Sleep and the single neuron: the role of global slow oscillations in individual cell rest
Open accessAbstract
Sleep is universal in animals, but its specific functions remain elusive. We propose that sleep's primary function is to allow individual neurons to perform prophylactic cellular maintenance. Just as muscle cells must rest after strenuous exercise to prevent long-term damage, brain cells must rest after intense synaptic activity. We suggest that periods of reduced synaptic input ('off periods' or 'down states') are necessary for such maintenance. This in turn requires a state of globally synchronized neuronal activity, reduced sensory input and behavioural immobility - the well-known manifestations of sleep.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
During human NREM sleep, the EEG exhibits low-frequency (<4 Hz) oscillatory dynamics that support memory and neural computation.
“During human non-rapid eye movement (NREM) sleep, the electroencephalogram (EEG) exhibits low-frequency (<4 Hz) oscillatory dynamics that support memory and neural computation (1-8).”
From Coupled electrophysiological, hemodynamic, and cerebrospinal fluid oscillations in human sleep (2019) · cites this paper as [7]
The Abstract describes NREM-related EEG slow waves at approximately 1–4 Hz. The Conclusions propose that slow oscillations may facilitate information processing and could enable memory consolidation, but do not establish that these dynamics support memory and neural computation specifically in humans. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes
Buzsáki, G., Anastassiou, C. A., & Koch, C. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3241 · Cited by 4,225 · see citing works
Neurocognitive consequences of sleep deprivation
Goel, N., Rao, H., Durmer, J., & Dinges, D. (2009) · Seminars in Neurology · doi:10.1055/s-0029-1237117 · Cited by 2,154 · see citing works
Huber, R., Felice Ghilardi, M., Massimini, M., & Tononi, G. (2004) · Nature · doi:10.1038/nature02663 · Cited by 1,854 · see citing works
Coordinated memory replay in the visual cortex and hippocampus during sleep
Ji, D., & Wilson, M. A. (2007) · Nature Neuroscience · doi:10.1038/nn1825 · Cited by 1,669 · see citing works
Effects of sleep deprivation on cognition
Killgore, W. D. S. (2010) · Progress in Brain Research · doi:10.1016/b978-0-444-53702-7.00007-5 · Cited by 1,421 · see citing works
The sleep slow oscillation as a traveling wave
Massimini, M., Huber, R., Ferrarelli, F., Hill, S., & Tononi, G. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1318-04.2004 · Cited by 1,221 · see citing works
Vyazovskiy, V. V., Olcese, U., Hanlon, E. C., Nir, Y., Cirelli, C., & Tononi, G. (2011) · Nature · doi:10.1038/nature10009 · Cited by 865 · see citing works
Self-citationCirelli, C., & Tononi, G. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060216 · Cited by 646 · see citing works
Extensive and divergent effects of sleep and wakefulness on brain gene expression
Cirelli, C., Gutierrez, C. M., & Tononi, G. (2004) · Neuron · doi:10.1016/s0896-6273(03)00814-6 · Cited by 627 · see citing works
A deficit in the ability to form new human memories without sleep
Yoo, S.-S., Hu, P. T., Gujar, N., Jolesz, F. A., & Walker, M. P. (2007) · Nature Neuroscience · doi:10.1038/nn1851 · Cited by 597 · see citing works
Destexhe, A., Contreras, D., & Steriade, M. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-11-04595.1999 · Cited by 573 · see citing works
A 4 Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities
Fujisawa, S., & Buzsáki, G. (2011) · Neuron · doi:10.1016/j.neuron.2011.08.018 · Cited by 501 · see citing works
Achermann, P., Dijk, D.-J., Brunner, D. P., & Borbély, A. A. (1993) · Brain Research Bulletin · doi:10.1016/0361-9230(93)90016-5 · Cited by 470 · see citing works
Endoplasmic reticulum dysfunction in neurological disease
Roussel, B. D., Kruppa, A. J., Miranda, E., Crowther, D. C., Lomas, D. A., & Marciniak, S. J. (2013) · The Lancet Neurology · doi:10.1016/s1474-4422(12)70238-7 · Cited by 441 · see citing works
The slow (<1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators
Crunelli, V., & Hughes, S. W. (2010) · Nature Neuroscience · doi:10.1038/nn.2445 · Cited by 435 · see citing works
Riedner, B. A., Vyazovskiy, V. V., Huber, R., Massimini, M., Esser, S., Murphy, M., & Tononi, G. (2007) · Sleep · doi:10.1093/sleep/30.12.1643 · Cited by 424 · see citing works
Self-citationHippocampal-cortical interaction during periods of subcortical silence
Logothetis, N. K., Eschenko, O., Murayama, Y., Augath, M., Steudel, T., Evrard, H. C., Besserve, M., & Oeltermann, A. (2012) · Nature · doi:10.1038/nature11618 · Cited by 420 · see citing works
Lo, J. C., Groeger, J. A., Santhi, N., Arbon, E. L., Lazar, A. S., Hasan, S., von Schantz, M., Archer, S. N., & Dijk, D.-J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045987 · Cited by 342 · see citing works
Biochemical regulation of non-rapid-eye-movement sleep
Krueger, J. M. (2003) · Frontiers in Bioscience · doi:10.2741/1033 · Cited by 329 · 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
Hippocampal sharp wave bursts coincide with neocortical “up-state” transitions
Battaglia, F. P., Sutherland, G. R., & McNaughton, B. L. (2004) · Learning & Memory · doi:10.1101/lm.73504 · Cited by 310 · see citing works
Slow oscillations orchestrating fast oscillations and memory consolidation
Mölle, M., & Born, J. (2011) · Progress in Brain Research · doi:10.1016/b978-0-444-53839-0.00007-7 · Cited by 270 · see citing works
Spectral Analysis of the Sleep Electroencephalogram During Adolescence
(2004) · Sleep · doi:10.1093/sleep/27.4.774 · Cited by 231 · see citing works
Sleep function: current questions and new approaches
Vassalli, A., & Dijk, D. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06767.x · Cited by 110 · see citing works
Flagged first, then by citations
Research works printed but not linked: 179
- Tobler, I. in Principles and Practice of Sleep Medicine (eds Kryger, M. H., Roth, T. & Dement, W. C.) 77–90 (Saunders, 2005). · DOI
- Van Dongen, H. P., Maislin, G., Mullington, J. M. & Dinges, D. F. The cumulative cost of additional wakefulness: dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation. Sleep 26, 117–126 (2003). · DOI · Paper page
- McCoy, J. G. & Strecker, R. E. The cognitive cost of sleep lost. Neurobiol. Learn. Mem. 96, 564–582 (2011). · DOI
- Siegel, J. M. Clues to the functions of mammalian sleep. Nature 437, 1264–1271 (2005). · DOI · Paper page
- Steriade, M., Timofeev, I. & Grenier, F. Natural waking and sleep states: a view from inside neocortical neurons. J. Neurophysiol. 85, 1969–1985 (2001). · DOI · Paper page
- Hobson, J. A. & McCarley, R. W. Cortical unit activity in sleep and waking. Electroencephalogr. Clin. Neurophysiol. 30, 97–112 (1971). · DOI
- Buzsáki, G. Rhythms of the Brain (Oxford Univ. Press, 2006). · DOI · Paper page
- Vyazovskiy, V. V. et al. Cortical firing and sleep homeostasis. Neuron 63, 865–878 (2009). · DOI · Paper page
- Verzeano, M. & Negishi, K. Neuronal activity in cortical and thalamic networks. J. Gen. Physiol. 43, 177–195 (1960). · DOI
- Noda, H. & Adey, W. R. Firing of neuron pairs in cat association cortex during sleep and wakefulness. J. Neurophysiol. 33, 672–684 (1970). · DOI
- Burns, B. D., Stean, J. P. & Webb, A. C. The effects of sleep on neurons in isolated cerebral cortex. Proc. R. Soc. Lond. B 206, 281–291 (1979). · DOI
- Harris, K. D. & Thiele, A. Cortical state and attention. Nature Rev. Neurosci. 12, 509–523 (2011). · DOI
- Nir, Y. et al. Regional slow waves and spindles in human sleep. Neuron 70, 153–169 (2011). · DOI · Paper page
- Chauvette, S., Volgushev, M. & Timofeev, I. Origin of active states in local neocortical networks during slow sleep oscillation. Cereb. Cortex 20, 2660–2674 (2010). · DOI · Paper page
- Poulet, J. F. & Petersen, C. C. Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454, 881–885 (2008). · DOI · Paper page
- Saleem, A. B., Chadderton, P., Apergis-Schoute, J., Harris, K. D. & Schultz, S. R. Methods for predicting cortical UP and DOWN states from the phase of deep layer local field potentials. J. Comput. Neurosci. 29, 49–62 (2010). · DOI
- Okun, M. & Lampl, I. Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities. Nature Neurosci. 11, 535–537 (2008). · DOI
- Mackiewicz, M. et al. Macromolecule biosynthesis: a key function of sleep. Physiol. Genomics 31, 441–457 (2007). · DOI
- Reimund, E. The free radical flux theory of sleep. Med. Hypotheses 43, 231–233 (1994). · DOI
- Inoue, S., Honda, K. & Komoda, Y. Sleep as neuronal detoxification and restitution. Behav. Brain Res. 69, 91–96 (1995). · DOI
- Benington, J. H. & Heller, H. C. Restoration of brain energy metabolism as the function of sleep. Prog. Neurobiol. 45, 347–360 (1995). · DOI
- Scharf, M. T., Naidoo, N., Zimmerman, J. E. & Pack, A. I. The energy hypothesis of sleep revisited. Prog. Neurobiol. 86, 264–280 (2008). · DOI
- Buzsaki, G. Memory consolidation during sleep: a neurophysiological perspective. J. Sleep Res. 7, 17–23 (1998). · DOI
- Sejnowski, T. J. & Destexhe, A. Why do we sleep? Brain Res. 886, 208–223 (2000). · DOI · Paper page
- Born, J., Rasch, B. & Gais, S. Sleep to remember. Neuroscientist 12, 410–424 (2006). · DOI · Paper page
- Tononi, G. & Cirelli, C. Time to be SHY? Some comments on sleep and synaptic homeostasis. Neural Plast. 2012, 415250 (2012). · DOI
- Hernandez, P. J. & Abel, T. A molecular basis for interactions between sleep and memory. Sleep Med. Clin. 6, 71–84 (2011). · DOI
- Krueger, J. M. & Tononi, G. Local use-dependent sleep; synthesis of the new paradigm. Curr. Top. Med. Chem. 11, 2490–2492 (2011). · DOI
- Tononi, G. & Cirelli, C. Sleep function and synaptic homeostasis. Sleep Med. Rev. 10, 49–62 (2006). · DOI · Paper page
- Frank, M. G. The mystery of sleep function: current perspectives and future directions. Rev. Neurosci. 17, 375–392 (2006). · DOI · Paper page
- Wilson, M. A. & McNaughton, B. L. Reactivation of hippocampal ensemble memories during sleep. Science 265, 676–679 (1994). · DOI · Paper page
- Tononi, G., Massimini, M. & Riedner, B. A. Sleepy dialogues between cortex and hippocampus: who talks to whom? Neuron 52, 748–749 (2006). · DOI
- Frank, M. G. Erasing synapses in sleep: is it time to be SHY? Neural Plast. 2012, 264378 (2012). · DOI · Paper page
- Diekelmann, S. & Born, J. The memory function of sleep. Nature Rev. Neurosci. 11, 114–126 (2010). · DOI · Paper page
- Doran, S. M., Van Dongen, H. P. & Dinges, D. F. Sustained attention performance during sleep deprivation: evidence of state instability. Arch. Ital. Biol. 139, 253–267 (2001).
- Van Dongen, H. P., Belenky, G. & Krueger, J. M. A local, bottom-up perspective on sleep deprivation and neurobehavioral performance. Curr. Top. Med. Chem. 11, 2414–2422 (2011). · DOI
- Piantoni, G. et al. Individual differences in white matter diffusion affect sleep oscillations. J. Neurosci. 33, 227–233 (2013). · DOI
- Leger, J. F., Stern, E. A., Aertsen, A. & Heck, D. Synaptic integration in rat frontal cortex shaped by network activity. J. Neurophysiol. 93, 281–293 (2005). · DOI
- Petersen, C. C., Hahn, T. T., Mehta, M., Grinvald, A. & Sakmann, B. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc. Natl Acad. Sci. USA 100, 13638–13643 (2003). · DOI
- Constantinople, C. M. & Bruno, R. M. Effects and mechanisms of wakefulness on local cortical networks. Neuron 69, 1061–1068 (2011). · DOI · Paper page
- Krueger, J. M. et al. Sleep as a fundamental property of neuronal assemblies. Nature Rev. Neurosci. 9, 910–919 (2008). · DOI · Paper page
- Rattenborg, N. C., Lima, S. L. & Lesku, J. A. Sleep locally, act globally. Neuroscientist 18, 533–546 (2012). · DOI
- Borbely, A. A. A two process model of sleep regulation. Hum. Neurobiol. 1, 195–204 (1982).
- Borbély, A. A. & Achermann, P. in Principles and Practice of Sleep Medicine (eds Kryger, M. H., Roth, T. & Dement, W. C.) 405–417 (Saunders, 2005). · DOI
- Ferrara, M., De Gennaro, L., Casagrande, M. & Bertini, M. Auditory arousal thresholds after selective slow-wave sleep deprivation. Clin. Neurophysiol. 110, 2148–2152 (1999). · DOI
- Daan, S., Beersma, D. G. & Borbely, A. A. Timing of human sleep: recovery process gated by a circadian pacemaker. Am. J. Physiol. 246, R161–R183 (1984).
- Franken, P., Chollet, D. & Tafti, M. The homeostatic regulation of sleep need is under genetic control. J. Neurosci. 21, 2610–2621 (2001). · DOI
- Tobler, I. & Borbely, A. A. Sleep EEG in the rat as a function of prior waking. Electroencephalogr. Clin. Neurophysiol. 64, 74–76 (1986). · DOI
- Vyazovskiy, V. V., Achermann, P. & Tobler, I. Sleep homeostasis in the rat in the light and dark period. Brain Res. Bull. 74, 37–44 (2007). · DOI
- Vyazovskiy, V., Borbely, A. A. & Tobler, I. Unilateral vibrissae stimulation during waking induces interhemispheric EEG asymmetry during subsequent sleep in the rat. J. Sleep Res. 9, 367–371 (2000). · DOI · Paper page
- Kristiansen, K. & Courtois, G. Rhythmic electrical activity from isolated cerebral cortex. Electroencephalogr. Clin. Neurophysiol. 1, 265–272 (1949). · DOI
- Krueger, J. M. & Obal, F. A neuronal group theory of sleep function. J. Sleep Res. 2, 63–69 (1993). · DOI
- Pigarev, I. N., Nothdurft, H. C. & Kastner, S. Evidence for asynchronous development of sleep in cortical areas. Neuroreport 8, 2557–2560 (1997). · DOI
- Mukhametov, L. M., Supin, A. Y. & Polyakova, I. G. Interhemispheric asymmetry of the electroencephalographic sleep patterns in dolphins. Brain Res. 134, 581–584 (1977). · DOI
- Lyamin, O. I., Pavlova, I. F., Kosenko, P. O., Mukhametov, L. M. & Siegel, J. M. Regional differences in cortical electroencephalogram (EEG) slow wave activity and interhemispheric EEG asymmetry in the fur seal. J. Sleep Res. 21, 603–611 (2012). · DOI
- Werth, E., Achermann, P. & Borbely, A. A. Brain topography of the human sleep EEG: antero-posterior shifts of spectral power. Neuroreport 8, 123–127 (1996). · DOI
- Cajochen, C., Foy, R. & Dijk, D. J. Frontal predominance of a relative increase in sleep delta and theta EEG activity after sleep loss in humans. Sleep Res. Online 2, 65–69 (1999).
