Abnormal locus coeruleus sleep activity alters sleep signatures of memory consolidation and impairs place cell stability and spatial memory
Open accessAbstract
Sleep is critical for proper memory consolidation. The locus coeruleus (LC) releases norepinephrine throughout the brain except when the LC falls silent throughout rapid eye movement (REM) sleep and prior to each non-REM (NREM) sleep spindle. We hypothesize that these transient LC silences allow the synaptic plasticity that is necessary to incorporate new information into pre-existing memory circuits. We found that spontaneous LC activity within sleep spindles triggers a decrease in spindle power. By optogenetically stimulating norepinephrine-containing LC neurons at 2 Hz during sleep, we reduced sleep spindle occurrence, as well as NREM delta power and REM theta power, without causing arousals or changing sleep amounts. Stimulating the LC during sleep following a hippocampus-dependent food location learning task interfered with consolidation of newly learned locations and reconsolidation of previous locations, disrupting next-day place cell activity. The LC stimulation-induced reduction in NREM sleep spindles, delta, and REM theta and reduced ripple-spindle coupling all correlated with decreased hippocampus-dependent performance on the task. Thus, periods of LC silence during sleep following learning are essential for normal spindle generation, delta and theta power, and consolidation of spatial memories.
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.
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
Normality Tests for Statistical Analysis: A Guide for Non-Statisticians
Ghasemi, A., & Zahediasl, S. (2012) · International Journal of Endocrinology and Metabolism · doi:10.5812/ijem.3505 · Cited by 4,368 · cited 1× · see citing works
“All data sets were first tested for normality using Shapiro-Wilk normality test as recommended [55].”
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
Berridge, C. W., & Waterhouse, B. D. (2003) · Brain Research Reviews · doi:10.1016/s0165-0173(03)00143-7 · Cited by 2,529 · 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
Self-citationThe locus coeruleus and noradrenergic modulation of cognition
Sara, S. J. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2573 · Cited by 1,848 · see citing works
Self-citationBoosting slow oscillations during sleep potentiates memory
Marshall, L., Helgadóttir, H., Mölle, M., & Born, J. (2006) · Nature · doi:10.1038/nature05278 · Cited by 1,792 · 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
Selective suppression of hippocampal ripples impairs spatial memory
Girardeau, G., Benchenane, K., Wiener, S. I., Buzsáki, G., & Zugaro, M. B. (2009) · Nature Neuroscience · doi:10.1038/nn.2384 · Cited by 1,560 · see citing works
β-Adrenergic activation and memory for emotional events
Cahill, L., Prins, B., Weber, M., & McGaugh, J. L. (1994) · Nature · doi:10.1038/371702a0 · Cited by 1,271 · see citing works
Coordinated interactions between hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep
Siapas, A. G., & Wilson, M. A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80629-7 · Cited by 1,052 · 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
Communication between neocortex and hippocampus during sleep in rodents
Sirota, A., Csicsvari, J., Buhl, D., & Buzsáki, G. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0437938100 · Cited by 930 · see citing works
Causal evidence for the role of REM sleep theta rhythm in contextual memory consolidation
Boyce, R., Glasgow, S. D., Williams, S., & Adamantidis, A. (2016) · Science · doi:10.1126/science.aad5252 · Cited by 696 · see citing works
Hippocampo-cortical coupling mediates memory consolidation during sleep
Maingret, N., Girardeau, G., Todorova, R., Goutierre, M., & Zugaro, M. (2016) · Nature Neuroscience · doi:10.1038/nn.4304 · Cited by 667 · see citing works
Kempadoo, K. A., Mosharov, E. V., Choi, S. J., Sulzer, D., & Kandel, E. R. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616515114 · Cited by 647 · see citing works
Visual Discrimination Task Improvement: A Multi-Step Process Occurring During Sleep
Stickgold, R., Whidbee, D., Schirmer, B., Patel, V., & Hobson, J. A. (2000) · Journal of Cognitive Neuroscience · doi:10.1162/089892900562075 · Cited by 560 · see citing works
Sleep, Plasticity and Memory from Molecules to Whole-Brain Networks
Abel, T. G., Havekes, R., Saletin, J., & Walker, M. P. (2013) · Current Biology · doi:10.1016/j.cub.2013.07.025 · Cited by 551 · see citing works
REM sleep selectively prunes and maintains new synapses in development and learning
Li, W., Ma, L., Yang, G., & Gan, W.-B. (2017) · Nature Neuroscience · doi:10.1038/nn.4479 · Cited by 543 · see citing works
An Information-Theoretic Approach to Deciphering the Hippocampal Code
Skaggs, W. E., McNaughton, B. L., & Gothard, K. M. (1992) · Cited by 536 · see citing works
Daytime naps, motor memory consolidation and regionally specific sleep spindles
Nishida, M., & Walker, M. P. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000341 · Cited by 531 · see citing works
Experience-dependent, asymmetric expansion of hippocampal place fields
Mehta, M. R., Barnes, C. A., & McNaughton, B. L. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.16.8918 · Cited by 528 · see citing works
Homer1a drives homeostatic scaling-down of excitatory synapses during sleep
Diering, G. H., Nirujogi, R. S., Roth, R. H., Worley, P. F., Pandey, A., & Huganir, R. L. (2017) · Science · doi:10.1126/science.aai8355 · Cited by 516 · see citing works
Experience-Dependent Asymmetric Shape of Hippocampal Receptive Fields
Mehta, M. R., Quirk, M. C., & Wilson, M. A. (2000) · Neuron · doi:10.1016/s0896-6273(00)81072-7 · Cited by 488 · see citing works
Sleep spindle activity is associated with the integration of new memories and existing knowledge
Tamminen, J., Payne, J. D., Stickgold, R., Wamsley, E. J., & Gaskell, M. G. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3028-10.2010 · Cited by 478 · see citing works
Przybyslawski, J., Roullet, P., & Sara, S. J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-15-06623.1999 · Cited by 470 · see citing works
Self-citationThompson, L. T., & Best, P. J. (1990) · Brain Research · doi:10.1016/0006-8993(90)90555-p · Cited by 370 · see citing works
Novelty acquisition is associated with induction of hippocampal long-term depression
Manahan‐Vaughan, D., & Braunewell, K. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.15.8739 · Cited by 358 · see citing works
Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep
Poe, G. R., Nitz, D. A., McNaughton, B. L., & Barnes, C. A. (2000) · Brain Research · doi:10.1016/s0006-8993(99)02310-0 · Cited by 318 · see citing works
Self-citationThe Critical Role of Sleep Spindles in Hippocampal-Dependent Memory: A Pharmacology Study
Mednick, S. C., McDevitt, E. A., Walsh, J. K., Wamsley, E. J., Paulus, M. P., Kanady, J. C., & Drummond, S. P. A. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3127-12.2013 · Cited by 318 · see citing works
Roozendaal, B., Nguyen, B. T., Power, A. E., & McGaugh, J. L. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.20.11642 · Cited by 293 · see citing works
State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep
Wierzynski, C. M., Lubenov, E. V., Gu, M., & Siapas, A. G. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.011 · Cited by 289 · see citing works
Locus coeruleus input to hippocampal CA3 drives single-trial learning of a novel context
Wagatsuma, A., Okuyama, T., Sun, C., Smith, L. M., Abe, K., & Tonegawa, S. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1714082115 · Cited by 283 · 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-citationNMDA Receptor Antagonism Blocks Experience-Dependent Expansion of Hippocampal “Place Fields”
Ekstrom, A. D., Meltzer, J., McNaughton, B. L., & Barnes, C. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00401-9 · Cited by 245 · see citing works
Noradrenergic Regulation of Synaptic Plasticity in the Hippocampal CA1 Region
Katsuki, H., Izumi, Y., & Zorumski, C. F. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.6.3013 · Cited by 244 · see citing works
Sharp wave ripples during learning stabilize the hippocampal spatial map
Roux, L., Hu, B., Eichler, R., Stark, E., & Buzsáki, G. (2017) · Nature Neuroscience · doi:10.1038/nn.4543 · Cited by 229 · see citing works
Sara, S. J., & Segal, M. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)63835-2 · Cited by 223 · see citing works
Self-citationLearning increases human electroencephalographic coherence during subsequent slow sleep oscillations
Mölle, M., Marshall, L., Gais, S., & Born, J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402820101 · Cited by 222 · see citing works
Nocturnal/daytime urine noradrenergic measures and sleep in combat-related PTSD
Mellman, T. A., Kumar, A., Kulick-Bell, R., Kumar, M., & Nolan, B. (1995) · Biological Psychiatry · doi:10.1016/0006-3223(94)00238-x · Cited by 219 · 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-citationThe Role of Slow Wave Sleep in Memory Processing.
Walker, M. P. (2009) · Journal of Clinical Sleep Medicine · doi:10.5664/jcsm.5.2s.s20 · Cited by 169 · see citing works
O'Dell, T. J., Connor, S. A., Guglietta, R., & Nguyen, P. V. (2015) · Learning & Memory · doi:10.1101/lm.031088.113 · Cited by 163 · see citing works
Long-Term Depression: A Cellular Basis for Learning?
Braunewell, K., & Manahan‐Vaughan, D. (2001) · Reviews in the Neurosciences · doi:10.1515/revneuro.2001.12.2.121 · Cited by 157 · see citing works
Kaestner, E. J., Wixted, J. T., & Mednick, S. C. (2013) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00433 · Cited by 149 · 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
Poe, G. R. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0820-16.2017 · Cited by 130 · see citing works
Self-citationGazarini, L., Stern, C. A. J., Carobrez, A. P., & Bertoglio, L. J. (2013) · Learning & Memory · doi:10.1101/lm.030007.112 · Cited by 119 · see citing works
Eschenko, O., & Sara, S. J. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn020 · Cited by 115 · see citing works
Self-citationBrain aminergic axons exhibit marked variability in conduction velocity
Aston‐Jones, G., Segal, M., & Bloom, F. E. (1980) · Brain Research · doi:10.1016/0006-8993(80)90880-x · Cited by 110 · see citing works
Self-citationDetection of seven sleep-waking stages in the rat
Gottesmann, C. (1992) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80048-x · Cited by 110 · see citing works
Sara, S. J. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0297-16.2017 · Cited by 100 · see citing works
Self-citationLi, Y., Hickey, L., Perrins, R., Werlen, E., Patel, A. A., Hirschberg, S., Jones, M. W., Salinas, S., Kremer, E. J., & Pickering, A. E. (2016) · Brain Research · doi:10.1016/j.brainres.2016.02.023 · Cited by 97 · see citing works
Self-citationNovitskaya, Y., Sara, S., Logothetis, N., & Eschenko, O. (2016) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.040923.115 · Cited by 86 · see citing works
Self-citationLee, K. H., & McCormick, D. A. (1996) · Neuron · doi:10.1016/s0896-6273(00)80162-2 · Cited by 85 · see citing works
Aston‐Jones, G., Foote, S. L., & Segal, M. (1985) · Neuroscience · doi:10.1016/0306-4522(85)90077-6 · Cited by 74 · see citing works
Self-citationREM restriction persistently alters strategy used to solve a spatial taskPreprint
Bjorness, T. E., Riley, B. T., Tysor, M. K., & Poe, G. R. (2005) · Learning & Memory · doi:10.1101/lm.84805 · Cited by 69 · see citing works
Self-citationWatts, A., Gritton, H. J., Sweigart, J., & Poe, G. R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0170-12.2012 · Cited by 68 · see citing works
Self-citationGross, B. A., Walsh, C. M., Turakhia, A. A., Booth, V., Mashour, G. A., & Poe, G. R. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.07.009 · Cited by 58 · see citing works
Self-citationFuhs, M. C., VanRhoads, S. R., Casale, A. E., McNaughton, B., & Touretzky, D. S. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00132.2005 · Cited by 53 · see citing works
Different simultaneous sleep states in the hippocampus and neocortex
Emrick, J. J., Gross, B. A., Riley, B. T., & Poe, G. R. (2016) · Sleep · doi:10.5665/sleep.6326 · Cited by 38 · see citing works
Self-citationBooth, V., & Poe, G. R. (2006) · Hippocampus · doi:10.1002/hipo.20143 · Cited by 36 · see citing works
Self-citationA spatial memory task appropriate for electrophysiological recordings
Poe, G. R., Thompson, C. M., Riley, B. T., Tysor, M. K., Bjorness, T. E., Steinhoff, B. P., & Ferluga, E. D. (2002) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(02)00233-9 · Cited by 9 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- [35]Tamminen J, Payne JD, Stickgold R, Wamsley EJ, and Gareth M. (2011). Sleep spindle activity is associated with the integration of new memories into existing knowledge. J. Neurosci. 30, 14356– 14360. PMC2989532 20980591
Cited by
Sorted by citations
Locus coeruleus: a new look at the blue spot
Poe, G. R., Foote, S., Eschenko, O., Johansen, J. P., Bouret, S., Aston-Jones, G., Harley, C. W., Manahan-Vaughan, D., Weinshenker, D., Valentino, R., et al. (2020) · Nature Reviews Neuroscience · doi:10.1038/s41583-020-0360-9 · Cited by 720 · see citing works
Self-citationSleep spindles: mechanisms and functions
Fernandez, L. M. J., & Lüthi, A. (2020) · Physiological Reviews · doi:10.1152/physrev.00042.2018 · Cited by 716 · see citing works
Brain mechanisms of insomnia: new perspectives on causes and consequences
Someren, E. J. W. V. (2020) · Physiological Reviews · doi:10.1152/physrev.00046.2019 · Cited by 558 · see citing works
Sleep—A brain-state serving systems memory consolidation
Brodt, S., Inostroza, M., Niethard, N., & Born, J. (2023) · Neuron · doi:10.1016/j.neuron.2023.03.005 · Cited by 343 · 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
Self-citationLocus coeruleus norepinephrine activity mediates sensory-evoked awakenings from sleep
Hayat, H., Regev, N., Matosevich, N., Sales, A. C., Paredes-Rodriguez, E., Krom, A. J., Bergman, L., Li, Y., Lavigne, M., Kremer, E. J., et al. (2020) · Science Advances · doi:10.1126/sciadv.aaz4232 · Cited by 255 · see citing works
Self-citationNoradrenergic 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
Hyperarousal in insomnia disorder: Current evidence and potential mechanisms
Dressle, R. J., & Riemann, D. (2023) · Journal of Sleep Research · doi:10.1111/jsr.13928 · Cited by 218 · see citing works
Breton‐Provencher, V., Drummond, G. T., & Sur, M. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.638007 · Cited by 172 · see citing works
Restless REM Sleep Impedes Overnight Amygdala Adaptation
Wassing, R., Lakbila‐Kamal, O., Ramautar, J. R., Stoffers, D., Schalkwijk, F. W., & Someren, E. J. W. V. (2019) · Current Biology · doi:10.1016/j.cub.2019.06.034 · Cited by 172 · see citing works
Neuromodulation in circuits of aversive emotional learning
Likhtik, E., & Johansen, J. P. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0503-3 · Cited by 165 · see citing works
The Neural Circuits Underlying General Anesthesia and Sleep
Moody, O. A., Zhang, E. R., Vincent, K. F., Kato, R., Melonakos, E. D., Nehs, C. J., & Solt, K. (2021) · Anesthesia & Analgesia · doi:10.1213/ane.0000000000005361 · Cited by 165 · see citing works
Egroo, M. V., Koshmanova, E., Vandewalle, G., & Jacobs, H. I. L. (2022) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2022.101592 · Cited by 132 · see citing works
Pupil diameter is not an accurate real-time readout of locus coeruleus activity
Megemont, M., McBurney-Lin, J., & Yang, H. (2022) · eLife · doi:10.7554/elife.70510 · Cited by 115 · see citing works
When the Locus Coeruleus Speaks Up in Sleep: Recent Insights, Emerging Perspectives
Osorio-Forero, A., Cherrad, N., Banterle, L., Fernandez, L. M. J., & Lüthi, A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23095028 · Cited by 101 · see citing works
A noradrenergic-hypothalamic neural substrate for stress-induced sleep disturbances
Antila, H., Kwak, I., Choi, A., Pisciotti, A., Covarrubias, I., Baik, J., Eisch, A. J., Beier, K. T., THOMAS, S. A., Weber, F., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2123528119 · Cited by 91 · see citing works
Role of the locus coeruleus and basal forebrain in arousal and attention
Maness, E. B., Burk, J. A., McKenna, J. T., Schiffino, F. L., Strecker, R. E., & McCoy, J. G. (2022) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2022.07.014 · Cited by 81 · see citing works
Overnight worsening of emotional distress indicates maladaptive sleep in insomnia
Wassing, R., Benjamins, J. S., Talamini, L. M., Schalkwijk, F., & Van Someren, E. J. W. (2019) · Sleep · doi:10.1093/sleep/zsy268 · Cited by 78 · see citing works
Lüthi, A., & Nedergaard, M. (2025) · Neuron · doi:10.1016/j.neuron.2024.12.009 · Cited by 84 · see citing works
Conscious experiences and high-density EEG patterns predicting subjective sleep depth
Stephan, A., Lecci, S., Cataldi, J., & Siclari, F. (2021) · Current Biology · doi:10.1016/j.cub.2021.10.012 · Cited by 73 · see citing works
Haunted by the past: old emotions remain salient in insomnia disorder
Wassing, R., Schalkwijk, F. W., Lakbila‐Kamal, O., Ramautar, J. R., Stoffers, D., Mutsaerts, H. J. M. M., Talamini, L. M., & Someren, E. J. W. V. (2019) · Brain · doi:10.1093/brain/awz089 · Cited by 72 · see citing works
Ehrenberg, A. J., Kelberman, M. A., Liu, K. Y., Dahl, M. J., Weinshenker, D., Falgàs, N., Dutt, S., Mather, M., Ludwig, M., Betts, M. J., et al. (2023) · Alzheimer s & Dementia · doi:10.1002/alz.12937 · Cited by 72 · see citing works
Self-citationO’Callaghan, C., Walpola, I. C., & Shine, J. M. (2020) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0699 · Cited by 72 · see citing works
The locus coeruleus as a global model failure system
Jordan, R. (2023) · Trends in Neurosciences · doi:10.1016/j.tins.2023.11.006 · Cited by 77 · see citing works
Sleep scoring in rodents: Criteria, automatic approaches and outstanding issues
Rayan, A., Agarwal, A., Samanta, A., Severijnen, E., van der Meij, J., & Genzel, L. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15884 · Cited by 62 · see citing works
Overnight neuronal plasticity and adaptation to emotional distress
Cabrera, Y., Koymans, K. J., Poe, G. R., Kessels, H. W. H. G., Someren, E. J. W. V., & Wassing, R. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00799-w · Cited by 66 · see citing works
Self-citationAntidepressant medications in dementia: evidence and potential mechanisms of treatment-resistance
Costello, H., Roiser, J. P., & Howard, R. (2023) · Psychological Medicine · doi:10.1017/s003329172200397x · Cited by 60 · see citing works
Sex differences within sleep in gonadally intact rats
Swift, K. M., Keus, K., Echeverria, C. G., Cabrera, Y., Jimenez, J., Holloway, J., Clawson, B. C., & Poe, G. R. (2019) · SLEEP · doi:10.1093/sleep/zsz289 · Cited by 60 · see citing works
Self-citationSleep microstructure organizes memory replay
Chang, H., Tang, W., Wulf, A. M., Nyasulu, T., Wolf, M. E., Fernández‐Ruiz, A., & Oliva, A. (2025) · Nature · doi:10.1038/s41586-024-08340-w · Cited by 64 · see citing works
Bacon, T., Pickering, A. E., & Mellor, J. R. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa159 · Cited by 54 · see citing works
Self-citationThe role of Locus Coeruleus in neuroinflammation occurring in Alzheimer’s disease
Giorgi, F. S., Saccaro, L. F., Galgani, A., Busceti, C. L., Biagioni, F., Frati, A., & Fornai, F. (2019) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2019.08.007 · Cited by 53 · see citing works
Pupil size reveals arousal level fluctuations in human sleep
Carro‐Domínguez, M., Huwiler, S., Oberlin, S., Oesch, T. L., Badii, G., Lüthi, A., Wenderoth, N., Meissner, S. N., & Lustenberger, C. (2025) · Nature Communications · doi:10.1038/s41467-025-57289-5 · Cited by 58 · see citing works
Janitzky, K. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00371 · Cited by 50 · see citing works
Omoluabi, T., Torraville, S. E., Maziar, A., Ghosh, A., Power, K. D., Reinhardt, C., Harley, C. W., & Yuan, Q. (2021) · Alzheimer s & Dementia Translational Research & Clinical Interventions · doi:10.1002/trc2.12231 · Cited by 47 · see citing works
The role of the locus coeruleus in shaping adaptive cortical melodies
Wainstein, G., Müller, E. J., Taylor, N. L., Munn, B., & Shine, J. M. (2022) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2022.03.006 · Cited by 45 · see citing works
Osorio-Forero, A., Foustoukos, G., Cardis, R., Cherrad, N., Devenoges, C., Fernandez, L. M. J., & Lüthi, A. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.20.541586 · Cited by 35 · see citing works
Ghosh, A., Massaeli, F., Power, K. D., Omoluabi, T., Torraville, S. E., Pritchett, J. B., Sepahvand, T., Strong, V., Reinhardt, C., Chen, X., et al. (2021) · Cerebral Cortex Communications · doi:10.1093/texcom/tgab026 · Cited by 26 · see citing works
Monari, S., de Suduiraut, I. G., Grosse, J., Zanoletti, O., Walker, S. E., Mesquita, M. S., Wood, T., Cash, D., Astori, S., & Sandi, C. (2023) · Biological Psychiatry · doi:10.1016/j.biopsych.2023.09.015 · Cited by 32 · see citing works
Tukker, J. J., Beed, P. S., Schmitz, D., Larkum, M. E., & Sachdev, R. N. S. (2020) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2020.00022 · Cited by 28 · see citing works
Spontaneous slow oscillation—slow spindle features predict induced overnight memory retention
Dehnavi, F., Koo, P. C., Ghorbani, M., & Marshall, L. (2021) · SLEEP · doi:10.1093/sleep/zsab127 · Cited by 31 · see citing works
Modulation of Prefrontal Cortex Slow Oscillations by Phasic Activation of the Locus Coeruleus
Durán, E., Yang, M., Neves, R. M., Logothetis, N. K., & Eschenko, O. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2020.11.028 · Cited by 29 · see citing works
Van Egroo, M., van Someren, E. J. W., Grinberg, L. T., Bennett, D. A., & Jacobs, H. I. L. (2024) · Annals of Neurology · doi:10.1002/ana.26880 · Cited by 28 · see citing works
Rapid eye movement sleep and neuronal development
Wolfe, K. M., & Ralls, F. M. (2019) · Current Opinion in Pulmonary Medicine · doi:10.1097/mcp.0000000000000622 · Cited by 28 · see citing works
The Locus Coeruleus in Chronic Pain
España, J. C., Mohan, A., & Vanneste, S. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25168636 · Cited by 26 · see citing works
Sleep’s contribution to memory formation
Lutz, N. D., Harkotte, M., & Jan Born, A. (2025) · Physiological Reviews · doi:10.1152/physrev.00054.2024 · Cited by 40 · see citing works
Sleep disturbances in autism spectrum disorder: Animal models, neural mechanisms, and therapeutics
Maurer, J. J., Choi, A., An, I., Sathi, N., & Chung, S. (2023) · Neurobiology of Sleep and Circadian Rhythms · doi:10.1016/j.nbscr.2023.100095 · Cited by 28 · see citing works
Orlando, I. F., O’Callaghan, C., Lam, A. K. F., McKinnon, A. C., Tan, J. B., Michaelian, J. C., Kong, S. D. X., D'Rozario, A. L., & Naismith, S. L. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02335-1 · Cited by 25 · see citing works
