Proprioceptive Coupling within Motor Neurons Drives C. elegans Forward Locomotion

Abstract

Summary 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.

A proprioceptive neuromechanical theory of crawling

“…The dynamics of the body must be complemented with a muscular programme to induce forward propulsion, via one of two basic circuit strategies: (i) a global CPG for muscle activation with the correct timing and built-in global synchronization between different CPG subunits [6], and (ii) a local feedback mechanism that couples the segment deformation with the muscle activation locally via stretch receptors [7,15]. We start with a discussion of this latter framework, and eventually treat the general case where one or both types of circuit may be at play.…”

“…In the second family (biomechanical models), the focus has been on coupling neural excitation on the motion of the body interacting with the substrate (see [12,13] as examples). Few approaches integrate these different perspectives, although important exceptions are the recent studies of worm locomotion in Caenorhabditis elegans [14,15].…”

Durable spatiotemporal surveillance of Caenorhabditis elegans response to environmental cues

“…Microfluidics has been used for multiple applications in worm biology in recent years 10,11 . These applications include preparing and immobilizing worms for imaging and microsurgery 12 ; rapid control of changes in chemical environment for studies of the chemosensory system 13 ; trapping of worms for quantification of undulatory dynamics 14 ; as well as animal sorting 15 and screening 16 . In particular, several approaches to long-term imaging have been proposed [17][18][19] .…”

Scalable electrophysiology in intact small animals with nanoscale suspended electrode arrays

“…Future work will also help determine if spiking activity originates solely from individual muscle-cell APs; however, the small size of the electrode ensures that it is not in contact with* more than a few muscle cells at the same time, suggesting that activity from only one or two cells dominate the recordings. It should also be noted that the tapered linear channels used for worm immobilization likely reduce muscle cell activity, which is known to depend upon posture and proprioception 35 . Thus, comparisons between immobilized worms may not represent muscle activity in freely moving animals, but is nevertheless sufficient to identify phenotypic differences between mutant strains.…”