Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-10T17:43:50.024Z Has data issue: false hasContentIssue false
  • English
  • Français

The receptive field of the primate P retinal ganglion cell, I: Linear 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 ganglion cells of the primate retina include two major anatomical and functional classes: P cells which project to the four parvocellular layers of the lateral geniculate nucleus (LGN), and M cells which project to the two magnocellular layers. The characteristics of the P-cell receptive field are central to understanding early form and color vision processing (Kaplan et al., 1990; Schiller & Logothetis, 1990). In this and in the following paper, P-cell dynamics are systematically analyzed in terms of linear and nonlinear response properties. Stimuli that favor either the center or the surround of the receptive field were produced on a CRT and modulated with a broadband signal composed of multiple m-sequences (Benardete et al., 1992b; Benardete & Victor, 1994). The first-order responses were calculated and analyzed in this paper (part I). The findings are: (1) The first-order responses of the center and surround depend linearly on contrast. (2) The dynamics of the center and surround are well described by a bandpass filter model. The most significant difference between center and surround dynamics is a delay of approximately 8 ms in the surround response. (3) In the LGN, these responses are attenuated and delayed by an additional 1–5 ms. (4) The spatial transfer function of the P cell in response to drifting sine gratings at three temporal frequencies was measured. This independent method confirmed the delay between the (first-order) responses of the center and surround. This delay accounts for the dependence of the spatial transfer function on the frequency of stimulation.