The Molecular Relationship between Stress and Insomnia
Birch, J., & Vanderheyden, W. M. (2022) · Advanced Biology · doi:10.1002/adbi.202101203 · Cited by 24 · see citing works
The role of ascending arousal network in patients with chronic insomnia disorder
Gong, L., He, K., Fang, C., Deng, Z., Cheng, K., Zhang, X., Zhou, W., Ou, J., Wang, J., Zhang, B., et al. (2022) · Human Brain Mapping · doi:10.1002/hbm.26072 · Cited by 24 · see citing works
Optogenetic control of neural activity: The biophysics of microbial rhodopsins in neuroscience
Piatkevich, K. D., & Boyden, E. S. (2023) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583523000033 · Cited by 24 · see citing works
On the basis of sex and sleep: the influence of the estrous cycle and sex on sleep-wake behavior
Swift, K. M., Gary, N. C., & Urbanczyk, P. J. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1426189 · Cited by 30 · see citing works
Self-citationEmerging Functions of Neuromodulation during Sleep
Sulaman, B. A., Zhang, Y., Matosevich, N., Kjærby, C., Foustoukos, G., Andersen, M., & Eban-Rothschild, A. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1277-24.2024 · Cited by 21 · see citing works
Matsuda, Y., Ozawa, N., Shinozaki, T., Aoki, K., Nihonmatsu-Kikuchi, N., Shinba, T., & Tatebayashi, Y. (2021) · Scientific Reports · doi:10.1038/s41598-021-96094-0 · Cited by 23 · see citing works
Durán, E., Pandinelli, M., Logothetis, N. K., & Eschenko, O. (2023) · Scientific Reports · doi:10.1038/s41598-023-31308-1 · Cited by 25 · see citing works
Sleep as a default state of cortical and subcortical networks
Bandarabadi, M., Vassalli, A., & Tafti, M. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2019.12.004 · Cited by 19 · see citing works
Tkaczynski, J. A., Borodovitsyna, O., & Chandler, D. J. (2022) · Brain Sciences · doi:10.3390/brainsci12070860 · Cited by 17 · see citing works
Locus coeruleus activity while awake is associated with REM sleep quality in older individuals
Koshmanova, E., Berger, A., Beckers, E., Campbell, I., Mortazavi, N., Sharifpour, R., Paparella, I., Balda, F., Berthomier, C., Degueldre, C., et al. (2023) · JCI Insight · doi:10.1172/jci.insight.172008 · Cited by 19 · see citing works
Bai, Z., Han, Y., Zhuang, D., & Sun, C. T. (2024) · Building and Environment · doi:10.1016/j.buildenv.2024.112214 · Cited by 17 · see citing works
van den Berg, N., Gibbings, A., Baena, D., Alyssa, P., Al-Kuwatli, J., Ray, L. B., & Fogel, S. M. (2023) · SLEEP · doi:10.1093/sleep/zsad151 · Cited by 17 · see citing works
BaHammam, A. S., Pirzada, A. R., & Pandi-Perumal, S. R. (2022) · Sleep And Breathing · doi:10.1007/s11325-022-02602-5 · Cited by 18 · see citing works
Diverse ancestral brainstem noradrenergic neuron activity across species and biological factorsPreprint
Kelberman, M. A., Rodberg, E. M., Munn, B. R., Arabzadeh, E., Bair-Marshall, C. J., Berridge, C. W., Berrocoso, E., Breton‐Provencher, V., Chandler, D. J., Che, A., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.10.14.618224 · Cited by 19 · see citing works
Self-citationA time window for memory consolidation during NREM sleep revealed by cAMP oscillation
Deng, Z., Fei, X., Zhang, S., & Xu, M. (2025) · Neuron · doi:10.1016/j.neuron.2025.03.020 · Cited by 17 · see citing works
Gheidi, A., Davidson, C. J., Simpson, S. C., Yahya, M. A., Sadik, N., Mascarin, A. T., & Perrine, S. A. (2023) · Psychopharmacology · doi:10.1007/s00213-023-06453-0 · Cited by 16 · see citing works
The Many Unknowns of Partial Sensory Disconnection during Sleep: A Review of the Literature
Cirelli, C., & Tononi, G. (2024) · Clinical and Translational Neuroscience · doi:10.3390/ctn8010009 · Cited by 15 · see citing works
Shining a Light on the Mechanisms of Sleep for Memory Consolidation
Frazer, M. A., Cabrera, Y., Guthrie, R. S., & Poe, G. R. (2021) · Current Sleep Medicine Reports · doi:10.1007/s40675-021-00204-3 · Cited by 15 · see citing works
Self-citationPotential Interactions Between Cerebellar Dysfunction and Sleep Disturbances in Dystonia
Leon, L. E. S., & Sillitoe, R. V. (2022) · Dystonia · doi:10.3389/dyst.2022.10691 · Cited by 15 · see citing works
Li, P., Yang, L., Shao, X., Zou, Z., Shi, H., Sun, Y., Wu, X., Li, Z., Li, Y., & Li, Z. (2025) · Microbiological Research · doi:10.1016/j.micres.2025.128276 · Cited by 14 · see citing works
Self-citationHuo, C., Lombardi, F., Blanco‐Centurion, C., Shiromani, P. J., & Ivanov, P. C. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1939-23.2024 · Cited by 14 · see citing works
Visual Plasticity in Adulthood: Perspectives from Hebbian and Homeostatic Plasticity
Bang, J. W., Hamilton-Fletcher, G., & Chan, K. C. (2021) · The Neuroscientist · doi:10.1177/10738584211037619 · Cited by 15 · see citing works
The Future of Insomnia Research—There's Still Work to Be Done
Dressle, R. J., Spiegelhalder, K., Schiel, J. E., Benz, F., Johann, A. F., Feige, B., Jernelöv, S., Perlis, M. L., & Riemann, D. W. (2025) · Journal of Sleep Research · doi:10.1111/jsr.70091 · Cited by 12 · see citing works
Mir, F. A., Jha, S. K., & Nehs, C. J. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106442 · Cited by 16 · see citing works
Systems memory consolidation during sleep: oscillations, neuromodulators, and synaptic remodeling
Kim, J., & Park, M. (2025) · BMB Reports · doi:10.5483/bmbrep.2025-0033 · Cited by 14 · see citing works
Noradrenergic therapies in neurodegenerative disease: from symptomatic to disease modifying therapy?
Durcan, R., O’Callaghan, C., & Rowe, J. B. (2025) · Brain Communications · doi:10.1093/braincomms/fcaf310 · Cited by 14 · see citing works
Monoaminergic signaling during mammalian NREM sleep - Recent insights and next-level questions
Foustoukos, G., & Lüthi, A. (2025) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2025.103025 · Cited by 12 · see citing works
Disrupted sleep in dystonia depends on cerebellar function but not motor symptoms in mice
Leon, L. E. S., & Sillitoe, R. V. (2023) · Dystonia · doi:10.3389/dyst.2023.11487 · Cited by 11 · see citing works
Insomnia and intestinal microbiota: a narrative review
Liu, L., Zhu, J.-W., Wu, J.-L., Li, M., Lu, M.-L., Yu, Y., & Pan, L. (2024) · Sleep And Breathing · doi:10.1007/s11325-024-03206-x · Cited by 11 · see citing works
Neurophysiological effects of targeting sleep spindles with closed-loop auditory stimulation
Jourde, H. R., Sobral, M., Beltrame, G., & Coffey, E. B. J. (2025) · SLEEP Advances · doi:10.1093/sleepadvances/zpaf007 · Cited by 12 · see citing works
Stephan, A., Cataldi, J., Virk, A. S., & Siclari, F. (2025) · Current Biology · doi:10.1016/j.cub.2025.06.064 · Cited by 11 · see citing works
Memory reactivations and consolidation: considering neuromodulators across wake and sleep
Samanta, A., Alonso, A., & Genzel, L. (2020) · Current Opinion in Physiology · doi:10.1016/j.cophys.2020.01.003 · Cited by 11 · see citing works
Kam, K., Rapoport, D. M., Parekh, A., Ayappa, I. A., & Varga, A. W. (2021) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2021.109224 · Cited by 11 · see citing works
Purkinje cell dysfunction causes disrupted sleep in ataxic mice
Leon, L. E. S., Brown, A. M., Kaku, H., & Sillitoe, R. V. (2024) · Disease Models & Mechanisms · doi:10.1242/dmm.050379 · Cited by 10 · see citing works
Traumatic brain injury and sleep in military and veteran populations: A literature review
Landvater, J., Kim, S. Y., Caswell, K., Kwon, C., Odafe, E., Roe, G., Tripathi, A., Vukovics, C., Wang, J., Ryan, K., et al. (2024) · Neurorehabilitation · doi:10.3233/nre-230380 · Cited by 11 · see citing works
Lahlou, S., Kamińska, M., Doyon, J., Carrier, J., & Sharp, M. E. (2024) · Journal of Clinical Sleep Medicine · doi:10.5664/jcsm.11080 · Cited by 9 · see citing works
Aksamaz, S., Mölle, M., Akinola, E. O., Gromodka, E., Bazhenov, M., & Marshall, L. (2023) · European Journal of Neuroscience · doi:10.1111/ejn.16116 · Cited by 9 · see citing works
Cabrera, Y., Holloway, J., & Poe, G. R. (2020) · Journal of Women s Health · doi:10.1089/jwh.2020.8332 · Cited by 8 · see citing works
Self-citationGrydeland, H., Sederevičius, D., Wang, Y., David Bartrés-faz, A., Bertram, L., Dobričić, V., Düzel, S., Ebmeier, K. P., Lindenberger, U., Nyberg, L. H., et al. (2021) · SLEEP · doi:10.1093/sleep/zsab110 · Cited by 9 · see citing works
Maurer, L., Sharman, R. L., Espie, C. A., & Kyle, S. D. (2023) · Journal of Sleep Research · doi:10.1111/jsr.13982 · Cited by 8 · see citing works
Phasic Dopamine Release in the Nucleus Accumbens Influences REM Sleep Timing
Toth, B. A., & Burgess, C. R. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1374-24.2024 · Cited by 8 · see citing works
Experience alters hippocampal and cortical network communication via a KIBRA-dependent mechanism
Quigley, L. D., Pendry, R., Mendoza, M. L., Pfeiffer, B. E., & Volk, L. J. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112662 · Cited by 8 · see citing works
Koshmanova, E., Muto, V., Chylinski, D., Mouraux, C., Reyt, M., Grinard, M., Talwar, P., Lambot, E., Berthomier, C., Brandewinder, M., et al. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105924 · Cited by 8 · see citing works
Do all norepinephrine surges disrupt sleep?
Lüthi, A., Franken, P., Fulda, S., Siclari, F., & Someren, E. J. W. V. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01313-8 · Cited by 8 · see citing works
Sleeping through brain excitation and inhibition
Pereira, S. I. R., & Lewis, P. A. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0697-4 · Cited by 7 · see citing works
Noradrenaline Regulation of Brain-Body Communication
Fernandes, G., Lam, R. M., Park, J. H., Drummond, G. T., & Sur, M. (2025) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-89525-8_2 · Cited by 7 · see citing works
Cumpana, L., Zanoletti, O., Kankanamge, D., Copits, B. A., Sandi, C., & Astori, S. (2025) · Nature Communications · doi:10.1038/s41467-025-63118-6 · Cited by 7 · see citing works
Rethinking early Alzheimer’s disease: An impaired internal model updating disorder?
Antonioni, A. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106790 · Cited by 7 · see citing works
Reinhold, F. L., Gerlicher, A. M. V., Someren, E. J. W. V., & Kindt, M. (2022) · SLEEP · doi:10.1093/sleep/zsac220 · Cited by 7 · see citing works
Disruption of Sleep Microarchitecture Is a Sensitive and Early Marker of Parkinson’s Disease
Doppler, C. E. J., Smit, J. A. M., Hommelsen, M., Seger, A., Okkels, N., Horsager, J., Kinnerup, M. B., Hansen, A. K., Fedorova, T. D., Knudsen, K., et al. (2022) · Journal of Parkinson s Disease · doi:10.3233/jpd-223442 · Cited by 6 · see citing works
Brunswick, C. A., Carpenter, C. M., Dennis, N. A., & Kwapis, J. L. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106195 · Cited by 8 · see citing works
The influence of peripheral glucose on sleep brain oscillations
Yu, L., Hallschmid, M., Jan Born, A., & Niethard, N. (2025) · SLEEP · doi:10.1093/sleep/zsaf151 · Cited by 6 · see citing works
Are the biomedical sciences ready for synthetic biology?
DeNies, M. S., Liu, A. P., & Schnell, S. D. (2020) · BioMolecular Concepts · doi:10.1515/bmc-2020-0003 · Cited by 6 · see citing works
- Authors
- Swift, 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., & Poe, G. R.
- Affiliations
- University of Michigan (US)
- University of California, Los Angeles (US)
- University of Massachusetts Amherst (US)
- University of Bristol (GB)
- Collège de France (FR)
- Corresponding author
- Poe, Gina R.
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2018-11
- Volume
- 28
- Issue
- 22
- Pages
- 3599-3609.e4
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC7556718
- OpenAlex
- W2899315813
- Cited by
- 158
- References
- 62
- Citations by year
- 2026: 19 · 2025: 34 · 2024: 21 · 2023: 25 · 2022: 19 · 2021: 19 · 2020: 12 · 2019: 8 · 2018: 1
- FWCI
- 5.95
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 383 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Bristol Research (University of Bristol) (acceptedVersion, cc-by-nc-nd)
- Rutgers University Community Repository (Rutgers University) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Explore Bristol Research (submittedVersion, cc-by-nc-nd)
- Funders
- NIMH (R01 60670, br088373)
- Wellcome Senior Clinical
- University of Michigan Systems and Integrative Biology T32
- 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, norepinephrine, sleep spindles, memory consolidation, spatial memory, REM sleep, NREM sleep, hippocampus-dependent learning, memory reconsolidation, optogenetic stimulation, synaptic plasticity
- MeSH terms
- Memory Consolidation, Place Cells, Sleep, Slow-Wave, Animals, Brain, Electroencephalography, Hippocampus, Locus Coeruleus, Male, Sleep, Sleep Stages, Sleep, REM, Theta Rhythm, Rats, Long-Evans, Rats, CA1 Region, Hippocampal, Spatial Memory
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