Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Awake replay of remote experiences in the hippocampus

Abstract

Hippocampal replay is thought to be essential for the consolidation of event memories in hippocampal-neocortical networks. Replay is present during both sleep and waking behavior, but although sleep replay involves the reactivation of stored representations in the absence of specific sensory inputs, awake replay is thought to depend on sensory input from the current environment. Here, we show that stored representations are reactivated during both waking and sleep replay. We found frequent awake replay of sequences of rat hippocampal place cells from a previous experience. This spatially remote replay was as common as local replay of the current environment and was more robust when the rat had recently been in motion than during extended periods of quiescence. Our results indicate that the hippocampus consistently replays past experiences during brief pauses in waking behavior, suggesting a role for waking replay in memory consolidation and retrieval.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Overview of experimental design.
Figure 2: Spatially remote awake replay in the rest box.
Figure 3: Replay of environment 1 in the rest box is more robust during awake than quiescent periods.
Figure 4: Robust replay of environment 1 while the rat was located in environment 2.
Figure 5: Local spatial rate and replay initiation for environment 1 replay in environment 2 and the rest box.

References

  1. Scoville, W.B. & Milner, B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 11–21 (1957).

    CAS  Article  Google Scholar 

  2. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Oxford University Press, London, 1978).

    Google Scholar 

  3. Buzsáki, G. The hippocampo-neocortical dialogue. Cereb. Cortex 6, 81–92 (1996).

    Article  Google Scholar 

  4. Sutherland, G.R. & McNaughton, B. Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr. Opin. Neurobiol. 10, 180–186 (2000).

    CAS  Article  Google Scholar 

  5. Suzuki, W.A. Encoding new episodes and making them stick. Neuron 50, 19–21 (2006).

    CAS  Article  Google Scholar 

  6. Wilson, M.A. & McNaughton, B.L. Reactivation of hippocampal ensemble memories during sleep. Science 265, 676–679 (1994).

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  9. Buzsáki, G. Hippocampal sharp waves: their origin and significance. Brain Res. 398, 242–252 (1986).

    Article  Google Scholar 

  10. Csicsvari, J., Hirase, H., Mamiya, A. & Buzsaki, G. Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave–associated population events. Neuron 28, 585–594 (2000).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  12. Kudrimoti, H.S., Barnes, C.A. & McNaughton, B.L. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience and EEG dynamics. J. Neurosci. 19, 4090–4101 (1999).

    CAS  Article  Google Scholar 

  13. O'Neill, J., Senior, T.J., Allen, K., Huxter, J.R. & Csicsvari, J. Reactivation of experience-dependent cell assembly patterns in the hippocampus. Nat. Neurosci. 11, 209–215 (2008).

    CAS  Article  Google Scholar 

  14. Lee, A.K. & Wilson, M.A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183–1194 (2002).

    CAS  Article  Google Scholar 

  15. Ji, D. & Wilson, M.A. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci. 10, 100–107 (2007).

    CAS  Article  Google Scholar 

  16. Nádasdy, Z., Hirase, H., Czurko, A., Csicsvari, J. & Buzsaki, G. Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 19, 9497–9507 (1999).

    Article  Google Scholar 

  17. Foster, D.J. & Wilson, M.A. Reverse replay of behavioral sequences in hippocampal place cells during the awake state. Nature 440, 680–683 (2006).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  19. 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. 26, 704–716 (2007).

    Article  Google Scholar 

  20. Karlsson, M.P. & Frank, L.M. Network dynamics underlying the formation of sparse, informative representations in the hippocampus. J. Neurosci. 28, 14271–14281 (2008).

    CAS  Article  Google Scholar 

  21. Frank, L.M., Brown, E.N. & Wilson, M.A. Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27, 169–178 (2000).

    CAS  Article  Google Scholar 

  22. Kim, S.M. & Frank, L.M. Hippocampal lesions impair rapid learning of a continuous alternation task. PLoS One 4, e5494 (2009).

    Article  Google Scholar 

  23. O'Keefe, J. & Recce, M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317–330 (1993).

    CAS  Article  Google Scholar 

  24. Brown, E.N., Frank, L.M., Tang, D., Quirk, M.C. & Wilson, M.A. A statistical paradigm for neural spike train decoding applied to position prediction from ensemble firing patterns of rat hippocampal place cells. J. Neurosci. 18, 7411–7425 (1998).

    CAS  Article  Google Scholar 

  25. Zhang, K., Ginzburg, I., McNaughton, B.L. & Sejnowski, T.J. Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. J. Neurophysiol. 79, 1017–1044 (1998).

    CAS  Article  Google Scholar 

  26. Johnson, A. & Redish, A.D. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 27, 12176–12189 (2007).

    CAS  Article  Google Scholar 

  27. Frank, L.M., Stanley, G.B. & Brown, E.N. Hippocampal plasticity across multiple days of exposure to novel environments. J. Neurosci. 24, 7681–7689 (2004).

    CAS  Article  Google Scholar 

  28. Euston, D.R., Tatsuno, M. & McNaughton, B.L. Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 318, 1147–1150 (2007).

    CAS  Article  Google Scholar 

  29. de Hoz, L. & Wood, E.R. Dissociating the past from the present in the activity of place cells. Hippocampus 16, 704–715 (2006).

    Article  Google Scholar 

  30. Cheng, S. & Frank, L.M. New experiences enhance coordinated neural activity in the hippocampus. Neuron 57, 303–313 (2008).

    CAS  Article  Google Scholar 

  31. O'Neill, J., Senior, T. & Csicsvari, J. Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron 49, 143–155 (2006).

    CAS  Article  Google Scholar 

  32. Gelbard-Sagiv, H., Mukamel, R., Harel, M., Malach, R. & Fried, I. Internally generated reactivation of single neurons in human hippocampus during free recall. Science 322, 96–101 (2008).

    CAS  Article  Google Scholar 

  33. Pastalkova, E., Itskov, V., Amarasingham, A. & Buzsaki, G. Internally generated cell assembly sequences in the rat hippocampus. Science 321, 1322–1327 (2008).

    CAS  Article  Google Scholar 

  34. Buzsáki, G. & Draguhn, A. Neuronal oscillations in cortical networks. Science 304, 1926–1929 (2004).

    Article  Google Scholar 

  35. Mehta, M.R. Cortico-hippocampal interaction during up-down states and memory consolidation. Nat. Neurosci. 10, 13–15 (2007).

    CAS  Article  Google Scholar 

  36. Frank, L.M., Brown, E.N. & Wilson, M.A. A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex. J. Neurophysiol. 86, 2029–2040 (2001).

    CAS  Article  Google Scholar 

  37. Fox, S.E. & Ranck, J.B.J. Electrophysiological characteristics of hippocampal complex–spike cells and theta cells. Exp. Brain Res. 41, 399–410 (1981).

    CAS  PubMed  Google Scholar 

  38. Battaglia, F.P., Sutherland, G.R. & McNaughton, B.L. Local sensory cues and place cell directionality: additional evidence of prospective coding in the hippocampus. J. Neurosci. 24, 4541–4550 (2004).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank M. Brainard, D. Feldman, S. Lisberger, M. Stryker and the members of the Frank laboratory for comments on the manuscript. We also thank T. Davidson for a helpful discussion and M. Carr for help with histology photographs. This work was supported by the John Merck Scholars Program, the McKnight Scholars Program and US National Institutes of Health grants MH077970 and MH080283.

Author information

Authors and Affiliations

Authors

Contributions

M.P.K. and L.M.F. designed the experimental procedure. M.P.K. carried out all of the data collection and the majority of the analyses. L.M.F. carried out the remaining analyses. M.P.K. and L.M.F. wrote the manuscript.

Corresponding author

Correspondence to Loren M Frank.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–15, Supplementary Table 1, Supplementary Results and Supplementary Clusters (PDF 4337 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Karlsson, M., Frank, L. Awake replay of remote experiences in the hippocampus. Nat Neurosci 12, 913–918 (2009). https://doi.org/10.1038/nn.2344

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2344

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing