Abstract
Animals must slow or halt locomotion to integrate sensory inputs or to change direction. In Caenorhabditis elegans, the GABAergic and peptidergic neuron RIS mediates developmentally timed quiescence. Here, we show RIS functions additionally as a locomotion stop neuron. RIS optogenetic stimulation caused acute and persistent inhibition of locomotion and pharyngeal pumping, phenotypes requiring FLP-11 neuropeptides and GABA. RIS photoactivation allows the animal to maintain its body posture by sustaining muscle tone, yet inactivating motor neuron oscillatory activity. During locomotion, RIS axonal Ca2+ signals revealed functional compartmentalization: Activity in the nerve ring process correlated with locomotion stop, while activity in a branch correlated with induced reversals. GABA was required to induce, and FLP-11 neuropeptides were required to sustain locomotion stop. RIS attenuates neuronal activity and inhibits movement, possibly enabling sensory integration and decision making, and exemplifies dual use of one cell across development in a compact nervous system.
Highlights
Animals must slow or halt locomotion to integrate sensory inputs or to change direction
Neuronal circuits regulate and fine-tune locomotion. While in mammals this is orchestrated by whole-brain systems like motor and prefrontal cortex, cerebellum, and spinal cord neurons, much fewer neurons must fulfill these tasks in compressed nervous systems
We analyzed the role of one neuron, RIS, which orchestrates locomotion slowing and reversals in C. elegans
Summary
Animals must slow or halt locomotion to integrate sensory inputs or to change direction. A class of interneurons in the murine brainstem was shown to induce a stop command for the pattern generation systems[8] These V2a “stop” neurons project to excitatory and inhibitory spinal cord neurons, inducing locomotion halt likely via inhibition of rhythm-generating neurons. The animal does not collapse but rather can quickly resume locomotion Equivalents of these “stop neurons” and systems for slowing were identified in non-limbed vertebrates[9,10] and recently in Drosophila[11], where descending interneurons induce locomotion stop during navigation of odorant gradients, while activity of other neurons causes slowing[12]. Both states are similar with a lack of locomotion and feeding, as well as increased arousal threshold
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