Rod inputs arrive at horizontal cell somas in mouse retina solely via rod-cone coupling

Abstract

Rod and cone photoreceptor cells selectively contact different compartments of axon-bearing retinal horizontal cells in the 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 to allow spectrally opponent interactions between rods and cones, but there is conflicting data about whether this actually occurs. Because of spectral overlap between rod and cone visual pigments in mouse, we analyzed photoreceptor inputs into horizontal somata by selectively expressing channelrhodopsin in rods and/or cones. Optogenetic stimulation of rods and cones both evoked large fast inward currents in horizontal cell somata. Cone-driven responses were abolished by eliminating synaptic release in a cone-specific knockout of the exocytotic calcium sensor, synaptotagmin 1. However, rod-driven responses in horizontal somata were unchanged after eliminating synaptic release from rods but abolished by eliminating release from both rods and cones. This suggests that cones transmit rod signals that arrive via rod-cone gap junctions. Consistent with this, eliminating Cx36 gap junctions between rods and cones also abolished rod-driven optogenetic responses in horizontal cell somata. These results show that rod signals reach the somas of B-type horizontal cells exclusively via gap junctions with cones and not by traveling down the axon from the axon terminal. SignificanceRods and cones contact different compartments of retinal horizontal cells: cones contact the soma whereas rods contact a large axon terminal. Cone signals can travel through the axon from soma to terminal, but it is not clear whether rod signals travel the other direction. This latter pathway has been proposed to mediate opponent interactions between rods and cones that could shape vision in dim lights. However, our results show that rod signals cannot travel from axon terminal to soma, but mix with cone signals via gap junctions between the two cell types. This finding limits mechanisms for explaining opponent rod-cone interactions in color and contrast perception.