Heat pulse excitability of vestibular hair cells and afferent neurons

Richard D. Rabbitt, Alan M. Brichta, Hessam Tabatabaee, Peter J. Boutros, Joong Ho Ahn, Charles C. Della Santina, Lauren A. Poppi, Rebecca Lim

Research output: Contribution to journalArticle

Abstract

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 (ΔT ≈ 0.25°C per pulse). Afferent spike trains evoked by heat pulse stimuli were diverse and included asynchronous inhibition, asynchronous excitation, and/or phase-locked APs synchronized to each infrared heat pulse. Thermal responses of membrane currents responsible for APs in ganglion neurons were strictly excitatory, with Q10 ≈ 2. 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 (dT/dt) and an inward conduction current driven by ΔT. An iberiotoxin-sensitive inhibitory conduction current was also evoked by ΔT, rising in <3 ms and decaying with a time constant of ~24 ms. The inhibitory component dominated whole cell currents in 50% of hair cells at -68 mV and in 67% of hair cells at -60 mV. Responses were quantified and described on the basis of 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.

Original languageEnglish (US)
Pages (from-to)825-843
Number of pages19
JournalJournal of neurophysiology
Volume116
Issue number2
DOIs
StatePublished - Aug 2016

Keywords

  • Crista ampullaris
  • Heat pulse
  • Infrared neural stimulation
  • Semicircular canals
  • Thermal excitability
  • Vestibular

ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology

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    Rabbitt, R. D., Brichta, A. M., Tabatabaee, H., Boutros, P. J., Ahn, J. H., Della Santina, C. C., Poppi, L. A., & Lim, R. (2016). Heat pulse excitability of vestibular hair cells and afferent neurons. Journal of neurophysiology, 116(2), 825-843. https://doi.org/10.1152/jn.00110.2016