Relationship Between Amacrine-Ganglion Cell Coupling and Concerted Spike Activity of Ganglion Cells

Abstract

Abstract: : Purpose: To determine the role of amacrine-ganglion cell coupling in the concerted spike activity of ganglion cells in the rabbit retina. Methods: Dual, simultaneous extracellular recordings were obtained from ganglion cells visualized with transcleral infrared illumination in a flattened retinal-scleral preparation of the rabbit. Cells were subsequently injected intracellularly with Neurobiotin for morphological identification. Results: We showed previously that off-center alpha ganglion cells are tracer coupled to neighboring alpha cells as well as to at least 2 classes of amacrine cell, whereas on-center alpha cells are uncoupled. Further, off-center alpha cells show concerted activity consisting of two peaks in the cross-correlogram with latencies of 2.5 msec, whereas on-center alpha cells show no correlation of spontaneous activity and a broad (50 msec) light-evoked cross-correlogram with a single peak at time zero. These data suggest that the dual peaks in the cross-correlogram of off-center alpha cells reflect reciprocal innervation via electrical coupling. However, the exact role played by ganglion-ganglion or ganglion-amacrine coupling in alpha cell spike synchrony remains unclear. To more clearly define the role of amacrine-ganglion cell coupling in the synchronous activity of neighboring ganglion cells, we studied the concerted firing of a unique class of on-center ganglion cell which shows heterologous coupling to wide-field amacrine cells, but no homologous coupling. These cells appear to fall into the morphological delta cell class and they showed physiological properties identifying them as on-center direction selective (DS) ganglion cells. These cells showed a very transient response to full-field illumination and were keenly sensitive to the direction of slowly moving stimuli. Cross-correlograms of both light-evoked and spontaneous spike activity showed a single peak at time zero and an intermediate width of 15-20 msec. Conclusions: Our results suggest that amacrine-ganglion cell coupling underlies the concerted spiking of neighboring on-center DS ganglion cells, but this synchrony is distinct from that of alpha cells. In this scheme, excitation from amacrine cells arriving via gap junctions appears to synchronize both the spontaneous and light-evoked activity of postsynaptic DS ganglion cells. Our results also suggest that reciprocal correlations found for off-center alpha cells reflect ganglion-ganglion cell coupling.

Keywords: ganglion cells • gap junctions/coupling • retinal connections, networks, circuitry