Analysis of glutamatergic actions in the outer plexiform layer of the goldfish retina

Studies of synaptic transmission between photoreceptors and second order neurons in the retina have revealed that horizontal cells and depolarizing bipolar cells (DBCs) possess receptor/channel complexes with different pharmacological and conductance properties. Since these studies focused on postsynaptic cell type, paying less attention to the source of the synaptic input (i.e., rod or cone), less is known about the possible differences between synaptic transmission in the rod and cone pathways. In the present study, intracellular recordings from DBCs and horizontal cells were obtained in the isolated retina of the goldfish (Carassius auratus), using a dissection protocol which selectively eliminated either rod or cone input. Conductance measurements of DBCs which, under ordinary conditions, receive synaptic input from both rods and cones, demonstrated that the rod transmitter closed channels with an average reversal potential of {dollar}-{dollar}0.2 mV (SD: 11.3 mV), while the cone transmitter opened channels with an average reversal potential of {dollar}-{dollar}59 mV, (SD: 8.5 mV). The pharmacology of the two synapses differed as well. The glutamate analog 2-amino-4-phosphonobutyrate (ABP) mimicked the action of the rod transmitter, closing channels with an average reversal potential of {dollar}-{dollar}1.0 mV (SD: 11.1 mV), but was not an agonist for the cone transmitter. Glutamate, the putative transmitter for both rods and cones, produced no net conductance change, suggesting that it acted at both postsynaptic sites. Evidence for this idea was obtained with cesium, a potassium channel blocker which eliminated the channel-opening component of glutamate's action. With cesium in the microelectrode, glutamate closed channels with the same reversal potential ({dollar}-{dollar}0.5 mV, SD 18.5 mV) as the channels which were closed by APB, or the rod transmitter. A difference between the rod and cone synapses onto horizontal cells was detected as well. APB had no effect on rod-driven horizontal cells, bu antagonized the cone transmitter on cone-driven horizontal cells. The precise location and mechanism of APB antagonism remains in doubt. APB may act directly on the cones to antagonize transmitter release, or on a part of the postsynaptic receptor that is separate from the agonist binding site. These results demonstrate differences in the pharmacology and conductance mechanisms of the rod and cone synaptic pathways.