The Computation of Lightness by the Primate Retina

  • David Marr
  • Norberto M. Grzywacz


It is proposed that one function of the retina is to compute lightness using a two-dimensional parallel algorithm. There are three stages: (1) a centre-surround difference operation; (2) a threshold applied to the difference signal; (3) the inverse of (1), whose output is lightness. The operation of the midget bipolar—midget ganglion channel is analysed in detail, and a functional interpretation of various retinal structures is given. Requirements of the theory are stated concerning the arrangement and connexions of cells, and the signs of the synapses. in the inner plexiform layer.


Ganglion Cell Receptive Field Retinal Ganglion Cell Bipolar Cell Amacrine Cell 
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  1. Alpern M. (1965) Rod-cone independence in the after-flash effect. J. Physiol.. Loud. 176, 462–472.Google Scholar
  2. Alpern M. and Rushton W. A. H. (1967) The nature of rise in threshold produced by contrast-flashes. J. Physiol., Lond. 189, 519–534.Google Scholar
  3. Alpern M., Rushton W. A. H. and Torii, S. (1970a) The size of rod signals. J. Physiol., Lond. 206, 193–208.Google Scholar
  4. Alpern M., Rushton W. A. H. and Torii S. (1970b) The attenuation of rod signals by backgrounds. J. Physiol., Lond. 206, 209–227.Google Scholar
  5. Alpern M., Rushton W. A. H. and Torii S. (1970e) The attenuation of rod signals by bleachings. J. Physiol., Lond. 207, 449–461.Google Scholar
  6. Alpern M., Rushton W. A. H. and Torii S. (1970d) Signals from cones. J. Physiol., Lond. 207, 463–475.Google Scholar
  7. Barlow H. B. (1956) Retinal noise and absolute threshold. J. opt. Soc. Am. 46, 634–639.CrossRefGoogle Scholar
  8. Barlow H. B. (1957) Increment thresholds at low intensities considered as signal-noise discriminations. J. Physiol., Loud. 136, 469–488.Google Scholar
  9. Barlow H. B. (1958) Temporal and spatial summation in human vision at different background intensities. J. Physiol., Loud. 141, 337–350.Google Scholar
  10. Barlow H. B., Fitzhugh R. and Kuffler S. W. (1957) Change of organization in the receptive field of the cat’s retina during dark adaptation. J. Physiol., Lond. 137, 338–354.Google Scholar
  11. Barlow H. B. and Sakitt B. (1973) Doubts about scotopic interactions in stabilized vision. Vision Res. 13, 523–524. Boycott B. B. and Dowling J. E. (1969) Organization of the primate retina: light microscopy (with an appendix by H. Kolb). Phil. Trans. R. Soc. B. 255, 109–184.Google Scholar
  12. Brindley G. S. (1970) Physiology of the Retina and I isual Pathway (Physiological Society Monograph no. 6 ). Edward Arnold Ltd.. London.Google Scholar
  13. Cajal S. R. (1911) Histologie du Système.Aerreux. C.S. I. C.. Madrid.Google Scholar
  14. Cleland B. G., Dubin M. W. and Levick W. R. (1971) Sustained and transient neurones in the cat’s retina and lateral geniculate nucleus. J. Physiol.. Lond. 217, 473–496.Google Scholar
  15. Cone R. A. and Ebrey T. G. (1965) Functional independence of the two major components of the rod electroretinogram. Nature, Lond. 221, 818–820.CrossRefGoogle Scholar
  16. De Valois R. L. (1965) Analysis and coding of colour vision in the primate visual system. Cold Spring Harh. Symp. quant. Biol. 30, 567–579.Google Scholar
  17. Dowling J. E. and Boycott B. B. (1966) Organization of the primate retina: electron microscopy. Proc. R. Soc. B. 166, 80 - I11.CrossRefGoogle Scholar
