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Visual responses to stimulation at high temporal frequency are generally considered to result from signals that avoid light adaptive gain adjustment, simply reflecting linear summation of luminance. Under conditions of high photopic illuminance, the center of the receptive field of the cat X-cell has been shown to expand in size when stimulated at high temporal frequency, raising the possibility that there is spatiotemporal interaction in luminance summation. Here we show that this expansion maintains constant the product of the center's luminance summing area and the temporal period of luminance modulation, implying that spatial and temporal integration of luminance can be traded for one another by the X-cell center. As such the X-cell has a spatiotemporal window for luminance integration that fuses the classical concepts of a spatial window of luminance integration (Ricco's Law) with a temporal window of luminance integration (Bloch's Law). We were interested to determine whether this tradeoff between spatial and temporal summation of luminance occurs also at lower light levels, where the temporal-frequency bandwidth of the X-cell is narrower. We found that it does not. Center radius does not expand with temporal frequency under either low photopic or scotopic conditions. These results are discussed within the context of the known retinal circuitry that underlies the X-cell center for photopic and scotopic conditions.

It has been suggested for a number of years that ganglion cells inform the rest of the brain about contrast in the retinal image. The purpose of the work undertaken here was to demonstrate this fact explicitly. Extracellular recordings were made from X- and Y-cell axons of the optic tracts of anesthetized cats. Responses of these cells to gratings that were near optimal in spatial and temporal frequency were measured for a range of contrasts. For each cell, similar measurements were made at a number of light levels, spanning the photopic to high scotopic (inclusive) ranges. A monotonic relationship between response and contrast was found at all light levels studied, and the same relationship was retained to a good approximation across all light levels. A similar result was also found when nonoptimal spatial frequencies were used as stimuli. These results indicate strongly that X and Y cells inform the cat's brain about contrast in the retinal image. It was also observed that the mean discharge rate of X and Y cells did not change with light level, indicating that no information is relayed to the brain by these cells on the mean light level.

Spatiotemporal frequency responses were measured at different levels of light adaptation for cat X and Y retinal ganglion cells. Stationary sinusoidal luminance gratings whose contrast was modulated sinusoidally in time or drifting gratings were used as stimuli. Under photopic illumination, when the spatial frequency was held constant at or above its optimum value, an X cell's responsivity was essentially constant as the temporal frequency was changed from 1.5 to 30 Hz. At lower temporal frequencies, responsivity rolled off gradually, and at higher ones it rolled off rapidly. In contrast, when the spatial frequency was held constant at a low value, an X cell's responsivity increased continuously with temporal frequency from a very low value at 0.1 Hz to substantial values at temporal frequencies higher than 30 Hz, from which responsivity rolled off again. Thus, 0 cycles X deg-1 became the optimal spatial frequency above 30 Hz. For Y cells under photopic illumination, the spatiotemporal interaction was even more complex. When the spatial frequency was held constant at or above its optimal value, the temporal frequency range over which responsivity was constant was shorter than that of X cells. At lower spatial frequencies, this range was not appreciably different. As for X cells, 0 cycles X deg-1 was the optimal spatial frequency above 30 Hz. Temporal resolution (defined as the high temporal frequency at which responsivity had fallen to 10 impulses X s-1) for a uniform field was approximately 95 Hz for X cells and approximately 120 Hz for Y cells under photopic illumination. Temporal resolution was lower at lower adaptation levels. The results were interpreted in terms of a Gaussian center-surround model. For X cells, the surround and center strengths were nearly equal at low and moderate temporal frequencies, but the surround strength exceeded the center strength above 30 Hz. Thus, the response to a spatially uniform stimulus at high temporal frequencies was dominated by the surround. In addition, at temporal frequencies above 30 Hz, the center radius increased.

Cat retinal ganglion cells with center-surround receptive fields have an irregular discharge whose rate is altered by visual stimulation. In assessing the detectability of stimulus-induced changes in the discharge, a consideration of the power spectral density of the discharge is helpful. The power spectral density of Q, X, and Y cells is flat at low frequencies, rises to a peak at the mean frequency of firing, and then decays away at higher frequencies in an oscillatory manner to an asymptotic level equal to the mean rate of discharge. Measured spectra correspond closely with spectra predicted by a renewal-point process with gamma-distributed intervals. When the rate of the discharge is altered by visual stimulation, the spectral density at low frequencies remains roughly constant. Assuming that it is the noise power at these frequencies that is effective in limiting the detectability of visual stimuli, it appears that at the retinal level the irregularity of the discharge can be treated as an additive noise.

We examined the dependence of the center radius of X cells on temporal frequency and found that at temporal frequencies above 40 Hz the radius increases in a monotonic fashion, reaching a size approximately 30% larger at 70 Hz. This kind of spatial expansion has been predicted with cable models of receptive fields where inductive elements are included in modeling the neuronal membranes. Hence, the expansion of the center radius is clearly important for modeling X cell receptive fields. On the other hand, we feel that it might be of only minor functional significance, since the responsivity of X cells is attenuated at these high temporal frequencies and the signal-to-noise ratio is considerably worse than at low and midrange temporal frequencies.