The Endolymphatic Potential Can Control the Gating Force of the Hair Cell's Transduction Channels

Taking advantage of a two-compartment preparation of the frog saccule, we measured the effect of steps or slow ramps of electric current across the sensory tissue on the transduction channels’ gating force. Transepithelial currents afforded a means to control the endolymphatic potential in the top compartment with respect to the potential in perilymph that bathed the basal aspect of the hair cells. Under each condition, we estimated the transduction channels’ gating force from nonlinearity of the bundle’s force-displacement relation. We found that the gating force could nearly double upon application of a negative endolymphatic potential until, beyond a threshold value, the gating force abruptly dropped to a low level, resulting in linear force-displacement relations. The hair-bundle stiffness at large displacements, outside the region of channel gating, was only weakly affected by transepithelial currents. In addition, when descending and ascending ramps of transepithelial currents were applied in succession, the transition between strong and weak gating forces displayed hysteresis. All these effects were fully reversible. We conclude that the endolymphatic potential may serve as a control parameter of the transduction channel’s gating force. Our work further indicates that the molecular movement associated to channel gating—the gating swing—can be of variable magnitude in the same hair cell depending on electrical conditions. We propose that modulation of channel gating by the endolymphatic potential results from electric control of the resting calcium influx into the hair cell, which must be large enough to allow for large gating swings and in turn for high mechanosensitivity by the hair cell.