Glutamate receptors at rod bipolar ribbon synapses in the rabbit retina

In the mammalian retina, maximum sensitivity is achieved in the rod pathway, which serves dark-adapted vision. Rod bipolar cells carry the highly convergent rod input and make ribbon synapses with two postsynaptic elements in the inner retina. One postsynaptic neuron is the AII amacrine cell, which feeds the rod signal into the cone pathways. The other postsynaptic element is either an S1 or S2 amacrine cell. These two wide-field GABA amacrine cells both make reciprocal synapses with rod bipolar terminals but their individual roles are unknown. AII and S1/S2 dendrites come in close together and form a dyad opposing the presynaptic ribbon, which is the site of glutamate release. Therefore, two postsynaptic neurons sense the very same neurotransmitter yet serve different functions in the rod pathway. This functional diversity could be derived partly from the expression of different glutamate receptors on each postsynaptic element. In this study, we labeled all pre- and postsynaptic combinations and a signal-averaging method was developed to locate glutamate receptor subunits. In summary, GluR2/3 and GluR4 are expressed by AII amacrine cells but not by S1/S2 amacrine cells. In contrast, the orphan subunit delta1/2 is exclusively located on S1 varicosities but not on AII or S2 amacrine cells. These results confirm the prediction of divergence mediated by different glutamate receptors at the rod bipolar dyad. Each different amacrine cell type appears to express specific glutamate receptors. Finally, the differential expression of glutamate receptors by S1 and S2 may partly explain the need for two wide-field GABA amacrine cells with the same feedback connections to rod bipolar terminals.