Learning-Dependent, Transient Increase of Activity in Noradrenergic Neurons of Locus Coeruleus during Slow Wave Sleep in the Rat: Brain Stem–Cortex Interplay for Memory Consolidation?
Abstract
Memory consolidation during sleep is regaining attention due to a wave of recent reports of memory improvements after sleep or deficits after sleep disturbance. Neuromodulators have been proposed as possible players in this putative off-line memory processing, without much experimental evidence. We recorded neuronal activity in the rat noradrenergic nucleus locus coeruleus (LC) using chronically implanted movable microelectrodes while monitoring the behavioral state via electrocorticogram and online video recording. Extracellular recordings of physiologically identified noradrenergic neurons of LC were made in freely behaving rats for 3 h before and after olfactory discrimination learning. On subsequent days, if LC recording remained stable, additional learning sessions were made within the olfactory discrimination protocol, including extinction, reversals, learning new odors. Contrary to the long-standing dogma about the quiescence of noradrenergic neurons of LC, we found a transient increase in LC activity in trained rats during slow wave sleep (SWS) 2 h after learning. The discovery of learning-dependent engagement of LC neurons during SWS encourages exploration of brain stem-cortical interaction during this delayed phase of memory consolidation and should bring new insights into mechanisms underlying memory formation.
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?
A specific sleep-related window of increased LC burst activity about 120 min after learning of odor-reward associations has been identified in rats.
“Moreover, a specific sleep-related window of increased LC burst activity ϳ120 min after learning of odor-reward associations has been identified in rats (356).”
From About Sleep's Role in Memory (2013) · cites this paper as [356]
Cites
Reactivation of hippocampal ensemble memories during sleep
Wilson, M. A., & McNaughton, B. L. (1994) · Science · doi:10.1126/science.8036517 · Cited by 3,118 · see citing works
Aston-Jones, G., & Bloom, F. (1981) · The Journal of Neuroscience · doi:10.1523/jneurosci.01-08-00876.1981 · Cited by 1,960 · see citing works
Sleep-dependent memory consolidation
Stickgold, R. (2005) · Nature · doi:10.1038/nature04286 · Cited by 1,857 · 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
Sleep Cycle Oscillation: Reciprocal Discharge by Two Brainstem Neuronal Groups
Hobson, J. A., McCarley, R. W., & Wyzinski, P. (1975) · Science · doi:10.1126/science.1094539 · Cited by 1,238 · see citing works
Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience
Skaggs, W. E., & McNaughton, B. L. (1996) · Science · doi:10.1126/science.271.5257.1870 · Cited by 1,173 · see citing works
Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep
Louie, K., & Wilson, M. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00186-6 · Cited by 1,148 · see citing works
Walker, M. P., & Stickgold, R. (2006) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070307 · Cited by 1,075 · cited 2× · see citing works
“2Present address: College de France, Centre National de la Recherche Scientifique, UMR 7152, F-75005, Paris, France.”
BackgroundGennaro, L. D., & Ferrara, M. (2003) · Sleep Medicine Reviews · doi:10.1053/smrv.2002.0252 · Cited by 925 · see citing works
Retrieval and reconsolidation: Toward a neurobiology of remembering
Sara, S. J. (2000) · Learning & Memory · doi:10.1101/lm.7.2.73 · Cited by 919 · see citing works
Self-citationFoote, S. L., Aston-Jones, G., & Bloom, F. E. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.5.3033 · Cited by 857 · see citing works
Network reset: a simplified overarching theory of locus coeruleus noradrenaline function
Bouret, S., & Sara, S. J. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.09.002 · Cited by 806 · see citing works
Self-citationPavlides, C., & Winson, J. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-08-02907.1989 · Cited by 684 · see citing works
Declarative memory consolidation: mechanisms acting during human sleep
Gais, S., & Born, J. (2004) · Learning & Memory · doi:10.1101/lm.80504 · Cited by 536 · see citing works
Bernabeu, R., Bevilaqua, L. R., Ardenghi, P. G., Bromberg, E., Schmitz, P. K., Bianchin, M. M., Izquierdo, I., & Medina, J. H. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.13.7041 · Cited by 499 · see citing works
Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation
Gais, S., & Born, J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0305404101 · Cited by 412 · see citing works
