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The Journal of Neurophysiology Vol. 86 No. 3 September 2001, pp. 1139-1148
Copyright ©2001 by the American Physiological Society
Medical Research Council Centre for Synaptic Plasticity, Department of Anatomy, University of Bristol, Bristol BS8 1TD, United Kingdom
Kidd, Fleur L. and
John T. R. Isaac.
Kinetics and Activation of Postsynaptic Kainate Receptors at
Thalamocortical Synapses: Role of Glutamate Clearance. J. Neurophysiol. 86: 1139-1148, 2001. Kainate
(KA) receptor-mediated excitatory postsynaptic currents (EPSCs) exhibit
slow kinetics at the great majority of synapses. However, native or
heterologously expressed KA receptors exhibit rapid kinetics in
response to agonist application. One possibility to explain this
discrepancy is that KA receptors are extrasynaptic and sense glutamate
diffusing from the synaptic cleft. We investigated this by studying the
effect of three manipulations that change glutamate clearance on evoked
KA EPSCs at thalamocortical synapses. First, we used high-frequency
stimulation to increase extrasynaptic glutamate levels. This caused an
apparent increase in the relative contribution of the KA EPSC to
transmission and slowed the decay kinetics. However, scaling and
summing the EPSC evoked at low frequency reproduced this, demonstrating
that the effect was due to postsynaptic summation of KA EPSCs. Second,
we applied inhibitors of high-affinity glutamate transport. This caused
a depression in both AMPA and KA EPSC amplitude due to the activation
of a presynaptic glutamatergic autoreceptor. However, transport
inhibitors had no selective effect on the amplitude or kinetics of the
KA EPSC. Third, to increase glutamate clearance, we raised temperature during recordings. This shortened the decay of both the AMPA and KA
components and increased their amplitudes, but this effect was the same
for both. Therefore these data provide evidence against glutamate
diffusion out of the synaptic cleft as the mechanism for the slow
kinetics of KA EPSCs. Other possibilities such as interactions of KA
receptors with other proteins or novel properties of native synaptic
heteromeric receptors are required to explain the slow kinetics.
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