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Light adaptation in the primate retina: Analysis of changes in gain and dynamics of monkey retinal ganglion cells

Published online by Cambridge University Press:  02 June 2009

Keith Purpura ,
Daniel Tranchina ,
Ehud Kaplan  and
Robert M. Shapley
Keith Purpura
Affiliation:
Department of Neurology and Neuroscience, Cornell University Medical College, New York
Daniel Tranchina
Affiliation:
Department of Biology, New York University, New York Courant Institute of Mathematical Sciences, New York University, New York Center for Neural Science, New York University, New York
Ehud Kaplan
Affiliation:
Laboratory of Biophysics, The Rockefeller University, New York
Robert M. Shapley
Affiliation:
Department of Biology, New York University, New York Center for Neural Science, New York University, New York Department of Psychology, New York University, New York
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Abstract

The responses of monkey retinal ganglion cells to sinusoidal stimuli of various temporal frequencies were measured and analyzed at a number of mean light levels. Temporal modulation tuning functions (TMTFs) were measured at each mean level by varying the drift rate of a sine-wave grating of fixed spatial frequency and contrast. The changes seen in ganglion cell temporal responses with changes in adaptation state were similar to those observed in human subjects and in turtle horizontal cells and cones tested with sinusoidally flickering stimuli; “Weber's Law” behavior was seen at low temporal frequencies but not at higher temporal frequencies. Temporal responses were analyzed in two ways: (1) at each light level, the TMTFs were fit by a model consisting of a cascade of low- and high-pass filters; (2) the family of TMTFs collected over a range of light levels for a given cell was fit by a linear negative feedback model in which the gain of the feedback was proportional to the mean light level. Analysis (1) revealed that the temporal responses of one class of monkey ganglion cells (M cells) were more phasic at both photopic and mesopic light levels than the responses of P ganglion cells. In analysis (2), the linear negative feedback model accounted reasonably well for changes in gain and dynamics seen in three P cells and one M cell. From the feedback model, it was possible to estimate the light level at which the dark-adapted gain of the cone pathways in the primate retina fell by a factor of two. This value was two to three orders of magnitude lower than the value estimated from recordings of isolated monkey cones. Thus, while a model which includes a single stage of negative feedback can account for the changes in gain and dynamics associated with light adaptation in the photopic and mesopic ranges of vision, the underlying physical mechanisms are unknown and may involve elements in the primate retina other than the cone.

Keywords

Primate retinaLight adaptationDynamics
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 1 , January 1990 , pp. 75 - 93
Copyright
Copyright © Cambridge University Press 1990

