Skip to main content

A Role for Neuronal Oscillations of Sleep in Memory and Cognition

  • Chapter
  • First Online:
Book cover Neuronal Oscillations of Wakefulness and Sleep

Abstract

This chapter gives an overview on relevant topics pertaining to cognition, in particular to memory consolidation during sleep. First, a brief overview on the extent of research on this topic in several nonmammalian species is given. Then neuronal oscillations are described with a main focus on sleep spindles and slow oscillations, and their occurrence in human scalp EEG. In particular, the relevance of discriminating between slow and fast spindle oscillations measured in different sleep states is underscored. Findings on memory consolidation based on the ability to induce neuronal oscillations of sleep without significant perturbation of the subsequent sleep architecture are reported next. Studies highlighting essential aspects of sleep’s effect on memory are then presented together with a discussion on postexperience neuronal oscillations during sleep. A summary puts the interdependence of neuronal oscillations and cognitive processes during sleep into a broader biological perspective.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Notes

  1. 1.

    Note that slow oscillation will be used here as defined electrophysiologically, i.e. human EEG large amplitude oscillations during NREM sleep, >−80 μV negative peak, >140 μV peak-to peak, in a 3.5 Hz low-pass filtered signal, with lengths between positive-to-negative zero crossings from 0.9 to 2 s [39].

References

  1. Abel T, Kandel E. Positive and negative regulatory mechanisms that mediate long-term memory storage. Brain Res Brain Res Rev. 1998;26(2–3):360–78.

    Article  CAS  PubMed  Google Scholar 

  2. Bushey D, Cirelli C. From genetics to structure to function: exploring sleep in Drosophila. Int Rev Neurobiol. 2011;99:213–44.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Kamyshev NG, Iliadi KG, Bragina JV. Drosophila conditioned courtship: two ways of testing memory. Learn Mem. 1999;6(1):1–20.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Zimmerman JE, Naidoo N, Raizen DM, Pack AI. Conservation of sleep: insights from non-mammalian model systems. Trends Neurosci. 2008;31(7):371–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Yap MHW, Grabowska MJ, Rohrscheib C, Jeans R, Troup M, Paulk AC, et al. Oscillatory brain activity in spontaneous and induced sleep stages in flies. Nat Commun. 2017;8(1):1815.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Davis RL. Traces of Drosophila memory. Neuron. 2011;70(1):8–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Pan Y, Zhou Y, Guo C, Gong H, Gong Z, Liu L. Differential roles of the fan-shaped body and the ellipsoid body in Drosophila visual pattern memory. Learn Mem. 2009;16(5):289–95.

    Article  PubMed  Google Scholar 

  8. Van Swinderen B. Fly memory: a mushroom body story in parts. Curr Biol. 2009;19(18):R855–7.

    Article  PubMed  CAS  Google Scholar 

  9. Beyaert L, Greggers U, Menzel R. Honeybees consolidate navigation memory during sleep. J Exp Biol. 2012;215(Pt 22):3981–8.

    Article  PubMed  Google Scholar 

  10. Zwaka H, Bartels R, Gora J, Franck V, Culo A, Gotsch M, et al. Context odor presentation during sleep enhances memory in honeybees. Curr Biol. 2015;25(21):2869–74.

    Article  CAS  PubMed  Google Scholar 

  11. Ramon F, Mendoza-Angeles K, Hernandez-Falcon J. Sleep in invertebrates: crayfish. Front Biosci (Schol Ed). 2012;4:1190–200.

    Article  Google Scholar 

  12. Bierbower SM, Shuranova ZP, Viele K, Cooper RL. Comparative study of environmental factors influencing motor task learning and memory retention in sighted and blind crayfish. Brain Behav. 2013;3(1):4–13.

    Article  PubMed  Google Scholar 

  13. Tierney AJ, Lee J. Spatial learning in a T-maze by the crayfish Orconectes rusticus. J Comp Psychol. 2011;125(1):31–9.

    Article  PubMed  Google Scholar 

  14. Rattenborg NC, Martinez-Gonzalez D, Roth TC, Pravosudov VV. Hippocampal memory consolidation during sleep: a comparison of mammals and birds. Biol Rev Camb Philos Soc. 2011;86(3):658–91.

    Article  PubMed  Google Scholar 

  15. Tobler I, Borbély A. Sleep and EEG spectra in the pigeon (Columba livia) under baseline condtions and after sleep deprivation. J Comp Physiol A. 1988;163:729–38.

    Article  Google Scholar 

  16. van der Meij J, Martinez-Gonzalez D, Beckers GJL, Rattenborg NC. Intra-“cortical” activity during avian non-REM and REM sleep: variant and invariant traits between birds and mammals. Sleep. 2019;42(2).

    Google Scholar 

  17. Jackson C, McCabe BJ, Nicol AU, Grout AS, Brown MW, Horn G. Dynamics of a memory trace: effects of sleep on consolidation. Curr Biol. 2008;18(6):393–400.

    Article  CAS  PubMed  Google Scholar 

  18. Nelini C, Bobbo D, Mascetti GG. Local sleep: a spatial learning task enhances sleep in the right hemisphere of domestic chicks (Gallus gallus). Exp Brain Res. 2010;205(2):195–204.

