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Visual latency and brightness: An interpretation based on the responses of rods and ganglion cells in the frog retina

Published online by Cambridge University Press:  02 June 2009

Kristian Donner
Kristian Donner
Affiliation:
Department of Zoology, University of Helsinki, SF-00100 Helsinki, Finland
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Abstract

Rod and cone photoresponses in a variety of species have been accurately described with linear multistage filter models. In this study, the response latency and initial coding of intensity at two higher levels of visual processing are related to such photoreceptor responses. One level is the retinal output (spiking discharges from frog ganglion cells, based on experimental data reported here), the other is the perceptual level in humans (psychophysical latency and brightness functions, based on data from the literature). Photoreceptor responses are described with the “independent activation” model of Baylor et al. (1974). The intensity dependence of the early ganglion cell discharge, its latency and initial impulse frequency, is shown to follow from such a waveform, assuming that 1) latency L = l + D, where l is the time it takes for the rod response linearly summed over the ganglion cell's receptive field to reach a criterion amplitude, and D is a constant delay; and 2) the initial frequency (below saturation) is proportional to the steepness of rise of the summed rod response at time l. It is shown that the intensity dependences of 1) human visual latency and 2) brightness sensation, including effects of stimulus area and duration, are accounted for by the same model. The predicted functions are not power functions of intensity, but approximate such over wide ranges. Thus, a large body of psychophysical data is explained simply by the waveform of photoreceptor responses.

Keywords

PhotoreceptorsImpulse frequencyNeural intensity codingPsychophysical power law
Type
Research Articles
Information
Visual Neuroscience , Volume 3 , Issue 1 , July 1989 , pp. 39 - 51
Copyright
Copyright © Cambridge University Press 1989

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References

Aho, A.-C., Donner, K., Hydén, C., Reuter, T. & Orlov, O. Yu. (1987). Retinal noise, the performance of retinal ganglion cells, and visual sensitivity in the dark-adapted frog. Journal of the Optical Society of America A 4, 2321–2329.CrossRefGoogle ScholarPubMed
Aiba, T.S. & Stevens, S.S. (1964). Relation of brightness to duration and luminance under light and dark adaptation. Vision Research 4, 391–401.CrossRefGoogle ScholarPubMed
Alpern, M. (1968). A note on visual latency. Psychological Review 75, 260–264.CrossRefGoogle ScholarPubMed
Alpern, M., Rushton, W.A.H. & Torh, S. (1970 a). The size of rod signals. Journal of Physiology 206, 193–208.CrossRefGoogle ScholarPubMed
Alpern, M., Rushton, W.A.H. & Torh, S. (1970 b). Signals from cones. Journal of Physiology 207, 463–475.CrossRefGoogle ScholarPubMed
Bäckström, A.-C. & Reuter, T. (1975). Receptive-field organization of ganglion cells in the frog retina: contributions from cones, green rods, and red rods. Journal of Physiology 246, 79–107.CrossRefGoogle ScholarPubMed
Bäckström, A.-C., Hemilä, S. & Reuter, T. (1978). Directional selectivity and colour coding in the frog retina. Medical Biology 56, 72–83.Google ScholarPubMed
Barlow, R.B. Jr. & Verrillo, R.T. (1976). Brightness sensation in a Ganzfeld. Vision Research 16, 1291–1297.CrossRefGoogle Scholar
Barlow, R.B. Jr, Snodderly, D.M. & Swadlow, H.A. (1978). Intensity coding in primate visual system. Experimental Brain Research 31, 163–177.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Fettiplace, R. (1977). Kinetics of synaptic transfer from receptors to ganglion cells in turtle retina. Journal of Physiology 271, 425–448.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Fuortes, M.G.F. (1970). Electrical responses of single cones in the retina of the turtle. Journal of Physiology 207, 77–92.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Hodgkin, A.L. (1973). Detection and resolution of visual stimuli by turtle photoreceptors. Journal of Physiology 214, 265–294.CrossRefGoogle Scholar
Baylor, D.A., Hodgkin, A.L. & Lamb, T.D. (1974). The electrical response of turtle cones to flashes and steps of light. Journal of Physiology 242, 685–727.CrossRefGoogle ScholarPubMed
Baylor, D.A., Lamb, T.D. & Yau, K.-W. (1979). The membrane current of single rod outer segments. Journal of Physiology 288, 589–611.CrossRefGoogle ScholarPubMed
Baylor, D.A., Matthews, G. & Yau, K.-W. (1983). Temperature effects on the membrane current of retinal rods of the toad. Journal of Physiology 337, 723–734.CrossRefGoogle ScholarPubMed
Baylor, D.A., Nunn, B.J. & Schnapf, J.F. (1984). The photocurrent, noise, and spectral sensitivity of rods of the monkey (Macaca fascicularis). Journal of Physiology 357, 575–607.CrossRefGoogle ScholarPubMed
Burkhardt, D.A. & Gottesman, J. (1987). Light adaptation and the responses to contrast flashes in cones of the walleye retina. Vision Research 27, 1409–1420.CrossRefGoogle ScholarPubMed
Burkhardt, D.A., Gottesman, J. & Keenan, R.M. (1987). Sensory latency and reaction time: dependence on contrast polarity and early linearity in human vision. Journal of the Optical Society of America A 4, 530–539.CrossRefGoogle ScholarPubMed
Burkhardt, D.A., Gottesman, J., Kersten, D. & Legge, G.E. (1984). Symmetry and constancy in the perception of negative and positive luminance contrast. Journal of the Optical Society of America A 1, 309–316.CrossRefGoogle ScholarPubMed
Cervetto, L., Pasino, E. & Torre, V. (1977). Electrical responses of rods in the retina of Bufo marinus. Journal of Physiology 267, 17–51.CrossRefGoogle ScholarPubMed
Cleland, B.G. & Enroth-Cugell, C. (1968). Quantitative aspects of sensitivity and summation in the cat retina. Journal of Physiology 198, 17–38.CrossRefGoogle ScholarPubMed
Copenhagen, D.R., Donner, K. & Reuter, T. (1987). Ganglion cell performance at absolute threshold in toad retina: effects of dark events in rods. Journal of Physiology 393, 667–680.CrossRefGoogle ScholarPubMed
Detwiler, P.B., Hodgkin, A.L. & McNaughton, P.A. (1980). Temporal and spatial characteristics of the voltage response of rods in the retina of the snapping turtle. Journal of Physiology 300, 213–250.CrossRefGoogle ScholarPubMed
Donner, K. (1981). Receptive fields of frog retinal ganglion cells: response formation and light-dark adaptation. Journal of Physiology 319, 131–142.CrossRefGoogle ScholarPubMed
Donner, K. (1985). The ganglion cells of the frog retina: receptive-field mechanisms and adaptational changes in these. Ph.D. Thesis, University of Helsinki.Google Scholar
Donner, K. (1987 a). Surround control of center adaptation in the receptive fields of frog retinal ganglion cells. Vision Research 27, 1211–1221.CrossRefGoogle ScholarPubMed