- Huber, R., Deboer, T. & Tobler, I. Topography of EEG dynamics after sleep deprivation in mice. J. Neurophysiol. 84, 1888–1893 (2000). · DOI · Paper page
- Vyazovskiy, V. V. & Tobler, I. Regional differences in NREM sleep slow-wave activity in mice with congenital callosal dysgenesis. J. Sleep Res. 14, 299–304 (2005). · DOI
- Vyazovskiy, V. V., Borbely, A. A. & Tobler, I. Interhemispheric sleep EEG asymmetry in the rat is enhanced by sleep deprivation. J. Neurophysiol. 88, 2280–2286 (2002). · DOI
- Achermann, P., Finelli, L. A. & Borbely, A. A. Unihemispheric enhancement of delta power in human frontal sleep EEG by prolonged wakefulness. Brain Res. 913, 220–223 (2001). · DOI
- Volgushev, M., Chauvette, S., Mukovski, M. & Timofeev, I. Precise long-range synchronization of activity and silence in neocortical neurons during slow-wave oscillations [corrected]. J. Neurosci. 26, 5665–5672 (2006). · DOI · Paper page
- Luczak, A., Bartho, P., Marguet, S. L., Buzsaki, G. & Harris, K. D. Sequential structure of neocortical spontaneous activity in vivo. Proc. Natl Acad. Sci. USA 104, 347–352 (2007). · DOI · Paper page
- Mohajerani, M. H., McVea, D. A., Fingas, M. & Murphy, T. H. Mirrored bilateral slow-wave cortical activity within local circuits revealed by fast bihemispheric voltage-sensitive dye imaging in anesthetized and awake mice. J. Neurosci. 30, 3745–3751 (2010). · DOI
- Sirota, A. & Buzsaki, G. Interaction between neocortical and hippocampal networks via slow oscillations. Thalamus Relat. Syst. 3, 245–259 (2005). · DOI · Paper page
- Vyazovskiy, V. V., Faraguna, U., Cirelli, C. & Tononi, G. Triggering slow waves during NREM sleep in the rat by intracortical electrical stimulation: effects of sleep/wake history and background activity. J. Neurophysiol. 101, 1921–1931 (2009). · DOI
- Kattler, H., Dijk, D. J. & Borbely, A. A. Effect of unilateral somatosensory stimulation prior to sleep on the sleep EEG in humans. J. Sleep Res. 3, 159–164 (1994). · DOI · Paper page
- Vyazovskiy, V. V., Welker, E., Fritschy, J. M. & Tobler, I. Regional pattern of metabolic activation is reflected in the sleep EEG after sleep deprivation combined with unilateral whisker stimulation in mice. Eur. J. Neurosci. 20, 1363–1370 (2004). · DOI
- Vyazovskiy, V. V. & Tobler, I. Handedness leads to interhemispheric EEG asymmetry during sleep in the rat. J. Neurophysiol. 99, 969–975 (2008). · DOI
- Miyamoto, H., Katagiri, H. & Hensch, T. Experience-dependent slow-wave sleep development. Nature Neurosci. 6, 553–554 (2003). · DOI
- Dang-Vu, T. T. et al. Neuroimaging in sleep medicine. Sleep Med. 8, 349–372 (2007). · DOI
- Hofle, N. et al. Regional cerebral blood flow changes as a function of delta and spindle activity during slow wave sleep in humans. J. Neurosci. 17, 4800–4808 (1997). · DOI
- Vyazovskiy, V., Achermann, P., Borbely, A. A. & Tobler, I. Interhemispheric coherence of the sleep electroencephalogram in mice with congenital callosal dysgenesis. Neuroscience 124, 481–488 (2004). · DOI
- Kultz, D. Molecular and evolutionary basis of the cellular stress response. Annu. Rev. Physiol. 67, 225–257 (2005). · DOI
- Kourtis, N. & Tavernarakis, N. Cellular stress response pathways and ageing: intricate molecular relationships. EMBO J. 30, 2520–2531 (2011). · DOI
- Martindale, J. L. & Holbrook, N. J. Cellular response to oxidative stress: signaling for suicide and survival. J. Cell. Physiol. 192, 1–15 (2002). · DOI
- Richter, K., Haslbeck, M. & Buchner, J. The heat shock response: life on the verge of death. Mol. Cell 40, 253–266 (2010). · DOI
- Walter, P. & Ron, D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081–1086 (2011). · DOI
- Groenendyk, J. Sreenivasaiah, P. K., Kim do, H., Agellon, L. B. & Michalak, M. Biology of endoplasmic reticulum stress in the heart. Circ. Res. 107, 1185–1197 (2010). · DOI
- Doyle, K. M. et al. Unfolded proteins and endoplasmic reticulum stress in neurodegenerative disorders. J. Cell. Mol. Med. 15, 2025–2039 (2011). · DOI
- Allen, D. G., Lamb, G. D. & Westerblad, H. Skeletal muscle fatigue: cellular mechanisms. Physiol. Rev. 88, 287–332 (2008). · DOI · Paper page
- Garland, S. J. & Gossen, E. R. The muscular wisdom hypothesis in human muscle fatigue. Exerc. Sport Sci. Rev. 30, 45–49 (2002). · DOI
- Powers, S. K. & Jackson, M. J. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol. Rev. 88, 1243–1276 (2008). · DOI · Paper page
- Westerblad, H. & Allen, D. G. Emerging roles of ROS/RNS in muscle function and fatigue. Antioxid. Redox Signal. 15, 2487–2499 (2011). · DOI
- Keyser, R. E. Peripheral fatigue: high-energy phosphates and hydrogen ions. PM R 2, 347–358 (2010). · DOI
- Fitts, R. H. The cross-bridge cycle and skeletal muscle fatigue. J. Appl. Physiol. 104, 551–558 (2008). · DOI
- Debold, E. P. Recent insights into muscle fatigue at the cross-bridge level. Front. Physiol. 3, 151 (2012). · DOI
- Salo, D. C., Donovan, C. M. & Davies, K. J. HSP70 and other possible heat shock or oxidative stress proteins are induced in skeletal muscle, heart, and liver during exercise. Free Radic. Biol. Med. 11, 239–246 (1991). · DOI
- MacIntosh, B. R., Holash, R. J. & Renaud, J. M. Skeletal muscle fatigue-regulation of excitation-contraction coupling to avoid metabolic catastrophe. J. Cell Sci. 125, 2105–2114 (2012). · DOI
- Wu, J. et al. The unfolded protein response mediates adaptation to exercise in skeletal muscle through a PGC-1α/ATF6α complex. Cell Metab. 13, 160–169 (2011). · DOI · Paper page
- Naidoo, N., Giang, W., Galante, R. J. & Pack, A. I. Sleep deprivation induces the unfolded protein response in mouse cerebral cortex. J. Neurochem. 92, 1150–1157 (2005). · DOI · Paper page
- Terao, A. et al. Differential increase in the expression of heat shock protein family members during sleep deprivation and during sleep. Neuroscience 116, 187–200 (2003). · DOI
- Shaw, P. J., Tononi, G., Greenspan, R. J. & Robinson, D. F. Stress response genes protect against lethal effects of sleep deprivation in Drosophila. Nature 417, 287–291 (2002). · DOI · Paper page
- Franken, P., Dijk, D. J., Tobler, I. & Borbely, A. A. Sleep deprivation in rats: effects on EEG power spectra, vigilance states, and cortical temperature. Am. J. Physiol. 261, R198–R208 (1991).