    Article  PubMed  Google Scholar 

  19. Peyrache A, Battaglia FP, Destexhe A. Inhibition recruitment in prefrontal cortex during sleep spindles and gating of hippocampal inputs. Proc Natl Acad Sci U S A. 2011;108(41):17207–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Wierzynski CM, Lubenov EV, Gu M, Siapas AG. State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron. 2009;61(4):587–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Csercsa R, Dombovari B, Fabo D, Wittner L, Eross L, Entz L, et al. Laminar analysis of slow wave activity in humans. Brain. 2010;133(9):2814–29.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Sanchez-Vives MV, Mattia M, Compte A, Perez-Zabalza M, Winograd M, Descalzo VF, et al. Inhibitory modulation of cortical up states. J Neurophysiol. 2010;104(3):1314–24.

    Article  PubMed  Google Scholar 

  23. Destexhe A, Sejnowski TJ. Thalamocortical assemblies. Oxford, UK: Oxford University Press; 2001.

    Google Scholar 

  24. Steriade M, Deschenes M. The thalamus as a neuronal oscillator. Brain Res. 1984;320(1):1–63.

    Article  CAS  PubMed  Google Scholar 

  25. Steriade M, McCarley RW. Synchronized brain oscillations leading to neuronal plasticity during waking and sleep states. In: Brain control of wakefulness and sleep. 2nd ed. New York: Springer; 2005. p. 255–344.

    Google Scholar 

  26. Contreras D, Destexhe A, Sejnowski TJ, Steriade M. Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback. Science. 1996;274(5288):771–4.

    Article  CAS  PubMed  Google Scholar 

  27. Mak-McCully RA, Rolland M, Sargsyan A, Gonzalez C, Magnin M, Chauvel P, et al. Coordination of cortical and thalamic activity during non-REM sleep in humans. Nat Commun. 2017;8:15499.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Gardner RJ, Hughes SW, Jones MW. Differential spike timing and phase dynamics of reticular thalamic and prefrontal cortical neuronal populations during sleep spindles. J Neurosci. 2013;33(47):18469–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Bartho P, Slezia A, Matyas F, Faradzs-Zade L, Ulbert I, Harris KD, et al. Ongoing network state controls the length of sleep spindles via inhibitory activity. Neuron. 2014;82(6):1367–79.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Andrillon T, Ni Y, Staba RJ, Ferrarelli F, Cirelli C, Tononi G, et al. Sleep spindles in humans: insights from intracranial EEG and unit recordings. J Neurosci. 2011;31(49):17821–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Dehghani N, Cash SS, Halgren E. Emergence of synchronous EEG spindles from asynchronous MEG spindles. Hum Brain Mapp. 2011;32(12):2217–27.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Nakamura M, Uchida S, Maehara T, Kawai K, Hirai N, Nakabayashi T, et al. Sleep spindles in human prefrontal cortex: an electrocorticographic study. Neurosci Res. 2003;45(4):419–27.

    Article  PubMed  Google Scholar 

  33. Peter-Derex L, Comte JC, Mauguiere F, Salin PA. Density and frequency caudo-rostral gradients of sleep spindles recorded in the human cortex. Sleep. 2012;35(1):69–79.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Dehghani N, Cash SS, Chen CC, Hagler DJ Jr, Huang M, Dale AM, et al. Divergent cortical generators of MEG and EEG during human sleep spindles suggested by distributed source modeling. PLoS One. 2010;5(7):e11454.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Del Felice A, Arcaro C, Storti SF, Fiaschi A, Manganotti P. Electrical source imaging of sleep spindles. Clin EEG Neurosci. 2013;45(3):184–92.

    Article  Google Scholar 

  36. Clemens Z, Mölle M, Eross L, Barsi P, Halasz P, Born J. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain. 2007;130(Pt 11):2868–78.

    Article  PubMed  Google Scholar 

  37. Anderer P, Klosch G, Gruber G, Trenker E, Pascual-Marqui RD, Zeitlhofer J, et al. Low-resolution brain electromagnetic tomography revealed simultaneously active frontal and parietal sleep spindle sources in the human cortex. Neuroscience. 2001;103(3):581–92.

    Article  CAS  PubMed  Google Scholar 

  38. Clemens Z, Mölle M, Eross L, Jakus R, Rasonyi G, Halasz P, et al. Fine-tuned coupling between human parahippocampal ripples and sleep spindles. Eur J Neurosci. 2011;33(3):511–20.

    Article  PubMed  Google Scholar 

  39. Mölle M, Bergmann TO, Marshall L, Born J. Fast and slow spindles during the sleep slow oscillation: disparate coalescence and engagement in memory processing. Sleep. 2011;34(10):1411–21.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Slezia A, Hangya B, Ulbert I, Acsady L. Phase advancement and nucleus-specific timing of thalamocortical activity during slow cortical oscillation. J Neurosci. 2011;31(2):607–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hagler DJ Jr, Ulbert I, Wittner L, Eross L, Madsen JR, Devinsky O, et al. Heterogeneous origins of human sleep spindles in different cortical layers. J Neurosci. 2018;38(12):3013–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Clawson BC, Durkin J, Aton SJ. Form and function of sleep spindles across the lifespan. Neural Plast. 2016;2016:6936381.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Cox R, Schapiro AC, Manoach DS, Stickgold R. Individual differences in frequency and topography of slow and fast sleep spindles. Front Hum Neurosci. 2017;11:433.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Fogel SM, Smith CT. Learning-dependent changes in sleep spindles and stage 2 sleep. J Sleep Res. 2006;15(3):250–5.

