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The fundamental plan of the retina

Abstract

The retina, like many other central nervous system structures, contains a huge diversity of neuronal types. Mammalian retinas contain approximately 55 distinct cell types, each with a different function. The census of cell types is nearing completion, as the development of quantitative methods makes it possible to be reasonably confident that few additional types exist. Although much remains to be learned, the fundamental structural principles are now becoming clear. They give a bottom-up view of the strategies used in the retina's processing of visual information and suggest new questions for physiological experiments and modeling.

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Figure 1: The major cell types of a typical mammalian retina.
Figure 2: The bipolar cell pathways of mammalian retinas, assembled from individual components.
Figure 3: The connections with cones and axonal stratification of different types of bipolar cells.
Figure 4: How transient (high-pass) and sustained (low-pass) bipolar cells decompose the output of a cone.
Figure 6: The fundamental signal-carrying pathways of a generic mammalian retina, reduced to a conceptual minimum.
Figure 5: The types of ganglion cells identified thus far in the retina of the cat.

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References

  1. Vaney, D. I. A quantitative comparison between the ganglion cell populations and axonal outflows of the visual streak and periphery of the rabbit retina. J. Comp. Neurol. 189, 215–233 (1980).

    Article  CAS  PubMed  Google Scholar 

  2. Martin, P. R. & Grünert, U. Spatial density and immunoreactivity of bipolar cells in the macaque monkey retina. J. Comp. Neurol. 323, 269–287 (1992).

    Article  CAS  PubMed  Google Scholar 

  3. MacNeil, M. A. & Masland, R. H. Extreme diversity among amacrine cells: implications for function. Neuron 20, 971–982 (1998).

    Article  CAS  PubMed  Google Scholar 

  4. MacNeil, M. A., Heussy, J. K., Dacheux, R., Raviola, E. & Masland, R. H. The shapes and numbers of amacrine cells: matching of photofilled with Golgi-stained cells in the rabbit retina and comparison with other mammalian species. J. Comp. Neurol. 413, 305–326 (1999).

    Article  CAS  PubMed  Google Scholar 

  5. Masland, R. H. Neuronal diversity in the retina. Curr. Opin. Neurobiol. 11 431–436 (2001).

    Article  CAS  PubMed  Google Scholar 

  6. Vaney, D. I. in Progress in Retinal Research (eds. Osborne, N. & Chader, G.) 49–100 (Pergamon, New York, 1990).

    Google Scholar 

  7. Wässle, H. & Boycott, B. B. Functional architecture of the mammalian retina. Physiol. Rev. 71, 447–480 (1991).

    Article  PubMed  Google Scholar 

  8. Sterling, P. in The Synaptic Organization of the Brain Vol. 4 (ed. Shepherd, G. M.), 205–253 (Oxford Univ. Press, New York, 1998).

    Google Scholar 

  9. Rodieck, R.W. The First Steps in Seeing (Sinauer Associates, Sunderland, Massachusetts, 1998).

    Google Scholar 

  10. Nathans, J. The evolution and physiology of human color vision: insights from molecular genetic studies of visual pigments. Neuron 24, 299–312 (1999).

    Article  CAS  PubMed  Google Scholar 

  11. Boycott, B. B. & Wässle, H. Parallel processing in the mammalian retina: The Proctor Lecture. Invest. Ophthalmol. Vis. Sci. 40, 1313–1327 (1999).

    CAS  PubMed  Google Scholar 

  12. Okano, T., Kojima, D., Fukada, Y. & Shichida, Y. Primary structures of chicken cone visual pigments: vertebrate rhodopsins have evolved out of cone visual pigments. Proc. Natl. Acad. Sci. USA 89, 5932–5936 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Johnson, R. L. et al. Cloning and expression of goldfish opsin sequences. Biochemistry 32, 208–214 (1993).

