Neuronal mechanism for acute mechanosensitivity in tactile-foraging waterfowl

Proc Natl Acad Sci U S A. 2014 Oct 14;111(41):14941-6. doi: 10.1073/pnas.1413656111. Epub 2014 Sep 22.

Abstract

Relying almost exclusively on their acute sense of touch, tactile-foraging birds can feed in murky water, but the cellular mechanism is unknown. Mechanical stimuli activate specialized cutaneous end organs in the bill, innervated by trigeminal afferents. We report that trigeminal ganglia (TG) of domestic and wild tactile-foraging ducks exhibit numerical expansion of large-diameter mechanoreceptive neurons expressing the mechano-gated ion channel Piezo2. These features are not found in visually foraging birds. Moreover, in the duck, the expansion of mechanoreceptors occurs at the expense of thermosensors. Direct mechanical stimulation of duck TG neurons evokes high-amplitude depolarizing current with a low threshold of activation, high signal amplification gain, and slow kinetics of inactivation. Together, these factors contribute to efficient conversion of light mechanical stimuli into neuronal excitation. Our results reveal an evolutionary strategy to hone tactile perception in vertebrates at the level of primary afferents.

Keywords: Piezo2; TRPM8; TRPV1; mechanotransduction.

Publication types

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

MeSH terms

  • Animals
  • Down-Regulation
  • Ducks / physiology*
  • Feeding Behavior*
  • Ion Channel Gating
  • Ion Channels / metabolism
  • Mechanotransduction, Cellular*
  • Neurons / physiology*
  • Sensory Thresholds
  • TRPM Cation Channels / metabolism
  • TRPV Cation Channels / metabolism
  • Thermoreceptors / metabolism
  • Touch / physiology*
  • Trigeminal Ganglion / physiology
  • Up-Regulation

Substances

  • Ion Channels
  • TRPM Cation Channels
  • TRPV Cation Channels