    Article  PubMed  Google Scholar 

  45. Gaillard JM, Blois R. Spindle density in sleep of normal subjects. Sleep. 1981;4(4):385–91.

    Article  CAS  PubMed  Google Scholar 

  46. Gais S, Molle M, Helms K, Born J. Learning-dependent increases in sleep spindle density. J Neurosci. 2002;22(15):6830–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Mölle M, Marshall L, Gais S, Born J. Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations. Proc Natl Acad Sci U S A. 2004;101(38):13963–8.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Peters KR, Ray L, Smith V, Smith C. Changes in the density of stage 2 sleep spindles following motor learning in young and older adults. J Sleep Res. 2008;17(1):23–33.

    Article  PubMed  Google Scholar 

  49. van Kesteren MT, Rijpkema M, Ruiter DJ, Fernandez G. Retrieval of associative information congruent with prior knowledge is related to increased medial prefrontal activity and connectivity. J Neurosci. 2010;30(47):15888–94.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Wamsley EJ, Tucker MA, Shinn AK, Ono KE, McKinley SK, Ely AV, et al. Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation? Biol Psychiatry. 2012;71(2):154–61.

    Article  PubMed  Google Scholar 

  51. Martin N, Lafortune M, Godbout J, Barakat M, Robillard R, Poirier G, et al. Topography of age-related changes in sleep spindles. Neurobiol Aging. 2013;34(2):468–76.

    Article  PubMed  Google Scholar 

  52. Mölle M, Eschenko O, Gais S, Sara SJ, Born J. The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats. Eur J Neurosci. 2009;29(5):1071–81.

    Article  PubMed  Google Scholar 

  53. Steriade M. Cellular substrates of brain rhythms. In: Niedermeyer E, Lopes F, editors. Electroencephalography: basic principles, clinical applications, and related fields. Baltimore: William & Wilkins; 1993. p. 27–62.

    Google Scholar 

  54. Steriade M, Nunez A, Amzica F. Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci. 1993;13(8):3266–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Steriade M, Nunez A, Amzica F. A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci. 1993;13(8):3252–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Nir Y, Staba RJ, Andrillon T, Vyazovskiy VV, Cirelli C, Fried I, et al. Regional slow waves and spindles in human sleep. Neuron. 2011;70(1):153–69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Steriade M. Grouping of brain rhythms in corticothalamic systems. Neuroscience. 2006;137(4):1087–106.

    Article  CAS  PubMed  Google Scholar 

  58. Timofeev I, Grenier F, Steriade M. Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study. Proc Natl Acad Sci U S A. 2001;98(4):1924–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Volgushev M, Chauvette S, Mukovski M, Timofeev I. Precise long-range synchronization of activity and silence in neocortical neurons during slow-wave oscillations. J Neurosci. 2006;26(21):5665–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Huber R, Ghilardi MF, Massimini M, Ferrarelli F, Riedner BA, Peterson MJ, et al. Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nat Neurosci. 2006;9(9):1169–76.

    Article  CAS  PubMed  Google Scholar 

  61. Huber R, Ghilardi MF, Massimini M, Tononi G. Local sleep and learning. Nature. 2004;430(6995):78–81.

    Article  CAS  PubMed  Google Scholar 

  62. Krueger JM, Nguyen JT, Dykstra-Aiello CJ, Taishi P. Local sleep. Sleep Med Rev. 2018;43:14–21.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Poskanzer KE, Yuste R. Astrocytes regulate cortical state switching in vivo. Proc Natl Acad Sci U S A. 2016;113(19):E2675–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Szabo Z, Heja L, Szalay G, Kekesi O, Furedi A, Szebenyi K, et al. Extensive astrocyte synchronization advances neuronal coupling in slow wave activity in vivo. Sci Rep. 2017;7(1):6018.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Menicucci D, Piarulli A, Debarnot U, d’Ascanio P, Landi A, Gemignani A. Functional structure of spontaneous sleep slow oscillation activity in humans. PLoS One. 2009;4(10):e7601.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Riedner BA, Vyazovskiy VV, Huber R, Massimini M, Esser S, Murphy M, et al. Sleep homeostasis and cortical synchronization: III. A high-density EEG study of sleep slow waves in humans. Sleep. 2007;30(12):1643–57.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Diekelmann S, Born J. The memory function of sleep. Nat Rev Neurosci. 2010;11(2):114–26.

    Article  CAS  PubMed  Google Scholar 

  68. Funk CM, Peelman K, Bellesi M, Marshall W, Cirell C, Tononi G. Role of Somatostatin-positive cortical interneurons in the generation of sleep slow waves. J Neurosci. 2017;37(38):9132–48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Niethard N, Ngo HV, Ehrlich I, Born J. Cortical circuit activity underlying sleep slow oscillations and spindles. Proc Natl Acad Sci U S A. 2018;115(39):E9220–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Rasch B, Born J. About sleep’s role in memory. Physiol Rev. 2013;93(2):681–766.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Crunelli V, David F, Lorincz ML, Hughes SW. The thalamocortical network as a single slow wave-generating unit. Curr Opin Neurobiol. 2015;31:72–80.

    Article  CAS  PubMed  Google Scholar 

  72. Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, et al. High gamma power is phase-locked to theta oscillations in human neocortex. Science. 2006;313(5793):1626–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Cox R, Mylonas DS, Manoach DS, Stickgold R. Large-scale structure and individual fingerprints of locally coupled sleep oscillations. Sleep. 2018;41(12).

    Google Scholar 

  74. Dang-Vu TT, Bonjean M, Schabus M, Boly M, Darsaud A, Desseilles M, et al. Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep. Proc Natl Acad Sci U S A. 2011;108(37):15438–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Ngo HV, Martinetz T, Born J, Molle M. Auditory closed-loop stimulation of the sleep slow oscillation enhances memory. Neuron. 2013;78(3):545–53.

    Article  CAS  PubMed  Google Scholar 

  76. Riedner BA, Hulse BK, Murphy MJ, Ferrarelli F, Tononi G. Temporal dynamics of cortical sources underlying spontaneous and peripherally evoked slow waves. Prog Brain Res. 2011;193:201–18.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Ruch S, Koenig T, Mathis J, Roth C, Henke K. Word encoding during sleep is suggested by correlations between word-evoked up-states and post-sleep semantic priming. Front Psychol. 2014;5:1319.

    PubMed  PubMed Central  Google Scholar 

  78. Schabus M, Dang-Vu TT, Heib DP, Boly M, Desseilles M, Vandewalle G, et al. The fate of incoming stimuli during NREM sleep is determined by spindles and the phase of the slow oscillation. Front Neurol. 2012;3:40.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Vyazovskiy VV, Faraguna U, Cirelli C, Tononi G. Triggering slow waves during NREM sleep in the rat by intracortical electrical stimulation: effects of sleep/wake history and background activity. J Neurophysiol. 2009;101(4):1921–31.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Wilckens KA, Ferrarelli F, Walker MP, Buysse DJ. Slow-wave activity enhancement to improve cognition. Trends Neurosci. 2018;41(7):470–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Weigenand A, Molle M, Werner F, Martinetz T, Marshall L. Timing matters: open-loop stimulation does not improve overnight consolidation of word pairs in humans. Eur J Neurosci. 2016;44(6):2357–68.

    Article  PubMed  PubMed Central  Google Scholar 

  82. Binder S, Baier PC, Molle M, Inostroza M, Born J, Marshall L. Sleep enhances memory consolidation in the hippocampus-dependent object-place recognition task in rats. Neurobiol Learn Mem. 2012;97(2):213–9.

    Article  PubMed  Google Scholar 

  83. Cox R, Hofman WF, Talamini LM. Involvement of spindles in memory consolidation is slow wave sleep-specific. Learn Mem. 2012;19(7):264–7.

    Article  PubMed  Google Scholar 

  84. Bergmann TO, Mölle M, Schmidt MA, Lindner C, Marshall L, Born J, et al. EEG-guided transcranial magnetic stimulation reveals rapid shifts in motor cortical excitability during the human sleep slow oscillation. J Neurosci. 2012;32(1):243–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Manganotti P, Formaggio E, Del FA, Storti SF, Zamboni A, Bertoldo A, et al. Time-frequency analysis of short-lasting modulation of EEG induced by TMS during wake, sleep deprivation and sleep. Front Hum Neurosci. 2013;7:767.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Marshall L, Born J. Brain stimulation during sleep. In: Stickgold R, editor. Sleep medicine clinics. Philadelphia: WB Saunders; 2011. p. 85–95.

    Google Scholar 

  87. Massimini M, Ferrarelli F, Esser SK, Riedner BA, Huber R, Murphy M, et al. Triggering sleep slow waves by transcranial magnetic stimulation. Proc Natl Acad Sci U S A. 2007;104(20):8496–501.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Bergmann TO, Mölle M, Marshall L, Kaya-Yildiz L, Born J, Roman SH. A local signature of LTP- and LTD-like plasticity in human NREM sleep. Eur J Neurosci. 2008;27(9):2241–9.

    Article  PubMed  Google Scholar 

  89. Huber R, Maatta S, Esser SK, Sarasso S, Ferrarelli F, Watson A, et al. Measures of cortical plasticity after transcranial paired associative stimulation predict changes in electroencephalogram slow-wave activity during subsequent sleep. J Neurosci. 2008;28(31):7911–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Fröhlich F, McCormick DA. Endogenous electric fields may guide neocortical network activity. Neuron. 2010;67(1):129–43.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Liu A, Voroslakos M, Kronberg G, Henin S, Krause MR, Huang Y, et al. Immediate neurophysiological effects of transcranial electrical stimulation. Nat Commun. 2018;9:5092.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Ali MM, Sellers KK, Frohlich F. Transcranial alternating current stimulation modulates large-scale cortical network activity by network resonance. J Neurosci. 2013;33(27):11262–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Vosskuhl J, Struber D, Herrmann CS. Non-invasive brain stimulation: a paradigm shift in understanding brain oscillations. Front Hum Neurosci. 2018;12:211.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Campos-Beltrán D, Marshall L. Electric stimulation to improve memory consolidation during sleep. In: Axmacher N, Rasch B, editors. Cognitive neuroscience of memory consolidation. New York: Springer; 2017. p. 301–12.

    Chapter  Google Scholar 

  95. Ladenbauer J, Ladenbauer J, Kulzow N, de Boor R, Avramova E, Grittner U, et al. Promoting sleep oscillations and their functional coupling by transcranial stimulation enhances memory consolidation in mild cognitive impairment. J Neurosci. 2017;37(30):7111–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Marshall L, Binder S. Contribution of transcranial oscillatory stimulation to research on neural networks: an emphasis on hippocampo-neocortical rhythms. Front Hum Neurosci. 2013;7:614.

    Article  PubMed  PubMed Central  Google Scholar 

  97. Marshall L, Helgadottir H, Mölle M, Born J. Boosting slow oscillations during sleep potentiates memory. Nature. 2006;444(7119):610–3.

    Article  CAS  PubMed  Google Scholar 

  98. Voss U, Holzmann R, Tuin I, Hobson JA. Lucid dreaming: a state of consciousness with features of both waking and non-lucid dreaming. Sleep. 2009;32(9):1191–200.

