Abstract
At the frog semicircular canals, the afferent fibers display high spontaneous activity (mEPSPs), due to transmitter release from hair cells. mEPSP and spike frequencies are modulated by stimulation that activates the hair cell receptor conductance. The relation between receptor current and transmitter release cannot be studied at the intact semicircular canal. To circumvent the problem, we combined patch-clamp recordings at the isolated hair cell and electrophysiological recordings at the cytoneural junction in the intact preparation. At isolated hair cells, the K channel blocker tetraethylammonium (TEA) is shown to block a fraction of total voltage-dependent K-conductance (IKD) that depends on TEA concentration but not on membrane potential (Vm). Considering the bioelectric properties of the hair cell, as previously characterized by this lab, a fixed fractional block of IKD is shown to induce a relatively fixed shift in Vm, provided it lies in the range −30 to −10 mV. The same concentrations of TEA were applied to the intact labyrinth while recording from single afferent fibers of the posterior canal, at rest and during mechanical stimulation. At the peak of stimulation, TEA produced increases in mEPSP rate that were linearly related to the shifts produced by the same TEA concentrations (0.1–3 mM) in hair cell Vm (0.7–5 mV), with a slope of 29.8 Hz/mV. The membrane potential of the hair cell is not linearly related to receptor conductance, so that the slope of quantal release vs. receptor conductance depends on the prevailing Vm (19.8 Hz/nS at −20 mV; 11 Hz/nS at −10 mV). Changes in mEPSP peak size were negligible at rest as well as during stimulation. Since ample spatial summation of mEPSPs occurs at the afferent terminal and threshold-governed spike firing is intrinsically nonlinear, the observed increases in mEPSP frequency, though not very large, may suffice to trigger afferent spike discharge.
Highlights
A number of different approaches have been used to study the function of vestibular hair cells in processing the mechanical stimulus and producing the activation of the first afferent neuron
We studied some basic features of early sensory processing in the frog semicircular canal, a preparation in which the isolated hair cells are accessible to the patch-clamp analysis, while the afferent information can be recorded in the intact labyrinth
The Problem of the Hair Cell Membrane Potential Data from the literature suggest that amphibian saccular hair cells in situ and in vivo should have a resting membrane potential around –70 mV (Bracho and Budelli, 1978) and that the receptor conductance can change the membrane potential by some 8 mV in mechanically stimulated isolated saccular hair cells (Hudspeth and Corey, 1977); in type II hair cells, a model derived from available data suggested a membrane potential fluctuation, in response to maximal cilium deflection, from −70 to −40 or −30 mV, depending on the expression of the various conductances (Soto et al, 2002); a depolarization up to −19 mV was measured in vestibular hair cells of the chick held at a resting potential of −43 mV (Ohmori, 1985)
Summary
A number of different approaches have been used to study the function of vestibular hair cells in processing the mechanical stimulus and producing the activation of the first afferent neuron. The complex interplay of ionic currents at the isolated hair cell has been described in detail (Housley et al, 1989; Lang and Correia, 1989; Masetto et al, 1994; Rennie and Correia, 1994; Brichta et al, 2002; Catacuzzeno et al, 2003; Martini et al, 2009), and a number of categories of sensory units have been discriminated, based on electrophysiological properties and spike firing patterns (Wilson and Melvill Jones, 1979; Goldberg, 1991; Goldberg and Brichta, 2002; Pfanzelt et al, 2008). The semicircular canal cupula-endolymph system is tuned for low-frequency signals, so that the type and kinetics of voltage-dependent channels in the hair cell may differ from those previously described in saccular or cochlear hair cells
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