The size and shape of rod and cone centres of cat retinal ganglion cells

Summary Receptive field centres of cat retinal ganglion cells, as mediated by rod and by cone inputs, were mapped as contours of iso-sensitivity at a mid-mesopic adapting luminance using, respec-tively, 452 nm-blue and 578 nm-yellow narrow-band lights at an intensity 1 log unit above threshold for the most sensitive locus. Based on the sizes and shapes of mapped rod and cone centres for 74 ganglion cells, four receptive field centre categories were distinguished. Cone and rod centres were usually elliptical, and in almost 60% of cells the major axis through the receptive field centre was oriented within ±20 ° of horizontal. In 69%, rod and cone centres were non-concentric, 66% had larger rod than cone centres — area ratios ranging from 0.6 1 to 2.9 1, and in only two cases was the rod centre actually smaller than the cone centre.     

Orientation biased extended surround of the receptive field of cat retinal ganglion cells

Here we report that the extended surround outside the classical receptive center (hereafter called the extended surround) of most retinal ganglion cells in the cat exhibit significant orientation bias to grating stimuli, and that the center and the extended surround show different orientation biases at different spatial frequencies.As a result, some retinal ganglion cells possess a complex receptive field structure, which allows them to detect sophisticated image segmentation (e.g. texture segmentation) in addition to simple luminance edges. This property was previously thought to exist primarily in the visual cortex. Moreover, in about one quarter of 128 cells studied the center did not exhibit an orientation bias. Thus, these surrounds alone may determine the cells' orientation bias.In conclusion, the extended surround may play an important role in processing more complex pattern in natural scenes since the classical receptive field is too small to describe all the properties of a retinal ganglion cell.     

The outer disinhibitory surround of the retinal ganglion cell receptive field

1. There is an outer disinhibitory zone surrounding the classical inhibitory surround of the retinal ganglion cell receptive field.2. The disinhibitory surround is strong and narrow in ;sustained' cells but weak and laterally spread in ;transient' cells.3. The disinhibitory surround can be demonstrated using a black spot as a probing stimulus as well as by a white spot, and is therefore not an artifact of scattered light.4. Stimulation with a light spot in the disinhibitory zone gives an increase in firing to ;stimulus on' in on-centre cells and to ;stimulus off' in off-centre cells.5. The disinhibitory surround may be revealed by plotting the latency of the first spike discharge following stimulation against position in the receptive field. The disinhibitory zone shows a decrease in latency to the centre-type stimulus.6. The disinhibitory surround may be revealed by plotting the threshold intensity of a spot against position in the receptive field. It is thus a feature of the sensitivity gradients of both ;transient' and ;sustained' cells.7. Using two spots, one at the centre of the receptive field and the other at varying distances from the receptive field centre, dynamic interactions between the centre, inhibitory and disinhibitory zones are demonstrated. A spot presented in the disinhibitory zone causes an enhancement of the centre response when flashing in phase with the centre spot, while it causes inhibition of the centre response when presented 180 degrees out of phase.8. A scheme for the anatomical basis of the disinhibitory surround is proposed, and the relation of disinhibition to the spatial transfer characteristics of the visual pathways is discussed.     

Goldfish ganglion cells with unusual receptive field properties

Goldfish retinal ganglion cells with unusual response properties are described. Each cell was classified as either Y-like or W-like, based upon its responses to sinusoidally modulated contrast-reversal gratings presented at various positions across the cell's receptive field. The unusual responses of the cells (which distinguish them from typical Y-like and W-like cells) occurred when sinusoidal gratings were drifted across the receptive field at a constant temporal rate. These cells responded at double the stimulus temporal rate to low-spatial-frequency gratings; a Fourier decomposition of the response revealed a large second harmonic component. However, to high-spatial-frequency stimuli, the response modulated at the temporal frequency of the stimulus; the Fourier fundamental component dominated the response. To examine the underlying receptive field mechanisms of these cells, each cell's response was analyzed using several different response measures. The results suggest that the receptive field properties of these unusual cells differ from the typical center/surround organization and confirm recent findings that the receptive fields of goldfish ganglion cells consist of inhomogeneities and subareas.     

Development of receptive field properties of retinal ganglion cells in kittens raised with a convergent squint

Summary The effects on retinal ganglion cell receptive fields of rearing kittens with convergent squint, surgically induced on the 12th post-natal day, were investigated by utilizing the extracellular single unit recording technique. The data revealed that responses of cross-eyed cat ganglion cells to contrast reversal stimuli were severely depressed and the retinal region exhibiting the best responses varied according to the degree of convergent misalignment of the eyes displayed by each animal. Receptive field sizes of X-type (but not Y-type) units located within 10 ° of the area centralis of cross-eyed cats were significantly larger than those in normally reared cats. Finally, the encounter rate for units exhibiting non-linearity of spatial summation (Y-type) were much lower in cross-eyed cats. The results suggest developmental alterations in the retinal neurophysiology of common cats reared with a large convergent squint.This investigation was supported by NIH grants EY01444 and EY00701     

The control of retinal ganglion cell discharge by receptive field surrounds.

1. This paper describes the behaviour of the receptive field surround, and how surround signals combine with those from the centre to generate the discharge of the retinal ganglion cells of the cat. 2. A small test spot is flashed upon the middle of the receptive field of an on-centre X-cell, alone, or together with a concentric annulus of fixed luminance. The reduction in discharge brought about by the annulus is independent of spot luminance. From this it is inferred that centre and surround signals combine additively. 3. Knowing that the combination of signals is additive, the surround signal can be estimated by comparing the ganglion cell's response to diffuse illumination of its receptive field with that to an equiluminous spot which optimally stimulates the centre while encroaching minimally upon the periphery. 4. Application of this technique to X-cells shows that although the surround seems to have a threshold, it is at its most sensitive in the dark-adapted eye, and typically is only 0.3-0.5 log units less sensitive than the centre. 5. Centre and surround sensitivities are decreased from their dark-adapted levels by increasing background illumination, but the decline of surround sensitivity is initially less rapid than that of the centre. Thus with increasing light-adaptation the surround becomes relatively more sensitive. In the light-adapted eye centre and surround are about equally sensitive to diffuse illumination. 6. Although, in the dark-adapted eye, illumination of the receptive field periphery of an on-centre unit depresses firing, removal of that illumination produces no off-discharge. Off-discharges appear only when background illumination exceeds about 104 quanta (507)/deg 2 sec. This confirms Barlow & Levick (1969b). 7. In the dark-adapted eye surround latency is longer than that of the centre. With increasing background illumination the latency difference is reduced. 8. For X-cells, the rate of the maintained discharge depends to some extent on the balance of centre-surround antagonism. But this antagonism is not the major factor accounting for the relative constancy of mean rate at high background luminances, for the rate then can be almost independent of the size of a steady pot. 9. The mean rate of discharge of Y-cells seems to depend even less upon the balance of centre-surround antagonism. 10. Y-cell surrounds could not properly be isolated with the optimal spot-diffuse illumination technique, so detailed measurements of their behaviour were not made. However, the dark-adapted surround appear to be as sensitive as those of X-cells.     

Nonlinear measurement and classification of receptive fields in cat retinal ganglion cells

Originally, modeling of ganglion-cell responses in cat was based mainly on linear analysis. This is satisfactory for those cells in which spatial summation of excitation is approximately linear (X-cells) but it fails for Y-cells, where summation has strong nonlinear components. Others have shown the utility of using sinusoidal analysis to study harmonic and intermodulation nonlinearities in the temporal frequency domain. We have used Wiener-kernel analysis to obtain directly both temporal and spatial impulse responses and their nonlinear interactions. From these, we were able to predict accurately the responses that a counterphase modulated grating elicited in both X-cells and Y-cells. In addition, we show that the first-order responses can measure the two-dimensional spatial features of the receptive field with high resolution. Thus, nonlinear analysis of responses to white-noise stimuli may be sufficient to both classify and measure the receptive fields of many different types of ganglion cells.     