    Article  PubMed  PubMed Central  Google Scholar 

  99. Voss U, Holzmann R, Hobson A, Paulus W, Koppehele-Gossel J, Klimke A, et al. Induction of self awareness in dreams through frontal low current stimulation of gamma activity. Nat Neurosci. 2014;17(6):810–2.

    Article  CAS  PubMed  Google Scholar 

  100. Berryhill ME, Peterson DJ, Jones KT, Stephens JA. Hits and misses: leveraging tDCS to advance cognitive research. Front Psychol. 2014;5:800.

    Article  PubMed  PubMed Central  Google Scholar 

  101. Koo PC, Molle M, Marshall L. Efficacy of slow oscillatory-transcranial direct current stimulation on EEG and memory—contribution of an inter-individual factor. Eur J Neurosci. 2018;47(7):812–23.

    Article  PubMed  Google Scholar 

  102. David F, Schmiedt JT, Taylor HL, Orban G, Di GG, Uebele VN, et al. Essential thalamic contribution to slow waves of natural sleep. J Neurosci. 2013;33(50):19599–610.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Alhola P, Polo-Kantola P. Sleep deprivation: impact on cognitive performance. Neuropsychiatr Dis Treat. 2007;3(5):553–67.

    PubMed  PubMed Central  Google Scholar 

  104. Goel N, Rao H, Durmer JS, Dinges DF. Neurocognitive consequences of sleep deprivation. Semin Neurol. 2009;29(4):320–39.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Jenkins JK, Dallenbach KM. Obliviscence during sleep and waking. Am J Phys. 1924;35:605–12.

    Google Scholar 

  106. Graves EA. The effect of sleep on retention. J Exp Psychol. 1937;19:316–22.

    Article  Google Scholar 

  107. Newman EB. Forgetting of meaningful material during sleep and waking. Am J Psychol. 1939;52:65–71.

    Article  Google Scholar 

  108. Talamini LM, Nieuwenhuis IL, Takashima A, Jensen O. Sleep directly following learning benefits consolidation of spatial associative memory. Learn Mem. 2008;15(4):233–7.

    Article  PubMed  Google Scholar 

  109. Maatta S, Landsness E, Sarasso S, Ferrarelli F, Ferreri F, Ghilardi MF, et al. The effects of morning training on night sleep: a behavioral and EEG study. Brain Res Bull. 2010;82(1–2):118–23.

    Article  PubMed  PubMed Central  Google Scholar 

  110. McGaugh JL. Memory—a century of consolidation. Science. 2000;287(5451):248–51.

    Article  CAS  PubMed  Google Scholar 

  111. Aserinsky E, Kleitman N. Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. J Neuropsychiatry Clin Neurosci. 1953;15(4):454–5.

    Article  Google Scholar 

  112. Dement WC, Kleitman N. Cyclic variations in EEG during sleep and their relation to eye movements, body motility, and dreaming. Electroencephalogr Clin Neurophysiol. 1957;9(4):673–90.

    Article  CAS  PubMed  Google Scholar 

  113. Empson JA, Clarke PR. Rapid eye movements and remembering. Nature. 1970;227(5255):287–8.

    Article  CAS  PubMed  Google Scholar 

  114. Fowler MJ, Sullivan MJ, Ekstrand BR. Sleep and memory. Science. 1973;179(4070):302–4.

    Article  CAS  PubMed  Google Scholar 

  115. Yaroush R, Sullivan MJ, Ekstrand BR. Effect of sleep on memory. II. Differential effect of the first and second half of the night. J Exp Psychol. 1971;88(3):361–6.

    Article  CAS  PubMed  Google Scholar 

  116. Cipolli C. Sleep and memory. In: Parmeggiani PL, Velluti RA, editors. The physiologic nature of sleep. London: Imperial College Press; 2005. p. 601–23.

    Chapter  Google Scholar 

  117. Giuditta A, Ambrosini MV, Montagnese P, Mandile P, Cotugno M, Grassi ZG, et al. The sequential hypothesis of the function of sleep. Behav Brain Res. 1995;69(1–2):157–66.

    Article  CAS  PubMed  Google Scholar 

  118. Rauchs G, Desgranges B, Foret J, Eustache F. The relationships between memory systems and sleep stages. J Sleep Res. 2005;14(2):123–40.

    Article  PubMed  Google Scholar 

  119. Mednick SC, Ca DJ, Shuman T, Anagnostaras S, Wixted JT. An opportunistic theory of cellular and systems consolidation. Trends Neurosci. 2011;34(10):504–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Baran B, Pace-Schott EF, Ericson C, Spencer RM. Processing of emotional reactivity and emotional memory over sleep. J Neurosci. 2012;32(3):1035–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Groch S, Wilhelm I, Diekelmann S, Born J. The role of REM sleep in the processing of emotional memories: evidence from behavior and event-related potentials. Neurobiol Learn Mem. 2013;99:1–9.

    Article  CAS  PubMed  Google Scholar 

  122. Menz MM, Rihm JS, Salari N, Born J, Kalisch R, Pape HC, et al. The role of sleep and sleep deprivation in consolidating fear memories. NeuroImage. 2013;75:87–96.

    Article  CAS  PubMed  Google Scholar 

  123. Nishida M, Pearsall J, Buckner RL, Walker MP. REM sleep, prefrontal theta, and the consolidation of human emotional memory. Cereb Cortex. 2009;19(5):1158–66.

    Article  PubMed  Google Scholar 

  124. Wagner U, Gais S, Born J. Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep. Learn Mem. 2001;8(2):112–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Datta S, O’Malley MW. Fear extinction memory consolidation requires potentiation of pontine-wave activity during REM sleep. J Neurosci. 2013;33(10):4561–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Popa D, Duvarci S, Popescu AT, Lena C, Pare D. Coherent amygdalocortical theta promotes fear memory consolidation during paradoxical sleep. Proc Natl Acad Sci U S A. 2010;107(14):6516–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Genzel L, Spoormaker VI, Konrad BN, Dresler M. The role of rapid eye movement sleep for amygdala-related memory processing. Neurobiol Learn Mem. 2015;122:110–21.

    Article  CAS  PubMed  Google Scholar 

  128. Totty MS, Chesney LA, Geist PA, Datta S. Sleep-dependent oscillatory synchronization: a role in fear memory consolidation. Front Neural Circuits. 2017;11:49.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  129. Cantero JL, Atienza M, Stickgold R, Kahana MJ, Madsen JR, Kocsis B. Sleep-dependent theta oscillations in the human hippocampus and neocortex. J Neurosci. 2003;23(34):10897–903.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Navarro-Lobato I, Genzel L. The up and down of sleep: from molecules to electrophysiology. Neurobiol Learn Mem. 2019;160:3–10.

    Article  PubMed  Google Scholar 

  131. Skelin I, Kilianski S, McNaughton BL. Hippocampal coupling with cortical and subcortical structures in the context of memory consolidation. Neurobiol Learn Mem. 2019;160:21–31.

    Article  PubMed  Google Scholar 

  132. Ulrich D. Sleep spindles as facilitators of memory formation and learning. Neural Plast. 2016;2016:1796715.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  133. Eschenko O, Magri C, Panzeri S, Sara SJ. Noradrenergic neurons of the locus coeruleus are phase locked to cortical up-down states during sleep. Cereb Cortex. 2012;22(2):426–35.

    Article  PubMed  Google Scholar 

  134. Lee MG, Hassani OK, Alonso A, Jones BE. Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J Neurosci. 2005;25(17):4365–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Naji M, Krishnan GP, McDevitt EA, Bazhenov M, Mednick SC. Coupling of autonomic and central events during sleep benefits declarative memory consolidation. Neurobiol Learn Mem. 2018;157:139–50.

    Article  PubMed  PubMed Central  Google Scholar 

  136. Genzel L, Dresler M, Wehrle R, Grozinger M, Steiger A. Slow wave sleep and REM sleep awakenings do not affect sleep dependent memory consolidation. Sleep. 2009;32(3):302–10.

    Article  PubMed  PubMed Central  Google Scholar 

  137. Morgenthaler J, Wiesner CD, Hinze K, Abels LC, Prehn-Kristensen A, Goder R. Selective REM-sleep deprivation does not diminish emotional memory consolidation in young healthy subjects. PLoS One. 2014;9(2):e89849.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  138. Feld GB, Born J. Sculpting memory during sleep: concurrent consolidation and forgetting. Curr Opin Neurobiol. 2017;44:20–7.

    Article  CAS  PubMed  Google Scholar 

  139. Gupta AS, van der Meer MA, Touretzky DS, Redish AD. Hippocampal replay is not a simple function of experience. Neuron. 2010;65(5):695–705.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Spencer RM. Neurophysiological basis of sleep’s function on memory and cognition. ISRN Physiol. 2013;2013:619319.

    Article  PubMed  PubMed Central  Google Scholar 

  141. Tamminen J, Payne JD, Stickgold R, Wamsley EJ, Gaskell MG. Sleep spindle activity is associated with the integration of new memories and existing knowledge. J Neurosci. 2010;30(43):14356–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Hirase H, Leinekugel X, Czurko A, Csicsvari J, Buzsaki G. Firing rates of hippocampal neurons are preserved during subsequent sleep episodes and modified by novel awake experience. Proc Nat. Acad Sci U S A. 2001;98(16):9386–90.

    Article  CAS  Google Scholar 

  143. Wilson MA, McNaughton BL. Reactivation of hippocampal ensemble memories during sleep. Science. 1994;265(5172):676–9. [See comments].

    Article  CAS  PubMed  Google Scholar 

  144. Clemens Z, Fabo D, Halasz P. Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience. 2005;132(2):529–35.

    Article  CAS  PubMed  Google Scholar 

  145. Pugin F, Metz AJ, Wolf M, Achermann P, Jenni OG, Huber R. Local increase of sleep slow wave activity after three weeks of working memory training in children and adolescents. Sleep. 2015;38(4):607–14.

    Article  PubMed  PubMed Central  Google Scholar 

  146. Ramadan W, Eschenko O, Sara SJ. Hippocampal sharp wave/ripples during sleep for consolidation of associative memory. PLoS One. 2009;4(8):e6697.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  147. Schmidt C, Peigneux P, Muto V, Schenkel M, Knoblauch V, Munch M, et al. Encoding difficulty promotes postlearning changes in sleep spindle activity during napping. J Neurosci. 2006;26(35):8976–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Buzsaki G. Two-stage model of memory trace formation: a role for “noisy” brain states. Neuroscience. 1989;31(3):551–70.

    Article  CAS  PubMed  Google Scholar 

  149. Buzsaki G, Haas HL, Anderson EG. Long-term potentiation induced by physiologically relevant stimulus patterns. Brain Res. 1987;435(1–2):331–3.

