Frequency tuning in a frog vestibular organ

Abstract

Several distinct mechanisms have evolved in the auditory periphery to extract frequency information from a sound. In the mammalian cochlea, a travelling wave on the basilar membrane¹ enhanced by a physiologically vulnerable neuro-mechanical interaction^2,3 performs the primary frequency separation. In lizards, tuning is likely to depend on structures in the papilla other than the basilar membrane⁴, and tuning in the auditory nerve is correlated with the length of the stereocilia⁵. In turtles⁶ and possibly some bird species⁷, an electrical resonance in the receptor cells is responsible for frequency selectivity. In addition to those organs obviously specialized to detect acoustic stimuli, afferents of the vestibular system can exhibit tuning to low-frequency airborne sounds^8,9, despite the absence of mechanical frequency separation by accessory structures. I report here that in the frog saccule, a vestibular organ apparently constructed for the detection of vibratory accelerations^8–10, frequency tuning may arise from an electrical resonance intrinsic to the hair cells. The mechanism is similar to that found in turtle⁶ and ensures that a stimulus with frequency corresponding to the membrane resonant frequency will produce the largest signal in the cell. This type of tuning may thus be quite widespread. Oscillatory mechanisms have been reported in sensory cells of other modalities in several lower vertebrates^6,11,12, and may even contribute to their sensitivity, although such mechanisms do imply that the signal-to-noise ratio is degraded near threshold.