- Nikonova, E. V. et al. Changes in components of energy regulation in mouse cortex with increases in wakefulness. Sleep 33, 889–900 (2010). · DOI
- Denker, A. & Rizzoli, S. O. Synaptic vesicle pools: an update. Front. Synaptic Neurosci. 2, 135 (2010).
- Esposito, G., Ana Clara, F. & Verstreken, P. Synaptic vesicle trafficking and Parkinson's disease. Dev. Neurobiol. 72, 134–144 (2011). · DOI
- Vanden Berghe, P. & Klingauf, J. Synaptic vesicles in rat hippocampal boutons recycle to different pools in a use-dependent fashion. J. Physiol. 572, 707–720 (2006). · DOI
- Burre, J. et al. α-synuclein promotes SNARE-complex assembly in vivo and in vitro. Science 329, 1663–1667 (2010). · DOI
- Attwell, D. & Gibb, A. Neuroenergetics and the kinetic design of excitatory synapses. Nature Rev. Neurosci. 6, 841–849 (2005). · DOI
- Hinard, V. et al. Key electrophysiological, molecular, and metabolic signatures of sleep and wakefulness revealed in primary cortical cultures. J. Neurosci. 32, 12506–12517 (2012). · DOI
- Cirelli, C., Shaw, P. J., Rechtschaffen, A. & Tononi, G. No evidence of brain cell degeneration after long-term sleep deprivation in rats. Brain Res. 840, 184–193 (1999). · DOI
- Gopalakrishnan, A., Ji, L. L. & Cirelli, C. Sleep deprivation and cellular responses to oxidative stress. Sleep 27, 27–35 (2004). · DOI
- Vyazovskiy, V. V. & Tobler, I. Theta activity in the waking EEG is a marker of sleep propensity in the rat. Brain Res. 1050, 64–71 (2005). · DOI
- Okun, M., Naim, A. & Lampl, I. The subthreshold relation between cortical local field potential and neuronal firing unveiled by intracellular recordings in awake rats. J. Neurosci. 30, 4440–4448 (2010). · DOI
- Cajochen, C., Wyatt, J. K., Czeisler, C. A. & Dijk, D. J. Separation of circadian and wake duration-dependent modulation of EEG activation during wakefulness. Neuroscience 114, 1047–1060 (2002). · DOI
- Finelli, L. A., Baumann, H., Borbely, A. A. & Achermann, P. Dual electroencephalogram markers of human sleep homeostasis: correlation between theta activity in waking and slow-wave activity in sleep. Neuroscience 101, 523–529 (2000). · DOI · Paper page
- Landolt, H. P. et al. Caffeine attenuates waking and sleep electroencephalographic markers of sleep homeostasis in humans. Neuropsychopharmacology 29, 1933–1939 (2004). · DOI
- Leemburg, S. et al. Sleep homeostasis in the rat is preserved during chronic sleep restriction. Proc. Natl Acad. Sci. USA 107, 15939–15944 (2010). · DOI · Paper page
- Hung, C. S. et al. Local experience-dependent changes in the wake EEG after prolonged wakefulness. Sleep 36, 59–72 (2013). · DOI
- Crochet, S. & Petersen, C. C. Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nature Neurosci. 9, 608–610 (2006). · DOI
- Haider, B., Duque, A., Hasenstaub, A. R., Yu, Y. & McCormick, D. A. Enhancement of visual responsiveness by spontaneous local network activity in vivo. J. Neurophysiol. 97, 4186–4202 (2007). · DOI · Paper page
- Hasenstaub, A., Sachdev, R. N. & McCormick, D. A. State changes rapidly modulate cortical neuronal responsiveness. J. Neurosci. 27, 9607–9622 (2007). · DOI · Paper page
- Sachdev, R. N., Ebner, F. F. & Wilson, C. J. Effect of subthreshold up and down states on the whisker-evoked response in somatosensory cortex. J. Neurophysiol. 92, 3511–3521 (2004). · DOI
- Vyazovskiy, V. V., Olcese, U., Cirelli, C. & Tononi, G. Prolonged wakefulness alters neuronal responsiveness to local electrical stimulation of the neocortex in awake rats. J. Sleep Res. 21 Nov 2012 (doi:10.1111/jsr.12009). · DOI
- Luczak, A., Bartho, P. & Harris, K. D. Gating of sensory input by spontaneous cortical activity. J. Neurosci. 33, 1684–1695 (2013). · DOI
- Goard, M. & Dan, Y. Basal forebrain activation enhances cortical coding of natural scenes. Nature Neurosci. 12, 1444–1449 (2009). · DOI
- Marguet, S. L. & Harris, K. D. State-dependent representation of amplitude-modulated noise stimuli in rat auditory cortex. J. Neurosci. 31, 6414–6420 (2011). · DOI
- Aeschbach, D. et al. Dynamics of the human EEG during prolonged wakefulness: evidence for frequency-specific circadian and homeostatic influences. Neurosci. Lett. 239, 121–124 (1997). · DOI · Paper page
