Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events

Abstract

The correlated firing of neighboring cat retinal ganglion cells was examined at low background levels and in darkness. At these backgrounds, cross-correlograms showed a strong, broad peak for a pair of on-center cells, a weak, broad peak for a pair of off-center cells, and a broad well for 2 cells of opposite center sign. The broad peaks and wells are caused by a single type of common input event lasting 40-50 ms. This input event is excitatory to on-center cells and often causes 2 or 3 spikes in a single on-center cell, giving these cells a tendency to fire in bursts at low backgrounds. The input event is inhibitory to off-center cells and causes visible gaps in their maintained discharge at low backgrounds. Two neighboring on-center cells have a strong tendency to fire together because they are both excited by shared input events. Two off-center cells show a weak tendency to fire together because they are both restricted to firing at the times when they are not inhibited together by shared input events. An on- and an off-center cell have a tendency not to fire together because the off-center cell is inhibited when the on-center cell is excited by their shared input events. The rate of the input events received by ganglion cells at the lowest backgrounds was linearly related to the quantity of background light and matched the calculated rate of effective photon absorptions in the rods. The events appear to originate as individual quantal events in the rods. The characteristic shapes of the correlograms for the different types of pairs at low light levels imply that the average excitatory response of on Y-cells to these quantal events is more transient than that of on X-cells, and that the average inhibition of off Y-cells by quantal events is more transient than that of off X-cells. The primary source of the more sustained response of on X-cells to quantal events is a relatively sustained excitation that does not pass through the active inputs described earlier. It is considerably stronger for on X-cells than for on Y-cells. The analysis provides evidence for an analogous sustained inhibition of off-center cells that is considerably stronger for off X-cells. On-active inputs may have a rather transient response to quantal events and provide an initial transient excitation of on-center cells and inhibition of off-center cells. Cone bipolar cells may be the final pathway for the relatively sustained effects of quantal events and tonic signals from these bipolar cells are a major source of maintained activity for X-cells and a minor source for Y-cells at higher backgrounds. Two hypotheses (light-adapted X-cells show a greater sustained response than Y-cells to a central stimulus because they receive stronger input from cone bipolar cells; and active inputs serve as a final common pathway to ganglion cells for the signals responsible for some of the distinctive properties of Y-cells) are discussed.