    Article  CAS  PubMed  Google Scholar 

  150. Marr D. A theory for cerebral neocortex. Proc R Soc Lond B Biol Sci. 1970;76(43):161–234.

    Google Scholar 

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

    CAS  Google Scholar 

  152. Chrobak JJ, Buzsaki G. High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci. 1996;16(9):3056–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Contreras D, Destexhe A, Steriade M. Intracellular and computational characterization of the intracortical inhibitory control of synchronized thalamic inputs in vivo. J Neurophysiol. 1997;78(1):335–50.

    Article  CAS  PubMed  Google Scholar 

  154. Rosanova M, Ulrich D. Pattern-specific associative long-term potentiation induced by a sleep spindle-related spike train. J Neurosci. 2005;25(41):9398–405.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Sejnowski TJ, Destexhe A. Why do we sleep? Brain Res. 2000;886(1–2):208–23.

    Article  CAS  PubMed  Google Scholar 

  156. Steriade M, McCormick DA, Sejnowski TJ. Thalamocortical oscillations in the sleeping and aroused brain. Science. 1993;262(5134):679–85.

    Article  CAS  PubMed  Google Scholar 

  157. O’Keefe J, Recce ML. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus. 1993;3(3):317–30.

    Article  PubMed  Google Scholar 

  158. Lee AK, Wilson MA. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron. 2002;36(6):1183–94.

    Article  CAS  PubMed  Google Scholar 

  159. Louie K, Wilson MA. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron. 2001;29(1):145–56.

    Article  CAS  PubMed  Google Scholar 

  160. Nadasdy Z, Hirase H, Czurko A, Csicsvari J, Buzsaki G. Replay and time compression of recurring spike sequences in the hippocampus. J Neurosci. 1999;19(21):9497–507.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Pavlides C, Winson J. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J Neurosci. 1989;9(8):2907–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Skaggs WE, McNaughton BL. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science. 1996;271(5257):1870–3.

    Article  CAS  PubMed  Google Scholar 

  163. Mölle M, Yeshenko O, Marshall L, Sara SJ, Born J. Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J Neurophysiol. 2006;96(1):62–70.

    Article  PubMed  Google Scholar 

  164. Siapas AG, Wilson MA. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron. 1998;21(5):1123–8.

    Article  CAS  PubMed  Google Scholar 

  165. Sirota A, Csicsvari J, Buhl D, Buzsaki G. Communication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci U S A. 2003;100(4):2065–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Brodt S, Pohlchen D, Flanagin VL, Glasaue S, Gais S, Schonauer M. Rapid and independent memory formation in the parietal cortex. Proc Natl Acad Sci U S A. 2016;113(46):13251–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Buhry L, Azizi AH, Cheng S. Reactivation, replay, and preplay: how it might all fit together. Neural Plast. 2011;2011:203462.

    Article  PubMed  PubMed Central  Google Scholar 

  168. Cox R, Hofman WF, de Boer M, Talamini LM. Local sleep spindle modulations in relation to specific memory cues. NeuroImage. 2014;99:103–10.

    Article  PubMed  Google Scholar 

  169. Fogel S, Albouy G, King BR, Lungu O, Vien C, Bore A, et al. Reactivation or transformation? Motor memory consolidation associated with cerebral activation time-locked to sleep spindles. PLoS One. 2017;12(4):e0174755.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  170. Oudiette D, Paller KA. Upgrading the sleeping brain with targeted memory reactivation. Trends Cogn Sci. 2013;17(3):142–9.

    Article  PubMed  Google Scholar 

  171. Pennartz CM, Lee E, Verheul J, Lipa P, Barnes CA, McNaughton BL. The ventral striatum in off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples. J Neurosci. 2004;24(29):6446–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Rasch B, Born J. Maintaining memories by reactivation. Curr Opin Neurobiol. 2007;17(6):698–703.

    Article  CAS  PubMed  Google Scholar 

  173. Sadowski JH, Jones MW, Mellor JR. Ripples make waves: binding structured activity and plasticity in hippocampal networks. Neural Plast. 2011;2011:960389.

    Article  PubMed  PubMed Central  Google Scholar 

  174. Plihal W, Born J. Effects of early and late nocturnal sleep on declarative and procedural memory. J Cogn Neurosci. 1997;9(4):534–47.

    Article  CAS  PubMed  Google Scholar 

  175. Schabus M, Gruber G, Parapatics S, Sauter C, Klosch G, Anderer P, et al. Sleep spindles and their significance for declarative memory consolidation. Sleep. 2004;27(8):1479–85.

    Article  PubMed  Google Scholar 

  176. Meier-Koll A, Bussmann B, Schmidt C, Neuschwander D. Walking through a maze alters the architecture of sleep. Percept Mot Skills. 1999;88(3 Pt 2):1141–59.

    Article  CAS  PubMed  Google Scholar 

  177. Tamminen J, Lambon Ralph MA, Lewis PA. The role of sleep spindles and slow-wave activity in integrating new information in semantic memory. J Neurosci. 2013;33(39):15376–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Wilhelm I, Diekelmann S, Molzow I, Ayoub A, Molle M, Born J. Sleep selectively enhances memory expected to be of future relevance. J Neurosci. 2011;31(5):1563–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Schabus M, Hoedlmoser K, Pecherstorfer T, Anderer P, Gruber G, Parapatics S, et al. Interindividual sleep spindle differences and their relation to learning-related enhancements. Brain Res. 2008;1191:127–35.

    Article  CAS  PubMed  Google Scholar 

  180. Saletin JM, Goldstein AN, Walker MP. The role of sleep in directed forgetting and remembering of human memories. Cereb Cortex. 2011;21(11):2534–41.

    Article  PubMed  PubMed Central  Google Scholar 

  181. Fogel SM, Smith CT, Cote KA. Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems. Behav Brain Res. 2007;180(1):48–61.

