Cited by 536Sleep and Wakefulness ResearchNeurobiology and Insect Physiology ResearchCircadian rhythm and melatonin

The DOI matches its Crossref record; 31 of the 31 references it cites were found in a registry or an index.

Lethargus is a Caenorhabditis elegans sleep-like state

Raizen, David M., Zimmerman, John E., Maycock, Matthew H., Ta, Uyen D., You, Young-jai, Sundaram, Meera V., Pack, Allan I.·2008·Nature

DOI 10.1038/nature06535

Open this paper in CoChat — free account

Abstract

There are fundamental similarities between sleep in mammals and quiescence in the arthropod Drosophila melanogaster, suggesting that sleep-like states are evolutionarily ancient. The nematode Caenorhabditis elegans also has a quiescent behavioural state during a period called lethargus, which occurs before each of the four moults. Like sleep, lethargus maintains a constant temporal relationship with the expression of the C. elegans Period homologue LIN-42 (ref. 5). Here we show that quiescence associated with lethargus has the additional sleep-like properties of reversibility, reduced responsiveness and homeostasis. We identify the cGMP-dependent protein kinase (PKG) gene egl-4 as a regulator of sleep-like behaviour, and show that egl-4 functions in sensory neurons to promote the C. elegans sleep-like state. Conserved effects on sleep-like behaviour of homologous genes in C. elegans and Drosophila suggest a common genetic regulation of sleep-like states in arthropods and nematodes. Our results indicate that C. elegans is a suitable model system for the study of sleep regulation. The association of this C. elegans sleep-like state with developmental changes that occur with larval moults suggests that sleep may have evolved to allow for developmental changes.

Integrity signals

Registry

Crossref · 10.1038/nature06535

Cites

31 of 31 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Two-Process Model of Sleep Regulation
Binder, M. D., Hirokawa, N., & Windhorst, U. (2008) · Springer eBooks · doi:10.1007/978-3-540-29678-2_6166 · Cited by 3,900
Hormones, Brain and Behavior
(2009) · Elsevier eBooks · doi:10.1016/c2009-1-03789-7 · Cited by 1,543
Correlates of Sleep and Waking in Drosophila melanogaster
Shaw, P. J., Cirelli, C., Greenspan, R. J., & Tononi, G. (2000) · Science · doi:10.1126/science.287.5459.1834 · Cited by 1,300
Rest in Drosophila is a sleep-like state
Hendricks, J. C., Finn, S. M., Panckeri, K. A., Chavkin, J., Williams, J. A., Sehgal, A., & Pack, A. I. (2000) · Neuron · doi:10.1016/s0896-6273(00)80877-6 · Cited by 1,050
Self-citation
The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans
Cassada, R. C., & Russell, R. L. (1975) · Developmental Biology · doi:10.1016/0012-1606(75)90109-8 · Cited by 914
Natural Behavior Polymorphism Due to a cGMP-Dependent Protein Kinase of Drosophila
Osborne, K. A., Robichon, A., Burgess, E., Butland, S. L., Shaw, R. A., Coulthard, A. B., Pereira, H. S., Greenspan, R. J., & Sokolowski, M. B. (1997) · Science · doi:10.1126/science.277.5327.834 · Cited by 532
Sleep Enhances Plasticity in the Developing Visual Cortex
Frank, M. G., Issa, N. P., & Stryker, M. P. (2001) · Neuron · doi:10.1016/s0896-6273(01)00279-3 · Cited by 523
The genetics of feeding in Caenorhabditis elegans.
Avery, L. (1993) · Genetics · doi:10.1093/genetics/133.4.897 · Cited by 500
Reprogramming Chemotaxis Responses: Sensory Neurons Define Olfactory Preferences in C. elegans
Troemel, E. R., Kimmel, B. E., & Bargmann, C. I. (1997) · Cell · doi:10.1016/s0092-8674(00)80399-2 · Cited by 464
Sleep Homeostasis in Drosophila Melanogaster
Huber, R., Hill, S., Holladay, C., Biesiadecki, M., Tononi, G., & Cirelli, C. (2004) · SLEEP · doi:10.1093/sleep/27.4.628 · Cited by 412

