Skip to main content

Neuronal Oscillations and Reactivation Subserving Memory Consolidation

  • Chapter
  • First Online:
Cognitive Neuroscience of Memory Consolidation

Abstract

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.

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 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 139.99
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

Similar content being viewed by others

References

  • Achermann P, Borbely AA (1997) Low-frequency (<1 Hz) oscillations in the human sleep electroencephalogram. Neuroscience 81:213–222

    Article  PubMed  Google Scholar 

  • Amzica F, Steriade M (1997) The K-complex: its slow (<1-Hz) rhythmicity and relation to delta waves. Neurology 49:952–959

    Article  PubMed  Google Scholar 

  • 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 20:1604–1612

    Article  PubMed  Google Scholar 

  • 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 31:10331–10339

    Article  PubMed  Google Scholar 

  • 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 31:17821–17834

    Article  PubMed  PubMed Central  Google Scholar 

  • Astori S, Wimmer RD, Luthi A (2013) Manipulating sleep spindles—expanding views on sleep, memory, and disease. Trends Neurosci 36:738–748

    Article  PubMed  Google Scholar 

  • Atherton LA, Dupret D, Mellor JR (2015) Memory trace replay: the shaping of memory consolidation by neuromodulation. Trends Neurosci 38:560–570

    Article  PubMed  PubMed Central  Google Scholar 

  • Axmacher N, Elger CE, Fell J (2008) Ripples in the medial temporal lobe are relevant for human memory consolidation. Brain 131:1806–1817

    Article  PubMed  Google Scholar 

  • Bal T, Debay D, Destexhe A (2000) Cortical feedback controls the frequency and synchrony of oscillations in the visual thalamus. J Neurosci 20:7478–7488

    PubMed  Google Scholar 

  • Battaglia FP, Sutherland GR, McNaughton BL (2004) Hippocampal sharp wave bursts coincide with neocortical “up-state” transitions. Learn Mem 11:697–704

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 27:2241–2249

    Article  PubMed  Google Scholar 

  • 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 59:2733–2742

    Article  PubMed  Google Scholar 

  • 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 32:243–253

    Article  PubMed  Google Scholar 

  • 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. Neuroimage

    Google Scholar 

  • 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 37:462–476

    Article  PubMed  Google Scholar 

  • Bonjean M, Baker T, Lemieux M, Timofeev I, Sejnowski T, Bazhenov M (2011) Corticothalamic feedback controls sleep spindle duration in vivo. J Neurosci 31:9124–9134

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 32:5250–5263

    Article  PubMed  PubMed Central  Google Scholar 

  • Born J, Wilhelm I (2012) System consolidation of memory during sleep. Psychol Res 76:192–203

    Article  PubMed  Google Scholar 

  • Born J, Rasch B, Gais S (2006) Sleep to remember. Neuroscientist 12:410–424

    Article  PubMed  Google Scholar 

  • Bragin A, Engel J Jr, Wilson CL, Fried I, Buzsaki G (1999) High-frequency oscillations in human brain. Hippocampus 9:137–142

    Article  PubMed  Google Scholar 

  • Buzsaki G (1986) Hippocampal sharp waves: their origin and significance. Brain Res 398:242–252

    Article  PubMed  Google Scholar 

  • Buzsaki G (1996) The hippocampo-neocortical dialogue. Cereb Cortex 6:81–92

    Article  PubMed  Google Scholar 

  • Buzsaki G (1998) Memory consolidation during sleep: a neurophysiological perspective. J Sleep Res 7(Suppl 1):17–23

    Article  PubMed  Google Scholar 

  • Buzsaki G (2015) Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus 25:1073–1188

    Article  PubMed  PubMed Central  Google Scholar 

  • Buzsaki G, Horvath Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256:1025–1027

    Article  PubMed  Google Scholar 

  • 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 324:1084–1087

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 111:34–52

    Article  PubMed  PubMed Central  Google Scholar 

  • Chrobak JJ, Buzsaki G (1996) High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci 16:3056–3066

    PubMed  Google Scholar 

  • Clemens Z, Fabo D, Halasz P (2005) Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience 132:529–535

    Article  PubMed  Google Scholar 

  • Clemens Z, Fabo D, Halasz P (2006) Twenty-four hours retention of visuospatial memory correlates with the number of parietal sleep spindles. Neurosci Lett 403:52–56

    Article  PubMed  Google Scholar 

  • 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 130:2868–2878

    Article  PubMed  Google Scholar 

  • 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 33:511–520

    Article  PubMed  Google Scholar 

  • Colgin LL (2015) Theta-gamma coupling in the entorhinal-hippocampal system. Curr Opin Neurobiol 31:45–50

    Article  PubMed  Google Scholar 

  • Colgin LL (2016) Rhythms of the hippocampal network. Nat Rev Neurosci 17:239–249

    Article  PubMed  Google Scholar 

  • Colrain IM (2005) The K-complex: a 7-decade history. Sleep 28:255–273

    PubMed  Google Scholar 

  • Contreras D, Steriade M (1995) Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J Neurosci 15:604–622

    PubMed  Google Scholar 

  • Contreras D, Destexhe A, Sejnowski TJ, Steriade M (1996) Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback. Science 274:771–774

    Article  PubMed  Google Scholar 

  • Contreras D, Destexhe A, Sejnowski TJ, Steriade M (1997) Spatiotemporal patterns of spindle oscillations in cortex and thalamus. J Neurosci 17:1179–1196

    PubMed  Google Scholar 

  • Cox R, Hofman WF, Talamini LM (2012) Involvement of spindles in memory consolidation is slow wave sleep-specific. Learn Mem 19:264–267

    Article  PubMed  Google Scholar 

  • Cox R, Hofman WF, de Boer M, Talamini LM (2014) Local sleep spindle modulations in relation to specific memory cues. Neuroimage 99:103–110

    Article  PubMed  Google Scholar 

  • Crunelli V, Hughes SW (2009) The slow (<1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators. Nat Neurosci

    Google Scholar 

  • Dan Y, Poo MM (2004) Spike timing-dependent plasticity of neural circuits. Neuron 44:23–30

    Article  PubMed  Google Scholar 

  • 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 31:775–824

    Article  PubMed  PubMed Central  Google Scholar 

  • De Gennaro L, Ferrara M (2003) Sleep spindles: an overview. Sleep Med Rev 7:423–440

    Article  PubMed  Google Scholar 

  • Destexhe A, Contreras D, Sejnowski TJ, Steriade M (1994) Modeling the control of reticular thalamic oscillations by neuromodulators. NeuroReport 5:2217–2220

    Article  PubMed  Google Scholar 

  • Diba K, Buzsaki G (2007) Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci 10:1241–1242

    Article  PubMed  PubMed Central  Google Scholar 

  • Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neurosci 11:114–126

    Article  PubMed  Google Scholar 

  • Diekelmann S, Wilhelm I, Born J (2009) The whats and whens of sleep-dependent memory consolidation. Sleep Med Rev 13(5):309--321

    Google Scholar 

  • Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55:51–86

    Article  PubMed  Google Scholar 

  • Düzel E, Penny WD, Burgess N (2010) Brain oscillations and memory. Curr Opin Neurobiol 20:143–149

    Article  PubMed  Google Scholar 

  • Ego-Stengel V, Wilson MA (2009) Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20:1–10

    Google Scholar 

  • Eichenbaum H (2004) Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44:109–120

    Article  PubMed  Google Scholar 

  • 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 18:2596–2603

    Article  PubMed  Google Scholar 

  • 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 Cortex

    Google Scholar 

  • Fell J, Axmacher N (2011) The role of phase synchronization in memory processes. Nat Rev Neurosci 12:105–118

    Article  PubMed  Google Scholar 

  • Fogel SM, Smith CT (2006) Learning-dependent changes in sleep spindles and Stage 2 sleep. J Sleep Res 15:250–255

    Article  PubMed  Google Scholar 

  • Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440:680–683

    Article  PubMed  Google Scholar 

  • Frankland PW, Bontempi B (2005) The organization of recent and remote memories. Nat Rev Neurosci 6:119–130

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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):730–737

