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The Journal of Neurophysiology Vol. 79 No. 1 January 1998,
pp. 190-196
Copyright ©1998 The American Physiological Society
1 Department of Molecular and Cell Biology, Division of Neurobiology, University of California at Berkeley, Berkeley, California 94720; 2 Cullen Eye Institute, Baylor College of Medicine, Houston, Texas 77030; and 3 Moran Eye Center, University of Utah, Salt Lake City, Utah 84132
Gaal, Lubor, Botond Roska, Serge A. Picaud, Samuel M. Wu, Robert
Marc, and Frank S. Werblin. Postsynaptic response kinetics
are controlled by a glutamate transporter at cone photoreceptors.
J. Neurophysiol. 79: 190-196, 1998. We evaluated the role of the
sodium/glutamate transporter at the synaptic terminals of cone
photoreceptors in controlling postsynaptic response kinetics. The
strategy was to measure the changes in horizontal cell response rate
induced by blocking transporter uptake in cones with dihydrokainate
(DHK). DHK was chosen as the uptake blocker because, as we show throu
gh autoradiographic uptake measurements, DHK specifically blocked upt
ake in cones without affecting uptake in Mueller cells. Horizontal ce
lls depolarized from about 
70 to 20
mV as the exogenous glutamate concentration was increased from ~1 to
40 µM, so horizontal cells can serve as "glutamate electrod
es" during the light response. DHK slowed the rate of hyperpolarizati
on of the horizontal cells in a dose-dependent way, but didn't affect
the kinetics of the cone responses. At 300 µM DHK, the rat
e of the horizontal cell hyperpolarization was slowed to only 17
;± 8.5% (mean ± SD) of control. Translating
this to changes in glutamate concentration using the slice dose respo
nse curve as calibration in Fig. 2, DHK reduced the
rate of removal of glutamate from ~0.12 to 0.031 µM/s. The volt
age dependence of uptake rate in the transporter alone was capable of
modulating glutamate concentration: we blocked vesicular released gl
utamate with bathed 20 mM Mg2+ and then added 30 µM gl
utamate to the bath to reestablish a physiological glutamate concentr
ation level at the synapse and thereby depolarize the horizontal cell
s. Under these conditions, a light flash elicited a 17-mV hyperpolari
zation in the horizontal cells. When we substituted kainate, which is
not transported, for glutamate, horizontal cells were depolarized bu
t light did not elicit any response, indicating that the transporter
alone was responsible for the removal of glutamate under these condit
ions. This suggests that the transporter was both voltage dependent a
nd robust enough to modulate glutamate concentration. The transporter
must be at least as effective as diffusion in removing glutamate fro
m the synapse because there is only a very small light response once
the transporter is blocked. The transporter, via its voltage dependen
ce on cone membrane potential, appears to contribute significantly to
the control of postsynaptic response kinetics.
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