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References

Ashmore, J.F. & Falk, G. (1979). Transmission of visual signals to bipolar cells near absolute threshold. Vision Research 19, 419–423.CrossRefGoogle ScholarPubMed
Barlow, H.B. & Levick, W.R. (1969). Three factors limiting the reliable detection of light by retinal ganglion cells of the cat. Journal of Physiology (London) 200, 1–24.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Hodgkin, A.L. (1974) Changes in time scale and sensitivity in turtle photoreceptors. Journal of Physiology (London) 242, 729–758.CrossRefGoogle ScholarPubMed
Baylor, D.A., Fuortes, M.G.F. & O'bryan, P.M.. (1971). Receptive fields in the retina of the turtle. Journal of Physiology (London) 214, 433–464.CrossRefGoogle ScholarPubMed
Baylor, D.A., Hodgkin, A.L. & Lamb, T.D. (1974). Reconstruction of the electrical responses of turtle cones to flashes and steps of light. Journal of Physiology (London) 242, 759–791.CrossRefGoogle ScholarPubMed
Baylor, D.A., Nunn, B.J. & Schnapf, J.L. (1984). The photocurrent, noise and spectral sensitivity of rods of the monkey (Macaca fascicularis). Journal of Physiology (London) 357, 575–607.CrossRefGoogle ScholarPubMed
Burkhardt, D.A., Gottesman, J. & Thoreson, W.B. (1988). Prolonged depolarization in turtle cones evoked by current injection and stimulation of the receptive-field surround. Journal of Physiology 407, 324–348.CrossRefGoogle ScholarPubMed
Chappell, R.Z., Naka, K.-I. & Sakuranaga, M. (1985) Dynamics of turtle horizontal cell responses. Journal of General Physiology 86, 423–453.CrossRefGoogle Scholar
Cleland, B.G. & Enroth-Cugell, C. (1968). Quantitative aspects of sensitivity and summation in the cat retina. Journal of Physiology (London) 198, 17–38.CrossRefGoogle ScholarPubMed
Copenhagen, D.R. & Green, D.G. (1987). Spatial spread of adaptalion within the cone network of turtle retina. Journal of Physiology (London) 393, 763–776.CrossRefGoogle ScholarPubMed
Daly, S.J. & Normann, R.A. (1985). Temporal information processing in cones: effects of light adaptation on temporal summation and modulation. Vision Research 25, 1197–1206.CrossRefGoogle ScholarPubMed
De Lange, H. (1952). Experiments on flicker and some calculations on an electrical analogue of the fovea systems. Physics 28, 935–950.Google Scholar
De Lange, H. (1958). Research into the dynamic nature of the human fovea-cortex systems with intermittent and modulated light, I: Attenuation characteristics with white and colored light. Journal of the Optical Society of America 48, 777–784.CrossRefGoogle Scholar
De Monasterio, F.M. (1978). Properties of concentrically organized X and Y ganglion cells of macaque retina. Journal of Neurophysiology 41, 1394–1417.CrossRefGoogle ScholarPubMed
De Monasterto, F.M. & Gouras, P. (1975). Functional organization of ganglion cells of the rhesus monkey retina. Journal of Physiology (London) 251, 167–195.CrossRefGoogle Scholar
Derrington, A.M. & Lennie, P. (1982). The influence of temporal frequency and adaptation level on receptive-field organization of retinal ganglion cells in cat. Journal of Physiology (London) 333, 343–366.CrossRefGoogle ScholarPubMed
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology 357, 219–240.CrossRefGoogle ScholarPubMed
DeValois, R.L. & Jacobs, G.F.I. (1968). Primate color vision. Science 162, 533–540.CrossRefGoogle Scholar
DeValois, R.L., Morgan, H.C. & Snodderly, D.M. (1974). Psychophysical studies of monkey vision, III: Spatial luminance contrast sensitivity tests of macaque and human observers. Vision Research 14, 75–81.CrossRefGoogle Scholar
Dodge, F.A., Knight, B.W. & Toyoda, J. (1968). Voltage noise in Limulus visual cells. Science 160, 88–90.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Shapley, R.M. (1973a). Adaptation and dynamics of cat retinal ganglion cells. Journal of Physiology (London) 233, 271–309.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Shapley, R.M. (1973b). Flux, not retinal illumination, is what cat retinal ganglion cells really care about. Journal of Physiology 233, 311–326.CrossRefGoogle Scholar
Enroth-Cugell, C., Hertz, B.G. & Lennie, P. (1977). Cone signals in the cat&s retina. Journal of Physiology (London) 269, 273–296.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C., Robson, J.G., Schweitzer-Tong, D.E. & Watson, A.B. (1983). Spatio-temporal interactions in cat retinal ganglion cells showing linear spatial summation. Journal of Physiology (London) 341, 279–307.CrossRefGoogle ScholarPubMed
