Effect of temperature on electrical resonance in leopard frog saccular hair cells.

Abstract

Leopard frog saccular hair cells exhibit an electrical resonance in response to a depolarizing stimulus that has been proposed to contribute to the tuning properties of the frog sacculus by acting as an electrical band-pass filter. With the whole cell patch-clamp technique, we have investigated the effect of temperature on electrical resonances in isolated saccular hair cells, and we have described the effects of temperature on the currents and channel kinetics underlying electrical resonance. A hair cell's onset resonant frequency in response to a constant depolarizing current pulse increases linearly with temperature at a rate of 11 Hz/1 degrees C, exhibiting a mean Q10 of 1.7 between 15 and 35 degrees C. However, offset resonant frequencies continue to double every 10 degrees C, exhibiting a mean Q10 of 2.1. If steady-state voltage during the stimulus is held constant, all oscillatory frequencies increase with a mean Q10 of 2.1. The average level of steady-state depolarization during a +150-pA depolarizing current pulse decreases with increasing temperature (-6 mV from 15 to 25 degrees C). This temperature-dependent reduction of the steady-state membrane potential causes a shift in the voltage-dependent channel kinetics to slower rates, thus reducing the apparent Q10 for onset resonant frequencies. The peak outward tail current and net steady-state outward current, which is the sum of a voltage-dependent inward calcium current (ICa) and an outward calcium-dependent potassium current (IK(Ca)), increase with temperature, exhibiting a mean Q10 of 1.7 between 15 and 25 degrees C. The activation rate (T1/2) of the outward current exhibits a mean Q10 of 2.3 between 15 and 25 degrees C, while the deactivation rate (taurel) exhibits a mean Q10 of 2.9 over the same temperature range. These results support previous models of the molecular determination of resonant frequency, which have proposed that a combination of IK(Ca) channel kinetics and the overall magnitude of the outward current are primarily responsible for determining the resonant frequency of an isolated hair cell. The robust temperature sensitivity of the hair cell receptor potential contrasts sharply with the temperature-insensitive tuning properties of in vivo saccular nerve fiber recordings. Possible explanations for this discrepancy are discussed.