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Cone synapses in macaque fovea: I. Two types of non-S cones are distinguished by numbers of contacts with OFF midget bipolar cells

Published online by Cambridge University Press:  28 January 2011

STAN SCHEIN*
Affiliation:
Department of Psychology, Franz Hall, University of California, Los Angeles, Los Angeles, California Brain Research Institute, University of California, Los Angeles, Los Angeles, California California NanoSystems Institute, University of California, Los Angeles, Los Angeles, California
IVY TRAN NGO
Affiliation:
Department of Psychology, Franz Hall, University of California, Los Angeles, Los Angeles, California
TERESA M. HUANG
Affiliation:
Department of Psychology, Franz Hall, University of California, Los Angeles, Los Angeles, California
KARL KLUG
Affiliation:
Brain Research Institute, University of California, Los Angeles, Los Angeles, California
PETER STERLING
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania
STEVE HERR
Affiliation:
Department of Psychology, Franz Hall, University of California, Los Angeles, Los Angeles, California
*
*Address correspondence and reprint requests to: Stan Schein, Department of Psychology, Franz Hall, Mailcode 951563, University of California, Los Angeles, Los Angeles, CA 90095-1563. E-mail: schein@ucla.edu

Abstract

L and M cones, divided into two groups by absorption spectra, have not been distinguished by structure. Here, we report what may be such a difference. We reconstructed the synaptic terminals of 16 non-S cones and the dendritic arbors of their ON and OFF midget bipolar cells from high-magnification electron micrographs of serial thin sections of a small region of macaque fovea. Each cone terminal contacted a similar number (~16) of invaginating central elements provided by its ON midget bipolar cell. By contrast, the numbers of connections between a cone terminal and its OFF midget bipolar cell were grouped into two clusters: 30–37 versus 43–50 basal contacts in the triad-associated position and 41–47 versus 61–74 Outer Densities within those basal contacts. The coefficients of variation of these distributions were all in the range of 10% or lower, characteristic of single populations. If these two clusters correspond to M- and L-cone circuits, the results reveal structural differences between M and L cones and between their corresponding OFF midget bipolar cells.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