Frumkes, T.E. (1987). Tonic inhibition of cone pathways by rods in distal vertebrate retina. Investigative Ophthalmology and Visual Science (Suppl.) 28, 50.Google Scholar
Frumkes, T.E. & Eysteinsson, T. (1987). Suppressive rod-cone interaction in distal vertebrate retina: intracellular records from Xenopus and Necturus. Journal of Neurophysiology 57, 1361–1382.CrossRefGoogle ScholarPubMed
Fuortes, M.G.F. & Hodgkin, A.L. (1964). Changes in time scale and sensitivity in the ommatidia of Limulus. Journal of Physiology (London) 172, 239–263.CrossRefGoogle ScholarPubMed
Geisler, W.S. (1981). Effects of bleaching and backgrounds on the flash response of the cone system. Journal of Physiology (London) 312, 413–434.CrossRefGoogle ScholarPubMed
Gouras, P. (1968). Identification of cone mechanisms in monkey ganglion cells. Journal of Physiology (London) 199, 533–547.CrossRefGoogle ScholarPubMed
Hayhoe, M.M., Benimoff, N.I. & Hood, D.C. (1987). The time course of multiplicative and subtractive adaptation process. Vision Research 27, 1981–1996.CrossRefGoogle ScholarPubMed
Hochstein, S. & Shapley, R.M. (1976). Quantitative analysis of retinal ganglion cell classifications. Journal of Physiology (London) 262, 237–264.CrossRefGoogle ScholarPubMed
Hood, D.C. & Finkelstein, M.A. (1986). Sensitivity to light. In Handbook of Perception and Human Performance, Vol. 1, Sensory Processes and Perception, ed. Boff, K.R., Kaufmann, L. & Thomas, J.P., pp. (5)1–(5)66. New York: John Wiley and Sons.Google Scholar
Itzhaki, A. & Perlman, I. (1987). Light adaptation of red cones and L1-horizontal cells in the turtle retina: effects of the background spatial pattern. Vision Research 27, 685–696.CrossRefGoogle ScholarPubMed
Ives, H.E. (1922). Critical frequency relations in scotopic vision. Journal of the Optical Society of America 6, 254–268.CrossRefGoogle Scholar
Kaplan, E. & Shapley, R. (1984). The origin of the S (slow) potential in the mammalian lateral geniculate nucleus. Experimental Brain Research 55, 111–116.CrossRefGoogle Scholar
Kaplan, E. & Shapley, R.M. (1986). The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proceedings of the National Academy of Sciences of the U.S.A. 83, 755–2757.CrossRefGoogle ScholarPubMed
Kaplan, E., Lee, B.B. & Shapley, R.M. (1990). New views of primate retinal function. In Progress in Retinal Research. Oxford: Pergamon Press.Google Scholar
Kelly, D.H. (1961). Visual responses to time-dependent stimuli, I: Amplitude sensitivity measurements. Journal of the Optical Society of America 51, 422–429.CrossRefGoogle ScholarPubMed
Kelly, D.H. (1971). Theory of flicker and transient responses, II: Counterphase gratings. Journal of the Optical Society of America 61, 632–640.CrossRefGoogle ScholarPubMed
Kelly, D.H. (1972). Adaptation effects on spatio-temporal sine-wave thresholds. Vision Research 12, 89–101.CrossRefGoogle ScholarPubMed
Kelly, D.H. (1979). Motion and vision, II: Stabilized spatio-temporal threshold surface. Journal of the Optical Society of America 69, 1340–1349.CrossRefGoogle ScholarPubMed
King, F.A., Yarbrough, C.J., Anderson, D.C., Gordon, T.P. & Gould, K.G. (1988). Primates. Science 240, 1475–1482.CrossRefGoogle ScholarPubMed
Lennie, P. (1980). Parallel visual pathways: a review. Vision Research 20, 561–594.CrossRefGoogle ScholarPubMed
Marrocco, R.T. (1972). Maintained activity of monkey optic tract fibers and lateral geniculate nucleus cells. Vision Research 12, 1175–1181.CrossRefGoogle ScholarPubMed
Marmarelis, P.Z. & Naka, K.-I. (1973). Nonlinear analysis and synthesis of receptive-field responses in the catfish retina, III: Two-input white-noise analysis. Journal of Neurophysiology 36, 634–648.CrossRefGoogle Scholar
Milkman, N., Schick, G., Rossetto, M., Ratliff, F., Shapley, R.M. & Victor, J.D. (1980). A two-dimensional computer-controlled visual stimulator. Behavioral Research Methods and Instrumentation 12, 283–292.CrossRefGoogle Scholar
Naka, K.-I., Chan, R.Y. & Yasui, S. (1979). Adaptation in catfish retina. Journal of Neurophysiology 42, 441–454.CrossRefGoogle ScholarPubMed
Naka, K.-I., Itoh, M.-A. & Chappell, R.L. (1987). Dynamics of turtle cones. Journal of General Physiology 89, 321–337.CrossRefGoogle ScholarPubMed
Normann, R.A. & Perlman, I. (1979). The effects of background illumination on the photoresponses of red and green cones. Journal of Physiology (London) 286, 491–507.CrossRefGoogle ScholarPubMed
