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. We performed in vitro patch-clamp recordings of hair cells and their afferent fibers in bullfrog amphibian papillae under room (23-25{degrees}C) and high (30-33{degrees}C) temperature. Afferent fibers exhibited a wide heterogeneity in membrane input resistance (Rin) from 100 M{Omega} to 1000 M{Omega}, which may contribute to variations in spike threshold and firing frequency. At higher temperatures, most fibers increased their frequency of action potential firing due to an increase in spontaneous EPSC frequencies. Hair cell resting membrane potential (Vrest) remained surprisingly stable during temperature increases, although both inward Ca2+ current and outward K+ current increased in amplitude. This increase in Ca2+ current may explain the higher spontaneous EPSC frequencies. The larger \"leak currents\" at Vrest lowered Rin and produced higher electrical resonant frequencies. However, lower Rin should decrease sensitivity to sound detection via smaller receptor potentials. 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 become shorter and multivesicular release becomes more synchronous at higher temperatures, which should improve temporal precision. Altogether, our results explain many previous in vivo observations on the temperature dependence of spikes in auditory nerves.\n\nSignificance StatementThe vertebrate inner ear detects and transmits auditory information over a broad dynamic range of sound frequency and intensity. It achieves remarkable sensitivity to soft sounds and precise frequency selectivity. How does the ear of cold-blooded vertebrates maintain its performance level as temperature changes? More specifically, how does the hair cell to afferent fiber synapse in bullfrog amphibian papilla adjust to a wide range of physiological temperatures without losing its sensitivity and temporal fidelity to sound signals? This study uses in vitro experiments to reveal the biophysical mechanisms that explain many observations made from in vivo auditory nerve fiber recordings. We find that higher temperature facilitates vesicle exocytosis and electrical tuning to higher sound frequencies, which benefits sensitivity and selectivity.