The neural code of the retina

Neuron

Volumn 22, Issue 3, 1999, Pages 435-450

  Meister, Markus ^a   Berry II, Michael J ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ANIMAL CELL; CAT; CELL POPULATION; NERVE CELL EXCITABILITY; NERVE POTENTIAL; NONHUMAN; OPTIC NERVE FIBER; PHOTORECEPTOR; PRIORITY JOURNAL; RECEPTIVE FIELD; RETINA GANGLION CELL; REVIEW; VISUAL INFORMATION; VISUAL STIMULATION;

EID: 0033103165     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80700-X     Document Type: Review

References (128)

1. Adelson, E.H. (1982). Saturation and adaptation in the rod system. Vision Res. 22, 1299-1312.
2. Aho, A.C., Donner, K., and Reuter, T. (1993a). Retinal origins of the temperature effect on absolute visual sensitivity in frogs. J. Physiol. 463, 501-521.
3. Aho, A.C., Donner, K., Helenius, S., Larsen, L.O., and Reuter, T. (1993b). Visual performance of the toad (Bufo bufo) at low light levels: Retinal ganglion cell responses and prey-catching accuracy. J. Comp. Physiol. [A] 172, 671-682.
4. Albrecht, D.G., Farrar, S.B., and Hamilton, D.B. (1984). Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex. J. Physiol. 347, 713-739.
5. Allison, J.D., Casagrande, V.A., Debruyn, E.J., and Bonds, A.B. (1993). Contrast adaptation in striate cortical neurons of the nocturnal primate bush baby (Galago crassicaudatus). Vis. Neurosci. 10, 1129-1139.
6. Alonso, J.M., Usrey, W.M., and Reid, R.C. (1996). Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 383, 815-819.
7. Arnett, D.W. (1978). Statistical dependence between neighboring retinal ganglion cells in goldfish. Exp. Brain Res. 32, 49-53.
8. Arnett, D., and Spraker, T.E. (1981). Cross-correlation analysis of the maintained discharge of rabbit retinal ganglion cells. J. Physiol. 317, 29-47.
9. Atick, J.J. (1992). Could information theory provide an ecological theory of sensory processing? Network 3, 213-251.
10. Atick, J.J., and Redlich, A.N. (1992). What does the retina know about natural scenes? Neural Comput. 4, 196-210.
11. Atick, J.J., Li, Z., and Redlich, A.N. (1992). Understanding retinal color coding from first principles. Neural Comput. 4, 559-572.
12. Attneave, F. (1954). Some informational aspects of visual perception. Psychol. Rev. 61, 183-193.
13. Barlow, H.B. (1953). Summation and inhibition in the frog's retina. J. Physiol. 119, 69-88.
14. Barlow, H.B. (1961). Possible principles underlying the transformation of sensory messages. In Sensory Communication, W.A. Rosenblith, ed. (Cambridge, MA: MIT Press), pp. 217-234.
15. Barlow, H.B. (1990). A theory about the functional role and synaptic mechanism of visual after-effects. In Vision: Coding and Efficiency, C. Blakemore, ed. (Cambridge: University Press), pp. 363-375.
16. Barlow, H.B., and Levick, W.R. (1965). The mechanism of directionally selective units in rabbit's retina. J. Physiol. 178, 477-504.
17. Barlow, H.B., and Levick, W.R. (1969). Changes in the maintained discharge with adaptation level in the cat retina. J. Physiol. 202, 699-718.
18. Barlow, H.B., and Levick, W.R. (1969). Three factors limiting the reliable detection of light by retinal ganglion cells of the cat. J. Physiol. 200, 1-24.
19. Barlow, H.B., FitzHugh, R., and Kuffler, S.W. (1957). Change of organization of the receptive fields of the cat's retina during dark adaptation. J. Physiol. 137, 338-354.
20. Barlow, H.B., Levick, W.R., and Yoon, M. (1971). Responses to single quanta of light in retinal ganglion cells of the cat. Vision Res. 3, 87-101.
21. Baylor, D.A., and Hodgkin, A.L. (1974). Changes in time scale and sensitivity in turtle photoreceptors. J. Physiol. 242, 729-758.
22. Benardete, E.A., and Kaplan, E. (1997a). The receptive field of the primate P retinal ganglion cell, I: Linear dynamics. Vis. Neurosci. 14, 169-185.
23. Benardete, E.A., and Kaplan, E. (1997b). The receptive field of the primate P retinal ganglion cell, II: Nonlinear dynamics. Vis. Neurosci. 14, 187-205.
24. Berry, M.J., and Meister, M. (1998). Refractoriness and neural precision. J. Neurosci. 18, 2200-2211.
25. Berry, M.J., Warland, D.K., and Meister, M. (1997). The structure and precision of retinal spike trains. Proc. Nat. Acad. Sci. USA 94, 5411-5416.
26. Blakemore, C., and Campbell, F.W. (1969). On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images. J. Physiol. 203, 237-260.
27. Bolz, J., Rosner, G., and Wässle, H. (1982). Response latency of brisk-sustained (X) and brisk-transient (Y) cells in the cat retina. J. Physiol. 328, 171-190.
28. Borg-Graham, L.J., and Grzywacz, N.M. (1992). A model of the directional selectivity circuit in retina: Transformations by neurons singly and in concert. In Single Neuron Computation, T. McKenna, J. Davis, and S.F. Zornetzer, eds. (New York: Academic Press), pp. 347-375.
29. Bowling, D.B. (1980). Light responses of ganglion cells in the retina of the turtle. J. Physiol. 299, 173-196.
30. Brivanlou, I.H., Warland, D.K., and Meister, M. (1998). Mechanisms of concerted firing among retinal ganglion cells. Neuron 20, 527-539.
31. Buchsbaum, G., and Gottschalk, A. (1983). Trichromacy, opponent colours coding and optimum colour information transmission in the retina. Proc. R. Soc. Lond. B Biol. Sci. 220, 89-113.
32. Carandini, M., and Ferster, D. (1997). A tonic hyperpolarization underlying contrast adaptation in cat visual cortex. Science 276, 949-952.
33. Chow, K.-L., Blum, J.S., and Blum, R.A. (1950). Cell ratios in the thalamo-cortical visual system of Macaca mulatta. J. Comp. Neurol. 92, 227-239.
34. Croner, L.J., Purpura, K., and Kaplan, E. (1993). Response variability in retinal ganglion cells of primates. Proc. Natl. Acad. Sci. USA 90, 8128-8130.
35. Dan, Y., Atick, J.J., and Reid, R.C. (1996). Efficient coding of natural scenes in the lateral geniculate nucleus: Experimental test of a computational theory. J. Neurosci. 16, 3351-3362.
36. Dawis, S., Shapley, R., Kaplan, E., and Tranchina, D. (1984). The receptive field organization of X-cells in the cat: Spatiotemporal coupling and asymmetry. Vision Res. 24, 549-564.
37. DeVries, H.L. (1943). The quantum character of light and its bearing upon threshold of vision, the differential sensitivity and visual acuity of the eye. Physica 10, 553-564.
38. DeVries, S.H. (1999). Correlated firing in rabbit retinal ganglion cells. J. Neurophysiol., in press.
39. DeVries, S.H., and Baylor, D.A. (1997). Mosaic arrangement of ganglion cell receptive fields in rabbit retina. J. Neurophysiol. 78, 2048-2060.
40. DeWeese, M., and Zador, A. (1998). Asymmetric dynamics in optimal variance adaptation. Neural Comput. 10, 1179-1202.
41. Dong, D.W., and Atick, J.J. (1995). Statistics of natural time-varying images. Network 6, 345-358.
42. Donner, K.O., and Reuter, T. (1965). The dark-adaptation of single units in the frog's retina and its relation to the regeneration of rhodopsin. Vision Res. 5, 615-632.
43. Donner, K., Copenhagen, D.R., and Reuter, T. (1990). Weber and noise adaptation in the retina of the toad Bufo marinus. J. Gen. Physiol. 95, 733-753.
44. Donner, K., Djupsund, K., Reuter, T., and Vaisanen, I. (1991). Adaptation to light fluctuations in the frog retina. Neurosci. Res. Suppl. 15, S175-S184.
45. Donner, K., Koskelainen, A., Djupsund, K., and Hemila, S. (1995). Changes in retinal time scale under background light: Observations on rods and ganglion cells in the frog retina. Vision Res. 35, 2255-2266.
46. Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain (Cambridge, MA: Harvard University Press).
47. Enroth-Cugell, C., and Freeman, A.W. (1987). The receptive-field spatial structure of cat retinal Y cells. J. Physiol. 384, 49-79.
