J. Kremers

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.

Temporal response of ganglion cells of the macaque retina to cone-specific modulation

The temporal response of cone inputs to macaque retinal ganglion cells were compared with cone-specific sinusoidal modulation used to isolate each cone type. For all cell types of the parvocellular (PC) pathway, temporal responsivity was similar for short (S)-, middle (M)-, and long (L)-wavelength-sensitive cone inputs, apart from small latency differences between inputs to center and surround. The temporal response resembled that expected from receptor physiology. Responses of cells of the magnocellular pathway to M- or L-cone modulation showed more complex properties indicative of postreceptoral processing. Human psychophysical temporal-sensitivity functions were acquired with S-cone modulation under conditions similar to those for the physiological measurements. Ratios of psychophysical to physiological data from S-cone cells (the only cells that respond to this stimulus) yielded an estimate of the central filter acting upon PC-pathway signals. The filter characteristic could be described by a four-stage low-pass filter with corner frequency 3-5 Hz.

Rod inputs to macaque ganglion cells

The strength of rod inputs to ganglion cells was assessed in the macaque retina at retinal positions within 3-15 deg eccentricity. The experimental paradigm used temporally modulated heterochromatic lights whose relative phase was varied. This paradigm provided a sensitive test to detect rod input. In parvocellular (PC) pathway cells, the gain of the cone-driven signal decreased with decrease in luminance. At 2 td a weak rod response, of a few impulses per second for 100% rod modulation, was revealed in about 60% of cells. For blue-on cells, the cone-driven response also decreased with retinal illuminance, but no rod response could be found. In magnocellular (MC) pathway cells, rod input was much more apparent. Responses became rod dominated at and below 20 td; we cannot exclude rod intrusion at higher retinal illuminances. Responsivity was maintained even at low retinal illuminances. Temporal-frequency dependent rod-cone interactions were observed in MC-pathway cells. Rod responses were of longer latency than cone responses, but there was no evidence of any difference in rod latency between parvocellular and magnocellular pathways.

Responses of macaque ganglion cells and human observers to compound periodic waveforms

We measured responses of macaque retinal ganglion cells to different periodic waveforms (sinusoidal, square, rapid-on and rapid-off sawtooth waveforms) for both luminance and equiluminant chromatic modulation. We analyzed the responses with a peak-to-trough detector. At low frequencies, on-center and off-center magnocellular (MC-) pathway cells showed a ten-fold higher responsivity to the rapid-on and rapid-off sawtooth respectively. Red-on (+L-M) and green-on (+M-L) parvocellular (PC-) pathway cells showed a four-fold greater responsivity to rapid red-on and rapid green-on equiluminant chromatic sawtooth waveforms respectively. At an equivalent retinal eccentricity, we measured psychophysical thresholds for luminance stimuli and chromatic stimuli. We concluded that luminance sawtooth sensitivities from psychophysics are consistent with selective detection through MC-pathway on- and off-center channels in the visual system. The differences between the compound periodic waveforms seen in the PC-pathway cell data did not occur in the psychophysics. In a second analysis, cell responses to sinusoidal modulation were used to predict the linear response to square-wave and sawtooth waveforms. PC-pathway cells showed linear temporal behavior over a wide range of contrasts, but MC-pathway cells displayed linear behavior only for low-contrast luminance modulation. Using these linear fits, we implemented a model incorporating central low-pass filtering in the MC- and PC-pathways before the peak-to-trough detector. This model captured better the time scale and relative sensitivity to periodic waveforms found in the psychophysical data.

