A spinal organ of proprioception for integrated motor action feedback

Neuron. 2021 Apr 7;109(7):1188-1201.e7. doi: 10.1016/j.neuron.2021.01.018. Epub 2021 Feb 11.

Abstract

Proprioception is essential for behavior and provides a sense of our body movements in physical space. Proprioceptor organs are thought to be only in the periphery. Whether the central nervous system can intrinsically sense its own movement remains unclear. Here we identify a segmental organ of proprioception in the adult zebrafish spinal cord, which is embedded by intraspinal mechanosensory neurons expressing Piezo2 channels. These cells are late-born, inhibitory, commissural neurons with unique molecular and physiological profiles reflecting a dual sensory and motor function. The central proprioceptive organ locally detects lateral body movements during locomotion and provides direct inhibitory feedback onto rhythm-generating interneurons responsible for the central motor program. This dynamically aligns central pattern generation with movement outcome for efficient locomotion. Our results demonstrate that a central proprioceptive organ monitors self-movement using hybrid neurons that merge sensory and motor entities into a unified network.

Keywords: Piezo2; locomotion; motor control; proprioception; spinal cord.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Central Pattern Generators / physiology
  • Feedback, Sensory / physiology*
  • Female
  • Interneurons / physiology
  • Ion Channels / physiology
  • Locomotion / physiology
  • Male
  • Mechanotransduction, Cellular
  • Motor Neurons / physiology
  • Movement / physiology*
  • Nerve Net / cytology
  • Nerve Net / physiology
  • Proprioception / physiology*
  • RNA / genetics
  • Sensory Receptor Cells / physiology
  • Spinal Cord / diagnostic imaging
  • Spinal Cord / physiology
  • Tomography, X-Ray Computed
  • Zebrafish / physiology*
  • Zebrafish Proteins / physiology

Substances

  • Ion Channels
  • Zebrafish Proteins
  • piezo2b protein, zebrafish
  • RNA