A wake-active locomotion circuit depolarizes a sleep-active neuron to switch on sleep.
Animals
Arousal
/ physiology
Behavior, Animal
/ physiology
Caenorhabditis elegans
/ physiology
Caenorhabditis elegans Proteins
/ genetics
Calcium
/ metabolism
Homeostasis
Interneurons
/ metabolism
Larva
/ physiology
Locomotion
/ physiology
Neural Pathways
/ physiology
Neurons
/ metabolism
Optogenetics
Sleep Stages
/ physiology
Wakefulness
/ physiology
Journal
PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
15
06
2019
accepted:
23
01
2020
revised:
03
03
2020
pubmed:
23
2
2020
medline:
15
5
2020
entrez:
21
2
2020
Statut:
epublish
Résumé
Sleep-active neurons depolarize during sleep to suppress wakefulness circuits. Wake-active wake-promoting neurons in turn shut down sleep-active neurons, thus forming a bipartite flip-flop switch. However, how sleep is switched on is unclear because it is not known how wakefulness is translated into sleep-active neuron depolarization when the system is set to sleep. Using optogenetics in Caenorhabditis elegans, we solved the presynaptic circuit for depolarization of the sleep-active RIS neuron during developmentally regulated sleep, also known as lethargus. Surprisingly, we found that RIS activation requires neurons that have known roles in wakefulness and locomotion behavior. The RIM interneurons-which are active during and can induce reverse locomotion-play a complex role and can act as inhibitors of RIS when they are strongly depolarized and as activators of RIS when they are modestly depolarized. The PVC command interneurons, which are known to promote forward locomotion during wakefulness, act as major activators of RIS. The properties of these locomotion neurons are modulated during lethargus. The RIMs become less excitable. The PVCs become resistant to inhibition and have an increased capacity to activate RIS. Separate activation of neither the PVCs nor the RIMs appears to be sufficient for sleep induction; instead, our data suggest that they act in concert to activate RIS. Forward and reverse circuit activity is normally mutually exclusive. Our data suggest that RIS may be activated at the transition between forward and reverse locomotion states, perhaps when both forward (PVC) and reverse (including RIM) circuit activity overlap. While RIS is not strongly activated outside of lethargus, altered activity of the locomotion interneurons during lethargus favors strong RIS activation and thus sleep. The control of sleep-active neurons by locomotion circuits suggests that sleep control may have evolved from locomotion control. The flip-flop sleep switch in C. elegans thus requires an additional component, wake-active sleep-promoting neurons that translate wakefulness into the depolarization of a sleep-active neuron when the worm is sleepy. Wake-active sleep-promoting circuits may also be required for sleep state switching in other animals, including in mammals.
Identifiants
pubmed: 32078631
doi: 10.1371/journal.pbio.3000361
pii: PBIOLOGY-D-19-01720
pmc: PMC7053779
doi:
Substances chimiques
Caenorhabditis elegans Proteins
0
Calcium
SY7Q814VUP
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e3000361Subventions
Organisme : Medical Research Council
ID : MR/N004574/1
Pays : United Kingdom
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
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