Flagged first, then by citations

Show all 31 references

Sorted by citations

Items 301–400 of 523

Structural neuroplasticity after sleep loss modifies behavior and requires neurexin and neuroligin
Cowen, M. H., Raizen, D. M., & Hart, M. P. (2024) · iScience · doi:10.1016/j.isci.2024.109477 · Cited by 14
Self-citation
Sleeping Beauty? Developmental Timing, Sleep, and the Circadian Clock in Caenorhabditis elegans
Olmedo, M., Merrow, M. W., & Geibel, M. (2017) · Advances in genetics · doi:10.1016/bs.adgen.2017.05.001 · Cited by 12
Thick cuticles as an anti-predator defence in nematodes
Ichiishi, K., Ekino, T., Kanzaki, N., & Shinya, R. (2021) · Nematology · doi:10.1163/15685411-bja10107 · Cited by 11
Pigment‐dispersing factor signaling in the circadian system of Caenorhabditis elegans
Herrero, A., Romanowski, A., Meelkop, E., Caldart, C. S., Schoofs, L., & Golombek, D. A. (2015) · Genes Brain & Behavior · doi:10.1111/gbb.12231 · Cited by 11
Automated analysis of sleep control via a single neuron active at sleep onset in C. elegans
Urmersbach, B., Besseling, J., Spies, J., & Bringmann, H. (2016) · genesis · doi:10.1002/dvg.22924 · Cited by 11
C. elegans episodic swimming is driven by multifractal kinetics
Ikeda, Y., Jurica, P., Kimura, H., Takagi, H., Struzik, Z. R., Kiyono, K., Arata, Y., & Sako, Y. (2020) · Scientific Reports · doi:10.1038/s41598-020-70319-0 · Cited by 11
To sleep, perchance to live
Hunter, P. (2008) · EMBO Reports · doi:10.1038/embor.2008.197 · Cited by 11
The evolution of sleep is inevitable in a periodic world
Field, J. M., & Bonsall, M. B. (2018) · PLoS ONE · doi:10.1371/journal.pone.0201615 · Cited by 11
Sleep in Animals
Siegel, J. M. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-24288-2.00010-6 · Cited by 12
Pharmacological and molecular dynamics analyses of differences in inhibitor binding to human and nematode PDE4: Implications for management of parasitic nematodes
Schuster, K. D., Mohammadi, M., Cahill, K. B., Matte, S. L., Maillet, A. D., Vashisth, H., & Cote, R. (2019) · PLoS ONE · doi:10.1371/journal.pone.0214554 · Cited by 11
Analysis of the NK2 homeobox gene ceh-24 reveals sublateral motor neuron control of left-right turning during sleep
Schwarz, J., & Bringmann, H. (2017) · eLife · doi:10.7554/elife.24846 · Cited by 10
“Animals during lethargus motion bouts are more responsive to stimulation compared with animals during a quiescence bout yet have dampened sensory neuron activity and reduced body curvature compared with animals outside of lethargus (Iwanir et al., 2013; Raizen et al., 2008; Schwarz et al., 2011; Cho and Sternberg, 201…”
Background
Four novel sleep-promoting peptides screened and identified from bovine casein hydrolysates using a patch-clamp model in vitro and Caenorhabditis elegans in vivo
Chen, Y., Xu, L., Lan, Y., Liang, C., Liu, X., Li, J., Liu, F., Miao, J., Chen, Y., Cao, Y., et al. (2023) · Food & Function · doi:10.1039/d3fo01246h · Cited by 10
Appetite control: worm's-eye-view
You, Y., & Avery, L. (2012) · Animal Cells and Systems · doi:10.1080/19768354.2012.716791 · Cited by 12
Self-citation
Bioelectronics for Millimeter-Sized Model Organisms
Gonzales, D. L., Badhiwala, K. N., Avants, B. W., & Robinson, J. T. (2020) · iScience · doi:10.1016/j.isci.2020.100917 · Cited by 10
Job switching in ants
Lucas, C., Hughson, B. N., & Sokolowski, M. B. (2010) · Communicative & Integrative Biology · doi:10.4161/cib.3.1.9723 · Cited by 10
Sleep: Dozy Worms and Sleepy Flies
Olofsson, B., & de Bono, M. (2008) · Current Biology · doi:10.1016/j.cub.2008.01.002 · Cited by 10
A Simple Light Stimulation of Caenorhabditis elegans
Lee, K. H., & Aschner, M. (2016) · Current Protocols in Toxicology · doi:10.1002/0471140856.tx1121s67 · Cited by 10
Genetics of Behavior in C. elegans
Walker, D. S., Chew, Y. L., & Schafer, W. R. (2017) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780190456757.013.5 · Cited by 10
Evolution of the acoustic startle response of Mexican cavefish
Paz, A., McDole, B., Kowalko, J. E., Duboué, E. R., & Keene, A. C. (2020) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22988 · Cited by 10
Adaptive evolution of stress response genes in parasites aligns with host niche diversity
Cruz-Laufer, A. J., Vanhove, M. P. M., Bachmann, L., Barson, M., Bassirou, H., Nyom, A. R. B., Geraerts, M., Hahn, C., Huyse, T., Kasembele, G. K., et al. (2025) · BMC Biology · doi:10.1186/s12915-024-02091-w · Cited by 9
Quiescence Enhances Survival during Viral Infection inCaenorhabditis elegans
Iannacone, M. J., Um, P., Grubbs, J. J., van der Linden, A. M., & Raizen, D. M. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1700-22.2024 · Cited by 11
Self-citation
The Sleep in Caenorhabditis elegans: What We Know Until Now
Moosavi, M., & Hatam, G. (2017) · Molecular Neurobiology · doi:10.1007/s12035-016-0362-9 · Cited by 10
aptf-1 mutants are primarily defective in head movement quiescence during C. elegans sleep
Robinson, B., Goetting, D. L., Desir, J. C., & Buskirk, C. V. (2019) · PubMed Central · doi:10.17912/micropub.biology.000148 · Cited by 9
Metabolomic and pharmacologic analyses of brain substances associated with sleep pressure in mice
Suzuki-Abe, H., Sonomura, K., Nakata, S., Miyanishi, K., Mahmoud, A. A., Hotta-Hirashima, N., Miyoshi, C., Sato, T., Funato, H., & Yanagisawa, M. (2021) · Neuroscience Research · doi:10.1016/j.neures.2021.11.008 · Cited by 9
Non-mammalian Genetic Model Systems in Sleep Research
Raizen, D. M., & Zimmerman, J. E. (2011) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2011.04.005 · Cited by 9
Self-citation
Forward genetic approach for behavioral neuroscience using animal models
Funato, H. (2020) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.96.002 · Cited by 9
Differential Gene Expression in Brain and Liver Tissue of Wistar Rats after Rapid Eye Movement Sleep Deprivation
Pandey, A., Oliver, R., & Kar, S. K. (2020) · Clocks & Sleep · doi:10.3390/clockssleep2040033 · Cited by 9
Using neurons to maintain autonomy: Learning from C. elegans
Bechtel, W., & Bich, L. (2023) · Biosystems · doi:10.1016/j.biosystems.2023.105017 · Cited by 8
Harnessing Simple Animal Models to Decode Sleep Mysteries
Pandi-Perumal, S. R., Saravanan, K. M., Paul, S., & Chidambaram, S. B. (2024) · Molecular Biotechnology · doi:10.1007/s12033-024-01318-z · Cited by 8
Sleep, Immunity, and Stress: Novel Insights From Drosophila
Williams, J. A. (2019) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-813743-7.00023-2 · Cited by 8
A robotic system for automated genetic manipulation and analysis ofCaenorhabditis elegans
Li, Z., Fouad, A. D., Bowlin, P. D., Fan, Y., He, S., Chang, M.-C., Du, A., Teng, C., Kassouni, A., Ji, H., et al. (2023) · PNAS Nexus · doi:10.1093/pnasnexus/pgad197 · Cited by 8
Self-citation
Role for neuronal nitric oxide synthase in sleep homeostasis and arousal
Greene, R. W. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1319863110 · Cited by 8
Investigating the Evolution of Sleep in the Mexican Cavefish
Duboué, E. R., & Keene, A. C. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-802148-4.00015-3 · Cited by 8
The existence of two states of sleep as a common trait in various animals and its molecular and neuronal mechanisms
Kashiwagi, M., & Hayashi, Y. (2020) · Current Opinion in Physiology · doi:10.1016/j.cophys.2020.03.007 · Cited by 8
DoC. elegansSleep? A Closer Look
Singh, K., Huang, H., & Hart, A. C. (2013) · SLEEP · doi:10.5665/sleep.2436 · Cited by 8
Sleep regulation in Drosophila: a review of neural circuits and genetics
Zhao, Y., Zhang, K., Bian, H., Ma, X., Wang, S., Wang, Y., Yu, S., & Huang, L. (2026) · Frontiers in Neuroscience · doi:10.3389/fnins.2026.1750211 · Cited by 8
Sleep circuits and physiology in non-mammalian systems
Lyons, D. G., & Rihel, J. (2020) · Current Opinion in Physiology · doi:10.1016/j.cophys.2020.03.006 · Cited by 8
Stereotyped behavioral maturation and rhythmic quiescence in C. elegans embryos
Ardiel, E. L., Lauziere, A., Xu, S., Harvey, B. J., Christensen, R. P., Nurrish, S., Kaplan, J. M., & Shroff, H. (2022) · eLife · doi:10.7554/elife.76836 · Cited by 7
High-throughput submicron-resolution microscopy of Caenorhabditis elegans populations under strong immobilization by cooling cultivation plates
Wang, Y. L., Grooms, N. W. F., Jaklitsch, E. L., Schulting, L. G., & Chung, S. (2023) · iScience · doi:10.1016/j.isci.2023.105999 · Cited by 7
Development Features on the Selection of Animal Models for Teratogenic Testing
Alves‐Pimenta, S., Colaço, B., Oliveira, P. A., & Venâncio, C. A. S. (2024) · Methods in molecular biology · doi:10.1007/978-1-0716-3625-1_3 · Cited by 7
Postnatal persistence of episodic spontaneous rapid-body-movement bursts and twitches in the cuttlefish, Sepia officinalis
Corner, M. A. (2013) · Behaviour · doi:10.1163/1568539x-00003091 · Cited by 7
High‐Throughput Analysis of Behavior Under the Control of Optogenetics in Caenorhabditis elegans
Yu, A. J., McDiarmid, T. A., Ardiel, E. L., & Rankin, C. H. (2018) · Current Protocols in Neuroscience · doi:10.1002/cpns.57 · Cited by 7
A quiescent state following mild sensory arousal in Caenorhabditis elegans is potentiated by stress
McClanahan, P. D., Dubuque, J. M., Kontogiorgos-Heintz, D., Habermeyer, B. F., Xu, J. H., Ma, A. M., Raizen, D. M., & Fang-Yen, C. M. (2020) · Scientific Reports · doi:10.1038/s41598-020-60994-4 · Cited by 7
Self-citation
Diet-responsive transcriptional regulation of insulin in a single neuron controls systemic metabolism
Handley, A., Wu, Q., Sherry, T., Cornell, R., & Pocock, R. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001655 · Cited by 7
The interplay between Caenorhabditis elegans larval development and Orsay virus infection
Melero, Í., Castiglioni, V. G., Olmo-Uceda, M. J., Villena-Giménez, A., Olmedo, M., González, R., & Elena, S. F. (2025) · iScience · doi:10.1016/j.isci.2025.114193 · Cited by 6
Automated multimodal imaging of Caenorhabditis elegans behavior in multi-well plates
Ji, H., Chen, D., & Fang-Yen, C. M. (2024) · Genetics · doi:10.1093/genetics/iyae158 · Cited by 6
Circadian Rhythm Mechanisms Underlying Convergent Adaptation of Unihemispheric Slow-Wave Sleep in Marine Mammals
Yin, D., Yu, Z., Jiang, H., Chong, Y., Zhong, C., Xu, S., & Yang, G. (2024) · Molecular Biology and Evolution · doi:10.1093/molbev/msae257 · Cited by 6
G protein-coupled receptor kinase-2 (GRK-2) controls exploration through neuropeptide signaling in Caenorhabditis elegans
Davis, K. C., Mitchell, C., Weissenfels, O., Bai, J., Raizen, D. M., Ailion, M., & Topalidou, I. (2023) · PLoS Genetics · doi:10.1371/journal.pgen.1010613 · Cited by 6
Self-citation
Small-molecule screening in aged Drosophila identifies mGluR as a regulator of age-related sleep impairment
Hou, X., Hayashi, R., Itoh, M., & Tonoki, A. (2023) · SLEEP · doi:10.1093/sleep/zsad018 · Cited by 6
Abnormal behavioral episodes associated with sleep and quiescence in Octopus insularis : Possible nightmares in a cephalopod?Preprint
Ramos, E. A., Steinblatt, M., Demsey, R., Reiss, D., & Magnasco, M. O. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.11.540348 · Cited by 6
The cGMP‐dependent protein kinase gene can regulate trail‐following behaviour and locomotion in the termite Reticulitermes chinensis Snyder
Xu, H., Yu, Y., Gao, Y., Hassan, A., Jia, B., & Huang, Q. (2022) · Insect Molecular Biology · doi:10.1111/imb.12781 · Cited by 5
Reverse genetic screening during L1 arrest reveals a role of the diacylglycerol kinase 1 gene dgk-1 and sphingolipid metabolism genes in sleep regulation
Koutsoumparis, A., Busack, I., Chen, C., Hayashi, Y., Braeckman, B. P., Meierhofer, D., & Bringmann, H. (2023) · Genetics · doi:10.1093/genetics/iyad124 · Cited by 5
Repurposing the Killing Machine: Non-canonical Roles of the Cell Death Apparatus in Caenorhabditis elegans Neurons
Juanez, K., & Ghose, P. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.825124 · Cited by 5
Sleep and its possible role in learning: a phylogenetic view
Piscopo, S. (2009) · Frontiers in Bioscience-Elite · doi:10.2741/e36 · Cited by 5
Insulin signaling and osmotic stress response regulate arousal and developmental progression of C. elegans at hatching
Bayer, E. A., Liberatore, K. M., Schneider, J. R., Schlesinger, E., He, Z., Birnbaum, S. K., & Wightman, B. (2021) · Genetics · doi:10.1093/genetics/iyab202 · Cited by 5
The neuropeptide receptor npr-38 regulates avoidance and stress-induced sleep in Caenorhabditis elegans
Le, E., McCarthy, T., Honer, M. A., Curtin, C. E., Fingerut, J. T., & Nelson, M. D. (2023) · Current Biology · doi:10.1016/j.cub.2023.06.042 · Cited by 5
Unsupervised Learning Facilitates Neural Coordination Across the Functional Clusters of the C. elegans Connectome
Morales, A., & Froese, T. (2020) · Frontiers in Robotics and AI · doi:10.3389/frobt.2020.00040 · Cited by 5
Discriminating between sleep and exercise-induced fatigue using computer vision and behavioral genetics
Schuch, K. N., Govindarajan, L. N., Guo, Y., Baskoylu, S., Kim, S. Y., Kimia, B. B., Serre, T., & Hart, A. C. (2020) · Journal of Neurogenetics · doi:10.1080/01677063.2020.1804565 · Cited by 5
Erratum: Lethargus is a Caenorhabditis elegans sleep-like state
Raizen, D. M., Zimmerman, J. E., Maycock, M. H., Ta, U. D., You, Y., Sundaram, M. V., & Pack, A. I. (2008) · Nature · doi:10.1038/nature07044 · Cited by 5
Self-citation
Rethinking Neuroscientific Methodology: Lived Experience in Behavioral Studies
Nemati, N. (2024) · Biological Theory · doi:10.1007/s13752-024-00460-w · Cited by 4
A familial natural short sleep mutation in dec2 extends healthspan and lifespan in Drosophila
Pandey, P., Wall, P. K., Lopez, S. R., Zunica, E. R. M., Dubuisson, O. S., Dantas, W. S., Davuluri, G., Taylor, A. L., Wall, T. K., Juge, H. J., et al. (2025) · iScience · doi:10.1016/j.isci.2025.113388 · Cited by 4
Track-A-Worm 2.0: A Software Suite for Quantifying Properties of C. elegans Locomotion, Bending, Sleep, and Action Potentials
Vedantham, K., Niu, L., Ma, R., Connelly, L., Nagella, A., Wang, S. J., & Wang, Z. (2025) · eNeuro · doi:10.1523/eneuro.0224-25.2025 · Cited by 4
Circadian regulation of locomotion, respiration, and arousability in adult blacklegged ticks (Ixodes scapularis)
Marshall, J. P., Marinko, E., To, A., Morejon, J. L., Joshi, R., Shea, J., Gibbs, A. G., & Meiselman, M. R. (2024) · Scientific Reports · doi:10.1038/s41598-024-65498-z · Cited by 4
Accelerated hermaphrodite maturation on male pheromones suggests a general principle of coordination between larval behavior and development