- Cajochen, C., Brunner, D. P., Krauchi, K., Graw, P. & Wirz-Justice, A. Power density in theta/α frequencies of the waking EEG progressively increases during sustained wakefulness. Sleep 18, 890–894 (1995). · DOI
- Oleksenko, A. I., Mukhametov, L. M., Polyakova, I. G., Supin, A. Y. & Kovalzon, V. M. Unihemispheric sleep deprivation in bottlenose dolphins. J. Sleep Res. 1, 40–44 (1992). · DOI
- Lyamin, O. I., Kosenko, P. O., Lapierre, J. L., Mukhametov, L. M. & Siegel, J. M. Fur seals display a strong drive for bilateral slow-wave sleep while on land. J. Neurosci. 28, 12614–12621 (2008). · DOI
- Sanchez-Vives, M. V. et al. Inhibitory modulation of cortical up states. J. Neurophysiol. 104, 1314–1324 (2010). · DOI
- Chen, J. Y., Chauvette, S., Skorheim, S., Timofeev, I. & Bazhenov, M. Interneuron-mediated inhibition synchronizes neuronal activity during slow oscillation. J. Physiol. 590, 3987–4010 (2012). · DOI
- Lamb, G. D. & Westerblad, H. Acute effects of reactive oxygen and nitrogen species on the contractile function of skeletal muscle. J. Physiol. 589, 2119–2127 (2011). · DOI
- Wang, T. A. et al. Circadian rhythm of redox state regulates excitability in suprachiasmatic nucleus neurons. Science 337, 839–842 (2012). · DOI
- Kapas, L., Obal, F. Jr & Krueger, J. M. Humoral regulation of sleep. Int. Rev. Neurobiol. 35, 131–160 (1993). · DOI
- Porkka-Heiskanen, T. et al. Adenosine: a mediator of the sleep-inducing effects of prolonged wakefulness. Science 276, 1265–1268 (1997). · DOI · Paper page
- Latini, S. & Pedata, F. Adenosine in the central nervous system: release mechanisms and extracellular concentrations. J. Neurochem. 79, 463–484 (2001). · DOI
- Krueger, J. M., Obal, F. J., Fang, J., Kubota, T. & Taishi, P. The role of cytokines in physiological sleep regulation. Ann. NY Acad. Sci. 933, 211–221 (2001). · DOI
- Kilduff, T. S., Cauli, B. & Gerashchenko, D. Activation of cortical interneurons during sleep: an anatomical link to homeostatic sleep regulation? Trends Neurosci. 34, 10–19 (2011). · DOI
- Kang, J. E. et al. Amyloid-β dynamics are regulated by orexin and the sleep-wake cycle. Science 326, 1005–1007 (2009). · DOI · Paper page
- Brown, R. E., Basheer, R., McKenna, J. T., Strecker, R. E. & McCarley, R. W. Control of sleep and wakefulness. Physiol. Rev. 92, 1087–1187 (2012). · DOI · Paper page
- Kamenetz, F. et al. APP processing and synaptic function. Neuron 37, 925–937 (2003). · DOI · Paper page
- Saper, C. B., Fuller, P. M., Pedersen, N. P., Lu, J. & Scammell, T. E. Sleep state switching. Neuron 68, 1023–1042 (2010). · DOI · Paper page
- Sirota, A., Csicsvari, J., Buhl, D. & Buzsaki, G. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl Acad. Sci. USA 100, 2065–2069 (2003). · DOI · Paper page
- Isomura, Y. et al. Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron 52, 871–882 (2006). · DOI · Paper page
- Ros, H., Sachdev, R. N., Yu, Y., Sestan, N. & McCormick, D. A. Neocortical networks entrain neuronal circuits in cerebellar cortex. J. Neurosci. 29, 10309–10320 (2009). · DOI · Paper page
- Timofeev, I. & Steriade, M. Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats. J. Neurophysiol. 76, 4152–4168 (1996). · DOI · Paper page
- Cowan, R. L. & Wilson, C. J. Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J. Neurophysiol. 71, 17–32 (1994). · DOI
- Lancel, M., van Riezen, H. & Glatt, A. Enhanced slow-wave activity within NREM sleep in the cortical and subcortical EEG of the cat after sleep deprivation. Sleep 15, 102–118 (1992). · DOI
- Khazipov, R. & Luhmann, H. J. Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci. 29, 414–418 (2006). · DOI · Paper page
- Nelson, A. B., Faraguna, U., Tononi, G. & Cirelli, C. Effects of anesthesia on the response to sleep deprivation. Sleep 33, 1659–1667 (2010). · DOI · Paper page
- Murphy, M. et al. Propofol anesthesia and sleep: a high-density EEG study. Sleep 34, 283–291 (2011). · DOI · Paper page
- Amzica, F. & Kroeger, D. Cellular mechanisms underlying EEG waveforms during coma. Epilepsia 52, 25–27 (2011). · DOI
- Marshall, L., Helgadottir, H., Molle, M. & Born, J. Boosting slow oscillations during sleep potentiates memory. Nature 444, 610–613 (2006). · DOI · Paper page
- Moruzzi, G. The sleep-waking cycle. Ergeb. Physiol. 64, 1–165 (1972).