Bouret, S., & Sara, S. J. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03526.x · Cited by 371 · see citing works
Self-citationLatest Homo erectus of Java: Potential Contemporaneity with Homo sapiens in Southeast Asia
Swisher, C. C., Rink, W. J., Antón, S. C., Schwarcz, H. P., Curtis, G. H., Suprijo, A., & Widiasmoro (1996) · Science · doi:10.1126/science.274.5294.1870 · Cited by 323 · see citing works
Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles
Qin, Y., McNaughton, B. L., Skaggs, W. E., & Barnes, C. A. (1997) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1997.0139 · Cited by 308 · see citing works
Maloney, K. J., Mainville, L., & Jones, B. E. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-08-03057.1999 · Cited by 284 · see citing works
Pennartz, C. M. A., Lee, E., Verheul, J., Lipa, P., Barnes, C. A., & McNaughton, B. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0575-04.2004 · Cited by 282 · see citing works
Elevated Sleep Spindle Density after Learning or after Retrieval in Rats
Eschenko, O., Mölle, M., Jan Born, A., & Sara, S. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3175-06.2006 · Cited by 257 · see citing works
Self-citationSara, S. J., & Segal, M. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)63835-2 · Cited by 223 · see citing works
Self-citationGervasoni, D., Darracq, L., Fort, P., Soulière, F., Chouvet, G., & Luppi, P. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00106.x · Cited by 205 · see citing works
Bernabeu, R. (1997) · Medical Entomology and Zoology · Cited by 188 · see citing works
Sleep, dreams, and memory consolidation: the role of the stress hormone cortisol
Payne, J. D., & Nadel, L. (2004) · Learning & Memory · doi:10.1101/lm.77104 · Cited by 184 · see citing works
Tronel, S., & Sara, S. J. (2002) · Learning & Memory · doi:10.1101/lm.47802 · Cited by 147 · see citing works
Self-citationStrengthening the shaky trace through retrieval
Sara, S. J. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044575 · Cited by 144 · see citing works
Self-citationVerret, L., Fort, P., Gervasoni, D., Léger, L., & Luppi, P. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20891 · Cited by 125 · see citing works
Jones, B. E. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)63797-8 · Cited by 114 · see citing works
Noradrenergic Action in Prefrontal Cortex in the Late Stage of Memory ConsolidationPreprint
Tronel, S., Feenstra, M. G. P., & Sara, S. J. (2004) · Learning & Memory · doi:10.1101/lm.74504 · Cited by 112 · see citing works
Self-citationLocus Ceruleus Control of State-Dependent Gene Expression
Cirelli, C. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0949-04.2004 · Cited by 103 · see citing works
Roullet, P., & Sara, S. J. (1998) · Neural Plasticity · doi:10.1155/np.1998.63 · Cited by 98 · see citing works
Self-citationRapid habituation of auditory responses of locus coeruleus cells in anaesthetized and awake rats
Hervé‐Minvielle, A., & Sara, S. J. (1995) · Neuroreport · doi:10.1097/00001756-199507100-00001 · Cited by 92 · see citing works
Self-citationThe possible role of the adrenergic systems of the cortex in learning.
Ss, K. (1972) · PubMed · Cited by 80 · see citing works
EEG Power Densities (0.5–20 Hz) in Different Sleep–Wake Stages in Rats
Bjorvatn, B., Fagerland, S., & Ursin, R. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00460-5 · Cited by 59 · see citing works
Colgin, L. L., & Moser, E. I. (2006) · Nature · doi:10.1038/440615a · Cited by 41 · see citing works
The Neurophysiology of Reminiscence
McNaughton, B. L. (1998) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3851 · Cited by 38 · see citing works
[Locus ceruleus, paradoxal sleep, and cerebral noradrenaline].
Roussel, B., Buguet, A., Bobillier, P., & Jouvet, M. (1967) · PubMed · Cited by 23 · see citing works
Changes in gene expression during the sleep-waking cycle: a new view of activating systems.
Tononi, G., Cirelli, C., & Pompeiano, M. (1995) · PubMed · Cited by 15 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Diekelmann, S., & Born, J. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2762 · Cited by 3,760 · see citing works
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
“Moreover, a specific sleep-related window of increased LC burst activity 120 min after learning of odor-reward associations has been identified in rats (356).”
BackgroundHippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning
Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759 · see citing works
Pupillometry: A Window to the Preconscious?
