal ganglion cells. The Journal of Neuroscience 22, 9945–9960.Google Scholar
Vaney, D.I., Levick, W.R. & Thibos, L.N. (1981). Rabbit retinal ganglion cells. Receptive field classification and axonal conduction properties. Experimental Brain Research 44, 27–33.Google Scholar
Venkataramani, S. & Taylor, W.R. (2010). Orientation selectivity in rabbit retinal ganglion cells is mediated by presynaptic inhibition. The Journal of Neuroscience 30, 15664–15676.Google Scholar
Werblin, F.S. (2011). The retinal hypercircuit: A repeating synaptic interactive motif underlying visual function. The Journal of Physiology 589, 3691–3702.Google Scholar
West, R.W. (1976). Light and electron microscopy of the ground squirrel retina: functional considerations. The Journal of Comparative Neurology 168, 355–377.Google Scholar
Yamada, E.S., Bordt, A.S. & Marshak, D.W. (2005). Wide-field ganglion cells in macaque retinas. Visual Neuroscience 22, 383–393.Google Scholar
Yeh, T., Lee, B.B. & Kremers, J. (1995). Temporal response of ganglion cells of the macaque retina to cone-specific modulation. Journal of the Optical Society of America A, Optics, Image Science, and Vision 12, 456–464.Google Scholar
Yin, L., Smith, R.G., Sterling, P. & Brainard, D.H. (2009). Physiology and morphology of color-opponent ganglion cells in a retina expressing a dual gradient of S and M opsins. The Journal of Neuroscience 29, 2706–2724.Google Scholar
Zrenner, E. (1983). Neurophysiological Aspects of Color Vision in Primates. New York: Springer-Verlag.Google Scholar
Zrenner, E. & Gouras, P. (1981). Characteristics of the blue sensitive cone mechanism in primate retinal ganglion cells. Vision Research 21, 1605–1609.Google Scholar