Rod Inputs Arrive at Horizontal Cell Somas in Mouse Retina Solely via Rod–Cone Coupling

Rod and cone photoreceptor cells selectively contact different compartments of axon-bearing retinal horizontal cells in the mammalian retina. Cones synapse exclusively on the soma whereas rods synapse exclusively on a large axon terminal compartment. The possibility that rod signals can travel down the axon from terminal to soma has been proposed as a means of producing spectrally opponent interactions between rods and cones, but there is conflicting data about whether this actually occurs. The spectral overlap between rods and cones in mouse makes it difficult to stimulate rod and cone pigments separately. We therefore used optogenetic techniques to analyze photoreceptor inputs into horizontal somas by selectively expressing channelrhodopsin in rods and/or cones. Optogenetic stimulation of rods and cones both evoked large fast inward currents in horizontal cell somas. Cone-driven responses were abolished by eliminating synaptic release in a cone-specific knock-out of the exocytotic calcium sensor, synaptotagmin 1 (Syt1). However, rod-driven responses in horizontal somas were unchanged after eliminating synaptic release from rods but abolished by eliminating release from both rods and cones. This suggests that release from cones is required for transmission of rod signals to horizontal cell somas. Rods and cones are coupled by Cx36 gap junctions, and we found that selective elimination of Cx36 from rods also abolished rod-driven optogenetic responses in horizontal cell somas. Together, these results show that rod signals reach the somas of B-type horizontal cells exclusively via gap junctions with cones and not by transmission down the axon from the axon terminal.