gamma-Aminobutyric acid exerts a local inhibitory action on the axon terminal of bipolar cells: evidence for negative feedback from amacrine cells.

It is well-established morphologically that bipolar cells, the second-order neurons in the vertebrate retina, make reciprocal synapses with amacrine cells in the inner plexiform layer. However, neither the property nor the physiological function of the feedback synapse is understood. Autoradiographic and immunohistochemical studies suggest the presence of gamma-aminobutyric acid (GABA)-ergic amacrine cells, and therefore the bipolar cells are thought to receive GABAergic inputs from amacrine cells. This possibility was investigated in the present study, in which we used solitary bipolar cells dissociated from the goldfish retina enzymatically. Dissociated solitary bipolar cells showed a large variety in morphology. In the present study, we selected the bipolar cells with a huge bulbous axon terminal. Bipolar cells of this subtype were identical in morphology to the on-center cells with rod-dominant inputs as revealed in earlier studies by intracellular staining. Membrane currents were measured under voltage clamp with a patch pipette in the whole cell configuration. In some experiments, GABA-sensitive membrane was excised as an outside-out patch from the axon terminal bulb of solitary bipolar cells. All cells of this type responded to GABA. The highest sensitivity was located at the axon terminal. The minimal effective dose was on the order of 10(-7) M. GABA increased the chloride conductance and evoked a membrane hyperpolarization. Partial desensitization was observed during the application of GABA. The bipolar cells had GABA type A receptors. These results are consistent with the idea that the rod-dominant on-center bipolar cells receive negative feedback inputs from GABAergic amacrine cells.