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Network Homeostasis and State Dynamics of Neocortical Sleep
Open accessAbstract
Sleep exerts many effects on mammalian forebrain networks, including homeostatic effects on both synaptic strengths and firing rates. We used large-scale recordings to examine the activity of neurons in the frontal cortex of rats and first observed that the distribution of pyramidal cell firing rates was wide and strongly skewed toward high firing rates. Moreover, neurons from different parts of that distribution were differentially modulated by sleep substates. Periods of nonREM sleep reduced the activity of high firing rate neurons and tended to upregulate firing of slow-firing neurons. By contrast, the effect of REM was to reduce firing rates across the entire rate spectrum. Microarousals, interspersed within nonREM epochs, increased firing rates of slow-firing neurons. The net result of sleep was to homogenize the firing rate distribution. These findings are at variance with current homeostatic models and provide a novel view of sleep in adjusting network excitability.
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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 [8]
The Results section, “Firing rate and LFP changes within nonREM episodes and packets” (page unavailable), identifies a 0.5–4 Hz delta band during NREM sleep. But the Experimental Procedures describe recordings of rat cortical local field potentials, not human EEG, and the paper does not establish that these low-frequency dynamics support memory and neural computation. (LLM, conf=0.86)
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Cites
Sleep Drives Metabolite Clearance from the Adult Brain
Xie, L., Kang, H., Xu, Q., Chen, M. J., Liao, Y., Thiyagarajan, M., O’Donnell, J., Christensen, D. J., Nicholson, C., Iliff, J. J., et al. (2013) · Science · doi:10.1126/science.1241224 · Cited by 5,411
Bienenstock, E., Cooper, L., & Munro, P. (1982) · The Journal of Neuroscience · doi:10.1523/jneurosci.02-01-00032.1982 · Cited by 2,896
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · cited 8×
“, 2012), which is of particular interest when combined with findings that REM and nonREM sleep may contribute to different types of memory (Grosmark and Buzsáki, 2016; Rasch and Born, 2013) and that alterations of REM sleep can affect cognitive and affective disorders (Gierz et al.”
BackgroundInfluentialTononi, G., & Cirelli, C. (2014) · Neuron · doi:10.1016/j.neuron.2013.12.025 · Cited by 2,356
Activity-dependent scaling of quantal amplitude in neocortical neurons
Turrigiano, G. G., Leslie, K. R., Desai, N. S., Rutherford, L. C., & Nelson, S. B. (1998) · Nature · doi:10.1038/36103 · Cited by 2,226
Synaptic scaling mediated by glial TNF-α
Stellwagen, D., & Malenka, R. C. (2006) · Nature · doi:10.1038/nature04671 · Cited by 1,715
Dijk, D., & Czeisler, C. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-05-03526.1995 · Cited by 1,356
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
Vyazovskiy, V. V., Riedner, B. A., Cirelli, C., & Tononi, G. (2007) · SLEEP · doi:10.1093/sleep/30.12.1631 · Cited by 225
Kim, J., & Tsien, R. W. (2008) · Neuron · doi:10.1016/j.neuron.2008.05.009 · Cited by 124 · cited 1×
“However, uniform synaptic scaling may produce instability in recurrent circuits (Blanco et al., 2015; Buonomano, 2005; Kim and Tsien, 2008; Mitra et al., 2012).”
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Flagged first, then by citations
Research works printed but not linked: 61
- Avramescu, 2008, Synaptic strength modulation after cortical trauma: a role in epileptogenesis, J. Neurosci., 28, 6760, 10.1523/JNEUROSCI.0643-08.2008 · DOI
- Axmacher, 2006, Memory formation by neuronal synchronization, Brain Res. Brain Res. Rev., 52, 170, 10.1016/j.brainresrev.2006.01.007 · DOI
- Bergmann, 1987, NREM sleep with low-voltage EEG in the rat, Sleep, 10, 1, 10.1093/sleep/10.1.1 · DOI
- Besedovsky, 2012, Sleep and immune function, Pflugers Arch., 463, 121, 10.1007/s00424-011-1044-0 · DOI · Paper page
- Blanco, 2015, Synaptic homeostasis and restructuring across the sleep-wake cycle, PLoS Comput. Biol., 11, e1004241, 10.1371/journal.pcbi.1004241 · DOI
- Borbély, 1982, A two process model of sleep regulation, Hum. Neurobiol., 1, 195
- Brailowsky, 1990, Electroencephalographic study of the GABA-withdrawal syndrome in rats, Epilepsia, 31, 369, 10.1111/j.1528-1157.1990.tb05490.x · DOI
- Buonomano, 2005, A learning rule for the emergence of stable dynamics and timing in recurrent networks, J. Neurophysiol., 94, 2275, 10.1152/jn.01250.2004 · DOI
- Buzsáki, 2015, Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning, Hippocampus, 25, 1073, 10.1002/hipo.22488 · DOI · Paper page
- Buzsáki, 2014, The log-dynamic brain: how skewed distributions affect network operations, Nat. Rev. Neurosci., 15, 264, 10.1038/nrn3687 · DOI
- Buzsáki, 1988, Electric activity in the neocortex of freely moving young and aged rats, Neuroscience, 26, 735, 10.1016/0306-4522(88)90095-4 · DOI
- Buzsáki, 2002, Homeostatic maintenance of neuronal excitability by burst discharges in vivo, Cereb. Cortex, 12, 893, 10.1093/cercor/12.9.893 · DOI
- Calvet, 1973, Electrical activity in neocortical projection and association areas during slow wave sleep, Brain Res., 52, 173, 10.1016/0006-8993(73)90657-4 · DOI
- Campbell, 1993, Dissociation of delta EEG amplitude and incidence in rat NREM sleep, Brain Res. Bull., 30, 143, 10.1016/0361-9230(93)90050-L · DOI
- Cohen, 2016, Excitation-transcription coupling in parvalbumin-positive interneurons employs a novel CaM Kinase-dependent pathway distinct from excitatory neurons, Neuron, 10.1016/j.neuron.2016.03.001 · DOI · Paper page
- Connors, 1990, Intrinsic firing patterns of diverse neocortical neurons, Trends Neurosci., 13, 99, 10.1016/0166-2236(90)90185-D · DOI
- Delgado, 2010, Pyramidal neuron conductance state gates spike-timing-dependent plasticity, J. Neurosci., 30, 15713, 10.1523/JNEUROSCI.3068-10.2010 · DOI
- Douglas, 1996, Arousals and the sleep apnea/hypopnea syndrome, Sleep, 19, S196
- Feinberg, 1974, Changes in sleep cycle patterns with age, J. Psychiatr. Res., 10, 283, 10.1016/0022-3956(74)90011-9 · DOI
- Gervasoni, 2004, Global forebrain dynamics predict rat behavioral states and their transitions, J. Neurosci., 24, 11137, 10.1523/JNEUROSCI.3524-04.2004 · DOI
- Gierz, 1987, Sleep disturbances in various nonaffective psychiatric disorders, Psychiatr. Clin. North Am., 10, 565, 10.1016/S0193-953X(18)30534-3 · DOI
- Grosmark, 2016, Diversity in neural firing dynamics supports both rigid and learned hippocampal sequences, Science, 351, 1440, 10.1126/science.aad1935 · DOI · Paper page
- Grosmark, 2012, REM sleep reorganizes hippocampal excitability, Neuron, 75, 1001, 10.1016/j.neuron.2012.08.015 · DOI · Paper page
- Halász, 1979, Micro-arousals during nocturnal sleep, Acta Physiol. Acad. Sci. Hung., 54, 1
- Ibata, 2008, Rapid synaptic scaling induced by changes in postsynaptic firing, Neuron, 57, 819, 10.1016/j.neuron.2008.02.031 · DOI · Paper page
- Inostroza, 2013, Sleep for preserving and transforming episodic memory, Annu. Rev. Neurosci., 36, 79, 10.1146/annurev-neuro-062012-170429 · DOI
- Lim, 2015, Inferring learning rules from distributions of firing rates in cortical neurons, Nat. Neurosci., 18, 1804, 10.1038/nn.4158 · DOI
- Luczak, 2007, Sequential structure of neocortical spontaneous activity in vivo, Proc. Natl. Acad. Sci. USA, 104, 347, 10.1073/pnas.0605643104 · DOI · Paper page
- Luczak, 2015, Packet-based communication in the cortex, Nat. Rev. Neurosci., 16, 745, 10.1038/nrn4026 · DOI
- Margolis, 2012, Reorganization of cortical population activity imaged throughout long-term sensory deprivation, Nat. Neurosci., 15, 1539, 10.1038/nn.3240 · DOI · Paper page
- Markram, 1997, Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs, Science, 275, 213, 10.1126/science.275.5297.213 · DOI · Paper page
- McCarley, 2007, Neurobiology of REM and NREM sleep, Sleep Med., 8, 302, 10.1016/j.sleep.2007.03.005 · DOI
- Miller, 1996, Synaptic economics: competition and cooperation in synaptic plasticity, Neuron, 17, 371, 10.1016/S0896-6273(00)80169-5 · DOI
- Mitra, 2012, Heterogeneous reallocation of presynaptic efficacy in recurrent excitatory circuits adapting to inactivity, Nat. Neurosci., 15, 250, 10.1038/nn.3004 · DOI
- Miyawaki, 2016, Regulation of hippocampal firing by network oscillations during sleep, Curr. Biol., 26, 893, 10.1016/j.cub.2016.02.024 · DOI
- Mizuseki, 2013, Preconfigured, skewed distribution of firing rates in the hippocampus and entorhinal cortex, Cell Rep., 4, 1010, 10.1016/j.celrep.2013.07.039 · DOI
- Panas, 2015, Sloppiness in spontaneously active neuronal networks, J. Neurosci., 35, 8480, 10.1523/JNEUROSCI.4421-14.2015 · DOI
- Peyrache, 2010, Sequential reinstatement of neocortical activity during slow oscillations depends on cells’ global activity, Front. Syst. Neurosci., 3, 18, 10.3389/neuro.06.018.2009 · DOI
- Pickenhain, 1967, Hippocampal slow wave activity as a correlate of basic behavioral mechanisms in the rat, Prog. Brain Res., 27, 218, 10.1016/S0079-6123(08)63101-5 · DOI
- Rabinowitch, 2008, Two opposing plasticity mechanisms pulling a single synapse, Trends Neurosci., 31, 377, 10.1016/j.tins.2008.05.005 · DOI
- Rossant, 2016, Spike sorting for large, dense electrode arrays, Nat. Neurosci, 19, 634, 10.1038/nn.4268 · DOI
- Rutherford, 1998, BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses, Neuron, 21, 521, 10.1016/S0896-6273(00)80563-2 · DOI · Paper page
- Schieber, 1971, [Phases of spontaneous transitory activation during normal sleep in humans], Arch. Sci. Physiol. (Paris), 25, 443
- Schmitzer-Torbert, 2005, Quantitative measures of cluster quality for use in extracellular recordings, Neuroscience, 131, 1, 10.1016/j.neuroscience.2004.09.066 · DOI
- Sejnowski, 2000, Why do we sleep?, Brain Res., 886, 208, 10.1016/S0006-8993(00)03007-9 · DOI · Paper page
- Shoham, 2006, How silent is the brain: is there a “dark matter” problem in neuroscience?, J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol., 192, 777, 10.1007/s00359-006-0117-6 · DOI