Ahmad, K.M., Klug, K., Herr, S., Sterling, P. & Schein, S. (2003). Cell density ratios in a foveal patch in macaque retina. Visual Neuroscience 20, 189209.CrossRefGoogle Scholar
Ahnelt, P.K., Keri, C. & Kolb, H. (1990). Identification of terminals of putative blue-sensitive cones in human and primate retina. The Journal of Comparative Neurology 293, 3953.CrossRefGoogle Scholar
Ahnelt, P.K., Kolb, H. & Pflug, R. (1987). Identification of subtype of cone photoreceptor, likely to be blue sensitive, in the human retina. The Journal of Comparative Neurology 255, 1834.Google Scholar
Bowmaker, J.K., Parry, J.W.L. & Mollon, J.D. (2003). The arrangement of L and M cones in human and a primate retina. In Normal and Defective Colour Vision, ed. Mollon, J.D., Pokorny, J. & Knoblauch, K., pp. 3950. Oxford: Oxford University Press.CrossRefGoogle Scholar
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: Light microscopy. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 255, 109176.Google Scholar
Boycott, B.B. & Hopkins, J.M. (1991). Cone bipolar cells and cone synapses in the primate retina. Visual Neuroscience 7, 4960.Google Scholar
Brainard, D.H., Roorda, A., Yamauchi, Y., Calderone, J.B., Metha, A., Neitz, M., Neitz, J., Williams, D.R. & Jacobs, G.H. (2000). Functional consequences of the relative numbers of L and M cones. Journal of the Optical Society of America A, Optics, Image Science, and Vision 17, 607614.Google Scholar
Calkins, D. (1994). Microcircuitry of M and L Cone Midget Ganglion Cell Pathways in the Primate Fovea. PhD thesis, Philadelphia, PA: University of Pennsylvania.Google Scholar
Calkins, D., Schein, S., Tsukamoto, Y. & Sterling, P. (1994). M and L cones in macaque fovea connect to midget ganglion cells by different numbers of excitatory synapses. Nature 371, 7072.CrossRefGoogle ScholarPubMed
Calkins, D. & Sterling, P. (2007). Microcircuitry for two types of achromatic ganglion cell in primate fovea. The Journal of Neuroscience 27, 26462653.CrossRefGoogle ScholarPubMed
Carroll, J., Neitz, M. & Neitz, J. (2002). Estimates of L:M cone ratio from ERG flicker photometry and genetics. Journal of Vision 2, 531542.CrossRefGoogle ScholarPubMed
Chun, M., Grünert, U., Martin, P. & Wässle, H. (1996). The synaptic complex of cones in the fovea and in the periphery of the macaque monkey retina. Vision Research 36, 33733381.CrossRefGoogle ScholarPubMed
Cicerone, C.M. & Nerger, J.L. (1989). The relative numbers of long-wavelength-sensitive to middle-wavelength-sensitive cones in the human fovea centralis. Vision Research 29, 115128.Google Scholar
Cohen, E. & Sterling, P. (1990) Demonstration of cell types among cone bipolar neurons of cat retina. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 330, 305321.Google ScholarPubMed
Cohen, E. & Sterling, P. (1992). Parallel circuits from cones to the on-beta ganglion cell. The European Journal of Neuroscience 4, 506520.Google Scholar
Deeb, S.S., Diller, L.C., Williams, D.R. & Dacey, D.M. (2000). Interindividual and topographical variation in L:M cone ratios in monkey retinas. Journal of the Optical Society of America A, Optics, Image Science, and Vision 17, 538544.CrossRefGoogle Scholar
Dobkins, K.R., Thiele, A. & Albright, T.D. (2000). Comparison of red-green equiluminance points in humans and macaques: Evidence for different L:M cone ratios between species. Journal of the Optical Society of America A, Optics, Image Science, and Vision 17, 545556.Google Scholar
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, MA: Harvard University Press.Google Scholar
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: Electron microscopy. Proceedings of the Royal Society of London. Series B, Biological Sciences 166, 80111.Google Scholar
Eggers, G., Sterling, P. & Schein, S. (1999). Midget bipolar cells makes three types of membrane density with midget ganglion cells. Investigative Ophthalmology & Visual Science 40, S813.Google Scholar
Eriköz, B., Jusuf, P.R., Percival, K.A. & Grünert, U. (2008). Distribution of bipolar input to midget and parasol ganglion cells in marmoset retina. Visual Neuroscience 25, 6776.Google Scholar
Hagstrom, S.A., Neitz, J. & Neitz, M. (1998). Variations in cone populations for red-green color vision examined by analysis of mRNA. Neuroreport 9, 19631967.CrossRefGoogle ScholarPubMed
Hartigan, J.A. & Hartigan, P.M. (1985). The dip test of unimodality. Annals of Statistics 13, 7084.Google Scholar
Haverkamp, S., Grünert, U. & Wässle, H. (2001). The synaptic architecture of AMPA receptors at the cone pedicle of the primate retina. The Journal of Neuroscience 21, 24882500.CrossRefGoogle ScholarPubMed
Hering, E. (1878). Zur Lehre von Lichtsinne. Vienna, Austria: C. Gerold’s Sohn.Google Scholar
Hering, E. (1920). Outlines of a Theory of the Light Sense, trans. Hurvich, L.M. & Jameson, D. (1964). Cambridge, MA: Harvard University Press.Google Scholar
Herr, S., Klug, K., Sterling, P. & Schein, S. (2003). Inner S-cone bipolar cells provide all of the central elements for S cones in macaque retina. The Journal of Comparative Neurology 457, 185201.Google Scholar
Herr, S., Ngo, I.T., Huang, T.M., Klug, K., Sterling, P. & Schein, S. (2011). Cone synapses in macaque fovea: II. Dendrites of OFF midget bipolar cells exhibit Inner Densities similar to their outer synaptic densities in basal contacts with cone terminals. Visual Neuroscience, 28, xxxxxx.Google Scholar
Hofer, H., Carroll, J., Neitz, J., Neitz, M. & Williams, D.R. (2005). Organization of the human trichromatic cone mosaic. The Journal of Neuroscience 25, 96699679.Google Scholar
Hopkins, J.M. & Boycott, B.B. (1992). Synaptic contacts of a two-cone flat bipolar cell in a primate retina. Visual Neuroscience 8, 379384.CrossRefGoogle Scholar
Hopkins, J.M. & Boycott, B.B. (1997). The cone synapses of cone bipolar cells of primate retina. Journal of Neurocytology 26, 313325.Google Scholar
