Timing of neural excitation in relation to basilar membrane motion in the basal region of the guinea pig cochlea during the presentation of low-frequency acoustic stimulation

Hiroshi Wada, Akira Takeda, and Tetsuaki Kawase

Hearing Research 2002 Mar, 165: 165-176

Abstract:

In spite of many studies concerning auditory nerve action potentials, the timing of neural excitation in relation to basilar membrane (BM) motion is still not well understood. In this study, therefore, BM vibrations in the basal region of the guinea pig cochlea were measured using a laser Doppler velocimeter, and action potentials in auditory nerve fibers were recorded by a conventional microelectrode technique. An attempt was then made to determine the relationship between BM motion and neural excitation in auditory nerve fibers. To obtain BM responses in the high-characteristic frequency (CF) region (18–22 kHz) and responses of auditory nerve fibers with high CFs (14–22 kHz), low-frequency stimuli (50–2000 Hz), frequencies of which were well below CFs, were presented at 60–100 dB SPL. The results indicated that neural excitation occurred when the BM was displaced toward the scala vestibuli. Moreover, the neural excitatory phase did not significantly vary with the fiber's CF between 14 and 22 kHz nor with the stimulus level between 60 and 100 dB SPL. (Bold text emphasis by Martin Braun)

Comment:

The results of Wada et al. settle a long-standing controversy in cochlear mechanics. It had been known for several decades that nerve fibers from the apex of the cochlea have longer response delays than those from the base of the cochlea. One school of thoughts attributed the delay difference to the time needed by the basilar membrane (BM) traveling wave on its way from the base to the apex. The other school of thoughts suggested than all hair cells are excited instantaneously by the sound waves in the cochlear liquids and that the delay differences are due to differences between the hair cells. Low-frequency hair cells in the apex are mechanically and electrically tuned to slow oscillations, and thus are bound to need a longer time for signal transduction than hair cells at the base.

The new results reject the first hypothesis and confirm the second one. Between the cochlear places 22 and 14 kHz in the guinea pig, a 2 kHz traveling wave on the BM shows a phase difference of 65 degrees (Kohllöffel, 1972; Robertson, 1984). A phase difference of this size would definitely have been visible in the regression analyses of Wada et al. (their Figs. 6A-E). But it is fully absent. We have to conclude that the hair cells at the places of 22 and 14 kHz were excited directly through the cochlear fluids at the speed of sound, which is faster than that of the BM traveling wave by several orders of magnitude and therefore invisible in the phase data (phase difference < 1 degree). Also the difference in transduction speed between hair cells at the places of 22 and 14 kHz can be assumed to be so small that it does not show in the data.

Kohllöffel, L.U.E. (1972) A study of basilar membrane vibrations. II. The vibratory amplitude and phase pattern along the basilar membrane (postmortem). Acoustica 27, 66-81.

Robertson D. (1984) Horseradish peroxidase injection of physiologically characterized afferent and efferent neurones in the guinea pig spiral ganglion. Hear Res 15, 113-121.

(Comment Martin Braun)

Further technical details and discussions concerning these results are in the archives of the Cochlea List: May 2002, June 2002.

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