The rat is a popular animal model for vision research, yet there is little quantitative information about the physiological properties of the cells that provide its brain with visual input, the retinal ganglion cells. It is not clear whether rats even possess the full complement of ganglion cell types found in other mammals. Since such information is important for evaluating rodent models of visual disease and elucidating the function of homologous and heterologous cells in different animals, we recorded from rat ganglion cells in vivo and systematically measured their spatial receptive field (RF) properties using spot, annulus, and grating patterns. Most of the recorded cells bore likeness to cat X and Y cells, exhibiting brisk responses, center-surround RFs, and linear or nonlinear spatial summation. The others resembled various types of mammalian W cell, including local-edge-detector cells, suppressed-by-contrast cells, and an unusual type with an ON–OFF surround. They generally exhibited sluggish responses, larger RFs, and lower responsiveness. The peak responsivity of brisk-nonlinear (Y-type) cells was around twice that of brisk-linear (X-type) cells and several fold that of sluggish cells. The RF size of brisk-linear and brisk-nonlinear cells was indistinguishable, with average center and surround diameters of 5.6 ± 1.3 and 26.4 ± 11.3 deg, respectively. In contrast, the center diameter of recorded sluggish cells averaged 12.8 ± 7.9 deg. The homogeneous RF size of rat brisk cells is unlike that of cat X and Y cells, and its implication regarding the putative roles of these two ganglion cell types in visual signaling is discussed.

We have used frequency-domain methods to characterize the spatial receptive-field structure of cat retinal W cells. For most ON- and OFF-center tonic and phasic W cells, measurements of responsivity to drifting gratings at various spatial frequencies could be adequately described by a difference-of-Gaussians (DOG) function, consistent with the presence of center and surround mechanisms that are approximately Gaussian in shape and whose signals are combined additively. Estimates of the responsivity of the center mechanisms of tonic and phasic W cells were similar, but both were significantly lower than the corresponding values for X or Y cells. The width of the center mechanisms of tonic W cells, phasic W cells, and Y cells did not differ significantly from each other, but all were significantly larger than the width of X-cell centers. Surround parameters did not vary significantly among the four groups of ganglion cells. Measurements of contrast gain in both tonic and phasic W cells gave values that were significantly lower than in X or Y cells.

Virtually all of the phasic W cells in our sample displayed evidence of spatial non-linearities in their receptive fields, in the form of either d.c. responses to drifting sine-wave gratings or second harmonic responses to counterphased gratings. The spatial resolution of the mechanism underlying these nonlinearities was typically higher than that of the center mechanism of these cells. Most tonic W cells exhibited linear spatial summation, although a subset gave strong second harmonic responses to counterphased gratings.

Spatial-responsivity measurements for most ON-OFF and directionally selective W cells were not adequately described by DOG functions. These cells did, however, show evidence of spatial nonlinearities similar to those seen in phasic W cells. Suppressed-by-contrast cells gave both modulated and unmodulated responses to drifting gratings which both appeared to involved rectification, but which differed from each other in both spatial resolution and contrast gain.

These data confirm earlier reports that the receptive fields of tonic and most ON- or OFF-center phasic W cells appear to include classical center and surround mechanisms. However, the receptive fields of some phasic cells, as well as ON-OFF and directionally selective W cells may have quite different structures. Our results also suggest that phasic, ON-OFF, directionally selective, suppressed-by-contrast, and a subset of tonic W cells may all receive nonlinear inputs with characteristics similar to those described in the receptive fields of retinal Y cells. If so, this has important implications for identifying and understanding the presynaptic circuitry of W cells, as well as the nature of their output to both telencephalic and midbrain visual targets.

Perhaps 35% of all of the ganglion cells of the cat do not have classical center-surround organized receptive fields. This paper describes, quantitatively, the responses of two such cell types to stimulation with sinusoidal luminance gratings, whose spatial frequency, mean luminance, contrast, and temporal frequency were varied independently. The patterns were well-focused on the retina of the anesthetized and paralyzed cat. In one type of cell, the maintained discharge was depressed or completely suppressed when a contrast pattern was imaged onto the receptive field (suppressed-by-contrast cell). In the other type of cell, the introduction of a pattern elicited a burst of spikes (impressed-by-contrast cell).

When stimulated with drifting gratings, the cell's mean rate of discharge was reduced (suppressed-by-contrast cell) or elevated (impressed-by-contrast cell) over a limited band of spatial frequencies. There was no significant modulated component of response. The reduction in mean rate of suppressed-by-contrast cells caused by drifting gratings had a monotonic dependence on contrast, a relatively low-pass temporal-frequency characteristic and was greater under photopic than mesopic illuminance. If gratings of spatial frequency, that when drifted evoked a response from these cells, were instead held stationary and contrast-reversed, the mean rate of a suppressed-by-contrast cell was also reduced and that of an impressed-by-contrast cell increased. But, for contrast-reversed gratings, the discharge contained substantial modulation at even harmonic frequencies, the largest being the second harmonic. The amplitude of this second harmonic did not depend on the spatial phase of the grating, and its dependence on spatial frequency, at least for suppressed-by-contrast cells, was similar to that of the reduction in mean rate of discharge. Our results suggest that the receptive fields of suppressed-by-contrast and impressed-by-contrast cells can be modeled with the general form of the nonlinear subunit components of Hochstein and Shapley's (1976) Y cell model.

The superior colliculus (SC) projects to all layers of the cat's lateral geniculate nucleus (LGN) and thus is in a position to influence information transmission through the LGN. We investigated the function of the tecto-geniculate pathway by studying the responses of cat LGN neurons before, during, and after inactivating the SC with microinjections of lidocaine. The LGN cells were stimulated with drifting sine-wave gratings that varied in spatial frequency and contrast. Among 71 LGN neurons that were studied, 53 showed a statistically significant change in response during SC inactivation. Control experiments with mock injections indicated that some changes could be attributed to slow waxing and waning of responsiveness over time. However, this could not account for all of the effects of SC inactivation that were observed. Forty cells showed changes that were attributed to the removal of tecto-geniculate influences. About equal numbers of cells showed increases (22 cells) and decreases (18 cells) in some aspect of their response to visual stimuli during SC inactivation. The proportion of cells that showed tecto-geniculate influences was somewhat higher in the C layers (68% of the cells) than in the A layers (44% of the cells). In addition, among cells that showed a significant change in maximal response to visual stimulation, the change was larger for cells in the C layers (64% average change) than in the A layers (26% average change) and it was larger for W cells (61% average change) than for X and Y cells (29% average change). Nearly all of the X cells that showed changes had an increase in response, and nearly all of the Y cells had a decrease in response. In addition, across all cell classes, 80% of the cells with receptive fields < 15 deg from the area centralis had an increase in response, and 80% of the cells with receptive fields > 15 deg from the area centralis had a decrease in response. None of the LGN cells had significant changes in spatial resolution, and only three cells had changes in optimal spatial frequency. Ten cells had a change in contrast threshold, 25 cells had a change in contrast gain, and 29 cells had a change in the maximal response to a high-contrast stimulus. Thus, our results suggest that the tecto-geniculate pathway has little or no effect on spatial processing by LGN neurons. Rather, the major influence is on maximal response levels and the relationship between response and stimulus contrast. Several hypotheses about the role of the tecto-geniculate pathway in visual behavior are considered.