  18. Dowling J. E. and Werblin F. S. (1969) Organization of the retina of the mud-puppy. Necturus maculosus: I. Synaptic structure. J. Neurophysiol. 32, 315–338.Google Scholar
  19. Enroth-Cugell C. and Robson J. G. (1966) The contrast sensitivity of retinal ganglion cells of the cat. J. Physiol., Lond. 187, 517–552.Google Scholar
  20. Fukada Y. (1971) Receptive field organization of cat optic nerve fibres with special reference to conduction velocity. Vision Res. 11, 209–226.CrossRefGoogle Scholar
  21. Fukada Y. and Saito H.-A. (1971) The relationship between response characteristics to flicker stimulation and receptive field organization in the cat’s optic nerve fibres. Vision Res. 11, 227–240.CrossRefGoogle Scholar
  22. Gouras P. (1966) Rod and cone independence in the eleetroretinogram of the dark-adapted monkey’s perifovea. J. Physiol., Lond. 187, 455–464.Google Scholar
  23. Gouras P. (1967) The effects of light-adaptation on rod and cone receptive field organization of monkey ganglion cells. J. Physiol., Lond. 192, 747–760.Google Scholar
  24. Gouras P. (1968) Identification of cone mechanisms in monkey ganglion cells. J. Physiol., Lond. 199, 533–547.Google Scholar
  25. Gouras P. and Link K. (1966) Rod and cone interaction in dark-adapted monkey ganglion cells. J. Physiol., Lond. 184, 499–510.Google Scholar
  26. Helmholtz H. (1962) Treatise on Physiological Optics. Dover Publications Inc.. New York (First edition of Handbuch der Phrsiologischen Optik published in 1867 by Voss. Leipzig).Google Scholar
  27. Horn B. K. P. (1974) On lightness (submitted for publication. )Google Scholar
  28. Hubel D. H. and Wiesel T. N. (1960) Receptive fields of optic nerve fibres in the spider monkey. J. Physiol., Lond. 154, 572–580.Google Scholar
  29. Hubel D. H. and Wiesel T. N. (1966) Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. J. Neurophysiol. 29, 1115–1156.Google Scholar
  30. Kaneko A. and Hashimoto H. (1967) Recording site of the single cone response determined by an electrode marking technique. Vision Res. 7, 847–851.CrossRefGoogle Scholar
  31. Kolb Helga (1970) Organization of the outer plexiform layer of the primate retina: electron microscopy of Golgi-impregnated cells. Phil. Trans. R. Soc. B. 258, 261–283.CrossRefGoogle Scholar
  32. Kuffler S. W. (1953) Discharge patterns and functional organization of mammalian retina. J.Neurophysiol.. Land. 16, 37–68.Google Scholar
  33. Land E. H. (1964) The retinex. Am. Scientist 52, 247–264.Google Scholar
  34. Land E. H. and McCann J. J. (1971) Lightness and retinex theory. J. opt. Soc. Am. 61, 1–11.CrossRefGoogle Scholar
  35. Lennie P. and MacLeod D. I. A. (1973) Background configuration and rod threshold. J. Physiol.. Land. 233, 143–156.Google Scholar
  36. Mcllwain J. T. (1964) Receptive fields of optic tract axons and lateral geniculate cells: peripheral extent and barbiturate sensitivity. J. Neurophrsiol. 27, 1154–1173.Google Scholar
  37. Mcllwain J. T. (1966) Some evidence concerning the physiological basis of the periphery effect in the cat’s retina. E.vpl Brais Res. 1, 265–271.Google Scholar
  38. McKee S. and Westheimer G. (1970) Specificity of cone mechanisms in lateral interactions. J. PhysioL, Land. 206, 117–128.Google Scholar
  39. Maffei L. and Fiorentini A. (1972) Retinogeniculate convergence and analysis of contrast. J. Neurophysiol. 35, 65–72.Google Scholar
  40. Missotten L. (1965) The L ltra.structure Othe Human Retina.Google Scholar
  41. Naka K. I. and Rushton W. A. H. (1966) S-potentials from colour units in the retina of fish (Cyprinidae). J. Plnsiol., Lond. 185, 536–555.Google Scholar
