The Journal of Neuroscience, August 15, 1999, 19(16):6755-6766
Active Role of Glutamate Uptake in the Synaptic Transmission from
Retinal Nonspiking Neurons
Ko
Matsui,
Nobutake
Hosoi, and
Masao
Tachibana
Department of Psychology, Graduate School of Humanities and
Sociology, The University of Tokyo, Tokyo 113-0033, Japan
We examined the role of glutamate uptake in the synaptic
transmission of graded responses from newt retinal bipolar cells (BCs)
to ganglion layer cells (GLCs). In dissociated Müller cells (retinal glia), glutamate evoked an uptake current that was effectively inhibited by
L-trans-pyrrolidine-2,4-dicarboxylic acid
(PDC). PDC had no effect on the non-NMDA receptors of dissociated
spiking neurons. In the retinal slice preparation, dual whole-cell
recordings were performed from a pair of BC and GLC. A depolarizing
pulse applied to a BC activated the Ca2+ current
(ICa) in the BC and evoked an
EPSC in the GLC. Application of PDC prolonged both non-NMDA and NMDA
receptor-mediated components of the evoked EPSC but changed neither the
amplitude nor time course of ICa. When the
slice preparation was superfused with a solution containing glutamate
but not PDC, the evoked EPSC decreased in amplitude without changing
the time course, suggesting that the prolongation of the evoked EPSC is
not attributable to a simple increase in ambient glutamate
concentration after inhibition of glutamate uptake. Because PDC did not
affect the amplitude, time course, or frequency of spontaneous
EPSCs, it is unlikely that PDC modified presynaptic and/or postsynaptic
mechanisms. These results indicate that inhibition of glutamate uptake
slows the clearance of glutamate accumulated in the synaptic cleft by
multiple quantal release and prolongs the evoked EPSC. The role of
glutamate uptake at synapses in the inner retina is not only to
maintain the extracellular glutamate concentration at a low level but
also to terminate the light-evoked EPSCs rapidly.
Key words:
retina; bipolar cell; ganglion cell; Müller cell; synaptic transmission; glutamate; uptake; transporter; non-NMDA
receptor; NMDA receptor; EPSC; spontaneous EPSC
Copyright © 1999 Society for Neuroscience 0270-6474/99/19166755-12$05.00/0
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