The receptive field of the primate P retinal ganglion cell, I: Linear dynamics

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.

[1]  B. B. Lee,et al.  Temporal response of ganglion cells of the macaque retina to cone-specific modulation. , 1995, Journal of the Optical Society of America. A, Optics, image science, and vision.

[2]  Joel Pokorny,et al.  Responses to pulses and sinusoids in macaque ganglion cells , 1994, Vision Research.

[3]  David J. Calkins,et al.  M and L cones in macaque fovea connect to midget ganglion cells by different numbers of excitatory synapses , 1994, Nature.

[4]  Jonathan D. Victor,et al.  AN EXTENSION OF THE M-SEQUENCE TECHNIQUE FOR THE ANALYSIS OF MULTI-INPUT NONLINEAR SYSTEMS , 1994 .

[5]  E. Benardete,et al.  Functional Dynamics of Primate Retinal Ganglion Cells , 1994 .

[6]  B. B. Lee,et al.  Physiological mechanisms underlying psychophysical sensitivity to combined luminance and chromatic modulation. , 1993, Journal of the Optical Society of America. A, Optics and image science.

[7]  J. Pokorny,et al.  Responses of macaque ganglion cells to the relative phase of heterochromatically modulated lights. , 1992, The Journal of physiology.

[8]  C W Tyler,et al.  Analysis of visual modulation sensitivity. V. Faster visual response for G- than for R-cone pathway? , 1992, Journal of the Optical Society of America. A, Optics and image science.

[9]  B. Knight,et al.  Contrast gain control in the primate retina: P cells are not X-like, some M cells are , 1992, Visual Neuroscience.

[10]  R. Shapley,et al.  Spatial structure of cone inputs to receptive fields in primate lateral geniculate nucleus , 1992, Nature.

[11]  Ee Sutter,et al.  A deterministic approach to nonlinear systems analysis , 1992 .

[12]  Erich E. Sutter,et al.  The Fast m-Transform: A Fast Computation of Cross-Correlations with Binary m-Sequences , 1991, SIAM J. Comput..

[13]  J. Pokorny,et al.  Luminance and chromatic modulation sensitivity of macaque ganglion cells and human observers. , 1990, Journal of the Optical Society of America. A, Optics and image science.

[14]  Nikos K Logothetis,et al.  The color-opponent and broad-band channels of the primate visual system , 1990, Trends in Neurosciences.

[15]  A. L. Humphrey,et al.  Spatial and temporal response properties of lagged and nonlagged cells in cat lateral geniculate nucleus. , 1990, Journal of neurophysiology.

[16]  R. Kingslake Book-Review - Numerical Recipes in Pascal - the Art of Scientific Computing , 1990 .

[17]  S. Sherman,et al.  Brainstem control of response modes in neurons of the cat's lateral geniculate nucleus. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Barry B. Lee,et al.  Chapter 7 New views of primate retinal function , 1990 .

[19]  J. Victor The dynamics of the cat retinal X cell centre. , 1987, The Journal of physiology.

[20]  C. Enroth-Cugell,et al.  Spatiotemporal frequency responses of cat retinal ganglion cells , 1987, The Journal of general physiology.

[21]  D N Mastronarde,et al.  Two classes of single-input X-cells in cat lateral geniculate nucleus. I. Receptive-field properties and classification of cells. , 1987, Journal of neurophysiology.

[22]  J. M. Hopkins,et al.  Cone connections of the horizontal cells of the rhesus monkey’s retina , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[23]  R. Shapley,et al.  The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[24]  R. Shapley,et al.  The receptive field organization of X-cells in the cat: Spatiotemporal coupling and asymmetry , 1984, Vision Research.

[25]  P. Lennie,et al.  Chromatic mechanisms in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[26]  P. Lennie,et al.  Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[27]  C. R. Ingling,et al.  The relationship between spectral sensitivity and spatial sensitivity for the primate r-g X-channel , 1983, Vision Research.

[28]  C. Enroth-Cugell,et al.  Spatio‐temporal interactions in cat retinal ganglion cells showing linear spatial summation. , 1983, The Journal of physiology.

[29]  P. Lennie,et al.  The influence of temporal frequency and adaptation level on receptive field organization of retinal ganglion cells in cat , 1982, The Journal of physiology.

[30]  R. Shapley,et al.  X and Y cells in the lateral geniculate nucleus of macaque monkeys. , 1982, The Journal of physiology.

[31]  J D Victor,et al.  How the contrast gain control modifies the frequency responses of cat retinal ganglion cells. , 1981, The Journal of physiology.

[32]  Jonathan D. Victor,et al.  A two-dimensional computer-controlled visual stimulator , 1980 .

[33]  E Kaplan,et al.  Effects of dark adaptation on spatial and temporal properties of receptive fields in cat lateral geniculate nucleus. , 1979, The Journal of physiology.

[34]  P Gouras,et al.  Enchancement of luminance flicker by color-opponent mechanisms. , 1979, Science.

[35]  D. Hamasaki,et al.  Temporal characteristics of peripheral inhibition of sustained and transient ganglion cells in cat retina , 1976, Vision Research.

[36]  Murat Kunt On Computation of the Hadamard Transform and the R Transform in Ordered Form , 1975, IEEE Transactions on Computers.

[37]  P. Gouras,et al.  Functional properties of ganglion cells of the rhesus monkey retina. , 1975, The Journal of physiology.

[38]  P Lennie,et al.  The control of retinal ganglion cell discharge by receptive field surrounds. , 1975, The Journal of physiology.

[39]  O. Estévez,et al.  A spectral compensation method for determining the flicker characteristics of the human colour mechanisms. , 1974, Vision research.

[40]  R. L. de Valois,et al.  Psychophysical studies of monkey vision. 3. Spatial luminance contrast sensitivity tests of macaque and human observers. , 1974, Vision research.

[41]  R. L. Valois,et al.  Psychophysical studies of monkey vision. I. Macaque luminosity and color vision tests. , 1974, Vision research.

[42]  H K Hartline,et al.  Enhancement of Flicker by Lateral Inhibition , 1967, Science.

[43]  D. Hubel,et al.  Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. , 1966, Journal of neurophysiology.

[44]  R. L. Valois,et al.  Analysis of response patterns of LGN cells. , 1966, Journal of the Optical Society of America.

[45]  P. O. BISHOP,et al.  Synapse Discharge by Single Fibre in Mammalian Visual System , 1958, Nature.