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Exocytosis of Vesicular Zinc Reveals Persistent Depression of Neurotransmitter Release during Metabotropic Glutamate Receptor Long-Term Depression at the Hippocampal CA3–CA1 Synapse

Exocytosis can be directly measured in mammalian brain slices by fluorescence detection of vesicular zinc release. Detection of the low-level evoked zinc signal [Zn]t was first demonstrated at the zinc-rich hippocampal mossy fiber pathway and required the use of high-frequency presynaptic stimulation. Here, we show that release after individual action potentials can be reliably detected even at non-mossy fiber, zinc-poor synapses in the hippocampus, a major enhancement in the temporal resolution of the technique. Short-term facilitation of release properties of zinc-positive CA3–CA1 Schaffer collateral/commissural synapses in the stratum radiatum differ from those at mossy fibers but are similar to those measured for the EPSP [field EPSP (fEPSP)]. The N-type Ca2+ channel toxin ω-conotoxin GVIA inhibited both the [Zn]t and fEPSP equally, and the modulation of neurotransmitter release by neuropeptide Y, baclofen, and adenosine as revealed by [Zn]t closely resembles that measured for the fEPSP. A long-standing controversy in hippocampal synaptic plasticity involves the site of long-term depression (LTD) at these synapses. Using zinc release as a direct marker for exocytotic events and a surrogate marker for glutamate release, we demonstrate that persistent depression of presynaptic release occurs in the late expression of DHPG [(S)-3,5-dihydroxyphenylglycine]-induced LTD at this synapse. The ability to examine release dynamics with zinc fluorescence detection will facilitate exploration of the molecular pharmacology and plasticity of exocytosis at many CNS synapses.