Visual Stimuli Evoked Action Potentials Trigger Rapidly Propagating Dendritic Calcium Transients in the Frog Optic Tectum Layer 6 Neurons

PLoS One. 2015 Sep 28;10(9):e0139472. doi: 10.1371/journal.pone.0139472. eCollection 2015.

Abstract

The superior colliculus in mammals or the optic tectum in amphibians is a major visual information processing center responsible for generation of orientating responses such as saccades in monkeys or prey catching avoidance behavior in frogs. The conserved structure function of the superior colliculus the optic tectum across distant species such as frogs, birds monkeys permits to draw rather general conclusions after studying a single species. We chose the frog optic tectum because we are able to perform whole-cell voltage-clamp recordings fluorescence imaging of tectal neurons while they respond to a visual stimulus. In the optic tectum of amphibians most visual information is processed by pear-shaped neurons possessing long dendritic branches, which receive the majority of synapses originating from the retinal ganglion cells. Since the first step of the retinal input integration is performed on these dendrites, it is important to know whether this integration is enhanced by active dendritic properties. We demonstrate that rapid calcium transients coinciding with the visual stimulus evoked action potentials in the somatic recordings can be readily detected up to the fine branches of these dendrites. These transients were blocked by calcium channel blockers nifedipine CdCl2 indicating that calcium entered dendrites via voltage-activated L-type calcium channels. The high speed of calcium transient propagation, >300 μm in <10 ms, is consistent with the notion that action potentials, actively propagating along dendrites, open voltage-gated L-type calcium channels causing rapid calcium concentration transients in the dendrites. We conclude that such activation by somatic action potentials of the dendritic voltage gated calcium channels in the close vicinity to the synapses formed by axons of the retinal ganglion cells may facilitate visual information processing in the principal neurons of the frog optic tectum.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials* / drug effects
  • Animals
  • Calcium / metabolism*
  • Calcium Channel Blockers / pharmacology
  • Calcium Channels, L-Type / metabolism
  • Dendrites / drug effects
  • Dendrites / metabolism*
  • Nimodipine / pharmacology
  • Patch-Clamp Techniques
  • Photic Stimulation*
  • Ranidae / physiology*
  • Superior Colliculi / drug effects
  • Superior Colliculi / physiology*

Substances

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

Grants and funding

This work was supported by the Lithuanian Research Council grant No. VP1-3.1-ŠMM-07-K-02-059 to TT that is a part of the Global Grant measure of the European Social Fund.