Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells

The shared inputs to cat retinal ganglion cells have been investigated by studying correlations in the maintained firing of neighboring ganglion cells. The firing of one cell was recorded from its axon in the optic tract, while that of a neighboring cell was simultaneously recorded with a second electrode in the retina. The recorded cells were of the X- or Y-type and viewed a uniform screen having a luminance of 10 cd/m2. 2. Ganglion cells with overlapping receptive-field centers showed two basic forms of correlated firing: if they had the same center sign (both on-center or both off-center), then they tended to fire at the same time, as shown by a peak in their cross-correlogram; but if they had opposite center signs (an on- and and off-center cell), they tended not to fire at the same time, as shown by a well, or dip, in their cross-correlogram. 3. Both of these tendencies were strongest for cells that were close together and did not appear for cells with nonoverlapping receptive-field centers. The strongest correlations were between neighboring Y-cells, cells with large fields, and the weakest were between X-cells, cells with small fields. In general, the strength of the correlations depended primarily on the area of the overlap between fields. 4. These correlations in maintained firing appear to be principally or entirely caused by shared inputs to the ganglion cells from more distal retinal neurons. The signals from these distal neurons appear to have strong, brief (4-8 ms), well-defined effects on ganglion cells, which are observed even in the absence of a visual stimulus. The inputs responsible for the correlated firing are thus referred to as spontaneously active inputs or simply as active inputs. 5. An analysis of the features in the various types of cross-correlograms supports the following statements about these spontaneously active inputs. a) There are two types of active inputs: inputs excitatory to on-center cells and simultaneously inhibitory to off-center center cells and inputs excitatory to off-center cells and simultaneously inhibitory to on-center cells. b) The active inputs of each type provide excitation to both X- and Y-cells of one center sign and inhibition to both X- and Y-cells of the other center sign. There is no evidence for a special class of more selective inputs providing input only to X-cells or only to Y-cells. c) Active inputs account for the majority (about 80%) of the spikes in the maintained activity of Y-cells but only a small fraction (about 15%) of the spikes in the maintained activity of X-cells. 6. A likely source of the active input signals appears to be spiking amacrine cells with a low rate of spontaneous activity.