Electrical resonance and Ca2+ influx in the synaptic terminal of depolarizing bipolar cells from the goldfish retina

J Physiol. 1997 Dec 15;505 ( Pt 3)(Pt 3):571-84. doi: 10.1111/j.1469-7793.1997.571ba.x.


1. Whole-cell recordings and fura-2 measurements of cytoplasmic [Ca2+] were made in depolarizing bipolar cells isolated from the retinae of goldfish. The aim was to study the voltage signal that regulates Ca2+ influx in the synaptic terminal. 2. The current-voltage relation was linear up to about -44 mV. At this threshold, the injection of 1 pA of current triggered a maintained 'all-or-none' depolarization to a plateau of -34 mV, associated with a decrease in input resistance and a damped voltage oscillation with a frequency of 50-70 Hz and initial amplitude of 4-10 mV. A second frequency component of 5-10 Hz was often observed. In a minority of cells the response to current injection was transient, recovering with an undershoot. 3. Unstimulated bipolar cells generated similar voltage signals, driven by current entering the cell through a non-specific cation conductance that continuously varied in amplitude. 4. The threshold for activation of the Ca2+ current was -43 mV and free [Ca2+]i in the synaptic terminal rose during a depolarizing response. Simultaneous measurements of the fluorescence associated with the membrane marker FM1-43 demonstrated that these Ca2+ signals stimulated exocytosis. Regenerative depolarizations and associated rises in [Ca2+]i were blocked by inhibiting L-type Ca2+ channels with 30 microM nifedipine. 5. Depolarization beyond -40 mV also elicited an outwardly rectifying K+ current. Blocking this current by replacing external Ca2+ with Ba2+ caused the voltage reached during a depolarizing response to increase to +10 mV. 6. The majority of the K+ current was blocked by 100 nM charybdotoxin, indicating that it was carried by large-conductance Ca2+ activated K+ channels. A transient voltage-gated K+ current remained, which began to activate at -40 mV. High-frequency voltage oscillations were blocked by 100 nM charybdotoxin, but low-frequency oscillations remained. 7. These results indicate that the voltage response of depolarizing bipolar cells is shaped by L-type Ca2+ channels, Ca(2+)-activated K+ channels and voltage-dependent K+ channels. This combination of conductances regulates Ca2+ influx into the synaptic terminal and confers an electrical resonance on the bipolar cell.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium / metabolism*
  • Calcium Channels / physiology
  • Electric Conductivity
  • Goldfish
  • In Vitro Techniques
  • Ion Channel Gating
  • Large-Conductance Calcium-Activated Potassium Channels
  • Membrane Potentials / physiology
  • Patch-Clamp Techniques
  • Potassium Channels / physiology
  • Potassium Channels, Calcium-Activated*
  • Presynaptic Terminals / metabolism
  • Presynaptic Terminals / physiology*
  • Retina / cytology
  • Retina / metabolism
  • Retina / physiology*


  • Calcium Channels
  • Large-Conductance Calcium-Activated Potassium Channels
  • Potassium Channels
  • Potassium Channels, Calcium-Activated
  • Calcium