Different roles of ribbon-associated and ribbon-free active zones in retinal bipolar cells

Nat Neurosci. 2007 Oct;10(10):1268-76. doi: 10.1038/nn1963. Epub 2007 Sep 9.


Synaptic ribbons with a halo of synaptic vesicles are seen at the active zones of sensory neurons that release transmitter tonically. Thus, ribbons are assumed to be a prerequisite for sustained exocytosis. By applying total internal reflection fluorescence microscopy to goldfish retinal bipolar cell terminals, we visualized Ca2+ entry sites, ribbons, and vesicle fusion events. Here we show that the main Ca2+ entry sites were located at ribbons, and that activation of the Ca2+ current induced immediate and delayed vesicle fusion events at ribbon-associated and ribbon-free 'hot spots', respectively. The activation of protein kinase C (PKC) specifically potentiated vesicle fusion at ribbon-free sites. Electron microscopy showed that PKC activation selectively increased the number of docked vesicles at ribbon-free sites, which faced neuronal processes with the postsynaptic density. Retinal bipolar cells have both ribbon-associated and ribbon-free active zones in their terminals and might send functionally distinct signals through ribbon-associated and ribbon-free synapses to postsynaptic neurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analysis of Variance
  • Animals
  • Bicuculline / pharmacology
  • Calcium / metabolism
  • Dose-Response Relationship, Radiation
  • Electric Stimulation
  • Enzyme Inhibitors / pharmacology
  • GABA Antagonists / pharmacology
  • Goldfish
  • Imaging, Three-Dimensional / methods
  • Membrane Potentials / physiology
  • Membrane Potentials / radiation effects
  • Microscopy, Electron / methods
  • Patch-Clamp Techniques
  • Protein Kinase C-alpha / metabolism
  • Retina / cytology*
  • Retinal Bipolar Cells / cytology*
  • Synapses / classification
  • Synapses / drug effects
  • Synapses / ultrastructure*
  • Synaptic Vesicles / ultrastructure*
  • Tetradecanoylphorbol Acetate / pharmacology
  • Time Factors


  • Enzyme Inhibitors
  • GABA Antagonists
  • Protein Kinase C-alpha
  • Tetradecanoylphorbol Acetate
  • Calcium
  • Bicuculline