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Retinal bipolar cells are known to form a complex, interconnecting network through electrical synapses that are either heterologous (with amacrine cells) or homologous (with other bipolar cells). These electrical synapses can be functionally as important as chemical synapses because their distinct properties provide a different character for the network. Much less is known, however, about electrical synapses in retinal bipolar cells than about chemical synapses. Here we report the molecular basis for electrical synapses in retinal bipolar cells, particularly ON cone bipolar cells. We have found variable connexin 36 (cx36) expression in different types of ON cone bipolar cells: cx36 message was found in some, but not all, ON cone bipolar cells (4 of 14 cells). In one specific type of ON cone bipolar cell (BPGus-GFP), however, cx36 was detected in 17 of 19 cells. Moreover, we have located cx36 puncta at the axonal terminals of BPGus-GFP cells, and we have found that these BPGus-GFP-associated cx36 puncta always colocalized with AII amacrine cell processes. Molecular and immunocytochemical evidence obtained in this study also shows that connexin 45 (cx45) is not present in BPGus-GFP cells. Taken together, our results suggest that connexins are expressed in bipolar cells in a neuronal subtype-specific manner and that cx36/cx36 gap junctions form the heterologous electrical synapses between AII amacrine cells and BPGus-GFP cells. Our findings imply that visual information can be differently processed by distinct subtypes of ON cone bipolar cells via electrical synapses.

Electrical synapses in retinal ON cone bipolar cells: Subtype-specific expression of connexins