Skip to main content

Reorganization of Hippocampal Place-Selective Patterns During Goal-Directed Learning and Their Reactivation During Sleep

  • Chapter
  • First Online:
Analysis and Modeling of Coordinated Multi-neuronal Activity

Part of the book series: Springer Series in Computational Neuroscience ((NEUROSCI,volume 12))

  • 1714 Accesses

Abstract

Firing patterns of hippocampal principal cells are thought to participate in the formation of mnemonic representations of place, which ultimately can be used to guide the behavior of animals in space. Past studies have suggested that place-selective activity in the hippocampus can emphasize the representation of discrete locations associated with a strong behavioral salience. In the first part of this book chapter, we review work that has described how that hippocampal neuronal activity patterns reorganize during spatial learning. These studies revealed that new hippocampal maps emerge during spatial learning to represent the location of goal locations and demonstrated that, during recall, the reinstatement of these maps predicts successful memory performance. In the second part of this chapter, we discuss the role of sleep in memory consolidation in the context of goal-oriented spatial learning. We summarize work that has demonstrated the replay of goal-oriented neuronal assembly patterns that predict subsequent memory recall. Moreover, we argue that the initial strengthening of new maps may in fact take place during learning, triggered by waking sharp-wave/ripple patterns occurring at goal locations. These reviewed studies highlight that the reorganization and replay of place cell firing patterns might constitute a circuit signature for the expression of newly acquired hippocampal engrams.

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 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
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

  1. Morris RG. Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci. 2006;23(11):2829–46.

    Article  CAS  PubMed  Google Scholar 

  2. Squire LR. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev. 1992;99(2):195–231.

    Article  CAS  PubMed  Google Scholar 

  3. Eichenbaum H. A cortical-hippocampal system for declarative memory. Nat Rev Neurosci. 2000;1(1):41–50.

    Article  CAS  PubMed  Google Scholar 

  4. O’Keefe J, Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971;34(1):171–5.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  6. Muller RU, Kubie JL, Ranck Jr JB. Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J Neurosci. 1987;7(7):1935–50.

    CAS  PubMed  Google Scholar 

  7. Kentros C, Hargreaves E, Hawkins RD, Kandel ER, Shapiro M, Muller RV. Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science. 1998;280(5372):2121–6.

    Article  CAS  PubMed  Google Scholar 

  8. Muller RU, Kubie JL. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci. 1987;7(7):1951–68.

    CAS  PubMed  Google Scholar 

  9. Muller R. A quarter of a century of place cells. Neuron. 1996;17(5):813–22.

    Article  CAS  PubMed  Google Scholar 

  10. Ferbinteanu J, Shapiro ML. Prospective and retrospective memory coding in the hippocampus. Neuron. 2003;40(6):1227–39.

    Article  CAS  PubMed  Google Scholar 

  11. Frank LM, Brown EN, Wilson M. Trajectory encoding in the hippocampus and entorhinal cortex. Neuron. 2000;27(1):169–78.

    Article  CAS  PubMed  Google Scholar 

  12. Huxter J, Burgess N, O’Keefe J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature. 2003;425(6960):828–32.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Huxter JR, Senior TJ, Allen K, Csicsvari J. Theta phase-specific codes for two-dimensional position, trajectory and heading in the hippocampus. Nat Neurosci. 2008;11(5):587–94.

    Article  CAS  PubMed  Google Scholar 

  14. Markus EJ, Qin YL, Leonard B, Skaggs WE, McNaughton BL, Barnes CA. Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci. 1995;15(11):7079–94.

    CAS  PubMed  Google Scholar 

  15. Navratilova Z, Hoang LT, Schwindel CD, Tatsuno M, McNaughton BL. Experience-dependent firing rate remapping generates directional selectivity in hippocampal place cells. Front Neur Circ. 2012;6:6.

    Google Scholar 

  16. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, Moser MB. Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science. 2005;309(5734):619–23.

    Article  CAS  PubMed  Google Scholar 

  17. Allen K, Rawlins JNP, Bannerman DM, Csicsvari J. Hippocampal place cells can encode multiple trial-dependent features through rate remapping. J Neurosci. 2012;32(42):14752–66.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Colgin LL, Moser EI, Moser MB. Understanding memory through hippocampal remapping. Trends Neurosci. 2008;31(9):469–77.

    Article  CAS  PubMed  Google Scholar 

  19. Knierim JJ. Dynamic interactions between local surface cues, distal landmarks, and intrinsic circuitry in hippocampal place cells. J Neurosci. 2002;22(14):6254–64.

    CAS  PubMed  Google Scholar 

  20. Anderson MI, Jeffery KJ. Heterogeneous modulation of place cell firing by changes in context. J Neurosci. 2003;23(26):8827–35.

    CAS  PubMed  Google Scholar 

  21. Jackson J, Redish AD. Network dynamics of hippocampal cell-assemblies resemble multiple spatial maps within single tasks. Hippocampus. 2007;17(12):1209–29.

    Article  PubMed  Google Scholar 

  22. Gothard KM, Skaggs WE, Moore KM, McNaughton BL. Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J Neurosci. 1996;16(2):823–35.

    CAS  PubMed  Google Scholar 

  23. Kobayashi T, Tran AH, Nishijo H, Ono T, Matsumoto G. Contribution of hippocampal place cell activity to learning and formation of goal-directed navigation in rats. Neuroscience. 2003;117(4):1025–35.

    Article  CAS  PubMed  Google Scholar 

  24. Kobayashi T, Nishijo H, Fukuda M, Bures J, Ono T. Task-dependent representations in rat hippocampal place neurons. J Neurophysiol. 1997;78(2):597–613.

    CAS  PubMed  Google Scholar 

  25. Fyhn M, Molden S, Hollup S, Moser MB, Moser E. Hippocampal neurons responding to first-time dislocation of a target object. Neuron. 2002;35(3):555–66.

    Article  CAS  PubMed  Google Scholar 

  26. Hollup SA, Molden S, Donnett JG, Moser MB, Moser EI. Accumulation of hippocampal place fields at the goal location in an annular water maze task. J Neurosci. 2001;21(5):1635–44.

    CAS  PubMed  Google Scholar 

  27. Hok V, Lenck-Santini PP, Roux S, Save E, Muller RU, Poucet B. Goal-related activity in hippocampal place cells. J Neurosci. 2007;27(3):472–82.

    Article  CAS  PubMed  Google Scholar 

  28. Lee I, Griffin AL, Zilli EA, Eichenbaum H, Hasselmo ME. Gradual translocation of spatial correlates of neuronal firing in the hippocampus toward prospective reward locations. Neuron. 2006;51(5):639–50.

    Article  CAS  PubMed  Google Scholar 

  29. Kelemen E, Fenton AA. Dynamic grouping of hippocampal neural activity during cognitive control of two spatial frames. PLoS Biol. 2010;8(6):e1000403.

    Article  PubMed Central  PubMed  Google Scholar 

  30. Barnes CA. Memory deficits associated with senescence - neurophysiological and behavioral-study in the rat. J Comp Physiol Psychol. 1979;93(1):74–104.

    Article  CAS  PubMed  Google Scholar 

  31. Kentros CG, Agnihotri NT, Streater S, Hawkins RD, Kandel ER. Increased attention to spatial context increases both place field stability and spatial memory. Neuron. 2004;42(2):283–95.

    Article  CAS  PubMed  Google Scholar 

  32. Gilbert PE, Kesner RP, DeCoteau WE. Memory for spatial location: role of the hippocampus in mediating spatial pattern separation. J Neurosci. 1998;18(2):804–10.

    CAS  PubMed  Google Scholar 

  33. Dupret D, O’Neill J, Pleydell-Bouverie B, Csicsvari J. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat Neurosci. 2010;13(8):995–1002.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Breese CR, Hampson RE, Deadwyler SA. Hippocampal place cells - stereotypy and plasticity. J Neurosci. 1989;9(4):1097–111.

    CAS  PubMed  Google Scholar 

  35. Smith DM, Mizumori SJY. Learning-related development of context-specific neuronal responses to places and events. The hippocampal role in context processing. J Neurosci. 2006;26(12):3154–63.

    Article  CAS  PubMed  Google Scholar 

  36. Jezek K, Henriksen EJ, Treves A, Moser EI, Moser MB. Theta-paced flickering between place-cell maps in the hippocampus. Nature. 2011;478(7368):246–U136.

    Article  CAS  PubMed  Google Scholar 

  37. Hopfield JJ. Pattern-recognition computation using action-potential timing for stimulus representation. Nature. 1995;376(6535):33–6.

    Article  CAS  PubMed  Google Scholar 

  38. Grossberg S. How does a brain build a cognitive code. Psychol Rev. 1980;87(1):1–51.

    Article  CAS  PubMed  Google Scholar 

  39. Dupret D, O’Neill J, Csicsvari J. Dynamic reconfiguration of hippocampal interneuron circuits during spatial learning. Neuron. 2013;78(1):166–80.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Glickman SE. Perseverative neural processes and consolidation of the memory trace. Psychol Bull. 1961;58:218–33.

    Article  CAS  PubMed  Google Scholar 

  41. McGaugh JL. Time-dependent processes in memory storage. Science. 1966;153(742):1351–8.

    Article  CAS  PubMed  Google Scholar 

  42. 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 

  43. Maquet P. The role of sleep in learning and memory. Science. 2001;294(5544):1048–52.

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  45. Stickgold R, Hobson JA, Fosse R, Fosse M. Sleep, learning, and dreams: off-line memory reprocessing. Science. 2001;294(5544):1052–7.

    Article  CAS  PubMed  Google Scholar 

  46. Rasch B, Buchel C, Gais S, Born J. Odor cues during slow-wave sleep prompt declarative memory consolidation. Science. 2007;315(5817):1426–9.

    Article  CAS  PubMed  Google Scholar 

  47. Bendor D, Wilson MA. Biasing the content of hippocampal replay during sleep. Nat Neurosci. 2012;15(10):1439–44.

    Article  CAS  PubMed  Google Scholar 

  48. Steriade M, Timofeev I. Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron. 2003;37(4):563–76.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  50. Buzsaki G. Hippocampal sharp waves: their origin and significance. Brain Res. 1986;398(2):242–52.

    Article  CAS  PubMed  Google Scholar 

  51. O’Keefe J, Nadel L. The hippocampus as a cognitive map. Oxford: Oxford University Press; 1978.

    Google Scholar 

  52. Csicsvari J, Hirase H, Mamiya A, Buzsaki G. Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron. 2000;28(2):585–94.

    Article  CAS  PubMed  Google Scholar 

  53. Csicsvari J, Hirase H, Czurko A, Mamiya A, Buzsaki G. Fast network oscillations in the hippocampal CA1 region of the behaving rat. J Neurosci. 1999;19(16):RC20.

    CAS  PubMed  Google Scholar 

  54. Kudrimoti HS, Barnes CA, McNaughton BL. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci. 1999;19(10):4090–101.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  56. O’Neill J, Senior TJ, Allen K, Huxter JR, Csicsvari J. Reactivation of experience-dependent cell assembly patterns in the hippocampus. Nat Neurosci. 2008;11(2):209–15.

    Article  PubMed  Google Scholar 

  57. King C, Henze DA, Leinekugel X, Buzsaki G. Hebbian modification of a hippocampal population pattern in the rat. J Physiol. 1999;521(Pt 1):159–67.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  58. O’Neill J, Pleydell-Bouverie B, Dupret D, Csicsvari J. Play it again: reactivation of waking experience and memory. Trends Neurosci. 2010;33(5):220–9.

    Article  PubMed  Google Scholar 

  59. Girardeau G, Benchenane K, Wiener SI, Buzsaki G, Zugaro MB. Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci. 2009;12(10):1222–3.

    Article  CAS  PubMed  Google Scholar 

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

    PubMed Central  PubMed  Google Scholar 

  61. Singer AC, Frank LM. Rewarded outcomes enhance reactivation of experience in the hippocampus. Neuron. 2009;64(6):910–21.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  62. O’Neill J, Senior T, Csicsvari J. Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron. 2006;49(1):143–55.

    Article  PubMed  Google Scholar 

  63. Csicsvari J, O’Neill J, Allen K, Senior T. Place-selective firing contributes to the reverse-order reactivation of CA1 pyramidal cells during sharp waves in open-field exploration. Eur J Neurosci. 2007;26:704–16.

    Article  PubMed Central  PubMed  Google Scholar 

  64. Jackson JC, Johnson A, Redish AD. Hippocampal sharp waves and reactivation during awake states depend on repeated sequential experience. J Neurosci. 2006;26(48):12415–26.

    Article  CAS  PubMed  Google Scholar 

  65. Foster DJ, Wilson MA. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature. 2006;440(7084):680–3.

    Article  CAS  PubMed  Google Scholar 

  66. Davidson TJ, Kloosterman F, Wilson MA. Hippocampal replay of extended experience. Neuron. 2009;63(4):497–507.

    Article  CAS  PubMed  Google Scholar 

  67. Diba K, Buzsaki G. Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci. 2007;10(10):1241–2.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  68. Cheng S, Frank LM. New experiences enhance coordinated neural activity in the hippocampus. Neuron. 2008;57(2):303–13.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  69. Carr MF, Jadhav SP, Frank LM. Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat Neurosci. 2011;14(2):147–53.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  70. Jadhav SP, Kemere C, German PW, Frank LM. Awake hippocampal sharp-wave ripples support spatial memory. Science. 2012;336(6087):1454–8.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Dupret Ph.D. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media New York

About this chapter

Cite this chapter

Dupret, D., Csicsvari, J. (2015). Reorganization of Hippocampal Place-Selective Patterns During Goal-Directed Learning and Their Reactivation During Sleep. In: Tatsuno, M. (eds) Analysis and Modeling of Coordinated Multi-neuronal Activity. Springer Series in Computational Neuroscience, vol 12. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1969-7_6

Download citation

Publish with us

Policies and ethics