A wake-active locomotion circuit depolarizes a sleep-active neuron to switch on sleep

Autor: Judith Besseling, Michal Turek, Henrik Bringmann, Inka Busack, Elisabeth Maluck, Florentin Masurat, Karl Emanuel Busch
Jazyk: angličtina
Rok vydání: 2020
Předmět:
0301 basic medicine
Life Cycles
Physiology
Polymers
0302 clinical medicine
Larvae
Animal Cells
Neural Pathways
Medicine and Health Sciences
Homeostasis
Biology (General)
Polyvinyl Chloride
Materials
Caenorhabditis elegans
Neurons
0303 health sciences
Brain Mapping
Behavior
Animal
Chemistry
General Neuroscience
Depolarization
Sleep in non-human animals
Electrophysiology
medicine.anatomical_structure
Bioassays and Physiological Analysis
Macromolecules
Larva
Physical Sciences
Wakefulness
Sleep Stages
Cellular Types
General Agricultural and Biological Sciences
Arousal
Shut down
Locomotion
Research Article
Sleep induction
QH301-705.5
Materials Science
Biology
Optogenetics
Research and Analysis Methods
Membrane Potential
General Biochemistry
Genetics and Molecular Biology
03 medical and health sciences
Interneurons
medicine
Animals
Caenorhabditis elegans Proteins
030304 developmental biology
General Immunology and Microbiology
Biological Locomotion
Biology and Life Sciences
Cell Biology
Neurophysiological Analysis
Forward locomotion
biology.organism_classification
Polymer Chemistry
030104 developmental biology
Cellular Neuroscience
Calcium
Neuron
Physiological Processes
Sleep
Neuroscience
030217 neurology & neurosurgery
Developmental Biology
Zdroj: PLoS Biology, Vol 18, Iss 2, p e3000361 (2020)
PLoS Biology
Maluck, E, Busack, I, Besseling, J, Turek, M, Busch, E & Bringmann, H 2020, ' A wake-active locomotion circuit depolarizes a sleep-active neuron to switch on sleep ', PLoS Biology . https://doi.org/10.1371/journal.pbio.3000361
ISSN: 1545-7885
1544-9173
DOI: 10.1371/journal.pbio.3000361
Popis: 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.
This study in nematodes shows that to understand sleep state switching, the flip-flop model for sleep regulation needs to be complemented by additional wake-active sleep-promoting neurons that activate sleep-active sleep-promoting neurons to induce sleep.
Databáze: OpenAIRE
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