Presynaptic and postsynaptic mechanisms underlie paired pulse depression at single GABAergic boutons in rat collicular cultures

Sergei Kirischuk, John D. Clements, Rosemarie Grantyn*

*Corresponding author for this work

    Research output: Contribution to journalReview articlepeer-review

    78 Citations (Scopus)

    Abstract

    Paired pulse depression (PPD) is a common form of short-term synaptic plasticity. The aim of this study was to characterise PPD at the level of a single inhibitory bouton. Low-density collicular cultures were loaded with the Ca2+ indicator Oregon Green-1, active boutons were stained with RH414, and action potentials were blocked with TTX. Evoked IPSCs (eIPSCs) and presynaptic Ca2+ transients were recorded in response to direct presynaptic depolarisation of an individual bouton. The single bouton eIPSCs had a low failure rate (< 0.1), large average quantal content (3-6) and slow decay (τ1 = 15 ms, τ2 = 81 ms). The PPD of eIPSCs had two distinct components: PPDfast and PPDslow (τ = 86 ms and 2 s). PPDslow showed no dependence on extracellular Ca2+ concentration, or on the first eIPSC's failure rate or amplitude. Most probably, it reflects a release-independent inhibition of exocytosis. PPDffast was only observed in normal or elevated Ca2+. It decreased with the failure rate and increased with the amplitude of the first eIPSC. It coincided with paired pulse depression of the presynaptic Ca2+ transients (τ = 120 ms). The decay of the latter was accelerated by EGTA, which also reduced PPDfast. Therefore, a suppressive effect of residual presynaptic Ca2+ on subsequent Ca2+ influx is considered the most likely cause of PPDfast, PPDfast may also have a postsynaptic component, because exposure to a low-affinity GABAA receptor antagonist (TPMPA; 300 μM) counteracted PPDfast and asynchronous IPSC amplitudes were depressed for a short interval following an eIPSC. Thus, at these synapses, PPD is produced by at least two release-independent presynaptic mechanisms and one release-dependent postsynaptic mechanism.

    Original languageEnglish
    Pages (from-to)99-116
    Number of pages18
    JournalJournal of Physiology
    Volume543
    Issue number1
    DOIs
    Publication statusPublished - 15 Aug 2002

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