48. Enroth-Cugell, C., and Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. J. Physiol. 187, 517-552.
49. Enroth-Cugell, C., and Shapley, R.M. (1973a). Adaptation and dynamics of cat retinal ganglion cells. J. Physiol. 233, 271-309.
50. Enroth-Cugell, C., and Shapley, R.M. (1973b). Flux, not retinal illumination, is what cat retinal ganglion cells really care about. J. Physiol. 233, 311-326.
51. Enroth-Cugell, C., Robson, J.G., Schweitzer-Tong, D.E., and Watson, A.B. (1983). Spatio-temporal interactions in cat retinal ganglion cells showing linear spatial summation. J. Physiol. 341, 279-307.
52. Field, D.J. (1987). Relations between the statistics of natural images and the response properties of cortical cells. J. Opt. Soc. Am. A 4, 2379-2394.
53. Field, D.J. (1994). What is the goal of sensory coding? Neural Comput. 6, 559-601.
54. Gallant, J.L., Connor, C.E., and Van Essen, D.C. (1998). Neural activity in areas V1, V2 and V4 during free viewing of natural scenes compared to controlled viewing. Neuroreport 9, 2153-2158.
55. Hecht, S., Shlaer, S., and Pirenne, M. (1942). Energy, quanta, and vision. J. Gen. Physiol. 25, 819-840.
56. Hochstein, S., and Shapley, R.M. (1976). Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. J. Physiol. 262, 265-284.
57. Hunter, I.W.,and Korenberg, M.J. (1986). The identification of nonlinear biological systems: Wiener and Hammerstein cascade models. Biol. Cybern. 55, 135-144.
58. Johnsen, J.A., and Levine, M.W. (1983). Correlation of activity in neighbouring goldfish ganglion cells: Relationship between latency and lag. J. Physiol. 345, 439-449.
59. Keat, J.R., and Meister, M. (1997). Prediction of precisely timed spike events in retinal ganglion cells. Soc. Neurosci. Abstr. 23,1960.
60. Korenberg, M.J., Sakai, H.M., and Naka, K. (1989). Dissection of the neuron network in the catfish inner retina. III. Interpretation of spike kernels. J. Neurophysiol. 61, 1110-1120.
61. Koutalos, Y., and Yau, K.W. (1996). Regulation of sensitivity in vertebrate rod photoreceptors by calcium. Trends Neurosci. 19, 73-81.
62. Kraft, T.W., Schneeweis, D.M., and Schnapf, J.L. (1993). Visual transduction in human rod photoreceptors. J. Physiol. 464, 747-765.
63. Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. J. Neurophysiol. 16, 37-68.
64. Kuffler, S.W., Fitzhugh, R., and Barlow, H.B. (1957). Maintained activity in the cat's retina in light and darkness. J. Gen. Physiol. 40, 683-702.
65. Land, M.F. (1992). Predictable eye-head coordination during driving. Nature 359, 318-320.
66. Lankheet, M.J., Molenaar, J., and van de Grind, W.A. (1989). The spike generating mechanism of cat retinal ganglion cells. Vision Res. 29, 505-517.
67. Lee, B.B. (1996). Receptive field structure in the primate retina. Vision Res. 36, 631-644.
68. Levick, W.R., and Zacks, J.L. (1970). Responses of cat retinal ganglion cells to brief flashes of light. J. Physiol. 206, 677-700.
69. Levine, M.W., and Shefner, J.M. (1977). A model for the variability of interspike intervals during sustained firing of a retinal neuron. Biophys. J. 19, 241-252.
70. Levine, M.W., Zimmerman, R.P., and Carrion-Carire, V. (1988). Variability in responses of retinal ganglion cells. J. Opt. Soc. Am. A 5, 593-597.
71. Levine, M.W., Cleland, B.G., and Zimmerman, R.P. (1992). Variability of responses of cat retinal ganglion cells. Vis. Neurosci. 8, 277-279.
72. MacKay, D.M., and McCulloch, W.S. (1952). The limiting information capacity of a neuronal link. Bull. Math. Biophys. 14, 127-135.
73. Masland, R.H., and Ames, A. (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. J. Neurophysiol. 39, 1220-1235.
74. Mastronarde, D.N. (1983). Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells. J. Neurophysiol. 49, 303-324.
75. Mastronarde, D.N. (1989). Correlated firing of retinal ganglion cells. Trends Neurosci. 12, 75-80.
76. Meister, M. (1996). Multineuronal codes in retinal signaling. Proc. Natl. Acad. Sci. USA 93, 609-614.
77. Meister, M., Lagnado, L., and Baylor, D.A. (1995). Concerted signaling by retinal ganglion cells. Science 270, 1207-1210.