  42. Naka K. 1. and Rushton W. A. H. (1967) The generation and spread of S-potentials in fish (Cyprinidae). J. Physiol.. Land. 192, 437–461.Google Scholar
  43. Naka K. I. and Rushton W. A. H. (1968) S-potential and dark adaptation in fish. J. Physiol.. Lond. 194, 259–269.Google Scholar
  44. Ratliff F. (1965) Maclt Bands: Quantitative Studies on Neural Networks in the Retina. Holden-Day. San Francisco.Google Scholar
  45. Rodieck R. W. (1967) Receptive fields in the cat retina: a new type. Science, N.Y. 157, 90–92.CrossRefGoogle Scholar
  46. Rushton W. A. H. (1972) Pigments and signals in colour vision (invited lecture to the Physiological Society). J. Physiol.. Land. 220, 1 P-31P.Google Scholar
  47. Stone J. and Dreher B. (1973) Projection of X- and Y-cells of the cats lateral geniculate nucleus to areas 17 and 18 of visual cortex. J. Neurophysiol. 36. 551–567.Google Scholar
  48. Stone J. and Hoffman K.-P. (1972) Very slow-moving ganglion cells in the cat’s retina: a major. new functional type? Brain Res. 43, 610–616.CrossRefGoogle Scholar
  49. Tornita T. (1968) Electrical responses of single photoreceptors. Prow I. E. E. E. 56, 1015–1023.Google Scholar
  50. Toyoda J. Nosaki H. and Tornita T. (1969) Light-induced resistance changes in single photoreceptors of Necturus and Gekko. Vision Res. 9, 453–463.Google Scholar
  51. Weber E. H. (1834) De Resorptione..Auditr et Tactu.4nnotationen.-lnatomicae et Phrsiolopicae (cited by Brindley. 1970 ). C. F. Koehler. Leipzig.Google Scholar
  52. Werblin F. S. and Dowling J. E. (1969) Organization of the retina of the mud-puppy. Necturus ntaculosus: II. Intracellular recording. J. Neurophlsioi. 32, 339–355.Google Scholar
  53. Westheimer G. (1970) Rod-cone independence for sensitizing interaction in the human retina. J. Physiol., Land. 206, 109–116.Google Scholar
  54. Westheimer G. and Wiley R. W. (1970) Distance effects in human scotopic retinal interaction. J. Physiol.. Lond. 206, 129–143.Google Scholar
  55. Zeki S. M. (1973) Colour coding in rhesus monkey prestriate cortex. Brain Res. 53, 422–427.CrossRefGoogle Scholar
  56. Ariel M, Adolph AR (1985): Neurotransmitter inputs to directionally sensitive turtle retinal ganglion cells. J Neurophysiol 54: 1123–143Google Scholar
  57. Ariel M, Daw NW (1982): Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. J Physiol 324: 161–185Google Scholar
  58. Boycott BB, Dowling JE (1969): Organization of the primate retina: light microscopy. Phil Trans R Soc B 255: 109–184CrossRefGoogle Scholar
  59. Brandon C (1987): Cholinergic neurons in the rabbit retina: dendritic branching and ultrastructural connectivity. Brain Res 426: 119–130CrossRefGoogle Scholar
  60. Crick F (1988): What Mad Pursuit. New York: Basic BooksGoogle Scholar
  61. Dacheux RF, Miller RF (1981): An intracellular electrophysiological study of the ontogeny of functional synapses in the rabbit retina. 1. Receptors, horizontal and bipolar cells. J Comp Neurol 198: 307–326CrossRefGoogle Scholar
  62. De Monasterio FM (1978): Properties of concentrically organized X and Y ganglion cells of macaque retina. J Neurophysiol 41: 1394–1417Google Scholar
  63. DeMonasterio FM, Gouras P (1975): Functional properties of ganglion cells of the rhesus monkey retina. J Physiol 251: 167–195Google Scholar
  64. DeValois RL (1960): Color vision mechanisms in the monkey. J Gen Physiol 43 (Suppl.): 115–128CrossRefGoogle Scholar
