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Memory corticalization triggered by REM sleep: mechanisms of cellular and systems consolidation

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Abstract

Once viewed as a passive physiological state, sleep is a heterogeneous and complex sequence of brain states with essential effects on synaptic plasticity and neuronal functioning. Rapid-eye-movement (REM) sleep has been shown to promote calcium-dependent plasticity in principal neurons of the cerebral cortex, both during memory consolidation in adults and during post-natal development. This article reviews the plasticity mechanisms triggered by REM sleep, with a focus on the emerging role of kinases and immediate-early genes for the progressive corticalization of hippocampus-dependent memories. The body of evidence suggests that memory corticalization triggered by REM sleep is a systemic phenomenon with cellular and molecular causes.

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References

  1. Hebb DO (1949) The organization of behavior: a neuropsychological theory. Wiley, New York

    Google Scholar 

  2. Squire LR (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99(2):195–231. https://doi.org/10.1037//0033-295x.99.2.195

    Article  CAS  PubMed  Google Scholar 

  3. McGaugh JL (2000) Memory—a century of consolidation. Science 287(5451):248–251

    Article  CAS  Google Scholar 

  4. Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55:51–86. https://doi.org/10.1146/annurev.psych.55.090902.142050

    Article  PubMed  Google Scholar 

  5. Wang H, Hu Y, Tsien JZ (2006) Molecular and systems mechanisms of memory consolidation and storage. Prog Neurobiol 79(3):123–135. https://doi.org/10.1016/j.pneurobio.2006.06.004

    Article  CAS  PubMed  Google Scholar 

  6. Goelet P, Castellucci VF, Schacher S, Kandel ER (1986) The long and the short of long–term memory—a molecular framework. Nature 322(6078):419–422. https://doi.org/10.1038/322419a0

    Article  CAS  PubMed  Google Scholar 

  7. Nader K (2003) Memory traces unbound. Trends Neurosci 26(2):65–72. https://doi.org/10.1016/S0166-2236(02)00042-5

    Article  CAS  PubMed  Google Scholar 

  8. McClelland JL, McNaughton BL, O’Reilly RC (1995) Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 102(3):419–457

    Article  CAS  Google Scholar 

  9. Lavenex P, Amaral DG (2000) Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 10(4):420–430. https://doi.org/10.1002/1098-1063(2000)10:4<420::aid-hipo8>3.0.co;2-5

  10. Frankland PW, Bontempi B (2005) The organization of recent and remote memories. Nat Rev Neurosci 6(2):119–130. https://doi.org/10.1038/nrn1607

    Article  CAS  PubMed  Google Scholar 

  11. Nadel L, Moscovitch M (1997) Memory consolidation, retrograde amnesia and the hippocampal complex. Curr Opin Neurobiol 7(2):217–227

    Article  CAS  Google Scholar 

  12. Dudai Y, Karni A, Born J (2015) The consolidation and transformation of memory. Neuron 88(1):20–32. https://doi.org/10.1016/j.neuron.2015.09.004

    Article  CAS  PubMed  Google Scholar 

  13. Poe GR (2017) Sleep is for forgetting. J Neurosci 37(3):464–473. https://doi.org/10.1523/JNEUROSCI.0820-16.2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Richards BA, Frankland PW (2017) The persistence and transience of memory. Neuron 94(6):1071–1084. https://doi.org/10.1016/j.neuron.2017.04.037

    Article  CAS  PubMed  Google Scholar 

  15. Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20(1):11–21

    Article  CAS  Google Scholar 

  16. Anagnostaras SG, Gale GD, Fanselow MS (2001) Hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus 11(1):8–17. https://doi.org/10.1002/1098-1063(2001)11:1<8::aid-hipo1015>3.0.co;2-7

  17. Goshen I, Brodsky M, Prakash R, Wallace J, Gradinaru V, Ramakrishnan C, Deisseroth K (2011) Dynamics of retrieval strategies for remote memories. Cell 147(3):678–689. https://doi.org/10.1016/j.cell.2011.09.033

    Article  CAS  PubMed  Google Scholar 

  18. Kitamura T, Ogawa SK, Roy DS, Okuyama T, Morrissey MD, Smith LM, Redondo RL, Tonegawa S (2017) Engrams and circuits crucial for systems consolidation of a memory. Science 356(6333):73–78. https://doi.org/10.1126/science.aam6808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Nadel L, Hardt O (2011) Update on memory systems and processes. Neuropsychopharmacology 36(1):251–273. https://doi.org/10.1038/npp.2010.169

    Article  PubMed  Google Scholar 

  20. Kim JJ, Clark RE, Thompson RF (1995) Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav Neurosci 109(2):195–203. https://doi.org/10.1037//0735-7044.109.2.195

    Article  CAS  PubMed  Google Scholar 

  21. Izquierdo I, Medina JH (1997) Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol Learn Mem 68(3):285–316. https://doi.org/10.1006/nlme.1997.3799

    Article  CAS  PubMed  Google Scholar 

  22. Winocur G, McDonald RM, Moscovitch M (2001) Anterograde and retrograde amnesia in rats with large hippocampal lesions. Hippocampus 11(1):18–26. https://doi.org/10.1002/1098-1063(2001)11:1<18::aid-hipo1016>3.0.co;2-5

  23. Bontempi B, Laurent-Demir C, Destrade C, Jaffard R (1999) Time-dependent reorganization of brain circuitry underlying long-term memory storage. Nature 400(6745):671–675. https://doi.org/10.1038/23270

    Article  CAS  PubMed  Google Scholar 

  24. Brodt S, Pöhlchen D, Flanagin VL, Glasauer S, Gais S, Schönauer M (2016) Rapid and independent memory formation in the parietal cortex. Proc Natl Acad Sci USA 113(46):13251–13256. https://doi.org/10.1073/pnas.1605719113

    Article  CAS  PubMed  Google Scholar 

  25. Haist F, Bowden Gore J, Mao H (2001) Consolidation of human memory over decades revealed by functional magnetic resonance imaging. Nat Neurosci 4(11):1139–1145. https://doi.org/10.1038/nn739

    Article  CAS  PubMed  Google Scholar 

  26. Kim JJ, Jung MW (2006) Neural circuits and mechanisms involved in Pavlovian fear conditioning: a critical review. Neurosci Biobehav Rev 30(2):188–202. https://doi.org/10.1016/j.neubiorev.2005.06.005

    Article  PubMed  Google Scholar 

  27. Fanselow MS (1980) Conditioned and unconditional components of post-shock freezing. Pavlov J Biol Sci Off J Pavlov 15(4):177–182

    CAS  Google Scholar 

  28. Shimizu E, Tang YP, Rampon C, Tsien JZ (2000) NMDA receptor-dependent synaptic reinforcement as a crucial process for memory consolidation. Science 290(5494):1170–1174

    Article  CAS  Google Scholar 

  29. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44(1):5–21. https://doi.org/10.1016/j.neuron.2004.09.012

    Article  CAS  PubMed  Google Scholar 

  30. Larson J, Munkácsy E (2015) Theta-burst LTP. Brain Res 1621:38–50. https://doi.org/10.1016/j.brainres.2014.10.034

    Article  CAS  PubMed  Google Scholar 

  31. Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313(5790):1093–1097. https://doi.org/10.1126/science.1128134

    Article  CAS  PubMed  Google Scholar 

  32. Serrano P, Yao Y, Sacktor TC (2005) Persistent phosphorylation by protein kinase Mzeta maintains late-phase long-term potentiation. J Neurosci 25(8):1979–1984. https://doi.org/10.1523/JNEUROSCI.5132-04.2005

    Article  CAS  PubMed  Google Scholar 

  33. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC (2006) Storage of spatial information by the maintenance mechanism of LTP. Science 313(5790):1141–1144. https://doi.org/10.1126/science.1128657

    Article  CAS  PubMed  Google Scholar 

  34. Feldman DE, Nicoll RA, Malenka RC (1999) Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD, and silent synapses. J Neurobiol 41(1):92–101

    Article  CAS  Google Scholar 

  35. Rioult-Pedotti MS, Friedman D, Donoghue JP (2000) Learning-induced LTP in neocortex. Science 290(5491):533–536

    Article  CAS  Google Scholar 

  36. Rodríguez-Durán LF, Martínez-Moreno A, Escobar ML (2017) Bidirectional modulation of taste aversion extinction by insular cortex LTP and LTD. Neurobiol Learn Mem 142(Pt A):85–90. https://doi.org/10.1016/j.nlm.2016.12.014

    Article  PubMed  Google Scholar 

  37. Nabavi S, Fox R, Proulx CD, Lin JY, Tsien RY, Malinow R (2014) Engineering a memory with LTD and LTP. Nature 511(7509):348–352. https://doi.org/10.1038/nature13294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Volianskis A, France G, Jensen MS, Bortolotto ZA, Jane DE, Collingridge GL (2015) Long-term potentiation and the role of N-methyl-d-aspartate receptors. Brain Res 1621:5–16. https://doi.org/10.1016/j.brainres.2015.01.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Park P, Volianskis A, Sanderson TM, Bortolotto ZA, Jane DE, Zhuo M, Kaang B-K, Collingridge GL (2014) NMDA receptor-dependent long-term potentiation comprises a family of temporally overlapping forms of synaptic plasticity that are induced by different patterns of stimulation. Philos Trans R Soc Lond B Biol Sci 369(1633):20130131. https://doi.org/10.1098/rstb.2013.0131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Dore K, Aow J, Malinow R (2016) The emergence of NMDA receptor metabotropic function: insights from imaging. Front Synaptic Neurosci 8:20. https://doi.org/10.3389/fnsyn.2016.00020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Jones MW, Errington ML, French PJ, Fine A, Bliss TV, Garel S, Charnay P, Bozon B, Laroche S, Davis S (2001) A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 4(3):289–296. https://doi.org/10.1038/85138

    Article  CAS  PubMed  Google Scholar 

  42. Bozon B, Kelly A, Josselyn SA, Silva AJ, Davis S, Laroche S (2003) MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos Trans R Soc Lond B Biol Sci 358(1432):805–814. https://doi.org/10.1098/rstb.2002.1224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Davis S, Bozon B, Laroche S (2003) How necessary is the activation of the immediate early gene zif268 in synaptic plasticity and learning? Behav Brain Res 142(1–2):17–30

    Article  CAS  Google Scholar 

  44. Alberini CM (2008) The role of protein synthesis during the labile phases of memory: revisiting the skepticism. Neurobiol Learn Mem 89(3):234–246. https://doi.org/10.1016/j.nlm.2007.08.007

    Article  CAS  PubMed  Google Scholar 

  45. Nader K, Hardt O (2009) A single standard for memory: the case for reconsolidation. Nat Rev Neurosci 10(3):224–234. https://doi.org/10.1038/nrn2590

    Article  CAS  PubMed  Google Scholar 

  46. Rosenberg T, Gal-Ben-Ari S, Dieterich DC, Kreutz MR, Ziv NE, Gundelfinger ED, Rosenblum K (2014) The roles of protein expression in synaptic plasticity and memory consolidation. Front Mol Neurosci 7:86. https://doi.org/10.3389/fnmol.2014.00086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Gisquet-Verrier P, Lynch JF, Cutolo P, Toledano D, Ulmen A, Jasnow AM, Riccio DC (2015) Integration of new information with active memory accounts for retrograde amnesia: a challenge to the consolidation/reconsolidation hypothesis? J Neurosci 35(33):11623–11633. https://doi.org/10.1523/JNEUROSCI.1386-15.2015

    Article  CAS  PubMed  Google Scholar 

  48. Ryan TJ, Roy DS, Pignatelli M, Arons A, Tonegawa S (2015) Memory. Engram cells retain memory under retrograde amnesia. Science 348(6238):1007–1013. https://doi.org/10.1126/science.aaa5542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Lee JLC, Nader K, Schiller D (2017) An update on memory reconsolidation updating. Trends Cogn Sci 21(7):531–545. https://doi.org/10.1016/j.tics.2017.04.006

    Article  PubMed  PubMed Central  Google Scholar 

  50. Lisman J, Schulman H, Cline H (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3(3):175–190. https://doi.org/10.1038/nrn753

    Article  CAS  PubMed  Google Scholar 

  51. Achterberg KG, Buitendijk GH, Kool MJ, Goorden SM, Post L, Slump DE, Silva AJ, van Woerden GM, Kushner SA, Elgersma Y (2014) Temporal and region-specific requirements of αCaMKII in spatial and contextual learning. J Neurosci 34(34):11180–11187. https://doi.org/10.1523/JNEUROSCI.0640-14.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Wang H, Peng RY (2016) Basic roles of key molecules connected with NMDAR signaling pathway on regulating learning and memory and synaptic plasticity. Mil Med Res 3(1):26. https://doi.org/10.1186/s40779-016-0095-0

    Article  PubMed  PubMed Central  Google Scholar 

  53. Wang H, Shimizu E, Tang YP, Cho M, Kyin M, Zuo W, Robinson DA, Alaimo PJ, Zhang C, Morimoto H, Zhuo M, Feng R, Shokat KM, Tsien JZ (2003) Inducible protein knockout reveals temporal requirement of CaMKII reactivation for memory consolidation in the brain. Proc Natl Acad Sci USA 100(7):4287–4292. https://doi.org/10.1073/pnas.0636870100

    Article  CAS  PubMed  Google Scholar 

  54. Silva A, Paylor R, Wehner J, Tonegawa S (1992) Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. Science 257(5067):206–211. https://doi.org/10.1126/science.1321493

    Article  CAS  PubMed  Google Scholar 

  55. Frankland PW, O’Brien C, Ohno M, Kirkwood A, Silva AJ (2001) Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature 411(6835):309–313. https://doi.org/10.1038/35077089

    Article  CAS  PubMed  Google Scholar 

  56. Frankland PW, Bontempi B, Talton LE, Kaczmarek L, Silva AJ (2004) The involvement of the anterior cingulate cortex in remote contextual fear memory. Science 304(5672):881–883. https://doi.org/10.1126/science.1094804

    Article  CAS  PubMed  Google Scholar 

  57. Bock J, Braun K (1999) Blockade of N-methyl-d-aspartate receptor activation suppresses learning-induced synaptic elimination. Proc Natl Acad Sci USA 96(5):2485–2490

    Article  CAS  Google Scholar 

  58. Govindarajan A, Kelleher RJ, Tonegawa S (2006) A clustered plasticity model of long-term memory engrams. Nat Rev Neurosci 7(7):575–583. https://doi.org/10.1038/nrn1937

    Article  CAS  PubMed  Google Scholar 

  59. De Roo M, Klauser P, Muller D (2008) LTP promotes a selective long-term stabilization and clustering of dendritic spines. PLoS Biol 6(9):e219. https://doi.org/10.1371/journal.pbio.0060219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Clopath C (2012) Synaptic consolidation: an approach to long-term learning. Cogn Neurodyn 6(3):251–257. https://doi.org/10.1007/s11571-011-9177-6

    Article  PubMed  Google Scholar 

  61. Caroni P, Chowdhury A, Lahr M (2014) Synapse rearrangements upon learning: from divergent-sparse connectivity to dedicated sub-circuits. Trends Neurosci 37(10):604–614. https://doi.org/10.1016/j.tins.2014.08.011

    Article  CAS  PubMed  Google Scholar 

  62. Attardo A, Fitzgerald JE, Schnitzer MJ (2015) Impermanence of dendritic spines in live adult CA1 hippocampus. Nature 523(7562):592–596. https://doi.org/10.1038/nature14467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Bhatt DH, Zhang S, Gan WB (2009) Dendritic spine dynamics. Annu Rev Physiol 71:261–282. https://doi.org/10.1146/annurev.physiol.010908.163140

    Article  CAS  PubMed  Google Scholar 

  64. Yang G, Pan F, Gan W-B (2009) Stably maintained dendritic spines are associated with lifelong memories. Nature 462(7275):920–924. https://doi.org/10.1038/nature08577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Miller R (1996) Neural assemblies and laminar interactions in the cerebral cortex. Biol Cybern 75(3):253–261

    Article  CAS  Google Scholar 

  66. Takashima A, Nieuwenhuis IL, Jensen O, Talamini LM, Rijpkema M, Fernández G (2009) Shift from hippocampal to neocortical centered retrieval network with consolidation. J Neurosci 29(32):10087–10093. https://doi.org/10.1523/JNEUROSCI.0799-09.2009

    Article  CAS  PubMed  Google Scholar 

  67. Maviel T (2004) Sites of neocortical reorganization critical for remote spatial memory. Science 305(5680):96–99. https://doi.org/10.1126/science.1098180

    Article  CAS  PubMed  Google Scholar 

  68. Sacco T, Sacchetti B (2010) Role of secondary sensory cortices in emotional memory storage and retrieval in rats. Science 329(5992):649–656. https://doi.org/10.1126/science.1183165

    Article  CAS  PubMed  Google Scholar 

  69. Restivo L, Vetere G, Bontempi B, Ammassari-Teule M (2009) The formation of recent and remote memory is associated with time-dependent formation of dendritic spines in the hippocampus and anterior cingulate cortex. J Neurosci 29(25):8206–8214. https://doi.org/10.1523/JNEUROSCI.0966-09.2009

    Article  CAS  PubMed  Google Scholar 

  70. Vetere G, Restivo L, Cole CJ, Ross PJ, Ammassari-Teule M, Josselyn SA, Frankland PW (2011) Spine growth in the anterior cingulate cortex is necessary for the consolidation of contextual fear memory. Proc Natl Acad Sci USA 108(20):8456–8460. https://doi.org/10.1073/pnas.1016275108

    Article  PubMed  Google Scholar 

  71. Flavell SW, Cowan CW, Kim T-K, Greer PL, Lin Y, Paradis S, Griffith EC, Hu LS, Chen C, Greenberg ME (2006) Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 311(5763):1008–1012. https://doi.org/10.1126/science.1122511

    Article  CAS  PubMed  Google Scholar 

  72. Pulipparacharuvil S, Renthal W, Hale CF, Taniguchi M, Xiao G, Kumar A, Russo SJ, Sikder D, Dewey CM, Davis MM, Greengard P, Nairn AC, Nestler EJ, Cowan CW (2008) Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 59(4):621–633. https://doi.org/10.1016/j.neuron.2008.06.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Lesburgueres E, Gobbo OL, Alaux-Cantin S, Hambucken A, Trifilieff P, Bontempi B (2011) Early tagging of cortical networks is required for the formation of enduring associative memory. Science 331(6019):924–928. https://doi.org/10.1126/science.1196164

    Article  CAS  PubMed  Google Scholar 

  74. Alvarez P, Lipton PA, Melrose R, Eichenbaum H (2001) Differential effects of damage within the hippocampal region on memory for a natural, nonspatial odor–odor association. Learn Mem 8(2):79–86. https://doi.org/10.1101/lm.38201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Frey U, Morris RG (1998) Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci 21(5):181–188

    Article  CAS  Google Scholar 

  76. Wiltgen BJ (2006) Context fear learning in the absence of the hippocampus. J Neurosci 26(20):5484–5491. https://doi.org/10.1523/jneurosci.2685-05.2006

    Article  CAS  PubMed  Google Scholar 

  77. Zelikowsky M, Bissiere S, Hast TA, Bennett RZ, Abdipranoto A, Vissel B, Fanselow MS (2013) Prefrontal microcircuit underlies contextual learning after hippocampal loss. Proc Natl Acad Sci USA 110(24):9938–9943. https://doi.org/10.1073/pnas.1301691110

