Hostname: page-component-745bb68f8f-kw2vx Total loading time: 0 Render date: 2025-01-11T22:53:53.389Z Has data issue: false hasContentIssue false
  • English
  • Français

The receptive field of the primate P retinal ganglion cell, II: Nonlinear dynamics

Published online by Cambridge University Press:  02 June 2009

Ethan A. Benardete  and
Ehud Kaplan
Ethan A. Benardete
Affiliation:
The Rockefeller University, New York
Ehud Kaplan
Affiliation:
The Rockefeller University, New York
Get access Rights & Permissions [Opens in a new window]

Abstract

The receptive-field properties of retinal ganglion cells (RGCs) provide information about early visual processing. In the primate retina, P cells form the largest class of RGCs (Rodieck, 1988). A detailed exploration of the dynamics of the two subdivisions of the P-cell receptive field—the center and the surround—was undertaken. In the preceding paper (Benardete & Kaplan, 1996), the first-order responses of the center and the surround of P cells were described, which were obtained with a new technique, the multiple m-sequence stimulus (Benardete & Victor, 1994). In this paper, the investigation of P-cell responses measured as S-potentials in the lateral geniculate nucleus (LGN) is continued, and significant nonlinear, second-order responses from the center and the surround are described. These responses are quantified by fitting a mathematical model, the linear-nonlinear-linear (LNL) model (Korenberg, 1973; Korenberg & Hunter, 1986; Victor, 1988) to the data. In a second series of experiments, demonstration that steady illumination of the surround modifies the gain of the center to contrast signals (see also Kaplan & Shapley, 1989) is made. In P ON cells, increasing the steady illumination of the surround decreases the gain and speeds up the center's first-order response. In P OFF cells, increasing the steady illumination of the surround increases the gain of the center while speeding up the response. The results of both sets of experiments are related to the known anatomy and physiology of the P cell.

Keywords

P cellReceptive fieldNonlinear dynamicsCenter, Surround
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 1 , January 1997 , pp. 187 - 205
Copyright
Copyright © Cambridge University Press 1997

