Glutamate transporters are believed to remove glutamate from the synaptic cleft only slowly because they cycle slowly. However, we show that when glutamate binds to postsynaptic transporters at the cerebellar climbing fiber synapse, it evokes a conformation change and inward current that reflect glutamate removal from the synaptic cleft within a few milliseconds, a time scale much faster than the overall cycle time. Contrary to present models, glutamate removal does not require binding of an extracellular proton, and the time course of transporter anion conductance activation differs from that of glutamate removal. The charge movement associated with glutamate removal is consistent with the majority of synaptically released glutamate being removed from the synaptic cleft by postsynaptic transporters.
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