    Article  PubMed  Google Scholar 

  78. Zelikowsky M, Bissiere S, Fanselow MS (2012) Contextual fear memories formed in the absence of the dorsal hippocampus decay across time. J Neurosci 32(10):3393–3397. https://doi.org/10.1523/JNEUROSCI.4339-11.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Witter M (2011) Entorhinal cortex. Scholarpedia J 6(10):4380. https://doi.org/10.4249/scholarpedia.4380

    Article  Google Scholar 

  80. Tovote P, Fadok JP, Lüthi A (2015) Neuronal circuits for fear and anxiety. Nat Rev Neurosci 16(6):317–331. https://doi.org/10.1038/nrn3945

    Article  CAS  PubMed  Google Scholar 

  81. Zhou Y, Won J, Karlsson MG, Zhou M, Rogerson T, Balaji J, Neve R, Poirazi P, Silva AJ (2009) CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala. Nat Neurosci 12(11):1438–1443. https://doi.org/10.1038/nn.2405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Nonaka A, Toyoda T, Miura Y, Hitora-Imamura N, Naka M, Eguchi M, Yamaguchi S, Ikegaya Y, Matsuki N, Nomura H (2014) Synaptic plasticity associated with a memory engram in the basolateral amygdala. J Neurosci 34(28):9305–9309. https://doi.org/10.1523/JNEUROSCI.4233-13.2014

    Article  CAS  PubMed  Google Scholar 

  83. Reijmers LG, Perkins BL, Matsuo N, Mayford M (2007) Localization of a stable neural correlate of associative memory. Science 317(5842):1230–1233. https://doi.org/10.1126/science.1143839

    Article  CAS  PubMed  Google Scholar 

  84. Jenkins JG, Dallenbach KM (1924) Obliviscence during sleep and waking. Am J Psychol 35(4):605–612

    Article  Google Scholar 

  85. Stickgold R, Scott L, Rittenhouse C, Hobson JA (1999) Sleep-induced changes in associative memory. J Cogn Neurosci 11(2):182–193

    Article  CAS  Google Scholar 

  86. Stickgold R (2005) Sleep-dependent memory consolidation. Nature 437(7063):1272–1278. https://doi.org/10.1038/nature04286

    Article  CAS  PubMed  Google Scholar 

  87. Marshall L, Helgadóttir H, Mölle M, Born J (2006) Boosting slow oscillations during sleep potentiates memory. Nature 444(7119):610–613. https://doi.org/10.1038/nature05278

    Article  CAS  PubMed  Google Scholar 

  88. Cai DJ, Mednick SA, Harrison EM, Kanady JC, Mednick SC (2009) REM, not incubation, improves creativity by priming associative networks. Proc Natl Acad Sci 106(25):10130–10134. https://doi.org/10.1073/pnas.0900271106

    Article  PubMed  Google Scholar 

  89. Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neurosci. https://doi.org/10.1038/nrn2762

    Article  PubMed  Google Scholar 

  90. Diekelmann S (2014) Sleep for cognitive enhancement. Front Syst Neurosci 8:46. https://doi.org/10.3389/fnsys.2014.00046

    Article  PubMed  PubMed Central  Google Scholar 

  91. Rasch B, Born J (2013) About sleep’s role in memory. Physiol Rev 93(2):681–766. https://doi.org/10.1152/physrev.00032.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Rasch B, Büchel C, Gais S, Born J (2007) Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 315(5817):1426–1429. https://doi.org/10.1126/science.1138581

    Article  CAS  PubMed  Google Scholar 

  93. Tucker MA, Fishbein W (2008) Enhancement of declarative memory performance following a daytime nap is contingent on strength of initial task acquisition. Sleep 31(2):197–203

    Article  Google Scholar 

  94. Ruch S, Markes O, Duss SB, Oppliger D, Reber TP, Koenig T, Mathis J, Roth C, Henke K (2012) Sleep stage II contributes to the consolidation of declarative memories. Neuropsychologia 50(10):2389–2396. https://doi.org/10.1016/j.neuropsychologia.2012.06.008

    Article  PubMed  Google Scholar 

  95. Laureys S, Peigneux P, Phillips C, Fuchs S, Degueldre C, Aerts J, Del Fiore G, Petiau C, Luxen A, van der Linden M, Cleeremans A, Smith C, Maquet P (2001) Experience-dependent changes in cerebral functional connectivity during human rapid eye movement sleep. Neuroscience 105(3):521–525

    Article  CAS  Google Scholar 

  96. Nishida M, Pearsall J, Buckner RL, Walker MP (2009) REM sleep, prefrontal theta, and the consolidation of human emotional memory. Cereb Cortex 19(5):1158–1166. https://doi.org/10.1093/cercor/bhn155

    Article  PubMed  Google Scholar 

  97. Wagner U, Gais S, Born J (2001) Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep. Learn Mem 8(2):112–119. https://doi.org/10.1101/lm.36801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Smith C (2001) Sleep states and memory processes in humans: procedural versus declarative memory systems. Sleep Med Rev 5(6):491–506. https://doi.org/10.1053/smrv.2001.0164

    Article  CAS  PubMed  Google Scholar 

  99. Ackermann S, Rasch B (2014) Differential effects of non-REM and REM sleep on memory consolidation? Curr Neurol Neurosci Rep 14(2):430. https://doi.org/10.1007/s11910-013-0430-8

    Article  PubMed  Google Scholar 

  100. Pavlides C, Winson J (1989) Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J Neurosci 9(8):2907–2918

    Article  CAS  Google Scholar 

  101. Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265(5172):676–679

    Article  CAS  Google Scholar 

  102. Lee AK, Wilson MA (2002) Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36(6):1183–1194

    Article  CAS  Google Scholar 

  103. Diba K, Buzsáki G (2007) Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci 10(10):1241–1242. https://doi.org/10.1038/nn1961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Marr D (1971) Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci 262(841):23–81

    Article  CAS  Google Scholar 

  105. Chrobak JJ, Buzsáki G (1994) Selective activation of deep layer (V–VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat. J Neurosci 14(10):6160–6170

    Article  CAS  Google Scholar 

  106. Treves A, Rolls ET (1994) Computational analysis of the role of the hippocampus in memory. Hippocampus 4(3):374–391. https://doi.org/10.1002/hipo.450040319

    Article  CAS  PubMed  Google Scholar 

  107. Sejnowski TJ, Destexhe A (2000) Why do we sleep? Brain Res 886(1–2):208–223

    Article  CAS  Google Scholar 

  108. Timofeev I, Chauvette S (2017) Sleep slow oscillation and plasticity. Curr Opin Neurobiol 44:116–126. https://doi.org/10.1016/j.conb.2017.03.019

    Article  CAS  PubMed  Google Scholar 

  109. Tononi G, Cirelli C (2014) Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81(1):12–34. https://doi.org/10.1016/j.neuron.2013.12.025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Giuditta A, Ambrosini MV, Montagnese P, Mandile P, Cotugno M, Zucconi GG, Vescia S (1995) The sequential hypothesis of the function of sleep. Behav Brain Res 69(1–2):157–166. https://doi.org/10.1016/0166-4328(95)00012-i

    Article  CAS  PubMed  Google Scholar 

  111. Ribeiro S, Nicolelis MAL (2004) Reverberation, storage, and postsynaptic propagation of memories during sleep. Learn Mem 11(6):686–696. https://doi.org/10.1101/lm.75604

    Article  PubMed  PubMed Central  Google Scholar 

  112. Poe GR, Walsh CM, Bjorness TE (2010) Cognitive neuroscience of sleep. Prog Brain Res 185:1–19. https://doi.org/10.1016/B978-0-444-53702-7.00001-4

    Article  PubMed  PubMed Central  Google Scholar 

  113. Ribeiro S (2012) Sleep and plasticity. Pflugers Arch 463(1):111–120. https://doi.org/10.1007/s00424-011-1031-5

    Article  CAS  PubMed  Google Scholar 

  114. Li W, Ma L, Yang G, Gan W-B (2017) REM sleep selectively prunes and maintains new synapses in development and learning. Nat Neurosci 20(3):427–437. https://doi.org/10.1038/nn.4479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Born J, Wilhelm I (2011) System consolidation of memory during sleep. Psychol Res 76(2):192–203. https://doi.org/10.1007/s00426-011-0335-6

    Article  PubMed  PubMed Central  Google Scholar 

  116. Chauvette S, Seigneur J, Timofeev I (2012) Sleep oscillations in the thalamocortical system induce long-term neuronal plasticity. Neuron 75(6):1105–1113. https://doi.org/10.1016/j.neuron.2012.08.034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Brown RE, Basheer R, McKenna JT, Strecker RE, McCarley RW (2012) Control of sleep and wakefulness. Physiol Rev 92(3):1087–1187. https://doi.org/10.1152/physrev.00032.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Khodagholy D, Gelinas JN, Buzsáki G (2017) Learning-enhanced coupling between ripple oscillations in association cortices and hippocampus. Science 358(6361):369–372. https://doi.org/10.1126/science.aan6203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85(5):1969–1985. https://doi.org/10.1152/jn.2001.85.5.1969

    Article  CAS  PubMed  Google Scholar 

  120. Gray CM, McCormick DA (1996) Chattering cells: superficial pyramidal neurons contributing to the generation of synchronous oscillations in the visual cortex. Science 274(5284):109–113

    Article  CAS  Google Scholar 

  121. Thomson AM, West DC, Hahn J, Deuchars J (1996) Single axon IPSPs elicited in pyramidal cells by three classes of interneurons in slices of rat neocortex. J Physiol 496(Pt 1):81–102

    Article  CAS  Google Scholar 

  122. Steriade M, Timofeev I, Dürmüller N, Grenier F (1998) Dynamic properties of corticothalamic neurons and local cortical interneurons generating fast rhythmic (30–40 Hz) spike bursts. J Neurophysiol 79(1):483–490. https://doi.org/10.1152/jn.1998.79.1.483

    Article  CAS  PubMed  Google Scholar 

  123. Roxin A, Brunel N, Hansel D, Mongillo G, van Vreeswijk C (2011) On the distribution of firing rates in networks of cortical neurons. J Neurosci. https://doi.org/10.1523/jneurosci.1677-11.2011

    Article  PubMed  Google Scholar 

  124. Rahmati V, Kirmse K, Marković D, Holthoff K, Kiebel SJ (2016) Inferring neuronal dynamics from calcium imaging data using biophysical models and Bayesian inference. PLoS Comput Biol 12(2):e1004736. https://doi.org/10.1371/journal.pcbi.1004736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Rahmati V, Kirmse K, Holthoff K, Kiebel SJ (2018) Ultra-fast accurate reconstruction of spiking activity from calcium imaging data. J Neurophysiol. https://doi.org/10.1152/jn.00934.2017

    Article  PubMed  Google Scholar 

  126. Grosmark AD, Mizuseki K, Pastalkova E, Diba K, Buzsáki G (2012) REM sleep reorganizes hippocampal excitability. Neuron 75(6):1001–1007. https://doi.org/10.1016/j.neuron.2012.08.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Blanco W, Pereira CM, Cota VR, Souza AC, Rennó-Costa C, Santos S, Dias G, Guerreiro AMG, Tort ABL, Neto AD, Ribeiro S (2015) Synaptic homeostasis and restructuring across the sleep-wake cycle. PLoS Comput Biol 11(5):e1004241. https://doi.org/10.1371/journal.pcbi.1004241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Vyazovskiy VV, Olcese U, Lazimy YM, Faraguna U, Esser SK, Williams JC, Cirelli C, Tononi G (2009) Cortical firing and sleep homeostasis. Neuron 63(6):865–878. https://doi.org/10.1016/j.neuron.2009.08.024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Koike BDV, Farias KS, Billwiller F, Almeida-Filho D, Libourel PA, Tiran-Cappello A, Parmentier R, Blanco W, Ribeiro S, Luppi PH, Queiroz CM (2017) Electrophysiological evidence that the retrosplenial cortex displays a strong and specific activation phased with hippocampal theta during paradoxical (REM) sleep. J Neurosci 37(33):8003–8013. https://doi.org/10.1523/JNEUROSCI.0026-17.2017

    Article  PubMed  Google Scholar 

  130. Watson BO, Levenstein D, Greene JP, Gelinas JN, Buzsáki G (2016) Network homeostasis and state dynamics of neocortical sleep. Neuron 90(4):839–852. https://doi.org/10.1016/j.neuron.2016.03.036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Niethard N, Hasegawa M, Itokazu T, Oyanedel CN, Born J, Sato TR (2016) Sleep-stage-specific regulation of cortical excitation and inhibition. Curr Biol 26(20):2739–2749. https://doi.org/10.1016/j.cub.2016.08.035

    Article  CAS  PubMed  Google Scholar 

  132. Tononi G, Cirelli C (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10(1):49–62. https://doi.org/10.1016/j.smrv.2005.05.002

    Article  PubMed  Google Scholar 

  133. Skaggs WE, McNaughton BL (1996) Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271(5257):1870–1873

    Article  CAS  Google Scholar 

  134. Paller KA, Voss JL (2004) Memory reactivation and consolidation during sleep. Learn Mem 11(6):664–670. https://doi.org/10.1101/lm.75704

    Article  PubMed  PubMed Central  Google Scholar 

  135. Ribeiro S, Gervasoni D, Soares ES, Zhou Y, Lin S-C, Pantoja J, Lavine M, Nicolelis MAL (2004) Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas. PLoS Biol 2(1):E24. https://doi.org/10.1371/journal.pbio.0020024

    Article  PubMed  PubMed Central  Google Scholar 

  136. O’Neill J, Pleydell-Bouverie B, Dupret D, Csicsvari J (2010) Play it again: reactivation of waking experience and memory. Trends Neurosci 33(5):220–229. https://doi.org/10.1016/j.tins.2010.01.006

    Article  CAS  PubMed  Google Scholar 

  137. Buzsáki G (2015) Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus 25(10):1073–1188. https://doi.org/10.1002/hipo.22488

    Article  PubMed  PubMed Central  Google Scholar 

  138. Destexhe A, Hughes SW, Rudolph M, Crunelli V (2007) Are corticothalamic ‘up’ states fragments of wakefulness? Trends Neurosci 30(7):334–342. https://doi.org/10.1016/j.tins.2007.04.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Girardeau G, Inema I, Buzsáki G (2017) Reactivations of emotional memory in the hippocampus-amygdala system during sleep. Nat Neurosci 20(11):1634–1642. https://doi.org/10.1038/nn.4637

    Article  CAS  PubMed  Google Scholar 

  140. Siapas AG, Wilson MA (1998) Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21(5):1123–1128

    Article  CAS  Google Scholar 

  141. Ji D, Wilson MA (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10(1):100–107. https://doi.org/10.1038/nn1825

    Article  CAS  PubMed  Google Scholar 

  142. Girardeau G, Benchenane K, Wiener SI, Buzsáki G, Zugaro MB (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 12(10):1222–1223. https://doi.org/10.1038/nn.2384

    Article  CAS  PubMed  Google Scholar 

  143. Peyrache A, Khamassi M, Benchenane K, Wiener SI, Battaglia FP (2009) Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat Neurosci 12(7):919–926

    Article  CAS  Google Scholar 

  144. Wierzynski CM, Lubenov EV, Gu M, Siapas AG (2009) State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron 61(4):587–596. https://doi.org/10.1016/j.neuron.2009.01.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Wang DV, Ikemoto S (2016) Coordinated interaction between hippocampal sharp-wave ripples and anterior cingulate unit activity. J Neurosci 36(41):10663–10672. https://doi.org/10.1523/JNEUROSCI.1042-16.2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Miyamoto D, Hirai D, Fung CC, Inutsuka A, Odagawa M, Suzuki T, Boehringer R, Adaikkan C, Matsubara C, Matsuki N, Fukai T, McHugh TJ, Yamanaka A, Murayama M (2016) Top-down cortical input during NREM sleep consolidates perceptual memory. Science 352(6291):1315–1318. https://doi.org/10.1126/science.aaf0902

    Article  CAS  PubMed  Google Scholar 

  147. Maingret N, Girardeau G, Todorova R, Goutierre M, Zugaro M (2016) Hippocampo-cortical coupling mediates memory consolidation during sleep. Nat Neurosci 19(7):959–964. https://doi.org/10.1038/nn.4304

    Article  CAS  PubMed  Google Scholar 

  148. Latchoumane CV, Ngo HV, Born J, Shin HS (2017) Thalamic spindles promote memory formation during sleep through triple phase-locking of cortical, thalamic, and hippocampal rhythms. Neuron 95(2):424–435. https://doi.org/10.1016/j.neuron.2017.06.025

    Article  CAS  PubMed  Google Scholar 

  149. Schouten DI, Pereira SIR, Tops M, Louzada FM (2017) State of the art on targeted memory reactivation: sleep your way to enhanced cognition. Sleep Med Rev 32:123–131. https://doi.org/10.1016/j.smrv.2016.04.002

    Article  PubMed  Google Scholar 

  150. de Lavilléon G, Lacroix MM, Rondi-Reig L, Benchenane K (2015) Explicit memory creation during sleep demonstrates a causal role of place cells in navigation. Nat Neurosci 18(4):493–495. https://doi.org/10.1038/nn.3970

    Article  CAS  PubMed  Google Scholar 

  151. Jadhav SP, Kemere C, German PW, Frank LM (2012) Awake hippocampal sharp-wave ripples support spatial memory. Science 336(6087):1454–1458. https://doi.org/10.1126/science.1217230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Gelinas JN, Khodagholy D, Thesen T, Devinsky O, Buzsaki G (2016) Interictal epileptiform discharges induce hippocampal–cortical coupling in temporal lobe epilepsy. Nat Med 22(6):641–648. https://doi.org/10.1038/nm.4084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Rasch B, Born J (2007) Maintaining memories by reactivation. Curr Opin Neurobiol 17(6):698–703. https://doi.org/10.1016/j.conb.2007.11.007

    Article  CAS  PubMed  Google Scholar 

  154. Ramadan W, Eschenko O, Sara SJ (2009) Hippocampal sharp wave/ripples during sleep for consolidation of associative memory. PLoS One 4(8):e6697. https://doi.org/10.1371/journal.pone.0006697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Furini CRG, Myskiw JC, Benetti F, Izquierdo I (2013) New frontiers in the study of memory mechanisms. Rev Bras Psiquiatr 35(2):173–177

    Article  Google Scholar 

  156. Alberini CM, Kandel ER (2015) The regulation of transcription in memory consolidation. Cold Spring Harb Perspect Biol 7(1):a021741. https://doi.org/10.1101/cshperspect.a021741

    Article  PubMed Central  Google Scholar 

  157. Ribeiro S, Goyal V, Mello CV, Pavlides C (1999) Brain gene expression during REM sleep depends on prior waking experience. Learn Mem 6(5):500–508

    Article  CAS  Google Scholar 

  158. Ribeiro S, Mello CV, Velho T, Gardner TJ, Jarvis ED, Pavlides C (2002) Induction of hippocampal long-term potentiation during waking leads to increased extrahippocampal zif-268 expression during ensuing rapid-eye-movement sleep. J Neurosci 22(24):10914–10923

    Article  CAS  Google Scholar 

  159. Ulloor J, Datta S (2005) Spatio-temporal activation of cyclic AMP response element-binding protein, activity-regulated cytoskeletal-associated protein and brain-derived nerve growth factor: a mechanism for pontine-wave generator activation-dependent two-way active-avoidance memory processing in the rat. J Neurochem 95(2):418–428. https://doi.org/10.1111/j.1471-4159.2005.03378.x

    Article  CAS  PubMed  Google Scholar 

  160. Frank MG, Benington JH (2006) The role of sleep in memory consolidation and brain plasticity: dream or reality? Neuroscientist 12(6):477–488. https://doi.org/10.1177/1073858406293552

    Article  PubMed  Google Scholar 

  161. Ribeiro S, Shi X, Engelhard M, Zhou Y, Zhang H, Gervasoni D, Lin S-C, Wada K, Lemos NA, Nicolelis MA (2007) Novel experience induces persistent sleep-dependent plasticity in the cortex but not in the hippocampus. Front Neurosci 1(1):43

    Article  Google Scholar 

  162. Ravassard P, Pachoud B, Comte JC, Mejia-Perez C, Scote-Blachon C, Gay N, Claustrat B, Touret M, Luppi PH, Salin PA (2009) Paradoxical (REM) sleep deprivation causes a large and rapidly reversible decrease in long-term potentiation, synaptic transmission, glutamate receptor protein levels, and ERK/MAPK activation in the dorsal hippocampus. Sleep 32(2):227–240

    Article  Google Scholar 

  163. Abel T, Havekes R, Saletin JM, Walker MP (2013) Sleep, plasticity and memory from molecules to whole-brain networks. Curr Biol 23(17):R774–R788. https://doi.org/10.1016/j.cub.2013.07.025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Luo J, Phan TX, Yang Y, Garelick MG, Storm DR (2013) Increases in cAMP, MAPK activity, and CREB phosphorylation during REM sleep: implications for REM sleep and memory consolidation. J Neurosci 33(15):6460–6468. https://doi.org/10.1523/JNEUROSCI.5018-12.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Calais JB, Ojopi EB, Morya E, Sameshima K, Ribeiro S (2015) Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep. Neurobiol Learn Mem 122:19–27. https://doi.org/10.1016/j.nlm.2015.01.002

    Article  CAS  PubMed  Google Scholar 

  166. Bramham CR, Alme MN, Bittins M, Kuipers SD, Nair RR, Pai B, Panja D, Schubert M, Soule J, Tiron A, Wibrand K (2010) The Arc of synaptic memory. Exp Brain Res 200(2):125–140. https://doi.org/10.1007/s00221-009-1959-2

    Article  PubMed  Google Scholar 

  167. Malkani S, Wallace KJ, Donley MP, Rosen JB (2004) An egr-1 (zif268) antisense oligodeoxynucleotide infused into the amygdala disrupts fear conditioning. Learn Mem 11(5):617–624. https://doi.org/10.1101/lm.73104

    Article  PubMed  PubMed Central  Google Scholar 

  168. Lonergan ME, Gafford GM, Jarome TJ, Helmstetter FJ (2010) Time-dependent expression of Arc and zif268 after acquisition of fear conditioning. Neural Plast 2010:139891. https://doi.org/10.1155/2010/139891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Shepherd JD, Bear MF (2011) New views of Arc, a master regulator of synaptic plasticity. Nat Neurosci 14(3):279–284. https://doi.org/10.1038/nn.2708

    Article  CAS  PubMed  Google Scholar 

  170. Katche C, Goldin A, Gonzalez C, Bekinschtein P, Medina JH (2012) Maintenance of long-term memory storage is dependent on late posttraining Egr-1 expression. Neurobiol Learn Mem 98(3):220–227. https://doi.org/10.1016/j.nlm.2012.08.001

    Article  CAS  PubMed  Google Scholar 

  171. Nakayama D, Iwata H, Teshirogi C, Ikegaya Y, Matsuki N, Nomura H (2015) Long-delayed expression of the immediate early gene Arc/Arg3.1 refines neuronal circuits to perpetuate fear memory. J Neurosci 35(2):819–830. https://doi.org/10.1523/JNEUROSCI.2525-14.2015

    Article  CAS  PubMed  Google Scholar 

  172. Ravassard P, Hamieh AM, Joseph MA, Fraize N, Libourel P-A, Lebarillier L, Arthaud S, Meissirel C, Touret M, Malleret G, Salin P-A (2016) REM sleep-dependent bidirectional regulation of hippocampal-based emotional memory and LTP. Cereb Cortex 26(4):1488–1500. https://doi.org/10.1093/cercor/bhu310

    Article  PubMed  Google Scholar 

  173. Ravassard P, Hamieh AM, Malleret G, Salin PA (2015) Paradoxical sleep: a vigilance state to gate long-term brain plasticity? Neurobiol Learn Mem 122:4–10. https://doi.org/10.1016/j.nlm.2014.11.013

    Article  PubMed  Google Scholar 

  174. Norman ED, Thiels E, Barrionuevo G, Klann E (2000) Long-term depression in the hippocampus in vivo is associated with protein phosphatase-dependent alterations in extracellular signal-regulated kinase. J Neurochem 74(1):192–198

    Article  CAS  Google Scholar 

  175. Thiels E, Kanterewicz BI, Knapp LT, Barrionuevo G, Klann E (2000) Protein phosphatase-mediated regulation of protein kinase C during long-term depression in the adult hippocampus in vivo. J Neurosci 20(19):7199–7207

    Article  CAS  Google Scholar 

  176. Bekinschtein P, Cammarota M, Igaz LM, Bevilaqua LRM, Izquierdo I, Medina JH (2007) Persistence of long-term memory storage requires a late protein synthesis- and BDNF-dependent phase in the hippocampus. Neuron 53(2):261–277. https://doi.org/10.1016/j.neuron.2006.11.025

    Article  CAS  PubMed  Google Scholar 

  177. Gonzalez MC, Kramar CP, Tomaiuolo M, Katche C, Weisstaub N, Cammarota M, Medina JH (2014) Medial prefrontal cortex dopamine controls the persistent storage of aversive memories. Front Behav Neurosci 8:408. https://doi.org/10.3389/fnbeh.2014.00408

    Article  PubMed  PubMed Central  Google Scholar 

  178. Rossato JI, Bevilaqua LRM, Izquierdo I, Medina JH, Cammarota M (2009) Dopamine controls persistence of long-term memory storage. Science 325(5943):1017–1020. https://doi.org/10.1126/science.1172545

    Article  CAS  PubMed  Google Scholar 

  179. Katche C, Dorman G, Gonzalez C, Kramar CP, Slipczuk L, Rossato JI, Cammarota M, Medina JH (2013) On the role of retrosplenial cortex in long-lasting memory storage. Hippocampus 23(4):295–302. https://doi.org/10.1002/hipo.22092

    Article  CAS  PubMed  Google Scholar 

  180. Katche C, Dorman G, Slipczuk L, Cammarota M, Medina JH (2013) Functional integrity of the retrosplenial cortex is essential for rapid consolidation and recall of fear memory. Learn Mem 20(4):170–173. https://doi.org/10.1101/lm.030080.112

    Article  PubMed  Google Scholar 

  181. Cowansage KK, Shuman T, Dillingham BC, Chang A, Golshani P, Mayford M (2014) Direct reactivation of a coherent neocortical memory of context. Neuron 84(2):432–441. https://doi.org/10.1016/j.neuron.2014.09.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Haijima A, Ichitani Y (2008) Anterograde and retrograde amnesia of place discrimination in retrosplenial cortex and hippocampal lesioned rats. Learn Mem 15(7):477–482. https://doi.org/10.1101/lm.862308

    Article  PubMed  Google Scholar 

  183. Haijima A, Ichitani Y (2012) Dissociable anterograde amnesic effects of retrosplenial cortex and hippocampal lesions on spontaneous object recognition memory in rats. Hippocampus 22(9):1868–1875. https://doi.org/10.1002/hipo.22021

    Article  PubMed  Google Scholar 

  184. Katche C, Medina JH (2017) Requirement of an early activation of BDNF/c-Fos cascade in the retrosplenial cortex for the persistence of a long-lasting aversive memory. Cereb Cortex 27(2):1060–1067. https://doi.org/10.1093/cercor/bhv284

    Article  PubMed  Google Scholar 

  185. Renouard L, Billwiller F, Ogawa K, Clément O, Camargo N, Abdelkarim M, Gay N, Scoté-Blachon C, Touré R, Libourel P-A, Ravassard P, Salvert D, Peyron C, Claustrat B, Léger L, Salin P, Malleret G, Fort P, Luppi P-H (2015) The supramammillary nucleus and the claustrum activate the cortex during REM sleep. Sci Adv 1(3):e1400177. https://doi.org/10.1126/sciadv.1400177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Smith C, Young J, Young W (1980) Prolonged increases in paradoxical sleep during and after avoidance-task acquisition. Sleep 3(1):67–81

    CAS  PubMed  Google Scholar 

  187. Smith C, Lapp L (1986) Prolonged increases in both PS and number of REMs following a shuttle avoidance task. Physiol Behav 36(6):1053–1057. https://doi.org/10.1016/0031-9384(86)90479-8

    Article  CAS  PubMed  Google Scholar 

  188. Smith C, Butler S (1982) Paradoxical sleep at selective times following training is necessary for learning. Physiol Behav 29(3):469–473

    Article  CAS  Google Scholar 

  189. Graves LA, Heller EA, Pack AI, Abel T (2003) Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning. Learn Mem 10(3):168–176. https://doi.org/10.1101/lm.48803

    Article  PubMed  PubMed Central  Google Scholar 

  190. Prince TM, Wimmer M, Choi J, Havekes R, Aton S, Abel T (2014) Sleep deprivation during a specific 3-hour time window post-training impairs hippocampal synaptic plasticity and memory. Neurobiol Learn Mem 109:122–130. https://doi.org/10.1016/j.nlm.2013.11.021

    Article  PubMed  Google Scholar 

  191. França AS, Lobão-Soares B, Muratori L, Nascimento G, Winne J, Pereira CM, Jeronimo SM, Ribeiro S (2015) D2 dopamine receptor regulation of learning, sleep and plasticity. Eur Neuropsychopharmacol 25(4):493–504. https://doi.org/10.1016/j.euroneuro.2015.01.011

    Article  CAS  PubMed  Google Scholar 

  192. Yasenkov R, Deboer T (2012) Circadian modulation of sleep in rodents. In: Progress in brain research, pp 203–218. https://doi.org/10.1016/b978-0-444-59427-3.00012-5

  193. Gerstner JR, Yin JCP (2010) Circadian rhythms and memory formation. Nat Rev Neurosci 11(8):577–588. https://doi.org/10.1038/nrn2881

    Article  CAS  PubMed  Google Scholar 

  194. Frank MG (2016) Circadian regulation of synaptic plasticity. Biology 5(3):31. https://doi.org/10.3390/biology5030031

    Article  PubMed Central  Google Scholar 

  195. Eckel-Mahan KL, Phan T, Han S, Wang H, Chan GCK, Scheiner ZS, Storm DR (2008) Circadian oscillation of hippocampal MAPK activity and cAmp: implications for memory persistence. Nat Neurosci 11(9):1074–1082

    Article  CAS  Google Scholar 

  196. Yang G, Gan WB (2012) Sleep contributes to dendritic spine formation and elimination in the developing mouse somatosensory cortex. Dev Neurobiol 72(11):1391–1398. https://doi.org/10.1002/dneu.20996

    Article  PubMed  PubMed Central  Google Scholar 

  197. Liston C, Cichon JM, Jeanneteau F, Jia Z, Chao MV, Gan W-B (2013) Circadian glucocorticoid oscillations promote learning-dependent synapse formation and maintenance. Nat Neurosci 16(6):698–705. https://doi.org/10.1038/nn.3387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. Tononi G, Cirelli C (2003) Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull 62(2):143–150. https://doi.org/10.1016/j.brainresbull.2003.09.004

    Article  PubMed  Google Scholar 

  199. Diekelmann S, Wilhelm I, Born J (2009) The whats and whens of sleep-dependent memory consolidation. Sleep Med Rev 13(5):309–321. https://doi.org/10.1016/j.smrv.2008.08.002

    Article  PubMed  Google Scholar 

  200. Denk W, Horstmann H (2004) Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol 2(11):e329. https://doi.org/10.1371/journal.pbio.0020329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  201. Yang G, Pan F, Chang PC, Gooden F, Gan W-B (2013) Transcranial two-photon imaging of synaptic structures in the cortex of awake head-restrained mice. In: Methods in molecular biology, pp 35–43. https://doi.org/10.1007/978-1-62703-411-1_3

  202. de Vivo L, Bellesi M, Marshall W, Bushong EA, Ellisman MH, Tononi G, Cirelli C (2017) Ultrastructural evidence for synaptic scaling across the wake/sleep cycle. Science 355(6324):507–510. https://doi.org/10.1126/science.aah5982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  203. Lewis PA, Durrant SJ (2011) Overlapping memory replay during sleep builds cognitive schemata. Trends Cogn Sci 15(8):343–351. https://doi.org/10.1016/j.tics.2011.06.004

    Article  PubMed  Google Scholar 

  204. Norimoto H, Makino K, Gao M, Shikano Y, Okamoto K, Ishikawa T, Sasaki T, Hioki H, Fujisawa S, Ikegaya Y (2018) Hippocampal ripples down-regulate synapses. Science 359(6383):1524–1527. https://doi.org/10.1126/science.aao0702

    Article  CAS  PubMed  Google Scholar 

  205. Sadowski JH, Jones MW, Mellor JR (2016) Sharp-wave ripples orchestrate the induction of synaptic plasticity during reactivation of place cell firing patterns in the hippocampus. Cell Rep 14(8):1916–1929. https://doi.org/10.1016/j.celrep.2016.01.061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  206. Hashmi A, Nere A, Tononi G (2013) Sleep-dependent synaptic down-selection (II): single-neuron level benefits for matching, selectivity, and specificity. Front Neurol. https://doi.org/10.3389/fneur.2013.00148

    Article  PubMed  PubMed Central  Google Scholar 

  207. Nere A, Hashmi A, Cirelli C, Tononi G (2013) Sleep-dependent synaptic down-selection (I): modeling the benefits of sleep on memory consolidation and integration. Front Neurol 4:143. https://doi.org/10.3389/fneur.2013.00143

    Article  PubMed  PubMed Central  Google Scholar 

  208. Yang G, Lai CSW, Cichon J, Ma L, Li W, Gan W-B (2014) Sleep promotes branch-specific formation of dendritic spines after learning. Science 344(6188):1173–1178. https://doi.org/10.1126/science.1249098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  209. El-Boustani S, Ip JPK, Breton-Provencher V, Knott GW, Okuno H, Bito H, Sur M (2018) Locally coordinated synaptic plasticity of visual cortex neurons in vivo. Science 360(6395):1349–1354. https://doi.org/10.1126/science.aao0862

    Article  CAS  PubMed  Google Scholar 

  210. Bramham CR, Messaoudi E (2005) BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog Neurobiol 76(2):99–125. https://doi.org/10.1016/j.pneurobio.2005.06.003

    Article  CAS  PubMed  Google Scholar 

  211. Nikolaienko O, Patil S, Eriksen MS, Bramham CR (2018) Arc protein: a flexible hub for synaptic plasticity and cognition. Semin Cell Dev Biol 77:33–42. https://doi.org/10.1016/j.semcdb.2017.09.006

    Article  CAS  PubMed  Google Scholar 

  212. Pavlides C, Greenstein YJ, Grudman M, Winson J (1988) Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of θ-rhythm. Brain Res 439(1–2):383–387. https://doi.org/10.1016/0006-8993(88)91499-0

    Article  CAS  PubMed  Google Scholar 

  213. Hölscher C, Anwyl R, Rowan MJ (1997) Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can be depotentiated by stimulation on the negative phase in area CA1 in vivo. J Neurosci 17(16):6470–6477

    Article  Google Scholar 

  214. Poe GR, Nitz DA, McNaughton BL, Barnes CA (2000) Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res 855(1):176–180

    Article  CAS  Google Scholar 

  215. Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME (2003) Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J Neurosci 23(37):11725–11731

    Article  CAS  Google Scholar 

  216. Booth V, Poe GR (2006) 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(2):161–173. https://doi.org/10.1002/hipo.20143

    Article  PubMed  PubMed Central  Google Scholar 

  217. Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, Buzsáki G (2008) Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60(4):683–697. https://doi.org/10.1016/j.neuron.2008.09.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  218. Boyce R, Glasgow SD, Williams S, Adamantidis A (2016) Causal evidence for the role of REM sleep theta rhythm in contextual memory consolidation. Science 352(6287):812–816. https://doi.org/10.1126/science.aad5252

    Article  CAS  PubMed  Google Scholar 

  219. Frank MG (2014) Sleep and synaptic plasticity in the developing and adult brain. In: Current topics in behavioral neurosciences, pp 123–149. https://doi.org/10.1007/7854_2014_305

  220. Roffwarg HP, Muzio JN, Dement WC (1966) Ontogenetic development of the human sleep-dream cycle. Science 152(3722):604–619. https://doi.org/10.1126/science.152.3722.604

    Article  CAS  PubMed  Google Scholar 

  221. Thurber A, Jha SK, Coleman T, Frank MG (2008) A preliminary study of sleep ontogenesis in the ferret (Mustela putorius furo). Behav Brain Res 189(1):41–51. https://doi.org/10.1016/j.bbr.2007.12.019

    Article  PubMed  PubMed Central  Google Scholar 

  222. Frank MG (2011) The ontogeny and function(s) of REM sleep. In: Rapid eye movement sleep, pp 49–57. https://doi.org/10.1017/cbo9780511921179.008

  223. Lohmann C, Kessels HW (2013) The developmental stages of synaptic plasticity. J Physiol 592(1):13–31. https://doi.org/10.1113/jphysiol.2012.235119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  224. Hubel DH, Wiesel TN (1969) Anatomical demonstration of columns in the monkey striate cortex. Nature 221(5182):747–750

    Article  CAS  Google Scholar 

  225. Frank MG (2017) Sleep and plasticity in the visual cortex: more than meets the eye. Curr Opin Neurobiol 44:8–12. https://doi.org/10.1016/j.conb.2017.01.001

    Article  CAS  PubMed  Google Scholar 

  226. Crair MC, Shah RD (2009) Long-term potentiation and long-term depression in experience-dependent plasticity. In: Encyclopedia of neuroscience, pp 561–570. https://doi.org/10.1016/b978-008045046-9.01213-4

  227. Espinosa JS, Stryker MP (2012) Development and plasticity of the primary visual cortex. Neuron 75(2):230–249. https://doi.org/10.1016/j.neuron.2012.06.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  228. Frank MG, Issa NP, Stryker MP (2001) Sleep enhances plasticity in the developing visual cortex. Neuron 30(1):275–287

    Article  CAS  Google Scholar 

  229. Jha SK, Jones BE, Coleman T, Steinmetz N, Law C-T, Griffin G, Hawk J, Dabbish N, Kalatsky VA, Frank MG (2005) Sleep-dependent plasticity requires cortical activity. J Neurosci 25(40):9266–9274. https://doi.org/10.1523/JNEUROSCI.2722-05.2005

