Search

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.

Studies on the receptive field properties of cat retinal ganglion cells over the past half-century are reviewed within the context of the role played by the receptive field in visual information processing. Emphasis is placed on the work conducted within the past 20 years, but a summary of key contributions from the 1950s to 1970s is provided. We have sought to review aspects of the ganglion cell receptive field that have not been featured prominently in previous review articles. Our review of the receptive field properties of X- and Y-cells focuses on quantitative studies and includes consideration of the function of the receptive field in visual signal processing. We discuss the non-classical as well as the classical receptive field. Attention is also given to the receptive field properties of the less well-studied cat ganglion cells-the W-cells-and the effect of pathology on cat ganglion cell properties. Although work from our laboratories is highlighted, we hope that we have given a reasonably balanced view of the current state of the field.

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.

1. The genetic basis of colour vision in New-World primates differs from that in humans and other Old-World primates. Most New-World primate species show a polymorphism; all males are dichromats and most females trichromats. 2. In the retina of Old-World primates such as the macaque, the physiological correlates of trichromacy are well established. Comparison of the retinae in New- and Old-World species may help constrain hypotheses as to the evolution of colour vision and the pathways associated with it. 3. Ganglion cell behaviour was recorded from trichromatic and dichromatic members of a New-World species (the capuchin monkey, Cebus apella) and compared with macaque data. Despite some differences in quantitative detail (such as a temporal response extended to higher frequencies), results from trichromatic animals strongly resembled those from the macaque. 4. In particular, cells of the parvocellular (PC) pathway showed characteristic frequency-dependent changes in responsivity to luminance and chromatic modulation, cells of the magnocellular (MC) pathway showed frequency-doubled responses to chromatic modulation, and the surround of MC cells received a chromatic input revealed on changing the phase of heterochromatically modulated lights. 5. Ganglion cells of dichromats were colour-blind versions of those of trichromats. 6. This strong physiological homology is consistent with a common origin of trichromacy in New- and Old-World monkeys; in the New-World primate the presence of two pigments in the middle-to-long wavelength range permits full expression of the retinal mechanisms of trichromatic vision.

There were three objectives to the work undertaken for this paper: (1) to provide a comprehensive characterization of the statistical properties of arrays of beta-cell somata; (2) to develop a model that simulates cellular arrays with the same properties; and (3) to use this model to examine whether the array of beta-cells should be viewed as one array or as two arrays, one each for its OFF- and ON-center cells. Beta-cells are morphological correlates of the electrophysiological X-cells and those beta-cells whose dendrites stratify within the outer and inner sublamina of the retina's inner plexiform layer correspond, respectively, to OFF- and ON-center X-cells. Arrays of peripheral beta-cell somata from two retinas were studied. A Delaunay triangulation and a Voronoi tessellation were generated for each array and measures derived from these constructs used to analyze the arrays' spatial organization. As others have shown previously with a less complete statistical characterization, we found that the arrays of OFF- and ON-center beta-cells have similar spatial properties and are more regular than the array of all beta-cells. We developed a model to simulate cellular arrays with spatial properties like those of arrays of beta-cells. A good fit between model and real arrays was found when the model assumed an explicit spatial dependence between the placement of OFF- and ON-center cells. We propose therefore that a single array of beta-cells formed of both OFF- and ON-center cells is consistent with the data currently available for beta-cell somatic arrays.