Faerberg, D. F., Zucker-Aprison, E., & Ruvinsky, I. (2024) · Development · doi:10.1242/dev.202961 · Cited by 4
In vivo Toxicity Evaluation of a Nano-drug Delivery System Using a Caenorhabditis elegans Model System
Han, W., Li, H., Yu, X., Ke, J., Guo, F., & Wang, L. (2021) · Chemical Research in Chinese Universities · doi:10.1007/s40242-021-1257-5 · Cited by 4
Forward genetic screen of Caenorhabditis elegans mutants with impaired sleep reveals a crucial role of neuronal diacylglycerol kinase DGK-1 in regulating sleep
Chen, C., Kawano, T., Yanagisawa, M., & Hayashi, Y. (2023) · Genetics · doi:10.1093/genetics/iyad140 · Cited by 4
The foraging gene affects alcohol sensitivity, metabolism and memory in Drosophila
Oepen, A. S., Catalano, J. L., Azanchi, R., & Kaun, K. R. (2021) · Journal of Neurogenetics · doi:10.1080/01677063.2021.1931178 · Cited by 4
Sleep- and Wake-Like States in Small Networks In Vivo and In Vitro
McKillop, L. E., & Vyazovskiy, V. V. (2018) · Handbook of experimental pharmacology · doi:10.1007/164_2018_174 · Cited by 4
Sleep: Findings in Invertebrates and Lower Vertebrates
Jha, V. M., & Jha, S. K. (2020) · Springer eBooks · doi:10.1007/978-981-15-7175-6_2 · Cited by 4
Multifaceted role of galanin in brain excitabilityPreprint
Rieser, N. N., Ronchetti, M., Hotz, A. L., & Neuhauss, S. C. F. (2024) · eLife · doi:10.7554/elife.98634.4 · Cited by 4
Anesthesia isn’t sleep: The neuronal dynamics of immobility in isoflurane-anesthetized C. elegans differ from the activity patterns of previously established sleep-like quiescent states
Chang, A. S., Mazuera, L., Gabel, C. V., & Connor, C. W. (2025) · PLoS ONE · doi:10.1371/journal.pone.0324323 · Cited by 3
Regulation of the sperm‐to‐oocyte transition in Caenorhabditis briggsae hermaphrodites by the Cbr‐met‐2 and Cbr‐fem‐3 genes
Berenson, A. L., & Baird, S. E. (2018) · Molecular Reproduction and Development · doi:10.1002/mrd.22991 · Cited by 3
Motivated displacement assay distinguishes ALA neuron mutants from RIS neuron mutants during recovery from heat stress in Caenorhabditis elegans
Chávez-Pérez, C., Jafari, N., Keenan, B. T., Raizen, D. M., & Rohacek, A. M. (2021) · Europe PMC (PubMed Central) · doi:10.17912/micropub.biology.000468 · Cited by 3
Self-citation
Ontogeny of sleeping behaviour in four solitary species of Anolis lizard
Barnett, J., & Poe, S. (2023) · Behaviour · doi:10.1163/1568539x-bja10237 · Cited by 3
Drosophilamodel systems for genetic sleep research
Dissel, S., & Shaw, P. J. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139649469.007 · Cited by 3
Glia in Invertebrate Models: Insights from Caenorhabditis elegans
Purice, M. D., Severs, L. J., & Singhvi, A. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-64839-7_2 · Cited by 3
A Core Process in Receptor Function, General Anesthesia, Sleep, and Aging
Kier, L. B., & Slattum, P. W. (2012) · Chemistry & Biodiversity · doi:10.1002/cbdv.201100357 · Cited by 3
SLEEPLESS‐ness and Insomnia in Fruit Flies
Treweek, J. B., Moreno, A. Y., & Janda, K. D. (2008) · Angewandte Chemie International Edition · doi:10.1002/anie.200804552 · Cited by 3
NemaCount: quantification of nematode chemotaxis behavior in a browser
O’Halloran, D. M. (2016) · Invertebrate Neuroscience · doi:10.1007/s10158-016-0188-1 · Cited by 3
Biological Concerns on the Selection of Animal Models for Teratogenic Testing
Alves‐Pimenta, S., Colaço, B., Oliveira, P. A., & Venâncio, C. A. S. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-7883-0_3 · Cited by 3
The Role of Glia in Sleep-Wake Regulation and Function
Frank, M. G. (2019) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-813743-7.00013-x · Cited by 3
