Trpm5 channels encode bistability of spinal motoneurons and ensure motor control of hindlimbs in mice

Nat Commun. 2021 Nov 24;12(1):6815. doi: 10.1038/s41467-021-27113-x.

Abstract

Bistable motoneurons of the spinal cord exhibit warmth-activated plateau potential driven by Na+ and triggered by a brief excitation. The thermoregulating molecular mechanisms of bistability and their role in motor functions remain unknown. Here, we identify thermosensitive Na+-permeable Trpm5 channels as the main molecular players for bistability in mouse motoneurons. Pharmacological, genetic or computational inhibition of Trpm5 occlude bistable-related properties (slow afterdepolarization, windup, plateau potentials) and reduce spinal locomotor outputs while central pattern generators for locomotion operate normally. At cellular level, Trpm5 is activated by a ryanodine-mediated Ca2+ release and turned off by Ca2+ reuptake through the sarco/endoplasmic reticulum Ca2+-ATPase (SERCA) pump. Mice in which Trpm5 is genetically silenced in most lumbar motoneurons develop hindlimb paresis and show difficulties in executing high-demanding locomotor tasks. Overall, by encoding bistability in motoneurons, Trpm5 appears indispensable for producing a postural tone in hindlimbs and amplifying the locomotor output.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology
  • Animals
  • Animals, Newborn
  • Computer Simulation
  • Disease Models, Animal
  • Female
  • Gene Silencing
  • HEK293 Cells
  • Hindlimb / physiology
  • Humans
  • Locomotion / drug effects
  • Locomotion / physiology*
  • Male
  • Mice
  • Motor Neurons / drug effects
  • Motor Neurons / metabolism*
  • Paresis / genetics
  • Paresis / physiopathology*
  • Patch-Clamp Techniques
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Ryanodine / metabolism
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases / antagonists & inhibitors
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases / metabolism
  • Spinal Cord / cytology
  • Spinal Cord / physiology*
  • TRPM Cation Channels / antagonists & inhibitors
  • TRPM Cation Channels / genetics
  • TRPM Cation Channels / metabolism*

Substances

  • Recombinant Proteins
  • TRPM Cation Channels
  • Trpm5 protein, mouse
  • Ryanodine
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases