New insights into short-term synaptic facilitation at the frog neuromuscular junction

J Neurophysiol. 2015 Jan 1;113(1):71-87. doi: 10.1152/jn.00198.2014. Epub 2014 Sep 10.

Abstract

Short-term synaptic facilitation occurs during high-frequency stimulation, is known to be dependent on presynaptic calcium ions, and persists for tens of milliseconds after a presynaptic action potential. We have used the frog neuromuscular junction as a model synapse for both experimental and computer simulation studies aimed at testing various mechanistic hypotheses proposed to underlie short-term synaptic facilitation. Building off our recently reported excess-calcium-binding-site model of synaptic vesicle release at the frog neuromuscular junction (Dittrich M, Pattillo JM, King JD, Cho S, Stiles JR, Meriney SD. Biophys J 104: 2751-2763, 2013), we have investigated several mechanisms of short-term facilitation at the frog neuromuscular junction. Our studies place constraints on previously proposed facilitation mechanisms and conclude that the presence of a second class of calcium sensor proteins distinct from synaptotagmin can explain known properties of facilitation observed at the frog neuromuscular junction. We were further able to identify a novel facilitation mechanism, which relied on the persistent binding of calcium-bound synaptotagmin molecules to lipids of the presynaptic membrane. In a real physiological context, both mechanisms identified in our study (and perhaps others) may act simultaneously to cause the experimentally observed facilitation. In summary, using a combination of computer simulations and physiological recordings, we have developed a stochastic computer model of synaptic transmission at the frog neuromuscular junction, which sheds light on the facilitation mechanisms in this model synapse.

Keywords: MCell; frog neuromuscular junction; short-term synaptic plasticity; stochastic simulation; synaptic vesicle release.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Calcium / metabolism
  • Calcium Channels, N-Type / metabolism
  • Calcium-Binding Proteins / metabolism
  • Computer Simulation
  • Kinetics
  • Membrane Lipids / metabolism
  • Microelectrodes
  • Models, Neurological
  • Neuromuscular Junction / physiology*
  • Neuronal Plasticity / physiology*
  • Presynaptic Terminals / physiology
  • Rana pipiens
  • Stochastic Processes
  • Synaptic Transmission / physiology*
  • Synaptic Vesicles / physiology
  • Tissue Culture Techniques

Substances

  • Calcium Channels, N-Type
  • Calcium-Binding Proteins
  • Membrane Lipids
  • Calcium