Correlated firing among major ganglion cell types in primate retina

Abstract

Retinal ganglion cells exhibit substantial correlated firing: a tendency to fire nearly synchronously at rates different from those expected by chance. These correlations suggest that network interactions significantly shape the visual signal transmitted from the eye to the brain. This study describes the degree and structure of correlated firing among the major ganglion cell types in primate retina. Correlated firing among ON and OFF parasol, ON and OFF midget, and small bistratified cells, which together constitute roughly 75% of the input to higher visual areas, was studied using large-scale multi-electrode recordings. Correlated firing in the presence of constant, spatially uniform illumination exhibited characteristic strength, time course and polarity within and across cell types. Pairs of nearby cells with the same light response polarity were positively correlated; cells with the opposite polarity were negatively correlated. The strength of correlated firing declined systematically with distance for each cell type, in proportion to the degree of receptive field overlap. The pattern of correlated firing across cell types was similar at photopic and scotopic light levels, although additional slow correlations were present at scotopic light levels. Similar results were also observed in two other retinal ganglion cell types. Most of these observations are consistent with the hypothesis that shared noise from photoreceptors is the dominant cause of correlated firing. Surprisingly, small bistratified cells, which receive ON input from S cones, fired synchronously with ON parasol and midget cells, which receive ON input primarily from L and M cones. Collectively, these results provide an overview of correlated firing across cell types in the primate retina, and constraints on the underlying mechanisms.

Figure 1. Correlated firing among ON and OFF parasol cells

A, receptive field outlines of complete ON and OFF parasol cell mosaics, simultaneously recorded. Outlines are drawn at the 1 s.d. contour of Gaussian fits (see Methods). Rectangle indicates the outline of the electrode array. B, cross-correlation of the spontaneous activity between cells labelled in A; cell pairs are given in insets. Note the positive correlation in the ON–ON and OFF–OFF pairs, the negative correlation in ON–OFF pairs, and the decline in correlation with distance. Bin size: 1 ms.

Figure 2. Spatial organization of spontaneous correlated firing within and across RGC types at a photopic light level. Bin size: 10 ms. Light level: 830 (840, 440) P* (L (M, S) cone)⁻¹ s⁻¹)

A, average CCF of nearby cell pairs of each cell type combination. Data from ON and OFF parasol, ON and OFF midget, and small bistratified cells were obtained in a single recording; data from OFF upsilon cells and unidentified wide-field ON cells were obtained in separate recordings (bin size: 1 ms; zero bin omitted; grey shaded region represents 1 s.d. across cell pairs). B, correlation coefficient at time zero as a function of distance between cells. Curves show the dependence of the average receptive field overlap on distance (see Methods). In panels that represent correlations between cells of the same type, neighbouring pairs of cells in the mosaic are indicated with black points, other cell pairs are represented with grey points. The normalized nearest neighbour distance is marked with a arrowhead on the abscissa. Bin size: 10 ms.

Figure 3. Spatial organization of spontaneous correlated firing within and across RGC types at a scotopic light level

Panels are as in Fig. 2. All data were obtained in a single recording. Light level: 1.2 P* rod⁻¹s⁻¹.

Figure 4. CCFs across light levels for pairs of ON parasol cells and pairs of ON midget cells

The light level increases from left to right. 4500 P* rod⁻¹ s⁻¹ corresponds to 1550 (1570, 740) P* (L (M, S) cone)⁻¹ s⁻¹. Bin size: 1 ms.

Figure 5. CCFs in the presence of stimuli with correlations of increasing spatial extent, for pairs of ON parasol cells and pairs of one ON and one OFF parasol cell

Left: CCFs of activity during constant illumination. Four CCFs are overlaid from recordings interleaved between recordings with visual stimulation. Right: CCFs in the presence of a time-varying stimulus (see text for details). Extent of spatial correlation in the stimulus is expressed as the standard deviation of the low-pass filter used to construct the stimuli. The mean ON parasol receptive field diameter was ∼140 μm. For each condition, the raw CCF, the CCF from shuffled identical stimulus repeats (shift predictor), and the difference between the two (corrected CCF) are shown. Grey shaded region represents 1 s.d. across cell pairs; for clarity this is only shown for the corrected CCF. Bin size: 1 ms.