Gap junctional coupling underlies the short-latency spike synchrony of retinal alpha ganglion cells

We examined whether coupling between neighboringalpha-type ganglion cells (alpha-GCs) in the rabbit retina underlies their synchronous spike activity. Simultaneous recordings were made from arrays of alpha-GCs to determine the synchrony of both spontaneous and light-evoked spike activity. One cell within each array was then injected with the biotinylated tracer Neurobiotin to determine which of the cells were coupled via gap junctions. Cross-correlation analyses indicated that neighboring off-center alpha-GCs maintain short-latency (approximately 2.5 msec) synchronous spiking, whereas the spontaneous spike activities of on-centeralpha-GC neighbors are not correlated. Without exception, those off-centeralpha-GCs showing synchronous spiking were found to be tracer coupled to both amacrine cells and neighboring off-centeralpha-GCs. In contrast, on-center alpha-GCs were never tracer coupled. Furthermore, whereas spikes initiated in an off-center alpha-GC with extrinsic current injection resulted in short-latency synchronized spiking in neighboring off-center alpha-GCs, this was never seen between on-center alpha-GCs. These results indicate that electrical coupling via gap junctions underlies the short-latency concerted spike activity of neighboring alpha-GCs.