Overnight neuronal plasticity and adaptation to emotional distress.
Journal
Nature reviews. Neuroscience
ISSN: 1471-0048
Titre abrégé: Nat Rev Neurosci
Pays: England
ID NLM: 100962781
Informations de publication
Date de publication:
05 Mar 2024
05 Mar 2024
Historique:
accepted:
01
02
2024
medline:
6
3
2024
pubmed:
6
3
2024
entrez:
5
3
2024
Statut:
aheadofprint
Résumé
Expressions such as 'sleep on it' refer to the resolution of distressing experiences across a night of sound sleep. Sleep is an active state during which the brain reorganizes the synaptic connections that form memories. This Perspective proposes a model of how sleep modifies emotional memory traces. Sleep-dependent reorganization occurs through neurophysiological events in neurochemical contexts that determine the fates of synapses to grow, to survive or to be pruned. We discuss how low levels of acetylcholine during non-rapid eye movement sleep and low levels of noradrenaline during rapid eye movement sleep provide a unique window of opportunity for plasticity in neuronal representations of emotional memories that resolves the associated distress. We integrate sleep-facilitated adaptation over three levels: experience and behaviour, neuronal circuits, and synaptic events. The model generates testable hypotheses for how failed sleep-dependent adaptation to emotional distress is key to mental disorders, notably disorders of anxiety, depression and post-traumatic stress with the common aetiology of insomnia.
Identifiants
pubmed: 38443627
doi: 10.1038/s41583-024-00799-w
pii: 10.1038/s41583-024-00799-w
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. Springer Nature Limited.
Références
Hamann, S. Cognitive and neural mechanisms of emotional memory. Trends Cogn. Sci. 5, 394–400 (2001).
pubmed: 11520704
doi: 10.1016/S1364-6613(00)01707-1
LaBar, K. S. & Cabeza, R. Cognitive neuroscience of emotional memory. Nat. Rev. Neurosci. 7, 54–64 (2006).
pubmed: 16371950
doi: 10.1038/nrn1825
Crowley, R., Bendor, D. & Javadi, A.-H. A review of neurobiological factors underlying the selective enhancement of memory at encoding, consolidation, and retrieval. Prog. Neurobiol. 179, 101615 (2019).
pubmed: 31054931
doi: 10.1016/j.pneurobio.2019.04.004
Ashton, J. E., Harrington, M. O., Guttesen, A. Á. V., Smith, A. K. & Cairney, S. A. Sleep preserves physiological arousal in emotional memory. Sci. Rep. 9, 5966 (2019).
pubmed: 30979941
pmcid: 6461689
doi: 10.1038/s41598-019-42478-2
Bolinger, E. et al. Sleep’s benefits to emotional processing emerge in the long term. Cortex 120, 457–470 (2019).
pubmed: 31476555
doi: 10.1016/j.cortex.2019.07.008
Lipinska, G. & Thomas, K. G. F. The interaction of REM fragmentation and night-time arousal modulates sleep-dependent emotional memory consolidation. Front. Psychol. 10, 1766 (2019).
pubmed: 31428021
pmcid: 6688536
doi: 10.3389/fpsyg.2019.01766
Conte, F., Cerasuolo, M., Giganti, F. & Ficca, G. Sleep enhances strategic thinking at the expense of basic procedural skills consolidation. J. Sleep Res. 29, e13034 (2020).
pubmed: 32255237
doi: 10.1111/jsr.13034
Tucker, M. A., Humiston, G. B., Summer, T. & Wamsley, E. Comparing the effects of sleep and rest on memory consolidation. Nat. Sci. Sleep 12, 79–91 (2020).
pubmed: 32099493
pmcid: 7007500
doi: 10.2147/NSS.S223917
Short, M. A., Booth, S. A., Omar, O., Ostlundh, L. & Arora, T. The relationship between sleep duration and mood in adolescents: a systematic review and meta-analysis. Sleep Med. Rev. 52, 101311 (2020).
pubmed: 32240932
doi: 10.1016/j.smrv.2020.101311
Tononi, G. & Cirelli, C. Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81, 12–34 (2014).
pubmed: 24411729
pmcid: 3921176
doi: 10.1016/j.neuron.2013.12.025
Niethard, N. & Born, J. Back to baseline: sleep recalibrates synapses. Nat. Neurosci. 22, 149–151 (2019).
pubmed: 30617259
doi: 10.1038/s41593-018-0327-6
Genzel, L., Kroes, M. C. W., Dresler, M. & Battaglia, F. P. Light sleep versus slow wave sleep in memory consolidation: a question of global versus local processes? Trends Neurosci. 37, 10–19 (2014).
pubmed: 24210928
doi: 10.1016/j.tins.2013.10.002
Osorio-Forero, A., Cherrad, N., Banterle, L., Fernandez, L. M. J. & Lüthi, A. When the locus coeruleus speaks up in sleep: recent insights, emerging perspectives. Int. J. Mol. Sci. 23, 5028 (2022).
pubmed: 35563419
pmcid: 9099715
doi: 10.3390/ijms23095028
Kjaerby, C. et al. Memory-enhancing properties of sleep depend on the oscillatory amplitude of norepinephrine. Nat. Neurosci. 25, 1059–1070 (2022). This paper shows that long LC silences during sleep promote memory, sleep spindles and REM sleep, whereas shorter LC silences and more frequent increases in NA promote microarousals and decrease memory performance, thereby reinforcing the concept that NA absences are important to sleep-dependent memory consolidation.
pubmed: 35798980
pmcid: 9817483
doi: 10.1038/s41593-022-01102-9
Swift, K. M. et al. Abnormal locus coeruleus sleep activity alters sleep signatures of memory consolidation and impairs place cell stability and spatial memory. Curr. Biol. 28, 3599–3609.e4 (2018). This paper shows how aberrant activity of the LC during normally silent times (that is, REM sleep and the transition to REM sleep period) disrupts spindle generation and weakens delta and theta oscillation power, interfering with proper learning.
pubmed: 30393040
pmcid: 7556718
doi: 10.1016/j.cub.2018.09.054
Osorio-Forero, A. et al. Noradrenergic circuit control of non-REM sleep substates. Curr. Biol. 31, 5009–5023.e7 (2021).
pubmed: 34648731
doi: 10.1016/j.cub.2021.09.041
Wassing, R. et al. Restless REM sleep impedes overnight amygdala adaptation. Curr. Biol. 29, 2351–2358.e4 (2019). This paper shows that overnight amygdala adaptation is proportional to the duration of sound REM sleep and preceding NREM sleep spindles, but that adaptation fails proportionally to the number of awakenings and arousals in REM sleep.
pubmed: 31303489
doi: 10.1016/j.cub.2019.06.034
Poe, G. R. Sleep is for forgetting. J. Neurosci. 37, 464–473 (2017).
pubmed: 28100731
pmcid: 5242402
doi: 10.1523/JNEUROSCI.0820-16.2017
Guskjolen, A. & Cembrowski, M. S. Engram neurons: encoding, consolidation, retrieval, and forgetting of memory. Mol. Psychiatry 28, 3207–3219 (2023).
pubmed: 37369721
pmcid: 10618102
doi: 10.1038/s41380-023-02137-5
Roy, D. S. et al. Brain-wide mapping reveals that engrams for a single memory are distributed across multiple brain regions. Nat. Commun. 13, 1799 (2022).
pubmed: 35379803
pmcid: 8980018
doi: 10.1038/s41467-022-29384-4
Ghosh, V. E. & Gilboa, A. What is a memory schema? A historical perspective on current neuroscience literature. Neuropsychologia 53, 104–114 (2014).
pubmed: 24280650
doi: 10.1016/j.neuropsychologia.2013.11.010
van Kesteren, M. T. R., Rijpkema, M., Ruiter, D. J. & Fernández, G. Retrieval of associative information congruent with prior knowledge is related to increased medial prefrontal activity and connectivity. J. Neurosci. 30, 15888–15894 (2010).
pubmed: 21106827
pmcid: 6633736
doi: 10.1523/JNEUROSCI.2674-10.2010
Takashima, A. et al. Shift from hippocampal to neocortical centered retrieval network with consolidation. J. Neurosci. 29, 10087–10093 (2009).
pubmed: 19675242
pmcid: 6664975
doi: 10.1523/JNEUROSCI.0799-09.2009
Nieuwenhuis, I. L. C. & Takashima, A. The role of the ventromedial prefrontal cortex in memory consolidation. Behav. Brain Res. 218, 325–334 (2011).
pubmed: 21147169
doi: 10.1016/j.bbr.2010.12.009
Lubenov, E. V. & Siapas, A. G. Decoupling through synchrony in neuronal circuits with propagation delays. Neuron 58, 118–131 (2008).
