Peripheral auditory physiology in the lemon shark: Evidence of parallel otolithic and non-otolithic sound detection

Abstract

The intact ear of the lemon shark,Negaprion brevirostris, is sensitive to sound at low frequencies by electrophysiological criteria. The click-evoked compound action potential of the eighth nerve has a dynamic range of at least 30 dB, with a latency shortening of 120 to 170 μs/dB and an amplitude increase of 4 to 11%/dB relative to a nearly saturated response. The shape of the potential is dependent on the click phase and with the top of the head out of water these potentials are evoked by clicks with air sound pressure levels as low as 19.5 dB re 1 μbar and velocity levels in the water as low as 23 dB re 1 μvar. The calculated displacement thresholds range from 5×10−8 to 4×10−7 cm for this response, overlapping and extending slightly below the thresholds previously reported for whole animals. The frequency sensitivity for this measure of the ear's response also agrees with behavioral data, suggesting that the ear is the primary site for sound detection. Units in the eighth nerve fall into three classes: regularly spontaneous and non-acoustic, irregularly spontaneous and acoustic, and nonspontaneous and acoustic. The best excitatory frequencies for the acoustic units range from 375 Hz down to 31 Hz if not lower, with the majority below 200 Hz. There are two maculae in this ear that are capable of detecting sound. One, the macula neglecta, is a non-otolithic detector composed of two large patches of sensory epithelium that line the walls of the posterior canal duct and extend cilia complexes toward a gelatinous cupula that fills the lumen of the duct. Units in the branch of the eighth nerve that serves this macula are responsive to sound that appears to be transmitted through parietal fossa connective tissue and a dorsal opening in the otic capsule wall. The other sound detector is the macula of the otolithic sacculus. In juvenile lemon sharks this epithelium contains an estimated 300,000 hair cells that extend their cilia toward a large mass of otoconia. It is proposed that these two maculae may detect sound by dissimilar mechanisms that provide different directional responses and possibly different frequency responses and might allow unambiguous sound localization.