Genetic Mechanisms Underlying SleepPreprint
Toda, H., Shi, M., Williams, J. A., & Sehgal, A. (2018) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2018.83.037705 · Cited by 3
Multiple neuronal networks coordinate Hydra mechanosensory behaviorPreprint
Badhiwala, K. N., Primack, A. S., Juliano, C. E., & Robinson, J. T. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.16.343384 · Cited by 3
Sleep is required for odor exposure to consolidate memory and remodel olfactory synapsesPreprint
Chandra, R., Farah, F., Muñoz-Lobato, F., Bokka, A., Benedetti, K. L., Brueggemann, C., Saifuddin, F. A., Miller, J. M., Li, J., Chang, E., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.24.395228 · Cited by 3
Serotonin modulates infraslow oscillation in the dentate gyrus during Non-REM sleepPreprint
Turi, G. F., Teng, S., Chen, X., Lim, E. C., Dias, C., Hu, R., Wang, R., Zhen, F., & Peng, Y. (2024) · eLife · doi:10.7554/elife.100196.1 · Cited by 3
Roles of Cyclic Nucleotide Phosphodiesterases in Signal Transduction Pathways in the Nematode Caenorhabditis elegans
Galande, K. K., & Cote, R. (2025) · Cells · doi:10.3390/cells14151174 · Cited by 2
Eye movement kinematics reveal novel circadian organization of sleep substates
Choudhary, V., Heller, C. R., Aimon, S., Schmid, L. D. S., Li, J. M., & Robson, D. N. (2026) · Nature Communications · doi:10.1038/s41467-026-72222-0 · Cited by 2
Artificial light pollution disrupts sleep and neuronal genomic stability in wild reef fish
Ben-Ezra, S., Harpaz, R., Krayden, G., Ohavia, M., Engert, F., Appelbaum, L., & Levy, O. (2026) · Current Biology · doi:10.1016/j.cub.2026.05.058 · Cited by 3
Sleep prevents brain phosphoproteome disruption to safeguard survival
Ma, J., Liu, J., Li, Y., Zhao, Y., Tian, Y., Hu, B., Yan, K., Li, Y., Ding, K., Wang, X., et al. (2025) · Cell Discovery · doi:10.1038/s41421-025-00809-w · Cited by 2
Agarose Microchambers for Long-term Calcium Imaging of Caenorhabditis elegans
Turek, M., Besseling, J., & Bringmann, H. (2015) · Journal of Visualized Experiments · doi:10.3791/52742-v · Cited by 2
Segmentation-free measurement of locomotor frequency in Caenorhabditis elegans using image invariants
Ji, H., Chen, D., & Fang-Yen, C. M. (2024) · G3 Genes Genomes Genetics · doi:10.1093/g3journal/jkae170 · Cited by 2
Sleep in insects
Hartse, K. M. (2001) · Cambridge University Press eBooks · doi:10.1017/cbo9780511642074.003 · Cited by 2
Genetics of Electroencephalography During Wakefulness and Sleep
Watson, N. F. (2011) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2011.04.003 · Cited by 2
Japanese studies on neural circuits and behavior of Caenorhabditis elegans
Sasakura, H., Tsukada, Y., Takagi, S., & Mori, I. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00187 · Cited by 2
Genetics of Sleep in a Simple Model Organism
Allada, R. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4160-6645-3.00013-x · Cited by 2
Animal Models in Sleep Research
Gulia, K. K. (2024) · Springer eBooks · doi:10.1007/978-981-97-0048-6_12 · Cited by 2
Phylogeny of Sleep
Hartse, K. (2017) · Springer eBooks · doi:10.1007/978-1-4939-6578-6_9 · Cited by 1
Motivational Processes in the Regulation of Sleep/Wake States
Eban-Rothschild, A. (2019) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-813743-7.00035-9 · Cited by 2
Definitions and measurements of the states of vigilance
Mondino, A., Torterolo, P., & Vanini, G. (2021) · Elsevier eBooks · doi:10.1016/b978-0-323-85235-7.00002-8 · Cited by 3
Sleep and the circadian clock in insects
Bertolini, E., & Helfrich‐Förster, C. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-822963-7.00037-2 · Cited by 2

