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The Journal of Neuroscience, November 26, 2003, 23(34):10971-10981

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Behavioral/Systems/Cognitive
The Development of a Single Frequency Place in the Mammalian Cochlea: The Cochlear Resonance in the Mustached Bat Pteronotus parnellii

Ian J. Russell,¹ Markus Drexl,² Elisabeth Foeller,³ Marianne Vater,⁴ and Manfred Kössl²

¹School of Life Sciences, University of Sussex, Brighton BN1 9QG, United Kingdom, ²Zoological Institute, University of Frankfurt, 60323 Frankfurt, Germany, ³Neurobiology Section, Division of Biology, University of California, San Diego, La Jolla, California 92093-0357, and ⁴Institute of Biochemistry and Biology, University of Potsdam, 14471 Potsdam, Germany

Cochlear microphonic potentials (CMs) were recorded from the sharply tuned, strongly resonant auditory foveae of 1- to 5-week-old mustached bats that were anesthetized with Rompun and Ketavet. The fovea processes Doppler-shifted echo responses of the constant-frequency component of echolocation calls. During development, the frequency and tuning sharpness of the cochlear resonance increases, and CM ringing persists for longer after the tone. CM is relatively insensitive at tone onset and grows linearly with increased stimulus level. During the tone, the CM is more sensitive and grows compressively with increased stimulus level and phase leads onset CM by 90° for frequencies below the resonance. CM during the ringing is also sensitive and compressive and phase leads onset CM by 180° below the resonance and lags it by 180° above the resonance. Throughout postnatal development, CMs measured during the tone and in the ringing increase both in sensitivity and compression. The cochlear resonance appears to be attributable to interaction between two oscillators. The more broadly tuned oscillator dominates the onset response, and the narrowly tuned oscillator dominates the ringing. Early in development, mechanical coupling between the oscillators results in a relatively broadly tuned system with several frequency modes in the CM at tone onset and in the CM ringing. Beating occurs between the resonance and the stimulus response during the tone and between two components of the narrowly tuned oscillator at tone offset. At maturity, the CM has three modes for frequencies within 10 kHz of the resonance at tone onset and a single, sharply tuned mode in the ringing.

Key words: mustached bat; cochlea; microphonic potential; frequency tuning; resonance; synchronization; basilar membrane; tectorial membrane; cochlear amplifier; auditory fovea

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Received June 2, 2003; revised September 30, 2003; accepted October 6, 2003.

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