    Article  CAS  PubMed  Google Scholar 

  14. Jacobs, G. H. The distribution and nature of colour vision among the mammals. Biol. Rev. 68, 413–471 (1993).

    Article  CAS  PubMed  Google Scholar 

  15. Westheimer, G. The maxwellian view. Vision Res. 6, 669–682 (1966).

    Article  CAS  PubMed  Google Scholar 

  16. Cohen, E. & Sterling, P. Demonstration of cell types among cone bipolar neurons of the cat retina. Phil. Trans. R. Soc. Lond. B Biol. Sci. 330, 305–321 (1990).

    Article  CAS  Google Scholar 

  17. Boycott, B. B. & Wässle, H. Morphological classification of bipolar cells of the primate retina. Eur. J. Neurosci. 3, 1069–1088 (1991).

    Article  PubMed  Google Scholar 

  18. Cajal, S. R. The Structure of the Retina (Thomas, Springfield, 1972).

    Google Scholar 

  19. McGuire, B. A., Stevens, J. K. & Sterling, P. Microcircuitry of bipolar cells in rat retina. J. Neurosci. 12, 2920–2938 (1984).

    Article  Google Scholar 

  20. Grünert, U., Martin, P. R. & Wässle, H. Immunocytochemical analysis of bipolar cells in the macaque monkey retina. J. Comp. Neurol. 348, 607–627 (1994).

    Article  PubMed  Google Scholar 

  21. Hartveit, E. et al. Localization and developmental expression of the NMDA receptor subunit NR2A in the mammalian retina. J. Comp. Neurol. 348, 570–582 (1994).

    Article  CAS  PubMed  Google Scholar 

  22. Haverkamp, S. & Wässle, H. Immunocytochemical analysis of the mouse retina. J. Comp. Neurol. 424, 1–23 (2000).

    Article  CAS  PubMed  Google Scholar 

  23. Greferath, U. et al. GABAA receptor subunits have differential distributions in the rat retina: in situ hybridization and immunohistochemistry. J. Comp. Neurol. 353, 553–571 (1995).

    Article  CAS  PubMed  Google Scholar 

  24. Euler, T. & Wässle, H. Different contributions of GABAA and GABAC receptors to rod and cone bipolar cells in a rat retinal slice preparation. J. Neurophysiol. 79, 1384–1395 (1998).

    Article  CAS  PubMed  Google Scholar 

  25. Euler, T. & Masland, R. H. Light-evoked responses of bipolar cells in a mammalian retina. J. Neurophysiol. 83, 1817–1829 (2000).

    Article  CAS  PubMed  Google Scholar 

  26. Nawy, S. & Jahr, C. E. Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature 346, 269–271 (1990).

    Article  CAS  PubMed  Google Scholar 

  27. Nawy, S. & Jahr, C. E. cGMP-gated conductance in retinal bipolar cells is suppressed by the photoreceptor transmitter. Neuron 7, 677–683 (1991).

    Article  CAS  PubMed  Google Scholar 

  28. Kaneko, A. Physiological and morphological identification of horizontal, bipolar and amacrine cells in goldfish retina. J. Physiol. (Lond.) 207, 623–633 (1970).

    Article  CAS  Google Scholar 

  29. Werblin, F. S. & Dowling, J. E. Organization of the retina of the mudpuppy, necturus maculosus II. Intracellular recording. J. Neurophysiol. 32, 339–355 (1969).

    Article  CAS  PubMed  Google Scholar 

  30. Awatramani, G. B. & Slaughter, M. M. Origin of transient and sustained responses in ganglion cells of the retina. J. Neurosci. 20, 7087–7095 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. DeVries, S. H. Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847–856 (2000).

    Article  CAS  PubMed  Google Scholar 

  32. Kouyama, N. & Marshak, D. W. Bipolar cells specific for blue cones in the macaque retina. J. Neurosci. 12, 1233–1252 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Dacey, D. M. & Lee, B. B. The 'blue-on' opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature 367, 731–735 (1994).

