Optimized Tuning of Auditory Inner Hair Cells to Encode Complex Sound through Synergistic Activity of Six Independent K+ Current Entities

Cell Rep. 2020 Jul 7;32(1):107869. doi: 10.1016/j.celrep.2020.107869.

Abstract

Auditory inner hair cells (IHCs) convert sound vibrations into receptor potentials that drive synaptic transmission. For the precise encoding of sound qualities, receptor potentials are shaped by K+ conductances tuning the properties of the IHC membrane. Using patch-clamp and computational modeling, we unravel this membrane specialization showing that IHCs express an exclusive repertoire of six voltage-dependent K+ conductances mediated by Kv1.8, Kv7.4, Kv11.1, Kv12.1, and BKCa channels. All channels are active at rest but are triggered differentially during sound stimulation. This enables non-saturating tuning over a far larger potential range than in IHCs expressing fewer current entities. Each conductance contributes to optimizing responses, but the combined activity of all channels synergistically improves phase locking and the dynamic range of intensities that IHCs can encode. Conversely, hypothetical simpler IHCs appear limited to encode only certain aspects (frequency or intensity). The exclusive channel repertoire of IHCs thus constitutes an evolutionary adaptation to encode complex sound through multifaceted receptor potentials.

Keywords: K(v)1.8; K(v)11.1; K(v)12.1; auditory inner hair cells; electrophysiology; evolutionary adaption; modelling; receptor potentials; sound encoding; voltage-gated K(+) channels/currents.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • 4-Aminopyridine / pharmacology
  • Animals
  • CHO Cells
  • Cricetulus
  • Hair Cells, Auditory, Inner / drug effects
  • Hair Cells, Auditory, Inner / metabolism*
  • Ion Channel Gating / drug effects
  • Membrane Potentials / drug effects
  • Mice, Inbred C57BL
  • Potassium Channels / metabolism*
  • Protein Subunits / metabolism
  • Sound*

Substances

  • Potassium Channels
  • Protein Subunits
  • 4-Aminopyridine