Proprioceptive coupling within motor neurons drives C. elegans forward locomotion

Neuron. 2012 Nov 21;76(4):750-61. doi: 10.1016/j.neuron.2012.08.039.

Abstract

Locomotion requires coordinated motor activity throughout an animal's body. In both vertebrates and invertebrates, chains of coupled central pattern generators (CPGs) are commonly evoked to explain local rhythmic behaviors. In C. elegans, we report that proprioception within the motor circuit is responsible for propagating and coordinating rhythmic undulatory waves from head to tail during forward movement. Proprioceptive coupling between adjacent body regions transduces rhythmic movement initiated near the head into bending waves driven along the body by a chain of reflexes. Using optogenetics and calcium imaging to manipulate and monitor motor circuit activity of moving C. elegans held in microfluidic devices, we found that the B-type cholinergic motor neurons transduce the proprioceptive signal. In C. elegans, a sensorimotor feedback loop operating within a specific type of motor neuron both drives and organizes body movement.

Publication types

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

MeSH terms

  • Analysis of Variance
  • Animals
  • Animals, Genetically Modified
  • Antiparasitic Agents / pharmacology
  • Caenorhabditis elegans
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Caenorhabditis elegans Proteins / physiology
  • Calcium / metabolism*
  • Central Pattern Generators / cytology
  • Central Pattern Generators / drug effects
  • Cholinergic Neurons / physiology
  • Color
  • GABAergic Neurons / physiology
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Halorhodopsins / genetics
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / physiology
  • Ivermectin / pharmacology
  • Kymography / methods
  • Laser Therapy / methods
  • Light
  • Locomotion / drug effects
  • Locomotion / physiology*
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Microfluidics
  • Models, Biological
  • Motor Neurons / classification
  • Motor Neurons / drug effects
  • Motor Neurons / physiology*
  • Movement
  • Muscle Cells / drug effects
  • Muscle Cells / metabolism
  • Muscle, Skeletal / cytology*
  • Muscle, Skeletal / physiology
  • Mutation / genetics
  • Optogenetics
  • Periodicity
  • Proprioception / drug effects
  • Proprioception / physiology*
  • Rhodopsin / genetics
  • Video Recording

Substances

  • Antiparasitic Agents
  • Caenorhabditis elegans Proteins
  • Halorhodopsins
  • Homeodomain Proteins
  • Luminescent Proteins
  • Membrane Proteins
  • Unc-9 protein, C elegans
  • VAB-7 protein, C elegans
  • red fluorescent protein
  • Green Fluorescent Proteins
  • Ivermectin
  • Rhodopsin
  • Calcium