Sleep and Synaptic Homeostasis: Structural Evidence in Drosophila
Open accessAbstract
The functions of sleep remain elusive, but a strong link exists between sleep need and neuronal plasticity. We tested the hypothesis that plastic processes during wake lead to a net increase in synaptic strength and sleep is necessary for synaptic renormalization. We found that, in three Drosophila neuronal circuits, synapse size or number increases after a few hours of wake and decreases only if flies are allowed to sleep. A richer wake experience resulted in both larger synaptic growth and greater sleep need. Finally, we demonstrate that the gene Fmr1 (fragile X mental retardation 1) plays an important role in sleep-dependent synaptic renormalization.
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The Synaptic Homeostasis Hypothesis has generated a number of new empirical findings.
“SHY has served as a model neuroscientific theory in that it has generated a number of new empirical findings.32”
From The overfitted brain: Dreams evolved to assist generalization (2021) · cites this paper as [32]
Sleep renormalizes synapses after potentiation during wakefulness.
“suggesting that sleep renormalized synapses after potentiation during wakefulness.”
From About Sleep's Role in Memory (2013) · cites this paper as [156]
In fruit flies, synapse size or number increased after a few hours of wakefulness and decreased only when flies were allowed to sleep.
“Using staining techniques in fruit flies, Bushey et al. (156) showed that synapse size or number increased after a few hours of wakefulness and decreased only when flies were allowed to sleep.”
From About Sleep's Role in Memory (2013) · cites this paper as [156]
In fruit flies, increased synaptic growth due to an enriched wake experience led to an increase in sleep, and time spent asleep after enriched experience was negatively correlated with spine density.
“Increased synaptic growth due to an enriched wake experience (12 h spent together with 100 other flies) led to an increase in sleep with the time spent asleep after enriched experience being negatively correlated with spine density, suggesting that sleep renormalized synapses after potentiation during wakefulness.”
From About Sleep's Role in Memory (2013) · cites this paper as [156]
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Cites
Diekelmann, S., & Born, J. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2762 · Cited by 3,760 · see citing works
Sleep function and synaptic homeostasis
Tononi, G., & Cirelli, C. (2006) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2005.05.002 · Cited by 2,151 · see citing works
Self-citationExperience-dependent structural synaptic plasticity in the mammalian brain
Holtmaat, A., & Svoboda, K. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2699 · Cited by 1,934 · see citing works
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 · see citing works
Self-citationHarris, K., & Stevens, J. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-08-02982.1989 · Cited by 1,073 · see citing works
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 · see citing works
Vyazovskiy, V. V., Cirelli, C., Pfister-Genskow, M., Faraguna, U., & Tononi, G. (2008) · Nature Neuroscience · doi:10.1038/nn2035 · Cited by 837 · see citing works
Making memories last: the synaptic tagging and capture hypothesis
Redondo, R. L., & Morris, R. G. M. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn2963 · Cited by 792 · see citing works
Lee, T., Lee, A. M., & Luo, L. (1999) · Development · doi:10.1242/dev.126.18.4065 · Cited by 720 · see citing works
Synaptic mechanisms for plasticity in neocortex
Feldman, D. E. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135516 · Cited by 704 · see citing works
Cirelli, C., & Tononi, G. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060216 · Cited by 646 · see citing works
Self-citationWeiler, I. J., Irwin, S. A., Klintsova, A. Y., Spencer, C. M., Brazelton, A. D., Miyashiro, K., Comery, T. A., Patel, B., Eberwine, J., & Greenough, W. T. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.10.5395 · Cited by 644 · see citing works
Inactivity produces increases in neurotransmitter release and synapse size
Murthy, V. N., Schikorski, T., Stevens, C. F., & Zhu, Y. (2001) · Neuron · doi:10.1016/s0896-6273(01)00500-1 · Cited by 612 · see citing works
Rodriguez, A., Ehlenberger, D. B., Dickstein, D. L., Hof, P. R., & Wearne, S. L. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001997 · Cited by 571 · see citing works
Sleep in Drosophila is regulated by adult mushroom bodies
Joiner, W. J., Crocker, A. J., White, B. H., & Sehgal, A. (2006) · Nature · doi:10.1038/nature04811 · Cited by 455 · see citing works
