Presynaptic kainate receptors at hippocampal mossy fiber synapses

  • Schmitz D
  • Mellor J
  • Frerking M
 et al. 
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Abstract

Hippocampal mossy fibers, which are the axons of dentate
granule cells, form powerful excitatory synapses onto the proximal
dendrites of CA3 pyramidal cells. It has long been known that
high-affinity binding sites for kainate, a glutamate receptor agonist,
are present on mossy fibers. Here we summarize recent experiments on
the role of these presynaptic kainate receptors (KARs). Application of
kainate has a direct effect on the amplitude of the extracellularly
recorded fiber volley, with an enhancement by low concentrations and a
depression by high concentrations. These effects are mediated by KARs,
because they persist in the presence of the
α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid
receptor-selective antagonist GYKI 53655, but are blocked by the
α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid/KAR antagonist
6-cyano-7-nitroquinoxaline-2,3-dione and the KAR antagonist SYM2081.
The effects on the fiber volley are most likely caused by a
depolarization of the fibers via the known ionotropic actions of
KARs, because application of potassium mimics the effects. In addition
to these effects on fiber excitability, low concentrations of kainate
enhance transmitter release, whereas high concentrations depress
transmitter release. Importantly, the synaptic release of glutamate
from mossy fibers also activates these presynaptic KARs, causing an
enhancement of the fiber volley and a facilitation of release that
lasts for many seconds. This positive feedback contributes to the
dramatic frequency facilitation that is characteristic of mossy fiber
synapses. It will be interesting to determine how widespread
facilitatory presynaptic KARs are at other synapses in the central
nervous system.

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Authors

  • Dietmar Schmitz

  • Jack Mellor

  • Matthew Frerking

  • Roger A. Nicoll

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