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

Yeon, Jihye; Kim, Jinmahn; Kim, Doyoung; Kim, Hyunmin; Kim, Jungha; Du, Eun Jo; Kang, Kyung-In; Lim, Hyun–Ho; Moon, DaeWon; Kim, Kyuhyung

doi:10.1371/journal.pbio.2004929

Cited by 64 publications

(68 citation statements)

References 71 publications

(89 reference statements)

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“…elegans male copulatory circuits contain many anatomical sensorymotor neurons (Jarrell et al, 2012) where experimental evidence supports their sensory-motor functions (LeBoeuf, Correa, Jee, & García, 2014). Nematode neurons without ostensible sensory endings are also capable of forming sensory-motor neurons, such as the stretch-sensitive motor neurons DVA (Li, Feng, Sternberg, & Xu, 2006) and SMD (Yeon et al, 2018). Other relatively simple nervous systems, for example, in the pond snail Helisoma trivolvis (Kuang, Doran, Wilson, Goss, & Goldberg, 2002) and Platynereis larva (Conzelmann et al, 2011) also contain functional sensory-motor neurons.…”

Section: Discussionmentioning

confidence: 99%

The connectome of the Caenorhabditis elegans pharynx

Cook

Crouse

Yemini

et al. 2020

J of Comparative Neurology

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Detailed anatomical maps of individual organs and entire animals have served as invaluable entry points for ensuing dissection of their evolution, development, and function. The pharynx of the nematode Caenorhabditis elegans is a simple neuromuscular organ with a self‐contained, autonomously acting nervous system, composed of 20 neurons that fall into 14 anatomically distinct types. Using serial electron micrograph (EM) reconstruction, we re‐evaluate here the connectome of the pharyngeal nervous system, providing a novel and more detailed view of its structure and predicted function. Contrasting the previous classification of pharyngeal neurons into distinct inter‐ and motor neuron classes, we provide evidence that most pharyngeal neurons are also likely sensory neurons and most, if not all, pharyngeal neurons also classify as motor neurons. Together with the extensive cross‐connectivity among pharyngeal neurons, which is more widespread than previously realized, the sensory‐motor characteristics of most neurons define a shallow network architecture of the pharyngeal connectome. Network analysis reveals that the patterns of neuronal connections are organized into putative computational modules that reflect the known functional domains of the pharynx. Compared with the somatic nervous system, pharyngeal neurons both physically associate with a larger fraction of their neighbors and create synapses with a greater proportion of their neighbors. We speculate that the overall architecture of the pharyngeal nervous system may be reminiscent of the architecture of ancestral, primitive nervous systems.

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Section: Discussionmentioning

confidence: 99%

The connectome of the Caenorhabditis elegans pharynx

Cook

Crouse

Yemini

et al. 2020

J of Comparative Neurology

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“…The somnogenic RPamide NLP-22 is expressed in a different site, the glutamatergic RIA interneurons 41 , which have no direct synaptic connections to AWA sensory neurons, but are also involved in sensorimotor integration and olfactory steering ( Supplementary Fig. S10) 97,98 . The NLP-22 receptor GNRR-6 is expressed in sublateral motor neurons and interneurons that project along the ventral nerve cord, which suggests a role in locomotion quiescence.…”

Section: Discussionmentioning

confidence: 99%

RPamide neuropeptides NLP-22 and NLP-2 act through GnRH-like receptors to promote sleep and wakefulness in C. elegans

