The neural architecture of sleep regulation – insights from Drosophila
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Raquel Suárez-Grimalt
in vivo imaging of electrical activity. During this time, Davide became increasingly interested in studying the neurophysiology of sleep regulation using the model organismDrosophila melanogaster . Currently, Davide works together with the Emmy Noether research group of David Owald and dedicates his work to combining sophisticated imaging techniques, optogenetics and behavioral assays to investigate the neurophysiological principles and network interactions that provide the neural architecture of sleep regulation.
Abstract
The neural mechanisms that balance waking and sleep to ensure adequate sleep quality in mammals are highly complex, often eluding functional insight. In the last two decades, researchers made impressive progress in studying the less complex brain of the invertebrate model organism Drosophila melanogaster, which has led to a deeper understanding of the neural principles of sleep regulation. Here, we will review these findings to illustrate that neural networks require sleep to undergo synaptic reorganization that allows for the incorporation of experiences made during the waking hours. Sleep need, therefore, can arise as a consequence of sensory processing, often signalized by neural networks as they synchronize their electrical patterns to generate slow-wave activity. The slow-wave activity provides the neurophysiological basis to establish a sensory gate that suppresses sensory processing to provide a resting phase which promotes synaptic rescaling and clearance of metabolites from the brain. Moreover, we demonstrate how neural networks for homeostatic and circadian sleep regulation interact to consolidate sleep into a specific daily period. We particularly highlight that the basic functions and physiological principles of sleep are highly conserved throughout the phylogenetic spectrum, allowing us to identify the functional components and neural interactions that construct the neural architecture of sleep regulation.
Zusammenfassung
Die neuronalen Mechanismen, die das Gleichgewicht zwischen Wachheit und Schlaf etablieren, um eine angemessene Schlafqualität in Säugetieren zu gewährleisten, sind hochkomplex und entziehen sich oft funktioneller Einsicht. Mit Hilfe des weniger komplexen Gehirns des wirbellosen Modellorganismus Drosophila melanogaster haben Forscher in den letzten zwei Jahrzehnten beeindruckende Fortschritte gemacht und ein tieferes Verständnis der neuronalen Prinzipien der Schlafregulation erlangt. In dieser Arbeit werden wir diese Erkenntnisse zusammenfassen, um zu veranschaulichen, dass neuronale Netzwerke Schlaf benötigen, um synaptische Verknüpfungen zu reorganisieren und somit die am Tag gemachten Erfahrungen zu verarbeiten. Schlafbedürfnis kann also als Folge sensorischer Verarbeitung entstehen, was in neuronalen Netzwerken häufig zur Synchronisierung elektrischer Muster führt und Slow-Wave-Aktivität erzeugt. Slow-Wave-Aktivität liefert die neurophysiologische Grundlage für die Etablierung eines sensorischen Tores, welches die sensorische Verarbeitung unterdrückt und somit eine Ruhephase schafft, die die Reorganisation synaptischer Verknüpfungen und den Abtransport von Stoffwechselprodukten aus dem Gehirn fördert. Darüber hinaus zeigen wir, wie neuronale Netzwerke für die homöostatische und zirkadiane Schlafregulation interagieren, um zu gewährleisten, dass ein Organismus immer innerhalb einer festen Periode schläft. In dieser Arbeit heben wir besonders hervor, dass die grundlegenden Funktionen und physiologischen Prinzipien des Schlafs über das gesamte phylogenetische Spektrum hinweg konserviert sind, was uns ermöglicht, die funktionellen Komponenten und neuronalen Interaktionen zu identifizieren, die die neuronale Architektur der Schlafregulation bilden.
Über die Autoren
Raquel Suárez-Grimalt studied biology at the University of A Coruña and received a master’s degree in neuroscience from the Autonomous University of Barcelona. During a research stay in Andrew Lin’s lab at the University of Sheffield, she became passionate about the neuronal networks responsible for complex behaviors in fruit flies. For her PhD, she joined the Emmy Noether research group of David Owald in Berlin, where she is now studying neural circuitries balancing wake and sleep in flies by using optogenetics and animal tracking. During this time, she received a PhD fellowship from the Einstein Center for Neurosciences Berlin. Raquel is planning on finishing her PhD end of 2021 and continuing her research career as a postdoc.
Dr. Davide Raccuglia is currently a research scientist and lecturer at the Institute of Neurophysiology at the Charité in Berlin. Davide studied Human and Molecular Biology at the Saarland University in Saarbrücken. During his PhD, he investigated temporal integration of excitatory and inhibitory inputs during olfactory learning in the honeybee. For his Postdoc, Davide joined the lab of Prof. Michael Nitabach at the Yale Medical School, where he was part of the team that pioneered the use of genetically encoded voltage indicators for in vivo imaging of electrical activity. During this time, Davide became increasingly interested in studying the neurophysiology of sleep regulation using the model organism Drosophila melanogaster. Currently, Davide works together with the Emmy Noether research group of David Owald and dedicates his work to combining sophisticated imaging techniques, optogenetics and behavioral assays to investigate the neurophysiological principles and network interactions that provide the neural architecture of sleep regulation.
Acknowledgements
We thank David Owald and Eric Reynolds for providing valuable comments on the manuscript. We thank Jörg Geiger for providing the infrastructure that makes our work possible. We also thank Scidraw for allowing us to modify and use their schematics (Figure 1B, https://doi.org/10.5281/zenodo.3926361; Figure 1C, https://doi.org/10.5281/zenodo.3926343, https://doi.org/10.5281/zenodo.3925941; Figure 2 https://doi.org/10.5281/zenodo.3925951, https://doi.org/10.5281/zenodo.4420079).
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Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
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Research funding: Raquel’s work in the Owald group was supported by the Deutsche Forschungsgemeinschaft (DFG; German Research Foundation) under Germany’s Excellence Strategy – EXC-2049 – 390688087 to David Owald and the Emmy Noether Programme (282979116) to David Owald.
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Conflict of interest statement: The authors declare no competing interests.
References
Alhola, P. and Polo-Kantola, P. (2007). Sleep deprivation: Impact on cognitive performance. Neuropsychiatric Dis. Treat. 3, 553–567.Suche in Google Scholar
Andrillon, T. and Kouider, S. (2020). The vigilant sleeper: Neural mechanisms of sensory (de)coupling during sleep. Curr. Opin. Physiol. 15, 47–59, https://doi.org/10.1016/j.cophys.2019.12.002.Suche in Google Scholar
Aserinsky, E. and Kleitman, N. (1953). Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. Science 118, 273–274, https://doi.org/10.1126/science.118.3062.273.Suche in Google Scholar
Aulinas, A. (2000). Physiology of the Pineal Gland and Melatonin. Endotext (South Dartmouth (MA): MDText.com, Inc.).Suche in Google Scholar
Beckwith, E.J., Geissmann, Q., French, A.S., and Gilestro, G.F. (2017). Regulation of sleep homeostasis by sexual arousal. Elife 6, e27445, https://doi.org/10.7554/eLife.27445.Suche in Google Scholar
Bocchio, M., Nabavi, S., and Capogna, M. (2017). Synaptic plasticity, engrams, and network oscillations in amygdala circuits for storage and retrieval of emotional memories. Neuron 94, 731–743, https://doi.org/10.1016/j.neuron.2017.03.022.Suche in Google Scholar
Bonnet, M.H., Johnson, L.C., and Webb, W.B. (1978). The reliability of arousal threshold during sleep. Psychophysiology 15, 412–416, https://doi.org/10.1111/j.1469-8986.1978.tb01407.x.Suche in Google Scholar
Borbely, A.A. (1982). A two process model of sleep regulation. Hum. Neurobiol. 1, 195–204.Suche in Google Scholar
Buzsaki, G. and Draguhn, A. (2004). Neuronal oscillations in cortical networks. Science 304, 1926–1929, https://doi.org/10.1126/science.1099745.Suche in Google Scholar
Donlea, J.M. (2019). Roles for sleep in memory: Insights from the fly. Curr. Opin. Neurobiol. 54, 120–126, https://doi.org/10.1016/j.conb.2018.10.006.Suche in Google Scholar
Donlea, J.M., Pimentel, D., Talbot, C.B., Kempf, A., Omoto, J.J., Hartenstein, V., and Miesenbock, G. (2018). Recurrent circuitry for balancing sleep need and sleep. Neuron 97, 378–389 e374, https://doi.org/10.1016/j.neuron.2017.12.016.Suche in Google Scholar
Donlea, J.M., Ramanan, N., and Shaw, P.J. (2009). Use-dependent plasticity in clock neurons regulates sleep need in Drosophila. Science 324, 105–108, https://doi.org/10.1126/science.1166657.Suche in Google Scholar
Dunlap, J.C. (1999). Molecular bases for circadian clocks. Cell 96, 271–290, https://doi.org/10.1016/s0092-8674(00)80566-8.Suche in Google Scholar
Flores-Valle, A., Gonçalves, P.J., and Seelig, J.D. (2021). Integration of sleep homeostasis and navigation in Drosophila. PLoS Comput Biol 17, e1009088, https://doi.org/10.1371/journal.pcbi.1009088.Suche in Google Scholar PubMed PubMed Central
Fultz, N.E., Bonmassar, G., Setsompop, K., Stickgold, R.A., Rosen, B.R., Polimeni, J.R., and Lewis, L.D. (2019). Coupled electrophysiological, hemodynamic, and cerebrospinal fluid oscillations in human sleep. Science 366, 628–631, https://doi.org/10.1126/science.aax5440.Suche in Google Scholar PubMed PubMed Central
Ganguly-Fitzgerald, I., Donlea, J., and Shaw, P.J. (2006). Waking experience affects sleep need in Drosophila. Science 313, 1775–1781, https://doi.org/10.1126/science.1130408.Suche in Google Scholar PubMed
Geissmann, Q., Beckwith, E.J., and Gilestro, G.F. (2019). Most sleep does not serve a vital function: Evidence from Drosophila melanogaster. Sci. Adv. 5, eaau9253, https://doi.org/10.1126/sciadv.aau9253.Suche in Google Scholar PubMed PubMed Central
Gent, T.C., Bandarabadi, M., Herrera, C.G., and Adamantidis, A.R. (2018). Thalamic dual control of sleep and wakefulness. Nat. Neurosci. 21, 974–984, https://doi.org/10.1038/s41593-018-0164-7.Suche in Google Scholar PubMed PubMed Central
Guo, F., Holla, M., Diaz, M.M., and Rosbash, M. (2018). A circadian output circuit controls sleep-wake arousal in Drosophila. Neuron 100, 624–635 e624, https://doi.org/10.1016/j.neuron.2018.09.002.Suche in Google Scholar PubMed
Hardcastle, B.J., Omoto, J.J., Kandimalla, P., Nguyen, B.M., Keles, M.F., Boyd, N.K., Hartenstein, V., and Frye, M.A. (2021). A visual pathway for skylight polarization processing in Drosophila. Elife 10, e63225, https://doi.org/10.7554/eLife.63225.Suche in Google Scholar PubMed PubMed Central
Hardin, P.E., Hall, J.C., and Rosbash, M. (1990). Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343, 536–540, https://doi.org/10.1038/343536a0.Suche in Google Scholar PubMed
Hastings, M.H., Maywood, E.S., and Brancaccio, M. (2018). Generation of circadian rhythms in the suprachiasmatic nucleus. Nat. Rev. Neurosci. 19, 453–469, https://doi.org/10.1038/s41583-018-0026-z.Suche in Google Scholar PubMed
Heinze, S. and Reppert, S.M. (2011). Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 69, 345–358, https://doi.org/10.1016/j.neuron.2010.12.025.Suche in Google Scholar PubMed
Helfrich-Förster, C. (2005). Neurobiology of the fruit fly’s circadian clock. Gene Brain Behav. 4, 65–76, https://doi.org/10.1111/j.1601-183X.2004.00092.x.Suche in Google Scholar PubMed
Horne, J.A. and Walmsley, B. (1976). Daytime visual load and the effects upon human sleep. Psychophysiology 13, 115–120, https://doi.org/10.1111/j.1469-8986.1976.tb00084.x.Suche in Google Scholar PubMed
Huang, S., Piao, C., Beuschel, C.B., Gotz, T., and Sigrist, S.J. (2020). Presynaptic active zone plasticity encodes sleep need in Drosophila. Curr. Biol. 30, 1077–1091.e5, https://doi.org/10.1016/j.cub.2020.01.019.Suche in Google Scholar PubMed
Huber, R., Ghilardi, M.F., Massimini, M., Ferrarelli, F., Riedner, B.A., Peterson, M.J., and Tononi, G. (2006). Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nat. Neurosci. 9, 1169–1176, https://doi.org/10.1038/nn1758.Suche in Google Scholar PubMed
Hulse, B.K., Haberkern, H., Franconville, R., Turner-Evans, D.B., Takemura, S., Wolff, T., Noorman, M., Dreher, M., Dan, C., Parekh, R., et al.. (2020). A connectome of the Drosophila central complex reveals network motifs suitable for flexible navigation and context-dependent action selection. bioRxiv, 2020.2012.2008.413955.10.7554/eLife.66039Suche in Google Scholar PubMed
Jagannath, A., Varga, N., Dallmann, R., Rando, G., Gosselin, P., Ebrahimjee, F., Taylor, L., Mosneagu, D., Stefaniak, J., Walsh, S., et al.. (2021). Adenosine integrates light and sleep signalling for the regulation of circadian timing in mice. Nat. Commun. 12, 2113, https://doi.org/10.1038/s41467-021-22179-z.Suche in Google Scholar PubMed PubMed Central
Joiner, W.J. (2016). Unraveling the evolutionary determinants of sleep. Curr. Biol. 26, R1073–R1087, https://doi.org/10.1016/j.cub.2016.08.068.Suche in Google Scholar PubMed PubMed Central
Kattler, H., Dijk, D.J., and Borbely, A.A. (1994). Effect of unilateral somatosensory stimulation prior to sleep on the sleep EEG in humans. J. Sleep Res. 3, 159–164, https://doi.org/10.1111/j.1365-2869.1994.tb00123.x.Suche in Google Scholar PubMed
Keene, A.C., Duboue, E.R., McDonald, D.M., Dus, M., Suh, G.S., Waddell, S., and Blau, J. (2010). Clock and cycle limit starvation-induced sleep loss in Drosophila. Curr. Biol. 20, 1209–1215, https://doi.org/10.1016/j.cub.2010.05.029.Suche in Google Scholar PubMed PubMed Central
Kempf, A., Song, S.M., Talbot, C.B., and Miesenbock, G. (2019). A potassium channel beta-subunit couples mitochondrial electron transport to sleep. Nature 568, 230–234, https://doi.org/10.1038/s41586-019-1034-5.Suche in Google Scholar PubMed PubMed Central
Kim, S.S., Rouault, H., Druckmann, S., and Jayaraman, V. (2017). Ring attractor dynamics in the Drosophila central brain. Science 356, 849–853, https://doi.org/10.1126/science.aal4835.Suche in Google Scholar PubMed
Kirszenblat, L., Ertekin, D., Goodsell, J., Zhou, Y., Shaw, P.J., and van Swinderen, B. (2018). Sleep regulates visual selective attention in Drosophila. J. Exp. Biol. 221, https://doi.org/10.1242/jeb.191429.Suche in Google Scholar PubMed PubMed Central
Kirszenblat, L., Yaun, R., and van Swinderen, B. (2019). Visual experience drives sleep need in Drosophila. Sleep 42, https://doi.org/10.1093/sleep/zsz102.Suche in Google Scholar PubMed PubMed Central
Klinzing, J.G., Niethard, N., and Born, J. (2019). Mechanisms of systems memory consolidation during sleep. Nat. Neurosci. 22, 1598–1610, https://doi.org/10.1038/s41593-019-0467-3.Suche in Google Scholar PubMed
Krueger, J.M., Nguyen, J.T., Dykstra-Aiello, C.J., and Taishi, P. (2019). Local sleep. Sleep Med. Rev. 43, 14–21, https://doi.org/10.1016/j.smrv.2018.10.001.Suche in Google Scholar PubMed PubMed Central
Krueger, J.M., Rector, D.M., Roy, S., Van Dongen, H.P., Belenky, G., and Panksepp, J. (2008). Sleep as a fundamental property of neuronal assemblies. Nat. Rev. Neurosci. 9, 910–919, https://doi.org/10.1038/nrn2521.Suche in Google Scholar PubMed PubMed Central
Lamaze, A., Kratschmer, P., Chen, K.F., Lowe, S., and Jepson, J.E.C. (2018). A wake-promoting circadian output circuit in Drosophila. Curr. Biol. 28, 3098–3105.e3, https://doi.org/10.1016/j.cub.2018.07.024.Suche in Google Scholar PubMed
Lazarus, M., Oishi, Y., Bjorness, T.E., and Greene, R.W. (2019). Gating and the need for sleep: Dissociable effects of adenosine A1 and A2A receptors. Front. Neurosci. 13, 740, https://doi.org/10.3389/fnins.2019.00740.Suche in Google Scholar PubMed PubMed Central
Leung, L.C., Wang, G.X., Madelaine, R., Skariah, G., Kawakami, K., Deisseroth, K., Urban, A.E., and Mourrain, P. (2019). Neural signatures of sleep in zebrafish. Nature 571, 198–204, https://doi.org/10.1038/s41586-019-1336-7.Suche in Google Scholar PubMed PubMed Central
Liu, S., Liu, Q., Tabuchi, M., and Wu, M.N. (2016). Sleep drive is encoded by neural plastic changes in a dedicated circuit. Cell 165, 1347–1360, https://doi.org/10.1016/j.cell.2016.04.013.Suche in Google Scholar PubMed PubMed Central
Llinas, R.R. and Steriade, M. (2006). Bursting of thalamic neurons and states of vigilance. J. Neurophysiol. 95, 3297–3308, https://doi.org/10.1152/jn.00166.2006.Suche in Google Scholar
Marshall, L., Helgadottir, H., Molle, M., and Born, J. (2006). Boosting slow oscillations during sleep potentiates memory. Nature 444, 610–613, https://doi.org/10.1038/nature05278.Suche in Google Scholar
Mascetti, G.G. (2016). Unihemispheric sleep and asymmetrical sleep: Behavioral, neurophysiological, and functional perspectives. Nat. Sci. Sleep 8, 221–238, https://doi.org/10.2147/nss.s71970.Suche in Google Scholar
Mascetti, L., Muto, V., Matarazzo, L., Foret, A., Ziegler, E., Albouy, G., Sterpenich, V., Schmidt, C., Degueldre, C., Leclercq, Y., et al.. (2013). The impact of visual perceptual learning on sleep and local slow-wave initiation. J. Neurosci. 33, 3323–3331, https://doi.org/10.1523/jneurosci.0763-12.2013.Suche in Google Scholar
Mazzotta, G.M., Damulewicz, M., and Cusumano, P. (2020). Better sleep at night: How light influences sleep in Drosophila. Front. Physiol. 11, 997, https://doi.org/10.3389/fphys.2020.00997.Suche in Google Scholar
McCormick, D.A. and Bal, T. (1994). Sensory gating mechanisms of the thalamus. Curr. Opin. Neurobiol. 4, 550–556, https://doi.org/10.1016/0959-4388(94)90056-6.Suche in Google Scholar
Melnattur, K., Kirszenblat, L., Morgan, E., Militchin, V., Sakran, B., English, D., Patel, R., Chan, D., van Swinderen, B., and Shaw, P.J. (2020). A conserved role for sleep in supporting spatial learning in Drosophila. Sleep 44, https://doi.org/10.1093/sleep/zsaa197.Suche in Google Scholar PubMed PubMed Central
Mullington, J.M., Cunningham, T.J., Haack, M., and Yang, H. (2021). Causes and consequences of chronic sleep deficiency and the role of orexin. Front. Neurol. Neurosci. 45, 128–138, https://doi.org/10.1159/000514956.Suche in Google Scholar PubMed
Nall, A.H., Shakhmantsir, I., Cichewicz, K., Birman, S., Hirsh, J., and Sehgal, A. (2016). Caffeine promotes wakefulness via dopamine signaling in Drosophila. Sci. Rep. 6, 20938, https://doi.org/10.1038/srep20938.Suche in Google Scholar PubMed PubMed Central
Neuser, K., Triphan, T., Mronz, M., Poeck, B., and Strauss, R. (2008). Analysis of a spatial orientation memory in Drosophila. Nature 453, 1244–1247, https://doi.org/10.1038/nature07003.Suche in Google Scholar PubMed