O'Bryan, P.M. (1973). Properties of the depolarizing synaptic potential evoked by peripheral illumination in cones of the turtle retina. Journal of Physiology (London) 235, 207–223.CrossRefGoogle ScholarPubMed
Purpura, K., Kaplan, E. & Shapley, R.M. (1988). Background light and the contrast gain of primate P and M retinal ganglion cells. Proceedings of the National Academy of Sciences of the U.S.A. 85, 4534–4537.CrossRefGoogle ScholarPubMed
Richter, J. & Ullman, S. (1982). A model for the temporal organization of X- and Y-type receptive fields in the primate retina. Biological Cybernetics 43, 127–145.CrossRefGoogle Scholar
Rodieck, R. (1973). The Vertebrate Retina. San Francisco, California: W.H. Freeman Press.Google Scholar
Rodleck, R. (1988). The Primate Retina. In:Comparative Primate Biology Vol. 4: NeuroSciences. New York: Alan R. Liss, pp.203–278.Google Scholar
Roufs, J.A.J. (1972). Dynamic properties of vision, I: Experimental relationships between flicker and flash thresholds. Vision Research 12, 261–278.CrossRefGoogle ScholarPubMed
Rushton, W.A.H. (1965). The Ferrier lecture, 1962. Visual adaptation. Proceedings of the Royal Society B (London) 162, 20–46.Google Scholar
Schiller, P.H. & Malpeli, J.G. (1977). Properties and tectal projections of monkey retinal ganglion cells. Journal of Neurophysiology 40, 428–445.CrossRefGoogle ScholarPubMed
Schiller, P.H & Malpeli, J.G. (1978). Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey. Journal of Neurophysiology 41, 788–797.CrossRefGoogle ScholarPubMed
Schnapf, J.L. & Baylor, D.A. (1988). Phototransduction in cones of the monkey (Macaca fascicularis). Investigative Ophthalmology and Visual Science (Suppl.) 29, 223.Google Scholar
Shapley, R. & Enroth-Cugell, C. (1984). Visual adaptation and retinal gain controls. In Progress in Retinal Research, ed. Osborne, N. & Chader, G., pp. 263–346. London, England: Pergamon Press.Google Scholar
Shapley, R.M. & Perry, V.H. (1986). Cat and monkey retinal ganglion cells and their visual functional roles. Trends in NeuroSciences 9, 229–235.CrossRefGoogle Scholar
Sneyd, J. & Tranchina, D. (1989). Phototransduction in turtle cones: an inverse problem in enzyme kinetics. Bulletin of Mathematical Biology 51, 749–784.CrossRefGoogle Scholar
Spekreuse, H., Van, Norren D. & Van, Den Berg T.J.T.P. (1971). Flicker responses in monkey lateral geniculate nucleus and human perception of flicker. Proceedings of the National Academy of Sciences of the U.S.A. 68, 2802–2805.CrossRefGoogle Scholar
Sperling, G. & Sondhi, M.M. (1968). Model for visual luminance discrimination and flicker detection. Journal of the Optical Society of America 58, 1133–1145.CrossRefGoogle ScholarPubMed
Toyoda, J.-I. (1974). Frequency characteristics of retinal neurons in the carp. Journal of General Physiology 63, 214–234.CrossRefGoogle ScholarPubMed
Tranchina, D. & Peskin, C.S. (1988). Light adaptation in the turtle retina: embedding a parametric family of linear models in a single nonlinear model. Visual NeuroScience 1, 339–348.CrossRefGoogle Scholar
Tranchina, D., Gordon, J. & Shapley, R.M. (1984). Retinal light adaptation–evidence for a feedback mechanism. Nature 310, 314–16.CrossRefGoogle ScholarPubMed
Tranchina, D., Sneyd, J. & Cadenas, I.D. (1990). Light adaptation in turtle cones: Testing and analysis of a model for phototransduction (submitted).CrossRefGoogle Scholar
Valeton, J.M. & Van Norren, D. (1983). Light adaptation of primate cones: an analysis based on extracellular data. Vision Research 23, 1539–1547.CrossRefGoogle ScholarPubMed
Victor, J.D. (1987). The dynamics of the cat retinal X cell centre. Journal of Physiology 386, 219–246.CrossRefGoogle ScholarPubMed
Virsu, V. & Lee, B.B. (1983). Light adaptation in cells in macaque lateral geniculate nucleus and its relation to human light adaptation. Journal of Neurophysiology 50, 864–878.CrossRefGoogle ScholarPubMed
Virsu, V., Lee, B.B. & Creutzfeldt, O.D. (1987). Mesopic spectral responses and the Purkinje shift of macaque lateral geniculate nucleus cells. Vision Research 27, 191–200.CrossRefGoogle ScholarPubMed
Watson, A.B. (1986). Temporal sensitivity. In Handbook of Perception and Human Performance, Vol. 1, Sensory Processes and Perception, ed. Boff, K.R., Kaufmann, L. & Thomas, J.P., pp. (6)1–(6)43. New York: John Wiley and Sons.Google Scholar
Zrenner, E. (1983). Neurophysiological Aspects of Color Vision in Primates: Comparative Studies on Simian Retinal Ganglion Cells and the Human Visual System. Berlin: Springer-Verlag.CrossRefGoogle Scholar