Voltage-Mediated Control of Bundle Dynamics in Hair Cells

Hair cells of the vertebrate vestibular and auditory end organs convert mechanical inputs into electrical responses. This mechano-electrical transduction (MET) involves the gating of mechanically sensitive ion channels, thus modulating the conductance and the membrane potential of the cell. MET includes one or more energy consuming feedback mechanisms that keep the channels in their most sensitive operating range. Coupling between the gating of the channels and this adaptation mechanism has been proposed to follow dynamics of a system that is close to a Hopf or other bifurcations. Such systems exhibit high responsiveness to external stimuli in the proximity of a critical point, and exhibit spontaneous limit-cycle oscillations when the system crosses a bifurcation. We present optical and electrophysiological recordings from hair cells that exhibit such spontaneous oscillations and explore how the cell's membrane potential may control the system's tuning near the critical point. Sacculi from the American bullfrog were mounted in a two-compartment chamber such that the natural fluid separation between the apical and basolateral surfaces of the hair cells was maintained. Spontaneous hair bundle oscillations were monitored using a high-speed video camera system, and the hair cell membrane potential was controlled using standard patch-clamp techniques. We found that the membrane potential of the hair cell can modulate or fully suppress innate oscillations, thus controlling the dynamic state of the bundle. This control is mediated by the cell's internal calcium concentration, which sets the resting open probability of the mechanosensitive channels. The auditory and vestibular systems could control the membrane potential of hair cells to tune the dynamic states of the system near (or away from) the critical point, thereby affecting the responsiveness of the hair cells. This work was supported by NIH grant RO1DC011380 to DB.