Acetylcholine systems and rhythmic activities during the waking—sleep cycle
Abstract
The two processes of activation in thalamocortical systems exerted by mesopontine cholinergic neurons are (a) a direct depolarization associated with increased input resistance of thalamic relay neurons, which is antagonized by muscarinic blockers, and (b) a disinhibition of the same neurons via hyperpolarization of inhibitory thalamic reticular neurons. Low-frequency (< 15 Hz) oscillations during slow-wave sleep, characterized by rhythmic and prolonged hyperpolarizations, are suppressed by brainstem cholinergic neurons and nucleus basalis cholinergic and GABAergic neurons projecting to thalamic reticular neurons. Fast rhythms (20-60 Hz) appear during the sustained depolarization of thalamic and neocortical neurons during brain-active states that are accompanied by increased release of acetylcholine (ACh) in the thalamus and cerebral cortex. Such fast rhythms also occur during the depolarizing phases of the slow oscillation (0.5-1 Hz) in non-REM sleep. Intracellular recordings of neocortical neurons during natural states of waking and sleep demonstrate stable and increased input resistance of corticocortical and corticothalamic neurons during the sustained depolarization in wakefulness, compared to the depolarizing phase of the slow oscillation in non-REM sleep. Despite the highly increased synaptic inputs along different afferent systems that open many conductances of cortical neurons during wakefulness, the increased input resistance is attributed to the effect of acetylcholine on cortical neurons.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Cholinergic signaling can alter thermoregulation, sleep patterns, food intake and endocrine functions such as pancreatic release of insulin and glucagon.
“Cholinergic signaling can alter thermoregulation (Myers and Waller, 1973), sleep patterns (Steriade, 2004), food intake (Grunberg et al., 1988; Mineur et al., 2011) and endocrine functions such as pancreatic release of insulin and glucagon (Ishikawa et al., 1982).”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Steriade, 2004
Cites
Thalamocortical oscillations in the sleeping and aroused brain
Steriade, M., McCormick, D. A., & Sejnowski, T. J. (1993) · Science · doi:10.1126/science.8235588 · Cited by 3,564 · see citing works
Self-citationSteriade, M., Nunez, A., & Amzica, F. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-08-03252.1993 · Cited by 1,903 · see citing works
Self-citationNatural waking and sleep states: a view from inside neocortical neurons
Steriade, M., Timofeev, I., & Grenier, F. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.5.1969 · Cited by 1,296 · see citing works
Self-citationMcCormick, D. A., & Pape, H. (1990) · The Journal of Physiology · doi:10.1113/jphysiol.1990.sp018331 · Cited by 1,140 · see citing works
McCormick, D. A. (1992) · Progress in Neurobiology · doi:10.1016/0301-0082(92)90012-4 · Cited by 1,117 · see citing works
Principles and practice of sleep medicine
Mazzoti, G. (2001) · Depression and Anxiety · doi:10.1002/da.1030 · Cited by 1,039 · see citing works
Steriade, M., Nunez, A., & Amzica, F. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-08-03266.1993 · Cited by 894 · see citing works
Self-citationSteriade, M., Datta, S., Paré, D., Oakson, G., & Dossi, R. C. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-08-02541.1990 · Cited by 775 · see citing works
Self-citationSteriade, M., Contreras, D., Dossi, R. C., & Núñez, Á. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-08-03284.1993 · Cited by 723 · see citing works
Self-citationOrigin of Slow Cortical Oscillations in Deafferented Cortical Slabs
Timofeev, I. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.12.1185 · Cited by 710 · see citing works
The mechanism of excitation by acetylcholine in the cerebral cortex
Krnjević, K., Pumain, R., & Renaud, L. P. (1971) · The Journal of Physiology · doi:10.1113/jphysiol.1971.sp009467 · Cited by 708 · see citing works
Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships
Contreras, D., & Steriade, M. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00604.1995 · Cited by 700 · see citing works
Self-citationSynchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation
Steriade, M., Amzica, F., & Contreras, D. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-01-00392.1996 · Cited by 646 · see citing works
Self-citationThe deafferented reticular thalamic nucleus generates spindle rhythmicity
Steriade, M., Domich, L., Oakson, G., & Deschenes, M. (1987) · Journal of Neurophysiology · doi:10.1152/jn.1987.57.1.260 · Cited by 640 · see citing works
Self-citationSteriade, M., Contreras, D., & Nuiiez, A. (1993) · Cited by 584 · see citing works
Self-citationLow-frequency (<1Hz) oscillations in the human sleep electroencephalogram
Achermann, P., & Borbély, A. A. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00186-3 · Cited by 577 · see citing works
Metherate, R., Cox, C. L., & Ashe, J. H. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-12-04701.1992 · Cited by 575 · see citing works
Llinás, R. R., Grace, A. A., & Yarom, Y. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.3.897 · Cited by 541 · see citing works
Impact of Network Activities on Neuronal Properties in Corticothalamic Systems
Steriade, M. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.1.1 · Cited by 530 · see citing works
Self-citationCorticothalamic activation modulates thalamic firing through glutamate "metabotropic" receptors.
