Spikes and membrane potential oscillations in hair cells generate periodic afferent activity in the frog sacculus.

To look for membrane potential oscillations that may contribute to sensory coding or amplification in the ear, we made whole-cell and perforated-patch recordings from hair cells and postsynaptic afferent neurites in the explanted frog sacculus, with mechanoelectrical transduction (MET) blocked. Small depolarizing holding currents, which may serve to replace the in vivo resting MET current, evoked all-or-none calcium spikes (39-75 mV amplitude) in 37% of hair cells tested, and continuous membrane potential oscillations (14-28 mV; 15-130 Hz) in an additional 14% of cells. Spiking hair cells were on average taller and thinner than nonspiking hair cells, and had smaller outward currents through delayed rectifier channels (I(KV)) and noninactivating calcium-activated potassium channels (I(BK,steady)), and larger inward rectifier currents (I(K1)). Some spiking hair cells fired only a brief train at the onset of a current step, but others could sustain repetitive firing (3-70 Hz). Partial blockade of I(BK) changed the amplitude and frequency of oscillations and spikes, and converted some nonspiking cells into spiking cells. Oscillatory hair cells preferentially amplified sinusoidal stimuli at frequencies near their natural oscillation frequency. Postsynaptic recordings revealed regularly timed bursts of EPSPs in some afferent neurites. EPSP bursts were able to trigger afferent spikes, which may be initiated at the sodium channel cluster located adjacent to the afferent axon's most peripheral myelin segment. These results show that some frog saccular hair cells can generate spontaneous rhythmic activity that may drive periodic background activity in afferent axons.