78. Muller, J.F., and Dacheux, R.F. (1997). Alpha ganglion cells of the rabbit retina lose antagonistic surround responses under dark adaptation. Vis. Neurosci. 14, 395-401.
79. Naka, K.I., Chan, R.Y., and Yasui, S. (1979). Adaptation in catfish retina. J. Neurophysiol. 42, 441-454.
80. Nakatani, K., Tamura, T., and Yau, K.W. (1991). Light adaptation in retinal rods of the rabbit and two other nonprimate mammals. J. Gen. Physiol. 97, 413-435.
81. Ohzawa, I., Sclar, G., and Freeman, R.D. (1985). Contrast gain control in the cat's visual system. J. Neurophysiol. 54, 651-667.
82. Peichl, L., and Wässle, H. (1979). Size, scatter and coverage of ganglion cell receptive field centres in the cat retina. J. Physiol. 291, 117-141.
83. Perkel, D.H., and Bullock, T.H. (1968). Neural coding. Neurosci. Res. Program Bull. 6, 221-348.
84. Purpura, K., Tranchina, D., Kaplan, E., and Shapley, R.M. (1990). Light adaptation in the primate retina: Analysis of changes in gain and dynamics of monkey retinal ganglion cells. Vis. Neurosci. 4, 75-93.
85. Reich, D.S., Victor, J.D., Knight, B.W., Ozaki, T., and Kaplan, E. (1997). Response variability and timing precision of neuronal spike trains in vivo. J. Neurophysiol. 77, 2836-2841.
86. Reinagel, P., and Reid, R.C. (1998). Visual stimulus statistics and the reliability of spike timing in the LGN. Soc. Neurosci. Abstr. 24, 139.
87. Rieke, F., Warland, D., de Ruyter van Steveninck, R.R., and Bialek, W. (1997). Spikes: Exploring the Neural Code (Cambridge, MA: MIT Press).
88. Rodieck, R.W. (1965). Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Res. 5, 583-601.
89. Rodieck, R.W. (1998). The First Steps in Seeing (Sunderland, MA: Sinauer Associates).
90. Rodieck, R.W., and Stone, J. (1965). Response of cat retinal ganglion cells to moving visual patterns. J. Neurophysiol. 28, 819-832.
91. Rodieck, R.W., Brening, R.K., and Watanabe, M. (1993). The origin of parallel visual pathways. In Contrast Sensitivity, R. Shapley and D.M.-K. Lam, eds. (Cambridge, MA: MIT Press).
92. Ruderman, D.L. (1994). The statistics of natural images. Network 5, 517-548.
93. Ruderman, D.L. (1997). Origins of scaling in natural images. Vision Res. 37, 3385-3398.
94. Ruderman, D.L., Cronin, T.W., and Chiao, C.-C. (1998). Statistics of cone responses to natural images: Implications for visual coding. J. Opt. Soc. Am. A 15, 2036-2045.
95. Sakai, H.M., and Naka, K. (1987). Signal transmission in the catfish retina. V. sensitivity and circuit. J. Neurophysiol. 58, 1329-1350.
96. Sakai, H.M., and Naka, K.-I. (1988). Neuron network in catfish retina. Prog. Ret. Res. 7, 149-208.
97. Sakai, H.M., and Naka, K. (1995). Response dynamics and receptive-field organization of catfish ganglion cells. J. Gen. Physiol. 105, 795-814.
98. Sakai, H.M., Wang, J.L., and Naka, K. (1995). Contrast gain control in the lower vertebrate retinas. J. Gen. Physiol. 105, 815-835.
99. Schellart, N.A., and Spekreijse, H. (1972). Dynamic characteristics of retinal ganglion cell responses in goldfish. J. Gen. Physiol. 59, 1-21.
100. Schieting, S., and Spillmann, L. (1987). Flicker adaptation in the peripheral retina. Vision Res. 27, 277-284.
101. Schnitzer, M.J., and Meister, M. (1996). Multi-neuronal firing patterns among retinal ganglion cells carry distinct visual messages. Soc. Neurosci. Abstr. 22, 494.
102. Shannon, C.E., and Weaver, W. (1963). The Mathematical Theory of Communication, Second Edition (Chicago: University of Illinois Press).
