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The Journal of Neuroscience, April 13, 2005, 25(15):3842-3850; doi:10.1523/JNEUROSCI.5231-04.2005
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Cellular/Molecular
Reluctant Vesicles Contribute to the Total Readily Releasable Pool in Glutamatergic Hippocampal Neurons
Krista L. Moulder1 andSteven Mennerick1,2 Departments of 1Psychiatry and 2Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110
The size of the readily releasable pool (RRP) of vesicles is critically important for determining the size of postsynaptic currents generated in response to action potentials. However, discrepancies in RRP estimates exist among methods designed to measure RRP size. In glutamatergic hippocampal neurons, we found that hypertonic sucrose application yielded RRP size estimates approximately fivefold larger than values obtained with high-frequency action potential trains commonly assumed to deplete the RRP. This discrepancy was specific for glutamatergic neurons, because no difference was found between sucrose and train estimates of RRP size in GABAergic neurons. A small component of the difference in excitatory neurons was accounted for by postsynaptic receptor saturation. Train estimates of vesicle pool size obtained using more stimuli revealed that action potential-elicited EPSCs did not truly reach a steady state during shorter trains, and RRP estimates were closer to sucrose estimates made in the same neurons. This suggested that reluctant vesicles may contribute to the total available pool. Two additional lines of evidence supported this hypothesis. First, RRP estimates from strongly depolarizing hyperkalemic solutions closely matched those obtained with sucrose. Second, when Ca2+ influx was enhanced during trains, train estimates of pool size matched those obtained with sucrose. These data suggest that glutamatergic hippocampal neurons maintain a heterogeneous population of vesicles that can be differentially released with varying Ca2+ influx, thereby increasing the range of potential synaptic responses.
Key words: glutamate; voltage-clamp; readily releasable pool; probability of release; calcium; excitatory synaptic transmission
Received Dec 22, 2004; revised February 21, 2005; accepted March 8, 2005.
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