Abstract
The dynamics of vestibular afferent responses are thought to be strongly influenced by presynaptic properties. In this paper, by performing whole-cell perforated-patch experiments in the frog utricle, we characterized voltage-dependent currents and voltage responses to current steps and 0.3–100 Hz sinusoids. Current expression and voltage responses are strongly related to hair cell type. In particular, voltage responses of extrastriolar type eB (low pass, −3 dB corner at 52.5 ± 12.8 Hz) and striolar type F cells (resonant, tuned at 60 ± 46 Hz) agree with the dynamics (tonic and phasic, respectively) of the afferent fibers they contact. On the other hand, hair cell release (measured with single-sine membrane ΔCm measurements) was linearly related to Ca in both cell types, and therefore did not appear to contribute to dynamics differences. As a tool for quantifying the relative contribution of basolateral currents and other presynaptic factors to afferent dynamics, the recorded current, voltage and release data were used to build a NEURON model of the average extrastriolar type eB and striolar type F hair cell. The model contained all recorded conductances, a basic mechanosensitive hair bundle and a ribbon synapse sustained by stochastic voltage-dependent Ca channels, and could reproduce the recorded hair cell voltage responses. Simulated release obtained from eB-type and F-type models display significant differences in dynamics, supporting the idea that basolateral currents are able to contribute to afferent dynamics; however, release in type eB and F cell models does not reproduce tonic and phasic dynamics, mainly because of an excessive phase lag present in both cell types. This suggests the presence in vestibular hair cells of an additional, phase-advancing mechanism, in cascade with voltage modulation.
Highlights
Vestibular afferent responses to head movements are characterized by a response dynamics, reported in terms of gain and phase of the first harmonic of afferent modulation relative to a sinusoidal motion stimulus
In the turtle crista, postsynaptic recordings suggest that afferent response dynamics are determined presynaptically (Goldberg and Holt, 2013), patch clamp recordings suggest that, at vestibular frequencies, dynamics are not significantly affected by hair cell basolateral currents, because hair cell responses approach passive ones for slow stimuli (Goldberg and Brichta, 2002)
In the present study we show that, in hair cells from the frog utricle, voltage modulation by basolateral ion channels significantly affects postsynaptic dynamics at vestibular frequencies, but is not sufficient to explain postsynaptic dynamics
Summary
Vestibular afferent responses to head movements are characterized by a response dynamics, reported in terms of gain and phase of the first harmonic of afferent modulation relative to a sinusoidal motion stimulus. In the turtle crista, postsynaptic recordings suggest that afferent response dynamics are determined presynaptically (Goldberg and Holt, 2013), patch clamp recordings suggest that, at vestibular frequencies, dynamics are not significantly affected by hair cell basolateral currents, because hair cell responses approach passive ones for slow stimuli (Goldberg and Brichta, 2002). In the present study we show that, in hair cells from the frog utricle, voltage modulation by basolateral ion channels significantly affects postsynaptic dynamics at vestibular frequencies, but is not sufficient to explain postsynaptic dynamics. The frog utricle contains gravity and vibratory afferents (Koyama et al, 1982), and afferent response has been correlated with the type of contacted hair cells. For the present work we focused on extrastriolar type B and striolar type F cells
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