- Cirelli, C. & Tononi, G. Gene expression in the brain across the sleep-waking cycle. Brain Res. 885, 303–321 (2000). · DOI
- Vyazovskiy, V. V., Ruijgrok, G., Deboer, T. & Tobler, I. Running wheel accessibility affects the regional electroencephalogram during sleep in mice. Cereb. Cortex 16, 328–336 (2006). · DOI
- Vyazovskiy, V. V. & Tobler, I. The temporal structure of behaviour and sleep homeostasis. PLoS ONE 7, e50677 (2012). · DOI
- Kim, Y., Park, M., Boghossian, S. & York, D. A. Three weeks voluntary running wheel exercise increases endoplasmic reticulum stress in the brain of mice. Brain Res. 1317, 13–23 (2010). · DOI
- Churchill, L. et al. Tumor necrosis factor α: activity dependent expression and promotion of cortical column sleep in rats. Neuroscience 156, 71–80 (2008). · DOI
- Xue, X. et al. Tumor necrosis factor α (TNFα) induces the unfolded protein response (UPR) in a reactive oxygen species (ROS)-dependent fashion, and the UPR counteracts ROS accumulation by TNFα. J. Biol. Chem. 280, 33917–33925 (2005). · DOI
- Gao, B. et al. Sleep disruption aggravates focal cerebral ischemia in the rat. Sleep 33, 879–887 (2010). · DOI
- Du, F., Eid, T., Lothman, E. W., Kohler, C. & Schwarcz, R. Preferential neuronal loss in layer III of the medial entorhinal cortex in rat models of temporal lobe epilepsy. J. Neurosci. 15, 6301–6313 (1995). · DOI
- Drexel, M., Preidt, A. P. & Sperk, G. Sequel of spontaneous seizures after kainic acid-induced status epilepticus and associated neuropathological changes in the subiculum and entorhinal cortex. Neuropharmacology 63, 806–817 (2012). · DOI
- Fritsch, B. et al. Pathological alterations in GABAergic interneurons and reduced tonic inhibition in the basolateral amygdala during epileptogenesis. Neuroscience 163, 415–429 (2009). · DOI
- Arundine, M. & Tymianski, M. Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 34, 325–337 (2003). · DOI
- Brennan, G. P. et al. Transgenic overexpression of 14-3-3 zeta protects hippocampus against endoplasmic reticulum stress and status epilepticus in vivo. PLoS ONE 8, e54491 (2013). · DOI
- Murphy, N. et al. Depletion of 14-3-3 zeta elicits endoplasmic reticulum stress and cell death, and increases vulnerability to kainate-induced injury in mouse hippocampal cultures. J. Neurochem. 106, 978–988 (2008). · DOI
- Dauvilliers, Y. Insomnia in patients with neurodegenerative conditions. Sleep Med. 8, S27–S34 (2007). · DOI
- Frank, M. G. & Heller, H. C. The ontogeny of mammalian sleep: a reappraisal of alternative hypotheses. J. Sleep Res. 12, 25–34 (2003). · DOI
- Corner, M. & van der Togt, C. No phylogeny without ontogeny: a comparative and developmental search for the sources of sleep-like neural and behavioral rhythms. Neurosci. Bull. 28, 25–38 (2012). · DOI
- Blumberg, M. S. Homology, correspondence, and continuity across development: the case of sleep. Dev. Psychobiol. 55, 92–100 (2013). · DOI
- Khazipov, R. et al. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432, 758–761 (2004). · DOI
- Dreyfus-Brisac, C. & Larroche, J. C. Discontinuous electroencephalograms in the premature newborn and at term. Electro-anatomo-clinical correlations. Rev. Electroencephalogr. Neurophysiol. Clin. 1, 95–99 (1971) (in French). · DOI
- Andre, M. et al. Electroencephalography in premature and full-term infants. Developmental features and glossary. Neurophysiol. Clin. 40, 59–124 (2010). · DOI
- Kroeger, D. & Amzica, F. Hypersensitivity of the anesthesia-induced comatose brain. J. Neurosci. 27, 10597–10607 (2007). · DOI
- Katz, L. C. & Shatz, C. J. Synaptic activity and the construction of cortical circuits. Science 274, 1133–1138 (1996). · DOI · Paper page
- Frank, M. G. & Heller, H. C. Development of diurnal organization of EEG slow-wave activity and slow-wave sleep in the rat. Am. J. Physiol. 273, R472–R478 (1997).
- Alfoldi, P., Tobler, I. & Borbely, A. A. Sleep regulation in rats during early development. Am. J. Physiol. 258, R634–R644 (1990).
- Kurth, S. et al. Characteristics of sleep slow waves in children and adolescents. Sleep 33, 475–480 (2010). · DOI · Paper page
- Kurth, S. et al. Mapping of cortical activity in the first two decades of life: a high-density sleep electroencephalogram study. J. Neurosci. 30, 13211–13219 (2010). · DOI · Paper page
- Ohayon, M. M., Carskadon, M. A., Guilleminault, C. & Vitiello, M. V. Meta-analysis of quantitative sleep parameters from childhood to old age in healthy individuals: developing normative sleep values across the human lifespan. Sleep 27, 1255–1273 (2004). · DOI · Paper page
- Shahbazian, F. M., Jacobs, M. & Lajtha, A. Regional and cellular differences in rat brain protein synthesis in vivo and in slices during development. Int. J. Dev. Neurosci. 4, 209–215 (1986). · DOI
- Sun, Y. et al. Rates of local cerebral protein synthesis in the rat during normal postnatal development. Am. J. Physiol. 268, R549–R561 (1995).