    Article  PubMed  Google Scholar 

  • Gais S, Born J (2004a) Declarative memory consolidation: mechanisms acting during human sleep. Learn Mem 11:679–685

    Article  PubMed  PubMed Central  Google Scholar 

  • Gais S, Born J (2004b) Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation. Proc Natl Acad Sci U S A 101:2140–2144

    Article  PubMed  PubMed Central  Google Scholar 

  • Gais S, Mölle M, Helms K, Born J (2002) Learning-dependent increases in sleep spindle density. J Neurosci 22:6830–6834

    PubMed  Google Scholar 

  • 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 33:18469–18480

    Article  PubMed  PubMed Central  Google Scholar 

  • Girardeau G, Zugaro M (2011) Hippocampal ripples and memory consolidation. Curr Opin Neurobiol

    Google Scholar 

  • Girardeau G, Benchenane K, Wiener SI, Buzsaki G, Zugaro MB (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 12:1222–1223

    Article  PubMed  Google Scholar 

  • Giuditta A (2014) Sleep memory processing: the sequential hypothesis. Front Syst Neurosci 8:219

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 69:157–166

    Article  PubMed  Google Scholar 

  • Greenberg DL, Rubin DC (2003) The neuropsychology of autobiographical memory. Cortex 39:687–728

    Article  PubMed  Google Scholar 

  • Gruber MJ, Ritchey M, Wang SF, Doss MK, Ranganath C (2016) Post-learning hippocampal dynamics promote preferential retention of rewarding events. Neuron 89:1110–1120

    Article  PubMed  Google Scholar 

  • Harris KD, Thiele A (2011) Cortical state and attention. Nat Rev Neurosci 12:509–523

    Article  PubMed  PubMed Central  Google Scholar 

  • Hasselmo ME (1999) Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci 3:351–359

    Article  PubMed  Google Scholar 

  • 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 15:936–949

    Article  PubMed  Google Scholar 

  • 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 145:207–231

    Article  PubMed  Google Scholar 

  • Hill S, Tononi G (2005) Modeling sleep and wakefulness in the thalamocortical system. J Neurophysiol 93:1671–1698

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Hutchison IC, Rathore S (2015) The role of REM sleep theta activity in emotional memory. Front Psychol 6:1439

    Article  PubMed  PubMed Central  Google Scholar 

  • 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, IL

    Google Scholar 

  • 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 52:871–882

    Article  PubMed  Google Scholar 

  • Jensen O (2005) Reading the hippocampal code by theta phase-locking. Trends Cogn Sci 9:551–553

    Article  PubMed  Google Scholar 

  • Jones EG (2001) The thalamic matrix and thalamocortical synchrony. Trends Neurosci 24:595–601

    Article  PubMed  Google Scholar 

  • Josselyn SA, Kohler S, Frankland PW (2015) Finding the engram. Nat Rev Neurosci 16:521–534

    Article  PubMed  Google Scholar 

  • 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 28:6104–6110

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 30:7770–7782

    Article  PubMed  PubMed Central  Google Scholar 

  • Lisman JE, Jensen O (2013) The theta-gamma neural code. Neuron 77:1002–1016

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 99:449–454

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 491:547–553

    Article  PubMed  Google Scholar 

  • Lubenov EV, Siapas AG (2009) Hippocampal theta oscillations are travelling waves. Nature 459:534–539

    Article  PubMed  Google Scholar 

  • Luthi A (2014) Sleep spindles: where they come from, what they do. Neuroscientist 20:243–256

    Google Scholar 

  • Maquet P (2001) The role of sleep in learning and memory. Science 294:1048–1052

    Article  PubMed  Google Scholar 

  • 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 671:329–332

    Article  PubMed  Google Scholar 

  • Marshall L, Mölle M, Hallschmid M, Born J (2004) Transcranial direct current stimulation during sleep improves declarative memory. J Neurosci 24:9985–9992

    Article  PubMed  Google Scholar 

  • Marshall L, Helgadottir H, Mölle M, Born J (2006) Boosting slow oscillations during sleep potentiates memory. Nature 444:610–613

    Article  PubMed  Google Scholar 

  • 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 29:13484–13493

    Article  PubMed  Google Scholar 

  • Massimini M, Huber R, Ferrarelli F, Hill S, Tononi G (2004) The sleep slow oscillation as a traveling wave. J Neurosci 24:6862–6870

    Article  PubMed  Google Scholar 

  • 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 102:419–457

    Article  PubMed  Google Scholar 

  • McCormick DA (1992) Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog Neurobiol 39:337–388

    Article  PubMed  Google Scholar 

  • Meeter M, Murre JM (2004) Consolidation of long-term memory: evidence and alternatives. Psychol Bull 130:843–857

    Article  PubMed  Google Scholar 

  • 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 22:10941–10947

    PubMed  Google Scholar 

  • 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 101:13963–13968

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 96:62–70

    Article  PubMed  Google Scholar 

  • 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 29:1071–1081

    Article  PubMed  Google Scholar 

  • 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 34:1411–1421

    PubMed  PubMed Central  Google Scholar 

  • Morris RG (2006) Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci 23:2829–2846

    Article  PubMed  Google Scholar 

  • Müller GE, Pilzecker A (1900) Experimentelle Beiträge zur Lehre vom Gedächtnis. Z Psychol Ergänzungsband 1:1–300

    Google Scholar 

  • 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 106:1608–1613

    Article  PubMed  PubMed Central  Google Scholar 

  • Ngo HV, Martinetz T, Born J, Molle M (2013) Auditory closed-loop stimulation of the sleep slow oscillation enhances memory. Neuron 78:545–553

    Article  PubMed  Google Scholar 

  • 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 35:6630–6638

    Article  PubMed  PubMed Central  Google Scholar 

  • Nir Y, Staba RJ, Andrillon T, Vyazovskiy VV, Cirelli C, Fried I, Tononi G (2011) Regional slow waves and spindles in human sleep. Neuron 70:153–169

    Article  PubMed  PubMed Central  Google Scholar 

  • Norman KA, Polyn SM, Detre GJ, Haxby JV (2006) Beyond mind-reading: multi-voxel pattern analysis of fMRI data. Trends Cogn Sci 10:424–430

    Article  PubMed  Google Scholar 

  • O’Keefe J (1976) Place units in the hippocampus of the freely moving rat. Exp Neurol 51:78–109

    Article  PubMed  Google Scholar 

  • 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 33:17029–17041

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 44:535–545

    Article  PubMed  Google Scholar 

  • 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:e100

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 24:6446–6456

    Article  PubMed  Google Scholar 

  • 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--196

    Google Scholar 

  • 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 35:69–79

    PubMed  PubMed Central  Google Scholar 

  • 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 12:919–926

    Article  PubMed  Google Scholar 

  • Poppenk J, Evensmoen HR, Moscovitch M, Nadel L (2013) Long-axis specialization of the human hippocampus. Trends Cogn Sci 17:230–240

    Article  PubMed  Google Scholar 

  • Ramanathan DS, Gulati T, Ganguly K (2015) Sleep-dependent reactivation of ensembles in motor cortex promotes skill consolidation. PLoS Biol 13:e1002263

    Article  PubMed  PubMed Central  Google Scholar 

  • Ranganath C, Ritchey M (2012) Two cortical systems for memory-guided behaviour. Nat Rev Neurosci 13:713–726

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Rasch BH, Born J, Gais S (2006) Combined blockade of cholinergic receptors shifts the brain from stimulus encoding to memory consolidation. J Cogn Neurosci 18:793–802

    Article  PubMed  Google Scholar 

  • 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, DC

    Google Scholar 

  • 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 1:43–55

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosanova M, Ulrich D (2005) Pattern-specific associative long-term potentiation induced by a sleep spindle-related spike train. J Neurosci 25:9398–9405

    Article  PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • Sanchez-Vives MV, McCormick DA (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3:1027–1034

    Article  PubMed  Google Scholar 

  • Santoro A, Frankland PW (2014) Chasing the trace. Neuron 84:243–246

    Article  PubMed  Google Scholar 

  • 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 86:425–432

    Google Scholar 

  • 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 104:13164–13169

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 1191:127–135

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Sharma AV, Wolansky T, Dickson CT (2010) A comparison of sleep-like slow oscillations in the hippocampus under ketamine and urethane anaesthesia. J Neurophysiol 104:932–939

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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 100:2065–2069

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 98:898–910

    Article  PubMed  Google Scholar 

  • 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 88:1743–1752

    PubMed  Google Scholar 

  • Staresina BP, Alink A, Kriegeskorte N, Henson RN (2013) Awake reactivation predicts memory in humans. Proc Natl Acad Sci U S A 110:21159–21164

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 18:1679–1686

    Article  PubMed  PubMed Central  Google Scholar 

  • Steriade M (2003) The corticothalamic system in sleep. Front Biosci 8:d878–d899

    Article  PubMed  Google Scholar 

  • Steriade M (2004) Acetylcholine systems and rhythmic activities during the waking–sleep cycle. Prog Brain Res 145:179–196

    Article  PubMed  Google Scholar 

  • Steriade M (2006) Grouping of brain rhythms in corticothalamic systems. Neuroscience 137:1087–1106

    Article  PubMed  Google Scholar 

  • Steriade M, Timofeev I (2003) Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 37:563–576

    Article  PubMed  Google Scholar 

  • 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 13:3266–3283

    PubMed  Google Scholar 

  • Steriade M, Nunez A, Amzica F (1993b) A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13:3252–3265

    PubMed  Google Scholar 

  • Strange BA, Witter MP, Lein ES, Moser EI (2014) Functional organization of the hippocampal longitudinal axis. Nat Rev Neurosci 15:655–669

    Article  PubMed  Google Scholar 

  • 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 31:8605–8616

    Article  PubMed  PubMed Central  Google Scholar 

  • Sutherland GR, McNaughton B (2000) Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr Opin Neurobiol 10:180–186

    Article  PubMed  Google Scholar 

  • Tambini A, Davachi L (2013) Persistence of hippocampal multivoxel patterns into postencoding rest is related to memory. Proc Natl Acad Sci U S A 110:19591–19596

    Article  PubMed  PubMed Central  Google Scholar 

  • Tambini A, Ketz N, Davachi L (2010) Enhanced brain correlations during rest are related to memory for recent experiences. Neuron 65:280–290

    Article  PubMed  PubMed Central  Google Scholar 

  • Timofeev I, Grenier F, Bazhenov M, Sejnowski TJ, Steriade M (2000) Origin of slow cortical oscillations in deafferented cortical slabs. Cereb Cortex 10:1185–1199

    Article  PubMed  Google Scholar 

  • 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 542:583–598

    Article  PubMed  PubMed Central  Google Scholar 

  • Tononi G, Cirelli C (2003) Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull 62:143–150

    Article  PubMed  Google Scholar 

  • Urrestarazu E, Chander R, Dubeau F, Gotman J (2007) Interictal high-frequency oscillations (100-500 Hz) in the intracerebral EEG of epileptic patients. Brain 130:2354–2366

    Article  PubMed  Google Scholar 

  • van Kesteren MT, Ruiter DJ, Fernandez G, Henson RN (2012) How schema and novelty augment memory formation. Trends Neurosci 35:211–219

    Article  PubMed  Google Scholar 

  • 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 219:911–929

    Article  PubMed  Google Scholar 

  • Walker MP, Stickgold R (2010) Overnight alchemy: sleep-dependent memory evolution. Nat Rev Neurosci 11:218; author reply 218

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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 26:6213–6229

    Article  PubMed  Google Scholar 

  • 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 66:28–35

    Article  PubMed  Google Scholar 

  • Zhang H, Jacobs J (2015) Traveling theta waves in the human hippocampus. J Neurosci 35:12477–12487

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

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).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Til Ole Bergmann or Bernhard P. Staresina .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Bergmann, T.O., Staresina, B.P. (2017). Neuronal Oscillations and Reactivation Subserving Memory Consolidation. In: Axmacher, N., Rasch, B. (eds) Cognitive Neuroscience of Memory Consolidation. Studies in Neuroscience, Psychology and Behavioral Economics. Springer, Cham. https://doi.org/10.1007/978-3-319-45066-7_12

Download citation

Publish with us

Policies and ethics