  65. Dreher B, Fukuda Y, Rodieck RW (1976): Identification, classification, and anatomical segregation of cells with X-like and Y-like properties in the lateral geniculate nucleus of old world primates. J Physiol 258: 433–452Google Scholar
  66. Enroth-Cugell C, Robson JG (1966): The contrast sensitivity of retinal ganglion cells of the cat. J Physiol 187: 517–552Google Scholar
  67. Fain GL (1977): The threshold signal of photoreceptors. In: Vertebrate Photoreception, Barlow HB, Fatt P, eds. London: Academic Press, pp 305–323Google Scholar
  68. Fain GL, Granda AM, Maxwell JH (1977): The voltage signal of photoreceptors at the visual threshold. Nature, 265: 181–183CrossRefGoogle Scholar
  69. Famiglietti EV Jr. (1983): ON and OFF pathways through amacrine cells in mammalianGoogle Scholar
  70. retina: the synaptic connection of starburst amacrine cells. Vision Res 23:1265–1279Google Scholar
  71. Famiglietti EV Jr., Kolb H. (1975): A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Res 84: 293–300CrossRefGoogle Scholar
  72. Famiglietti EV Jr., Kolb H (1976): Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science, 194: 193–195CrossRefGoogle Scholar
  73. Gouras P, Kruger J (1979): Responses of cells in foveal visual cortex of the monkey to pure color contrast. J Neurophysiol 42: 850–860Google Scholar
  74. Grzywacz NM, Poggio T (1990): Computation of motion by real neurons. In: An Introduction to Neural and Electronic Networks, Zometzer SF, Davis JL and Lau C, eds. Orlando: Academic Press, pp 379–403Google Scholar
  75. Horn BKP (1974): Determining lightness from an image. Comput Graph Image Process 3: 277–299CrossRefGoogle Scholar
  76. Kaplan E, Shapley R (1986): The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proc Natl Acad Sci USA 83: 2755–2757CrossRefGoogle Scholar
  77. Kolb H (1970): Organization of the outer plexiform layer of the primate retina: electronGoogle Scholar
  78. microscopy of Golgi-impregnated cells. Phil Trans R Soc B 258:261–283Google Scholar
  79. Kolb H, Famiglietti EV Jr (1974): Rod and cone pathways in the inner plexiform layer of the cat retina. Science, 186: 47–49CrossRefGoogle Scholar
  80. Kolb H, Nelson R, Mariani A (1981): Amacrine cells, bipolar cells and ganglion cells of the cat retina: A Golgi study. Vision Res 21: 1081–1114CrossRefGoogle Scholar
  81. Land EH, McCann JJ (1971): Lightness and retinex theory. J Opt Soc Am. 61:1–11 MacLeod DIA (1978): Visual sensitivity. Ann Rev Psychol 29: 613–645Google Scholar
  82. Marc RE, Liu WS (1985): (3H) glycine accumulating neurons of the human retina. J Comp Neurol 232: 241–260Google Scholar
  83. Mariani AP, Hersh LB (1988): Synaptic organization of cholinergic amacrine cells in the rhesus monkey retina. J Comp Neurol 267: 269–280CrossRefGoogle Scholar
  84. Marr D (1974): The computation of lightness by the primate retina. Vision Res 14: 1377–1388CrossRefGoogle Scholar
  85. Marr D (1982): Vision. San Francisco: WH FreemanGoogle Scholar
  86. Masland RH, Mills JW, Hayden SA (1984): Acetylcholine synthesizing amacrine cells: identification and selective staining using autoradiography and fluorescent markers. Proc R Soc Gond B 223: 79–100CrossRefGoogle Scholar
  87. Matsumoto N, Naka KI (1972): Identification of the intracellular responses of the frog retina. Brain Res 42: 59–71CrossRefGoogle Scholar
  88. Michael CR (1978a): Color vision mechanisms in monkey striate cortex: dual opponent cells with concentric receptive fields. J Neurophysiol 41: 572–588Google Scholar
  89. Michael CR (1978b): Color vision mechanisms in monkey striate cortex: simple cellsGoogle Scholar