Omoto, J.J., Keles, M.F., Nguyen, B.M., Bolanos, C., Lovick, J.K., Frye, M.A., and Hartenstein, V. (2017). Visual input to the Drosophila central complex by developmentally and functionally distinct neuronal populations. Curr. Biol. 27, 1098–1110, https://doi.org/10.1016/j.cub.2017.02.063.Suche in Google Scholar PubMed PubMed Central
Pfeiffer, K. and Homberg, U. (2007). Coding of azimuthal directions via time-compensated combination of celestial compass cues. Curr. Biol. 17, 960–965, https://doi.org/10.1016/j.cub.2007.04.059.Suche in Google Scholar PubMed
Pfeiffer, K. and Homberg, U. (2014). Organization and functional roles of the central complex in the insect brain. Annu. Rev. Entomol. 59, 165–184, https://doi.org/10.1146/annurev-ento-011613-162031.Suche in Google Scholar PubMed
Pimentel, D., Donlea, J.M., Talbot, C.B., Song, S.M., Thurston, A.J.F., and Miesenbock, G. (2016). Operation of a homeostatic sleep switch. Nature 536, 333–337, https://doi.org/10.1038/nature19055.Suche in Google Scholar PubMed PubMed Central
Quercia, A., Zappasodi, F., Committeri, G., and Ferrara, M. (2018). Local use-dependent sleep in wakefulness links performance errors to learning. Front. Hum. Neurosci. 12, 122, https://doi.org/10.3389/fnhum.2018.00122.Suche in Google Scholar PubMed PubMed Central
Raccuglia, D., Huang, S., Ender, A., Heim, M.M., Laber, D., Suarez-Grimalt, R., Liotta, A., Sigrist, S.J., Geiger, J.R.P., and Owald, D. (2019). Network-specific synchronization of electrical slow-wave oscillations regulates sleep drive in Drosophila. Curr. Biol. 29, 3611–3621.e3, https://doi.org/10.1016/j.cub.2019.08.070.Suche in Google Scholar PubMed
Ramon, F., Hernandez-Falcon, J., Nguyen, B., and Bullock, T.H. (2004). Slow wave sleep in crayfish. Proc. Natl. Acad. Sci. U. S. A. 101, 11857–11861, https://doi.org/10.1073/pnas.0402015101.Suche in Google Scholar PubMed PubMed Central
Rector, D.M., Schei, J.L., Van Dongen, H.P., Belenky, G., and Krueger, J.M. (2009). Physiological markers of local sleep. Eur. J. Neurosci. 29, 1771–1778, https://doi.org/10.1111/j.1460-9568.2009.06717.x.Suche in Google Scholar PubMed PubMed Central
Rector, D.M., Topchiy, I.A., Carter, K.M., and Rojas, M.J. (2005). Local functional state differences between rat cortical columns. Brain Res. 1047, 45–55, https://doi.org/10.1016/j.brainres.2005.04.002.Suche in Google Scholar PubMed
Sanchez-Vives, M.V. (2020). Origin and dynamics of cortical slow oscillations. Curr. Opin. Physiol. 15, 217–223, https://doi.org/10.1016/j.cophys.2020.04.005.Suche in Google Scholar
Seelig, J.D. and Jayaraman, V. (2013). Feature detection and orientation tuning in the Drosophila central complex. Nature 503, 262–266, https://doi.org/10.1038/nature12601.Suche in Google Scholar PubMed PubMed Central
Shaw, P.J., Cirelli, C., Greenspan, R.J., and Tononi, G. (2000). Correlates of sleep and waking in Drosophila melanogaster. Science 287, 1834–1837, https://doi.org/10.1126/science.287.5459.1834.Suche in Google Scholar PubMed
Singh, S., Kaur, H., Singh, S., and Khawaja, I. (2018). Parasomnias: A comprehensive review. Cureus 10, e3807, https://doi.org/10.7759/cureus.3807.Suche in Google Scholar PubMed PubMed Central
Sitaraman, D., Aso, Y., Jin, X., Chen, N., Felix, M., Rubin, G.M., and Nitabach, M.N. (2015). Propagation of homeostatic sleep signals by segregated synaptic microcircuits of the Drosophila mushroom body. Curr. Biol. 25, 2915–2927, https://doi.org/10.1016/j.cub.2015.09.017.Suche in Google Scholar PubMed PubMed Central
Strauss, R. and Heisenberg, M. (1993). A higher control center of locomotor behavior in the Drosophila brain. J. Neurosci. 13, 1852–1861, https://doi.org/10.1523/jneurosci.13-05-01852.1993.Suche in Google Scholar