- Siccoli, 2008, Correlation between sleep and cognitive functions after hemispheric ischaemic stroke, Eur. J. Neurol., 15, 565, 10.1111/j.1468-1331.2008.02119.x · DOI
- Stepanski, 1984, Sleep fragmentation and daytime sleepiness, Sleep, 7, 18, 10.1093/sleep/7.1.18 · DOI
- Steriade, 2006, Grouping of brain rhythms in corticothalamic systems, Neuroscience, 137, 1087, 10.1016/j.neuroscience.2005.10.029 · DOI · Paper page
- Steriade, 1993, Thalamocortical oscillations in the sleeping and aroused brain, Science, 262, 679, 10.1126/science.8235588 · DOI · Paper page
- Steriade, 2001, Natural waking and sleep states: a view from inside neocortical neurons, J. Neurophysiol., 85, 1969, 10.1152/jn.2001.85.5.1969 · DOI · Paper page
- Stickgold, 2000, Visual discrimination task improvement: A multi-step process occurring during sleep, J. Cogn. Neurosci., 12, 246, 10.1162/089892900562075 · DOI · Paper page
- Thiagarajan, 2005, Adaptation to synaptic inactivity in hippocampal neurons, Neuron, 47, 725, 10.1016/j.neuron.2005.06.037 · DOI
- Tononi, 2003, Sleep and synaptic homeostasis: a hypothesis, Brain Res. Bull., 62, 143, 10.1016/j.brainresbull.2003.09.004 · DOI · Paper page
- Trachsel, 1988, Electroencephalogram analysis of non-rapid eye movement sleep in rats, Am. J. Physiol., 255, R27
- Turrigiano, 2004, Homeostatic plasticity in the developing nervous system, Nat. Rev. Neurosci., 5, 97, 10.1038/nrn1327 · DOI · Paper page
- Vandecasteele, 2012, Large-scale recording of neurons by movable silicon probes in behaving rodents, J. Vis. Exp., e3568
- Vyazovskiy, 2013, Sleep and the single neuron: the role of global slow oscillations in individual cell rest, Nat. Rev. Neurosci., 14, 443, 10.1038/nrn3494 · DOI · Paper page
- Vyazovskiy, 2009, Cortical firing and sleep homeostasis, Neuron, 63, 865, 10.1016/j.neuron.2009.08.024 · DOI · Paper page
- Walker, 2010, Sleep, memory and emotion, Prog. Brain Res., 185, 49, 10.1016/B978-0-444-53702-7.00004-X · DOI
- Wilson, 1981, Spontaneous firing patterns of identified spiny neurons in the rat neostriatum, Brain Res., 220, 67, 10.1016/0006-8993(81)90211-0 · DOI
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Metadata
- Authors
- Watson, B. O., Levenstein, D., Greene, J. P., Gelinas, J. N., & Buzsáki, G.
- Affiliations
- Weill Cornell Medicine (US)
- New York University (US)
- Corresponding author
- Buzsáki, György
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2016-05
- Volume
- 90
- Issue
- 4
- Pages
- 839-852
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC4873379
- OpenAlex
- W2343813323
- Cited by
- 375
- References
- 10
- Citations by year
- 2026: 48 · 2025: 37 · 2024: 38 · 2023: 31 · 2022: 31 · 2021: 34 · 2020: 36 · 2019: 59 · 2018: 27 · 2017: 28 · 2016: 6
- FWCI
- 19.79
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH054671, R01MH107396, K08MH107662)
- National Institute of Neurological Disorders and Stroke (U01NS090583, U01NS090526)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (K12HD000850)
- 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 homeostasis, frontal cortex, pyramidal neurons, neuronal firing rate, NREM sleep, REM sleep, microarousals, network excitability, synaptic homeostasis
- MeSH terms
- Action Potentials, Animals, Homeostasis, Male, Synaptic Transmission, Neurons, Sleep, Wakefulness, Neocortex, Rats, Long-Evans
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