Neuronal Oscillations and Reactivation Subserving Memory Consolidation

  • Til Ole BergmannEmail author
  • Bernhard P. StaresinaEmail author
Part of the Studies in Neuroscience, Psychology and Behavioral Economics book series (SNPBE)


Newly acquired memories are initially hippocampus-dependent and need to undergo a process of active system consolidation, during which they are redistributed to neocortical sites for long-term storage. This process is thought to take place during phases of quiet wakefulness and non-rapid-eye movement (NREM) sleep and is presumably based on the repeated reactivation of memory engrams (patterns of hippocampo-neocortical connections) which gradually drives the establishment of respective direct cortico-cortical connections. During NREM sleep (and similarly during quiet wakefulness), control via brainstem neuromodulatory systems (in particular the cholinergic one) enables a specific kind of oscillatory activity in the thalamo-neocortico-hippocampal system that facilitates memory reactivation. NREM oscillatory activity is characterized by the neocortical slow oscillation (SO; <1 Hz), the thalamic sleep spindle (~12–15 Hz) and the hippocampal ripple (>80 Hz). The intricate interaction of SOs, spindles and ripples constitutes a set of hierarchically nested oscillations, which provides the fine-tuned temporal and spatial structure that is required to orchestrate the reactivation of memory traces and the information flow between hippocampus and neocortex. In this chapter we (i) provide a conceptual introduction to system memory consolidation, (ii) describe the neuronal mechanisms thought to underlie the generation of and interaction between SOs, spindles and ripples, (iii) discuss how these oscillations presumably mediate memory reactivation and hippocampo-neocortical cross-talk, and (iv) outline new promising approaches to directly study the ongoing reactivation of memory representations in humans.


Neuronal oscillation Reactivation Memory representation Active system memory consolidation Slow oscillation Sleep spindle Ripple Hippocampus Neocortex Hippocampo-neocortical dialogue Acetylcholine 



T.O.B. was supported by the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG), via TR-SFB 654 (“Plasticity and Sleep”), and by the Hertie Foundation (Gemeinnützige Hertie-Stiftung), via the Hertie Institute for Clinical Brain Research. B.P.S. was supported by a Sir Henry Dale Fellowship to B.P.S. jointly funded by the Wellcome Trust and the Royal Society (107672/Z/15/Z).


  1. Achermann P, Borbely AA (1997) Low-frequency (<1 Hz) oscillations in the human sleep electroencephalogram. Neuroscience 81:213–222PubMedCrossRefGoogle Scholar
  2. Amzica F, Steriade M (1997) The K-complex: its slow (<1-Hz) rhythmicity and relation to delta waves. Neurology 49:952–959PubMedCrossRefGoogle Scholar
  3. Anderson KL, Rajagovindan R, Ghacibeh GA, Meador KJ, Ding M (2010) Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. Cereb Cortex 20:1604–1612PubMedCrossRefGoogle Scholar
  4. Andrade KC, Spoormaker VI, Dresler M, Wehrle R, Holsboer F, Samann PG, Czisch M (2011) Sleep spindles and hippocampal functional connectivity in human NREM sleep. J Neurosci 31:10331–10339PubMedCrossRefGoogle Scholar
  5. Andrillon T, Nir Y, Staba RJ, Ferrarelli F, Cirelli C, Tononi G, Fried I (2011) Sleep spindles in humans: insights from intracranial EEG and unit recordings. J Neurosci 31:17821–17834PubMedPubMedCentralCrossRefGoogle Scholar
  6. Astori S, Wimmer RD, Luthi A (2013) Manipulating sleep spindles—expanding views on sleep, memory, and disease. Trends Neurosci 36:738–748PubMedCrossRefGoogle Scholar
  7. Atherton LA, Dupret D, Mellor JR (2015) Memory trace replay: the shaping of memory consolidation by neuromodulation. Trends Neurosci 38:560–570PubMedPubMedCentralCrossRefGoogle Scholar
