Spatial receptive field properties of rat retinal ganglion cells

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.

Direction biases of X and Y type retinal ganglion cells in the cat

1. It has been reported that in the cat only a specialized group of retinal ganglion cells constituting approximately 1% of the overall population are direction sensitive. Two major groups of retinal ganglion cells, the X and Y cells, have been reported not to be sensitive to the direction of stimulus motion. 2. We recorded action potentials of retinal ganglion cells intraocularly. We studied quantitatively the visual responses elicited by drifting sinusoidal gratings of various spatial frequencies, bars, and spots. 3. The results confirm previous reports that most cat retinal ganglion cells exhibit orientation biases when tested with gratings of relatively high spatial frequency. 4. Additionally, we find that 22% of X and 34% of Y type retinal ganglion cells exhibit direction biases. Overall, Y cells displayed significantly stronger direction biases than did X cells. 5. In general, direction biases are clearest when the test gratings are of relatively low spatial frequency. 6. The direction biases of X and Y cells subserving the central 15 degrees of retina were weaker than those of cells subserving more peripheral regions. 7. The direction-biased responses of cat ganglion cells were similar to those of X and Y type relay cells in the cat dorsal lateral geniculate nucleus (LGNd). Thus we suggest that the direction biases of LGNd cells are a reflection of their retinal inputs.

Pharmacological inactivation of pretectal nuclei reveals different modulatory effects on retino-geniculate transmission by X and Y cells in the cat

The modulatory influence of pretectal neurons on retino-geniculate transmission in the cat was studied by cross-correlation analysis of single-unit activity simultaneously recorded from the dorsal lateral geniculate nucleus (dLGN) and the pretectum (PT) and with reversible inactivation of the PT by GABA microiontophoresis during simultaneous visual stimulation of PT and dLGN neurons. Visually induced population activity in PT nuclei was achieved by a moving (or counterphasing) grating which was presented in the background of the light spot used to stimulate the dLGN neuron. As a control, the light spot was presented on a stationary grating to avoid stimulation of PT neurons but to yield the same illumination of the background. Extracellularly recorded dLGN relay cells of the X- and Y-type were found to be differentially affected by the PT-dLGN projection. During visual stimulation of PT cells, X cells were strongly inhibited and this effect was significantly reduced during PT inactivation. By contrast, the visual responses of most Y cells were affected neither by PT stimulation nor by PT inactivation. In addition, the temporal structure of spike patterns during the light response was examined with autocorrelograms and spike-interval distributions. X-on cells often exhibited a multimodal interval distribution and oscillatory type of activity. During stimulation of the PT interval distributions changed in a characteristic manner and oscillations disappeared. Both effects could be almost totally cancelled by PT inactivation. By contrast, the temporal structure of Y-cell responses was not affected. Our results demonstrate for the first time a pretectal modulation of retino-geniculate transmission in cat dLGN which is clearly different for X and Y cells. This influence seems to be mediated via (inhibitory) interneurons, since we found no indication for a direct coupling between PT and dLGN units. This projection might contribute to the well-known phenomenon of saccadic suppression.

Direction-sensitive X and Y cells within the A laminae of the cat's LGNd

Drifting sinusoidal gratings, moving bars, and moving spots were employed to study the direction sensitivity of 425 neurons in the A laminae of the cat's LGNd. Thirty-two percent of X- and Y-type LGNd relay cells exhibit significant direction sensitivity when tested with drifting sinusoidal gratings. X and Y cells exhibit the same degree of direction sensitivity. Moving spots and bars elicit direction specific responses from LGNd cells that are consistent with those elicited when drifting sinusoidal gratings are employed. For cells that are both orientation and direction sensitive, the preferred direction tends to be orthogonal to the preferred orientation. In general, direction sensitivity is strongest at relatively low spatial frequencies, well below the spatial-frequency cutoff for the cell. The presence of significant numbers of direction-sensitive LGNd cells raises the possibility that subcortical direction specificity is important for the generation of this property in the visual cortex.

