Heat pulse excitability of vestibular hair cells and afferent neurons

In the present study we combined electrophysiology with optical heat pulse stimuli to examine thermodynamics of membrane electrical excitability in mammalian vestibular hair cells and afferent neurons. We recorded whole-cell currents in mammalian type II vestibular hair cells using an excised preparation (mouse), and action potentials (APs) in afferent neurons in vivo (chinchilla) in response to optical heat pulses applied to the crista (T0.25°C pulse _-1). Afferent spike trains evoked by heat pulse stimuli were diverse and included asynchronous inhibition, asynchronous excitation, and/or phase-locked APs synchronized to each IR heat pulse. Thermal responses of membrane currents responsible for APs in ganglion neurons were strictly excitatory, with a Q₁₀2. In contrast, hair cells responded with a mix of excitatory and inhibitory currents. Excitatory hair cell membrane currents included a thermoelectric capacitive current proportional to the rate of temperature rise , and an inward conduction current driven by T. An iberiotoxin-sensitive (ibTX) inhibitory conduction current (BK) was also evoked by T, rising in <3ms and decaying with a time constant of ~24ms. The inhibitory component dominated whole cell currents in 50% of hair cells at -68mV, and in 67% of hair cells at -60mV. Responses were quantified and described based on first principles of thermodynamics. Results identify key molecular targets underlying heat pulse excitability in vestibular sensory organs, and provide quantitative methods for rational application of optical heat pulses to examine protein biophysics and manipulate cellular excitability.

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