  8. Axmacher N, Elger CE, Fell J (2008) Ripples in the medial temporal lobe are relevant for human memory consolidation. Brain 131:1806–1817PubMedCrossRefGoogle Scholar
  9. Bal T, Debay D, Destexhe A (2000) Cortical feedback controls the frequency and synchrony of oscillations in the visual thalamus. J Neurosci 20:7478–7488PubMedGoogle Scholar
  10. Battaglia FP, Sutherland GR, McNaughton BL (2004) Hippocampal sharp wave bursts coincide with neocortical “up-state” transitions. Learn Mem 11:697–704PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bergmann TO, Molle M, Marshall L, Kaya-Yildiz L, Born J, Siebner HR (2008) A local signature of LTP- and LTD-like plasticity in human NREM sleep. Eur J Neurosci 27:2241–2249PubMedCrossRefGoogle Scholar
  12. Bergmann TO, Molle M, Diedrichs J, Born J, Siebner HR (2012a) Sleep spindle-related reactivation of category-specific cortical regions after learning face-scene associations. Neuroimage 59:2733–2742PubMedCrossRefGoogle Scholar
  13. Bergmann TO, Molle M, Schmidt MA, Lindner C, Marshall L, Born J, Siebner HR (2012b) EEG-guided transcranial magnetic stimulation reveals rapid shifts in motor cortical excitability during the human sleep slow oscillation. J Neurosci 32:243–253PubMedCrossRefGoogle Scholar
  14. Bergmann TO, Karabanov A, Hartwigsen G, Thielscher A, Siebner HR (2016) Combining non-invasive transcranial brain stimulation with neuroimaging and electrophysiology: current approaches and future perspectives. NeuroimageGoogle Scholar
  15. Blessing EM, Beissner F, Schumann A, Brunner F, Bar KJ (2016) A data-driven approach to mapping cortical and subcortical intrinsic functional connectivity along the longitudinal hippocampal axis. Hum Brain Mapp 37:462–476PubMedCrossRefGoogle Scholar
  16. Bonjean M, Baker T, Lemieux M, Timofeev I, Sejnowski T, Bazhenov M (2011) Corticothalamic feedback controls sleep spindle duration in vivo. J Neurosci 31:9124–9134PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bonjean M, Baker T, Bazhenov M, Cash S, Halgren E, Sejnowski T (2012) Interactions between core and matrix thalamocortical projections in human sleep spindle synchronization. J Neurosci 32:5250–5263PubMedPubMedCentralCrossRefGoogle Scholar
  18. Born J, Wilhelm I (2012) System consolidation of memory during sleep. Psychol Res 76:192–203PubMedCrossRefGoogle Scholar
  19. Born J, Rasch B, Gais S (2006) Sleep to remember. Neuroscientist 12:410–424PubMedCrossRefGoogle Scholar
  20. Bragin A, Engel J Jr, Wilson CL, Fried I, Buzsaki G (1999) High-frequency oscillations in human brain. Hippocampus 9:137–142PubMedCrossRefGoogle Scholar
  21. Buzsaki G (1986) Hippocampal sharp waves: their origin and significance. Brain Res 398:242–252PubMedCrossRefGoogle Scholar
  22. Buzsaki G (1996) The hippocampo-neocortical dialogue. Cereb Cortex 6:81–92PubMedCrossRefGoogle Scholar
  23. Buzsaki G (1998) Memory consolidation during sleep: a neurophysiological perspective. J Sleep Res 7(Suppl 1):17–23PubMedCrossRefGoogle Scholar
  24. Buzsaki G (2015) Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus 25:1073–1188PubMedPubMedCentralCrossRefGoogle Scholar
  25. Buzsaki G, Horvath Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256:1025–1027PubMedCrossRefGoogle Scholar
  26. Cash SS, Halgren E, Dehghani N, Rossetti AO, Thesen T, Wang C, Devinsky O, Kuzniecky R, Doyle W, Madsen JR, Bromfield E, Eross L, Halasz P, Karmos G, Csercsa R, Wittner L, Ulbert I (2009) The human K-complex represents an isolated cortical down-state. Science 324:1084–1087PubMedPubMedCentralCrossRefGoogle Scholar
  27. Cassel JC, Pereira de Vasconcelos A, Loureiro M, Cholvin T, Dalrymple-Alford JC, Vertes RP (2013) The reuniens and rhomboid nuclei: neuroanatomy, electrophysiological characteristics and behavioral implications. Prog Neurobiol 111:34–52PubMedPubMedCentralCrossRefGoogle Scholar
