Synaptic reliability and temporal precision are achieved via high quantal content and effective replenishment: auditory brainstem versus hippocampus

At early stations of the auditory pathway, information is encoded in the precise signal timing and rate. Auditory synapses must maintain the relative timing of events with submillisecond precision even during sustained and high–frequency stimulation. In non–auditory brain regions, e.g. telencephalic ones, synapses are activated at considerably lower frequencies. Central to understanding the heterogeneity of synaptic systems is to elucidate the physical, chemical, and biological factors that determine synapse performance. In this study, we used slice recordings from three synapse types in the mouse auditory brainstem and hippocampus. Whereas the auditory brainstem nuclei experience high–frequency activity in vivo, the hippocampal circuits are activated at much lower frequencies. We challenged the synapses with sustained high–frequency stimulation (60 s for up to 200 Hz) and found significant performance differences. Our results show that auditory brainstem synapses differ considerably from their hippocampal counterparts in several aspects, namely resistance to synaptic fatigue, low failure rate, and exquisite temporal precision. Their high–fidelity performance supports the functional demands and appears to be due to a large size of the readily releasable pool and a high release probability, which together result in a high quantal content. In conjunction with very efficient vesicle replenishment mechanisms, these properties provide extremely rapid and temporally precise signaling required for neuronal communication at early stations of the auditory system, even during sustained activation in the minute range.

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