Synaptic hyperpolarization and inhibition of turtle cochlear hair cells.

Abstract

Intracellular recordings were made from turtle cochlear hair cells in order to examine the properties of the post-synaptic potentials evoked by electrical stimulation of the efferent axons. Single shocks to the efferents generated a hair cell membrane hyperpolarization with an average amplitude generally < 1 mV and lasting for .apprx. 100 ms. With short trains of shocks, the size of the post-synaptic potential grew markedly to a maximum of 20-30 mV. The interaction between pairs of shocks separated by a varying interval was studied. For an interval of 4 ms, the response to the 2nd shock was increased on average by a factor of 3 and the conditioning effect of the first shock decayed with a time constant of .apprx. 100 ms. The augmentation in response to trains of shocks may be partly due to facilitation of efferent transmitter release. The efferent post-synaptic potentials could be reversibly abolished by perfusion with perilymphs containing 3 .mu.M curare or atropine, and infusion of acetylcholine gave a transient membrane hyperpolarization. These observations are consistent with efferent action being mediated via a cholinergic synapse onto the hair cells. The post-synaptic potentials could be reversed in polarity by injection of hyperpolarizing currents through the recording electrode. The reversal potential was estimated as .apprx. -80 mV, 30 mV negative to the resting potential. Near reversal, a small brief depolarization was evident and may constitute a minor component of the synaptic response. The value of the reversal potential was unaffected by substitution of the perilymphatic Cl, but was altered in a predictable manner by changes in extracellular K concentration indicating that the post-synaptic potentials arise mainly by an increase in the permeability of the hair cell membrane to K+. Throughout the post-synaptic hyperpolarization there was a reduction in the sensitivity of the hair cell to tones at its characteristic frequency. The desensitization, maximal for low sound pressures, varied in different cells from a factor of 1.6 to 28. At the peak of the largest synaptic potentials, the receptor potential remained negative to the resting potential with all but the loudest characteristic frequency tones. Apparently there are 2 factors in efferent inhibition: one a reduction in the receptor potential at the hair cell''s characteristic frequency and the other a hyperpolarization of its membrane potential which should reduce the release of excitatory transmitter onto the afferent terminals. On the assumption that a hair cell receptor potential of .apprx. 1.0 mV causes a threshold response in an auditory afferent fiber, then a maximum threshold elevation of 60-80 dB in the afferents can be accounted for by efferent action on the hair cells. Intracellular recordings from afferent nerve terminals showed that during efferent stimulation, there was a cessation of all driven activity with no change in the membrane potential.