  28. Chrobak JJ, Buzsaki G (1996) High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci 16:3056–3066PubMedGoogle Scholar
  29. Clemens Z, Fabo D, Halasz P (2005) Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience 132:529–535PubMedCrossRefGoogle Scholar
  30. Clemens Z, Fabo D, Halasz P (2006) Twenty-four hours retention of visuospatial memory correlates with the number of parietal sleep spindles. Neurosci Lett 403:52–56PubMedCrossRefGoogle Scholar
  31. Clemens Z, Mölle M, Eross L, Barsi P, Halasz P, Born J (2007) Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 130:2868–2878PubMedCrossRefGoogle Scholar
  32. Clemens Z, Molle M, Eross L, Jakus R, Rasonyi G, Halasz P, Born J (2011) Fine-tuned coupling between human parahippocampal ripples and sleep spindles. Eur J Neurosci 33:511–520PubMedCrossRefGoogle Scholar
  33. Colgin LL (2015) Theta-gamma coupling in the entorhinal-hippocampal system. Curr Opin Neurobiol 31:45–50PubMedCrossRefGoogle Scholar
  34. Colgin LL (2016) Rhythms of the hippocampal network. Nat Rev Neurosci 17:239–249PubMedCrossRefGoogle Scholar
  35. Colrain IM (2005) The K-complex: a 7-decade history. Sleep 28:255–273PubMedGoogle Scholar
  36. Contreras D, Steriade M (1995) Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J Neurosci 15:604–622PubMedGoogle Scholar
  37. Contreras D, Destexhe A, Sejnowski TJ, Steriade M (1996) Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback. Science 274:771–774PubMedCrossRefGoogle Scholar
  38. Contreras D, Destexhe A, Sejnowski TJ, Steriade M (1997) Spatiotemporal patterns of spindle oscillations in cortex and thalamus. J Neurosci 17:1179–1196PubMedGoogle Scholar
  39. Cox R, Hofman WF, Talamini LM (2012) Involvement of spindles in memory consolidation is slow wave sleep-specific. Learn Mem 19:264–267PubMedCrossRefGoogle Scholar
  40. Cox R, Hofman WF, de Boer M, Talamini LM (2014) Local sleep spindle modulations in relation to specific memory cues. Neuroimage 99:103–110PubMedCrossRefGoogle Scholar
  41. Crunelli V, Hughes SW (2009) The slow (<1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators. Nat NeurosciGoogle Scholar
  42. Dan Y, Poo MM (2004) Spike timing-dependent plasticity of neural circuits. Neuron 44:23–30PubMedCrossRefGoogle Scholar
  43. Datta S, Maclean RR (2007) Neurobiological mechanisms for the regulation of mammalian sleep-wake behavior: reinterpretation of historical evidence and inclusion of contemporary cellular and molecular evidence. Neurosci Biobehav Rev 31:775–824PubMedPubMedCentralCrossRefGoogle Scholar
  44. De Gennaro L, Ferrara M (2003) Sleep spindles: an overview. Sleep Med Rev 7:423–440PubMedCrossRefGoogle Scholar
  45. Destexhe A, Contreras D, Sejnowski TJ, Steriade M (1994) Modeling the control of reticular thalamic oscillations by neuromodulators. NeuroReport 5:2217–2220PubMedCrossRefGoogle Scholar
  46. Diba K, Buzsaki G (2007) Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci 10:1241–1242PubMedPubMedCentralCrossRefGoogle Scholar
  47. Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neurosci 11:114–126PubMedCrossRefGoogle Scholar
  48. Diekelmann S, Wilhelm I, Born J (2009) The whats and whens of sleep-dependent memory consolidation. Sleep Med Rev 13(5):309--321Google Scholar
  49. Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55:51–86PubMedCrossRefGoogle Scholar
  50. Düzel E, Penny WD, Burgess N (2010) Brain oscillations and memory. Curr Opin Neurobiol 20:143–149PubMedCrossRefGoogle Scholar
  51. Ego-Stengel V, Wilson MA (2009) Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20:1–10Google Scholar
  52. Eichenbaum H (2004) Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44:109–120PubMedCrossRefGoogle Scholar
  53. 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 18:2596–2603PubMedCrossRefGoogle Scholar
  54. Eschenko O, Magri C, Panzeri S, Sara SJ (2011) Noradrenergic neurons of the locus coeruleus are phase locked to cortical up-down states during sleep. Cereb CortexGoogle Scholar
  55. Fell J, Axmacher N (2011) The role of phase synchronization in memory processes. Nat Rev Neurosci 12:105–118PubMedCrossRefGoogle Scholar
  56. Fogel SM, Smith CT (2006) Learning-dependent changes in sleep spindles and Stage 2 sleep. J Sleep Res 15:250–255PubMedCrossRefGoogle Scholar
  57. Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440:680–683PubMedCrossRefGoogle Scholar
  58. Frankland PW, Bontempi B (2005) The organization of recent and remote memories. Nat Rev Neurosci 6:119–130PubMedCrossRefGoogle Scholar
  59. Frey U, Morris RG (1998) Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci 21:181–188PubMedCrossRefGoogle Scholar
  60. Fuentemilla L, Barnes GR, Duzel E, Levine B (2014) Theta oscillations orchestrate medial temporal lobe and neocortex in remembering autobiographical memories. Neuroimage 85(Pt 2):730–737PubMedCrossRefGoogle Scholar
  61. Gais S, Born J (2004a) Declarative memory consolidation: mechanisms acting during human sleep. Learn Mem 11:679–685PubMedPubMedCentralCrossRefGoogle Scholar
  62. Gais S, Born J (2004b) Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation. Proc Natl Acad Sci U S A 101:2140–2144PubMedPubMedCentralCrossRefGoogle Scholar
  63. Gais S, Mölle M, Helms K, Born J (2002) Learning-dependent increases in sleep spindle density. J Neurosci 22:6830–6834PubMedGoogle Scholar
  64. Gardner RJ, Hughes SW, Jones MW (2013) Differential spike timing and phase dynamics of reticular thalamic and prefrontal cortical neuronal populations during sleep spindles. J Neurosci 33:18469–18480PubMedPubMedCentralCrossRefGoogle Scholar
  65. Girardeau G, Zugaro M (2011) Hippocampal ripples and memory consolidation. Curr Opin NeurobiolGoogle Scholar
  66. Girardeau G, Benchenane K, Wiener SI, Buzsaki G, Zugaro MB (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 12:1222–1223PubMedCrossRefGoogle Scholar
  67. Giuditta A (2014) Sleep memory processing: the sequential hypothesis. Front Syst Neurosci 8:219PubMedPubMedCentralCrossRefGoogle Scholar
  68. Giuditta A, Ambrosini MV, Montagnese P, Mandile P, Cotugno M, Grassi Zucconi G, Vescia S (1995) The sequential hypothesis of the function of sleep. Behav Brain Res 69:157–166PubMedCrossRefGoogle Scholar
  69. Greenberg DL, Rubin DC (2003) The neuropsychology of autobiographical memory. Cortex 39:687–728PubMedCrossRefGoogle Scholar
  70. Gruber MJ, Ritchey M, Wang SF, Doss MK, Ranganath C (2016) Post-learning hippocampal dynamics promote preferential retention of rewarding events. Neuron 89:1110–1120PubMedCrossRefGoogle Scholar
  71. Harris KD, Thiele A (2011) Cortical state and attention. Nat Rev Neurosci 12:509–523PubMedPubMedCentralCrossRefGoogle Scholar
  72. Hasselmo ME (1999) Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci 3:351–359PubMedCrossRefGoogle Scholar
  73. Hasselmo ME (2005) What is the function of hippocampal theta rhythm?—Linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus 15:936–949PubMedCrossRefGoogle Scholar
  74. Hasselmo ME, McGaughy J (2004) High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidation. Prog Brain Res 145:207–231PubMedCrossRefGoogle Scholar
  75. Hill S, Tononi G (2005) Modeling sleep and wakefulness in the thalamocortical system. J Neurophysiol 93:1671–1698PubMedCrossRefGoogle Scholar
  76. Huber R, Ghilardi MF, Massimini M, Tononi G (2004) Local sleep and learning. Nature 430:78–81PubMedCrossRefGoogle Scholar
  77. Hutchison IC, Rathore S (2015) The role of REM sleep theta activity in emotional memory. Front Psychol 6:1439PubMedPubMedCentralCrossRefGoogle Scholar
  78. Iber C, Ancoli-Israel S, Chesson A, Quan SF (2007) The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications. American Academy of Sleep Medicine, Westchester, ILGoogle Scholar
  79. Isomura Y, Sirota A, Ozen S, Montgomery S, Mizuseki K, Henze DA, Buzsaki G (2006) Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron 52:871–882PubMedCrossRefGoogle Scholar
  80. Jensen O (2005) Reading the hippocampal code by theta phase-locking. Trends Cogn Sci 9:551–553PubMedCrossRefGoogle Scholar
  81. Jones EG (2001) The thalamic matrix and thalamocortical synchrony. Trends Neurosci 24:595–601PubMedCrossRefGoogle Scholar
  82. Josselyn SA, Kohler S, Frankland PW (2015) Finding the engram. Nat Rev Neurosci 16:521–534PubMedCrossRefGoogle Scholar
  83. Le Van Quyen M, Bragin A, Staba R, Crepon B, Wilson CL, Engel J Jr (2008) Cell type-specific firing during ripple oscillations in the hippocampal formation of humans. J Neurosci 28:6104–6110PubMedPubMedCentralCrossRefGoogle Scholar
  84. Le Van Quyen M, Staba R, Bragin A, Dickson C, Valderrama M, Fried I, Engel J (2010) Large-scale microelectrode recordings of high-frequency gamma oscillations in human cortex during sleep. J Neurosci 30:7770–7782PubMedPubMedCentralCrossRefGoogle Scholar
  85. Lisman JE, Jensen O (2013) The theta-gamma neural code. Neuron 77:1002–1016PubMedPubMedCentralCrossRefGoogle Scholar
  86. Llinas RR, Leznik E, Urbano FJ (2002) Temporal binding via cortical coincidence detection of specific and nonspecific thalamocortical inputs: a voltage-dependent dye-imaging study in mouse brain slices. Proc Natl Acad Sci U S A 99:449–454PubMedPubMedCentralCrossRefGoogle Scholar
  87. Logothetis NK, Eschenko O, Murayama Y, Augath M, Steudel T, Evrard HC, Besserve M, Oeltermann A (2012) Hippocampal-cortical interaction during periods of subcortical silence. Nature 491:547–553PubMedCrossRefGoogle Scholar
  88. Lubenov EV, Siapas AG (2009) Hippocampal theta oscillations are travelling waves. Nature 459:534–539PubMedCrossRefGoogle Scholar
  89. Luthi A (2014) Sleep spindles: where they come from, what they do. Neuroscientist 20:243–256 Google Scholar
  90. Maquet P (2001) The role of sleep in learning and memory. Science 294:1048–1052PubMedCrossRefGoogle Scholar
  91. Marrosu F, Portas C, Mascia MS, Casu MA, Fa M, Giagheddu M, Imperato A, Gessa GL (1995) Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain Res 671:329–332PubMedCrossRefGoogle Scholar
  92. Marshall L, Mölle M, Hallschmid M, Born J (2004) Transcranial direct current stimulation during sleep improves declarative memory. J Neurosci 24:9985–9992PubMedCrossRefGoogle Scholar
  93. Marshall L, Helgadottir H, Mölle M, Born J (2006) Boosting slow oscillations during sleep potentiates memory. Nature 444:610–613PubMedCrossRefGoogle Scholar
  94. Masquelier T, Hugues E, Deco G, Thorpe SJ (2009) Oscillations, phase-of-firing coding, and spike timing-dependent plasticity: an efficient learning scheme. J Neurosci 29:13484–13493PubMedCrossRefGoogle Scholar
  95. Massimini M, Huber R, Ferrarelli F, Hill S, Tononi G (2004) The sleep slow oscillation as a traveling wave. J Neurosci 24:6862–6870PubMedCrossRefGoogle Scholar
  96. 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 102:419–457PubMedCrossRefGoogle Scholar
  97. McCormick DA (1992) Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog Neurobiol 39:337–388PubMedCrossRefGoogle Scholar
  98. Meeter M, Murre JM (2004) Consolidation of long-term memory: evidence and alternatives. Psychol Bull 130:843–857PubMedCrossRefGoogle Scholar
  99. Mölle M, Marshall L, Gais S, Born J (2002) Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. J Neurosci 22:10941–10947PubMedGoogle Scholar
  100. Mölle M, Marshall L, Gais S, Born J (2004) Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations. Proc Natl Acad Sci U S A 101:13963–13968PubMedPubMedCentralCrossRefGoogle Scholar
  101. Mölle M, Yeshenko O, Marshall L, Sara SJ, Born J (2006) Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J Neurophysiol 96:62–70PubMedCrossRefGoogle Scholar