    Article  PubMed  Google Scholar 

  182. Smith C. Sleep states and memory processes in humans: procedural versus declarative memory systems. Sleep Med Rev. 2001;5(6):491–506.

    Article  CAS  PubMed  Google Scholar 

  183. Smith CT, Nixon MR, Nader RS. Posttraining increases in REM sleep intensity implicate REM sleep in memory processing and provide a biological marker of learning potential. Learn Mem. 2004;11(6):714–9.

    Article  PubMed  PubMed Central  Google Scholar 

  184. Miyauchi S, Misaki M, Kan S, Fukunaga T, Koike T. Human brain activity time-locked to rapid eye movements during REM sleep. Exp Brain Res. 2009;192(4):657–67.

    Article  PubMed  Google Scholar 

  185. Steriade M, Pare D, Bouhassira D, Deschenes M, Oakson G. Phasic activation of lateral geniculate and perigeniculate thalamic neurons during sleep with ponto-geniculo-occipital waves. J Neurosci. 1989;9(7):2215–29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Piantoni G, Van Der Werf YD, Jensen O, Van Someren EJ. Memory traces of long-range coordinated oscillations in the sleeping human brain. Hum Brain Mapp. 2015;36(1):67–84.

    Article  PubMed  Google Scholar 

  187. Morin A, Doyon J, Dostie V, Barakat M, Hadj TA, Korman M, et al. Motor sequence learning increases sleep spindles and fast frequencies in post-training sleep. Sleep. 2008;31(8):1149–56.

    PubMed  PubMed Central  Google Scholar 

  188. Walker MP. The role of slow wave sleep in memory processing. J Clin Sleep Med. 2009;5(2 Suppl):S20–6.

    Article  PubMed  PubMed Central  Google Scholar 

  189. Spoormaker VI, Czisch M, Maquet P, Jancke L. Large-scale functional brain networks in human non-rapid eye movement sleep: insights from combined electroencephalographic/functional magnetic resonance imaging studies. Philos Trans A Math Phys Eng Sci. 2011;369(1952):3708–29.

    Article  PubMed  Google Scholar 

  190. Barakat M, Carrier J, Debas K, Lungu O, Fogel S, Vandewalle G, et al. Sleep spindles predict neural and behavioral changes in motor sequence consolidation. Hum Brain Mapp. 2013;34(11):2918–28.

    Article  PubMed  Google Scholar 

  191. Tamaki M, Huang TR, Yotsumoto Y, Hamalainen M, Lin FH, Nanez JE Sr, et al. Enhanced spontaneous oscillations in the supplementary motor area are associated with sleep-dependent offline learning of finger-tapping motor-sequence task. J Neurosci. 2013;33(34):13894–902.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Verleger R, Ros M, Wagner U, Yordanova J, Kolev V. Insights into sleep’s role for insight: studies with the number reduction task. Adv Cogn Psychol. 2013;9(4):160–72.

    Article  PubMed  PubMed Central  Google Scholar 

  193. Sami S, Robertson EM, Miall RC. The time course of task-specific memory consolidation effects in resting state networks. J Neurosci. 2014;34(11):3982–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  194. Hanlon EC, Faraguna U, Vyazovskiy VV, Tononi G, Cirelli C. Effects of skilled training on sleep slow wave activity and cortical gene expression in the rat. Sleep. 2009;32(6):719–29.

    Article  PubMed  PubMed Central  Google Scholar 

  195. Fell J, Axmacher N. The role of phase synchronization in memory processes. Nat Rev Neurosci. 2011;12(2):105–18.

    Article  CAS  PubMed  Google Scholar 

  196. Benchenane K, Tiesinga PH, Battaglia FP. Oscillations in the prefrontal cortex: a gateway to memory and attention. Curr Opin Neurobiol. 2011;21(3):475–85.

    Article  CAS  PubMed  Google Scholar 

  197. Colgin LL. Oscillations and hippocampal-prefrontal synchrony. Curr Opin Neurobiol. 2011;21(3):467–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. Girardeau G, Zugaro M. Hippocampal ripples and memory consolidation. Curr Opin Neurobiol. 2011;21(3):452–9.

    Article  CAS  PubMed  Google Scholar 

  199. Heib DP, Hoedlmoser K, Anderer P, Zeitlhofer J, Gruber G, Klimesch W, et al. Slow oscillation amplitudes and up-state lengths relate to memory improvement. PLoS One. 2013;8(12):e82049.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  200. Ribeiro S. Sleep and plasticity. Pflugers Arch. 2012;463(1):111–20.

    Article  CAS  PubMed  Google Scholar 

  201. Zovkic IB, Guzman-Karlsson MC, Sweatt JD. Epigenetic regulation of memory formation and maintenance. Learn Mem. 2013;20(2):61–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the German Ministry of Education and Research (BMBF)/NSF, grant01GQ1706, and DFG (CRC/TR654, part A6). The author wishes to thank colleagues Sonja Binder, Sonat Aksamaz, and Dominc Aumann for comments on this or a previous version of the manuscript, as well as Abdullah-al-kamran Ripon for technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lisa Marshall .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Science+Business Media, LLC, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Marshall, L. (2020). A Role for Neuronal Oscillations of Sleep in Memory and Cognition. In: Dang-Vu, T., Courtemanche, R. (eds) Neuronal Oscillations of Wakefulness and Sleep. Springer, New York, NY. https://doi.org/10.1007/978-1-0716-0653-7_7

Download citation

Publish with us

Policies and ethics