Donner, K. (1987 b). Adaptation-related changes in the spatial and temporal summation of frog retinal ganglion cells. Acta Physiologica Scandinavica 131, 479–487.CrossRefGoogle ScholarPubMed
Donner, K. & Grönholm, M.-L. (1984). Center and surround excitation in the receptive fields of frog retinal ganglion cells. Vision Research 24, 1807–1819.CrossRefGoogle ScholarPubMed
Donner, K. & Hemilä, S. (1985). Rhodopsin phosphorylation inhibited by adenosine in frog rods: lack of effects on excitation. Comparative Biochemistry and Physiology 81 A, 431–439.CrossRefGoogle ScholarPubMed
Donner, K., Copenhagen, D.R. & Reuter, T. (1989). Weber and noise adaptation in the retina of the toad (Bufo marinus). Journal of General Physiology (to be published).Google Scholar
Donner, K., Hemilä, S. & Koskelainen, A. (1988). Temperature dependence of rod photoresponses from the aspartate-treated retina of the frog (Rana temporaria). Acta Physiologica Scandinavica 134, 535–541.CrossRefGoogle ScholarPubMed
Donner, K.O. & Reuter, T. (1968). Visual adaptation of the rhodopsin rods in the frog's retina. Journal of Physiology 199, 59–87.CrossRefGoogle Scholar
Fain, G.L. (1976). Sensitivity of toad rods: dependence on wave-length and background illumination. Journal of Physiology 261, 71–101.CrossRefGoogle ScholarPubMed
Fuortes, M.G.F. & Hodgkin, A.L. (1964). Changes in time scale and sensitivity in the ommatidia of Limulus. Journal of Physiology 172, 239–263.CrossRefGoogle ScholarPubMed
Gouras, P. & Link, K. (1966). Rod and cone interaction in dark-adapted monkey ganglion cells. Journal of Physiology 184, 499–510.CrossRefGoogle ScholarPubMed
Hartline, H.K. (1940). The effects of spatial summation in the retina on the excitation of the optic nerve. American Journal of Physiology 130, 700–711.CrossRefGoogle Scholar
Hemilä, S.O. (1977). Background adaptation in the rods of the frog's retina. Journal of Physiology 265, 721–741.CrossRefGoogle ScholarPubMed
Hemila, S. & Reuter, T. (1981). Longitudinal spread of adaptation in the rods of the frog's retina. Journal of Physiology 310, 501–528.CrossRefGoogle ScholarPubMed
Hopkinson, R.G. (1956). Light energy and brightness sensation. Nature 178, 1065–1066.CrossRefGoogle Scholar
Lamb, T.D. (1984). Effects of temperature changes on toad rod photocurrents. Journal of Physiology 346, 557–578.CrossRefGoogle ScholarPubMed
Mansfield, R.J.W. (1973 a). Latency functions in human vision. Vision Research 13, 2219–2234.CrossRefGoogle ScholarPubMed
Mansfield, R.J.W. (1973 b). Brightness function: effect of area and duration. Journal of the Optical Society of America 63, 913–920.CrossRefGoogle ScholarPubMed
Mansfield, R.J.W. & Daugman, J.D. (1978). Retinal mechanisms of visual latency. Vision Research 18, 1247–1260.CrossRefGoogle ScholarPubMed
Marks, L.E. (1972). Visual brightness: some applications of a model. Vision Research 12, 1409–1423.CrossRefGoogle ScholarPubMed
Marks, L.E. & Stevens, J.C. (1966). Individual brightness functions. Perception and Psychophysics 1, 17–24.CrossRefGoogle Scholar
Marrocco, R.T. (1975). Possible neural basis of brightness magnitude estimations. Brain Research 86, 128–133.CrossRefGoogle ScholarPubMed
Mecke, E., Orlov, O.Yu. & Reuter, T. (1989). Ganglion cell classes in the frog retina: anatomical characteristics limiting the information transmission in small and large ganglion cells. Vision Research (submitted).Google Scholar
Penn, R.D. & Hagins, W.A. (1972). Kinetics of the photocurrent of retinal rods. Biophysical Journal 12, 1073–1094.CrossRefGoogle ScholarPubMed
Reuter, T., Donner, K. & Copenhagen, D.R. (1986). Does the random distribution of discrete photoreceptor events limit the sensitivity of the retina? Neuroscience Research (Suppl.) 4, S163–S180.CrossRefGoogle ScholarPubMed
Schnapf, J.L. (1983). Dependence of the single photon response on longitudinal position of absorption in toad rod outer segments. Journal of Physiology 343, 147–159.CrossRefGoogle ScholarPubMed
Schwartz, E.A. (1976). Electrical properties of the rod syncytium in the retina of the turtle. Journal of Physiology 257, 379–406.CrossRefGoogle ScholarPubMed
Sillman, A.J., Ito, H. & Tomita, T. (1969). Studies on the mass receptor potential of the isolated frog retina. I. General properties of the response. Vision Research 9, 1435–1442.CrossRefGoogle ScholarPubMed
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
Stevens, S.S. (1961). To honour Fechner and repeal his law. Science 133, 80–86.CrossRefGoogle Scholar
Vaughan, H.G. Jr. & Hull, R.C. (1965). Functional relation between stimulus intensity and photically evoked cerebral responses in man. Nature 206, 720–722.CrossRefGoogle ScholarPubMed
Vaughan, H.G. Jr., Costa, L.D. & Gilden, L. (1966). The functional relation of visual evoked response and reaction time to stimulus intensity. Vision Research 6, 645–656.CrossRefGoogle ScholarPubMed