  90. with dual opponent-color receptive fields. J Neurophysiol 41:1233–1249Google Scholar
  91. Millar TJ and Morgan IG (1987): Cholinergic amacrine cells in the rabbit retina synapseGoogle Scholar
  92. onto other cholinergic amacrine cells. Neurosci Lett 74:281–285Google Scholar
  93. Mullen KT (1985): The contrast sensitivity of human colour vision to red-green and blue-yellow chromatic gratings. J Physiol 359: 381–400Google Scholar
  94. Nelson R (1982): All amacrine cells quicken time course of rod signals in the cat retina. J Neurophysiol 47: 928–947Google Scholar
  95. Nelson R, Famiglietti EV Jr., Kolb H (1978): Intracellular center ganglion cells in cat retina. J Neurophysiol 41: 472–483Google Scholar
  96. Nelson R, Kolb H, Famiglietti EV Jr, Gouras P (1976): Neural responses in the rod and cone systems of the cat retina: intracellular recordings and procion stains. Invest Ophthalmol 41: 472–483Google Scholar
  97. Polyak SL (1941): The Retina. Chicago: University of Chicago PressGoogle Scholar
  98. Pourcho RG (1982): Dopaminergic amacrine cells in the cat retina. Brain Res 252: 10 1109Google Scholar
  99. Pourcho RG and Goebel DJ (1985): A combined Golgi and autoradiographic study of [H]glycine-accumulating amacrine cells in the cat retina. J Comp Neurol 233: 473–480CrossRefGoogle Scholar
  100. Purpura K, Kaplan E, Shapley RM (1988): Background light and the contrast gain of primate P and M retinal ganglion cells. Proc Nat Acad Sci USA 85: 4534–4537CrossRefGoogle Scholar
  101. Rodieck RW (1988): The primate retina. In: Comparative Primate Biology, Steklis HD, Erwin J, eds., New York: Alan R. Liss, vol 4 pp 203–278Google Scholar
  102. Rodieck RW (1989): Starburst amacrine cells of the primate retina. J Comp Neurol 285: 18–37CrossRefGoogle Scholar
  103. Schiller PH, Malpeli JG (1978): Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey. J Neurophysiol 41: 788–797Google Scholar
  104. Schmidt M, Humphrey MF, Wassle H (1985): Action and localization of acetylcholine in the cat retina. J Neurophysiol 58: 997–1015Google Scholar
  105. Shapley R, Perry VH (1986): Cat and monkey retinal ganglion cells and their visual functional roles. Trends Neurosci 9: 229–235CrossRefGoogle Scholar
  106. Stelmach LB, Bourassa CM, Di Lollo V (1987): ON and OFF systems in human vision. Vision Res 27: 919–928CrossRefGoogle Scholar
  107. Sterling P (1983): Microcircuitry of the cat retina. Annu Rev Neurosci 3: 149–185CrossRefGoogle Scholar
  108. Vaney D (1990): The mosaic of amacrine cells in the mammalian retina. In: Progress in Retinal Research, Osborne N, Chader G eds. New York: Pergamon Press, vol. 9, pp 49–100Google Scholar
  109. Watanabe M, Rodieck RW (1989): Parasol and midget ganglion cells of the primate retina. J Comp Neurol 289: 434–454CrossRefGoogle Scholar
  110. Werblin FS, Dowling JE (1969): Organization of the retina of the mudpuppy. Necturus Maculosus. H. Intracellular recordings. J Neurophysiol 32: 339–355Google Scholar

Copyright information

© Pergamon Press plc. 1974

Authors and Affiliations

  • David Marr
    • 1
    • 2
  • Norberto M. Grzywacz
    • 3
  1. 1.The Artificial Intelligence LaboratoryMassachusetts Institute of TechnologyCambridgeUSA
  2. 2.M.R.C. Laboratory of Molecular BiologyCambridgeEngland
  3. 3.Center for Biological Information Processing Department of Brain and Cognitive SciencesMassachusetts Institute of TechnologyCambridgeUSA

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