Authors: Raizen, D. M., Zimmerman, J. E., Maycock, M. H., Ta, U. D., You, Y.-J., Sundaram, M. V., & Pack, A. I.
Affiliations: University of Pennsylvania (US)
The University of Texas Southwestern Medical Center (US)
Corresponding author: Raizen, David M.
ORCID: Raizen, David M.
You, Young-jai
Sundaram, Meera V.
Pack, Allan I.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2008-01-09
Volume: 451
Issue: 7178
Pages: 569-572
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature06535
OpenAlex: W2072681733
Cited by: 536
References: 31
Citations by year: 2026: 19 · 2025: 26 · 2024: 36 · 2023: 37 · 2022: 32 · 2021: 33 · 2020: 39 · 2019: 35 · 2018: 36 · 2017: 36 · 2016: 26 · 2015: 28 · 2014: 26 · 2013: 34 · 2012: 18
FWCI: 12.75
Type: journal article
Language: en
Update notices: erratum (2008-06-12)
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Keywords: sleep-like state, Caenorhabditis elegans, cGMP signaling, egl-4, cGMP-dependent protein kinase, sensory neurons, sleep homeostasis, sleep evolution, quiescence
MeSH terms: Animals, Arousal, Drosophila melanogaster, Biological Evolution, Homeostasis, Larva, Sleep, Conserved Sequence, Caenorhabditis elegans, Cyclic GMP-Dependent Protein Kinases, Molting, Caenorhabditis elegans Proteins, Lethargy

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Lethargus is a Caenorhabditis elegans sleep-like state

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks