Skip to main content
SpringerLink
Log in

Replay in Humans—First Evidence and Open Questions

  • Chapter
  • First Online:
Cognitive Neuroscience of Memory Consolidation

Abstract

Memory consolidation serves to stabilize initially fragile memory traces. Rodent studies suggest that consolidation relies on replay of previously acquired stimulus-specific activity patterns. This replay is coupled to hippocampal sharp wave-ripple (SWR) events and sleep spindles. More recently, the application of multivariate analysis methods has allowed identifying stimulus-specific “engram patterns” in humans as well. These analyses have been applied to various modalities including functional magnetic resonance imaging (fMRI) and intracranial EEG (iEEG). A few initial studies suggest that engram patterns are indeed replayed after learning in humans, during awake resting state, tasks, and sleep. Here, we review these studies and point to open questions. It has been repeatedly shown that the extent of engram pattern replay predicts later memory performance, and that replay occurs during both awake resting state and sleep. On the other hand, cuing of specific memories improves memory consolidation selectively during sleep. Brain stimulation may disrupt consolidation on a behavioral level, but its effect on replay of engram patterns has not been shown yet. Finally, replay has been indirectly linked to sleep spindles, while its relationship to SWRs remains to be investigated. To summarize, the investigation of engram pattern replay in the human brain is an emerging field with still many open questions.

……how are common subevents copied out of the memory during the codon formation for new classificatory units? …… When a subevent cluster of sufficient size and importance has been formed, this centre will (perhaps during sleep) call the information out from the memory during a period when codon formation is possible.

—David Marr (1971)

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

Access this chapter

Log in via an institution
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

References

  • Abeles M (1982) Local cortical circuites: an electrophysiological study. Springer, Berlin

    Book  Google Scholar 

  • Alvarez P, Squire LR (1994) Memory consolidation and the medial temporallobe: a simple network model. Proc Natl Acad Sci USA 91(15):7041–7045

    Google Scholar 

  • Axmacher N, Elger CE, Fell J (2008) Ripples in the medial temporal lobe are relevant for human memory consolidation. Brain 131(Pt 7):1806–1817

    Article  PubMed  Google Scholar 

  • Axmacher N et al (2009) Memory processes during sleep: beyond the standard consolidation theory. Cell Mol Life Sci 66(14):2285–2297

    Article  PubMed  Google Scholar 

  • Bergmann TO et al (2012) Sleep spindle-related reactivation of category-specific cortical regions after learning face-scene associations. Neuroimage 59(3):2733–2742

    Article  PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • Carr MF, Jadhav SP, Frank LM (2011) Hippocampal replay in the Awake state: a potential substrate for memory consolidation and retrieval. Nat Neurosci 14(2):147–153

    Article  PubMed  PubMed Central  Google Scholar 

  • Clemens Z et al (2007) Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 130(Pt 11):2868–2878

    Article  PubMed  Google Scholar 

  • Cohen NJ, Eichenbaum H (1993) Memory, amnesia, and the hippocampal system. MIT Press, Cambridge, MA

    Google Scholar 

  • Cox R et al (2014) Local sleep spindle modulations in relation to specific memory cues. Neuroimage 99:103–110

    Article  PubMed  Google Scholar 

  • Dave AS, Margoliash D (2000) Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290(5492):812–816

    Article  PubMed  Google Scholar 

  • Deuker L et al (2013) Memory consolidation by replay of stimulus-specific neural activity. J Neurosci 33(49):19373–19383

    Article  PubMed  Google Scholar 

  • Diekelmann S et al (2011) Labile or stable: opposing consequences for memory when reactivated during waking and sleep. Nat Neurosci 14(3):381–386

    Article  PubMed  Google Scholar 

  • Ego-Stengel V, Wilson MA (2010) Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20(1):1–10

    PubMed  PubMed Central  Google Scholar 

  • Engel AK et al (2005) Invasive recordings from the human brain: Clinical insights and beyond. Nat Rev Neurosci 6(1):35–47

    Article  PubMed  Google Scholar 

  • Farah MJ (1989) The neural basis of mental imagery. Trends Neurosci 12(10):395–399

    Article  PubMed  Google Scholar 

  • Girardeau G, Zugaro M (2011) Hippocampal ripples and memory consolidation. Curr Opin Neurobiol 21(3):452–459

    Article  PubMed  Google Scholar 

  • Girardeau G et al (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 12(10):1222–1223

    Article  PubMed  Google Scholar 

  • Haxby JV et al (2001) Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 293(5539):2425–2430

    Article  PubMed  Google Scholar 

  • Haynes JD (2015) A primer on pattern-based approaches to FMRI: principles, pitfalls, and perspectives. Neuron 87(2):257–270

    Article  PubMed  Google Scholar 

  • Josselyn SA, Kohler S, Frankland PW (2015) Finding the engram. Nat Rev Neurosci 16(9):521–534

    Article  PubMed  Google Scholar 

  • Kaplan R et al (2016) Hippocampal sharp-wave ripples influence selective activation of the default mode network. Curr Biol 26(5):686–691

    Article  PubMed  PubMed Central  Google Scholar 

  • Karlsson MP, Frank LM (2009) Awake replay of remote experiences in the hippocampus. Nat Neurosci 12(7):913–918

    Article  PubMed  PubMed Central  Google Scholar 

  • Kriegeskorte N, Mur M, Bandettini P (2008) Representational similarity analysis—connecting the branches of systems neuroscience. Front Syst Neurosci 2:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Kudrimoti HS, Barnes CA, McNaughton BL (1999) Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci 19(10):4090–4101

    PubMed  Google Scholar 

  • LaRocque JJ et al (2013) Decoding attended information in short-term memory: an EEG study. J Cogn Neurosci 25(1):127–142

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Lee H, Fell J, Axmacher N (2013) Electrical engram: how deep brain stimulation affects memory. Trends Cogn Sci 17(11):574–584

    Article  PubMed  Google Scholar 

  • Lepsien J, Nobre AC (2007) Attentional modulation of object representations in working memory. Cereb Cortex 17(9):2072–2083

    Article  PubMed  Google Scholar 

  • Logothetis NK et al (2012) Hippocampal-cortical interaction during periods of subcortical silence. Nature 491(7425):547–553

    Article  PubMed  Google Scholar 

  • Maquet P et al (2000) Experience-dependent changes in cerebral activation during human REM sleep. Nat Neurosci 3(8):831–836

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Mellet E et al (1998) Reopening the mental imagery debate: lessons from functional anatomy. Neuroimage 8(2):129–139

    Article  PubMed  Google Scholar 

  • Muellbacher W et al (2002) Early consolidation in human primary motor cortex. Nature 415(6872):640–644

    Article  PubMed  Google Scholar 

  • Nadasdy Z et al (1999) Replay and time compression of recurring spike sequences in the hippocampus. J Neurosci 19(21):9497–9507

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Nokia MS, Penttonen M, Wikgren J (2010) Hippocampal ripple-contingent training accelerates trace eyeblink conditioning and retards extinction in rabbits. J Neurosci 30(34):11486–11492

    Article  PubMed  Google Scholar 

  • O’Keefe J (1976) Place units in the hippocampus of the freely moving rat. Exp Neurol 51(1):78–109

    Article  PubMed  Google Scholar 

  • Oudiette D et al (2013) The role of memory reactivation during wakefulness and sleep in determining which memories endure. J Neurosci 33(15):6672–6678

    Article  PubMed  PubMed Central  Google Scholar 

  • Palm G (1990) Cell assemblies as a guideline for brain research. Concepts Neurosci 1:133–147

    Google Scholar 

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

    PubMed  Google Scholar 

  • Peigneux P et al (2004) Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44(3):535–545

    Article  PubMed  Google Scholar 

  • Peigneux P et al (2006) Offline persistence of memory-related cerebral activity during active wakefulness. PLoS Biol 4(4):e100

    Article  PubMed  PubMed Central  Google Scholar 

  • Polania R, Paulus W, Nitsche MA (2012) Noninvasively decoding the contents of visual working memory in the human prefrontal cortex within high-gamma oscillatory patterns. J Cogn Neurosci 24(2):304–314

    Article  PubMed  Google Scholar 

  • Polyn SM et al (2005) Category-specific cortical activity precedes retrieval during memory search. Science 310(5756):1963–1966

    Article  PubMed  Google Scholar 

  • Rasch B et al (2007) Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 315(5817):1426–1429

    Article  PubMed  Google Scholar 

  • Rissman J, Wagner AD (2012) Distributed representations in memory: insights from functional brain imaging. Annu Rev Psychol 63:101–128

    Article  PubMed  Google Scholar 

  • Robertson EM, Press DZ, Pascual-Leone A (2005) Off-line learning and the primary motor cortex. J Neurosci 25(27):6372–6378

    Article  PubMed  Google Scholar 

  • Rodriguez-Ortiz CJ, Bermudez-Rattoni F (2007) Memory reconsolidation or updating consolidation? In: Bermudez-Rattoni F (Ed.) Neural plasticity and memory: from genes to brain imaging, Boca Raton (FL)

    Google Scholar 

  • Rudoy JD et al (2009) Strengthening individual memories by reactivating them during sleep. Science 326(5956):1079–1079

    Article  PubMed  PubMed Central  Google Scholar 

  • Schacter DL (2001) Forgotten ideas, neglected pioneers: Richard Semon and the story of memory. illustrated ed. 2001. Psychology Press, UK

    Google Scholar 

  • Schreiner T, Rasch B (2015) Boosting vocabulary learning by verbal cueing during sleep. Cereb Cortex 25(11):4169–4179

    Article  PubMed  Google Scholar 

  • Semon R (1921) The Mneme. George Allen & Unwin, London

    Google Scholar 

  • Semon R (1923) Mnemic psychology. George Allen & Unwin, London

    Google Scholar 

  • Skaggs WE et al (2007) EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. J Neurophysiol 98(2):898–910

    Article  PubMed  Google Scholar 

  • Staresina BP et al (2012) Episodic reinstatement in the medial temporal lobe. J Neurosci 32(50):18150–18156

    Article  PubMed  PubMed Central  Google Scholar 

  • Staresina BP et al (2013) Awake reactivation predicts memory in humans. Proc Natl Acad Sci U S A 110(52):21159–21164

    Article  PubMed  PubMed Central  Google Scholar 

  • Staudigl T et al (2015) Temporal-pattern similarity analysis reveals the beneficial and detrimental effects of context reinstatement on human memory. J Neurosci 35(13):5373–5384

    Article  PubMed  Google Scholar 

  • Takashima A et al (2009) Shift from hippocampal to neocortical centered retrieval network with consolidation. J Neurosci 29(32):10087–10093

    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(48):19591–19596

    Article  PubMed  PubMed Central  Google Scholar 

  • van Dongen EV et al (2012) Memory stabilization with targeted reactivation during human slow-wave sleep. Proc Natl Acad Sci USA 109(26):10575–10580

    Article  PubMed  PubMed Central  Google Scholar 

  • Waldhauser GT, Braun V, Hanslmayr S (2016) Episodic memory retrieval functionally relies on very rapid reactivation of sensory information. J Neurosci 36(1):251–260

    Article  PubMed  Google Scholar 

  • Watrous AJ et al (2015) More than spikes: common oscillatory mechanisms for content specific neural representations during perception and memory. Curr Opin Neurobiol 31:33–39

    Article  PubMed  Google Scholar 

  • Waydo S et al (2006) Sparse representation in the human medial temporal lobe. J Neurosci 26(40):10232–10234

    Article  PubMed  Google Scholar 

  • Xue G et al (2010) Greater neural pattern similarity across repetitions is associated with better memory. Science 330(6000):97–101

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang H et al (2015) Gamma power reductions accompany stimulus-specific representations of dynamic events. Curr Biol 25(5):635–640

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neuropsychology, Institute of Cognitive Neuroscience, Faculty of Psychology, Ruhr University Bochum, Universitaetsstrasse 150, 44801, Bochum, Germany

    Hui Zhang, Lorena Deuker & Nikolai Axmacher

Authors
  1. Hui Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lorena Deuker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nikolai Axmacher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nikolai Axmacher .

Editor information

Editors and Affiliations

  1. Ruhr-University Bochum, Bochum, Germany

    Nikolai Axmacher

  2. University of Fribourg, Fribourg, Switzerland

    Björn Rasch

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Zhang, H., Deuker, L., Axmacher, N. (2017). Replay in Humans—First Evidence and Open Questions. 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_15

Download citation

Publish with us

Policies and ethics

Search

Navigation