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Amacrine cell contributions to red-green color opponency in central primate retina: A model study

Published online by Cambridge University Press:  28 September 2007

D.S. LEBEDEV  and
D.W. MARSHAK
D.S. LEBEDEV
Affiliation:
Laboratory of Sensory Information Processing, Institute for Information Transmission Problems, Moscow, Russia
D.W. MARSHAK
Affiliation:
Department of Neurobiology and Anatomy, University of Texas Medical School, Houston, Texas
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Abstract

To investigate the contributions of amacrine cells to red-green opponency, a linear computational model of the central macaque retina was developed based on a published cone mosaic. In the model, amacrine cells of ON and OFF types received input from all neighboring midget bipolar cells of the same polarity, but OFF amacrine cells had a bias toward bipolar cells whose center responses were mediated by middle wavelength sensitive cones. This bias might arise due to activity dependent plasticity because there are midget bipolar cells driven by short wavelength sensitive cones in the OFF pathway. The model midget ganglion cells received inputs from neighboring amacrine cells of both types. As in physiological experiments, the model ganglion cells showed spatially opponent responses to achromatic stimuli, but they responded to cone isolating stimuli as though center and surround were each driven by a single cone type. Without amacrine cell input, long and middle wavelength sensitive cones contributed to both the centers and surrounds of model ganglion cell receptive fields. According to the model, the summed amacrine cell input was red-green opponent even though inputs to individual amacrine cells were unselective. A key prediction is that GABA and glycine depolarize two of the four types of central midget ganglion cells; this may reflect lower levels of the potassium chloride co-transporter in their dendrites.

Keywords

Midget ganglion cellColor visionParvocellularPrimateParafovea
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 4 , July 2007 , pp. 535 - 547
Copyright
© 2007 Cambridge University Press

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References

REFERENCES

Abbott, L.F. & Nelson, S.B. (2000). Synaptic plasticity: Taming the beast. Nature Neuroscience 3, 1178–1183.CrossRefGoogle Scholar
Benardete, E.A. & Kaplan, E. (1999). Dynamics of primate P retinal ganglion cells: Responses to chromatic and achromatic stimuli. Journal of Physiology 519, 775–790.CrossRefGoogle Scholar
Boos, R., Schneider, H. & Wässle, H. (1993). Voltage- and transmitter-gated currents of All-amacrine cells in a slice preparation of the rat retina. Journal of Neuroscience 13, 2874–2888.Google Scholar
Boycott, B.B., Hopkins, J.M. & Sperling, H.G. (1987). Cone connections of the horizontal cells of the rhesus monkey's retina. Proceedings of the Royal Society B 229, 345–379.CrossRefGoogle Scholar
Buzás, P., Blessing, E.M., Szmajda, B.A. & Martin, P.R. (2006). Specificity of M and L cone inputs to receptive fields in the parvocellular pathway: Random wiring with functional bias. Journal of Neuroscience 26, 1148–1161.CrossRefGoogle Scholar
Calkins, D.J. & Sterling, P. (1996). Absence of spectrally specific lateral inputs to midget ganglion cells in primate retina. Nature 381, 613–615.CrossRefGoogle Scholar
Calkins, D.J, Schein, S.J., 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, 70–72.CrossRefGoogle Scholar
Calkins, D.J. (2001). Seeing with S cones. Progress in Retinal and Eye Research 20, 255–287.CrossRefGoogle Scholar
Callaway, E.M. (2005). Structure and function of parallel pathways in the primate early visual system. Journal of Physiology 566, 13–19.CrossRefGoogle Scholar
Campbell, F.W. & Gubish, R.W. (1966). Optical quality of the human eye. Journal of Physiology 186, 558–578.CrossRefGoogle Scholar
Croner, L.J. & Kaplan, E. (1995). Receptive fields of P and M ganglion cells across the primate retina. Vision Research 35, 7–24.CrossRefGoogle 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.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 Scholar
Dacey, D.M. (1999). Primate retina: Cell types, circuits and color opponency. Progress in Retinal and Eye Research 18, 737–763.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 Scholar
Dacheux, R.F. & Raviola, E. (1990). Physiology of H1 horizontal cells in the primate retina. Proceedings of the Royal Society B 239, 213–230.CrossRefGoogle Scholar
Dacheux, R.F., Chimento, M.F. & Amthor, F.R. (2003). Synaptic input to the On-Off directionally selective ganglion cell in the rabbit retina. Journal of Comparative Neurology 456, 267–278.CrossRefGoogle Scholar
Dan, Y. & Poo, M.M. (2004). Spike timing dependent plasticity of neural circuits. Neuron 44, 23–30.CrossRefGoogle Scholar
Deeb, S.S., Diller, L.C., Williams, D.R. & Dacey, D.M. (2000). Interindividual and topographical variation of L:M cone ratios in monkey retinas. Journal of the Optical Society of America A: Optics, Image Science and Vision 17, 538–544.CrossRefGoogle Scholar
De Monasterio, F.M. & Gouras, P. (1975). Functional properties of ganglion cells of the rhesus monkey retina. Journal of Physiology 251, 167–195.CrossRefGoogle Scholar
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: Electron microscopy. Proceedings of the Royal Society London B Biological Sciences 166, 80–111.CrossRefGoogle Scholar
Hornstein, H.P., Verveij, J. & Schnapf, J.L. (2004). Electrical coupling between red and green cones in primate retina. Nature Neuroscience 7, 745–750.CrossRefGoogle Scholar
Jusuf, P.R., Martin, P.R. & Grünert, U. (2006). Synaptic connectivity in the midget-parvocellular pathway of primate central retina. Journal of Comparative Neurology 494, 260–274.CrossRefGoogle Scholar
Kaplan, E., Purpura, K. & Shapley, R.M. (1988). Color and luminance contrast as tools for probing the primate retina. Neuroscience Research 8, S151–S165.CrossRefGoogle Scholar
Klug, K., Herr, S., Ngo, I.T., Sterling, P. & Schein, S. (2003). Macaque retina contains an S cone OFF midget pathway. Journal of Neuroscience 23, 9881–9887.Google Scholar
Kolb, H. & Dekorver, L. (1991). Midget ganglion cells of the parafovea of the human retina: A study by electron microscopy and serial section reconstructions. Journal of Comparative Neurology 303, 617–636.CrossRefGoogle Scholar
Kolb, H., Linberg, K.A. & Fisher, S.K. (1992). Neurons of the human retina: A Golgi study. Journal of Comparative Neurology 318, 147–187.CrossRefGoogle Scholar
Kolb, H. & Marshak, D.W. (2003). The midget pathways of the primate retina. Documenta Ophthalmologica 106, 67–81.CrossRefGoogle Scholar
Kolb, H., Zhang, L., DeKorver, L. & Cuenca, N. (2002). A new look at calretinin-immunoreactive amacrine cell types in the monkey retina. Journal of Comparative Neurology 453, 168–184.CrossRefGoogle Scholar
Koontz, M. & Hendrickson, A.E. (1987). Stratified distribution of synapses in the inner plexiform layer of primate retina. Journal of Comparative Neurology 263, 581–592.CrossRefGoogle Scholar
