The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse

Wade G. Regehr, Kerry R. Delaney, David W. Tank

Research output: Contribution to journalArticle

214 Scopus citations

Abstract

The mossy fiber synapse between dentate granule cells and CA3 pyramidal cells in the guinea pig hippocampus shows a robust short-term synaptic enhancement. We have simultaneously measured presynaptic residual free calcium ([Ca2+](i)) and postsynaptic field potentials at this synapse to examine the role of [Ca2+](i) in this enhancement. Single action potentials produced an increase in [Ca2+](i) of 10-50 nM that decayed to resting levels with a time constant of about 1 sec. Trains of action potentials produced larger [Ca2+](i) increases that returned more slowly to resting levels. Following the onset of moderate frequency stimulus trains (0.1-5 Hz), synaptic transmission and [Ca2+](i) both increased and eventually plateaued. During the steady-state phase a linear relationship between [Ca2+](i) and synaptic enhancement was observed. During the initial buildup, however, [Ca2+](i) rose more rapidly than synaptic enhancement. Similarly, during the decay phase immediately following termination of a stimulus train, [Ca2+](i) returned to prestimulus levels faster than synaptic enhancement. High concentrations of the calcium buffer EGTA in the presynaptic terminal slowed the buildup and decay of both [Ca2+](i) and synaptic enhancement produced by stimulus trains. Under these conditions, the time course of [Ca2+](i) and synaptic enhancement were well matched. This suggests that, despite the differences in kinetic rates observed for normal buffering conditions, increases in [Ca2+](i) play a causal role in short- term enhancement. An increase in [Ca2+](i) of 10-30 nM produced a twofold enhancement. We propose a simple kinetic model to explain these results. The model assumes that synaptic enhancement is controlled by a Ca-dependent first-order reaction. According to this scheme, a change in [Ca2+](i) alters neurotransmitter release, but the slow kinetics of the underlying reaction introduces a temporal filter, producing a delay in the change in synaptic enhancement.

Original languageEnglish (US)
Pages (from-to)523-537
Number of pages15
JournalJournal of Neuroscience
Volume14
Issue number2
DOIs
StatePublished - Feb 1994
Externally publishedYes

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

Keywords

  • calcium dynamics
  • fura-2
  • hippocampal mossy fibers
  • synaptic facilitation
  • transmitter release

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