Active flight increases the gain of visual motion processing in Drosophila
Maimon, G., Straw, A. D., & Dickinson, M. H. (2010) · Nature Neuroscience · doi:10.1038/nn.2492 · Cited by 420 · see citing works
PDF Cells Are a GABA-Responsive Wake-Promoting Component of the Drosophila Sleep Circuit
Parisky, K. M., Agosto, J. L., Pulver, S. R., Shang, Y., Kuklin, E. A., Hodge, J. J. L., Kang, K., Liu, X., Garrity, P., Rosbash, M., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.10.042 · Cited by 407 · see citing works
Bhatt, D. H., Zhang, S., & Gan, W.-B. (2009) · Annual Review of Physiology · doi:10.1146/annurev.physiol.010908.163140 · Cited by 380 · see citing works
Widespread Changes in Synaptic Markers as a Function of Sleep and Wakefulness in <i>Drosophila</i>
Gilestro, G. F., Tononi, G., & Cirelli, C. (2009) · Science · doi:10.1126/science.1166673 · Cited by 360 · see citing works
Self-citationA dynamic role for the mushroom bodies in promoting sleep in Drosophila
Pitman, J. L., McGill, J. J., Keegan, K. P., & Allada, R. (2006) · Nature · doi:10.1038/nature04739 · Cited by 330 · see citing works
Waking Experience Affects Sleep Need in Drosophila
Ganguly-Fitzgerald, I., Donlea, J. M., & Shaw, P. J. (2006) · Science · doi:10.1126/science.1130408 · Cited by 310 · see citing works
Why We Sleep: The Temporal Organization of Recovery
Mignot, E. J.-M. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060106 · Cited by 266 · see citing works
Use-Dependent Plasticity in Clock Neurons Regulates Sleep Need in Drosophila
Donlea, J. M., Ramanan, N., & Shaw, P. J. (2009) · Science · doi:10.1126/science.1166657 · Cited by 251 · see citing works
Liu, Z.-W., Faraguna, U., Cirelli, C., Tononi, G., & Gao, X.-B. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1409-10.2010 · Cited by 248 · see citing works
Self-citationLiving synaptic vesicle marker: Synaptotagmin‐GFP
Zhang, Y., Rodesch, C. K., & Broadie, K. S. (2002) · genesis · doi:10.1002/gene.10144 · Cited by 239 · see citing works
The Drosophila Fragile X Gene Negatively Regulates Neuronal Elaboration and Synaptic Differentiation
Pan, L., Zhang, Y., Woodruff, E. A., & Broadie, K. S. (2004) · Current Biology · doi:10.1016/j.cub.2004.09.085 · Cited by 194 · see citing works
Neurobiology of the fruit fly's circadian clock
Helfrich‐Förster, C. (2004) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2004.00092.x · Cited by 190 · see citing works
Experience-Dependent Strengthening ofDrosophilaNeuromuscular Junctions
Sigrist, S. J., Reiff, D. F., Thiel, P. R., Steinert, J. R., & Schuster, C. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-16-06546.2003 · Cited by 188 · see citing works
Circadian and Homeostatic Regulation of Structural Synaptic Plasticity in Hypocretin Neurons
Appelbaum, L., Wang, G. X., Yokogawa, T., Skariah, G. M., Smith, S. J., Mourrain, P., & Mignot, E. J.-M. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.006 · Cited by 172 · see citing works
TheDrosophilaFragile X Mental Retardation Gene Regulates Sleep Need
Bushey, D., Tononi, G., & Cirelli, C. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4830-08.2009 · Cited by 119 · see citing works
Self-citationBalling, A., Technau, G. M., & Heisenberg, M. (1987) · PubMed · Cited by 111 · see citing works
Activity-dependent modulation of neural circuit synaptic connectivity
Tessier, C. R. (2009) · Frontiers in Molecular Neuroscience · doi:10.3389/neuro.02.008.2009 · Cited by 75 · see citing works
Characterization of dendritic spines in the Drosophila central nervous system
Leiss, F., Koper, E., Hein, I., Fouquet, W., Lindner, J., Sigrist, S. J., & Tavosanis, G. (2009) · Developmental Neurobiology · doi:10.1002/dneu.20699 · Cited by 67 · see citing works
Todd, P. K., & Mack, K. J. (2000) · Molecular Brain Research · doi:10.1016/s0169-328x(00)00098-x · Cited by 63 · see citing works
Balling, A., Technau, G. M., & Heisenberg, M. (1987) · Journal of Neurogenetics · doi:10.3109/01677068709167218 · Cited by 52 · see citing works
Irwin, S. A., Christmon, C. A., Grossman, A. W., Galvez, R., Kim, S. H., DeGrush, B. J., Weiler, I. J., & Greenough, W. T. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.11.004 · Cited by 51 · see citing works
Gatto, C. L. (2009) · Frontiers in Neural Circuits · doi:10.3389/neuro.04.008.2009 · Cited by 50 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [20]Helfrich-Forster C Genes Brain Behav Mar 2005 4 65 15720403
- [27]Balling A Technau GM Heisenberg M J Neurogenet Apr 1987 4 65 3598769
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Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
“(156) showed that synapse size or number increased after a few hours of wakefulness and decreased only when flies were allowed to sleep.”
