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The Journal of Neuroscience, October 22, 2003, 23(29):9508-9518

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Behavioral/Systems/Cognitive
Synchronization of a Nonlinear Oscillator: Processing the Cf Component of the Echo-Response Signal in the Cochlea of the Mustached Bat

Ian J. Russell,^1,4 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 am Main, Germany, ³Neurobiology Section, Division of Biology, University of California, San Diego, La Jolla, California 92093-0357, and ⁴ Institute of Biochemistry and Biology, University of Potsdam, 14471 Potsdam, Germany

Cochlear microphonic potential (CM) was recorded from the CF2 region and the sparsely innervated zone (the mustached bat's cochlea fovea) that is specialized for analyzing the Doppler-shifted echoes of the first-harmonic (61 kHz) of the constant-frequency component of the echolocation call. Temporal analysis of the CM, which is tuned sharply to the 61 kHz cochlear resonance, revealed that at the resonance frequency, and within 1 msec of tone onset, CM is broadly tuned with linear magnitude level functions. CM measured during the ongoing tone and in the ringing after tone offset is 50 dB more sensitive, is sharply tuned, has compressive level functions, and the phase leads onset CM by 90°: an indication that cochlear responses are amplified during maximum basilar membrane velocity. For high-level tones above the resonance frequency, CM appears at tone onset and after tone offset. Measurements indicate that the two oscillators responsible for the cochlear resonance, presumably the basilar and tectorial membranes, move together in phase during the ongoing tone, thereby minimizing net shear between them and hair cell excitation. For tones within 2 kHz of the cochlear resonance the frequency of CM measured within 2 msec of tone onset is not that of the stimulus but is proportional to it. For tones just below the cochlear resonance region CM frequency is a constant amount below that of the stimulus depending on CM measurement delay from tone onset. The frequency responses of the CM recorded from the cochlear fovea can be accounted for through synchronization between the nonlinear oscillators responsible for the cochlear resonance and the stimulus tone.

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

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Received May 23, 2003; revised July 8, 2003; accepted July 9, 2003.

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