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

Benardete, E.A., Kaplan, E. & Knight, B.W. (1992 a). Contrast gain control in the primate retina: P cells are not X-like, some M cells are. Visual Neuroscience 8, 483–486.CrossRefGoogle ScholarPubMed
Benardete, E.A., Victor, J.D. & Kaplan, E. (1992 b). Temporal properties of primate P retinal ganglion cells investigated with a new discrete multi-level stimulus. Investigative Ophthalmology & Visual Science (Suppl.) 33(4), 1410(#3591).Google Scholar
Benardete, E.A. (1994). Functional dynamics of primate retinal ganglion cells. Ph.D. thesis, The Rockefeller University, New York. New York.Google Scholar
Benardete, E.A. & Victor, J.D. (1994). An extension of the m-sequence technique for the analysis of multiple-input nonlinear systems. In: Advanced Methods of Physiological Systems Modelling. Vol. 3. ed. Marmarelis, V.Z., pp. 87–110. New York: Plenum Press.CrossRefGoogle Scholar
Benardete, E.A. & Kaplan, E. (1996). The receptive field of the primate P retinal ganglion cell I, Linear dynamics. Visual Neuroscience 14, 169–185.CrossRefGoogle Scholar
Berninger, T.A. & Arden, G.B. (1988). The pattern electroretinogram. Eye 2, S257–S283.CrossRefGoogle ScholarPubMed
Bishop, P.O., Burke, W. & Davis, R. (1958). Synapse discharge by single fibre in mammalian visual system. Nature 182, 728–730.CrossRefGoogle ScholarPubMed
Boycott, B.B., Hopkins, J.M. & Sperling, H.G. (1987). Cone connections of the horizontal cells of the rhesus monkey's retina. Proceedings of the Royal Society B (London) 229, 345–379.Google ScholarPubMed
Burkhardt, D.A. (1974). Sensitization and centre-surround antagonism in Necturus retina. Journal of Physiology (London) 236, 593–610.CrossRefGoogle ScholarPubMed
Calkins, D.J. (1994). Microcircuitry of M and L cone midget ganglion cell pathways in the primate fovea. Ph.D. thesis. University of Pennsylvania.Google Scholar
Croner, L.J., Purpura, K. & Kaplan, E. (1993). Response variability in retinal ganglion cells of primates. Proceedings of the National Academy of Sciences of the U.S.A. 90, 8128–8130.CrossRefGoogle ScholarPubMed
Dacey, D.M., Lee, B.B., Stafford, D.K., Pokorny, J. & Smith, V.C. (1996). Horizontal cells of the primate retina: Cone specificity without spectral opponency. Science 271, 656–659.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Raviola, E. (1990). Physiology of H1 horizontal cells in the primate retina. Proceedings of the Royal Society B (London) 239, 213–230.Google Scholar
De Lange, H. (1958). Research into the dynamic nature of the human fovea-cortex systems with intermittent and modulated light. II. Phase shift in brightness and delay in color perception. Journal of the Optical Society of America 48, 784–789.CrossRefGoogle Scholar
De Monasterio, F.M. & Gouras, P. (1975). Functional properties of ganglion cells of the rhesus monkey retina. Journal of Physiology (London) 251, 167–195.CrossRefGoogle ScholarPubMed
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology (London) 357, 219–240.CrossRefGoogle ScholarPubMed
Derrington, A.M., Krauskopf, J. & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. Journal of Physiology (London) 357, 241–265.CrossRefGoogle ScholarPubMed
Dodge, F.A., Knight, B.W. & Toyoda, J. (1968). Voltage noise in Limulus visual cells. Science 160, 88–90.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology (London) 187, 517–552.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C., Hertz, B.C. & Lennie, P. (1974). Convergence of rod and cone signals on retinal ganglion cells of the cat. Journal of Physiology (London) 242, 126P–127P.Google ScholarPubMed
Gielen, C.C.A.M., van Gisbergen, J.A.M. & Vendrik, A.J.H. (1982). Reconstruction of cone-system contributions to responses of colour-opponent neurones in monkey lateral geniculate. Biological Cybernetics 44, 211–221.CrossRefGoogle ScholarPubMed
Golomb, S.W. (1968). Shift Register Sequences. San Francisco, Holden-Day, Inc.Google Scholar
Ingling, C.R. & Martinez-Uriegas, E. (1983). The relationship between spectral sensitivity and spatial sensitivity for the primate r-g X channel. Vision Research 23, 1495–1500.CrossRefGoogle ScholarPubMed
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, 2755–2757.CrossRefGoogle ScholarPubMed
Kaplan, E. & Shapley, R.M. (1989). Illumination of the receptive field surround controls the contrast gain of macaque P retinal ganglion cells. Society of Neuroscience Abstracts 15(1), 174(#75.1).Google Scholar
Kaplan, E., Lee, B.B. & Shapley, R.M. (1990). New views of primate retinal function. In: Progress in Retinal Research Vol. 9. ed. Osborne, N.N. & Chader, G.J., pp. 273–336. New York: Pergamon Press.Google Scholar
Kelly, D.H. (1972). Adaptation effects on spatio-temporal sine-wave thresholds. Vision Research 12, 89–101.CrossRefGoogle ScholarPubMed
Koch, C. & Poggio, T. (1992). Multiplying with synapses and neurons. In: Single Neuron Computation ed. Mckenna, T., Davis, J. & Zornetzer, S.F. London: Academic Press.Google Scholar