Auwera

Frooninckx

Buscemi

et al. 2020

Sci Rep

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Sleep and wakefulness are fundamental behavioral states of which the underlying molecular principles are becoming slowly elucidated. Transitions between these states require the coordination of multiple neurochemical and modulatory systems. In Caenorhabditis elegans sleep occurs during a larval transition stage called lethargus and is induced by somnogenic neuropeptides. Here, we identify two opposing neuropeptide/receptor signaling pathways: NLP-22 promotes behavioral quiescence, whereas NLP-2 promotes movement during lethargus, by signaling through gonadotropin-releasing hormone (GnRH) related receptors. Both NLP-2 and NLP-22 belong to the RPamide neuropeptide family and share sequence similarities with neuropeptides of the bilaterian GnRH, adipokinetic hormone (AKH) and corazonin family. RPamide neuropeptides dose-dependently activate the GnRH/AKH-like receptors GNRR-3 and GNRR-6 in a cellular receptor activation assay. In addition, nlp-22-induced locomotion quiescence requires the receptor gnrr-6. By contrast, wakefulness induced by nlp-2 overexpression is diminished by deletion of either gnrr-3 or gnrr-6. nlp-2 is expressed in a pair of olfactory AWA neurons and cycles with larval periodicity, as reported for nlp-22, which is expressed in RIA. Our data suggest that the somnogenic NLP-22 neuropeptide signals through GNRR-6, and that both GNRR-3 and GNRR-6 are required for the wake-promoting action of NLP-2 neuropeptides. Sleep is an essential quiescent state, conserved at the molecular level across distantly related animals 1-5. Because animals display a remarkable diversity of sleep traits, a consensus definition for sleep-like states has been set based on behavioral changes shared with human sleep. These include behavioral quiescence, reduced sensory responsiveness, reversibility, the assumption of a specific posture, and homeostatic regulation 1,4,6,7. Sleep deprivation is detrimental to diverse biological processes, including metabolism, longevity, and memory formation 8-11. Genetic studies in model organisms such as mice, zebrafish, Drosophila and C. elegans have provided powerful ways to dissect core mechanisms of sleep-like states that are evolutionarily conserved across these species 1-3,6,10. A well-known example is the circadian protein PERIOD that regulates the timing of sleep 12,13. Other conserved sleep pathways include epidermal growth factor (EGF) and notch signaling 14-16. Conserved wake-promoting pathways include dopamine and pigment dispersing factor (PDF) signaling 17-19. How these sleep and wake pathways interact is still unclear (for review, see 3,4,18). Mounting evidence indicates that sleep-wake transitions require the coordination of several brain regions and engage multiple neurochemical systems, including biogenic amines 1,17,20 and neuropeptides 19,21. In mammals, hypothalamic orexin/hypocretin neuropeptides promote

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“…While the importance of proprioception is well established in controlling posture and locomotion in a variety of limbless and legged species [4,[48][49][50][51], the roles of proprioception in shaping motor patterns in peripheral and central nervous systems is not well understood. In C. elegans, proprioception has been studied primarily with a focus on posture or locomotion [22][23][24][25][26][27][28]52]. Although the neural circuitry of C. elegans is fully mapped, the precise pattern generating mechanism responsible for locomotion remains undetermined.…”

Section: Discussionmentioning

confidence: 99%

Signatures of proprioceptive control inCaenorhabditis eleganslocomotion

Denham¹,

Ranner²,

Cohen³

2018

Phil. Trans. R. Soc. B

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Animal neuromechanics describes the coordinated self-propelled movement of a body, subject to the combined effects of internal neural control and mechanical forces. Here we use a computational model to identify effects of neural and mechanical modulation on undulatory forward locomotion of , with a focus on proprioceptively driven neural control. We reveal a fundamental relationship between body elasticity and environmental drag in determining the dynamics of the body and demonstrate the manifestation of this relationship in the context of proprioceptively driven control. By considering characteristics unique to proprioceptive neurons, we predict the signatures of internal gait modulation that contrast with the known signatures of externally or biomechanically modulated gait. We further show that proprioceptive feedback can suppress neuromechanical phase lags during undulatory locomotion, contrasting with well studied advancing phase lags that have long been a signature of centrally generated, feed-forward control.This article is part of a discussion meeting issue 'Connectome to behaviour: modelling at cellular resolution'.

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

Cited by 64 publications

References 71 publications

The connectome of the Caenorhabditis elegans pharynx

The connectome of the Caenorhabditis elegans pharynx

RPamide neuropeptides NLP-22 and NLP-2 act through GnRH-like receptors to promote sleep and wakefulness in C. elegans

Signatures of proprioceptive control inCaenorhabditis eleganslocomotion

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