Peripheral auditory physiology in the lemon shark: Evidence of parallel otolithic and non-otolithic sound detection
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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.
KeywordsSound Pressure Level Compound Action Potential Sensory Epithelium Otic Capsule Capsule Wall
compound action potential
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- Banner A (1967) Evidence of sensitivity to acoustic displacements in the lemon shark,Negaprion brevirostris (Poey). In: Cahn PH (ed) Lateral line detectors, Indiana University Press. Bloomington, Indiana, pp 265–273Google Scholar
- Banner A (1973) Simple velocity hydrophones for bioacoustic application. J Acoust Soc Am 53:1134–1136Google Scholar
- Bullock TH, Corwin JT (1979) Acoustic evoked activity in the brain in sharks. J Comp Physiol 129:223–234Google Scholar
- Corwin JT (1977a) Morphology of the macula neglecta in sharks of the genusCarcharhinus. J Morphol 152:341–362Google Scholar
- Corwin JT (1977b) Ongoing hair cell production, maturation, and degeneration in the shark ear. Neurosci Abstr 3:4Google Scholar
- Corwin JT (1978) The relation of inner ear structure to feeding behavior in sharks and rays. In: Johari O (ed) Scanning electron microscopy, vol II. SEM, Chicago, pp 1105–1112Google Scholar
- Corwin JT (1981) Postembryonic production and aging of inner ear hair cells in sharksGoogle Scholar
- Dijkgraaf S (1960) Hearing in bony fishes. Proc R Soc Lond [Biol] 152:51–54Google Scholar
- Dijkgraaf S (1963) Sound reception in the dogfish. Nature 197:93–94Google Scholar
- Fay RR, Kendall JI, Popper AN, Tester AL (1974) Vibration detection by the macula neglecta of sharks. Comp Biochem Physiol 47A: 1235–1240Google Scholar
- Feng AS, Narins PM, Capranica RR (1975) Three populations of primary auditory fibers in the bullfrog (Rana catesbeiana): their peripheral origins and frequency sensitivities. J Comp Physiol 100:221–229Google Scholar
- Furukawa T, Ishii Y (1967) Neurophysiological studies on hearing in goldfish. J Neurophysiol 30:1375–1403Google Scholar
- Kelly JC, Nelson DR (1975) Hearing thresholds of the horn shark,Heterodontus francisci. J Acoust Soc Am 58:905–909Google Scholar
- Lowenstein O, Roberts TDM (1950) The equilibrium function of the otolith organs of the thornback ray (Raja clavata). J Physiol (Lond) 110:392–415Google Scholar
- Lowenstein O, Roberts TDM (1951) The localization and analysis of the responses to vibration from the isolated elasmobranch labyrinth. A contribution to the problem of the evolution of hearing in vertebrates. J Physiol (Lond) 114:471–489Google Scholar
- Lowenstein O, Wersäll J (1959) Functional interpretation of the electron microscopic structure of the sensory hairs in the cristae of the elasmobranchRaja clavata in terms of directional sensitivity. Nature 184:1807Google Scholar
- Lowenstein O, Osborne MP, Wersäll J (1964) Structure and innervation of the sensory epithelia of the labyrinth in the thornback ray (Raja clavata). Proc R Soc Lond [Biol] 160:1–12Google Scholar
- Myrberg AA Jr (1978) Underwater sound —its effect on the behaviour of sharks. In: Hodgson ES, Mathewson RF (eds) Sensory biology of sharks, skates, and rays. Office of Naval Research, Arlington, Virginia, pp 391–417Google Scholar
- Myrberg AA Jr, Ha SJ, Walewski S, Banbury JC (1972) Effectiveness of acoustic signals in attracting epipelagic sharks to an underwater sound source. Bull Mar Sci 22:926–949Google Scholar
- Nelson DR (1967) Hearing thresholds, frequency discrimination and acoustic orientation in the lemon shark,Negaprion brevirostris (Poey). Bull Mar Sci 17:741–768Google Scholar
- Nelson DR, Gruber SH (1963) Sharks: attraction by low-frequency sounds. Science 142:975–977Google Scholar
- Nelson DR, Johnson RH (1972) Acoustic attraction of Pacific reef sharks: effect of pulse intermittency and variability. Comp Biochem Physiol 42A: 85–95Google Scholar
- Parker GH (1909) The sense of hearing in the dogfish. Science 29:428Google Scholar
- Piddington RW (1972) Auditory discrimination between compressions and rarefactions by goldfish. J Exp Biol 56:403–419Google Scholar
- Popper AN, Fay RR (1977) Structure and function of the elasmobranch auditory system. Am Zool 17:443–452Google Scholar
- Schuijf A (1975) Directional hearing of cod (Gadus morhua) under approximate free field conditions. J Comp Physiol 98:307–332Google Scholar
- Schuijf A (1976a) The phase model of directional hearing in fish. In: Schuijf A, Hawkins AD (eds) Sound reception in fish. Elsevier, New York, pp 63–86Google Scholar
- Schuijf A (1976b) Timing analysis and directional hearing in fish. In: Schuijf A, Hawkins AD (eds) Sound reception in fish. Elsevier, New York, pp 87–112Google Scholar
- Siler W (1969) Near- and farfields in a marine environment. J Acoust Soc Am 46:483–484Google Scholar
- Spaeth M, Schweickert W (1977) The effect of metacaine (MS-222) on the activity of the efferent and afferent nerves in the teleost lateral-line system. Naunyn Schmiedebergs Arch Pharmacol 297:9–16Google Scholar
- Tester AL, Kendall JI, Milisen WB (1972) Morphology of the ear of the shark genusCarcharhinus with particular reference to the macula neglecta. Pac Sci 26:264–274Google Scholar