Kolb, H. & Dekorver, L. (1991). Midget ganglion cells of the parafovea of the human retina: A study by electron microscopy and serial section reconstructions. Journal of Comparative Neurology 303, 617–636.CrossRefGoogle ScholarPubMed
Korenberg, M.J. (1973). Cross-correlation analysis of neural cascades. In: Proceedings of the 10th Annual Rocky Mountain Bioengineering Symposium, pp. 47–51. New York: IEEE.Google Scholar
Korenberg, M.J. & Hunter, I.W. (1986). The identification of nonlinear biological systems: LNL cascade models. Biological Cybernetics 55, 125–134.CrossRefGoogle ScholarPubMed
Marmarelis, P.Z. & Marmarelis, V.Z. (1978). Analysis of Physiological Systems: The White Noise Approach. New York: Plenum Press.CrossRefGoogle Scholar
Merrill, E.G. & Ainsworth, A. (1972). Glass-coated platinum-plated tungsten microelectrodes. Medical and Biological Engineering 10, 662–672.CrossRefGoogle ScholarPubMed
Milkman, N., Schick, G., Rossetto, M., Ratliff, F., Shapley, R. & Victor, J. (1980). A two-dimensional computer-controlled visual stimulator. Behavior Research Methods & Instrumentation 12, 283–292.CrossRefGoogle Scholar
Mullen, K.T. & Kingdom, F.A.A. (1991). Colour contrast in form perception. In: Vision and Visual Dysfunction (The Perception of Colour) Vol. 6. ed. Gouras, P., pp. 198–217. New York: Macmillan Press.Google Scholar
Naka, K.-I., Chappell, R.L., Sakuranaga, M. & Ripps, H. (1988). Dynamics of skate horizontal cells. Journal of General Physiology 92, 811–831.CrossRefGoogle ScholarPubMed
Press, W.H., Flannery, B.P., Teukolsky, S.A. & Vetterling, W.T. (1989). Numerical Recipes in Pascal, The Art of Scientific Computing. Cambridge: Cambridge University Press.Google Scholar
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
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
Ream, N. (1970). Nonlinear identification using inverse-repeat m-sequences. Proceedings of IEEE 117, 213–218.Google Scholar
Reichardt, W.E. & Poggio, T. (1981). Linear and nonlinear systems. In: Theoretical Approaches in Neurobiology, ed. Reichardt, W.E. & Poggio, T., pp. 185–187. Cambridge, MA: The MIT Press.Google Scholar
Rodieck, R.W. (1988). The primate retina. In: Comparative Primate Biology, Vol. 4, Neurosciences, ed. Steklis, H.D. & Erwin, J., pp. 203–278. New York: Alan R. Liss.Google Scholar
Sakai, H.M., Naka, K.-I. & Korenberg, M.J. (1988). White-noise analysis in visual neuroscience. Visual Neuroscience 1, 287–296.CrossRefGoogle ScholarPubMed
Shapley, R.M. & Victor, J.D. (1981). How the contrast gain control modifies the frequency responses of cat retinal ganglion cells. Journal of Physiology (London) 318, 161–179.CrossRefGoogle ScholarPubMed
Shapley, R., Kaplan, E., & Soodak, R. (1981). Spatial summation and contrast sensitivity of X and Y cells in the lateral geniculate nucleus of the macaque. Nature 292, 543–545.CrossRefGoogle ScholarPubMed
Shapley, R. & Enroth-Cugell, C. (1984). Visual adaptation and retinal gain controls. In: Progress in Retinal Research, Vol. 3. ed. Osborne, N.N. & Chader, G.J., pp. 263–346. New York: Pergamon Press.Google Scholar
Shapley, R. & Kaplan, E. (1990). Tonic suppressive interactions between center and surround in P ganglion cells and parvocellular neurons. Investigative Ophthalmology and Visual Science (Suppl.) 31(4), 88(#434).Google Scholar
Sutter, E.E. (1992). A deterministic approach to nonlinear systems analysis. In: Nonlinear Vision, Determination of Neural Receptive Fields, Function, and Networks, ed. Pinter, R.B. & Nabet, B., pp. 171–220. Boca Raton, FL: CRC Press.Google Scholar
Valberg, A., Lee, B.B. & Tigwell, D.A. (1985). A simultaneous contrast effect of steady remote surrounds on responses of cell in the macaque lateral geniculate nucleus. Experimental Brain Research 58, 604–608.CrossRefGoogle ScholarPubMed
Victor, J.D. (1987). The dynamics of the cat retinal X cell centre. Journal of Physiology (London) 386, 219–246.CrossRefGoogle ScholarPubMed
Victor, J.D. (1988). The dynamics of the cat retinal Y cell subunit. Journal of Physiology (London) 405, 289–320.CrossRefGoogle ScholarPubMed
Victor, J.D. & Knight, B.W. (1979). Nonlinear analysis with an arbitrary stimulus ensemble. Quarterly of Applied Mathematics 37, 113–136.CrossRefGoogle Scholar
Volterra, V. (1932). The Theory of Functionals and of Integrals and Integra-Differential Equations. London: Blackie.Google Scholar
Werblin, F.S. (1974). Control of retinal sensitivity. II. Lateral interactions at the outer plexiform layer. Journal of General Physiology 63, 62–87.CrossRefGoogle Scholar
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. Journal of Neurophysiology 32, 339–355.CrossRefGoogle ScholarPubMed
Westheimer, G. (1965). Spatial interaction in the human retina during scotopic vision. Journal of Physiology (London) 181, 881–894.CrossRefGoogle ScholarPubMed
Wiener, N. (1958). Nonlinear Problems in Random Theory. New York: John Wiley & Sons, Inc.Google Scholar
Wiesel, T.N. & Hubel, D.H. (1966). Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. Journal of Neurophysiology 29, 1115–1156.CrossRefGoogle ScholarPubMed