Cone bipolar cells as interneurons in the rod, pathway of the rabbit retina

Abstract

In the mammalian retina, rod signals are transmitted by rod bipolars to the narrow-field, bistratified (AII) amacrine cell. This neuron, in turn, makes gap junctions with the axonal arborization of cone bipolar cells that reside in the vitreal half (sublamina b) of the inner plexiform layer (IPL). After examining rod bipolars and AII amacrines in the rabbit retina, we have now reconstructed from electron micrographs of continuous series of thin sections the synaptic connections of the axonal arborizations of cone bipolar cells that make the highest number of gap junctions with AII amacrines. These axonal arborizations were narrowly confined to stratum 4 (S4) of the IPL and made ribbon synapses to dyads of postsynaptic dendrites that belonged to either ganglion or amacrine cells. In the population of postsynaptic processes, 30% were ganglion cell dendrites. These dendrites were probably originating, at least in part, from on-center ganglion cells because their course was confined to sublamina b of the IPL. Of the remaining postsynaptic processes, 51.7% belonged to amacrine cells and 18.3% were not identified. Among the postsynaptic amacrine cell processes, 33.3% returned a reciprocal synapse onto the cone bipolar endings. These reciprocal synapses represented 21.3% of the total input onto the axonal arborizations, the remaining fraction (78.7%) arising from a heterogeneous population of amacrine dendrites that were purely presynaptic to the cone bipolars endings. Pre- and postsynaptic amacrines were part of several distinct microcircuits which suggest complex local processing of both rod and cone signals. Thus, the cone bipolars that make gap junctions with AII amacrines in sublamina b of the rabbit IPL exhibit a substantial output onto ganglion cells. This fact, in conjunction with our previous observations that in this sublamina ganglion cells receive negligible input from rod bipolars and AII amacrines, demonstrates that in the rabbit cone bipolars represent a necessary link in the pathway followed by rod signals to enter on-center ganglion cells. Thus, rod and cone signals ultimately share the same integrating mechanisms and converge onto the same set of ganglion cells.