Responses to pulses and sinusoids in macaque ganglion cells

The goal of the study was to compare pulse responses with sinusoidal temporal responsivity. The response of macaque ganglion cells was measured to brief luminance and chromatic pulses and to luminance or chromatic sinusoidal modulation. To make both positive and negative lobes of the pulse response visible, responses to pulses of opposite polarity were combined to yield a linearized pulse response. Tests of superposition were used to evaluate the linearized pulse response to different combinations of pulse duration and Weber contrast. A prediction of the pulse response was derived using sinusoidal responsivity functions and Fourier synthesis. For ganglion cells of the parvocellular (PC) pathway, shape and absolute amplitude of linearized pulse responses corresponded well to the predicted responses over a range of pulse durations at 0.5 and 1.0 Weber contrast for both luminance and chromatic modulation. For ganglion cells of the magnocellular (MC) pathway, shape and amplitude of the linearized pulse responses and the predicted responses corresponded when the contrast-duration product was low. This correspondence held for luminance modulation over a thousand-fold range of retinal illuminance. For contrast-duration combinations that produced a more vigorous response, over 100 imp/sec, the linearized pulse responses of MC-pathway cells became larger and time-advanced relative to the linear prediction until saturation became apparent. Incorporation of high Michelson contrast responses in the Fourier synthesis captured the timing but not the amplitude of the linearized pulse response. The data suggest that a mechanism similar to a contrast gain control acts upon MC- but not PC-pathway-cells. The data confirm that use of linear modelling to describe temporal behaviour of retinal ganglion cells is appropriate for small signals.

[1]  L Matin,et al.  Critical duration, the differential luminance threshold, critical flicker frequency, and visual adaptation: a theoretical treatment. , 1968, Journal of the Optical Society of America.

[2]  J. Roufs Dynamic properties of vision. I. Experimental relationships between flicker and flash thresholds. , 1972, Vision research.

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

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

[5]  R A Smith,et al.  Adaptation of visual contrast sensitivity to specific temporal frequencies. , 1970, Vision research.

[6]  G Westheimer,et al.  The Maxwellian view. , 1966, Vision research.

[7]  K. Uchikawa,et al.  Temporal integration of chromatic double pulses for detection of equal-luminance wavelength changes. , 1986, Journal of the Optical Society of America. A, Optics and image science.

[8]  J. Roufs Dynamic properties of vision. IV. Thresholds of decremental flashes, incremental flashes and doublets in relation to flicker fusion. , 1974, Vision research.

[9]  Robert Sekuler,et al.  Handbook of Sensory Physiology, Vol. 7/4, Visual Psychophysics , 1973 .

[10]  W. Levick,et al.  Responses of cat retinal ganglion cells to brief flashes of light , 1970, The Journal of physiology.

[11]  B. B. Lee,et al.  Steady discharges of macaque retinal ganglion cells , 1991, Visual Neuroscience.

[12]  B. B. Lee,et al.  An account of responses of spectrally opponent neurons in macaque lateral geniculate nucleus to successive contrast , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[13]  J. Roufs,et al.  Dynamic properties of vision. II. Theoretical relationships between flicker and flash thresholds. , 1972, Vision research.

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

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

[16]  A Pantle,et al.  Flicker adaptation. I. Effect on visual sensitivity to temporal fluctuations of light intensity. , 1971, Vision research.

[17]  C W Tyler,et al.  Psychophysical derivation of the impulse response through generation of ultrabrief responses: complex inverse estimation without minimum-phase assumptions. , 1992, Journal of the Optical Society of America. A, Optics and image science.

[18]  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.

[19]  C. A. Burbeck,et al.  Spatiotemporal characteristics of visual mechanisms: excitatory-inhibitory model. , 1980, Journal of the Optical Society of America.

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

[21]  B. B. Lee,et al.  Light adaptation in cells of macaque lateral geniculate nucleus and its relation to human light adaptation. , 1983, Journal of neurophysiology.

[22]  D. Stork,et al.  Temporal impulse responses from flicker sensitivities. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[23]  J. Pokorny,et al.  Threshold temporal integration of chromatic stimuli , 1984, Vision Research.

[24]  S. Anstis,et al.  Intensity versus adaptation and the Pulfrich stereophenomenon. , 1972, Vision research.

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

[26]  J. Victor Temporal impulse responses from flicker sensitivities: causality, linearity, and amplitude data do not determine phase. , 1989, Journal of the Optical Society of America. A, Optics and image science.

[27]  R. Shapley,et al.  Light adaptation in the primate retina: Analysis of changes in gain and dynamics of monkey retinal ganglion cells , 1990, Visual Neuroscience.

[28]  J. Pokorny,et al.  Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm , 1975, Vision Research.

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

[30]  Joel Pokorny,et al.  Responses of macaque ganglion cells and human observers to compound periodic waveforms , 1993, Vision Research.

[31]  C. Enroth-Cugell,et al.  Chapter 9 Visual adaptation and retinal gain controls , 1984 .

[32]  V C Smith,et al.  Temporal modulation sensitivity and pulse-detection thresholds for chromatic and luminance perturbations. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[33]  Bb Lee,et al.  Nonlinear summation of M- and L-cone inputs to phasic retinal ganglion cells of the macaque , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  B. B. Lee,et al.  Sensitivity of macaque retinal ganglion cells to chromatic and luminance flicker. , 1989, The Journal of physiology.

[35]  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.

[36]  W. Levick,et al.  On the apparent orbit of the Pulfrich pendulum. , 1972, Vision research.