Frequency-selective exocytosis by ribbon synapses of hair cells

The activity of auditory afferent fibers depends strongly on the frequency of stimulation. Although the bullfrog’s amphibian papilla lacks the flexible basilar membrane that effects tuning in mammals, its afferent axons display comparable frequency selectivity. Seeking additional mechanisms of tuning in this organ, we monitored the synaptic output of hair cells by measuring changes in their membrane capacitance during sinusoidal electrical stimulation at various frequencies. Using perforated-patch recordings, we found that individual hair cells show frequency selectivity in synaptic exocytosis within the frequency range sensed by the amphibian papilla. Moreover, each cell’s tuning varies in accordance with its tonotopic position. Using confocal imaging, we observed a tonotopic gradient in the concentration of proteinaceous Ca2+ buffers. A model for synaptic release suggests that this gradient maintains the sharpness of tuning. We conclude that hair cells of the amphibian papilla use synaptic tuning as an additional mechanism for sharpening their frequency selectivity.

A schematic view of the bullfrog's amphibian papilla (left) indicates the approximate locations of hair cells tuned to different frequencies of stimulation. For a cell near the middle of the organ (right), the capacitance change during stimulation peaks at 400 Hz.