    Article  CAS  PubMed  Google Scholar 

  230. Frank MG, Jha SK, Coleman T (2006) Blockade of postsynaptic activity in sleep inhibits developmental plasticity in visual cortex. NeuroReport 17(13):1459–1463. https://doi.org/10.1097/01.wnr.0000233100.05408.e4

    Article  PubMed  Google Scholar 

  231. Aton SJ, Seibt J, Dumoulin M, Jha SK, Steinmetz N, Coleman T, Naidoo N, Frank MG (2009) Mechanisms of sleep-dependent consolidation of cortical plasticity. Neuron 61(3):454–466. https://doi.org/10.1016/j.neuron.2009.01.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  232. Aton SJ, Broussard C, Dumoulin M, Seibt J, Watson A, Coleman T, Frank MG (2013) Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons. Proc Natl Acad Sci USA 110(8):3101–3106. https://doi.org/10.1073/pnas.1208093110

    Article  PubMed  Google Scholar 

  233. Lee HK, Barbarosie M, Kameyama K, Bear MF, Huganir RL (2000) Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405(6789):955–959. https://doi.org/10.1038/35016089

    Article  CAS  PubMed  Google Scholar 

  234. Poser S, Storm DR (2001) Role of Ca2+-stimulated adenylyl cyclases in LTP and memory formation. Int J Dev Neurosci 19(4):387–394

    Article  CAS  Google Scholar 

  235. Dumoulin Bridi MC, Aton SJ, Seibt J, Renouard L, Coleman T, Frank MG (2015) Rapid eye movement sleep promotes cortical plasticity in the developing brain. Sci Adv 1(6):e1500105. https://doi.org/10.1126/sciadv.1500105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  236. El Gaamouch F, Buisson A, Moustie O, Lemieux M, Labrecque S, Bontempi B, De Koninck P, Nicole O (2012) Interaction between CaMKII and GluN2B controls ERK-dependent plasticity. J Neurosci 32(31):10767–10779. https://doi.org/10.1523/jneurosci.5622-11.2012

    Article  PubMed  Google Scholar 

  237. McDermott CM, Hardy MN, Bazan NG, Magee JC (2006) Sleep deprivation-induced alterations in excitatory synaptic transmission in the CA1 region of the rat hippocampus. J Physiol 570(Pt 3):553–565. https://doi.org/10.1113/jphysiol.2005.093781

    Article  CAS  PubMed  Google Scholar 

  238. Tartar JL, Ward CP, McKenna JT, Thakkar M, Arrigoni E, McCarley RW, Brown RE, Strecker RE (2006) Hippocampal synaptic plasticity and spatial learning are impaired in a rat model of sleep fragmentation. Eur J Neurosci 23(10):2739–2748. https://doi.org/10.1111/j.1460-9568.2006.04808.x

    Article  PubMed  PubMed Central  Google Scholar 

  239. Bekinschtein P, Katche C, Slipczuk LN, Igaz LM, Cammarota M, Izquierdo I, Medina JH (2007) mTOR signaling in the hippocampus is necessary for memory formation. Neurobiol Learn Mem 87(2):303–307. https://doi.org/10.1016/j.nlm.2006.08.007

    Article  CAS  PubMed  Google Scholar 

  240. Hoeffer CA, Klann E (2010) mTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci 33(2):67–75. https://doi.org/10.1016/j.tins.2009.11.003

    Article  CAS  PubMed  Google Scholar 

  241. Seibt J, Dumoulin MC, Aton SJ, Coleman T, Watson A, Naidoo N, Frank MG (2012) Protein synthesis during sleep consolidates cortical plasticity in vivo. Curr Biol 22(8):676–682. https://doi.org/10.1016/j.cub.2012.02.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  242. Aton SJ, Suresh A, Broussard C, Frank MG (2014) Sleep promotes cortical response potentiation following visual experience. Sleep 37(7):1163–1170. https://doi.org/10.5665/sleep.3830

    Article  PubMed  PubMed Central  Google Scholar 

  243. Hengen KB, Torrado Pacheco A, McGregor JN, Van Hooser SD, Turrigiano GG (2016) Neuronal firing rate homeostasis is inhibited by sleep and promoted by wake. Cell 165(1):180–191. https://doi.org/10.1016/j.cell.2016.01.046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  244. Puentes-Mestril C, Aton SJ (2017) Linking network activity to synaptic plasticity during sleep: hypotheses and recent data. Front Neural Circuits 11:61. https://doi.org/10.3389/fncir.2017.00061

    Article  PubMed  PubMed Central  Google Scholar 

  245. Zuo Y, Yang G, Kwon E, Gan W-B (2005) Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature 436(7048):261–265. https://doi.org/10.1038/nature03715

    Article  CAS  PubMed  Google Scholar 

  246. Turrigiano G (2011) Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. Annu Rev Neurosci 34:89–103. https://doi.org/10.1146/annurev-neuro-060909-153238

    Article  CAS  PubMed  Google Scholar 

  247. Levenstein D, Watson BO, Rinzel J, Buzsáki G (2017) Sleep regulation of the distribution of cortical firing rates. Curr Opin Neurobiol 44:34–42. https://doi.org/10.1016/j.conb.2017.02.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  248. Berardi N, Pizzorusso T, Ratto GM, Maffei L (2003) Molecular basis of plasticity in the visual cortex. Trends Neurosci 26(7):369–378. https://doi.org/10.1016/S0166-2236(03)00168-1

    Article  CAS  PubMed  Google Scholar 

  249. He H-Y, Hodos W, Quinlan EM (2006) Visual deprivation reactivates rapid ocular dominance plasticity in adult visual cortex. J Neurosci 26(11):2951–2955. https://doi.org/10.1523/JNEUROSCI.5554-05.2006

    Article  CAS  PubMed  Google Scholar 

  250. Lewin I, Gombosh D (1973) Increase in REM time as a function of the need for divergent thinking. In: European Congress on sleep research, pp 399–403. https://doi.org/10.1159/000428097

  251. Walker MP, Liston C, Hobson JA, Stickgold R (2002) Cognitive flexibility across the sleep–wake cycle: REM-sleep enhancement of anagram problem solving. Cogn Brain Res 14(3):317–324. https://doi.org/10.1016/s0926-6410(02)00134-9

    Article  Google Scholar 

  252. Barsky MM, Tucker MA, Stickgold R (2015) REM sleep enhancement of probabilistic classification learning is sensitive to subsequent interference. Neurobiol Learn Mem 122:63–68. https://doi.org/10.1016/j.nlm.2015.02.015

    Article  PubMed  PubMed Central  Google Scholar 

  253. Landmann N, Kuhn M, Maier J-G, Spiegelhalder K, Baglioni C, Frase L, Riemann D, Sterr A, Nissen C (2015) REM sleep and memory reorganization: potential relevance for psychiatry and psychotherapy. Neurobiol Learn Mem 122:28–40. https://doi.org/10.1016/j.nlm.2015.01.004

    Article  PubMed  Google Scholar 

  254. Whitehurst LN, Cellini N, McDevitt EA, Duggan KA, Mednick SC (2016) Autonomic activity during sleep predicts memory consolidation in humans. Proc Natl Acad Sci USA 113(26):7272–7277. https://doi.org/10.1073/pnas.1518202113

    Article  CAS  PubMed  Google Scholar 

  255. Abraham WC, Robins A (2005) Memory retention—the synaptic stability versus plasticity dilemma. Trends Neurosci 28(2):73–78. https://doi.org/10.1016/j.tins.2004.12.003

    Article  CAS  PubMed  Google Scholar 

  256. Seibt J, Richard CJ, Sigl-Glöckner J, Takahashi N, Kaplan DI, Doron G, de Limoges D, Bocklisch C, Larkum ME (2017) Cortical dendritic activity correlates with spindle-rich oscillations during sleep in rodents. Nat Commun 8(1):684. https://doi.org/10.1038/s41467-017-00735-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  257. Morris RGM (2006) Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci 23(11):2829–2846. https://doi.org/10.1111/j.1460-9568.2006.04888.x

    Article  CAS  PubMed  Google Scholar 

  258. Mizuseki K, Miyawaki H (2017) Hippocampal information processing across sleep/wake cycles. Neurosci Res 118:30–47. https://doi.org/10.1016/j.neures.2017.04.018

    Article  PubMed  Google Scholar 

  259. Wulff P, Ponomarenko AA, Bartos M, Korotkova TM, Fuchs EC, Bähner F, Both M, Tort AB, Kopell NJ, Wisden W, Monyer H (2009) Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons. Proc Natl Acad Sci USA 106(9):3561–3566. https://doi.org/10.1073/pnas.0813176106

    Article  PubMed  Google Scholar 

  260. Amilhon B, Huh CY, Manseau F, Ducharme G, Nichol H, Adamantidis A, Williams S (2015) Parvalbumin interneurons of hippocampus tune population activity at theta frequency. Neuron 86(5):1277–1289. https://doi.org/10.1016/j.neuron.2015.05.027

    Article  CAS  PubMed  Google Scholar 

  261. Averkin RG, Szemenyei V, Bordé S, Tamás G (2016) Identified cellular correlates of neocortical ripple and high-gamma oscillations during spindles of natural sleep. Neuron 92(4):916–928. https://doi.org/10.1016/j.neuron.2016.09.032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  262. Niethard N, Burgalossi A, Born J (2017) Plasticity during sleep is linked to specific regulation of cortical circuit activity. Front Neural Circuits 11:65. https://doi.org/10.3389/fncir.2017.00065

    Article  PubMed  PubMed Central  Google Scholar 

  263. Ognjanovski N, Schaeffer S, Wu J, Mofakham S, Maruyama D, Zochowski M, Aton SJ (2017) Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation. Nat Commun 8:15039. https://doi.org/10.1038/ncomms15039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  264. Steriade M, McCormick DA, Sejnowski TJ (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262(5134):679–685