Laeng, B., Sirois, S., & Gredebäck, G. (2012) · Perspectives on Psychological Science · doi:10.1177/1745691611427305 · Cited by 921 · see citing works
Mather, M., Clewett, D., Sakaki, M., & Harley, C. W. (2016) · Behavioral and Brain Sciences · doi:10.1017/s0140525x15000667 · Cited by 695 · see citing works
Memory-enhancing properties of sleep depend on the oscillatory amplitude of norepinephrine
Kjaerby, C., Andersen, M., Hauglund, N., Untiet, V., Dall, C., Sigurdsson, B., Ding, F., Feng, J., Li, Y., Weikop, P., et al. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01102-9 · Cited by 306 · see citing works
Bergmann, T. O., Mölle, M., Diedrichs, J., Born, J., & Siebner, H. R. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.10.036 · Cited by 228 · see citing works
Noradrenergic circuit control of non-REM sleep substates
Osorio-Forero, A., Cardis, R., Vantomme, G., Guillaume-Gentil, A., Katsioudi, G., Devenoges, C., Fernandez, L. M. J., & Lüthi, A. (2021) · Current Biology · doi:10.1016/j.cub.2021.09.041 · Cited by 230 · see citing works
Eschenko, O., Magri, C., Panzeri, S., & Sara, S. J. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr121 · Cited by 194 · see citing works
Self-citationLocus Coeruleus in time with the making of memories
Sara, S. J. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.07.004 · Cited by 156 · see citing works
Self-citationHippocampal Sharp Wave/Ripples during Sleep for Consolidation of Associative Memory
Ramadan, W., Eschenko, O., & Sara, S. J. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006697 · Cited by 173 · see citing works
Self-citationSwift, K. M., Gross, B. A., Frazer, M. A., Bauer, D. S., Clark, K. J. D., Vazey, E. M., Aston-Jones, G., Li, Y., Pickering, A. E., Sara, S. J., et al. (2018) · Current Biology · doi:10.1016/j.cub.2018.09.054 · Cited by 158 · see citing works
Self-citationNapping and the selective consolidation of negative aspects of scenes
Payne, J. D., Kensinger, E. A., Wamsley, E. J., Spreng, R. N., Alger, S. E., Gibler, K., Schacter, D. L., & Stickgold, R. (2015) · Emotion · doi:10.1037/a0038683 · Cited by 130 · see citing works
Contribution of norepinephrine to emotional memory consolidation during sleep
Groch, S., Wilhelm, I., Diekelmann, S., Sayk, F., Gais, S., & Born, J. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.03.006 · Cited by 93 · see citing works
CA1 hippocampal network activity changes during sleep-dependent memory consolidation
Ognjanovski, N., Maruyama, D., Lashner, N., Zochowski, M., & Aton, S. J. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00061 · Cited by 81 · see citing works
The memory function of noradrenergic activity in non-REM sleep
Gais, S., Rasch, B., Dahmen, J. C., Sara, S., & Born, J. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2011.21622 · Cited by 60 · see citing works
Self-citationOff-line concomitant release of dopamine and glutamate involvement in taste memory consolidation
Guzmán‐Ramos, K., Osorio‐Gómez, D., Moreno‐Castilla, P., & Bermúdez‐Rattoni, F. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06758.x · Cited by 63 · see citing works
Memory corticalization triggered by REM sleep: mechanisms of cellular and systems consolidation
Almeida-Filho, D. G., Queiroz, C. M., & Ribeiro, S. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2886-9 · Cited by 38 · see citing works
- Authors
- Eschenko, O., & Sara, S. J.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-03-04
- Volume
- 18
- Issue
- 11
- Pages
- 2596-2603
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- OpenAlex
- W2146958231
- Cited by
- 115
- References
- 40
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 5 · 2023: 4 · 2022: 6 · 2021: 6 · 2020: 5 · 2019: 5 · 2018: 13 · 2017: 7 · 2016: 3 · 2015: 7 · 2014: 5 · 2013: 11 · 2012: 8
- FWCI
- 3.11
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cerebral Cortex (publishedVersion)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- locus coeruleus, noradrenergic neurons, slow-wave sleep, memory consolidation, olfactory discrimination learning, sleep-dependent memory processing, neuromodulation, sleep spindles
- MeSH terms
- Animals, Cerebral Cortex, Discrimination Learning, Electrodes, Implanted, Electrophysiology, Extinction, Psychological, Locus Coeruleus, Male, Memory, Neuronal Plasticity, Norepinephrine, Olfactory Pathways, Reversal Learning, Sleep, Rats, Sprague-Dawley, Rats
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