Modulation of Ca(2+)-activated K+ currents and Ca(2+)-dependent action potentials by exocytosis in goldfish bipolar cell terminals

J Physiol. 2006 May 1;572(Pt 3):747-62. doi: 10.1113/jphysiol.2006.105205.


Retinal bipolar cells convey light-evoked potentials from photoreceptors to ganglion cells and mediate the initial stages of visual signal processing. They do not fire Na(+)-dependent action potentials (APs) but the Mb1 class of goldfish bipolar cell exhibits Ca(2+)-dependent APs and regenerative potentials that originate in the axon terminal. I have examined the properties of Ca(2+)-dependent APs in isolated bipolar-cell terminals in goldfish retinal slices. All recorded terminals fired spontaneous or evoked APs at frequencies of up to 15 Hz. When an AP waveform was used as a voltage stimulus, exocytosis was evoked by single APs, maintained throughout AP trains and modulated by AP frequency. Furthermore, feedback inhibition of the Ca2+ current (I(Ca)) by released vesicular protons reduced depression of exocytosis during AP trains. In the absence of K+ current inhibition, step depolarizations and AP waveforms evoked a rapidly activated outward current that was dependent on Ca2+ influx I(K(Ca). I therefore investigated whether proton-mediated feedback inhibition of I(Ca) affected the activation of I(K(Ca)). A transient inhibition of I(K(Ca)) was observed that was dependent on exocytosis, blocked by high-pH extracellular buffer, of similar magnitude to inhibition of I(Ca) but occurred with a delay of 2.7 ms. In addition, the amplitude of APs evoked under current clamp was inhibited by the action of vesicular protons released by the APs. Protons released via exocytosis may therefore be a significant modulator of Ca(2+)-dependent currents and regenerative potentials in bipolar-cell terminals.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology*
  • Adaptation, Physiological / physiology
  • Animals
  • Calcium / metabolism*
  • Calcium Signaling / physiology
  • Cells, Cultured
  • Exocytosis / physiology*
  • Goldfish
  • Ion Channel Gating / physiology*
  • Potassium Channels, Calcium-Activated / metabolism*
  • Presynaptic Terminals / physiology*
  • Retinal Bipolar Cells / physiology*


  • Potassium Channels, Calcium-Activated
  • Calcium