L-type calcium channels in the photoreceptor ribbon synapse: localization and role in plasticity

J Comp Neurol. 1999 Dec 6;415(1):1-16.

Abstract

Calcium (Ca(2+)) influx through voltage-gated Ca(2+)channels stimulates a variety of neural activities, including process outgrowth, neurotransmission, and synaptic plasticity. In general, L-type channels control Ca(2+) influx into the soma and dendrites, whereas other Ca(2+) channel types control presynaptic activities. Neurons that make ribbon synapses, however, are among a select group of nerve cells whose presynaptic Ca(2+)-dependent secretion is linked to L-type channels. Recently, photoreceptor ribbon synapses have been shown to be capable of dramatic structural remodeling and neuritic outgrowth. Here, we have examined 1) the distribution of dihydropyridine (DHP)-sensitive (L-type) Ca(2+) channels in photoreceptor presynaptic structures and 2) the role of these channels in axonal plasticity and process outgrowth in culture. Using anti-alpha(1C) and the fluorescent dihydropyridine, (-)-DM-BODIPY DHP, L-type channels were localized in the outer plexiform layer of retinal sections and in presynaptic terminals of freshly isolated photoreceptors. In the rod terminal, dense patches of label were present; their distribution and number matched that of synaptic ribbons. After 1-7 days in vitro, punctate alpha(1C) staining occurred along newly formed neurites and presynaptic varicosities. Functional channels were present throughout the culture period, as determined by fura-2 imaging. Channel blockage by nicardipine, a DHP antagonist, inhibited axonal remodeling. Specifically, it prevented axon retraction and lamellipodium formation, reduced neurite growth, and produced long, thin processes on some, primarily cone, photoreceptors. L-type Ca(2+) channel activity, therefore, not only stimulates neurotransmission but contributes to presynaptic structural plasticity at the ribbon synapse.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Ambystoma
  • Animals
  • Calcium Channel Blockers / pharmacology
  • Calcium Channels, L-Type / physiology*
  • Cells, Cultured
  • In Vitro Techniques
  • Microscopy, Confocal
  • Neurites / drug effects
  • Neurites / physiology
  • Neuronal Plasticity / physiology*
  • Nicardipine / pharmacology
  • Photoreceptor Cells, Vertebrate / cytology
  • Photoreceptor Cells, Vertebrate / drug effects
  • Photoreceptor Cells, Vertebrate / physiology*
  • Rats
  • Rats, Sprague-Dawley
  • Retina / cytology
  • Retina / physiology
  • Retinal Cone Photoreceptor Cells / cytology
  • Retinal Cone Photoreceptor Cells / drug effects
  • Retinal Cone Photoreceptor Cells / physiology
  • Retinal Rod Photoreceptor Cells / cytology
  • Retinal Rod Photoreceptor Cells / drug effects
  • Retinal Rod Photoreceptor Cells / physiology
  • Synapses / physiology*

Substances

  • Calcium Channel Blockers
  • Calcium Channels, L-Type
  • Nicardipine