The time course of adaptation in macaque retinal ganglion cells

The time course of adaptation of cells of the parvocellular (PC) and magnocellular (MC) pathways has been characterized following changes in retinal illuminance or chromaticity. Adaptation state was cycled between high and low luminance levels or between backgrounds with wavelengths metameric to 630 and 570 nm. Cell responsivity was probed with brief bursts of luminance or chromatic modulation. After a change in luminance, adaptation of both MC-cells (tested with a luminance probe) and red-green PC-cells (tested with a chromatic probe) was relatively rapid and largely complete within 100 msec or less. After a change in chromaticity, recovery of responsivity in red-green PC-cells was dependent on cell type. Recovery of responsivity with backgrounds elevating maintained firing was complete within a few seconds, but with backgrounds suppressing cell firing, recovery took many tens of seconds. This very slow time course may be due to a threshold effect. In experiments with backgrounds which selectively adapted one cone type, use of cone-isolating probes indicated that the time course of PC-cell chromatic adaptation may be determined at a site after the subtraction of cone signals. Recovery of responsivity of MC-cells was also prolonged over several seconds following a chromatic change. Our data suggest that adaptation in macaque ganglion cells depends on mechanisms both before and after the site of cone interaction, and that these mechanisms may differ in time course between MC- and PC-cells. The results indicate that it may be important in psychophysical adaptation experiments to consider the presence of multiple postreceptoral mechanisms with different adaptation characteristics.

The spatial precision of macaque ganglion cell responses in relation to vernier acuity of human observers

Responses of parafoveal macaque ganglion cells were measured as a function of the contrast and position of an edge flashed within their receptive fields. The goal was to determine the ability of different cell types to signal edge location. For comparison, parafoveal vernier thresholds of human observers were measured with pairs of flashed edges. Cells of the magnocellular (MC-) pathway gave larger responses than cells of the parvocellular (PC-) pathway. Neurometric analyses comparing a cells response at different edge positions were performed. The positional signal from single MC-pathway cells was more precise than from PC-pathway cells, especially at lower contrasts. In a second analysis, based on the neurophysiological results, responses from a matrix of ganglion cells were generated. Using a simple model, vernier performance expected from such a matrix was predicted as a function of edge length and contrast. Again, the MC-pathway gave a more precise positional signal than the PC-pathway despite the latters numerical advantage. At contrasts of 20% and below, only the MC-pathway would appear capable of supporting vernier performance with our stimuli. At higher contrasts either the MC- or PC-pathway could provide an adequate signal.

The Response of Macaque Retinal Ganglion Cells to Complex Temporal Waveforms

The responses of retinal ganglion cells depend on the temporal characteristics of the visual stimulus, and on the way visual information is processed in the retina. A powerful mathematical tool in relating the in- and output of the retinal system is linear systems analysis. If a system is linear, its output to a sinusoidal input is again a sine wave with the same frequency, although amplitude and phase may be modified. The modulation transfer function (MTF), in which amplitudes and phases are given as function of sine wave frequency, completely determines the system’s properties. Thus, when the temporal MTF of a linear system is known, one can calculate the system’s response to every temporal stimulus. We discuss here how far the responses of macaque retinal ganglion cells to complex temporal waveform can be predicted from the cell’s temporal MTF. We further relate the cells’ responses to human detection thresholds for complex waveforms.

The response of macaque ganglion cells and human observers to heterochromatically modulated lights: the effect of stimulus size

Psychophysical sensitivity of human observers closely resembles responsivity of retinal ganglion cells of the magnocellular (MC-) pathway as a function of the relative phase of heterochromatically modulated lights. The MC-pathway phase effect is absent if the receptive field centre alone is stimulated. Here we confirm this physiological result, and show that the psychophysical phase shift is also abolished with small stimuli. The space constant of the psychophysical effect is consistent with a surround diameter for MC-pathway cells in the fovea of about 50 min arc, about 10 times estimated centre diameter. On changing retinal illuminance, the amplitude of the physiological and psychophysical phase shifts also changed in a parallel manner. These experiments support the hypothesis that the physiological origin of psychophysical phase shifts is in the MC-pathway, and indicate the spatial frequency (c. 2c/deg) below which the psychophysical phase shift should become apparent.