Distinct Ionotropic GABA Receptors Mediate Presynaptic and Postsynaptic Inhibition in Retinal Bipolar Cells

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Abstract
Ionotropic GABA receptors can mediate presynaptic and postsynaptic inhibition. We assessed the contributions of GABAA and GABAC receptors to inhibition at the dendrites and axon terminals of ferret retinal bipolar cells by recording currents evoked by focal application of GABA in the retinal slice. Currents elicited at the dendrites were mediated predominantly by GABAA receptors, whereas responses evoked at the terminals had GABAA and GABAC components. The ratio of GABAC to GABAA(GABAC:GABAA) was highest in rod bipolar cell terminals and variable among cone bipolars, but generally was lower in OFF than in ON classes. Our results also suggest that the GABAC:GABAA could influence the time course of responses. Currents evoked at the terminals decayed slowly in cell types for which the GABAC:GABAA was high, but decayed relatively rapidly in cells for which this ratio was low. Immunohistochemical studies corroborated our physiological results. GABAA β2/3 subunit immunoreactivity was intense in the outer and inner plexiform layers (OPL and IPL, respectively). GABAC ρ subunit labeling was weak in the OPL but strong in the IPL in which puncta colocalized with terminals of rod bipolars immunoreactive for protein kinase C and of cone bipolars immunoreactive for calbindin or recoverin. These data demonstrate that GABAA receptors mediate GABAergic inhibition on bipolar cell dendrites in the OPL, that GABAA and GABACreceptors mediate inhibition on axon terminals in the IPL, and that the GABAC:GABAA on the terminals may tune the response characteristics of the bipolar cell.