Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-26T13:41:33.909Z Has data issue: false hasContentIssue false
  • English
  • Français

Modelling the spatio-temporal modulation response of ganglion cells with difference-of-Gaussians receptive fields: Relation to photoreceptor response kinetics

Published online by Cambridge University Press:  02 June 2009

Kristian Donner  and
Simo Hemilä
Kristian Donner
Affiliation:
Department of Biosciences and Department of Ecology and Systematics, P.O. Box 17, F1N-00014 University of Helsinki, Finland
Simo Hemilä
Affiliation:
laboratory of Physics, Helsinki University of Technology, F1N-02150 Espoo, Finland
Get access Rights & Permissions [Opens in a new window]

Abstract

Difference-of-Gaussians (DOG) models for the receptive fields of retinal ganglion cells accurately predict linear responses to both periodic stimuli (typically moving sinusoidal gratings) and aperiodic stimuli (typically circular fields presented as square-wave pulses). While the relation of spatial organization to retinal anatomy has received considerable attention, temporal characteristics have been only loosely connected to retinal physiology. Here we integrate realistic photoreceptor response waveforms into the DOG model to clarify how far a single set of physiological parameters predict temporal aspects of linear responses to both periodic and aperiodic stimuli. Traditional filter-cascade models provide a useful first-order approximation of the single-photon response in photoreceptors. The absolute time scale of these, plus a time for retinal transmission, here construed as a fixed delay, are obtained from flash/step data. Using these values, we find that the DOG model predicts the main features of both the amplitude and phase response of linear cat ganglion cells to sinusoidal flicker. Where the simplest model formulation fails, it serves to reveal additional mechanisms. Unforeseen facts are the attenuation of low temporal frequencies even in pure center-type responses, and the phase advance of the response relative to the stimulus at low frequencies. Neither can be explained by any experimentally documented cone response waveform, but both would be explained by signal differentiation, e.g. in the retinal transmission pathway, as demonstrated at least in turtle retina.