103. Shapley, R., and Enroth-Cugell, C. (1984). Visual adaptation and retinal gain controls. Prog. Ret. Res. 3, 263-346.
104. Shapley, R., and Lam, D.M.-K. (1993). Contrast Sensitivity (Cambridge, MA: MIT Press).
105. Shapley, R.M., and Victor, J.D. (1978). The effect of contrast on the transfer properties of cat retinal ganglion cells. J. Physiol. 285, 275-298.
106. Shapley, R.M., and Victor, J.D. (1979). Nonlinear spatial summation and the contrast gain control of cat retinal ganglion cells. J. Physiol. 290, 141-161.
107. Shapley, R.M., and Victor, J.D. (1981). How the contrast gain control modifies the frequency responses of cat retinal ganglion cells. J. Physiol. 318, 161-179.
108. Skavenski, A.A., Hansen, R.M., Steinman, R.M., and Winterson, B.J. (1979). Quality of retinal image stabilization during small natural and artificial body rotations in man. Vision Res. 19, 675-683.
109. Smirnakis, S.M., Berry, M.J., Warland, D.K., Bialek, W., and Meister, M. (1997). Adaptation of retinal processing to image contrast and spatial scale. Nature 386, 69-73.
110. Srinivasan, M.V., Laughlin, S.B., and Dubs, A. (1982). Predictive coding: A fresh view of inhibition in the retina. Proc. R. Soc. Lond. B Biol. Sci. 216, 427-459.
111. Stell, W.K., Detwiler, P.B., Wagner, H.G., and Wolbarsht, M.L. (1975). Giant retinal ganglion cells in dogfish (Mustelus): Electrophysiology of single on-center units. In Vision in Fishes, M.-A. Ali, ed. (New York: Plenum Press), pp. 99-112.
112. Stone, J. (1983). Parallel Processing in the Visual System (New York: Plenum Press).
113. Strong, S.P., Koberle, R., de Ruyter van Steveninck, R.R., and Bialek, W. (1998). Entropy and information in neural spike trains. Phys. Rev. Lett. 80, 197-200.
114. Troy, J.B., and Enroth-Cugell, C. (1993). X and Y ganglion cells inform the cat's brain about contrast in the retinal image. Exp. Brain Res. 93, 383-390.
115. Troy, J.B., and Lee, B.B. (1994). Steady discharges of macaque retinal ganglion cells. Vis. Neurosci. 11, 111-118.
116. Troy, J.B., and Robson, J.G. (1992). Steady discharges of X and Y retinal ganglion cells of cat under photopic illuminance. Vis. Neurosci. 9, 535-553.
117. van der Schaaf, A., and van Hateren, J.H. (1996). Modelling the power spectra of natural images - Statistics and information. Vision Res. 36, 2759-2770.
118. van Dijk, B.W., and Ringo, J.L. (1987). The variation in the light responses of carp retinal ganglion cells is independent of response amplitude. Vision Res. 27, 493-497.
119. van Hateren, J.H. (1992). A theory of maximizing sensory information. Biol. Cybern. 68, 23-29.
120. Victor, J.D. (1987). The dynamics of the cat retinal X cell centre. J. Physiol. 386, 219-246.
121. Victor, J.D. (1988). The dynamics of the cat retinal Y cell subunit. J. Physiol. 405, 289-320.
122. Victor, J.D., and Shapley, R.M. (1979). The nonlinear pathway of Y ganglion cells in the cat retina. J. Gen. Physiol. 74, 671-689.
123. Wandell, B.A. (1995). Foundations of Vision (Sunderland, MA: Sinauer).
124. Warland, D.K., Reinagel, P., and Meister, M. (1997). Decoding visual information from a population of retinal ganglion cells. J. Neurophysiol. 78, 2336-2350.
125. Wässle, H., and Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiol. Rev. 71, 447-480.
126. Winfield, D.A., and Powell, T.P. (1983). Laminar cell counts and geniculo-cortical boutons in area 17 of cat and monkey. Brain Res. 277, 223-229.
127. Yau, K.W. (1994). Phototransduction mechanism in retinal rods and cones. Invest. Ophthalmol. Vis. Sci. 35, 9-32.
128. Yeh, T., Lee, B.B., and Kremers, J. (1996). The time course of adaptation in macaque retinal ganglion cells. Vision Res. 36, 913-931.