  102. Mölle M, Eschenko O, Gais S, Sara SJ, Born J (2009) The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats. Eur J Neurosci 29:1071–1081PubMedCrossRefGoogle Scholar
  103. Mölle M, Bergmann TO, Marshall L, Born J (2011) Fast and slow spindles during the sleep slow oscillation: disparate coalescence and engagement in memory processing. Sleep 34:1411–1421PubMedPubMedCentralGoogle Scholar
  104. Morris RG (2006) Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci 23:2829–2846PubMedCrossRefGoogle Scholar
  105. Müller GE, Pilzecker A (1900) Experimentelle Beiträge zur Lehre vom Gedächtnis. Z Psychol Ergänzungsband 1:1–300Google Scholar
  106. Murphy M, Riedner BA, Huber R, Massimini M, Ferrarelli F, Tononi G (2009) Source modeling sleep slow waves. Proc Natl Acad Sci U S A 106:1608–1613PubMedPubMedCentralCrossRefGoogle Scholar
  107. Ngo HV, Martinetz T, Born J, Molle M (2013) Auditory closed-loop stimulation of the sleep slow oscillation enhances memory. Neuron 78:545–553PubMedCrossRefGoogle Scholar
  108. Ngo HV, Miedema A, Faude I, Martinetz T, Molle M, Born J (2015) Driving sleep slow oscillations by auditory closed-loop stimulation-a self-limiting process. J Neurosci 35:6630–6638PubMedPubMedCentralCrossRefGoogle Scholar
  109. Nir Y, Staba RJ, Andrillon T, Vyazovskiy VV, Cirelli C, Fried I, Tononi G (2011) Regional slow waves and spindles in human sleep. Neuron 70:153–169PubMedPubMedCentralCrossRefGoogle Scholar
  110. Norman KA, Polyn SM, Detre GJ, Haxby JV (2006) Beyond mind-reading: multi-voxel pattern analysis of fMRI data. Trends Cogn Sci 10:424–430PubMedCrossRefGoogle Scholar
  111. O’Keefe J (1976) Place units in the hippocampus of the freely moving rat. Exp Neurol 51:78–109PubMedCrossRefGoogle Scholar
  112. Patel J, Schomburg EW, Berenyi A, Fujisawa S, Buzsaki G (2013) Local generation and propagation of ripples along the septotemporal axis of the hippocampus. J Neurosci 33:17029–17041PubMedPubMedCentralCrossRefGoogle Scholar
  113. Peigneux P, Laureys S, Fuchs S, Collette F, Perrin F, Reggers J, Phillips C, Degueldre C, Del Fiore G, Aerts J, Luxen A, Maquet P (2004) Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44:535–545PubMedCrossRefGoogle Scholar
  114. Peigneux P, Orban P, Balteau E, Degueldre C, Luxen A, Laureys S, Maquet P (2006) Offline persistence of memory-related cerebral activity during active wakefulness. PLoS Biol 4:e100PubMedPubMedCentralCrossRefGoogle Scholar
  115. Pennartz CM, Lee E, Verheul J, Lipa P, Barnes CA, McNaughton BL (2004) The ventral striatum in off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples. J Neurosci 24:6446–6456PubMedCrossRefGoogle Scholar
  116. Pereira de Vasconcelos A, Cassel JC (2014) The nonspecific thalamus: A place in a wedding bed for making memories last? Neurosci Biobehav Rev 54:175--196Google Scholar
  117. Peter-Derex L, Comte JC, Mauguiere F, Salin PA (2012) Density and frequency caudo-rostral gradients of sleep spindles recorded in the human cortex. Sleep 35:69–79PubMedPubMedCentralGoogle Scholar
  118. 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 12:919–926PubMedCrossRefGoogle Scholar
  119. Poppenk J, Evensmoen HR, Moscovitch M, Nadel L (2013) Long-axis specialization of the human hippocampus. Trends Cogn Sci 17:230–240PubMedCrossRefGoogle Scholar
  120. Ramanathan DS, Gulati T, Ganguly K (2015) Sleep-dependent reactivation of ensembles in motor cortex promotes skill consolidation. PLoS Biol 13:e1002263PubMedPubMedCentralCrossRefGoogle Scholar
  121. Ranganath C, Ritchey M (2012) Two cortical systems for memory-guided behaviour. Nat Rev Neurosci 13:713–726PubMedCrossRefGoogle Scholar
  122. Rasch B, Born J (2007) Maintaining memories by reactivation. Curr Opin Neurobiol 17:698–703PubMedCrossRefGoogle Scholar
  123. Rasch B, Born J (2013) About sleep’s role in memory. Physiol Rev 93:681–766PubMedPubMedCentralCrossRefGoogle Scholar
  124. Rasch BH, Born J, Gais S (2006) Combined blockade of cholinergic receptors shifts the brain from stimulus encoding to memory consolidation. J Cogn Neurosci 18:793–802PubMedCrossRefGoogle Scholar
  125. Rechtschaffen A, Kales A (1968) A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. United States Government Printing Office, Washington, DCGoogle Scholar
  126. Ribeiro S, Shi X, Engelhard M, Zhou Y, Zhang H, Gervasoni D, Lin SC, Wada K, Lemos NA, Nicolelis MA (2007) Novel experience induces persistent sleep-dependent plasticity in the cortex but not in the hippocampus. Front Neurosci 1:43–55PubMedPubMedCentralCrossRefGoogle Scholar
  127. Rosanova M, Ulrich D (2005) Pattern-specific associative long-term potentiation induced by a sleep spindle-related spike train. J Neurosci 25:9398–9405PubMedCrossRefGoogle Scholar
  128. Sadowski JH, Jones MW, Mellor JR (2011) Ripples make waves: binding structured activity and plasticity in hippocampal networks. Neural Plast 2011:960389PubMedPubMedCentralGoogle Scholar
  129. Sanchez-Vives MV, McCormick DA (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3:1027–1034PubMedCrossRefGoogle Scholar
  130. Santoro A, Frankland PW (2014) Chasing the trace. Neuron 84:243–246PubMedCrossRefGoogle Scholar
  131. Sarasso S, Proserpio P, Pigorini A, Moroni F, Ferrara M, De Gennaro L, De Carli F, Russo GL, Massimini M, Nobili L (2014) Hippocampal sleep spindles preceding neocortical sleep onset in humans. Neuroimage 86:425–432Google Scholar
  132. Schabus M, Dang-Vu TT, Albouy G, Balteau E, Boly M, Carrier J, Darsaud A, Degueldre C, Desseilles M, Gais S, Phillips C, Rauchs G, Schnakers C, Sterpenich V, Vandewalle G, Luxen A, Maquet P (2007) Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc Natl Acad Sci U S A 104:13164–13169PubMedPubMedCentralCrossRefGoogle Scholar
  133. Schabus M, Hoedlmoser K, Pecherstorfer T, Anderer P, Gruber G, Parapatics S, Sauter C, Kloesch G, Klimesch W, Saletu B, Zeitlhofer J (2008) Interindividual sleep spindle differences and their relation to learning-related enhancements. Brain Res 1191:127–135PubMedCrossRefGoogle Scholar
  134. Sejnowski TJ, Destexhe A (2000) Why do we sleep? Brain Res 886:208–223PubMedCrossRefGoogle Scholar
  135. Sharma AV, Wolansky T, Dickson CT (2010) A comparison of sleep-like slow oscillations in the hippocampus under ketamine and urethane anaesthesia. J Neurophysiol 104:932–939Google Scholar
  136. Siapas AG, Wilson MA (1998) Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21:1123–1128PubMedCrossRefGoogle Scholar
  137. Sirota A, Csicsvari J, Buhl D, Buzsaki G (2003) Communication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci U S A 100:2065–2069PubMedPubMedCentralCrossRefGoogle Scholar
  138. Skaggs WE, McNaughton BL, Permenter M, Archibeque M, Vogt J, Amaral DG, Barnes CA (2007) EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. J Neurophysiol 98:898–910PubMedCrossRefGoogle Scholar
  139. Staba RJ, Wilson CL, Bragin A, Fried I, Engel J Jr (2002) Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. J Neurophysiol 88:1743–1752PubMedGoogle Scholar
  140. Staresina BP, Alink A, Kriegeskorte N, Henson RN (2013) Awake reactivation predicts memory in humans. Proc Natl Acad Sci U S A 110:21159–21164PubMedPubMedCentralCrossRefGoogle Scholar
  141. Staresina BP, Bergmann TO, Bonnefond M, van der Meij R, Jensen O, Deuker L, Elger CE, Axmacher N, Fell J (2015) Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep. Nat Neurosci 18:1679–1686PubMedPubMedCentralCrossRefGoogle Scholar
  142. Steriade M (2003) The corticothalamic system in sleep. Front Biosci 8:d878–d899PubMedCrossRefGoogle Scholar
  143. Steriade M (2004) Acetylcholine systems and rhythmic activities during the waking–sleep cycle. Prog Brain Res 145:179–196PubMedCrossRefGoogle Scholar
  144. Steriade M (2006) Grouping of brain rhythms in corticothalamic systems. Neuroscience 137:1087–1106PubMedCrossRefGoogle Scholar
  145. Steriade M, Timofeev I (2003) Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 37:563–576PubMedCrossRefGoogle Scholar
  146. Steriade M, Nunez A, Amzica F (1993a) Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci 13:3266–3283PubMedGoogle Scholar
  147. Steriade M, Nunez A, Amzica F (1993b) A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13:3252–3265PubMedGoogle Scholar
  148. Strange BA, Witter MP, Lein ES, Moser EI (2014) Functional organization of the hippocampal longitudinal axis. Nat Rev Neurosci 15:655–669PubMedCrossRefGoogle Scholar
  149. Sullivan D, Csicsvari J, Mizuseki K, Montgomery S, Diba K, Buzsaki G (2011) Relationships between Hippocampal Sharp Waves, Ripples, and Fast Gamma Oscillation: Influence of Dentate and Entorhinal Cortical Activity. J Neurosci 31:8605–8616PubMedPubMedCentralCrossRefGoogle Scholar
  150. Sutherland GR, McNaughton B (2000) Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr Opin Neurobiol 10:180–186PubMedCrossRefGoogle Scholar
  151. Tambini A, Davachi L (2013) Persistence of hippocampal multivoxel patterns into postencoding rest is related to memory. Proc Natl Acad Sci U S A 110:19591–19596PubMedPubMedCentralCrossRefGoogle Scholar
  152. Tambini A, Ketz N, Davachi L (2010) Enhanced brain correlations during rest are related to memory for recent experiences. Neuron 65:280–290PubMedPubMedCentralCrossRefGoogle Scholar
  153. Timofeev I, Grenier F, Bazhenov M, Sejnowski TJ, Steriade M (2000) Origin of slow cortical oscillations in deafferented cortical slabs. Cereb Cortex 10:1185–1199PubMedCrossRefGoogle Scholar
  154. Timofeev I, Grenier F, Bazhenov M, Houweling AR, Sejnowski TJ, Steriade M (2002) Short- and medium-term plasticity associated with augmenting responses in cortical slabs and spindles in intact cortex of cats in vivo. J Physiol 542:583–598PubMedPubMedCentralCrossRefGoogle Scholar
  155. Tononi G, Cirelli C (2003) Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull 62:143–150PubMedCrossRefGoogle Scholar
  156. Urrestarazu E, Chander R, Dubeau F, Gotman J (2007) Interictal high-frequency oscillations (100-500 Hz) in the intracerebral EEG of epileptic patients. Brain 130:2354–2366PubMedCrossRefGoogle Scholar
  157. van Kesteren MT, Ruiter DJ, Fernandez G, Henson RN (2012) How schema and novelty augment memory formation. Trends Neurosci 35:211–219PubMedCrossRefGoogle Scholar
  158. Varela C, Kumar S, Yang JY, Wilson MA (2014) Anatomical substrates for direct interactions between hippocampus, medial prefrontal cortex, and the thalamic nucleus reuniens. Brain Struct Funct 219:911–929PubMedCrossRefGoogle Scholar
  159. Walker MP, Stickgold R (2010) Overnight alchemy: sleep-dependent memory evolution. Nat Rev Neurosci 11:218; author reply 218Google Scholar
  160. Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265:676–679PubMedCrossRefGoogle Scholar
  161. Wolansky T, Clement EA, Peters SR, Palczak MA, Dickson CT (2006) Hippocampal slow oscillation: a novel EEG state and its coordination with ongoing neocortical activity. J Neurosci 26:6213–6229PubMedCrossRefGoogle Scholar
  162. Zarei M, Beckmann CF, Binnewijzend MA, Schoonheim MM, Oghabian MA, Sanz-Arigita EJ, Scheltens P, Matthews PM, Barkhof F (2013) Functional segmentation of the hippocampus in the healthy human brain and in Alzheimer’s disease. Neuroimage 66:28–35PubMedCrossRefGoogle Scholar
  163. Zhang H, Jacobs J (2015) Traveling theta waves in the human hippocampus. J Neurosci 35:12477–12487PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Institute for Medical Psychology and Behavioral NeurobiologyEberhard Karls University of TübingenTübingenGermany
  2. 2.Department of Neurology & Stroke, and Hertie Institute for Clinical Brain ResearchUniversity of TübingenTübingenGermany
  3. 3.School of PsychologyUniversity of BirminghamBirminghamUK

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