    Article  CAS  Google Scholar 

  265. Buzsáki G (2002) Theta oscillations in the hippocampus. Neuron 33(3):325–340. https://doi.org/10.1016/s0896-6273(02)00586-x

    Article  PubMed  Google Scholar 

  266. Norman KA, Newman EL, Perotte AJ (2005) Methods for reducing interference in the complementary learning systems model: oscillating inhibition and autonomous memory rehearsal. Neural Netw 18(9):1212–1228. https://doi.org/10.1016/j.neunet.2005.08.010

    Article  PubMed  Google Scholar 

  267. Dahan L, Astier B, Vautrelle N, Urbain N, Kocsis B, Chouvet G (2007) Prominent burst firing of dopaminergic neurons in the ventral tegmental area during paradoxical sleep. Neuropsychopharmacology 32(6):1232–1241. https://doi.org/10.1038/sj.npp.1301251

    Article  CAS  PubMed  Google Scholar 

  268. Valdes JL, McNaughton BL, Fellous JM (2015) Offline reactivation of experience-dependent neuronal firing patterns in the rat ventral tegmental area. J Neurophysiol 114(2):1183–1195. https://doi.org/10.1152/jn.00758.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  269. Gomperts SN, Kloosterman F, Wilson MA (2015) VTA neurons coordinate with the hippocampal reactivation of spatial experience. Elife. https://doi.org/10.7554/eLife.05360

    Article  PubMed  PubMed Central  Google Scholar 

  270. Eschenko O, Sara SJ (2008) Learning-dependent, transient increase of activity in noradrenergic neurons of locus coeruleus during slow wave sleep in the rat: brain stem-cortex interplay for memory consolidation? Cereb Cortex 18(11):2596–2603. https://doi.org/10.1093/cercor/bhn020

    Article  PubMed  Google Scholar 

  271. Takeuchi T, Duszkiewicz AJ, Sonneborn A, Spooner PA, Yamasaki M, Watanabe M, Smith CC, Fernández G, Deisseroth K, Greene RW, Morris RGM (2016) Locus coeruleus and dopaminergic consolidation of everyday memory. Nature 537(7620):357. https://doi.org/10.1038/nature19325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  272. Lee MG, Hassani OK, Alonso A, Jones BE (2005) Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J Neurosci 25(17):4365–4369. https://doi.org/10.1523/JNEUROSCI.0178-05.2005

    Article  CAS  PubMed  Google Scholar 

  273. Lin SC, Gervasoni D, Nicolelis MA (2006) Fast modulation of prefrontal cortex activity by basal forebrain noncholinergic neuronal ensembles. J Neurophysiol 96(6):3209–3219. https://doi.org/10.1152/jn.00524.2006

    Article  PubMed  Google Scholar 

  274. Lima RH, Radiske A, Köhler CA, Gonzalez MC, Bevilaqua LR, Rossato JI, Medina JH, Cammarota M (2013) Nicotine modulates the long-lasting storage of fear memory. Learn Mem 20(3):120–124. https://doi.org/10.1101/lm.029900.112

    Article  CAS  PubMed  Google Scholar 

  275. Floresco SB, West AR, Ash B, Moore H, Grace AA (2003) Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat Neurosci 6(9):968–973. https://doi.org/10.1038/nn1103

    Article  CAS  PubMed  Google Scholar 

  276. Leonard CS, Llinás R (1994) Serotonergic and cholinergic inhibition of mesopontine cholinergic neurons controlling REM sleep: an in vitro electrophysiological study. Neuroscience 59(2):309–330

    Article  CAS  Google Scholar 

  277. Datta S, Siwek DF (1997) Excitation of the brain stem pedunculopontine tegmentum cholinergic cells induces wakefulness and REM sleep. J Neurophysiol 77(6):2975–2988. https://doi.org/10.1152/jn.1997.77.6.2975

    Article  CAS  PubMed  Google Scholar 

  278. Rye DB (1997) Contributions of the pedunculopontine region to normal and altered REM sleep. Sleep 20(9):757–788

    Article  CAS  Google Scholar 

  279. Datta S, Spoley EE, Patterson EH (2001) Microinjection of glutamate into the pedunculopontine tegmentum induces REM sleep and wakefulness in the rat. Am J Physiol Regul Integr Comp Physiol 280(3):R752–R759. https://doi.org/10.1152/ajpregu.2001.280.3.R752

    Article  CAS  PubMed  Google Scholar 

  280. Datta S (2002) Evidence that REM sleep is controlled by the activation of brain stem pedunculopontine tegmental kainate receptor. J Neurophysiol 87(4):1790–1798. https://doi.org/10.1152/jn.00763.2001

    Article  CAS  PubMed  Google Scholar 

  281. Lu J, Sherman D, Devor M, Saper CB (2006) A putative flip–flop switch for control of REM sleep. Nature 441(7093):589–594. https://doi.org/10.1038/nature04767

    Article  CAS  PubMed  Google Scholar 

  282. Kim JJ, Fanselow MS (1992) Modality-specific retrograde amnesia of fear. Science 256(5057):675–677

    Article  CAS  Google Scholar 

  283. Tamminen J, Payne JD, Stickgold R, Wamsley EJ, Gaskell MG (2010) Sleep spindle activity is associated with the integration of new memories and existing knowledge. J Neurosci 30(43):14356–14360. https://doi.org/10.1523/JNEUROSCI.3028-10.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  284. Dragoi G, Tonegawa S (2013) Development of schemas revealed by prior experience and NMDA receptor knock-out. Elife 2:e01326. https://doi.org/10.7554/eLife.01326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  285. Tamminen J, Lambon Ralph MA, Lewis PA (2013) The role of sleep spindles and slow-wave activity in integrating new information in semantic memory. J Neurosci 33(39):15376–15381. https://doi.org/10.1523/JNEUROSCI.5093-12.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  286. Durrant SJ, Cairney SA, McDermott C, Lewis PA (2015) Schema-conformant memories are preferentially consolidated during REM sleep. Neurobiol Learn Mem 122:41–50. https://doi.org/10.1016/j.nlm.2015.02.011

    Article  PubMed  Google Scholar 

  287. Hennies N, Lambon Ralph MA, Kempkes M, Cousins JN, Lewis PA (2016) Sleep spindle density predicts the effect of prior knowledge on memory consolidation. J Neurosci 36(13):3799–3810. https://doi.org/10.1523/JNEUROSCI.3162-15.2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  288. Gilboa A, Marlatte H (2017) Neurobiology of schemas and schema-mediated memory. Trends Cogn Sci. https://doi.org/10.1016/j.tics.2017.04.013

    Article  PubMed  Google Scholar 

  289. Groch S, Schreiner T, Rasch B, Huber R, Wilhelm I (2017) Prior knowledge is essential for the beneficial effect of targeted memory reactivation during sleep. Sci Rep 7:39763. https://doi.org/10.1038/srep39763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  290. Noack H, Schick W, Mallot H, Born J (2017) Sleep enhances knowledge of routes and regions in spatial environments. Learn Mem 24(3):140–144. https://doi.org/10.1101/lm.043984.116

    Article  PubMed  PubMed Central  Google Scholar 

  291. Tamminen J, Lambon Ralph MA, Lewis PA (2017) Targeted memory reactivation of newly learned words during sleep triggers REM-mediated integration of new memories and existing knowledge. Neurobiol Learn Mem 137:77–82. https://doi.org/10.1016/j.nlm.2016.11.012

    Article  PubMed  Google Scholar 

  292. Ohki T, Takei Y (2018) Neural mechanisms of mental schema: a triplet of delta, low beta/spindle and ripple oscillations. Eur J Neurosci. https://doi.org/10.1111/ejn.13844

    Article  PubMed  Google Scholar 

  293. Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA, Wood ER, Witter MP, Morris RGM (2007) Schemas and memory consolidation. Science 316(5821):76–82. https://doi.org/10.1126/science.1135935

    Article  CAS  PubMed  Google Scholar 

  294. Bethus I, Tse D, Morris RGM (2010) Dopamine and memory: modulation of the persistence of memory for novel hippocampal NMDA receptor-dependent paired associates. J Neurosci 30(5):1610–1618. https://doi.org/10.1523/JNEUROSCI.2721-09.2010

    Article  CAS  PubMed  Google Scholar 

  295. Tse D, Takeuchi T, Kakeyama M, Kajii Y, Okuno H, Tohyama C, Bito H, Morris RGM (2011) Schema-dependent gene activation and memory encoding in neocortex. Science 333(6044):891–895. https://doi.org/10.1126/science.1205274

    Article  CAS  PubMed  Google Scholar 

  296. Wang S-H, Tse D, Morris RGM (2012) Anterior cingulate cortex in schema assimilation and expression. Learn Mem 19(8):315–318. https://doi.org/10.1101/lm.026336.112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

Support obtained from the Federal University of Rio Grande do Norte, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Grants 308775/2015-5 and 408145/2016-1 to SR; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (STIC AmSud 062/2015) to SR; Fundação de Amparo à Pesquisa do Rio Grande do Norte Grant Pronem 003/2011 to SR; Fundação de Amparo à Pesquisa do Estado de São Paulo Grant #2013/07699-0 Center for Neuromathematics to SR, Pew Latin American Fellows Program to SR; CAPES/COFECUB Grant 783/13 to CMQ; CAPES PhD scholarship to DGAF.

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Almeida-Filho, D.G., Queiroz, C.M. & Ribeiro, S. Memory corticalization triggered by REM sleep: mechanisms of cellular and systems consolidation. Cell. Mol. Life Sci. 75, 3715–3740 (2018). https://doi.org/10.1007/s00018-018-2886-9

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