    Article  CAS  PubMed  Google Scholar 

  34. Famiglietti, E. V. Jr. & Kolb, H. A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Res. 84, 293–300 (1975).

    Article  PubMed  Google Scholar 

  35. Smith, R. G., Freed, M. A. & Sterling, P. Microcircuitry of the dark-adapted cat retina: functional architecture of the rod–cone network. J. Neurosci. 6, 3505–3517 (1986).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Strettoi, E., Dacheux, R. F. & Raviola, E. Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina. J. Comp. Neurol. 295, 449–466 (1990).

    Article  CAS  PubMed  Google Scholar 

  37. Strettoi, E., Raviola, E. & Dacheux, R. F. Synaptic connections of the narrow-field, bistratified rod amacrine cell (AII) in the rabbit retina. J. Comp. Neurol. 325, 152–168 (1992).

    Article  CAS  PubMed  Google Scholar 

  38. Strettoi, E. & Masland, R. H. The organization of the inner nuclear layer of the rabbit retina. J. Neurosci. 15, 875–888 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Euler, T. & Wässle, H. Immunocytochemical identification of cone bipolar cells in the rat retina. J. Comp. Neurol. 361, 461–478 (1995).

    Article  CAS  PubMed  Google Scholar 

  40. Jeon, C.-J., Strettoi, E. & Masland, R. H. The major cell populations of the mouse retina. J. Neurosci. 18, 8936–8946 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Masland, R. H. Processing and encoding of visual information in the retina. Curr. Opin. Neurobiol. 6, 467–474 (1996).

    Article  CAS  PubMed  Google Scholar 

  42. Williams, R. W., Cavada, C. & Reinoso-Suarez, F. Rapid evolution of the visual system: a cellular assay of the retina and dorsal lateral geniculate nucleus of the Spanish wildcat and the domestic cat. J. Neurosci. 13, 208–228 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Williams, D. R. Seeing through the photoreceptor mosaic. Trends Neurosci. 9 193–198 (1986).

    Article  Google Scholar 

  44. Nathans, J., Piantanida, T. P., Eddy, R. L., Shows, T. B. & Hogness, D. S. Molecular genetics of inherited variation in human color vision. Science 232, 203–210 (1986).

    Article  CAS  PubMed  Google Scholar 

  45. Nathans, J., Thomas, D. & Hogness, D. S. Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. Science 232, 193–202 (1986).

    Article  CAS  PubMed  Google Scholar 

  46. Mollon, J. D. in Evolution of the Eye and Visual System (eds. Cronly-Dillon, J. R. & Gregory, R. L.) 306–319 (CRC Press, Boca Raton, Florida, 1991).

    Google Scholar 

  47. Dacey, D. M. Parallel pathways for spectral coding in primate retina. Annu. Rev. Neurosci. 23, 743–775 (2000).

    Article  CAS  PubMed  Google Scholar 

  48. Calkins, D. J. & Sterling, P. Evidence that circuits for spatial and color vision segregate at the first retinal synapse. Neuron 24, 313–321 (1999).

    Article  CAS  PubMed  Google Scholar 

  49. Boycott, B. B., Hopkins, J. M. & Sperling, H. G. Cone connections of the horizontal cells of the rhesus monkey's retina. Proc. R. Soc. Lond. B Biol. Sci. 229, 345–379 (1987).

    Article  CAS  PubMed  Google Scholar 

  50. Hack, I. & Peichl, L. Horizontal cells of the rabbit retina are non-selectively connected to the cones. Eur. J. Neurosci. 11, 2261–2274 (1999).

    Article  CAS  PubMed  Google Scholar 

  51. Peichl, L., Sandmann, D. & Boycott, B. B. in Development and Organization of the Retina (eds. Chalupa, L. M. & Finlay, B. L.) 147–172 (Plenum, New York, 1998).