Keywords

RetinaContrast sensitivityFlickerPhotoreceptors
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 1 , January 1996 , pp. 173 - 186
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Barlow, H.B. (1953). Summation and inhibition in the frog's retina. Journal of Physiology 119, 69–88.CrossRefGoogle ScholarPubMed
Baron, W.S. & Boynton, R.M. (1975). Response of primate cones to sinusoidally flickering homochromatic stimuli. Journal of Physiology 246, 311–331.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Fettiplace, R. (1977 a). Transmission from photoreceptors to ganglion cells in turtle retina. Journal of Physiology 271, 391–424.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Fettiplace, R. (1977 b). Kinetics of synaptic transfer from receptors to ganglion cells in turtle retina. Journal of Physiology 271, 425–448.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Fettiplace, R. (1979). Synaptic drive and impulse generation in ganglion cells of turtle retina. Journal of Physiology 288, 107–127.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. & 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., Nunn, B.J. & Schnapf, J.L. (1984). The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. Journal of Physiology 357, 575–607.CrossRefGoogle ScholarPubMed
Bolz, J., Rosner, G. & Wässle, H. (1982). Response latency of brisk-sustained (X) and brisk-transient (Y) cells in the cat retina. Journal of Physiology 328, 171–190.CrossRefGoogle ScholarPubMed
Chen, E.P. & Freeman, A.W. (1989). A model for spatiotempora! frequency responses in the X cell pathway of the cat's retina. Vision Research 29, 271–291.CrossRefGoogle Scholar
Creutzfeldt, O.D., Sakmann, B., Scheich, H. & Korn, A. (1970). Sensitivity distribution and spatial summation within receptive-field centre of retinal on-centre ganglion cells and transfer function of the retina. Journal of Neurophysiology 33, 654–671.CrossRefGoogle Scholar
Daly, S.J. & Normann, R.A. (1985). Temporal information processing in cones: Effect of light adaptation on temporal summation and modulation. Vision Research 25, 1197–1206.CrossRefGoogle ScholarPubMed
Dawis, S., Shapley, R., Kaplan, E. & Tranchina, D. (1984). The receptive field organization of X-cells in the cat: Spatiotemporal coupling and asymmetry. Vision Research 24, 549–564.CrossRefGoogle ScholarPubMed
de Lange, H. (1952). Experiments on flicker and some calculations on an electrical analogue of the foveal systems. Physica 18, 935–950.CrossRefGoogle Scholar
de Lange, H. (1958). Research into the dynamic nature of the human fovea-cortex systems with intermittent and modulated light. 1. Attenuation characteristics with white and colored light. Journal of the Optical Society of America 48, 777–784.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 the cat. Journal of Physiology 333, 343–366.CrossRefGoogle Scholar
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). How the latencies of excitation and inhibition determine ganglion cell thresholds and discharge patterns in the frog. Vision Research 21, 1689–1692.CrossRefGoogle ScholarPubMed
Donner, K. (1989). Visual latency and brightness: An interpretation based on the responses of rods and ganglion cells in the frog retina. Visual Neuroscience 3, 39–51.CrossRefGoogle ScholarPubMed
Donner, K., Djupsund, K., Reuter, T. & Väisänen, I. (1991). Adaptation to light fluctuations in the frog retina. Neuroscience Research (Suppl.) 15, S175–S184.Google ScholarPubMed
Donner, K., Koskelainen, A., Djupsund, K. & Hemilä, S. (1995). Changes in retinal time scale under background light: Observations on rods and ganglion cells in the frog retina. Vision Research 35, 2255–2266.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Lennie, P. (1975). The control of retinal ganglion cell discharge by receptive field surrounds. Journal of Physiology 247, 551–578.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology 187, 517–552.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Robson, J.G. (1984). Functional characteristics and diversity of cat retinal ganglion cells. Basic characteristics and quantitative description. Investigative Ophthalmology and Visual Science 25, 250–267.Google 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 341, 279–307.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Shapley, R.M. (1973). Flux, not retinal illumination, is what cat retinal ganglion cells really care about. Journal of Physiology 233, 311–326.CrossRefGoogle Scholar
Frishman, L.J., Freeman, A.W., Troy, J.B., Schweitzer-Tong, D.E. & Enroth-Cugell, C. (1987). Spatiotemporal frequency responses of cat retinal ganglion cells. Journal of General Physiology 89, 599–628.CrossRefGoogle ScholarPubMed
Frishman, L.J. & Linsenmeier, R.A. (1982). Effects of picrotoxin and strychnine on nonlinear responses of Y-type cat retinal ganglion cells. Journal of Physiology 324, 347–363.CrossRefGoogle ScholarPubMed
Fuortes, M.G.F. & Hodgkin, A.L. (1964). Changes in time scale and sensitivity in the ommatidia of Limulus. Journal of Physiology 156, 179–192.CrossRefGoogle Scholar
Gouras, P. & Link, K. (1966). Rod and cone interaction in dark-adapted monkey ganglion cells. Journal of Physiology 184, 499–510.CrossRefGoogle ScholarPubMed
Graham, N. & Hood, D.C. (1992). Modeling the dynamics of light adaptation: The merging of two traditions. Vision Research 32, 1373–1393.CrossRefGoogle ScholarPubMed
Grüsser, O.J. & Grüsser-Cornehls, U. (1973). Neuronal mechanisms of visual movement perception and some psychophysical and behavioral correlations. In Handbook of Sensory Physiology VII/3A. Centra/Processing of Visual Information, ed. Jung, R., pp. 333–429. Berlin, Germany: Springer.Google Scholar
Hochstein, S. & Shapley, R.M. (1976 a). Quantitative analysis of retinal ganglion cell classifications. Journal of Physiology 262, 237–264.CrossRefGoogle ScholarPubMed
Hochstein, S. & Shapley, R.M. (1976 b). Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. Journal of Physiology 262, 265–284.CrossRefGoogle ScholarPubMed
Hood, D.C. & Birch, D.G. (1993 a). Light adaptation of human rod receptors: The leading edge of the human a-wave and models of rod receptor activity. Vision Research 33, 1605–1618.CrossRefGoogle Scholar