BackgroundTononi, G., & Cirelli, C. (2014) · Neuron · doi:10.1016/j.neuron.2013.12.025 · Cited by 2,356 · see citing works
Self-citationControl of sleep and wakefulness
Brown, R. E., Basheer, R., McKenna, J. T., Strecker, R. E., & McCarley, R. W. (2012) · Physiological Reviews · doi:10.1152/physrev.00032.2011 · Cited by 1,477 · see citing works
Lim, A. S. P., Kowgier, M., Yu, L., Buchman, A. S., & Bennett, D. A. (2013) · Sleep · doi:10.5665/sleep.2802 · Cited by 793 · see citing works
Sleep promotes branch-specific formation of dendritic spines after learning
Yang, G., Lai, C. S. W., Cichon, J., Ma, L., Li, W., & Gan, W.-B. (2014) · Science · doi:10.1126/science.1249098 · Cited by 616 · see citing works
Ultrastructural evidence for synaptic scaling across the wake/sleep cycle
de Vivo, L., Bellesi, M., Marshall, W., Bushong, E. A., Ellisman, M. H., Tononi, G., & Cirelli, C. (2017) · Science · doi:10.1126/science.aah5982 · Cited by 574 · see citing works
Self-citationSleep Loss Can Cause Death through Accumulation of Reactive Oxygen Species in the Gut
Vaccaro, A., Kaplan Dor, Y., Nambara, K., Pollina, E. A., Lin, C., Greenberg, M. E., & Rogulja, D. (2020) · Cell · doi:10.1016/j.cell.2020.04.049 · Cited by 541 · see citing works
Hulse, B. K., Haberkern, H., Franconville, R., Turner-Evans, D., Takemura, S.-Y., Wolff, T., Noorman, M., Dreher, M., Dan, C., Parekh, R., et al. (2021) · eLife · doi:10.7554/elife.66039 · Cited by 392 · see citing works
Sleep and waking modulate spine turnover in the adolescent mouse cortex
Maret, S., Faraguna, U., Nelson, A. B., Cirelli, C., & Tononi, G. (2011) · Nature Neuroscience · doi:10.1038/nn.2934 · Cited by 315 · see citing works
Self-citationSlow waves, sharp waves, ripples, and REM in sleeping dragons
Shein-Idelson, M., Ondracek, J. M., Liaw, H.-P., Reiter, S., & Laurent, G. (2016) · Science · doi:10.1126/science.aaf3621 · Cited by 274 · see citing works
Unraveling the evolutionary determinants of sleep
Joiner, W. J. (2016) · Current Biology · doi:10.1016/j.cub.2016.08.068 · Cited by 232 · see citing works
Sleep and synaptic down-selection
Tononi, G., & Cirelli, C. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14335 · Cited by 217 · see citing works
Self-citationSleep and memory in mammals, birds and invertebrates
Vorster, A. P., & Born, J. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.09.020 · Cited by 169 · see citing works
Sleep Interacts with Aβ to Modulate Intrinsic Neuronal Excitability
Tabuchi, M., Lone, S. R., Liu, S., Liu, Q., Zhang, J., Spira, A. P., & Wu, M. N. (2015) · Current Biology · doi:10.1016/j.cub.2015.01.016 · Cited by 165 · see citing works
Sleep recalibrates homeostatic and associative synaptic plasticity in the human cortex
Kuhn, M., Wolf, E., Maier, J. G., Mainberger, F., Feige, B., Schmid, H., Bürklin, J., Maywald, S., Mall, V., Jung, N. H., et al. (2016) · Nature Communications · doi:10.1038/ncomms12455 · Cited by 152 · see citing works
Salehinejad, M. A., Ghanavati, E., Reinders, J., Hengstler, J. G., Kuo, M.-F., & Nitsche, M. A. (2022) · eLife · doi:10.7554/elife.69308 · Cited by 94 · see citing works
Plasticity during sleep is linked to specific regulation of cortical circuit activity
Niethard, N., Burgalossi, A., & Born, J. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00065 · Cited by 89 · see citing works
Circadian dynamics in measures of cortical excitation and inhibition balance