Tononi, G. and Massimini, M. (2008). Why does consciousness fade in early sleep? Ann. N. Y. Acad. Sci. 1129, 330–334, https://doi.org/10.1196/annals.1417.024.Suche in Google Scholar PubMed
Troup, M., Yap, M.H., Rohrscheib, C., Grabowska, M.J., Ertekin, D., Randeniya, R., Kottler, B., Larkin, A., Munro, K., Shaw, P.J., et al.. (2018). Acute control of the sleep switch in Drosophila reveals a role for gap junctions in regulating behavioral responsiveness. Elife 7, e37105, https://doi.org/10.7554/eLife.37105.Suche in Google Scholar PubMed PubMed Central
Turner-Evans, D., Wegener, S., Rouault, H., Franconville, R., Wolff, T., Seelig, J.D., Druckmann, S., and Jayaraman, V. (2017). Angular velocity integration in a fly heading circuit. Elife 6, e23496, https://doi.org/10.7554/eLife.23496.Suche in Google Scholar PubMed PubMed Central
Vaccaro, A., Kaplan Dor, Y., Nambara, K., Pollina, E.A., Lin, C., Greenberg, M.E., and Rogulja, D. (2020). Sleep loss can cause death through accumulation of reactive oxygen species in the gut. Cell 181, 1307–1328.e15, https://doi.org/10.1016/j.cell.2020.04.049.Suche in Google Scholar PubMed
van Alphen, B., Semenza, E.R., Yap, M., van Swinderen, B., and Allada, R. (2021). A deep sleep stage in Drosophila with a functional role in waste clearance. Sci. Adv. 7, https://doi.org/10.1126/sciadv.abc2999.Suche in Google Scholar PubMed PubMed Central
van Alphen, B., Yap, M.H., Kirszenblat, L., Kottler, B., and van Swinderen, B. (2013). A dynamic deep sleep stage in Drosophila. J. Neurosci. 33, 6917–6927, https://doi.org/10.1523/jneurosci.0061-13.2013.Suche in Google Scholar
Vyazovskiy, V.V., Olcese, U., Hanlon, E.C., Nir, Y., Cirelli, C., and Tononi, G. (2011). Local sleep in awake rats. Nature 472, 443–447, https://doi.org/10.1038/nature10009.Suche in Google Scholar
Yap, M.H.W., Grabowska, M.J., Rohrscheib, C., Jeans, R., Troup, M., Paulk, A.C., van Alphen, B., Shaw, P.J., and van Swinderen, B. (2017). Oscillatory brain activity in spontaneous and induced sleep stages in flies. Nat. Commun. 8, 1815, https://doi.org/10.1038/s41467-017-02024-y.Suche in Google Scholar
Zehring, W.A., Wheeler, D.A., Reddy, P., Konopka, R.J., Kyriacou, C.P., Rosbash, M., and Hall, J.C. (1984). P-element transformation with period locus DNA restores rhythmicity to mutant, arrhythmic Drosophila melanogaster. Cell 39, 369–376, https://doi.org/10.1016/0092-8674(84)90015-1.Suche in Google Scholar
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Artikel in diesem Heft
- Frontmatter
- Review articles
- The neural architecture of sleep regulation – insights from Drosophila
- Environmental exposures impact the nervous system in a life stage-specific manner
- Recent developments and future perspectives on neuroelectronic devices
- Neuroscience meets cancer: networks and neuronal input to brain tumors
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- DFG-Research Unit (FOR) 2974 “Affective and cognitive mechanisms of specific Internet-use disorders (ACSID)”
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Artikel in diesem Heft
- Frontmatter
- Review articles
- The neural architecture of sleep regulation – insights from Drosophila
- Environmental exposures impact the nervous system in a life stage-specific manner
- Recent developments and future perspectives on neuroelectronic devices
- Neuroscience meets cancer: networks and neuronal input to brain tumors
- Presentation of scientific institutions
- DFG-Research Unit (FOR) 2974 “Affective and cognitive mechanisms of specific Internet-use disorders (ACSID)”
- Nachrichten aus der Gesellschaft
- Nachrichten aus der Gesellschaft
