Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-12-07T12:00:20.592Z Has data issue: false hasContentIssue false
  • English
  • Français

Bipolar cell pathways for color vision in non-primate dichromats

Published online by Cambridge University Press:  12 November 2010

CHRISTIAN PULLER  and
SILKE HAVERKAMP
CHRISTIAN PULLER
Affiliation:
Department of Neuroanatomy, Max Planck Institute for Brain Research, Frankfurt a.M., Germany
SILKE HAVERKAMP*
Affiliation:
Department of Neuroanatomy, Max Planck Institute for Brain Research, Frankfurt a.M., Germany
*
†Address correspondence and reprint requests to: Silke Haverkamp, Max Planck Institute for Brain Research, Deutschordenstr 46, D-60528 Frankfurt a.M., Germany. E-mail: haverkamp@mpih-frankfurt.mpg.de
Get access Rights & Permissions [Opens in a new window]

Abstract

Color vision in mammals is based on the expression of at least two cone opsins that are sensitive to different wavelengths of light. Furthermore, retinal pathways conveying color-opponent signals are required for color discrimination. Most of the primates are trichromats, and “color-coded channels” of their retinas are unveiled to a large extent. In contrast, knowledge of cone-selective pathways in nonprimate dichromats is only slowly emerging, although retinas of dichromats like mice or rats are extensively studied as model systems for retinal information processing. Here, we review recent progress of research on color-coded pathways in nonprimate dichromats to identify differences or similarities between di- and trichromatic mammals. In addition, we applied immunohistochemical methods and confocal microscopy to retinas of different species and present data on their neuronal properties, which are expected to contribute to color vision. Basic neuronal features such as the “blue cone bipolar cell” exist in every species investigated so far. Moreover, there is increasing evidence for chromatic OFF channels in dichromats and retinal ganglion cells that relay color-opponent signals to the brain. In conclusion, di- and trichromats share similar retinal pathways for color transmission and processing.

Keywords

Color codingParallel pathwaysBlue cone bipolar cellsHorizontal cellsGlutamate receptors
Type
Review Article
Information
Visual Neuroscience , Volume 28 , Issue 1 , January 2011 , pp. 51 - 60
Copyright
Copyright © Cambridge University Press 2010

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.)

References

Ahnelt, P., Keri, C. & Kolb, H. (1990). Identification of pedicles of putative blue-sensitive cones in the human retina. The Journal of Comparative Neurology 293, 39–53.CrossRefGoogle ScholarPubMed
Berglund, K., Schleich, W., Krieger, P., Loo, L.S., Wang, D., Cant, N.B., Feng, G., Augustine, G.J. & Kuner, T. (2006). Imaging synaptic inhibition in transgenic mice expressing the chloride indicator, Clomeleon. Brain Cell Biology 35, 207–228.CrossRefGoogle ScholarPubMed
Boycott, B. & Wässle, H. (1999). Parallel processing in the mammalian retina: The Proctor Lecture. Investigative Ophthalmology & Visual Science 40, 1313–1327.Google ScholarPubMed
Breuninger, T., Puller, C., Haverkamp, S. & Euler, T. (2009). Chromatic pathways in the mouse retina. Invest. Ophthalmol. Vis. Sci. 50: E-Abstract 3476.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.CrossRefGoogle ScholarPubMed
Chan, T.L., Martin, P.R., Clunas, N. & Grünert, U. (2001). Bipolar cell diversity in the primate retina: Morphologic and immunocytochemical analysis of a new world monkey, the marmoset Callithrix jacchus. The Journal of Comparative Neurology 437, 219–239.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Cohen, E. & Sterling, P. (1990). 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 330, 323–328.Google ScholarPubMed
Crook, D., Manookin, M., Packer, O.S. & Dacey, D.M. (2010). Excitatory synaptic conductances mediate ‘blue-yellow’ and ‘red-green’ opponency in macaque monkey retinal ganglion cells. ARVO abstr 5178.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Dacey, D.M., Lee, B.B., Stafford, D.K., Pokorny, J. & Smith, V.C. (1996). Horizontal cells of the primate retina: Cone specificity without spectral opponency. Science 271, 656–659.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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
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.CrossRefGoogle ScholarPubMed
Ekesten, B. & Gouras, P. (2008). Cone inputs to murine striate cortex. BMC Neuroscience 9, 113.CrossRefGoogle ScholarPubMed
Ekesten, B., Gouras, P. & Yamamoto, S. (2000). Cone inputs to murine retinal ganglion cells. Vision Research 40, 2573–2577.CrossRefGoogle ScholarPubMed
Euler, T. & Wässle, H. (1995). Immunocytochemical identification of cone bipolar cells in the rat retina. The Journal of Comparative Neurology 361, 461–478.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1981). Functional architecture of cone bipolar cells in mammalian retina. Vision Research 21, 1559–1563.CrossRefGoogle ScholarPubMed
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
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. Visual Neuroscience 12, 1159–1164.Google 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.CrossRefGoogle ScholarPubMed
Fyk-Kolodziej, B. & Pourcho, R.G. (2007). Differential distribution of hyperpolarization-activated and cyclic nucleotide-gated channels in cone bipolar cells of the rat retina. The Journal of Comparative Neurology 501, 891–903.CrossRefGoogle ScholarPubMed
Ghosh, K.K., Bujan, S., Haverkamp, S., Feigenspan, A. & Wässle, H. (2004). Types of bipolar cells in the mouse retina. The Journal of Comparative Neurology 469, 70–82.CrossRefGoogle ScholarPubMed
Ghosh, K.K. & Grünert, U. (1999). Synaptic input to small bistratified (blue-ON) ganglion cells in the retina of a new world monkey, the marmoset Callithrix jacchus. The Journal of Comparative Neurology 413, 417–428.3.0.CO;2-H>CrossRefGoogle ScholarPubMed
Ghosh, K.K., Martin, P.R. & Grünert, 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
Goodchild, A.K., Chan, T.L. & Grünert, U. (1996). Horizontal cell connections with short-wavelength-sensitive cones in macaque monkey retina. Visual Neuroscience 13, 833–845.CrossRefGoogle ScholarPubMed
Hack, I. & Peichl, L. (1999). Horizontal cells of the rabbit retina are non-selectively connected to the cones. The European Journal of Neuroscience 11, 2261–2274.CrossRefGoogle Scholar
Haverkamp, S., Grünert, U. & Wässle, H. (2001 a). Localization of kainate receptors at the cone pedicles of the primate retina. The Journal of Comparative Neurology 436, 471–486.CrossRefGoogle ScholarPubMed
Haverkamp, S., Grünert, U. & Wässle, H. (2001 b). The synaptic architecture of AMPA receptors at the cone pedicle of the primate retina. The Journal of Neuroscience 21, 2488–2500.CrossRefGoogle ScholarPubMed
Haverkamp, S., Wässle, 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Jacobs, G.H., Blakeslee, B. & Tootell, R.B. (1981). Color-discrimination tests on fibers in ground squirrel optic nerve. Journal of Neurophysiology 45, 903–914.CrossRefGoogle ScholarPubMed
Jacobs, G.H. & Tootell, R.B. (1981). Spectral-response properties of optic-nerve fibers in the ground squirrel. Journal of Neurophysiology 45, 891–902.CrossRefGoogle ScholarPubMed
Jacobs, G.H., Williams, G.A., Cahill, H. & Nathans, J. (2007). Emergence of novel color vision in mice engineered to express a human cone photopigment. Science 315, 1723–1725.CrossRefGoogle ScholarPubMed
Jeon, C.J. & Masland, R.H. (1995). A population of wide-field bipolar cells in the rabbits retina. The Journal of Comparative Neurology 360, 403–412.CrossRefGoogle 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
Kolb, H. & Dekorver, L. (1991). Midget ganglion cells of the parafovea of the human retina: A study by electron microscopy and serial section reconstructions. The Journal of Comparative Neurology 303, 617–636.CrossRefGoogle ScholarPubMed
Kouyama, N. & Marshak, D. (1992). Bipolar cells specific for blue cones in the macaque retina. The Journal of Neuroscience 12, 1233–1252.CrossRefGoogle ScholarPubMed
Kryger, Z., Galli-Resta, L., Jacobs, G.H. & Reese, B.E. (1998). The topography of rod and cone photoreceptors in the retina of the ground squirrel. Visual Neuroscience 15, 685–691.CrossRefGoogle ScholarPubMed
