How to build a fast and highly sensitive sound detector that remains robust to temperature shifts

Frogs must have sharp hearing abilities during the warm summer months to successfully find mating partners. This study aims to understand how frog hair cell ribbon-type synapses preserve both sensitivity and temporal precision during temperature changes. Under room (~24°C) and high (~32°C) temperature, we performed in vitro patch-clamp recordings of hair cells and their afferent fibers in amphibian papillae of either male or female bullfrogs. Afferent fibers exhibited a wide heterogeneity in membrane input resistance (R_in ) from 100 Mωto 1000 Mω, which may contribute to variations in spike threshold and firing frequency. At higher temperatures, most fibers increased their frequency of spike firing due to an increase in spontaneous EPSC frequencies. Hair cell resting membrane potential (V_rest ) remained surprisingly stable during temperature increases, because Ca²⁺influx and K⁺outflux increased simultaneously. This increase in Ca²⁺ current likely enhanced spontaneous EPSC frequencies. These larger "leak currents" at V_rest also lowered R_in and produced higher electrical resonant frequencies. Lowering R_in will reduce the hair cells receptor potential and presumably moderate the systems sensitivity. Using membrane capacitance measurements, we suggest that hair cells can partially compensate for this reduced sensitivity by increasing exocytosis efficiency and the size of the readily releasable pool of synaptic vesicles. Furthermore, paired recordings of hair cells and their afferent fibers showed that synaptic delays shortened and multivesicular release becomes more synchronous at higher temperatures, which should improve temporal precision. Together, our results explain many previous in vivo observations on the temperature dependence of spikes in auditory nerves.