Keywords

P cellReceptive fieldLinear dynamicsCenterSurround
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 1 , January 1997 , pp. 169 - 185
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 and Visual Science (Suppl.) 33, 1410.Google Scholar
Benardete, E. (1994). Functional dynamics of primate retinal ganglion cells. Ph.D. Dissertation, The Rockefeller University, 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
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
Calkins, D.J., Schein, S.J., Tsukamoto, Y. & Sterling, P. (1994). M and L cones in macaque fovea connect to midget ganglion cells by different numbers of excitatory synapses. Nature 371, 70–72.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 Monasterio, P.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. (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 (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
De Valois, R.L., Abramov, I. & Jacobs, G.H. (1966). Analysis of response patterns of LGN cells. Journal of the Optical Society of America 56, 966–977.CrossRefGoogle ScholarPubMed
De Valois, R.L., Morgan, H.C., Polson, M.C., Mead, W.R. & Hull, E.M. (1974 a). Psychophysical studies of monkey vision—I. Macaque luminosity and color vision tests. Vision Research 14, 53–67.CrossRefGoogle ScholarPubMed
De Valois, R.L., Morgan, H. & Snodderly, D.M. (1974 b). Psychophysical studies of monkey vision—III. Spatial luminance contrast sensitivity tests of macaque and human observers. Vision Research 14, 75–81.CrossRefGoogle Scholar
Elliot, D.F. & Rao, K.R. (1982). Fast Transforms: Algorithms, Analyses, Applications, pp. 313–317. New York: Academic Press, Inc.Google Scholar
Enroth-Cugell, C. & Lennie, P. (1975). The control of retinal ganglion cell discharge by receptive field surrounds. Journal of Physiology (London) 247, 551–578.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 Physiology (London) 341, 279–307.CrossRefGoogle ScholarPubMed
Estévez, O. & Spekreijse, H. (1974). A spectral compensation method for determining the flicker characteristics of the human colour mechanisms. Vision Research 14, 823–830.CrossRefGoogle ScholarPubMed
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
Gielen, C.C.A.M., van Gisbergen, J.A.M. & Vendrik, A.J.H. (1982). Reconstruction of cone-system contributions to responses of colouropponent neurones in monkey lateral geniculate. Biological Cybernetics 44, 211–221.CrossRefGoogle ScholarPubMed
Golomb, S.W. (1968). Shift Register Sequences. San Francisco, California: Holden-Day, Inc.Google Scholar
Gouras, P. & Zrenner, E. (1979). Enhancement of luminance flicker by color-opponent mechanisms. Science 205, 587–589.CrossRefGoogle Scholar
Hamer, R.D. & Tyler, C.W. (1992). Analysis of visual modulation sensitivity. V. Faster visual response for G- than for R-cone pathway? Journal of the Optical Society of America A 9, 1889–1904.CrossRefGoogle 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., Marcus, S. & So, Y.T. (1979). Effects of dark adaptation on spatial and temporal properties of receptive fields in cat lateral geniculate nucleus. Journal of Physiology (London) 294, 561–580.CrossRefGoogle ScholarPubMed
Kaplan, E. & Shapley, R.M. (1982). X and Y cells in the lateral geniculate nucleus of macaque monkeys. Journal of Physiology (London) 330, 125–143.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, 174.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
Kunt, M. (1975). On computation of the Hadamard transform and the R transform in ordered form. IEEE Transactions on Computing C-24, 1120–1121.CrossRefGoogle Scholar
Lee, B.B., Pokorny, J., Smith, V.C., Martin, P.R. & Valberg, A. (1990). Luminance and chromatic modulation sensitivity of macaque ganglion cells and human observers. Journal of Optical Society of America A 7, 2223–2236.CrossRefGoogle ScholarPubMed
Lee, B.B., Martin, P.R., Valberg, A. & Kremers, J. (1993). Physiological mechanisms underlying psychophysical sensitivity to combined luminance and chromatic modulation. Journal of the Optical Society of America A 10, 1403–12.CrossRefGoogle ScholarPubMed
Lee, B.B., Pokorny, J., Smith, V.C. & Kremers, J. (1994). Responses to pulses and sinusoids in macaque ganglion cells. Vision Research 34, 3081–3096.CrossRefGoogle ScholarPubMed
Mastronarde, D.N. (1987). Two classes of single-input X-cells in cat lateral geniculate nucleus. I. Receptive-field properties and classification of cells. Journal of Neurophysiology 57, 357–380.CrossRefGoogle ScholarPubMed
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 and 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
Nawy, S. AND Jahr, C.E. (1991). Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature 346, 269–271.CrossRefGoogle Scholar
Press, W.H., Flannery, B.P., Teukolsky, S.A. & Vetterling, W.T. (1989). Numerical Recipes in Pascal: The Art of Scientific Computing. Cambridge, Massachusetts: Cambridge University Press.Google Scholar
Ratliff, F., Knight, B.W., Toyoda, J.-I. & Hartline, H.K. (1967). Enhancement of flicker by lateral inhibition. Science 158, 392–393.CrossRefGoogle ScholarPubMed
Reid, R.C. & Shapley, R.M. (1992). Spatial structure of cone inputs to receptive fields in primate lateral geniculate nucleus. Nature 356, 716–718.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1988). The primate retina. In Comparative Primate Biology, 4, Neurosciences, ed. Horst, D. & Erwin, J., pp. 203–278, New York: Alan R. Liss.Google Scholar
Saul, A.B. & Humphrey, A.L. (1990). Spatial and temporal response properties of lagged and nonlagged cells in cat lateral geniculate nucleus. Journal of Neurophysiology 64, 206–224.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Logothetis, N.K. (1990). The color-opponent and broadband channels of the primate visual system. Trends in Neuroscience 13, 392–398.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
Smith, V.C., Lee, B.B., Pokorny, J., Martin, P.R. & Valberg, A. (1992). Responses of macaque ganglion cells to the relative phase of heterochromatically modulated lights. Journal of Physiology 458, 191–221.CrossRefGoogle Scholar
Sutter, E.E. (1991). The fast m-transform: A fast computation of crosscorrelations with binary m-sequences. SIAM Journal of Computing 20, 686–694.CrossRefGoogle 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, Florida: CRC Press.Google Scholar
Uhlrich, D.J., Tamamaki, N. & Sherman, S.M. (1990). Brainstem control of response modes in neurons of the cat's lateral geniculate nucleus. Proceedings of the National Academy of Sciences of the U.S.A. 87, 2560–2563.CrossRefGoogle ScholarPubMed
Victor, J.D. (1987). The dynamics of the cat retinal X cell centre. Journal of Physiology (London) 386, 219–246.CrossRefGoogle ScholarPubMed
Wiesel, T.N. & Hubel, D.H. (1966). Spatial and chromatic interactions in the lateral genicolate body of the rhesus monkey. Journal of Neurophysiology 29, 1115–1156CrossRefGoogle ScholarPubMed
Winters, R.W. & Hamasaki, D.I. (1976). Temporal characteristics of peripheral inhibition of sustained and transient ganglion cells in cat retina. Vision Research 16, 37–45.CrossRefGoogle ScholarPubMed
Yeh, T., Lee, B.B. & Kremers, J. (1995). Temporal response of ganglion cells of the macaque retina to cone-specific modulation. Journal of the Optical Society of America A 12, 456–64.CrossRefGoogle ScholarPubMed