Effects of remote stimulation on the mean firing rate of cat retinal ganglion cells.

Visual stimulation outside the classical receptive field can have pronounced effects on cat retinal ganglion cells. We characterized the effects of such stimulation by varying the contrast, spatial frequency, temporal frequency, and spatial extent of remote drifting sinusoidal gratings. We found that the mean firing rate of some X-cells and most Y-cells increased to remote gratings of low spatial frequency and high temporal frequency and decreased to ones of high spatial frequency and low temporal frequency. At least 10-20% contrast was required to see either effect, which quickly saturated at higher contrasts. Both effects were substantial, raising or lowering the mean rate of some cells by over 40 impulses/sec. Classical receptive field mechanisms were not involved because the remote gratings caused little or no response modulation. We conclude that, in addition to a mean-increasing mechanism known from previous work, a mean-decreasing one operates in the cat retina. This mechanism prefers slower motion and resolves finer patterns than the mean-increasing one. We incorporate these findings into a model consisting of pools of small and large rectifying subunits of opposite polarity. Model estimates of subunit radius were primarily independent of eccentricity and averaged approximately 0.15 and approximately 0.60 degrees for the mean-decreasing and mean-increasing mechanisms, respectively. This makes the subunits approximately the center size of central X- and Y-cells. Because smooth movements of the eyes, head, or body should engage these mechanisms under natural conditions, we propose that the mean rate changes that would ensue are functionally relevant to cat vision.

Tests of the mouse visual system.

To apply the approach of forward genetics (e.g., gene identification with mutagenesis and screening, followed by positional cloning) to the mouse, it is necessary to have available screening tests that can be applied rapidly to individual mice and that give a reliable assessment of visual function. This paper reviews the strengths and limitations of two anatomical tests related to visual function, fundus examination and retinal histological examination. Two tests that do not depend on behavior of a conscious animal are reviewed: the electroretinogram and the visual evoked potentials of the cortex. Eight behavioral tests are also summarized: maze-based tests, cued fear conditioning, tests based on conditioned suppression, visual placing, optokinetic nystagmus, pupillary reflex, and light-induced shifts in circadian phase. It is recommended that retinal histology, the electroretinogram, and visual-evoked potentials be used at the present time for screening because they assess the function and structure of the visual system rapidly and reliably. In fact, the electroretinogram (or visually evoked potentials) can be recorded from several animals simultaneously in response to the same stimulus. It is also recommended that efforts be made to develop more appropriate, automated, behavioral tests of visual perception than are now available, particularly tests that rely solely on rewarding visually evoked behavior. Two other promising behavioral tests are cued fear conditioning and variants of maze tests.

The cat's pupillary light response under urethane anesthesia.

Pupillary area was measured in urethane-anesthetized cats as a function of retinal illuminance. When appropriate corrections are made for differences in experimental procedures, it was found that the pupillary response of the urethane-anesthetized cat's eyes to light was basically unchanged from that of the alert behaving cat. This preparation may therefore be a very satisfactory one in which to study the pupillary response pathway in a higher mammal.

Receptive-field properties of Q retinal ganglion cells of the cat.

The goal of this work was to provide a detailed quantitative description of the receptive-field properties of one of the types of rarely encountered retinal ganglion cells of cat; the cell named the Q-cell by Enroth-Cugell et al. (1983). Quantitative comparisons are made between the discharge statistics and between the spatial receptive properties of Q-cells and the most common of cat retinal ganglion cells, the X-cells. The center-surround receptive field of the Q-cell is modeled here quantitatively and the typical Q-cell is described. The temporal properties of the Q-cell receptive field were also investigated and the dynamics of the center mechanism of the Q-cell modeled quantitatively. In addition, the response vs. contrast relationship for a Q-cell at optimal spatial and temporal frequencies is shown, and Q-cells are also demonstrated to have nonlinear spatial summation somewhat like that exhibited by Y-cells, although much higher contrasts are required to reveal this nonlinear behavior. Finally, the relationship between Q-cells and Barlow and Levick's (1969) luminance units was investigated and it was found that most Q-cells could not be luminance units.

Effect of ambient illumination on the spatial properties of the center and surround of Y-cell receptive fields.

The primary goal of this study was to expand the description of the filtering properties of the Y-cell receptive field, by quantitatively characterizing the spatial filtering properties of the receptive field's center-and-surround components as a function of adapting light level. A range of more than five orders of magnitude in retinal illuminance were covered, including the vast majority of the cat's functional range of vision. Recordings were taken from optic tract fibers of Y cells in cats under general anesthesia. Sinusoidal gratings and a stimulus designed to selectively probe the properties of the surround mechanism were used. The cells' responses to these stimuli were fit to a Gaussian center-surround receptive-field model, in which six parameters define the properties of the center and surround. Fits were made independently to data collected at each light level and changes in the values of the model's parameters with illuminance are reported. A set of equations that summarize the changes in parameter values is given. From these summary equations, reasonable estimates of the parameters' values can be determined across a wide range of illuminances. Hence, a quantitative model of the spatial properties of the center and surround of the Y-cell receptive field can now be derived from these equations for most of the levels of retinal illuminance experienced by a Y cell. The consistency between the description provided by our equations and results from earlier work is considered.

X and Y ganglion cells inform the cat's brain about contrast in the retinal image.

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.

Dependence of center radius on temporal frequency for the receptive fields of X retinal ganglion cells of cat.

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.

Responses to sinusoidal gratings of two types of very nonlinear retinal ganglion cells of cat.

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 grating 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.

Spatiotemporal frequency responses of cat retinal ganglion cells.

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.

The receptive-field spatial structure of cat retinal Y cells.

1. Y-type ganglion cells in the cat's retina were stimulated with bars of light and grating patterns at photopic luminances. Stimuli were stationary, and luminance at each point was varied sinusoidally in time at 2 Hz. Impulse rates were recorded from single cells. 2. When the stimulus was a narrow bar of light, the impulse rate approached a sinusoidal function of time as contrast was reduced. The linear behaviour of each cell was therefore characterized by taking the limit of response parameters as contrast approached zero. 3. The ratio of surround strength to centre strength varied widely between cells but the two strengths were approximately equal on average. The difference between surround phase and centre phase averaged 168 deg. 4. As contrast increased, responses became rectified. Rectifier output was well described by a power law of stimulus amplitude, where the power was usually 1.4 or 1.5. 5. Response phase advanced with increasing contrast, and at high response amplitudes grew less than proportionally with contrast. These effects were assumed due to the contrast gain control described by Shapley & Victor (1978). 6. Gratings in which luminance varied sinusoidally with distance were used to determine Y cell spatial resolution. The second-harmonic amplitude of the response diminished rapidly with increasing spatial frequency: the radius of the best-fitting Gaussian mechanism was about 0.25 deg for a cell at 10 deg eccentricity. 7. This spatial resolution is close to the linear resolution of X cells as determined by Linsenmeier, Frishman, Jakiela & Enroth-Cugell (1982). 8. A receptive field model incorporating both linear and non-linear elements is described. The model consists of an array of subunit pathways, each of which has a centre-surround organization followed by a rectifier; a pool weights and sums subunit outputs, and signals are then passed through a contrast gain control. 9. The model accounts qualitatively for the over-all centre-surround organization of Y cell linear responses, the dependence of frequency-doubled responses on spatial frequency, and impulse rate as a function of time for a variety of bar and grating stimuli.

Interactions between the rod and the cone pathways in the cat retina.

The receptive field centers of 21 on-center X retinal ganglion cells in cat were tested with stimuli designed to detect nonlinear interactions between the rod and the cone systems. One red and one green stimulus light were always present, at a level such that modulation of the red light essentially affected only cones, and that of the green light only rods. The two lights could be superimposed spatially (overlapped configuration) or fall on separate subareas of the receptive field center (nonoverlapped configuration). In most cases, there was less complete summation of the responses to modulation of the lights in the overlapped than in the nonoverlapped configuration, with a corresponding difference in the summation of sensitivities. In 1/6 of the experiments, there was more complete summation of the responses to the lights in the overlapped configuration, with a corresponding difference in the summation of sensitivities. The mean magnitude of the interaction for all experiments was equivalent to an antagonistic interaction between the rod and cone pathways such that the signal in each was diminished by a quantity slightly greater than 30% of the signal in the other.

Spatio-temporal interactions in cat retinal ganglion cells showing linear spatial summation.

The spatio-temporal characteristics of cat retinal ganglion cells showing linear summation have been studied by measuring both magnitude and phase of the responses of these cells to drifting or sinusoidally contrast-modulated sinusoidal grating patterns. It has been demonstrated not only that X cells behave approximately linearly when responding with amplitudes of less than about 10 impulses/sec to stimuli of low contrast but also that cells of another type with larger receptive field centres (Q cells) behave approximately linearly under the same conditions. These Q cells appear to form a homogeneous group which is probably a subset of the tonic W cells (Stone & Fukuda, 1974) or sluggish centre-surround cells (Cleland & Levick, 1974). The over-all spatio-temporal frequency characteristics of cells showing linear spatial summation are not separable in space and time. The form of the spatial frequency responsivity function of these cells depends upon the temporal frequency at which it is measured while the temporal phase of their resonse measured at any constant temporal frequency depends upon the spatial frequency of the stimulus. The behaviour of X and Q cells is quite well explained by an extension of the model in which signals from centre and surround mechanisms with radially Gaussian weighting functions are summed to provide the drive to the retinal ganglion cell. While the general form of the temporal frequency response characteristics of these ganglion cells are probably provided by the characteristics of elements common to the centre and surround pathways, the spatio-temporal interactions can be explained by assuming that the surround signal is delayed relative to the centre signal by a few milliseconds.

Receptive field properties of x and y cells in the cat retina derived from contrast sensitivity measurements.

The contrast sensitivity to gratings drifting at 2.0 Hz has been measured for X and Y type retinal ganglion cells, and these data have been used to characterize the sizes and peak sensitivities of centers and surrounds. The assumption of Gaussian sensitivity distributions is adequate for both types of cells, but allows a better description of X than of Y cells. The size and peak sensitivity can be specified more precisely, in general, for the center than for the surround. The data also show that for both types of cells (1) center radius increases with eccentricity, but is two to three times larger than Y cells than for X cells at a given eccentricity, (2) spatial resolution is an excellent predictor of center size, (3) the larger the center or surround, the lower its small spot sensitivity at a specific mean lumminance and (4) the surround is nearly as strong as the center for large or diffuse stimuli. X cell surrounds are relatively weaker in the middle of the receptive field than Y cell surrounds, but X cell surrounds are larger relative to their centers.

Spatial consequences of bleaching adaptation in cat retinal ganglion cells.

1. Experiments were conducted to study the effects of localized bleaching on the centre responses of rod-driven cat retinal ganglion cells. 2. Stimulation as far as 2 degrees from the bleaching site yielded responses which were reduced nearly as much as those generated at the bleaching site. Bleaching in the receptive field middle reduced responsiveness at a site 1 degrees peripheral more than bleaching at that peripheral site itself. 3. The effectiveness of a bleach in reducing centre responsiveness is related to the sensitivity of the region in which the bleach is applied. 4. Response reduction after a 0.2 degree bleach followed the same temporal pattern for concentric test spots of from 0.2 to 1.8 degrees in diameter, implying a substantially uniform spread of adaptation within these bounds. 5. A linear trade-off between fraction of rhodopsin and area bleached over a range of 8:1 yields the same pattern of response reduction, implying that the non-linear nature of bleaching adaptation is a property of the adaptation pool rather than independent photoreceptors.

The contrast sensitivity of cat retinal ganglion cells at reduced oxygen tensions.

1. These experiments were done to investigate the effect of various degrees of hypoxia on the function of retinal ganglion cells (recorded in the optic tract) and on retinal oxygen tension. 2. The contrast sensitivity of the centre of X and Y cells, the surround of X cells and the non-linear subunits of Y cells were measured separately by choosing appropriate spatial and temporal parameters of a sinusoidal grating pattern. 3. Retinal oxygen tension was measured with a bipolar polarographic oxygen electrode positioned in the vitreous humor close to the retina. 4. The time course of changes in ganglion cell sensitivity and retinal oxygen tension was similar. However, oxygen tension frequently overshot the prehypoxic value at the end of hypoxia, while sensitivity did not. 5. The cat retina was rather resistant to hypoxia. Contrast sensitivity and mean firing rate did not change provided the arterial oxygen tension was above about 35 mmHg, but usually dropped precipitously at lower arterial values. 6. The apparent reason for this resistance is that retinal oxygen tension was well regulated, falling only 0.14 mmHg per mmHg of arterial oxygen tension for arterial values above about 35 mmHg, which corresponds to a retinal oxygen tension of about 10 mmHg. Retinal oxygen tension decreased more sharply (0.62 mmHg per mmHg) at lower values of arterial oxygen tension, where sensitivity also decreased. 7. The centre, surround and subunits reacted similarly to hypoxia. This suggests that lateral pathways (i.e. surround) and pathways which might be expected to use more synapses than the centre (i.e. surround and subunits) are not more susceptible to hypoxia.

Suppression of cat retinal ganglion cell responses by moving patterns.

1. Action potentials were recorded from single fibres in the optic tract of anaesthetized cats. 2. A sectored disk or 'windmill', concentric with the receptive field, was rotated about its centre to cause local changes in illumination throughout the receptive field without changing the total amount of light falling on the receptive field centre or surround. 3. A cell's response to a flashing test spot centered on its receptive field was measured both while the windmill was stationary and while it rotated. While the windmill rotated, the test spot evoked a smaller average number of spikes than while the windmill was stationary. 4. The induction in response occurred in both on-centre and off-centre cells and in both X-cells and Y-cells, though the reduction in response was smaller in X-cells. 5. Surround responses, evoked by an eccentric stimulus, were also reduced by a moving peripheral pattern. 6. Suppression was graded with the contrast of the moving pattern. 7. Gratings too fine to be resolved by the receptive field centre could suppress the response of Y-cells. This suggests that the local elements responsible for the suppression are smaller than the receptive field centres of Y-cells. 8. Response suppression started within the 100 msec of the onset of pattern motion.

Summation of rod signals within the receptive field centre of cat retinal ganglion cells.

1. The processing of rod signals within the receptive field centre of cat retinal ganglion cells was investigated in two spot summation experiments by using the analytical methods of response and sensitivity summation. 2. The rod system was isolated by presenting test stimuli of short wave-length light against either a completely dark background or a dim background of long wave-length light. 3. Stimulus--response curves were obtained for two small, square-wave modulated test spots applied at points in the receptive field centre of equal sensitivity. The test spots were presented either singly or simultaneously. 4. In the absence of surround antagonism, the flux required to evoke a weak criterion response was the same whether the spots were presented singly or together. However, the flux required to evoke larger responses was typically half as great when the two spots were delivered together as it was when either was presented alone. 5. Over a moderate response range, the magnitude of response to the two test spots presented together equalled the algebraic sum of the two responses to the test spots presented alone. However, for responses of large magnitude, the algebraic sum was larger. 6. Permitting the surround to contribute substantially to the cell's response changed the outcome of the two spot summation experiment. 7. The data are consistent with a three stage model of signal processing within the receptive field centre: an early compressive power law transformation (within each sub-area) of illuminance into a neural signal which is followed by linear summation of sub-area signals and then a second compressive transformation.

Recovery of cat retinal ganglion cell sensitivity following pigment bleaching.

1. The threshold illuminance for small spot stimulation of on-centre cat retinal ganglion cells was plotted vs. time after exposure to adapting light sufficiently strong to bleach significant amounts of rhodopsin. 2. When the entire receptive field of an X- or Y-type ganglion cell is bleached by at most 40%, recovery of the cell's rod-system proceeds in two phases: an early relatively fast one during which the response appears transient, and a late, slower one during which responses become more sustained. Log threshold during the later phase is well fit by an exponential in time (tau = 11.5-38 min). 3. After bleaches of 90% of the underlying pigment, threshold is cone-determined for as long as 40 min. Rod threshold continues to decrease for at least 85 min after the bleach. 4. The rate of recovery is slower after strong than after weak bleaches; 10 and 90% bleaches yield time constants for the later phase of 11.5 and 38 min, respectively. This contrasts with an approximate time constant of 11 min for rhodopsin regeneration following any bleach. 5. The relationship between the initial elevation of log rod threshold extrapolated from the fitted exponential curves and the initial amount of pigment bleached is monotonic, but nonlinear. 6. After a bleaching exposure, the maintained discharge is initially very regular. The firing rate first rises, then falls to the pre-bleach level, with more extended time courses of change in firing rate after stronger exposures. The discharge rate is restored before threshold has recovered fully. 7. The change in the response vs. log stimulus relationship after bleaching is described as a shift of the curve to the right, paired with a decrease in slope of the linear segment of the curve.