Interspike interval analysis of retinal ganglion cell receptive fields

The interspike interval (ISI) preceding a retinal spike has a strong influence on whether retinal spikes will drive postsynaptic responses in the lateral geniculate nucleus (LGN). This ISI-based filtering of retinal spikes could, in principle, be used as a mechanism for processing visual information en route from retina to cortex; however, this form of processing has not been previously explored. Using a white noise stimulus and reverse correlation analysis, we compared the receptive fields associated with retinal spikes over a range of ISIs (0-120 ms). Results showed that, although the location and sign of retinal ganglion cell receptive fields are invariant to ISI, the size and amplitude of receptive fields vary with ISI. These results support the notion that ISI-based filtering of retinal spikes can serve as a mechanism for shaping receptive fields.     

Spectral coding in cat retinal ganglion cell receptive fields

We have examined the spectral-coding properties of ganglion cell receptive fields in the cat retina. Two classes of spectral coding were found. The first class consists of cells in which color opponency is spatially local. That is, the opponent cone types cover the same (center or surround) region of the receptive field. The second class consists of cells that show color opponency only to large stimuli (relative to center diameter). Center and surround regions of cells of this class have different spectral sensitivities. Individually the regions are nonopponent. When both regions are stimulated, a spectral opponency is revealed. For example, we recorded from one unit in which the ON-center was mediated by the 556-nm cone type and the OFF-surround was mediated by both 450- and 556-nm cone types. Large-field, threshold-level stimulation in the short-wavelength end of the spectrum produced OFF-responses, while in the long-wavelength end produced ON-responses. For a small stimulus, cells of the second class could mediate spatial vision, largely unaffected by the chromatic properties of the stimulus. Cells of the second class (center/surround opponent) were more commonly encountered than cells of the first class (locally opponent). Color-opponent units of X, Y, and W types were all found.     

Cat retinal ganglion cells show transient responses to acetylcholine and sustained responses to L-glutamate.

The neuropharmacological basis for the different receptive field properties of cat retinal ganglion cells was investigated using whole cell voltage-clamp recordings from acutely dissociated adult tissue. Subclasses of physiologically characterised ganglion cells were determined on the basis of (i) their soma diameters and (ii) their projection to central visual nuclei (identified by microinjection of fluorescent dyes into the lateral geniculate and/or superior colliculus). The sensitivities of all categories of ganglion cells, prepared from peripheral retina were found to be similar for gamma-amino butyric acid, glycine, acetylcholine and glutamate. The kinetics of desensitisation differed among receptor subtypes, revealing possible physiologically significant molecular specialisations that could be involved in shaping synaptic transmission.     

The effects of light-adaptation on rod and cone receptive field organization of monkey ganglion cells

1. Receptive fields of perifoveal ganglion cells have been measured by determining threshold for eliciting a just detectable response using either concentric spot stimuli centred on the receptive field or small spot stimuli in different parts of the receptive field at various states of retinal adaptation and with stimuli selected to separate rod from cone function.2. Light-adaptation decreases the sensitivity, latency and duration of threshold responses throughout the receptive field of a ganglion cell.3. With all patterns of retinal stimulation and states of adaptation, threshold signals of the rods reach a ganglion cell later and those of the cones earlier than approximately 50 msec after a light stimulus.4. In the more dark-adapted retina threshold rod and cone signals can be transmitted to the brain by the same or by neighbouring ganglion cells but not simultaneously; in the light-adapted state only the cone signal is transmitted.     

Rabbit retinal ganglion cells

Summary The classification of concentrically organized receptive fields of rabbit retinal ganglion cells was extended along similar lines to that in the cat by distinguishing brisk and sluggish classes and then sustained and transient types of each. Quantitative measures of responsiveness to stationary and to moving stimuli revealed characteristic features which distinguished these classes. Brisk-transient and brisk-sustained classes are not as distinct from each other as in the cat: centre size distributions overlapped almost completely and there was also substantial overlap of axonal conduction properties whether expressed in terms of latency or conduction velocity between two central stimulus sites. Representatives of every class of rabbit ganglion cells sent axons to the superior colliculus.Supported by a Postdoctoral Fellowship of the US Public Health Service