Lee, S.C. & Grünert, U. (2007). Connections of diffuse bipolar cells in primate retina are biased against S-cones. The Journal of Comparative Neurology 502, 126–140.CrossRefGoogle ScholarPubMed
Lee, S.C., Telkes, I. & Grünert, U. (2005). S-cones do not contribute to the OFF-midget pathway in the retina of the marmoset, Callithrix jacchus. The European Journal of Neuroscience 22, 437–447.CrossRefGoogle ScholarPubMed
Li, W. & DeVries, S.H. (2004). Separate blue and green cone networks in the mammalian retina. Nature Neuroscience 7, 751–756.CrossRefGoogle ScholarPubMed
Li, W. & DeVries, S.H. (2006). Bipolar cell pathways for color and luminance vision in a dichromatic mammalian retina. Visual Neuroscience 9, 669–675.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.CrossRefGoogle ScholarPubMed
Luo, X., Ghosh, K.K., Martin, P.R. & Grünert, U. (1999). Analysis of two types of cone bipolar cells in the retina of a New World monkey, the marmoset, Callithrix jacchus. Visual Neuroscience 16, 707–719.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Mariani, A.P. (1984). Bipolar cells in monkey retina selective for the cones likely to be blue-sensitive. Nature 308, 184–186.CrossRefGoogle ScholarPubMed
Martin, P.R. (2004). Colour through the thalamus. Clinical & Experimental Optometry 87, 249–257. Review.CrossRefGoogle ScholarPubMed
Mataruga, A., Kremmer, E. & Müller, F. (2007). Type 3a and type 3b OFF cone bipolar cells provide for the alternative rod pathway in the mouse retina. The Journal of Comparative Neurology 502, 1123–1137.CrossRefGoogle ScholarPubMed
Michael, C.R. (1966). Receptive fields of opponent color units in the optic nerve of the ground squirrel. Science 152, 1095–1097.CrossRefGoogle ScholarPubMed
Mollon, J.D. (1989). “Tho’ she kneel’d in that place where they grew.” The uses and origins of primate colour vision. The Journal of Experimental Biology 146, 21–38.CrossRefGoogle ScholarPubMed
Müller, B. & Peichl, L. (1993). Horizontal cells in the cone-dominated tree shrew retina: Morphology, photoreceptor contacts, and topographical distribution. The Journal of Neuroscience 13, 3628–3646.CrossRefGoogle ScholarPubMed
Nathans, J. (1999). The evolution and physiology of human color vision: Insights from molecular genetic studies of visual pigments. Neuron 24, 299–312.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Peichl, L. (2005). Diversity of mammalian photoreceptor properties: Adaptations to habitat and lifestyle? The Anatomical Record. Part A, Discoveries in Molecular, Cellular, and Evolutionary Biology 287, 1001–1012. Review.CrossRefGoogle ScholarPubMed
Peichl, L. (2010). Morphology of interneurons: Horizontal cells. In Encyclopedia of the Eye, Vol. 3, ed. Dartt, D.A., pp. 56–64. Oxford, UK: Academic Press.Google Scholar
Peichl, L. & González-Soriano, J. (1994). Morphological types of horizontal cell in rodent retinae: a comparison of rat, mouse, gerbil and guinea pig. Visual Neuroscience 11, 501–517.CrossRefGoogle ScholarPubMed
Percival, K.A., Jusuf, P.R., Martin, P.R. & Grünert, U. (2009). Synaptic inputs onto small bistratified (blue-ON/yellow-OFF) ganglion cells in marmoset retina. The Journal of Comparative Neurology 517, 655–669.CrossRefGoogle ScholarPubMed
Pignatelli, V. & Strettoi, E. (2004). Bipolar cells of the mouse retina: A gene gun, morphological study. The Journal of Comparative Neurology 476, 254–266.CrossRefGoogle ScholarPubMed
Puller, C., Haverkamp, S. & Grünert, U. (2007). OFF midget bipolar cells in the retina of the marmoset, Callithrix jacchus, express AMPA receptors. The Journal of Comparative Neurology 502, 442–454.CrossRefGoogle ScholarPubMed
Röhrenbeck, J., Wässle, H. & Boycott, B.B. (1989) Horizontal cells in the monkey retina: Immunocytochemical staining with antibodies against calcium binding proteins. The European Journal of Neuroscience 1, 407–420.CrossRefGoogle ScholarPubMed
Röhrenbeck, J., Wässle, H. & Heizmann, C.W. (1987). Immunocytochemical labelling of horizontal cells in mammalian retina using antibodies against calcium-binding proteins. Neuroscience Letters 77, 255–260.CrossRefGoogle ScholarPubMed
Sandmann, D., Boycott, B.B. & Peichl, L. (1996). Blue-cone horizontal cells in the retinae of horses and other equidae. The Journal of Neuroscience 16, 3381–3396.CrossRefGoogle ScholarPubMed
Sher, J.L. Gauthier, Field, G.D., Greschner, M., Shlens, J., Machado, T.A., Gunning, D.E., Mathieson, K., Litke, A.M. & Chichilnisky, E.J. (2009). Functional Identification of Individual Cones in the Receptive Fields of Primate Retinal Ganglion Cells. Invest. Ophthalmol. Vis. Sci. 50: E-Abstract 6150.Google Scholar
Vaney, D.I., Nelson, J.C. & Pow, D.V. (1998) Neurotransmitter coupling through gap junctions in the retina. The Journal of Neuroscience 18, 10594–10602.CrossRefGoogle ScholarPubMed
Vardi, N., Duvoisin, R., Wu, G. & Sterling, P. (2000). Localization of mGluR6 to dendrites of ON bipolar cells in primate retina. The Journal of Comparative Neurology 423, 402–412.3.0.CO;2-E>CrossRefGoogle Scholar
Wässle, H., Dacey, D.M., Haun, T., Haverkamp, S., Grünert, U. & Boycott, B.B. (2000). The mosaic of horizontal cells in the macaque monkey retina: With a comment on biplexiform ganglion cells. Visual Neuroscience 17, 591–608.CrossRefGoogle ScholarPubMed
Wässle, H., Grünert, U., Martin, P.R. & Boycott, B.B. (1994). Immunocytochemical characterization and spatial distribution of midget bipolar cells in the macaque monkey retina. Vision Research 34, 561–579.CrossRefGoogle ScholarPubMed
West, R.W. (1976). Light and electron microscopy of the ground squirrel retina: Functional considerations. The Journal of Comparative Neurology 168, 355–377.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Supplementary material: File

Puller supplementary material

Appendix.doc

Download Puller supplementary material(File)
File 32.3 KB