pubmed: 18400168
doi: 10.1016/j.neuron.2008.01.036
Kim, J. et al. Amygdala depotentiation and fear extinction. Proc. Natl Acad. Sci. USA 104, 20955–20960 (2007).
pubmed: 18165656
pmcid: 2409248
doi: 10.1073/pnas.0710548105
Frey, U. & Morris, R. G. Synaptic tagging and long-term potentiation. Nature 385, 533–536 (1997).
pubmed: 9020359
doi: 10.1038/385533a0
Viola, H., Ballarini, F., Martínez, M. C. & Moncada, D. The tagging and capture hypothesis from synapse to memory. Prog. Mol. Biol. Transl. Sci. 122, 391–423 (2014).
pubmed: 24484708
doi: 10.1016/B978-0-12-420170-5.00013-1
Payne, J. D. & Kensinger, E. A. Stress, sleep, and the selective consolidation of emotional memories. Curr. Opin. Behav. Sci. 19, 36–43 (2018).
doi: 10.1016/j.cobeha.2017.09.006
Cunningham, T. J. et al. Higher post-encoding cortisol benefits the selective consolidation of emotional aspects of memory. Neurobiol. Learn. Mem. 180, 107411 (2021).
pubmed: 33609737
pmcid: 8076090
doi: 10.1016/j.nlm.2021.107411
Kitamura, T. et al. Engrams and circuits crucial for systems consolidation of a memory. Science 356, 73–78 (2017).
pubmed: 28386011
pmcid: 5493329
doi: 10.1126/science.aam6808
Hua, S.-S. et al. NMDA receptor-dependent synaptic potentiation via APPL1 signaling is required for the accessibility of a prefrontal neuronal assembly in retrieving fear extinction. Biol. Psychiatry 94, 262–277 (2023).
pubmed: 36842495
doi: 10.1016/j.biopsych.2023.02.013
Marek, R., Sun, Y. & Sah, P. Neural circuits for a top-down control of fear and extinction. Psychopharmacology 236, 313–320 (2019).
pubmed: 30215217
doi: 10.1007/s00213-018-5033-2
van Kesteren, M. T. R. et al. Differential roles for medial prefrontal and medial temporal cortices in schema-dependent encoding: from congruent to incongruent. Neuropsychologia 51, 2352–2359 (2013).
pubmed: 23770537
doi: 10.1016/j.neuropsychologia.2013.05.027
Sommer, T., Hennies, N., Lewis, P. A. & Alink, A. The assimilation of novel information into schemata and its efficient consolidation. J. Neurosci. 42, 5916–5929 (2022).
pubmed: 35710624
pmcid: 9337604
doi: 10.1523/JNEUROSCI.2373-21.2022
Cowan, E. et al. Sleep spindles promote the restructuring of memory representations in ventromedial prefrontal cortex through enhanced hippocampal-cortical functional connectivity. J. Neurosci. 40, 1909–1919 (2020).
pubmed: 31959699
pmcid: 7046449
doi: 10.1523/JNEUROSCI.1946-19.2020
Seibt, J. & Frank, M. G. Primed to sleep: the dynamics of synaptic plasticity across brain states. Front. Syst. Neurosci. 13, 2 (2019).
pubmed: 30774586
pmcid: 6367653
doi: 10.3389/fnsys.2019.00002
Cowan, E. T., Schapiro, A. C., Dunsmoor, J. E. & Murty, V. P. Memory consolidation as an adaptive process. Psychon. Bull. Rev. 28, 1796–1810 (2021).
pubmed: 34327677
doi: 10.3758/s13423-021-01978-x
Vanderheyden, W. M., Poe, G. R. & Liberzon, I. Trauma exposure and sleep: using a rodent model to understand sleep function in PTSD. Exp. Brain Res. 232, 1575–1584 (2014).
pubmed: 24623353
doi: 10.1007/s00221-014-3890-4
Makino, S., Hashimoto, K. & Gold, P. W. Multiple feedback mechanisms activating corticotropin-releasing hormone system in the brain during stress. Pharmacol. Biochem. Behav. 73, 147–158 (2002).
pubmed: 12076734
doi: 10.1016/S0091-3057(02)00791-8
Kaouane, N. et al. Glucocorticoids can induce PTSD-like memory impairments in mice. Science 335, 1510–1513 (2012).
pubmed: 22362879
doi: 10.1126/science.1207615
Atucha, E. et al. Noradrenergic activation of the basolateral amygdala maintains hippocampus-dependent accuracy of remote memory. Proc. Natl Acad. Sci. USA 114, 9176–9181 (2017).
pubmed: 28790188
pmcid: 5576838
doi: 10.1073/pnas.1710819114
Krenz, V., Sommer, T., Alink, A., Roozendaal, B. & Schwabe, L. Noradrenergic arousal after encoding reverses the course of systems consolidation in humans. Nat. Commun. 12, 6054 (2021).
pubmed: 34663784
pmcid: 8523710
doi: 10.1038/s41467-021-26250-7
Al Abed, A. S. et al. Preventing and treating PTSD-like memory by trauma contextualization. Nat. Commun. 11, 4220 (2020).
pubmed: 32839437
pmcid: 7445258
doi: 10.1038/s41467-020-18002-w
Desmedt, A., Marighetto, A. & Piazza, P.-V. Abnormal fear memory as a model for posttraumatic stress disorder. Biol. Psychiatry 78, 290–297 (2015).
pubmed: 26238378
doi: 10.1016/j.biopsych.2015.06.017
Lissek, S. et al. Generalized anxiety disorder is associated with overgeneralization of classically conditioned fear. Biol. Psychiatry 75, 909–915 (2014).
pubmed: 24001473
doi: 10.1016/j.biopsych.2013.07.025
Foote, S. L., Aston-Jones, G. & Bloom, F. E. Impulse activity of locus coeruleus neurons in awake rats and monkeys is a function of sensory stimulation and arousal. Proc. Natl Acad. Sci. USA 77, 3033–3037 (1980).
pubmed: 6771765
pmcid: 349541
doi: 10.1073/pnas.77.5.3033
Grant, S. J., Aston-Jones, G. & Redmond, D. E. Responses of primate locus coeruleus neurons to simple and complex sensory stimuli. Brain Res. Bull. 21, 401–410 (1988).
pubmed: 3145784
doi: 10.1016/0361-9230(88)90152-9
Sapolsky, R. M., Romero, L. M. & Munck, A. U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21, 55–89 (2000).
pubmed: 10696570
Waterhouse, B. D. & Navarra, R. L. The locus coeruleus-norepinephrine system and sensory signal processing: a historical review and current perspectives. Brain Res. 1709, 1–15 (2019).
pubmed: 30179606
doi: 10.1016/j.brainres.2018.08.032
Axmacher, N., Mormann, F., Fernández, G., Elger, C. E. & Fell, J. Memory formation by neuronal synchronization. Brain Res. Rev. 52, 170–182 (2006).
pubmed: 16545463
doi: 10.1016/j.brainresrev.2006.01.007
Jutras, M. J. & Buffalo, E. A. Synchronous neural activity and memory formation. Curr. Opin. Neurobiol. 20, 150–155 (2010).
pubmed: 20303255
pmcid: 2862842
doi: 10.1016/j.conb.2010.02.006
Fernández-Ruiz, A. et al. Entorhinal-CA3 dual-input control of spike timing in the hippocampus by theta-gamma coupling. Neuron 93, 1213–1226.e5 (2017).
pubmed: 28279355
pmcid: 5373668
doi: 10.1016/j.neuron.2017.02.017
Costa, M. et al. Aversive memory formation in humans involves an amygdala-hippocampus phase code. Nat. Commun. 13, 6403 (2022).
pubmed: 36302909
pmcid: 9613775
doi: 10.1038/s41467-022-33828-2
Andrade-Talavera, Y., Fisahn, A. & Rodríguez-Moreno, A. Timing to be precise? An overview of spike timing-dependent plasticity, brain rhythmicity, and glial cells interplay within neuronal circuits. Mol. Psychiatry 28, 2177–2188 (2023).
pubmed: 36991134
pmcid: 10611582
doi: 10.1038/s41380-023-02027-w
Teyler, T. J. & Rudy, J. W. The hippocampal indexing theory and episodic memory: updating the index. Hippocampus 17, 1158–1169 (2007).
pubmed: 17696170
doi: 10.1002/hipo.20350
Schlichting, M. L., Zeithamova, D. & Preston, A. R. CA1 subfield contributions to memory integration and inference. Hippocampus 24, 1248–1260 (2014).