    Book  Google Scholar 

  52. Dacey, D. M., Lee, B. B., Stafford, D. K., Pokorny, J. & Smith, V. C. Horizontal cells of the primate retina: cone specificity without spectral opponency. Science 271, 656–658 (1996).

    Article  CAS  PubMed  Google Scholar 

  53. Nelson, R., Lützow, A. V., Kolb, H. & Gouras, P. Horizontal cells in cat retina with independent dendritic systems. Science 189, 137–139 (1975).

    Article  CAS  PubMed  Google Scholar 

  54. Freed, M. A. & Sterling, P. The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. J. Neurosci. 8, 2303–2320 (1988).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Calkins, D. J., Schein, S. J., Tsukamoto, Y. & Sterling, P. M and L cones in macaque fovea connect to midget ganglion cells by different numbers of excitatory synapses. Nature 371, 70–72 (1994).

    Article  CAS  PubMed  Google Scholar 

  56. Jacoby, R., Stafford, D., Kouyama, N. & Marshak, D. Synaptic inputs to ON parasol ganglion cells in the primate retina. J. Neurosci. 16, 8041–8056 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Hubel, D. H. Eye, Brain and Vision (Freeman, New York, 1988).

    Google Scholar 

  58. Nolte, J. The Human Brain (Mosby-Year Book, St. Louis, Missouri, 1988).

    Google Scholar 

  59. Vaney, D. I. Patterns of neuronal coupling in the retina. Prog. Ret. Eye Res. 13, 301–355 (1994).

    Article  Google Scholar 

  60. Meister, M., Lagnado, L. & Baylor, D. A. Concerted signaling by retinal ganglion cells. Science 270, 1207–1210 (1995).

    Article  CAS  PubMed  Google Scholar 

  61. Meister, M. Multineuronal codes in retinal signaling. Proc. Natl. Acad. Sci. USA 93, 609–614 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Ehinger, B. Functional role of dopamine in the retina. Prog. Ret. Res. 2, 213–232 (1983).

    Article  CAS  Google Scholar 

  63. Dowling, J. E. Dopamine: a retinal neuromodulator? Trends Neurosci. 9, 236–240 (1986).

    Article  CAS  Google Scholar 

  64. Witkovsky, P. & Dearry, A. Functional roles of dopamine in the vertebrate retina. Prog. Ret. Res. 11, 247–292 (1991).

    Article  CAS  Google Scholar 

  65. Tauchi, M., Madigan, N. M. & Masland, R. H. Shapes and distributions of the catecholamine-accumulating neurons in the rabbit retina. J. Comp. Neurol. 293, 178–189 (1990).

    Article  CAS  PubMed  Google Scholar 

  66. Hampson, E. C. G. M., Vaney, D. I. & Weiler, R. Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. J. Neurosci. 12, 4911–4922 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Piccolino, M., Witkovsky, P. & Trimarchi, C. Dopaminergic mechanisms underlying the reduction of electrical coupling between horizontal cells of the turtle retina induced by d-amphetamine, bicuculline, and veratridine. J. Neurosci. 7, 2273–2284 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Jensen, R. J. & Daw, N. W. Effects of dopamine antagonists on receptive fields of brisk cells and directionally selective cells in the rabbit retina. J. Neurosci. 4, 2972–2985 (1984).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Jensen, R. J. & Daw, N. W. Effects of dopamine and its agonists and antagonists on the receptive field properties of ganglion cells in the rabbit retina. Neuroscience 17, 837–855 (1986).

    Article  CAS  PubMed  Google Scholar 

  70. Bruenner, U. & Burnside, B. Pigment granule migration in isolated cells of the teleost retinal pigment epithelium. Invest. Ophthalmol. Vis. Sci. 27, 1634–1643 (1986).

    CAS  PubMed  Google Scholar 

  71. Gustincich, S., Feigenspan, A., Wu, D. K., Koopman, L. J. & Raviola, E. Control of dopamine release in the retina: a transgenic approach to neural networks. Neuron 18, 723–736 (1997).

    Article  CAS  PubMed  Google Scholar 

  72. Puopolo, M., Hochstetler, S. E., Gustincich, S., Wightman, R. M. & Raviola, E. Extrasynaptic release of dopamine in a retinal neuron: activity dependence and transmitter modulation. Neuron 30, 211–225 (2001).

    Article  CAS  PubMed  Google Scholar 

  73. O' Malley, D. M., Sandell, J. H. & Masland, R. H. Co-release of acetylcholine and GABA by the starburst amacrine cells. J. Neurosci. 12, 1394–1408 (1992).

    Article  CAS  Google Scholar 

  74. Masland, R. H. & Tauchi, M. The cholinergic amacrine cell. Trends Neurosci. 9, 218–223 (1986).

    Article  CAS  Google Scholar 

  75. He, S.-G. & Masland, R. H. Retinal direction selectivity after targeted laser ablation of starburst amacrine cells. Nature 389, 378–382 (1997).

    Article  CAS  PubMed  Google Scholar 

  76. Yoshida, K. et al. A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron 30, 771–780 (2001).

    Article  CAS  PubMed  Google Scholar 

  77. Berson, D. M., Isayama, T. & Pu, M. The eta ganglion cell type of the cat retina. J. Comp. Neurol. 408, 204–219 (1999).

    Article  CAS  PubMed  Google Scholar 

  78. Berson, D. M., Pu, M. & Famiglietti, E. V. The zeta cell: a new ganglion cell type in cat retina. J. Comp. Neurol. 399, 269–288 (1998).

    Article  CAS  PubMed  Google Scholar 

  79. Isayama, T., Berson, D. M. & Pu, M. Theta ganglion cell type of the cat retina. J. Comp. Neurol. 417, 32–48 (2000).

    Article  CAS  PubMed  Google Scholar 

  80. Pu, M., Berson, D. M. & Pan, T. Structure and function of retinal ganglion cells innervating the cat's geniculate wing: an in vitro study. J. Neurosci. 14, 4338–4358 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Barlow, H. B. & Levick, W. R. The mechanism of directionally selective units in rabbit's retina. J. Physiol. (Lond.) 178, 477–504 (1965).

    Article  CAS  Google Scholar 

  82. Levick, W. R. Receptive fields and trigger features of ganglion cells in the visual streak of the rabbit's retina. J. Physiol. (Lond.) 188, 285–307 (1967).

    Article  CAS  Google Scholar 

  83. Oyster, C. W., Takahashi, E. & Collewijn, H. Direction selective retinal ganglion cells and control of optokinetic nystagmus in the rabbit. Vision Res. 12, 183–193 (1972).

    Article  CAS  PubMed  Google Scholar 

  84. Simpson, J. I. The accessory optic system. Annu. Rev. Neurosci. 7, 13–41 (1984).

    Article  CAS  PubMed  Google Scholar 

  85. Oyster, C. W., Simpson, J. I., Takahashi, E. S. & Soodak, R. E. Retinal ganglion cells projecting to the rabbit accessory optic system. J. Comp. Neurol. 190, 49–61 (1980).

    Article  CAS  PubMed  Google Scholar 

  86. Provencio, I. et al. A novel human opsin in the inner retina. J. Neurosci. 20, 600–605 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Pasik, P. & Pasik, T. in The Oculomotor System (ed. Bender, M. B.) 40–80 (Harper & Row, New York, 1964).

    Google Scholar 

  88. Tauchi, M. & Masland, R. H. Local order among the dendrites of an amacrine cell population. J. Neurosci. 5, 2494–2501 (1985).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Yang, G. & Masland, R. H. Direct visualization of the dendritic and receptive fields of directionally selective retinal ganglion cells. Science 258, 1949–1952 (1992).

    Article  CAS  PubMed  Google Scholar 

  90. Rodieck, R. W. & Watanabe, M. Survey of the morphology of macaque retinal ganglion cells that project to the pretectum, superior colliculus and the parvicellular laminae of the lateral geniculate nucleus. J. Comp. Neurol. 338, 289–303 (1993).