McCormick, D. A., & von Krosigk, M. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.7.2774 · Cited by 500 · see citing works
Steriade, M., Dossi, R. C., & Nunez, A. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-10-03200.1991 · Cited by 480 · see citing works
Self-citationSteriade, M., Dossi, R. C., Paré, D., & Oakson, G. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.10.4396 · Cited by 455 · see citing works
Self-citationTimofeev, I., Grenier, F., & Steriade, M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.4.1924 · Cited by 455 · see citing works
Self-citationParé, D., Shink, É., Gaudreau, H., Alain Destexhe, A., & Lang, E. J. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.3.1450 · Cited by 453 · see citing works
Acetylcholine released from cerebral cortex in relation to state of activation
Celesia, G. G., & Jasper, H. H. (1966) · Neurology · doi:10.1212/wnl.16.11.1053 · Cited by 429 · see citing works
Diffuse transmission by acetylcholine in the CNS
Descarries, L., Gisiger, V., & Steriade, M. (1997) · Progress in Neurobiology · doi:10.1016/s0301-0082(97)00050-6 · Cited by 406 · see citing works
Self-citationSteriade, M., Contreras, D., Amzica, F., & Timofeev, I. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-08-02788.1996 · Cited by 404 · see citing works
Self-citationContreras, D., Timofeev, I., & Steriade, M. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021488 · Cited by 374 · see citing works
Self-citationLow-frequency rhythms in the thalamus of intact-cortex and decorticated cats
Timofeev, I., & Steriade, M. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.6.4152 · Cited by 353 · see citing works
Self-citationBasic Mechanisms of Sleep-Wake States
Jones, B. E. (2005) · Elsevier eBooks · doi:10.1016/b0-72-160797-7/50018-5 · Cited by 352 · see citing works
Gutfreund, Y., Yarom, Y., & Segev, I. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp020611 · Cited by 340 · see citing works
The K-complex: Its slow (<1-Hz) rhythmicity and relation to delta waves
Amzica, F., & Steriade, M. (1997) · Neurology · doi:10.1212/wnl.49.4.952 · Cited by 329 · see citing works
Self-citationSteriade, M., Amzica, F., & Nunez, A. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.4.1385 · Cited by 302 · see citing works
Self-citationSynchronized sleep oscillations and their paroxysmal developments
Steriade, M., Contreras, D., & Amzica, F. (1994) · Trends in Neurosciences · doi:10.1016/0166-2236(94)90105-8 · Cited by 301 · see citing works
Self-citationLow‐frequency oscillatory activities intrinsic to rat and cat thalamocortical cells.
Leresche, N., Lightowler, S., Soltész, I., Jassik-Gerschenfeld, D., & Crunelli, V. (1991) · The Journal of Physiology · doi:10.1113/jphysiol.1991.sp018744 · Cited by 283 · see citing works
Leonard, C. S., & Llinas, R. H. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90599-1 · Cited by 264 · see citing works
Acetylcholine acts on m2‐muscarinic receptors to excite rat locus coeruleus neurones
Egan, T. M., & North, R. A. (1985) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1985.tb11070.x · Cited by 263 · see citing works
Lavoie, B. A., & Parent, A. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903440203 · Cited by 258 · see citing works
Semba, K. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00254-0 · Cited by 250 · see citing works
Steriade, M., Dossi, R. C., & Contreras, D. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90556-u · Cited by 241 · see citing works
Self-citationUmbriaco, D., Watkins, K. C., Descarries, L., Cozzari, C., & Hartman, B. K. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903480304 · Cited by 237 · see citing works
Luebke, J. I., Greene, R. W., Semba, K., Kamondi, A., McCarley, R. W., & Reiner, P. B. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.2.743 · Cited by 226 · see citing works
Nitric oxide controls oscillatory activity in thalamocortical neurons
Pape, H., & Mager, R. (1992) · Neuron · doi:10.1016/0896-6273(92)90182-d · Cited by 223 · see citing works
Intracortical and corticothalamic coherency of fast spontaneous oscillations.
