Abstract
The capacitance technique was used to investigate exocytosis at the ribbon synapse of depolarizing bipolar cells from the goldfish retina. When the Ca(2+) current was activated strongly, the rapidly releasable pool of vesicles (RRP) was released with a single rate-constant of approximately 300-500 sec(-1). However, when the Ca(2+) 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 Ca(2+) influx, as well as simple depletion of the RRP. In the resting state, the rate of exocytosis varied with the amplitude of the Ca(2+) current raised to the power of 2. In the depressed state, the sensitivity to Ca(2+) 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 Ca(2+) influx. This might occur if vesicles were docked to the plasma membrane at different distances from Ca(2+) channels. These results suggest that the ribbon synapse of depolarizing bipolar cells may be a site of adaptation in the retina.