Kouyama, N. & Marshak, D.W. (1992). Bipolar cells specific for blue cones in the macaque retina. Journal of Neuroscience 12, 1233–1252.Google Scholar
Lebedev, D.S. & Marshak, D.W. (2006). Amacrine cell contributions to red-green opponency in central primate retina: A model study. Perception 35, 21.Google Scholar
Lebedev, D.S. (2003). A computational model of the midget pathways in the central primate retina. Sensory Systems 17, 91–106 (In Russian).Google Scholar
Lee, B.B. (2003). Structure of receptive field centers of midget retinal ganglion cells. In Normal and Defective Colour Vision, eds. Mollon, J.D., Pokorny, J. & Knoblauch, K., pp. 63–70. New York: Oxford University Press.CrossRef
Lee, B.B., Kremers, J. & Yeh, T. (1998). Receptive fields of primate retinal ganglion cells studied with a novel technique. Visual Neuroscience 15, 161–175.CrossRefGoogle Scholar
Lee, S.C.S. & Grünert, U. (2007). Connections of diffuse bipolar cells in primate retina are biased against S-cones. Journal of Comparative Neurology 502, 126–140.CrossRefGoogle Scholar
Lee, S.C.S., Telkes, I. & Grünert, U. (2005). Scones do not contribute to the OFF midget pathway in the retina of the marmoset, Callithrix jacchus. European Journal of Neuroscience 22, 437–447.CrossRefGoogle Scholar
Lennie, P., Haake, W. & Williams, D.R. (1991). The design of chromatically opponent receptive fields. In Computational Models of Visual Processing, eds. Landy, M.S. & Movshon, J.A. Cambridge, MA: MIT Press.
Mariani, A.P. (1990). Amacrine cells of the rhesus monkey retina. Journal of Comparative Neurology 15, 382–400.CrossRefGoogle Scholar
Martin, P.R., Lee, B.B., White, A.J., Solomon, S.G. & Ruttiger, L. (2001). Chromatic sensitivity of ganglion cells in the peripheral primate retina. Nature 410, 933–936.CrossRefGoogle Scholar
Marty, A. & Llano, I. (2005). Excitatory effects of GABA in established brain networks. Trends in Neurosciences 28, 284–289.CrossRefGoogle Scholar
Maximov, P.V., Marshak, D.W. & Lebedev, D.S. (2006). A role for the blue pathway in the development of red green opponency. Perception 35, 195.Google Scholar
McMahon, M.J., Lankheet, M.J., Lennie, P. & Williams, D.R. (2000). Fine structure of parvocellular receptive fields in the primate fovea revealed by laser interferometry. Journal of Neuroscience 20, 2043–2053.Google Scholar
Momiji, H., Bharath, A.A., Hankins, M.W. & Kennard, C. (2006). Numerical study of short-term afterimages and associate properties in foveal vision. Vision Research 46, 365–381.CrossRefGoogle Scholar
Momiji, H., Hankins, M.W., Bharath, A.A. & Kennard, C. (2007). A numerical study of red-green colour opponent properties in the primate retina. European Journal of Neuroscience 25, 1155–1165.CrossRefGoogle Scholar
Neitz, J., Carroll, J., Yamauchi, Y., Neitz, M. & Williams, D.R. (2002). Color perception is mediated by a plastic neural mechanism that is adjustable in adults. Neuron 35, 783–792.CrossRefGoogle Scholar
Packer, O.S. & Dacey, D.M. (2002). Receptive field structure of H1 horizontal cells in macaque monkey retina. Journal of Vision 2, 272–292.CrossRefGoogle Scholar
Passaglia, C.L., Troy, J.B., Ruttiger, L. & Lee, B.B. (2002). Orientation sensitivity of ganglion cells in primate retina. Vision Research 42, 683–694.CrossRefGoogle Scholar
Reid, R.C. & Shapley, R.M. (1992). Spatial structure of cone inputs to receptive fields in primate lateral geniculate nucleus. Nature 356, 716–718.CrossRefGoogle Scholar
Rodieck, R.W. (1965). Quantitative analysis of cat retinal ganglion cell responses to visual stimuli. Vision Research 5, 583–601.CrossRefGoogle Scholar
Roorda, A., Metha, A.B., Lennie, P. & Williams, D.R. (2001). Packing arrangement of the three cone classes in primate retina. Vision Research 41, 1291–1306.CrossRefGoogle Scholar
Shapley, R., Reid, R.C. & Kaplan, E. (1991). Receptive fields of P and M cells in the monkey retina and their photoreceptor inputs. Neuroscience Research 15, S199–S211.Google Scholar
Smith, E.L., 3rd, Chino, Y.M., Ridder, W.H., 3rd, Kitagawa, K. & Langston, A. (1990). Orientation bias of neurons in the lateral geniculate nucleus of macaque monkeys. Visual Neuroscience 5, 525–545.CrossRefGoogle Scholar
Smith, V.C., Lee, B.B., Pokorny, J., Martin, P.R. & Valberg, A. (1992). Responses of macaque ganglion cells to the relative phase of heterochromatically modulated lights. Journal of Physiology 458, 191–221.CrossRefGoogle Scholar
Solomon, S.G. & Lennie, P. (2007). The machinery of colour vision. Nature Reviews Neuroscience 8, 276–286.CrossRefGoogle 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. Journal of Neuroscience 25, 4527–4539.CrossRefGoogle Scholar
Vu, T.Q., Payne, J.A. & Copenhagen, D.R. (2000). Localization and developmental expression patterns of the neuronal KCl cotransporter (KCC2) in the rat retina. Journal of Neuroscience 20, 1414–1423.Google Scholar
Woodin, M.A., Ganguly, K. & Poo, M.M. (2003). Coincident pre and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl transporter activity. Neuron 39, 807–820.CrossRefGoogle Scholar