Hurvich, L. & Jameson, D. (1957). An opponent-process theory of color vision. Psychological Review 64, 384404.Google Scholar
Jacobs, G.H. & Deegan, J.F. II (1997). Spectral sensitivity of macaque monkeys measured with ERG flicker photometry. Visual Neuroscience 14, 921928.CrossRefGoogle ScholarPubMed
Jusuf, P.R., Martin, P.R. & Grünert, U. (2006). Synaptic connectivity in the midget-parvocellular pathway of primate central retina. The Journal of Comparative Neurology 494, 260274.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, 98819887.Google Scholar
Kolb, H. (1970). Organization of the outer plexiform layer of the primate retina: Electron microscopy of Golgi-impregnated cells. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 258, 261283.Google Scholar
Kolb, H., Boycott, B.B. & Dowling, J.E. (1969). A second type of midget bipolar cell in the primate retina. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 255, 177184.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, 146187.Google Scholar
Kuchenbecker, J.A., Sahay, M., Tait, D.M., Neitz, M. & Neitz, J. (2008). Topography of the long- to middle-wavelength sensitive cone ratio in the human retina assessed with a wide-field color multifocal electroretinogram. Visual Neuroscience 25, 301306.CrossRefGoogle Scholar
Lerea, C.L., Bunt-Milam, A.H. & Hurley, B. (1989). Alpha transducin is present in blue-, green-, and red-sensitive cone photoreceptors in the human retina. Neuron 3, 367376.Google Scholar
Mechler, F. & Ringach, D.L. (2002). On the classification of simple and complex cells. Vision Research 42, 10171033.Google Scholar
Meyers, D., Skinner, S. & Sloan, K. (1992). Surfaces from contours. ACM Transactions on Graphics 11, 228258.Google Scholar
Missotten, L. (1965). The Ultrastructure of the Human Retina. Brussels, Belgium: Editions Arscia S.A.Google Scholar
Milam, A.H., Dacey, D.M. & Dizhoor, A.M. (1993). Recoverin immunoreactivity in mammalian cone bipolar cells. Visual Neuroscience 10, 112.CrossRefGoogle ScholarPubMed
Mollon, J.D. & Bowmaker, J.K. (1992). The spatial arrangement of cones in the primate fovea. Nature 360, 677679.CrossRefGoogle ScholarPubMed
Neitz, M., Balding, S.D., McMahon, C., Sjoberg, S.A. & Neitz, J. (2006). Topography of long- and middle-wavelength sensitive cone opsin gene expression in human and Old World monkey retina. Visual Neuroscience 23, 379385.CrossRefGoogle ScholarPubMed
Nomura, A., Shigemoto, R., Nakamura, Y., Okamoto, N., Mizuno, N. & Nakanishi, S. (1994). Developmentally regulated postsynaptic localization of a metabotropic glutamate receptor in rat rod bipolar cells. Cell 77, 361369.Google Scholar
Otake, S. & Cicerone, C. (2000). L and M cone relative numerosity and red-green opponency from fovea to mid-periphery in the human retina. Journal of the Optical Society of America A, Optics, Image Science, and Vision 17, 615627.CrossRefGoogle Scholar
Packer, O.S., Williams, D.R. & Bensinger, D.G. (1996). Photopigment transmittance imaging of the primate photoreceptor mosaic. The Journal of Neuroscience 16, 22512260.CrossRefGoogle ScholarPubMed
Polyak, S.L. (1941). The Retina. Chicago, IL: University of Chicago Press.Google Scholar
Raviola, E. & Gilula, N.B. (1975). Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits. The Journal of Cell Biology 65, 192222.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1991). Which cells code for color? In From Pigments to Perception: Advances in Understanding Visual Elements, ed. Valberg, A. & Lee, B.B., pp. 8389. New York: Plenum.Google Scholar
Roorda, A., Mehta, A.B., Lennie, P. & Williams, D.A. (2001). Packing arrangement of the three cone classes in the primate retina. Vision Research 41, 12911306.CrossRefGoogle ScholarPubMed
Roorda, A. & Williams, D.A. (1999). The arrangement of the three cone classes in the human eye. Nature 397, 520522.CrossRefGoogle Scholar
Schein, S.J. (1988). Anatomy of macaque fovea and spatial densities of neurons in foveal representation. The Journal of Comparative Neurology 269, 479505.CrossRefGoogle ScholarPubMed
Shevell, S.K. & Humanski, R.A. (1988). Color perception under chromatic adaptation: Red/green equilibria with adapted short-wavelength-sensitive cones. Vision Research 12, 13451356.CrossRefGoogle Scholar
Shinomori, K., Spillmann, L. & Werner, J.S. (1999). S-cone signals to temporal OFF-channels: Asymmetrical connections to postreceptoral chromatic mechanisms. Vision Research 39, 3949.Google Scholar
Smith, R.G. (1987). Montage: A system for three-dimensional reconstruction by personal computer. Journal of Neuroscience Methods 21, 5569.CrossRefGoogle ScholarPubMed
Szél, A., Diamantstein, T. & Rohlich, P. (1988). Identification of the blue-sensitive cones in the mammalian retina by anti-visual pigment antibody. The Journal of Comparative Neurology 273, 593602.CrossRefGoogle ScholarPubMed
Tan, P.-N., Steinbach, M. & Kumar, V. (2006). Introduction to Data Mining. Harlow, UK: Addison-Wesley Longman.Google Scholar
Telkes, I., Lee, S.C.S., Jusuf, P.R. & Grünert, U. (2008). The midget-parvocellular pathway of marmoset retina: A quantitative light microscopic study. The Journal of Comparative Neurology 510, 539549.Google Scholar
Tsukamoto, Y., Masarachia, P., Schein, S. & Sterling, P. (1992). Gap junctions between the terminals of macaque foveal cones. Vision Research 32, 18091815.Google Scholar
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, 402412.3.0.CO;2-E>CrossRefGoogle Scholar
Vardi, N., Morigiwa, K., Wang, T.L., Shi, Y.J. & Sterling, P. (1998). Neurochemistry of the mammalian cone ‘synaptic complex’. Vision Research 38, 13591369.Google Scholar
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, 561579.CrossRefGoogle ScholarPubMed
Wooten, B.R. & Werner, J.S. (1979). Short-wave cone input to the red-green opponent channel. Vision Research 19, 10531054.Google Scholar
Wuerger, S.M., Atkinson, P. & Cropper, S. (2005) The cone inputs to the unique-hue mechanisms. Vision Research 45, 32103223.CrossRefGoogle Scholar