Synaptic depression and the kinetics of exocytosis in retinal bipolar cells

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 similar to 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-consta nt of exocytosis fell by a factor of 4-10. Thus, synaptic depression was ca used by a reduced sensitivity to Ca2+ influx, as well as simple depletion o f the RRP. In the resting state, the rate of exocytosis varied with the amp litude of the Ca2+ current raised to the power of 2. In the depressed state , the sensitivity to Ca2+ influx was reduced approximately fourfold. The in itial phase of exocytosis accelerated e-fold for every 2.1 mV depolarizatio n over the physiological range and averaged 120 sec(-1) at -25 mV. The synapse of depolarizing bipolar cells therefore responds to a step depo larization in a manner similar to a high-pass filter. This transformation a ppears 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. Th ese results suggest that the ribbon synapse of depolarizing bipolar cells m ay be a site of adaptation in the retina.