Steriade, M., & Amzica, F. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.6.2533 · Cited by 221 · see citing works
Self-citationSteriade, M., Parent, A., Paré, D., & Smith, Y. (1987) · Brain Research · doi:10.1016/0006-8993(87)90408-2 · Cited by 194 · see citing works
Self-citationSteriade, M., Oakson, G., & Ropert, N. (1982) · Experimental Brain Research · doi:10.1007/bf00238096 · Cited by 185 · see citing works
Self-citationDossi, R. C., Paré, D., & Steriade, M. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.65.3.393 · Cited by 184 · see citing works
Self-citationCape, E. G., & Jones, B. E. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-07-02653.1998 · Cited by 176 · see citing works
Parent, A., Paré, D., Smith, Y., & Steriade, M. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902770209 · Cited by 175 · see citing works
Self-citationMetherate, R., & Ashe, J. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-12-05312.1993 · Cited by 166 · see citing works
Steriade, M., Deschênes, M., & Oakson, G. (1974) · Journal of Neurophysiology · doi:10.1152/jn.1974.37.5.1065 · Cited by 161 · see citing works
Self-citationMassimini, M., & Amzica, F. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.3.1346 · Cited by 160 · see citing works
Rasmusson, D. D., Clow, K. A., & Szerb, J. C. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90495-2 · Cited by 156 · see citing works
Noradrenaline hyperpolarizes identified rat mesopontine cholinergic neurons in vitro
Williams, J., & Reiner, P. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03878.1993 · Cited by 154 · see citing works
Steriade, M. (2001) · The MIT Press eBooks · doi:10.7551/mitpress/3822.001.0001 · Cited by 149 · see citing works
Self-citationVoltage-dependent 40-Hz oscillations in rat reticular thalamic neurons in vivo
Pinault, D., & Deschênes, M. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90312-p · Cited by 149 · see citing works
Hu, B., Steriade, M., & Deschênes, M. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90026-2 · Cited by 136 · see citing works
Self-citationVoltage-dependent fast (20–40 Hz) oscillations in long-axoned neocortical neurons
Núñez, Á., Amzica, F., & Steriade, M. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90464-d · Cited by 124 · see citing works
Self-citationAlertness, Quiet Sleep, Dreaming
Steriade, M. (1991) · Cerebral cortex · doi:10.1007/978-1-4615-6622-9_8 · Cited by 106 · see citing works
Self-citationHobson, J. A. (1975) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(75)90141-8 · Cited by 101 · see citing works
PRINCIPLES AND PRACTICE OF SLEEP MEDICINE
Jones, M. C. (1990) · CHEST Journal · doi:10.1016/s0012-3692(16)32068-2 · Cited by 90 · see citing works
Simon, N. R., Manshanden, I., & da Silva, F. H. L. (2000) · Brain Research · doi:10.1016/s0006-8993(00)01974-0 · Cited by 73 · see citing works
Petre-Quadens, O., & Schlag, J. D. (1974) · Medical Entomology and Zoology · Cited by 65 · see citing works
Rasmusson, D. D., Szerb, J. C., & Jordan, J. L. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00523-4 · Cited by 55 · see citing works
Modulation of cholinergic nucleus basalis neurons by acetylcholine and N-methyl-d-aspartate
Khateb, A., Fort, P., Williams, S., Serafin, M., Jones, B. E., & Mühlethaler, M. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00167-x · Cited by 55 · see citing works
Bremer, F., Stoupel, N., & Reeth, P. C. V. (1960) · ARCHIVES ITALIENNES DE BIOLOGIE · doi:10.4449/aib.v98i3.1732 · Cited by 40 · see citing works
Pape, H. (1995) · Seminars in Neuroscience · doi:10.1006/smns.1995.0036 · Cited by 30 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Breakdown of cortical effective connectivity during sleep
Massimini, M., Ferrarelli, F., Huber, R., Esser, S. K., Singh, H., & Tononi, G. (2005) · Science · doi:10.1126/science.1117256 · Cited by 1,534 · see citing works
Rethinking the Emotional Brain
LeDoux, J. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.004 · Cited by 1,594 · see citing works
“…of chemically specific neurons that underlie sleep-wake cycles and the degree of arousal, attention, and vigilance while awake (Jouvet, 1969, 1999; Steriade, 1995, 2004; Jacobs et al., 1990; Jones, 2003; Aston-Jones, 2005; Monti and Jantos, 2008; Sarter et al., 2005; Arnsten and Li, 2005;…”
Control 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
Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior
Picciotto, M. R., Higley, M. J., & Mineur, Y. S. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.036 · Cited by 1,404 · see citing works
Tuning arousal with optogenetic modulation of locus coeruleus neurons
Carter, M. E., Yizhar, O., Chikahisa, S., Nguyen, H., Adamantidis, A., Nishino, S., Deisseroth, K., & de Lecea, L. (2010) · Nature Neuroscience · doi:10.1038/nn.2682 · Cited by 993 · see citing works
Removing brakes on adult brain plasticity: From molecular to behavioral interventions
Bavelier, D., Levi, D. M., Li, R. W., Dan, Y., & Hensch, T. K. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4812-10.2010 · Cited by 589 · see citing works
Triggering sleep slow waves by transcranial magnetic stimulation
Massimini, M., Ferrarelli, F., Esser, S. K., Riedner, B. A., Huber, R., Murphy, M., Peterson, M. J., & Tononi, G. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702495104 · Cited by 489 · see citing works
REM sleep reorganizes hippocampal excitability
Grosmark, A. D., Mizuseki, K., Pastalkova, E., Diba, K., & Buzsáki, G. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.015 · Cited by 344 · see citing works
Cortical reactivity and effective connectivity during REM sleep in humans
Massimini, M., Ferrarelli, F., Murphy, M. J., Huber, R., Riedner, B. A., Casarotto, S., & Tononi, G. (2010) · Cognitive Neuroscience · doi:10.1080/17588921003731578 · Cited by 202 · see citing works
Nicotinic acetylcholine receptor β2 subunits in the medial prefrontal cortex control attention
Guillem, K., Bloem, B., Poorthuis, R. B., Loos, M., Smit, A. B., Maskos, U., Spijker, S., & Mansvelder, H. D. (2011) · Science · doi:10.1126/science.1207079 · Cited by 191 · see citing works
Nicotinic control of axon excitability regulates thalamocortical transmission
Kawai, H., Lazar, R., & Metherate, R. (2007) · Nature Neuroscience · doi:10.1038/nn1956 · Cited by 171 · see citing works
Selective activation of cholinergic basal forebrain neurons induces immediate sleep-wake transitions
Han, Y., Shi, Y.-F., Xi, W., Zhou, R., Tan, Z.-B., Wang, H., Li, X.-M., Chen, Z., Feng, G., Luo, M., et al. (2014) · Current Biology · doi:10.1016/j.cub.2014.02.011 · Cited by 137 · see citing works
Maskos, U. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.5 · Cited by 139 · see citing works
Ruggiero, R. N., Rossignoli, M. T., Marques, D. B., de Sousa, B. M., Romcy-Pereira, R. N., Lopes-Aguiar, C., & Leite, J. P. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.732360 · Cited by 111 · see citing works
Spoormaker, V. I., Gleiser, P. M., & Czisch, M. (2012) · Frontiers in Neurology · doi:10.3389/fneur.2012.00080 · Cited by 83 · see citing works
Childhood parasomnia – A disorder of sleep maturation?
Nevsimalova, S., Prihodova, I., Kemlink, D., & Skibova, J. (2013) · European Journal of Paediatric Neurology · doi:10.1016/j.ejpn.2013.05.004 · Cited by 31 · see citing works
Siclari, F., & Tononi, G. (2016) · The Neurology of Conciousness · doi:10.1016/b978-0-12-800948-2.00007-8 · Cited by 27 · see citing works
Tononi, G. (2009) · The Neurology of Consciousness · doi:10.1016/b978-0-12-374168-4.00008-3 · Cited by 16 · see citing works
- Authors
- Steriade, M.
- Affiliations
- Université Laval (CA)
- Corresponding author
- Steriade, Mircea
- Venue
- Progress in brain research
- Publisher
- Elsevier
- Published
- 2004
- Volume
- 145
- Pages
- 179-196
- ISSN
- 0079-6123 (ISSN-L)
- OpenAlex
- W1599216135
- Cited by
- 227
- References
- 67
- Citations by year
- 2026: 8 · 2025: 9 · 2024: 6 · 2023: 7 · 2022: 4 · 2021: 7 · 2020: 6 · 2019: 6 · 2018: 13 · 2017: 15 · 2016: 4 · 2015: 20 · 2014: 9 · 2013: 12 · 2012: 14
- FWCI
- 17.30
- Type
- book chapter
- Language
- en
- Open access
- closed
- Locations
- Progress in brain research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (1-R01 NS40522-01, R01NS040522)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- acetylcholine, thalamocortical system, thalamocortical neurons, thalamic reticular neurons, slow-wave sleep, fast oscillations, NREM sleep, slow oscillations, input resistance, cortical neurons, nucleus basalis of Meynert, GABAergic neurons, cholinergic modulation
- MeSH terms
- Acetylcholine, Animals, Brain, Cholinergic Fibers, Humans, Periodicity, Sleep Stages, Wakefulness
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