Chellappa, S. L., Gaggioni, G., Ly, J. Q. M., Papachilleos, S., Borsu, C., Brzozowski, A., Rosanova, M., Sarasso, S., Luxen, A., Middleton, B., et al. (2016) · Scientific Reports · doi:10.1038/srep33661 · Cited by 84 · see citing works
Synapse rearrangements upon learning: from divergent–sparse connectivity to dedicated sub-circuits
Caroni, P., Chowdhury, A., & Lahr, M. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.08.011 · Cited by 85 · see citing works
Neuronal reactivation during post-learning sleep consolidates long-term memory in Drosophila
Dag, U., Lei, Z., Le, J. Q., Wong, A., Bushey, D., & Keleman, K. (2019) · eLife · doi:10.7554/elife.42786 · Cited by 83 · see citing works
Self-citationHow Aging Affects Sleep-Dependent Memory Consolidation?
Harand, C., Bertran, F., Doidy, F., Guénolé, F., Desgranges, B., Eustache, F., & Rauchs, G. (2012) · Frontiers in Neurology · doi:10.3389/fneur.2012.00008 · Cited by 83 · see citing works
The yin and yang of sleep and attention
Kirszenblat, L., & van Swinderen, B. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.10.001 · Cited by 81 · see citing works
The why and how of sleep-dependent synaptic down-selection
Cirelli, C., & Tononi, G. (2022) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2021.02.007 · Cited by 74 · see citing works
Self-citationThe overfitted brain: Dreams evolved to assist generalization
Hoel, E. (2021) · Patterns · doi:10.1016/j.patter.2021.100244 · Cited by 70 · see citing works
“that synapses change during sleep in the form of synaptic homeostasis, regularization which occurs every night in the form of universal down-scaling of synaptic strength (Bushey et al., 2011).”
BackgroundHulse, 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) · doi:10.1101/2020.12.08.413955 · Cited by 392 · see citing works
“…control While its functions remain largely unknown, sleep is associated with a variety of processes in Drosophila, including synaptic homeostasis (Bushey et al., 2011), memory formation and consolidation (Berry et al., 2015; Dag et al., 2019; Donlea et al., 2011), changes in gene expression…”
BackgroundResultInfluential
- Authors
- Bushey, D., Tononi, G., & Cirelli, C.
- Affiliations
- University of Wisconsin–Madison (US)
- Corresponding author
- Cirelli, Chiara
- Venue
- Science
- Published
- 2011-06-24
- Volume
- 332
- Issue
- 6037
- Pages
- 1576-1581
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC3128387
- OpenAlex
- W2081610458
- Cited by
- 357
- References
- 37
- Citations by year
- 2026: 10 · 2025: 21 · 2024: 24 · 2023: 15 · 2022: 16 · 2021: 19 · 2020: 21 · 2019: 25 · 2018: 11 · 2017: 33 · 2016: 21 · 2015: 35 · 2014: 31 · 2013: 37 · 2012: 29
- FWCI
- 17.20
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (DP1OD000579)
- Canadian Institutes of Health Research
- National Institute of General Medical Sciences (R01GM075315)
- 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 › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- sleep function, synaptic homeostasis, synaptic plasticity, synaptic growth, sleep need, FMR1 gene, Drosophila, neural circuits
- MeSH terms
- Animals, Dendrites, Drosophila melanogaster, Female, Homeostasis, Male, Neuronal Plasticity, Neurons, Neuropeptides, Sleep, Sleep Deprivation, Synapses, Time Factors, Mushroom Bodies, Drosophila Proteins, Fragile X Messenger Ribonucleoprotein 1
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