NMDA and non-NMDA receptors mediate visual responses of neurons in the cat's lateral geniculate nucleus

1. We have examined the effects of iontophoresing specific antagonists to excitatory amino acid receptors on the visual responses of cells in lamina A or A1 of the cat's lateral geniculate nucleus (LGN). 2. Cells were classified as On- or Off-center, X or Y, and lagged or nonlagged. The effects of antagonists were studied while cells were stimulated with spots of the appropriate contrast covering the receptive-field center. 3. The N-methyl-D-aspartate (NMDA) receptor antagonists D-2-amino-5-phosphonovaleric acid (D-APV) and 3-(+/-)-2-carboxypiperazin-4-yl)- propyl-1-phosphonic acid (CPP), when iontophoresed at doses that specifically antagonized NMDA-induced responses but not kainate-induced responses, reduced the responses of all cell types in the LGN, including X and Y cells, lagged and nonlagged cells, and On- and Off-center cells. 4. The non-NMDA receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), when applied at doses that specifically antagonized kainate-induced responses but not NMDA-induced responses, also reduced the visual responses of each of the cell types in the LGN. 5. We analyzed quantitatively the effects of D-APV and CNQX on LGN cells. D-APV reduced the responses of lagged cells to a greater extent than the responses of nonlagged cells. CNQX reduced the responses of lagged and nonlagged cells to a similar extent. There was no difference in the effect of D-APV or of CNQX on X and Y cells or on On- and Off-center cells. 6. We analyzed the effects of the antagonists on separate components of responses, including an early component comprising the first 100 ms of response and a late component comprising the next 300 ms of response. D-APV reduced the late component of lagged cell responses to a greater extent than either the early component of the same cells or the early or late component of nonlagged cells. CNQX had nearly equivalent effects on both response components of all cell types. 7. These data indicate that NMDA and non-NMDA receptors make similar contributions to the responses of On- and Off-center and X and Y cells in the LGN. Lagged and nonlagged cells are not differentiated with respect to the contribution of non-NMDA receptors to their visual responses. The greater contribution of NMDA receptors to the responses of lagged cells is consistent with the large contribution made by these receptors to the late response components of lagged cells.(ABSTRACT TRUNCATED AT 250 WORDS)

Fine structure of receptive-field centers of X and Y cells of the cat

We investigated the fine structure of receptive field centers of X and Y cells of the retina and lateral geniculate nucleus of the cat using sinusoidal grating stimuli of high spatial frequency. By measuring orientation tuning and spatial-frequency tuning at multiple orientations, the two-dimensional sensitivity distribution was examined. We found that receptive-field centers typically have multiple sensitivity peaks that can be modeled as several spatially offset subunits. A subunit structure was found in both X and Y cells, with an average number of subunits per receptive-field center of approximately 2.9 in X cells and approximately 4.6 in Y cells. In X cells these subunits may correspond to individual cone bipolar inputs. In Y cells, the subunits may reflect the structure of the dendritic tree. The observation of the subunit structure of the receptive-field center, in conjunction with manipulation of the retinal wiring through pharmacological intervention, may provide a new tool for probing the circuitry of the retina.

Spatial and temporal response properties of lagged and nonlagged cells in cat lateral geniculate nucleus

1. It has recently been shown that the X- and Y-cell classes in the A-layers of the cat lateral geniculate nucleus (LGN) are divisible into lagged and nonlagged types. We have characterized the visual response properties of 153 cells in the A-layers to 1) reveal response features that are relevant to the X/Y and lagged/nonlagged classification schemes, and 2) provide a systematic description of the properties of lagged and nonlagged cells as a basis for understanding mechanisms that affect these two groups. Responses to flashing spots and drifting gratings were measured as the contrast and spatial and temporal modulation were varied. 2. X- and Y-cells were readily distinguished by their spatial tuning. Y-cells had much lower preferred spatial frequencies and spatial resolution than X-cells. Within each functional class (X or Y), however, lagged and nonlagged cells were similar in their spatial response properties. Thus the lagged/nonlagged distinction is not one related to the spatial domain. 3. In the temporal domain X- and Y-cells showed little difference in temporal tuning, whereas lagged and nonlagged cells showed distinctive response properties. The temporal tuning functions of lagged cells were slightly shifted toward lower frequencies with optimal temporal frequencies of lagged X-cells averaging an octave lower than those of nonlagged X-cells. Temporal resolution was much lower in lagged X- and Y-cells than in their nonlagged counterparts. 4. The most dramatic differences between lagged and nonlagged cells appeared in the timing of their responses, as measured by the phase of the response relative to the sinusoidal luminance modulation of a spot centered in the receptive field. Response phase varied approximately linearly with temporal frequency. The slope of the phase versus frequency line is a measure of total integration time, which we refer to as visual latency. Lagged cells has much longer latencies than nonlagged cells. 5. The intercept of the phase versus frequency line is a measure of when in the stimulus cycle the cell responds: we refer to this as the intrinsic or absolute phase of the cell. This measure of response timing not only distinguished lagged and nonlagged cells well but also covaried with the sustained or transient nature of cells' responses to flashed stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)