Our objective with this study was to provide a near complete characterization of how mean light level changes the spatial receptive-field properties of X-cells. Single X-cells were recorded extracellularly either from cell bodies in the retina or from their axons in the optic tract. Frequency responses of the cells at 2 Hz were measured for a set of gratings of different spatial frequencies and for a stimulus designed to probe the spatial properties of the receptive-field surround. Predicted frequency responses of a Gaussian center-surround model for the receptive field were fit simultaneously to both sets of measurements and the parameters of the model that best fit the data used to characterize the spatial properties of the receptive field. Measurements were made at a number of mean light levels for each cell and changes in receptive-field properties were characterized by changes in the parameters of the Gaussian center-surround model. The range of illuminances studied covered the bulk of the range encountered by a cat naturally and three distinct functional ranges appeared to express themselves in the data. One range corresponded to the cat's photopic range of vision. The other two ranges were where signals originating in rods dominate X-cell responses. We argue that one corresponds to the range that rod signals pass predominantly through rod bipolars en route to the X-cell, while the other is where rod signals flow predominantly through cones via gap junctions and then follow the path of cone signals to the X-cell. Among the major findings are that Weber's Law is followed throughout the photopic but not the scotopic range, that center radius expands under scotopic conditions, and that the surround is present even at the lowest scotopic levels we studied.

A method of using neurobiotin to stain both the dendrites and the soma mosaics of retinal ganglion cells in fresh retinae is described. This method is simple to use and efficient in revealing morphological details for a large number of retinal ganglion cells. It has five advantages over currently available staining methods. (1) It stains all ganglion cells in the whole retina or in a selected retinal area, permitting ganglion cell distributions across the retina to be obtained. (2) It reveals cell dendrites in great detail, especially in regions outside the area centralis. The dendritic field mosaics and, therefore the dendritic field coverage factors, of different ganglion cell types across the whole retina can be obtained easily. (3) It works reliably, efficiently, and does not require the expensive set-up or the pains-taking work needed when staining cells through intracellular injection. (4) It works under both in vivo and in vitro settings, permitting the use of retinae from animals sacrificed for other purposes and the use of postmortem human retinae. (5) The end product of the visualization process is optically dark and electron dense, permitting specimens to be examined under both light and electron microscopes.

VSApc is a suite of DOS programs that was developed to measure spatiotemporal frequency responses and to collect maintained discharge from retinal ganglion cells of cats and monkeys. The operation of the programs is described and their details summarized.

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.

Steady discharges were collected from ganglion cells of the magnocellular (MC) and parvocellular (PC) pathways of the macaque while their receptive fields were uniformly illuminated with a 4.7-deg steady yellow light of photopic illuminance. The mean rates, coefficients of variation, interval distributions, serial correlation coefficients, and power spectra of these discharges were determined. The results presented permit one to estimate the noise power in the discharges of macaque ganglion cells and hence determine how visual signals of different amplitudes will be affected by the noise resident in their discharges. Although there was some small serial correlation in the discharges of both MC- and PC-pathway cells, their discharges can be considered to result from renewal processes with reasonable accuracy. As with the discharges of cat ganglion cells, macaque ganglion cell discharges can be considered to have approximately gamma-distributed intervals. Steady discharges of MC- and PC-pathway cells show considerable overlap in their statistics, although small but significant differences are present.

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.

The discharges of ON- and OFF-center X and Y retinal ganglion cells in the presence of stationary patterns or of a uniform field of photopic luminance were recorded from urethane-anesthetized adult cats. The interval statistics and power spectra of these discharges were determined from these discharge records. The patterned stimuli were selected and positioned with respect to a cell's receptive field so as to generate steady discharges that were different in mean discharge rate from that cell's discharge for the diffuse field. The interval statistics of discharges recorded for diffuse or patterned illumination for all cell types can be modeled, approximately, as coming from renewal processes with gamma-distributed intervals. The gamma order of the interval distributions was found to be nearly proportional to the mean discharge rate for X cells, but not for Y cells. Typical values for the gamma orders and their dependence on mean rate for different cell types are given. The same model of a renewal process with gamma-distributed intervals is used to model the measured power spectra and performs well. When the gamma order is proportional to mean rate, the power spectral density at low temporal frequencies is independent of discharge rate. Gamma order was proportional to mean rate for X cells but not for Y cells. Nonetheless, the power spectral densities of both cell types at low frequencies were approximately independent of discharge rate. Hence, noise in this band of frequencies can be considered additive. The consequences of departures from the renewal process and of the gamma order not being proportional to mean rate are considered. The significance of different rates of discharge for signaling is discussed.

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 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.