- Giuffrida, A. M. et al. Mitochondrial DNA, RNA, and protein synthesis in different regions of developing rat brain. Neurochem. Res. 4, 37–52 (1979). · DOI
- Lerner, M. P. & Johnson, T. C. Regulation of protein synthesis in developing mouse brain tissue. Alteration in ribosomal activity. J. Biol. Chem. 245, 1388–1393 (1970). · DOI
- Zhang, X., Szabo, E., Michalak, M. & Opas, M. Endoplasmic reticulum stress during the embryonic development of the central nervous system in the mouse. Int. J. Dev. Neurosci. 25, 455–463 (2007). · DOI
Cited by
Sorted by citations
Tononi, G., & Cirelli, C. (2014) · Neuron · doi:10.1016/j.neuron.2013.12.025 · Cited by 2,356 · see citing works
Coupled electrophysiological, hemodynamic, and cerebrospinal fluid oscillations in human sleep
Fultz, N. E., Bonmassar, G., Setsompop, K., Stickgold, R. A., Rosen, B. R., Polimeni, J. R., & Lewis, L. D. (2019) · Science · doi:10.1126/science.aax5440 · Cited by 1,197 · see citing works
Sleep function: Toward elucidating an enigma
Krueger, J. M., Frank, M. G., Wisor, J. P., & Roy, S. (2016) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2015.08.005 · Cited by 440 · see citing works
Exploring phylogeny to find the function of sleep
Anafi, R. C., Kayser, M. S., & Raizen, D. M. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0098-9 · Cited by 259 · see citing works
NREM and REM Sleep: Complementary Roles in Recovery after Wakefulness
Vyazovskiy, V. V., & Delogu, A. (2014) · The Neuroscientist · doi:10.1177/1073858413518152 · Cited by 169 · see citing works
Self-citationHarris, S. S., Wolf, F., De Strooper, B., & Busche, M. A. (2020) · Neuron · doi:10.1016/j.neuron.2020.06.005 · Cited by 161 · see citing works
Deep sleep maintains learning efficiency of the human brain
Fattinger, S., de Beukelaar, T. T., Ruddy, K. L., Volk, C., Heyse, N. C., Herbst, J. A., Hahnloser, R. H. R., Wenderoth, N., & Huber, R. (2017) · Nature Communications · doi:10.1038/ncomms15405 · Cited by 148 · see citing works
The vigilant sleeper: neural mechanisms of sensory (de)coupling during sleep
Andrillon, T., & Kouider, S. (2020) · Current Opinion in Physiology · doi:10.1016/j.cophys.2019.12.002 · Cited by 133 · see citing works
Local sleep-like cortical reactivity in the awake brain after focal injury
Sarasso, S., D’Ambrosio, S., Fecchio, M., Casarotto, S., Viganò, A., Landi, C., Mattavelli, G., Gosseries, O., Quarenghi, M., Laureys, S., et al. (2020) · Brain · doi:10.1093/brain/awaa338 · Cited by 128 · see citing works
How Much Sleep Does an Elite Athlete Need?
Sargent, C., Lastella, M., Halson, S. L., & Roach, G. D. (2021) · International Journal of Sports Physiology and Performance · doi:10.1123/ijspp.2020-0896 · Cited by 124 · see citing works
Elmenhorst, D., Elmenhorst, E.-M., Hennecke, E., Kroll, T., Matusch, A., Aeschbach, D., & Bauer, A. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1614677114 · Cited by 92 · see citing works
Thomas, R. J., Mietus, J. E., Peng, C.-K., Guo, D., Gozal, D., Montgomery-Downs, H., Gottlieb, D. J., Wang, C.-Y., & Goldberger, A. L. (2014) · Sleep Medicine · doi:10.1016/j.sleep.2013.10.002 · Cited by 90 · see citing works
Sleep, circadian rhythms, and type 2 diabetes mellitus
Parameswaran, G., & Ray, D. W. (2022) · Clinical Endocrinology · doi:10.1111/cen.14607 · Cited by 85 · see citing works
Rodriguez, A. V., Funk, C. M., Vyazovskiy, V. V., Nir, Y., Tononi, G., & Cirelli, C. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.1614-16.2016 · Cited by 76 · see citing works
Self-citationApical drive-A cellular mechanism of dreaming?
Aru, J., Siclari, F., Phillips, W. A., & Storm, J. F. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.09.018 · Cited by 74 · see citing works
Neuroscience-driven discovery and development of sleep therapeutics
Dresler, M., Spoormaker, V. I., Beitinger, P., Czisch, M., Kimura, M., Steiger, A., & Holsboer, F. (2014) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.10.012 · Cited by 63 · see citing works
Cortical regulation of two-stage rapid eye movement sleep
Dong, Y., Li, J., Zhou, M., Du, Y., & Liu, D. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01195-2 · Cited by 60 · see citing works
Olcese, U., Bos, J. J., Vinck, M., & Pennartz, C. M. A. (2018) · Sleep · doi:10.1093/sleep/zsy167 · Cited by 18 · see citing works
- Authors
- Vyazovskiy, V. V., & Harris, K. D.
- Affiliations
- University of Surrey (GB)
- UCL Queen Square Institute of Neurology (GB)
- Corresponding author
- Vyazovskiy, Vladyslav V.
- Harris, Kenneth D.
- Venue
- Nature Reviews Neuroscience
- Published
- 2013-05-02
- Volume
- 14
- Issue
- 6
- Pages
- 443-451
- ISSN
- 1471-003X (ISSN-L)
- 1471-0048
- PMC
- PMC3972489
- OpenAlex
- W2058452561
- Cited by
- 386
- References
- 24
- Citations by year
- 2026: 27 · 2025: 35 · 2024: 49 · 2023: 26 · 2022: 30 · 2021: 27 · 2020: 21 · 2019: 42 · 2018: 29 · 2017: 32 · 2016: 18 · 2015: 22 · 2014: 22 · 2013: 6
- FWCI
- 1.78
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature reviews. Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Wellcome Trust (095668)
- Engineering and Physical Sciences Research Council (EP/I005102/2, EP/K015141/1, EP/I005102/1)
- National Institute on Deafness and Other Communication Disorders (R01DC009947)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
- Keywords
- sleep function, slow oscillations, synaptic homeostasis
- MeSH terms
- Animals, Cell Physiological Phenomena, Humans, Models, Biological, Neurons, Rest, Sleep, Brain Waves
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