Differential induction of long-lasting potentiation of inhibitory postsynaptic potentials by theta patterned stimulation versus 100-Hz tetanization in hippocampal pyramidal cells in vitro

Y. Perez, C. A. Chapman, G. Woodhall, R. Robitaille, J. C. Lacaille*

*Corresponding author for this work

Research output: Contribution to journalArticle

Abstract

Tetanization of Schaffer collaterals, which induces long-term potentiation of excitatory transmission in the hippocampus of the rat, also affects local inhibitory circuits. Mechanisms controlling plasticity of early and late components of inhibitory postsynaptic potentials in CA1 pyramidal cells were studied using intracellular recordings and Ca2+ imaging in rat hippocampal slices. High-frequency stimulation (100 Hz/s) of Schaffer collaterals resulted in no change in the mean amplitude of early or late inhibitory postsynaptic potentials 30 min post-tetanus. However, intracellular injection of the Ca2+ chelator 1,2-bis(2-aminophenoxy)ethane- N,N,N',N'-tetra-acetate unmasked a significant increase in mean amplitude of both inhibitory postsynaptic potentials 30 min post-tetanus and the induction of this potentiation was blocked by the N-methyl-D-aspartate receptor antagonist (±)-2-amino-5-phosphopentanoic acid. In contrast to high- frequency tetanization, 'theta-burst' stimulation in normal medium resulted in a significant potentiation of the mean amplitude of both early and late inhibitory postsynaptic potentials 30 min post-tetanus. This potentiation was blocked by the N-methyl-D-aspartate receptor antagonist. The more physiological tetanization pattern, which mimics the endogenous theta rhythm, therefore resulted in an N-methyl-D-aspartate, dependent increase in inhibition 30 min post-tetanus. Calcium imaging during whole-cell recordings from pyramidal cells revealed differences in the Ca2+ signal associated with high-frequency and theta-burst stimulations. During theta-burst stimulation of Schaffer collaterals, the mean time to peak of Ca2+ signals was significantly longer, and the mean peak amplitude and area under the Ca2+ response were larger than during high-frequency stimulation. These results indicate that tetanization induces long-lasting synaptic plasticity in hippocampal inhibitory circuits. This plasticity involves an interaction between a Ca2+-mediated postsynaptic depression and an N-methyl-D- aspartate-mediated potentiation of GABA(A) and GABA(B) inhibition, and these processes are differentially sensitive to tetanization parameters.

Original languageEnglish
Pages (from-to)747-757
Number of pages11
JournalNeuroscience
Volume90
Issue number3
DOIs
Publication statusPublished - 1 Jan 1999

Keywords

  • GABA
  • Interneuron
  • Plasticity
  • Rat
  • Theta

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