pubmed: 24888442
pmcid: 4159432
doi: 10.1002/hipo.22310
Villano, W. J., Otto, A. R., Ezie, C. E. C., Gillis, R. & Heller, A. S. Temporal dynamics of real-world emotion are more strongly linked to prediction error than outcome. J. Exp. Psychol. Gen. 149, 1755–1766 (2020).
pubmed: 32039625
doi: 10.1037/xge0000740
Simpkiss, J. L. & Devine, D. P. Responses of the HPA axis after chronic variable stress: effects of novel and familiar stressors. Neuro Endocrinol. Lett. 24, 97–103 (2003).
pubmed: 12743542
Wassing, R. et al. Haunted by the past: old emotions remain salient in insomnia disorder. Brain 142, 1783–1796 (2019).
pubmed: 31135050
pmcid: 6536850
doi: 10.1093/brain/awz089
Botvinick, M. M., Cohen, J. D. & Carter, C. S. Conflict monitoring and anterior cingulate cortex: an update. Trends Cogn. Sci. 8, 539–546 (2004).
pubmed: 15556023
doi: 10.1016/j.tics.2004.10.003
Vinogradova, O. S. Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11, 578–598 (2001).
pubmed: 11732710
doi: 10.1002/hipo.1073
Borisyuk, R., Denham, M., Hoppensteadt, F., Kazanovich, Y. & Vinogradova, O. An oscillatory neural network model of sparse distributed memory and novelty detection. BioSystems 58, 265–272 (2000).
pubmed: 11164655
doi: 10.1016/S0303-2647(00)00131-3
Albasser, M. M., Poirier, G. L. & Aggleton, J. P. Qualitatively different modes of perirhinal-hippocampal engagement when rats explore novel vs. familiar objects as revealed by c-Fos imaging. Eur. J. Neurosci. 31, 134–147 (2010).
pubmed: 20092559
doi: 10.1111/j.1460-9568.2009.07042.x
Kinnavane, L., Amin, E., Olarte-Sánchez, C. M. & Aggleton, J. P. Detecting and discriminating novel objects: the impact of perirhinal cortex disconnection on hippocampal activity patterns. Hippocampus 26, 1393–1413 (2016).
pubmed: 27398938
pmcid: 5082501
doi: 10.1002/hipo.22615
Sara, S. J., Vankov, A. & Hervé, A. Locus coeruleus-evoked responses in behaving rats: a clue to the role of noradrenaline in memory. Brain Res. Bull. 35, 457–465 (1994).
pubmed: 7859103
doi: 10.1016/0361-9230(94)90159-7
Straube, T., Korz, V., Balschun, D. & Frey, J. U. Requirement of beta-adrenergic receptor activation and protein synthesis for LTP-reinforcement by novelty in rat dentate gyrus. J. Physiol. 552, 953–960 (2003).
pubmed: 12937286
pmcid: 2343450
doi: 10.1113/jphysiol.2003.049452
Rajkumar, R., Kumar, J. R. & Dawe, G. S. Priming locus coeruleus noradrenergic modulation of medial perforant path-dentate gyrus synaptic plasticity. Neurobiol. Learn. Mem. 138, 215–225 (2017).
pubmed: 27400867
doi: 10.1016/j.nlm.2016.07.003
Otmakhova, N. A. & Lisman, J. E. Dopamine, serotonin, and noradrenaline strongly inhibit the direct perforant path-CA1 synaptic input, but have little effect on the Schaffer collateral input. Ann. N. Y. Acad. Sci. 911, 462–464 (2000).
pubmed: 10911894
doi: 10.1111/j.1749-6632.2000.tb06746.x
Xiao, Z. et al. Noradrenergic depression of neuronal excitability in the entorhinal cortex via activation of TREK-2 K+ channels. J. Biol. Chem. 284, 10980–10991 (2009).
pubmed: 19244246
pmcid: 2667783
doi: 10.1074/jbc.M806760200
Reyes, B. A. S., Carvalho, A. F., Vakharia, K. & Van Bockstaele, E. J. Amygdalar peptidergic circuits regulating noradrenergic locus coeruleus neurons: linking limbic and arousal centers. Exp. Neurol. 230, 96–105 (2011).
pubmed: 21515261
pmcid: 3112280
doi: 10.1016/j.expneurol.2011.04.001
McCall, J. G. et al. CRH engagement of the locus coeruleus noradrenergic system mediates stress-induced anxiety. Neuron 87, 605–620 (2015).
pubmed: 26212712
pmcid: 4529361
doi: 10.1016/j.neuron.2015.07.002
Lamotte, G., Shouman, K. & Benarroch, E. E. Stress and central autonomic network. Auton. Neurosci. 235, 102870 (2021).
pubmed: 34461325
doi: 10.1016/j.autneu.2021.102870
Mather, M., Clewett, D., Sakaki, M. & Harley, C. W. Norepinephrine ignites local hotspots of neuronal excitation: how arousal amplifies selectivity in perception and memory. Behav. Brain Sci. 39, e200 (2016).
pubmed: 26126507
doi: 10.1017/S0140525X15000667
Dahl, M. J., Mather, M. & Werkle-Bergner, M. Noradrenergic modulation of rhythmic neural activity shapes selective attention. Trends Cogn. Sci. 26, 38–52 (2022).
pubmed: 34799252
doi: 10.1016/j.tics.2021.10.009
O’Dell, T. J., Connor, S. A., Guglietta, R. & Nguyen, P. V. β-Adrenergic receptor signaling and modulation of long-term potentiation in the mammalian hippocampus. Learn. Mem. 22, 461–471 (2015).
pubmed: 26286656
pmcid: 4561407
doi: 10.1101/lm.031088.113
Malenka, R. C. & Bear, M. F. LTP and LTD: an embarrassment of riches. Neuron 44, 5–21 (2004).
pubmed: 15450156
doi: 10.1016/j.neuron.2004.09.012
Castillo, P. E. Presynaptic LTP and LTD of excitatory and inhibitory synapses. Cold Spring Harb. Perspect. Biol. 4, a005728 (2012).
pubmed: 22147943
pmcid: 3281573
doi: 10.1101/cshperspect.a005728
Herring, B. E. & Nicoll, R. A. Long-term potentiation: from CaMKII to AMPA receptor trafficking. Annu. Rev. Physiol. 78, 351–365 (2016).
pubmed: 26863325
doi: 10.1146/annurev-physiol-021014-071753
Kessels, H. W. & Malinow, R. Synaptic AMPA receptor plasticity and behavior. Neuron 61, 340–350 (2009).
pubmed: 19217372
pmcid: 3917551
doi: 10.1016/j.neuron.2009.01.015
Diering, G. H. & Huganir, R. L. The AMPA receptor code of synaptic plasticity. Neuron 100, 314–329 (2018).
pubmed: 30359599
pmcid: 6214363
doi: 10.1016/j.neuron.2018.10.018
Wenthold, R. J., Petralia, R. S., Blahos J, I. I. & Niedzielski, A. S. Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J. Neurosci. 16, 1982–1989 (1996).
pubmed: 8604042
pmcid: 6578515
doi: 10.1523/JNEUROSCI.16-06-01982.1996
Makino, H. & Malinow, R. Compartmentalized versus global synaptic plasticity on dendrites controlled by experience. Neuron 72, 1001–1011 (2011).
pubmed: 22196335
pmcid: 3310180
doi: 10.1016/j.neuron.2011.09.036
Watt, A. J., Sjöström, P. J., Häusser, M., Nelson, S. B. & Turrigiano, G. G. A proportional but slower NMDA potentiation follows AMPA potentiation in LTP. Nat. Neurosci. 7, 518–524 (2004).
pubmed: 15048122
doi: 10.1038/nn1220
Bellone, C. & Nicoll, R. A. Rapid bidirectional switching of synaptic NMDA receptors. Neuron 55, 779–785 (2007).
pubmed: 17785184
doi: 10.1016/j.neuron.2007.07.035
Holehonnur, R. et al. Increasing the GluN2A/GluN2B ratio in neurons of the mouse basal and lateral amygdala inhibits the modification of an existing fear memory trace. J. Neurosci. 36, 9490–9504 (2016). This paper shows that memories are stabilized and, therefore, become more resistant to modification through an NMDA receptor subunit switch at synapses.
pubmed: 27605622
pmcid: 5013194
doi: 10.1523/JNEUROSCI.1743-16.2016
Murphy, J. A. et al. Phosphorylation of Ser1166 on GluN2B by PKA is critical to synaptic NMDA receptor function and Ca2+ signaling in spines. J. Neurosci. 34, 869–879 (2014).
pubmed: 24431445
pmcid: 3891964
doi: 10.1523/JNEUROSCI.4538-13.2014
Renner, M. C. et al. Synaptic plasticity through activation of GluA3-containing AMPA-receptors. eLife 6, e25462 (2017).
pubmed: 28762944
pmcid: 5578739
doi: 10.7554/eLife.25462
Thomas, M. J., Moody, T. D., Makhinson, M. & O’Dell, T. J. Activity-dependent beta-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region. Neuron 17, 475–482 (1996).
pubmed: 8816710
doi: 10.1016/S0896-6273(00)80179-8
Katsuki, H., Izumi, Y. & Zorumski, C. F. Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region. J. Neurophysiol. 77, 3013–3020 (1997).
pubmed: 9212253
doi: 10.1152/jn.1997.77.6.3013
Hu, H. et al. Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell 131, 160–173 (2007).
pubmed: 17923095
doi: 10.1016/j.cell.2007.09.017
Hruska, M., Cain, R. E. & Dalva, M. B. Nanoscale rules governing the organization of glutamate receptors in spine synapses are subunit specific. Nat. Commun. 13, 920 (2022).
pubmed: 35177616
pmcid: 8854560
doi: 10.1038/s41467-022-28504-4
McReynolds, J. R., Anderson, K. M., Donowho, K. M. & McIntyre, C. K. Noradrenergic actions in the basolateral complex of the amygdala modulate Arc expression in hippocampal synapses and consolidation of aversive and non-aversive memory. Neurobiol. Learn. Mem. 115, 49–57 (2014).
pubmed: 25196704
doi: 10.1016/j.nlm.2014.08.016
Waltereit, R. et al. Arg3.1/Arc mRNA induction by Ca
pubmed: 11466419
pmcid: 6762636
doi: 10.1523/JNEUROSCI.21-15-05484.2001
Chowdhury, S. et al. Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 52, 445–459 (2006).
pubmed: 17088211
pmcid: 1784006
doi: 10.1016/j.neuron.2006.08.033
Rial Verde, E. M., Lee-Osbourne, J., Worley, P. F., Malinow, R. & Cline, H. T. Increased expression of the immediate-early gene Arc/Arg3.1 reduces AMPA receptor-mediated synaptic transmission. Neuron 52, 461–474 (2006).
pubmed: 17088212
pmcid: 3951199
doi: 10.1016/j.neuron.2006.09.031
Okuno, H. et al. Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIβ. Cell 149, 886–898 (2012).
pubmed: 22579289
pmcid: 4856149
doi: 10.1016/j.cell.2012.02.062
Okuno, H., Minatohara, K. & Bito, H. Inverse synaptic tagging: an inactive synapse-specific mechanism to capture activity-induced Arc/Arg3.1 and to locally regulate spatial distribution of synaptic weights. Semin. Cell Dev. Biol. 77, 43–50 (2018).
pubmed: 28939038
doi: 10.1016/j.semcdb.2017.09.025
El-Boustani, S. et al. Locally coordinated synaptic plasticity of visual cortex neurons in vivo. Science 360, 1349–1354 (2018).
pubmed: 29930137
pmcid: 6366621
doi: 10.1126/science.aao0862
Newpher, T. M., Harris, S., Pringle, J., Hamilton, C. & Soderling, S. Regulation of spine structural plasticity by Arc/Arg3.1. Semin. Cell Dev. Biol. 77, 25–32 (2018).
pubmed: 28943393
doi: 10.1016/j.semcdb.2017.09.022
Holtmaat, A. J. G. D. et al. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45, 279–291 (2005).
pubmed: 15664179
doi: 10.1016/j.neuron.2005.01.003
Yang, G., Pan, F. & Gan, W.-B. Stably maintained dendritic spines are associated with lifelong memories. Nature 462, 920–924 (2009).
pubmed: 19946265
pmcid: 4724802
doi: 10.1038/nature08577
Radley, J. J. et al. Associative Pavlovian conditioning leads to an increase in spinophilin-immunoreactive dendritic spines in the lateral amygdala. Eur. J. Neurosci. 24, 876–884 (2006).
pubmed: 16930415
doi: 10.1111/j.1460-9568.2006.04962.x
Hill, T. C. & Zito, K. LTP-induced long-term stabilization of individual nascent dendritic spines. J. Neurosci. 33, 678–686 (2013).
pubmed: 23303946
pmcid: 6704923
doi: 10.1523/JNEUROSCI.1404-12.2013
Harley, C. W. & Milway, J. S. Glutamate ejection in the locus coeruleus enhances the perforant path-evoked population spike in the dentate gyrus. Exp. Brain Res. 63, 143–150 (1986).
pubmed: 2874050
doi: 10.1007/BF00235656
Quinlan, M. A. L. et al. Locus coeruleus optogenetic light activation induces long-term potentiation of perforant path population spike amplitude in rat dentate gyrus. Front. Syst. Neurosci. 12, 67 (2018).
pubmed: 30687027
doi: 10.3389/fnsys.2018.00067
Lesuis, S. L., Timmermans, W., Lucassen, P. J., Hoogenraad, C. C. & Krugers, H. J. Glucocorticoid and β-adrenergic regulation of hippocampal dendritic spines. J. Neuroendocrinol. 32, e12811 (2020).
pubmed: 31715030
doi: 10.1111/jne.12811
Genoux, D. et al. Protein phosphatase 1 is a molecular constraint on learning and memory. Nature 418, 970–975 (2002).
pubmed: 12198546
doi: 10.1038/nature00928
Nabavi, S. et al. Engineering a memory with LTD and LTP. Nature 511, 348–352 (2014).
pubmed: 24896183
pmcid: 4210354
doi: 10.1038/nature13294
Moreno, A. Molecular mechanisms of forgetting. Eur. J. Neurosci. 54, 6912–6932 (2021).
pubmed: 32464703
doi: 10.1111/ejn.14839
Nabavi, S. et al. Metabotropic NMDA receptor function is required for NMDA receptor-dependent long-term depression. Proc. Natl Acad. Sci. USA 110, 4027–4032 (2013).
pubmed: 23431133
pmcid: 3593861
doi: 10.1073/pnas.1219454110
Holman, D., Feligioni, M. & Henley, J. M. Differential redistribution of native AMPA receptor complexes following LTD induction in acute hippocampal slices. Neuropharmacology 52, 92–99 (2007).
pubmed: 16815481
doi: 10.1016/j.neuropharm.2006.05.022
Granger, A. J. & Nicoll, R. A. LTD expression is independent of glutamate receptor subtype. Front. Synaptic Neurosci. 6, 15 (2014).
pubmed: 25071549
pmcid: 4086023
doi: 10.3389/fnsyn.2014.00015
Sanderson, T. M. Molecular mechanisms involved in depotentiation and their relevance to schizophrenia. Chonnam Med. J. 48, 1–6 (2012).
pubmed: 22570808
pmcid: 3341431
doi: 10.4068/cmj.2012.48.1.1
Man, H.-Y., Sekine-Aizawa, Y. & Huganir, R. L. Regulation of {alpha}-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor trafficking through PKA phosphorylation of the Glu receptor 1 subunit. Proc. Natl Acad. Sci. USA 104, 3579–3584 (2007).
pubmed: 17360685
pmcid: 1805611
doi: 10.1073/pnas.0611698104
Aston-Jones, G. & Bloom, F. E. Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J. Neurosci. 1, 876–886 (1981).
pubmed: 7346592
pmcid: 6564235
doi: 10.1523/JNEUROSCI.01-08-00876.1981
Nitz, D. & Siegel, J. M. GABA release in the locus coeruleus as a function of sleep/wake state. Neuroscience 78, 795–801 (1997).
pubmed: 9153658
doi: 10.1016/S0306-4522(96)00549-0
Maquet, P. et al. Functional neuroanatomy of human rapid-eye-movement sleep and dreaming. Nature 383, 163–166 (1996).
pubmed: 8774879
doi: 10.1038/383163a0
Braun, A. R. et al. Regional cerebral blood flow throughout the sleep-wake cycle. An H2(15)O PET study. Brain 120, 1173–1197 (1997).
pubmed: 9236630
doi: 10.1093/brain/120.7.1173
Nofzinger, E. A. et al. Human regional cerebral glucose metabolism during non-rapid eye movement sleep in relation to waking. Brain 125, 1105–1115 (2002).
pubmed: 11960899
doi: 10.1093/brain/awf103
Pace-Schott, E. F. & Hobson, J. A. The neurobiology of sleep: genetics, cellular physiology and subcortical networks. Nat. Rev. Neurosci. 3, 591–605 (2002).
pubmed: 12154361
doi: 10.1038/nrn895
Hasselmo, M. E. Neuromodulation: acetylcholine and memory consolidation. Trends Cogn. Sci. 3, 351–359 (1999).
pubmed: 10461198
doi: 10.1016/S1364-6613(99)01365-0
Clemens, Z. et al. Fine-tuned coupling between human parahippocampal ripples and sleep spindles. Eur. J. Neurosci. 33, 511–520 (2011).
pubmed: 21138489
doi: 10.1111/j.1460-9568.2010.07505.x
Purcell, S. M. et al. Characterizing sleep spindles in 11,630 individuals from the National Sleep Research Resource. Nat. Commun. 8, 15930 (2017).
pubmed: 28649997
pmcid: 5490197
doi: 10.1038/ncomms15930
Fernandez, L. M. J. & Lüthi, A. Sleep spindles: mechanisms and functions. Physiol. Rev. 100, 805–868 (2020).
pubmed: 31804897
doi: 10.1152/physrev.00042.2018
Kim, J., Gulati, T. & Ganguly, K. Competing roles of slow oscillations and delta waves in memory consolidation versus forgetting. Cell 179, 514–526.e13 (2019).
pubmed: 31585085
pmcid: 6779327
doi: 10.1016/j.cell.2019.08.040
Cox, R., Mylonas, D. S., Manoach, D. S. & Stickgold, R. Large-scale structure and individual fingerprints of locally coupled sleep oscillations. Sleep 41, zsy175 (2018).
pubmed: 30184179
pmcid: 6289240
doi: 10.1093/sleep/zsy175
Dehnavi, F., Koo-Poeggel, P. C., Ghorbani, M. & Marshall, L. Spontaneous slow oscillation-slow spindle features predict induced overnight memory retention. Sleep 44, zsab127 (2021).
pubmed: 34003291
pmcid: 8503833
doi: 10.1093/sleep/zsab127
McCormick, D. A. & Prince, D. A. Noradrenergic modulation of firing pattern in guinea pig and cat thalamic neurons, in vitro. J. Neurophysiol. 59, 978–996 (1988).
pubmed: 3367206
doi: 10.1152/jn.1988.59.3.978
Lee, K. H. & McCormick, D. A. Abolition of spindle oscillations by serotonin and norepinephrine in the ferret lateral geniculate and perigeniculate nuclei in vitro. Neuron 17, 309–321 (1996).
pubmed: 8780654
doi: 10.1016/S0896-6273(00)80162-2
Kjaerby, C. et al. Reply to: “Do all norepinephrine surges disrupt sleep?”. Nat. Neurosci. 26, 957–958 (2023).
pubmed: 37081298
doi: 10.1038/s41593-023-01314-7
Eschenko, O., Magri, C., Panzeri, S. & Sara, S. J. Noradrenergic neurons of the locus coeruleus are phase locked to cortical up-down states during sleep. Cereb. Cortex 22, 426–435 (2012).
pubmed: 21670101
doi: 10.1093/cercor/bhr121
Brodt, S., Inostroza, M., Niethard, N. & Born, J. Sleep — a brain-state serving systems memory consolidation. Neuron 111, 1050–1075 (2023).
pubmed: 37023710
doi: 10.1016/j.neuron.2023.03.005
Hutchison, I. C. & Rathore, S. The role of REM sleep theta activity in emotional memory. Front. Psychol. 6, 1439 (2015).
pubmed: 26483709
pmcid: 4589642
doi: 10.3389/fpsyg.2015.01439
Karashima, A. et al. Synchronization between hippocampal theta waves and PGO waves during REM sleep. Psychiatry Clin. Neurosci. 55, 189–190 (2001).
pubmed: 11422836
doi: 10.1046/j.1440-1819.2001.00820.x
Karashima, A., Nakao, M., Katayama, N. & Honda, K. Instantaneous acceleration and amplification of hippocampal theta wave coincident with phasic pontine activities during REM sleep. Brain Res. 1051, 50–56 (2005).
pubmed: 15982642
doi: 10.1016/j.brainres.2005.05.055
Karashima, A., Katayama, N. & Nakao, M. Enhancement of synchronization between hippocampal and amygdala theta waves associated with pontine wave density. J. Neurophysiol. 103, 2318–2325 (2010).
pubmed: 20164402
doi: 10.1152/jn.00551.2009
Lesting, J. et al. Patterns of coupled theta activity in amygdala-hippocampal-prefrontal cortical circuits during fear extinction. PloS ONE 6, e21714 (2011).
pubmed: 21738775
pmcid: 3125298
doi: 10.1371/journal.pone.0021714
Lesting, J. et al. Directional theta coherence in prefrontal cortical to amygdalo-hippocampal pathways signals fear extinction. PloS ONE 8, e77707 (2013). This paper reports that proper extinction memory recall results from theta oscillation coherence between the CA1 and amygdala that is phase locked to that of the mPFC. Rapid extinction learning occurred when the hippocampus and amygdala were anti-phase coupled.
pubmed: 24204927
pmcid: 3812006
doi: 10.1371/journal.pone.0077707
Totty, M. S., Chesney, L. A., Geist, P. A. & Datta, S. Sleep-dependent oscillatory synchronization: a role in fear memory consolidation. Front. Neural Circuits 11, 49 (2017).
pubmed: 28729826
pmcid: 5498516
doi: 10.3389/fncir.2017.00049
Datta, S., Saha, S., Prutzman, S. L., Mullins, O. J. & Mavanji, V. Pontine-wave generator activation-dependent memory processing of avoidance learning involves the dorsal hippocampus in the rat. J. Neurosci. Res. 80, 727–737 (2005).
pubmed: 15880522
pmcid: 1224707
doi: 10.1002/jnr.20501
Aime, M. et al. Paradoxical somatodendritic decoupling supports cortical plasticity during REM sleep. Science 376, 724–730 (2022). This series of studies demonstrates a REM sleep-specific amplification of distal dendrite activity in the prefrontal cortex at the same time that the perisomatic area of the same cells is silent — a process involving changed interneuronal activity levels which, when perturbed, prevent normal consolidation of emotional memories.
pubmed: 35549430
doi: 10.1126/science.abk2734
Brécier, A., Borel, M., Urbain, N. & Gentet, L. J. Vigilance and behavioral state-dependent modulation of cortical neuronal activity throughout the sleep/wake cycle. J. Neurosci. 42, 4852–4866 (2022).
pubmed: 35552234
pmcid: 9188387
doi: 10.1523/JNEUROSCI.1400-21.2022
Niethard, N., Ngo, H.-V. V., Ehrlich, I. & Born, J. Cortical circuit activity underlying sleep slow oscillations and spindles. Proc. Natl Acad. Sci. USA 115, E9220–E9229 (2018).
pubmed: 30209214
pmcid: 6166829
doi: 10.1073/pnas.1805517115
Niethard, N., Brodt, S. & Born, J. Cell-type-specific dynamics of calcium activity in cortical circuits over the course of slow-wave sleep and rapid eye movement sleep. J. Neurosci. 41, 4212–4222 (2021).
pubmed: 33833082
pmcid: 8143210
doi: 10.1523/JNEUROSCI.1957-20.2021
Katona, L. et al. Sleep and movement differentiates actions of two types of somatostatin-expressing GABAergic interneuron in rat hippocampus. Neuron 82, 872–886 (2014).
pubmed: 24794095
pmcid: 4041064
doi: 10.1016/j.neuron.2014.04.007
Kjaerby, C. et al. Memory-enhancing properties of sleep depend on the oscillatory amplitude of norepinephrine. Nat. Neurosci. 25, 1059–1070 (2022).
Havekes, R. & Aton, S. J. Impacts of sleep loss versus waking experience on brain plasticity: parallel or orthogonal? Trends Neurosci. 43, 385–393 (2020).
pubmed: 32459991
pmcid: 7505037
doi: 10.1016/j.tins.2020.03.010
Maret, S., Faraguna, U., Nelson, A. B., Cirelli, C. & Tononi, G. Sleep and waking modulate spine turnover in the adolescent mouse cortex. Nat. Neurosci. 14, 1418–1420 (2011).
pubmed: 21983682
pmcid: 3203346
doi: 10.1038/nn.2934
de Vivo, L. et al. Ultrastructural evidence for synaptic scaling across the wake/sleep cycle. Science 355, 507–510 (2017).
pubmed: 28154076
pmcid: 5313037
doi: 10.1126/science.aah5982
Vyazovskiy, V. V., Cirelli, C., Pfister-Genskow, M., Faraguna, U. & Tononi, G. Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat. Neurosci. 11, 200–208 (2008).
pubmed: 18204445
doi: 10.1038/nn2035
Diering, G. H. et al. Homer1a drives homeostatic scaling-down of excitatory synapses during sleep. Science 355, 511–515 (2017).
pubmed: 28154077
pmcid: 5382711
doi: 10.1126/science.aai8355
Diering, G. H. Remembering and forgetting in sleep: selective synaptic plasticity during sleep driven by scaling factors Homer1a and Arc. Neurobiol. Stress 22, 100512 (2023).
pubmed: 36632309
doi: 10.1016/j.ynstr.2022.100512
Miyamoto, D., Marshall, W., Tononi, G. & Cirelli, C. Net decrease in spine-surface GluA1-containing AMPA receptors after post-learning sleep in the adult mouse cortex. Nat. Commun. 12, 2881 (2021). This paper reveals that those synapses that are potentiated the most by learning are also least inclined to be weakened during sleep.
pubmed: 34001888
pmcid: 8129120
doi: 10.1038/s41467-021-23156-2
Yang, G. et al. Sleep promotes branch-specific formation of dendritic spines after learning. Science 344, 1173–1178 (2014). This paper shows that cortical neurons that are activated during a learning task are reactivated during REM sleep, and that this reactivation is crucial for maintaining the newly formed spines at these neurons.
pubmed: 24904169
pmcid: 4447313
doi: 10.1126/science.1249098
Seibt, J. et al. Cortical dendritic activity correlates with spindle-rich oscillations during sleep in rodents. Nat. Commun. 8, 684 (2017).
pubmed: 28947770
pmcid: 5612962
doi: 10.1038/s41467-017-00735-w
Feld, G. B., Lange, T., Gais, S. & Born, J. Sleep-dependent declarative memory consolidation — unaffected after blocking NMDA or AMPA receptors but enhanced by NMDA coagonist D-cycloserine. Neuropsychopharmacology 38, 2688–2697 (2013).
pubmed: 23887151
pmcid: 3828540
doi: 10.1038/npp.2013.179
Gisabella, B., Scammell, T., Bandaru, S. S. & Saper, C. B. Regulation of hippocampal dendritic spines following sleep deprivation. J. Comp. Neurol. 528, 380–388 (2020).
pubmed: 31454077
doi: 10.1002/cne.24764
Bolsius, Y. G., Meerlo, P., Kas, M. J., Abel, T. & Havekes, R. Sleep deprivation reduces the density of individual spine subtypes in a branch-specific fashion in CA1 neurons. J. Sleep Res. 31, e13438 (2022).
pubmed: 34263991
doi: 10.1111/jsr.13438
Varela, C. & Wilson, M. A. mPFC spindle cycles organize sparse thalamic activation and recently active CA1 cells during non-REM sleep. eLife 9, e48881 (2020).
pubmed: 32525480
pmcid: 7319772
doi: 10.7554/eLife.48881
Mavanji, V. & Datta, S. Activation of the phasic pontine-wave generator enhances improvement of learning performance: a mechanism for sleep-dependent plasticity. Eur. J. Neurosci. 17, 359–370 (2003).
pubmed: 12542673
doi: 10.1046/j.1460-9568.2003.02460.x
Tsunematsu, T., Patel, A. A., Onken, A. & Sakata, S. State-dependent brainstem ensemble dynamics and their interactions with hippocampus across sleep states. eLife 9, e52244 (2020).
pubmed: 31934862
pmcid: 6996931
doi: 10.7554/eLife.52244
Shin, J. N., Doron, G. & Larkum, M. E. Memories off the top of your head. Science 374, 538–539 (2021).
pubmed: 34709915
pmcid: 7612398
doi: 10.1126/science.abk1859
Palacios-Filardo, J. & Mellor, J. R. Neuromodulation of hippocampal long-term synaptic plasticity. Curr. Opin. Neurobiol. 54, 37–43 (2019).
pubmed: 30212713
pmcid: 6367596
doi: 10.1016/j.conb.2018.08.009
Nakauchi, S., Brennan, R. J., Boulter, J. & Sumikawa, K. Nicotine gates long-term potentiation in the hippocampal CA1 region via the activation of alpha2* nicotinic ACh receptors. Eur. J. Neurosci. 25, 2666–2681 (2007).
pubmed: 17466021
doi: 10.1111/j.1460-9568.2007.05513.x
Delorme, J. et al. Sleep loss drives acetylcholine- and somatostatin interneuron-mediated gating of hippocampal activity to inhibit memory consolidation. Proc. Natl Acad. Sci. USA 118, e2019318118 (2021).
pubmed: 34344824
pmcid: 8364159
doi: 10.1073/pnas.2019318118
Soulé, J. et al. Balancing Arc synthesis, mRNA decay, and proteasomal degradation: maximal protein expression triggered by rapid eye movement sleep-like bursts of muscarinic cholinergic receptor stimulation. J. Biol. Chem. 287, 22354–22366 (2012).
pubmed: 22584581
pmcid: 3381195
doi: 10.1074/jbc.M112.376491
Stefanelli, T., Bertollini, C., Lüscher, C., Muller, D. & Mendez, P. Hippocampal somatostatin interneurons control the size of neuronal memory ensembles. Neuron 89, 1074–1085 (2016).
pubmed: 26875623
doi: 10.1016/j.neuron.2016.01.024
Dannenberg, H., Young, K. & Hasselmo, M. Modulation of hippocampal circuits by muscarinic and nicotinic receptors. Front. Neural Circuits 11, 102 (2017).
pubmed: 29321728
pmcid: 5733553
doi: 10.3389/fncir.2017.00102
Rexrode, L. et al. Regulation of dendritic spines in the amygdala following sleep deprivation. Front. Sleep 2, 1145203 (2023).
pubmed: 37928499
pmcid: 10624159
doi: 10.3389/frsle.2023.1145203
Van Someren, E. J. W. Brain mechanisms of insomnia: new perspectives on causes and consequences. Physiol. Rev. 101, 995–1046 (2021).
pubmed: 32790576
doi: 10.1152/physrev.00046.2019
Bröcher, S., Artola, A. & Singer, W. Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex. Brain Res. 573, 27–36 (1992).
pubmed: 1349501
doi: 10.1016/0006-8993(92)90110-U
Suzuki, A., Yanagisawa, M. & Greene, R. W. Loss of Arc attenuates the behavioral and molecular responses for sleep homeostasis in mice. Proc. Natl Acad. Sci. USA 117, 10547–10553 (2020).
pubmed: 32350140
pmcid: 7229651
doi: 10.1073/pnas.1906840117
Poe, G. R., Nitz, D. A., McNaughton, B. L. & Barnes, C. A. Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res. 855, 176–180 (2000).
pubmed: 10650147
doi: 10.1016/S0006-8993(99)02310-0
Ramirez-Villegas, J. F. et al. Coupling of hippocampal theta and ripples with pontogeniculooccipital waves. Nature 589, 96–102 (2021).
pubmed: 33208951
doi: 10.1038/s41586-020-2914-4
Booth, V. & Poe, G. R. Input source and strength influences overall firing phase of model hippocampal CA1 pyramidal cells during theta: relevance to REM sleep reactivation and memory consolidation. Hippocampus 16, 161–173 (2006). This paper shows how the consolidation process of strengthening the familiarity-encoding temporoammonic distal hippocampal dendrites can cause CA1 neurons to fire at proximal theta troughs which, through spike timing-dependent plasticity, invokes depotentiation at novelty-encoding proximal dendrites.
pubmed: 16411243
pmcid: 1401491
doi: 10.1002/hipo.20143
Buzsáki, G. Theta oscillations in the hippocampus. Neuron 33, 325–340 (2002).
pubmed: 11832222
doi: 10.1016/S0896-6273(02)00586-X
Bi, G. Q. & Poo, M. M. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18, 10464–10472 (1998).
pubmed: 9852584
pmcid: 6793365
doi: 10.1523/JNEUROSCI.18-24-10464.1998
Grella, S. L. et al. Locus coeruleus phasic, but not tonic, activation initiates global remapping in a familiar environment. J. Neurosci. 39, 445–455 (2019).
pubmed: 30478033
pmcid: 6335751
doi: 10.1523/JNEUROSCI.1956-18.2018
Andrade, K. C. et al. Sleep spindles and hippocampal functional connectivity in human NREM sleep. J. Neurosci. 31, 10331–10339 (2011).
pubmed: 21753010
pmcid: 6623055
doi: 10.1523/JNEUROSCI.5660-10.2011
Buzsáki, G. Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus 25, 1073–1188 (2015).
pubmed: 26135716
pmcid: 4648295
doi: 10.1002/hipo.22488
Cox, R., Rüber, T., Staresina, B. P. & Fell, J. Sharp wave-ripples in human amygdala and their coordination with hippocampus during NREM sleep. Cereb. Cortex Commun. 1, tgaa051 (2020).
pubmed: 33015623
pmcid: 7521160
doi: 10.1093/texcom/tgaa051
Kim, W. B. & Cho, J.-H. Synaptic targeting of double-projecting ventral CA1 hippocampal neurons to the medial prefrontal cortex and basal amygdala. J. Neurosci. 37, 4868–4882 (2017).
pubmed: 28385873
pmcid: 6596479
doi: 10.1523/JNEUROSCI.3579-16.2017
Li, W., Ma, L., Yang, G. & Gan, W.-B. REM sleep selectively prunes and maintains new synapses in development and learning. Nat. Neurosci. 20, 427–437 (2017).
pubmed: 28092659
pmcid: 5535798
doi: 10.1038/nn.4479
Zhou, Y. et al. REM sleep promotes experience-dependent dendritic spine elimination in the mouse cortex. Nat. Commun. 11, 4819 (2020). This paper demonstrates that experience-dependent structural plasticity takes place during REM sleep in cortical neurons.
pubmed: 32968048
pmcid: 7511313
doi: 10.1038/s41467-020-18592-5
Popa, D., Duvarci, S., Popescu, A. T., Léna, C. & Paré, D. Coherent amygdalocortical theta promotes fear memory consolidation during paradoxical sleep. Proc. Natl Acad. Sci. USA 107, 6516–6519 (2010).
pubmed: 20332204
pmcid: 2851973
doi: 10.1073/pnas.0913016107
Gais, S. et al. Sleep transforms the cerebral trace of declarative memories. Proc. Natl Acad. Sci. USA 104, 18778–18783 (2007).
pubmed: 18000060
pmcid: 2141853
doi: 10.1073/pnas.0705454104
Sterpenich, V. et al. Sleep-related hippocampo-cortical interplay during emotional memory recollection. PloS Biol. 5, e282 (2007).
pubmed: 17958471
pmcid: 2039770
doi: 10.1371/journal.pbio.0050282
van der Helm, E. et al. REM sleep depotentiates amygdala activity to previous emotional experiences. Curr. Biol. 21, 2029–2032 (2011).
pubmed: 22119526
pmcid: 3237718
doi: 10.1016/j.cub.2011.10.052
Motomura, Y. et al. Sleep debt elicits negative emotional reaction through diminished amygdala-anterior cingulate functional connectivity. PloS ONE 8, e56578 (2013).
pubmed: 23418586
pmcid: 3572063
doi: 10.1371/journal.pone.0056578
Sollenberger, N. A. et al. Sleep fails to depotentiate amygdala-reactivity to negative emotional stimuli in youth with elevated symptoms of anxiety. Cogn. Affect. Behav. Neurosci. 23, 415–426 (2023).
pubmed: 36788201
doi: 10.3758/s13415-023-01066-8
Sterpenich, V. et al. Sleep promotes the neural reorganization of remote emotional memory. J. Neurosci. 29, 5143–5152 (2009).
pubmed: 19386910
pmcid: 6665458
doi: 10.1523/JNEUROSCI.0561-09.2009
Yoo, S.-S., Gujar, N., Hu, P., Jolesz, F. A. & Walker, M. P. The human emotional brain without sleep — a prefrontal amygdala disconnect. Curr. Biol. 17, R877–R878 (2007).
pubmed: 17956744
doi: 10.1016/j.cub.2007.08.007
Nowak, J. et al. Association of naturally occurring sleep loss with reduced amygdala resting-state functional connectivity following psychosocial stress. Psychoneuroendocrinology 114, 104585 (2020).
pubmed: 32018119
doi: 10.1016/j.psyneuen.2020.104585
Gilson, M. et al. REM-enriched naps are associated with memory consolidation for sad stories and enhance mood-related reactivity. Brain Sci. 6, 1 (2015).
pubmed: 26729175
pmcid: 4810171
doi: 10.3390/brainsci6010001
Werner, G. G., Schabus, M., Blechert, J., Kolodyazhniy, V. & Wilhelm, F. H. Pre- to postsleep change in psychophysiological reactivity to emotional films: late-night REM sleep is associated with attenuated emotional processing. Psychophysiology 52, 813–825 (2015).
pubmed: 25588962
doi: 10.1111/psyp.12404
Cunningham, T. J. et al. Psychophysiological arousal at encoding leads to reduced reactivity but enhanced emotional memory following sleep. Neurobiol. Learn. Mem. 114, 155–164 (2014).
pubmed: 24952130
doi: 10.1016/j.nlm.2014.06.002
Reinhold, F. L., Gerlicher, A. M. V., van Someren, E. J. W. & Kindt, M. Do your troubles today seem further away than yesterday? On sleep’s role in mitigating the blushing response to a reactivated embarrassing episode. Sleep 45, zsac220 (2022).
pubmed: 36130113
pmcid: 9644119
doi: 10.1093/sleep/zsac220
Jones, B. J. & Spencer, R. M. C. Sleep preserves subjective and sympathetic emotional response of memories. Neurobiol. Learn. Mem. 166, 107096 (2019).
pubmed: 31585163
pmcid: 7927201
doi: 10.1016/j.nlm.2019.107096
Pace-Schott, E. F. et al. Napping promotes inter-session habituation to emotional stimuli. Neurobiol. Learn. Mem. 95, 24–36 (2011).
pubmed: 20969968
doi: 10.1016/j.nlm.2010.10.006
Werner, G. G., Schabus, M., Blechert, J. & Wilhelm, F. H. Differential effects of REM sleep on emotional processing: initial evidence for increased short-term emotional responses and reduced long-term intrusive memories. Behav. Sleep Med. 19, 83–98 (2021).
pubmed: 31971007
doi: 10.1080/15402002.2020.1713134
Pesonen, A.-K. et al. Presleep physiological stress is associated with a higher cortical arousal in sleep and more consolidated REM sleep. Stress 24, 667–675 (2021).
pubmed: 33461366
doi: 10.1080/10253890.2020.1869936
Spoormaker, V. I., Gvozdanovic, G. A., Sämann, P. G. & Czisch, M. Ventromedial prefrontal cortex activity and rapid eye movement sleep are associated with subsequent fear expression in human subjects. Exp. Brain Res. 232, 1547–1554 (2014).
pubmed: 24452776
doi: 10.1007/s00221-014-3831-2
van Marle, H. J. F., Hermans, E. J., Qin, S., Overeem, S. & Fernández, G. The effect of exogenous cortisol during sleep on the behavioral and neural correlates of emotional memory consolidation in humans. Psychoneuroendocrinology 38, 1639–1649 (2013).
pubmed: 23484632
doi: 10.1016/j.psyneuen.2013.01.009
Beck, J., Loretz, E. & Rasch, B. Stress dynamically reduces sleep depth: temporal proximity to the stressor is crucial. Cereb. Cortex 33, 96–113 (2022).
pubmed: 35196708
pmcid: 9758584
doi: 10.1093/cercor/bhac055
Riemann, D. et al. REM sleep instability — a new pathway for insomnia? Pharmacopsychiatry 45, 167–176 (2012). This paper first describes REM sleep instability in insomnia as a transdiagnostic risk factor for disturbed emotion regulation and mental health problems.
pubmed: 22290199
Germain, A. Sleep disturbances as the hallmark of PTSD: where are we now? Am. J. Psychiatry 170, 372–382 (2013).
pubmed: 23223954
pmcid: 4197954
doi: 10.1176/appi.ajp.2012.12040432
Pesonen, A.-K. et al. REM sleep fragmentation associated with depressive symptoms and genetic risk for depression in a community-based sample of adolescents. J. Affect. Disord. 245, 757–763 (2019).
pubmed: 30448760
doi: 10.1016/j.jad.2018.11.077
Galbiati, A. et al. The association between emotional dysregulation and REM sleep features in insomnia disorder. Brain Cogn. 146, 105642 (2020).
pubmed: 33190030
doi: 10.1016/j.bandc.2020.105642
Halonen, R., Kuula, L., Makkonen, T., Kauramäki, J. & Pesonen, A.-K. Self-conscious affect is modulated by rapid eye movement sleep but not by targeted memory reactivation — a pilot study. Front. Psychol. 12, 730924 (2021).
pubmed: 34966319
pmcid: 8710454
doi: 10.3389/fpsyg.2021.730924
Bottary, R. et al. Fear extinction memory is negatively associated with REM sleep in insomnia disorder. Sleep 43, zsaa007 (2020).
pubmed: 31993652
pmcid: 7355402
doi: 10.1093/sleep/zsaa007
Seo, J. et al. Delayed fear extinction in individuals with insomnia disorder. Sleep 41, zsy095 (2018).
pubmed: 29860407
pmcid: 6093425
doi: 10.1093/sleep/zsy095
Insana, S. P., Kolko, D. J. & Germain, A. Early-life trauma is associated with rapid eye movement sleep fragmentation among military veterans. Biol. Psychol. 89, 570–579 (2012).
pubmed: 22266135
pmcid: 3299844
doi: 10.1016/j.biopsycho.2012.01.001
Mellman, T. A., Bustamante, V., Fins, A. I., Pigeon, W. R. & Nolan, B. REM sleep and the early development of posttraumatic stress disorder. Am. J. Psychiatry 159, 1696–1701 (2002).
pubmed: 12359675
doi: 10.1176/appi.ajp.159.10.1696
Mellman, T. A., Pigeon, W. R., Nowell, P. D. & Nolan, B. Relationships between REM sleep findings and PTSD symptoms during the early aftermath of trauma. J. Trauma. Stress. 20, 893–901 (2007).
pubmed: 17955526
doi: 10.1002/jts.20246
Cowdin, N., Kobayashi, I. & Mellman, T. A. Theta frequency activity during rapid eye movement (REM) sleep is greater in people with resilience versus PTSD. Exp. Brain Res. 232, 1479–1485 (2014).
pubmed: 24531640
pmcid: 4449337
doi: 10.1007/s00221-014-3857-5
Gong, L. et al. The abnormal functional connectivity in the locus coeruleus-norepinephrine system associated with anxiety symptom in chronic insomnia disorder. Front. Neurosci. 15, 678465 (2021). This paper has found direct evidence for the links between altered functional connectivity between the LC and salience network in insomnia and clinically relevant anxiety.
pubmed: 34093121
pmcid: 8175797
doi: 10.3389/fnins.2021.678465
Talamini, L. M., Bringmann, L. F., de Boer, M. & Hofman, W. F. Sleeping worries away or worrying away sleep? Physiological evidence on sleep-emotion interactions. PloS ONE 8, e62480 (2013).
pubmed: 23671601
pmcid: 3641038
doi: 10.1371/journal.pone.0062480
Cellini, N., Mercurio, M. & Sarlo, M. The fate of emotional memories over a week: does sleep play any role? Front. Psychol. 10, 481 (2019).
pubmed: 30890991
pmcid: 6411793
doi: 10.3389/fpsyg.2019.00481
Gujar, N., McDonald, S. A., Nishida, M. & Walker, M. P. A role for REM sleep in recalibrating the sensitivity of the human brain to specific emotions. Cereb. Cortex 21, 115–123 (2011).
pubmed: 20421251
doi: 10.1093/cercor/bhq064
Kleim, B. et al. Sleep enhances exposure therapy. Psychol. Med. 44, 1511–1519 (2014).
pubmed: 23842278
doi: 10.1017/S0033291713001748
Wassing, R., Benjamins, J. S., Talamini, L. M., Schalkwijk, F. & Van Someren, E. J. W. Overnight worsening of emotional distress indicates maladaptive sleep in insomnia. Sleep 42, zsz051 (2019).
Baran, B., Pace-Schott, E. F., Ericson, C. & Spencer, R. M. C. Processing of emotional reactivity and emotional memory over sleep. J. Neurosci. 32, 1035–1042 (2012).
pubmed: 22262901
pmcid: 3548452
doi: 10.1523/JNEUROSCI.2532-11.2012
Tempesta, D., De Gennaro, L., Natale, V. & Ferrara, M. Emotional memory processing is influenced by sleep quality. Sleep. Med. 16, 862–870 (2015).
pubmed: 26008959
doi: 10.1016/j.sleep.2015.01.024
Harrington, M. O., Nedberge, K. M. & Durrant, S. J. The effect of sleep deprivation on emotional memory consolidation in participants reporting depressive symptoms. Neurobiol. Learn. Mem. 152, 10–19 (2018).
pubmed: 29709569
doi: 10.1016/j.nlm.2018.04.013
Lau, E. Y. Y. et al. Effects of REM sleep during a daytime nap on emotional perception in individuals with and without depression. J. Affect. Disord. 260, 687–694 (2020).
pubmed: 31550615
doi: 10.1016/j.jad.2019.09.058
Zeng, S., Lin, X., Wang, J. & Hu, X. Sleep’s short-term memory preservation and long-term affect depotentiation effect in emotional memory consolidation: behavioral and EEG evidence. Sleep 44, zsab155 (2021).
pubmed: 34153105
doi: 10.1093/sleep/zsab155
Davidson, P. & Pace-Schott, E. Go to bed and you MIGHT feel better in the morning — the effect of sleep on affective tone and intrusiveness of emotional memories. Curr. Sleep Med. Rep. 7, 31–46 (2021).
doi: 10.1007/s40675-020-00200-z
Etkin, A., Büchel, C. & Gross, J. J. The neural bases of emotion regulation. Nat. Rev. Neurosci. 16, 693–700 (2015).
pubmed: 26481098
doi: 10.1038/nrn4044
Wiesner, C. D. et al. The effect of selective REM-sleep deprivation on the consolidation and affective evaluation of emotional memories. Neurobiol. Learn. Mem. 122, 131–141 (2015).
pubmed: 25708092
doi: 10.1016/j.nlm.2015.02.008
Wagner, U., Fischer, S. & Born, J. Changes in emotional responses to aversive pictures across periods rich in slow-wave sleep versus rapid eye movement sleep. Psychosom. Med. 64, 627–634 (2002).
pubmed: 12140353
Lara-Carrasco, J., Nielsen, T. A., Solomonova, E., Levrier, K. & Popova, A. Overnight emotional adaptation to negative stimuli is altered by REM sleep deprivation and is correlated with intervening dream emotions. J. Sleep Res. 18, 178–187 (2009).
pubmed: 19645964
doi: 10.1111/j.1365-2869.2008.00709.x
Greenberg, R., Pillard, R. & Pearlman, C. The effect of dream (stage REM) deprivation on adaptation to stress. Psychosom. Med. 34, 257–262 (1972).
pubmed: 4338295
doi: 10.1097/00006842-197205000-00007
Rosales-Lagarde, A. et al. Enhanced emotional reactivity after selective REM sleep deprivation in humans: an fMRI study. Front. Behav. Neurosci. 6, 25 (2012).
pubmed: 22719723
pmcid: 3376727
doi: 10.3389/fnbeh.2012.00025
Llewellyn, S. & Hobson, J. A. Not only … but also: REM sleep creates and NREM stage 2 instantiates landmark junctions in cortical memory networks. Neurobiol. Learn. Mem. 122, 69–87 (2015).
pubmed: 25921620
doi: 10.1016/j.nlm.2015.04.005
Cairney, S. A., Durrant, S. J., Power, R. & Lewis, P. A. Complementary roles of slow-wave sleep and rapid eye movement sleep in emotional memory consolidation. Cereb. Cortex 25, 1565–1575 (2015).
pubmed: 24408956
doi: 10.1093/cercor/bht349
Rihm, J. S. & Rasch, B. Replay of conditioned stimuli during late REM and stage N2 sleep influences affective tone rather than emotional memory strength. Neurobiol. Learn. Mem. 122, 142–151 (2015).
pubmed: 25933506
doi: 10.1016/j.nlm.2015.04.008
Hutchison, I. C. et al. Targeted memory reactivation in REM but not SWS selectively reduces arousal responses. Commun. Biol. 4, 404 (2021). This paper shows that targeted memory reactivation during REM sleep enhances overnight adaptation in subjective arousal ratings to multisensory emotional stimuli.
pubmed: 33767319
pmcid: 7994443
doi: 10.1038/s42003-021-01854-3
Xia, T. et al. Updating memories of unwanted emotions during human sleep. Curr. Biol. 33, 309–320.e5 (2023).
pubmed: 36584677
doi: 10.1016/j.cub.2022.12.004
Groch, S. et al. Targeted reactivation during sleep differentially affects negative memories in socially anxious and healthy children and adolescents. J. Neurosci. 37, 2425–2434 (2017).
pubmed: 28143960
pmcid: 6596843
doi: 10.1523/JNEUROSCI.1912-16.2017
Pereira, S. I. R. et al. Cueing emotional memories during slow wave sleep modulates next-day activity in the orbitofrontal cortex and the amygdala. NeuroImage 253, 119120 (2022).
pubmed: 35331867
doi: 10.1016/j.neuroimage.2022.119120
Borghese, F. et al. Targeted memory reactivation during REM sleep in patients with social anxiety disorder. Front. Psychiatry 13, 904704 (2022).
pubmed: 35845468
pmcid: 9281560
doi: 10.3389/fpsyt.2022.904704
Hauner, K. K., Howard, J. D., Zelano, C. & Gottfried, J. A. Stimulus-specific enhancement of fear extinction during slow-wave sleep. Nat. Neurosci. 16, 1553–1555 (2013).
pubmed: 24056700
pmcid: 3818116
doi: 10.1038/nn.3527
Spencer, R. L. & Bland, S. T. in Stress: Physiology, Biochemistry, and Pathology (ed. Fink, G.) 57–68 (Academic, 2019).