Low-frequency characteristics of intracellularly recorded receptor potentials in guinea-pig cochlear hair cells.

Intracellular receptor potentials were recorded from inner and outer hair cells in response to low-frequency tones, from the basal, high-frequency region of the guinea-pig cochlea. The receptor potentials recorded from inner hair cells are asymmetrical about the resting membrane potential with the depolarizing phase, which corresponds to rarefaction in sound pressure, exceeding the phase of hyperpolarization by a factor of about 3. It was found that the relationship between the peak-to-peak voltage responses and sound pressure level could be described by rectangular hyperbolae. When the frequency of the sound stimulus was progressively increased from 100 Hz to 4 kHz, the 'periodic' (a.c.) component of the receptor potential was attenuated with respect to the 'continuous' (d.c.) component. The characteristics of the inner hair cells could be described by two stages of low-pass filtering, with one of the filters having the same corner frequency as the electrical time constants which varied in different cells between 178 and 840 Hz. Receptor potentials recorded intracellularly from two morphologically identified outer hair cells were symmetrical about the resting membrane potential (about -65-70 mV) and had a maximal amplitude of only 5 mV at frequencies and intensities which yield 20-30 mV voltage responses from inner hair cells. No d.c. component receptor potentials were recorded in response to high-frequency tones. Phase and amplitude measurements were made from receptor potentials from inner hair cells, and from 'cochlear microphonic potentials' which were recorded from the organ of Corti and scala tympani. The phase of depolarization in both potentials was associated with displacement of the basilar membrane towards the scala vestibuli. The phase of the intracellular receptor potentials leads the cochlear microphonic by about 90 degrees and the sound pressure by about 180 degrees at frequencies below 100 Hz. Above this frequency the phase lead progressively declines and at higher frequencies becomes a phase lag. These phase relationships indicate that inner hair cells respond to the velocity of the basilar membrane at frequencies below 200-600 Hz, and to its displacement above this, and that the voltage responses of the inner hair cells are limited by their membrane time constants. It is suggested that outer hair cells respond to basilar membrane displacement throughout their frequency range. It is shown that, with respect to frequency, the different growth rates of the cochlear microphonic potentials and inner hair cell receptor potentials, and the dominance of cochlear microphonic potentials in the organ of Corti, result in an effective electrical interaction between inner hair cells and cochlear microphonic potentials.