Hood, D.C. & Birch, D.G. (1993 b). Human cone receptor activity: The leading edge of the a-wave and models of receptor activity. Visual Neuroscience 10, 857–871.CrossRefGoogle Scholar
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
Kolb, H. (1994). The architecture of functional neural circuits in the vertebrate retina. Investigative Ophthalmology and Visual Science 35, 2385–2404.Google ScholarPubMed
Kraft, T.W., Schneeweis, D.M. & Schnapf, J.L. (1993). Visual transduction in human rod photoreceptors. Journal of Physiology 464, 747–765.CrossRefGoogle ScholarPubMed
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 37–68.CrossRefGoogle ScholarPubMed
Lamb, T.D. & Pugh, E.N. Jr. (1992). A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. Journal of Physiology 449, 719–758.CrossRefGoogle ScholarPubMed
Lankheet, M.J.M., Prickaerts, J.H.H.J. & van de Grind, W.A. (1992). Responses of cat horizontal cells to sinusoidal gratings. Vision Research 32, 997–1008.CrossRefGoogle ScholarPubMed
Linsenmeier, R.A., Frishman, L.J., Jakiela, H.G. & Enroth-Cugell, C. (1982). Receptive field properties of X and Y cells in the cat retina derived from contrast sensitivity measurements. Vision Research 22, 1173–1183.CrossRefGoogle ScholarPubMed
Miller, R.F. & Dacheux, R.F. (1976). Synaptic organization and ionic basis of on and off channels in mudpuppy retina. III. A model of ganglion cell receptive field organization based on chloride-free experiments. Journal of General Physiology 67, 679–690.CrossRefGoogle Scholar
Nye, P.W. & Naka, K.-I. (1971). The dynamics of inhibitory interaction in a frog receptive field: A paradigm of paracontrast. Vision Research 11, 377–392.CrossRefGoogle Scholar
Peichl, L. & Wässle, H. (1979). Size, scatter and coverage of ganglion cell receptive field centres in the cat retina. Journal of Physiology 291, 117–141.CrossRefGoogle ScholarPubMed
Peichl, L. & Wässle, H. (1983). The structural correlate of the receptive field centre of Ó ganglion cells in the cat retina. Journal of Physiology 341, 309–324.CrossRefGoogle Scholar
Perry, R.J. & McNaughton, P.A. (1991). Response properties of cones from the retina of the tiger salamander. Journal of Physiology 433, 561–587.CrossRefGoogle ScholarPubMed
Purpura, K., Tranchina, D., Kaplan, E. & Shapley, R.M. (1990). Light adaptation in the primate retina: Analysis of changes in gain and dynamics of monkey retinal ganglion cells. Visual Neuroscience 4, 75–93.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1965). Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Research 5, 583–601.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Stone, J. (1965 a). Response of cat retinal ganglion cells to moving visual patterns. Journal of Neurophysiology 28, 819–832.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Stone, J. (1965 b). Analysis of receptive fields of cat retinal ganglion cells. Journal of Neurophysiology 28, 833–849.CrossRefGoogle ScholarPubMed
Roufs, J.A.J. (1972). Dynamic properties of vision. — I. Experimental relation between flicker and flash thresholds. Vision Research 12, 261–278.CrossRefGoogle Scholar
Rovamo, J., Luntinen, O. & Näsänen, R. (1993). Modelling the dependence of contrast sensitivity on grating area and spatial frequency. Vision Research 33, 2773–2788.CrossRefGoogle ScholarPubMed
Rovamo, J., Mustonen, J. & Näsänen, R. (1994). Modelling contrast sensitivity as a function of retinal illuminance and grating area. Vision Research 34, 1301–1314.CrossRefGoogle ScholarPubMed
Rovamo, J., Raninen, A., Lukkarinen, S. & Donner, K. (1995). Flicker sensitivity as a function of the spectral density of external white temporal noise. Vision Research (in press).Google Scholar
Schnapf, J.L., Nunn, B.J., Meister, M. & Baylor, D.A. (1990). Visual transduction in cones of the monkey Macaco fascicularis. Journal of Physiology 427, 681–713.CrossRefGoogle Scholar
Schneeweis, D.M. & Schnapf, J.L. (1995). Photovoltage of rods and cones in the macaque retina. Science 268, 1053–1056.CrossRefGoogle ScholarPubMed
Shapley, R., Kaplan, E. & Purpura, K. (1993). Contrast sensitivity and light adaptation in photoreceptors or in the retinal network. In Contrast Sensitivity, ed. Shapley, R. & Lam, D.M., pp. 103–116. Cambridge, Massachusetts: The MIT Press.Google Scholar
Tamura, T., Nakatani, K. & Yau, K.-W. (1989). Light adaptation in cat retinal rods. Science 245, 755–758.CrossRefGoogle ScholarPubMed
Tamura, T., Nakatani, K. & Yau, K.-W. (1991). Calcium feedback and sensitivity regulation in primate rods. Journal of General Physiology 98, 95–130.CrossRefGoogle ScholarPubMed
Troy, J.B. (1993). Modeling the receptive fields of mammalian retinal ganglion cells. In Contrast Sensitivity, ed. Shapley, R. & Lam, D.M., pp. 85–102. Cambridge, Massachusetts: The MIT Press.Google Scholar
Troy, J.B., Oh, J.K. & Enroth-Cugell, C. (1993). Effect of ambient illumination on the spatial properties of the center and surround of Y-cell receptive fields. Visual Neuroscience 10, 753–764.CrossRefGoogle Scholar
Victor, J.D. (1987). The dynamics of the cat retinal X cell centre. Journal of Physiology 386, 219–246.CrossRefGoogle ScholarPubMed
Wässle, H. & Creutzfeldt, O.D. (1973). Spatial resolution in visual system: A theoretical and experimental study on single units in the cat's lateral geniculate body. Journal of Neurophysiology 36, 13–27.CrossRefGoogle Scholar
Wässle, H., Peichl, L. & Boycott, B.B. (1981). Dendritic territories of cat ganglion cells. Nature 292, 344–345.CrossRefGoogle Scholar
Watson, A.B. (1986). Temporal sensitivity. In: Handbook of perception and human performance, ed. Boff, K.R., Kaufman, L. & Thomas, J.P., pp. 6.1–6.43. New York: John Wiley and Sons.Google Scholar
Werblin, F.S. & Copenhagen, D.R. (1974). Control of retinal sensitivity. III. Lateral interactions at the inner plexiform layer. Journal of General Physiology 63, 88–110.CrossRefGoogle Scholar
Winters, R.W. & Hamasaki, D.J. (1976). Temporal interactions of peripheral inhibition of sustained and transient ganglion cells in catretina. Vision Research 16, 37–45.CrossRefGoogle Scholar
Yau, K.-W. (1994). Phototransduction mechanism in retinal rods and cones. Investigative Ophthalmology and Visual Science 35, 9–32.Google ScholarPubMed