Synaptic Depression and the Kinetics of Exocytosis in Retinal Bipolar Cells

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Abstract
The capacitance technique was used to investigate exocytosis at the ribbon synapse of depolarizing bipolar cells from the goldfish retina. When the Ca2+ current was activated strongly, the rapidly releasable pool of vesicles (RRP) was released with a single rate-constant of ∼300–500 sec−1. However, when the Ca2+ current was activated weakly by depolarization in the physiological range (−45 to −25 mV), exocytosis from the RRP occurred in two phases. After the release of 20% or more of the RRP, the rate-constant of exocytosis fell by a factor of 4–10. Thus, synaptic depression was caused by a reduced sensitivity to Ca2+ influx, as well as simple depletion of the RRP. In the resting state, the rate of exocytosis varied with the amplitude of the Ca2+ current raised to the power of 2. In the depressed state, the sensitivity to Ca2+ influx was reduced approximately fourfold. The initial phase of exocytosis accelerated e-fold for every 2.1 mV depolarization over the physiological range and averaged 120 sec−1 at −25 mV. The synapse of depolarizing bipolar cells therefore responds to a step depolarization in a manner similar to a high-pass filter. This transformation appears to be determined by the presence of rapidly releasable vesicles with differing sensitivities to Ca2+ influx. This might occur if vesicles were docked to the plasma membrane at different distances from Ca2+ channels. These results suggest that the ribbon synapse of depolarizing bipolar cells may be a site of adaptation in the retina.