The dynamics of the cat retinal X cell centre.

1. The dynamics of the centre mechanism of individual cat X retinal ganglion cells is investigated. The visual stimuli consist of temporal contrast modulation of stationary patterns. In order to study the response of the centre mechanism, patterns were either sine gratings of high spatial frequency or small circular spots positioned over the receptive‐field centre. 2. Responses to contrast reversal are approximately linear. However, as the modulation depth of the stimulus increases, responses become more transient. Ganglion cell responses show this phenomenon at moderate contrasts (e.g. 0.1), which do not elicit discharges that approach the maximum firing rate of the ganglion cell. 3. A sequence of dynamical models are constructed from responses elicited by sum‐of‐sinusoids modulation of the spatial pattern. The first model is strictly linear. It consists of a series of low‐pass filters and a single high‐pass filter. The linear model predicts the approximate shape of the step response, but does not account for the change in shape of the response as a function of modulation depth. 4. The second model, a quasi‐linear model, allows the 'linear' dynamics to vary slowly with a neural measure of contrast. The main effect of high contrast is a shorter time constant in the high‐pass filter. This model accounts qualitatively for the increased transience of the response, but fails to predict the magnitude of the effect at higher modulation depths. 5. In the third model, the transfer characteristics of the centre response adjust rapidly as contrast changes. This intrinsically non‐linear model provides excellent agreement with observed response to steps and more complex modulation patterns. 6. The non‐linearity necessitated by a voltage‐to‐spikes transduction is analysed quantitatively. In most ganglion cells, a simple truncation at 0 impulses/s (and no saturation) explains the changes in apparent gain and mean firing rate that occur as modulation depth is increased. A non‐linear voltage‐to‐spike transduction per se cannot account for the observed effect of contrast on dynamics. 7. The parameters of the dynamical model are measured for a population of twenty‐seven X ganglion cells (nineteen on‐centre and eight off‐centre). The low‐pass stage and the strength of the high‐pass stage are relatively uniform across the population. The over‐all gain and the dynamics of the high‐pass stage vary substantially across the population, but show no consistent dependence on the on‐off distinction or on retinal location. Some implications of this variability for retinal function are discussed.

[1]  R. W. Rodieck Quantitative analysis of cat retinal ganglion cell response to visual stimuli. , 1965, Vision research.

[2]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

[3]  P. O. Bishop,et al.  Residual eye movements in receptive-field studies of paralyzed cats. , 1967, Vision research.

[4]  L Maffei,et al.  Transfer characteristics of excitation and inhibition in cat retinal ganglion cells. , 1970, Journal of neurophysiology.

[5]  W. Levick,et al.  Sustained and transient neurones in the cat's retina and lateral geniculate nucleus , 1971, The Journal of physiology.

[6]  W. Levick,et al.  Properties of sustained and transient ganglion cells in the cat retina , 1973, The Journal of physiology.

[7]  B. Boycott,et al.  The morphological types of ganglion cells of the domestic cat's retina , 1974, The Journal of physiology.

[8]  J. Stone,et al.  Properties of cat retinal ganglion cells: a comparison of W-cells with X- and Y-cells. , 1974, Journal of neurophysiology.

[9]  A. Hodgkin,et al.  Changes in time scale and sensitivity in turtle photoreceptors , 1974, The Journal of physiology.

[10]  J Toyoda,et al.  Frequency Characteristics of Retinal Neurons in the Carp , 1974, The Journal of general physiology.

[11]  D. Copenhagen,et al.  Control of Retinal Sensitivity II. Lateral Interactions at the Outer Plexiform Layer , 1974 .

[12]  R. Shapley,et al.  Quantitative analysis of retinal ganglion cell classifications. , 1976, The Journal of physiology.

[13]  R. Shapley,et al.  The effect of contrast on the transfer properties of cat retinal ganglion cells. , 1978, The Journal of physiology.

[14]  J. Movshon,et al.  Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex. , 1978, The Journal of physiology.

[15]  F. Ratliff,et al.  The response of the Limulus retina to moving stimuli: a prediction by Fourier synthesis , 1978, The Journal of general physiology.

[16]  R. Shapley,et al.  The nonlinear pathway of Y ganglion cells in the cat retina , 1979, The Journal of general physiology.

[17]  B. Cleland,et al.  Visual resolution and receptive field size: examination of two kinds of cat retinal ganglion cell. , 1979, Science.

[18]  B. Knight,et al.  Nonlinear analysis with an arbitrary stimulus ensemble , 1979 .

[19]  R. Shapley,et al.  Nonlinear spatial summation and the contrast gain control of cat retinal ganglion cells. , 1979, The Journal of physiology.

[20]  J. Bergen,et al.  A four mechanism model for threshold spatial vision , 1979, Vision Research.

[21]  R. Shapley,et al.  A method of nonlinear analysis in the frequency domain. , 1980, Biophysical journal.

[22]  R. Shapley,et al.  The effect of contrast on the non‐linear response of the Y cell. , 1980, The Journal of physiology.

[23]  P. Lennie Parallel visual pathways: A review , 1980, Vision Research.

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

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

[26]  O. Grüsser,et al.  Frequency transfer properties of cat retina horizontal cells , 1981, Vision Research.

[27]  W. Levick,et al.  Analysis of orientation bias in cat retina , 1982, The Journal of physiology.

[28]  Edward H. Adelson,et al.  Saturation and adaptation in the rod system , 1982, Vision Research.

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

[30]  D. Tranchina,et al.  Retinal light adaptation—evidence for a feedback mechanism , 1984, Nature.

[31]  Scott J. Daly,et al.  Temporal information processing in cones: Effects of light adaptation on temporal summation and modulation , 1985, Vision Research.

[32]  K Naka,et al.  Signal transmission in the catfish retina. I. Transmission in the outer retina. , 1985, Journal of neurophysiology.

[33]  R. Shapley,et al.  Hyperacuity in cat retinal ganglion cells. , 1986, Science.

[34]  B. Efron The jackknife, the bootstrap, and other resampling plans , 1987 .