Analysis of the NK2 homeobox gene ceh-24 reveals sublateral motor neuron control of left-right turning during sleep

Abstract

Sleep is a behavior that is found in all animals that have a nervous system and that have been studied carefully. In Caenorhabditis elegans larvae, sleep is associated with a turning behavior, called flipping, in which animals rotate 180° about their longitudinal axis. However, the molecular and neural substrates of this enigmatic behavior are not known. Here, we identified the conserved NK-2 homeobox gene ceh-24 to be crucially required for flipping. ceh-24 is required for the formation of processes and for cholinergic function of sublateral motor neurons, which separately innervate the four body muscle quadrants. Knockdown of cholinergic function in a subset of these sublateral neurons, the SIAs, abolishes flipping. The SIAs depolarize during flipping and their optogenetic activation induces flipping in a fraction of events. Thus, we identified the sublateral SIA neurons to control the three-dimensional movements of flipping. These neurons may also control other types of motion.DOI: http://dx.doi.org/10.7554/eLife.24846.001

A sensory-motor neuron type mediates proprioceptive coordination of steering in C. elegans via two TRPC channels

“…Since the oscillatory calcium transients of SMDD and SMDV are synchronized in the trp-1 trp-2 mutants, we next asked whether the simultaneous activation of SMDD and SMDV can induce a locomotion pattern that mimics the defect of the trp-1 trp-2 mutants. We performed optogenetic experiments using transgenic animals that express the channelrhodopsin variant ReaChR::mKate2 in the SMDD/V neurons under the control of the lad-2 p- Δ 1 promoter [ 42 , 43 ]. The lad-2 p- Δ 1 promoter is expressed in ALN, PLN, SAA, SDQ, and SMDD/V ( S7C Fig ).…”

“…0.5 ng of each transgene was injected with 50 ng of unc-122 p:: dsRed as an injection marker. lad-2 p- Δ 1 and myo-3 p were inserted into the ReaChR::mKate2 vector (a gift from Henrik Bringmann) [ 42 , 43 ], and 100 ng of each transgene was injected with 50 ng of unc-122 p:: dsRed or unc-122 p:: gfp as an injection marker, respectively.…”

Nematode Autotomy Requires Molting and Entails Tissue Healing without Obvious Regeneration

“…The observation of twisted links between segments of incompletely autotomized worms revealed a plausible mechanical explanation for autotomy, whereby twisting squeezes the soft body of the worm down to a point where segments can be separated by pinching off. The lethargus-associated flipping that precedes molting [11] was found to be unnecessary for autotomy, but twisting movements can still occur in flipping-defective mutants. Twisting may provide a means of severing body parts for other soft-bodied invertebrates.…”

“…If the posterior end of a molting worm were to be immobilized in a worm-star, the flipping might provide enough mechanical force to twist the worm and create a constriction, followed by severance. Recent work on flipping during lethargus has defined the neuroanatomical basis of this behavior, and demonstrated that the homeobox gene ceh-24 is required for the formation of the necessary processes and cholinergic function in the relevant SIA motor neurons [11]. Mutants of this gene are defective in flipping during lethargus but otherwise almost normal.…”

“…Surprisingly, they exhibit no abnormality or delay in molting. Two deletion mutants of ceh-24 and a mutant of the lethargus regulator aptf-1 [11] were tested and found to be fully competent for autotomy, demonstrating that lethargus-associated flipping is not essential for autotomy. However, the worms carrying these mutations were still seen to be writhing around each other in three dimensions when trapped in worm-stars, so the twisting mechanism for autotomy remains plausible.…”