    Article  CAS  PubMed  Google Scholar 

  91. Dacey, D. M. Morphology of a small-field bistratified ganglion cell type in the macaque and human retina. Vis. Neurosci. 10, 1081–1098 (1993).

    Article  CAS  PubMed  Google Scholar 

  92. Dacey, D. M. Physiology, morphology and spatial densities of identified ganglion cell types in the primate retina. Ciba Found. Symp. 184, 12–34 (1994).

    CAS  PubMed  Google Scholar 

  93. Peterson, B. B. & Dacey, D. M. Morphology of wide-field, monostratified ganglion cells of the human retina. Vis. Neurosci. 16, 107–120 (1999).

    Article  CAS  PubMed  Google Scholar 

  94. Calkins, D. J., Tsukamoto, Y. & Sterling, P. Microcircuitry and mosaic of a blue-yellow ganglion cell in the primate retina. J. Neurosci. 18, 3373–3385 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Wiesel, T. N. & Hubel, D. H. Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. J. Neurophysiol. 29, 1115–1156 (1966).

    Article  CAS  PubMed  Google Scholar 

  96. Curcio, C. A., Sloan, K. R., Kalina, R. E. & Hendrickson, A. E. Human photoreceptor topography. J. Comp. Neurol. 292, 497–523 (1990).

    Article  CAS  PubMed  Google Scholar 

  97. Buhl, E. H. & Peichl, L. Morphology of rabbit retinal ganglion cells projecting to the medial terminal nucleus of the accessory optic system. J. Comp. Neurol. 253, 163–174 (1986).

    Article  CAS  PubMed  Google Scholar 

  98. Ts'o, D. Y. & Gilbert, C. D. The organization of chromatic and spatial interactions in the primate striate cortex. J. Neurosci. 8, 1712–1727 (1988).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Hubel, D. & Livingstone, M. Color puzzles. Cold Spring Harb. Symp. Quant. Biol. 55, 643–649 (1990).

    Article  CAS  PubMed  Google Scholar 

  100. Conway, B. R. Spatial structure of cone inputs to color cells in alert macaque primary visual cortex (V1). J. Neurosci. 21, 2768–2783 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Hendry, S. H. & Yoshioka, T. A neurochemically distinct third channel in the macaque dorsal lateral geniculate nucleus. Science 264, 575–577 (1994).

    Article  CAS  PubMed  Google Scholar 

  102. Hendry, S. H.C. & Reid, R. C. The koniocellular pathway in primate vision. Annu. Rev. Neurosci. 23, 127–153 (2000).

    Article  CAS  PubMed  Google Scholar 

  103. Saul, A. B. & Humphrey, A. L. Spatial and temporal response properties of lagged and nonlagged cells in cat lateral geniculate nucleus. J. Neurophysiol. 64, 206–224 (1990).

    Article  CAS  PubMed  Google Scholar 

  104. Menger, N., Pow, D. V. & Wässle, H. Glycinergic amacrine cells of the rat retina. J. Comp. Neurol. 401, 34–46 (1998).

    Article  CAS  PubMed  Google Scholar 

  105. Kalloniatis, M., Marc, R. E. & Murry, R. F. Amino acid signatures in the primate retina. J. Neurosci. 16, 6807–6829 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Shapley, R. & Enroth-Cugell, C. Visual adaptation and retinal gain controls. Prog. Ret. Res. 3, 263–346 (1984).

    Article  Google Scholar 

  107. Berry, M. J., Brivanlou, I. H., Jordan, T. A. & Meister, M. Anticipation of moving stimuli by the retina. Nature 398, 334–338 (1999).

    Article  CAS  PubMed  Google Scholar 

  108. Nelson, R. AII amacrine cells quicken time course of rod signals in the cat retina. J. Neurophysiol. 47, 928–947 (1982).

    Article  CAS  PubMed  Google Scholar 

  109. Boos, R., Schneider, H. & Wässle, H. Voltage- and transmitter-gated currents of AII-amacrine cells in a slice preparation of the rat retina. J. Neurosci. 13, 2874–2888 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Roska, B. & Werblin, F. Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410, 583–587 (2001).

    Article  CAS  PubMed  Google Scholar 

  111. Famiglietti, E. V. Polyaxonal amacrine cells of rabbit retina: size and distribution of PA1 cells. J. Comp. Neurol. 316, 406–421 (1992).

    Article  CAS  PubMed  Google Scholar 

  112. Dacey, D. M. Axon-bearing amacrine cells of the macaque monkey retina. J. Comp. Neurol. 284, 275–293 (1989).

    Article  CAS  PubMed  Google Scholar 

  113. Cook, P. B. & Werblin, F. S. Action potentials are propagated by wide-field amacrine cells in the tiger salamander retina. J. Neurosci. 14, 3852–3861 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Stafford, D. K. & Dacey, D. M. Physiology of the A1 amacrine: a spiking, axon-bearing interneuron of the macaque monkey retina. Vis. Neurosci. 14, 507–522 (1997).

    Article  CAS  PubMed  Google Scholar 

  115. Taylor, W. R. Response properties of long-range axon-bearing amacrine cells in the dark-adapted rabbit retina. Vis. Neurosci. 13, 599–604 (1996).

    Article  CAS  PubMed  Google Scholar 

  116. McIlwain, J. B. Receptive fields of optic tract axons and lateral geniculate cells: peripheral extent and barbituate sensitivity. J. Neurophysiol. 27, 1154–1173 (1964).

    Article  CAS  PubMed  Google Scholar 

  117. Neuenschwander, S. & Singer, W. Long-range synchronization of oscillatory light responses in the cat retina and lateral geniculate nucleus. Nature 379, 728–733 (1996).

    Article  CAS  PubMed  Google Scholar 

  118. Smirnakis, S. M., Berry, M. J., Warland, D. K., Bialek, W. & Meister, M. Adaptation of retinal processing to image contrast and spatial scale. Nature 386, 69–73 (1997).

    Article  CAS  PubMed  Google Scholar 

  119. Brown, S. P. & Masland, R. H. Spatial scale and cellular substrate of contrast adaptation in retinal ganglion cell. Nat. Neurosci. 4, 44–51 (2001).

    Article  CAS  PubMed  Google Scholar 

  120. Dowling, J. E. The Retina: An Approachable Part of the Brain (Belknap, Cambridge, 1987).

    Google Scholar 

  121. Wu, S., Gao, F. & Maple, B. R. Functional architecture of synapses in the inner retina: segregation of visual signals by stratification of bipolar cell axon terminals. J. Neurosci. 20, 4462–4470 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. McBillem, G. S. & Dacheux, R. F. Responses to glutamate of morphologically defined rabbit cone bipolar cells. Invest. Ophthalmol. Vis. Sci. (2001).

  123. Freed, M. A. Parallel cone bipolar pathways to a ganglion cell use different rates and amplitudes of quantal excitation. J. Neurosci. 20, 3956–3963 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Packer, O. S., Williams, D. R. & Bensinger, D. G. Photopigment transmittance imaging of the primate photoreceptor mosaic. J. Neurosci. 16, 2251–2260 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Vaney, D. I. Neuronal coupling in rod-signal pathways of the retina. Invest. Ophthalmol. Vis. Sci. 38, 267–273 (1997).

    CAS  PubMed  Google Scholar 

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Acknowledgements

R. Rockhill made the illustrations. B. Boycott and P. Sterling made comments on the manuscript. The author is a Senior Investigator of Research to Prevent Blindness.

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Masland, R. The fundamental plan of the retina. Nat Neurosci 4, 877–886 (2001). https://doi.org/10.1038/nn0901-877

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