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Coordinated memory replay in the visual cortex and hippocampus during sleep

Nature Neuroscience volume 10, pages 100–107 (2007)Cite this article

Abstract

Sleep replay of awake experience in the cortex and hippocampus has been proposed to be involved in memory consolidation. However, whether temporally structured replay occurs in the cortex and whether the replay events in the two areas are related are unknown. Here we studied multicell spiking patterns in both the visual cortex and hippocampus during slow-wave sleep in rats. We found that spiking patterns not only in the cortex but also in the hippocampus were organized into frames, defined as periods of stepwise increase in neuronal population activity. The multicell firing sequences evoked by awake experience were replayed during these frames in both regions. Furthermore, replay events in the sensory cortex and hippocampus were coordinated to reflect the same experience. These results imply simultaneous reactivation of coherent memory traces in the cortex and hippocampus during sleep that may contribute to or reflect the result of the memory consolidation process.

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Figure 1: Experimental design.
Figure 2: Visual cortical and hippocampal spiking activities were organized as frames during SWS.
Figure 3: Visual cortical cells displayed localized firing fields.
Figure 4: Sleep frames replayed multicell firing sequences during RUN in both the visual cortex and the hippocampus.
Figure 5: Frame replays occurred significantly more often than chance in POST in both the visual cortex and hippocampus.
Figure 6: Visual cortical and hippocampal frames that replayed the same trajectories tended to occur at the same time.
Figure 7: Cortical and hippocampal frames co-replayed the same running trajectory as revealed by interval analysis.

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References

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

    Article  CAS  Google Scholar 

  2. Fortin, N.J., Agster, K.L. & Eichenbaum, H.B. Critical role of the hippocampus in memory for sequence of events. Nat. Neurosci. 5, 458–462 (2002).

    Article  CAS  Google Scholar 

  3. Squire, L.R., Stark, C.E. & Clark, R.E. The medial temporal lobe. Annu. Rev. Neurosci. 27, 279–306 (2004).

    Article  CAS  Google Scholar 

  4. Hasselmo, M.E. & McClelland, J.L. Neural models of memory. Curr. Opin. Neurobiol. 9, 184–188 (1999).

    Article  CAS  Google Scholar 

  5. Alvarez, P. & Squire, L.R. Memory consolidation and the medial temporal lobe: a simple network model. Proc. Natl. Acad. Sci. USA 91, 7041–7045 (1994).

    Article  CAS  Google Scholar 

  6. Káli, S. & Dayan, P. Off-line replay maintains declarative memories in a model of hippocampal-neocortical interactions. Nat. Neurosci. 7, 286–294 (2004).

    Article  Google Scholar 

  7. Siapas, A.G. & Wilson, M.A. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21, 1123–1128 (1998).

    Article  CAS  Google Scholar 

  8. Sirota, A., Csicsvari, J., Buhl, D. & Buzsáki, G. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. USA 100, 2065–2069 (2003).

    Article  CAS  Google Scholar 

  9. Battaglia, F.P., Sutherland, G.R. & McNaughton, B.L. Hippocampal sharp wave bursts coincide with neocortical up-state transitions. Learn. Mem. 11, 697–704 (2004).

    Article  Google Scholar 

  10. Mölle, M., Yeshenko, O., Marshall, L., Sara, S.J. & Born, J. Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J. Neurophysiol. 96, 62–70 (2006).

    Article  Google Scholar 

  11. Wolansky, T., Clement, E.A., Peters, S.R., Palczak, M.A. & Dickson, C.T. Hippocampal slow oscillation: a novel EEG state and its coordination with ongoing neocortical activity. J. Neurosci. 26, 6213–6229 (2006).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  13. Skaggs, W.E. & McNaughton, B.L. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271, 1870–1873 (1996).

    Article  CAS  Google Scholar 

  14. 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).

    Article  CAS  Google Scholar 

  15. Hoffman, K.L. & McNaughton, B.L. Coordinated reactivation of distributed memory traces in primate neocortex. Science 297, 2070–2073 (2002).

    Article  CAS  Google Scholar 

  16. Qin, Y.L., McNaughton, B.L., Skaggs, W.E. & Barnes, C.A. Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles. Phil. Trans. R. Soc. Lond. B 352, 1525–1533 (1997).

    Article  CAS  Google Scholar 

  17. Ribeiro, S. et al. Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas. PLoS Biol. 2, 24 (2004).

    Article  Google Scholar 

  18. Eichenbaum, H., Dudchunko, P., Wood, E., Shapiro, M. & Tanila, H. The hippocampus, memory, and place cells: is it spatial memory or a memory space? Neuron 23, 209–226 (1999).

    Article  CAS  Google Scholar 

  19. Jensen, O. & Lisman, J.E. Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer. Trends Neurosci. 28, 67–72 (2005).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  22. Louie, K. & Wilson, M.A. Temporally structural replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29, 145–156 (2001).

    Article  CAS  Google Scholar 

  23. Cossart, R., Aronov, D. & Yuste, R. Attractor dynamics of network up states in the neocortex. Nature 423, 283–288 (2003).

    Article  CAS  Google Scholar 

  24. Shu, Y., Hasenstaub, A. & McCormick, D.A. Turning on and off recurrent balanced cortical activity. Nature 423, 288–293 (2003).

    Article  CAS  Google Scholar 

  25. Sanchez-Vives, M.V. & McCormick, D.A. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 3, 1027–1034 (2000).

    Article  CAS  Google Scholar 

  26. Petersen, C.C., Hahn, T.T.G., Metha, M., Grinvald, A. & Sakmann, B. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc. Natl. Acad. Sci. USA 100, 13638–13643 (2003).

    Article  CAS  Google Scholar 

  27. Volgushev, M., Chauvette, S., Mukovski, M. & Timofeev, I. Precise long-range synchronization of activity and silence in neocortical neurons during slow-wave sleep. J. Neurosci. 26, 5665–5672 (2006).

    Article  CAS  Google Scholar 

  28. Amzica, F. & Steriade, M. Cellular substrates and laminar profile of sleep K-complex. Neuroscience 82, 671–686 (1998).

    Article  CAS  Google Scholar 

  29. Steriade, M., Timofeev, I. & Grenier, F. Natural waking and sleep states: a view from inside neocortical neurons. J. Neurophysiol. 85, 1969–1985 (2001).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  31. O'Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map: preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171–175 (1971).

    Article  CAS  Google Scholar 

  32. Hafting, T., Fyhn, M., Molden, S., Moser, M.B. & Moser, E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801–806 (2005).

    Article  CAS  Google Scholar 

  33. Hargreaves, E.L., Rao, G., Lee, I. & Knierim, J.J. Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308, 1792–1794 (2005).

    Article  CAS  Google Scholar 

  34. Lee, A.K. & Wilson, M.A. A combinatorial method for analyzing sequential firing patterns involving an arbitrary number of neurons based on relative time order. J. Neurophysiol. 92, 2555–2573 (2004).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  36. Steriade, M. & Amzica, F. Slow sleep oscillation, rhythmic K-complexes, and their paroxysmal developments. J. Sleep Res. 7 (suppl. 1): 30–35 (1998).

    Article  Google Scholar 

  37. Achermann, P. & Borbely, A.A. Low-frequency (<1 Hz) oscillations in the human sleep EEG. Neuroscience 81, 213–222 (1997).

    Article  CAS  Google Scholar 

  38. Hahn, T.T.G., Sakmann, B. & Mehta, M.R. Phase-locking of hippocampal interneurons' membrane potential to neocortical up-down states. Nat. Neurosci. 9, 1359–1361 (2006).

    Article  CAS  Google Scholar 

  39. Kosslyn, S.M. et al. The role of area 17 in visual imagery: convergent evidence from PET and rTMS. Science 284, 167–170 (1999).

    Article  CAS  Google Scholar 

  40. Wheeler, M.E., Petersen, S.E. & Buckner, R.L. Memory's echo: vivid remembering reactivates sensory-specific cortex. Proc. Natl. Acad. Sci. USA 97, 11125–11129 (2000).

    Article  CAS  Google Scholar 

  41. Harris, J.A., Petersen, R.S. & Diamond, M.E. The cortical distribution of sensory memories. Neuron 30, 315–318 (2001).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  43. McClelland, J.L. & Goddard, N.H. Considerations arising from a complementary learning systems perspective on hippocampus and neocortex. Hippocampus 6, 654–665 (1996).

    Article  CAS  Google Scholar 

  44. O'Reilly, R.C. & Rudy, J.W. Computational principals of learning in the neocortex and hippocampus. Hippocampus 10, 389–397 (2000).

    Article  CAS  Google Scholar 

  45. Lavenex, P. & Amaral, D.G. Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 10, 420–430 (2000).

    Article  CAS  Google Scholar 

  46. Rolls, E.T. Hippocampal-cortical and cortico-cortical backprojections. Hippocampus 10, 380–388 (2000).

    Article  CAS  Google Scholar 

  47. Paxinos, G. & Watson, C. The Rat Brain in Stereotaxic Coordinates 4th edn. (Academic, New York, 1998).

    Google Scholar 

  48. Robert, C., Guilpin, C. & Limoge, A. Automated sleep staging systems in rats. J. Neurosci. Methods 88, 111–122 (1999).

    Article  CAS  Google Scholar 

  49. Siapas, A.G., Lubenov, E.V. & Wilson, M.A. Prefrontal phase locking to hippocampal theta oscillations. Neuron 46, 141–145 (2005).

    Article  CAS  Google Scholar 

  50. Skaggs, W.E., McNaughton, B.L., Gothard, K.M. & Markus, E.J. An information-theoretic approach to deciphering the hippocampal code. In Advances in Neural Information Processing Systems Vol. 5 (eds. Hanson, S.J., Cowan, J.D. & Giles, C.J.) 1030–1037 (Morgan Kaufmann, San Mateo, California, USA, 1993).

    Google Scholar 

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Acknowledgements

We thank E. Miller, C. Moore, J. Fisher and F.-M. Zhou for critical readings on the manuscript, and Wilson laboratory members for technical help and suggestions and comments on the project and manuscript. Supported by grants to M.A.W. from the Brain Science Institute at the Institute of Physical and Chemical Research (RIKEN) in Japan and the US National Institutes of Health.

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Authors and Affiliations

  1. Department of Brain and Cognitive Sciences and Department of Biology, The Picower Institute for Learning and Memory, RIKEN-MIT Neuroscience Research Center, Massachusetts Institute of Technology, Building 46, Room 5233, 43 Vassar Street, Cambridge, 02139, Massachusetts, USA

    Daoyun Ji & Matthew A Wilson

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  1. Daoyun Ji
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Correspondence to Daoyun Ji or Matthew A Wilson.

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Supplementary information

Supplementary Fig. 1

Hippocampal frames were related to hippocampal EEG ripples. (PDF 212 kb)

Supplementary Fig. 2

Temporal relationship between cortical and hippocampal frames was not significantly different between PRE and POST, and was not sensitive to frame definition parameters. (PDF 85 kb)

Supplementary Fig. 3

Cell pairs between the visual cortex and hippocampus that had high correlation during RUN also had high correlation in POST, but not in PRE. (PDF 28 kb)

Supplementary Fig. 4

High but not low correlation during RUN boosted correlation in POST between the visual cortex and hippocampus, and within the hippocampus. (PDF 78 kb)

Supplementary Fig. 5

Firing patterns in the visual cortex and hippocampus during RUN were replayed in sleep frames during POST. (PDF 36 kb)

Supplementary Fig. 6

Frame replays were compressed during sleep. (PDF 85 kb)

Supplementary Fig. 7

Difference in frame properties did not significantly contribute to increase in replaying ratio from PRE to POST. (PDF 87 kb)

Supplementary Fig. 8

There were no significant differences in distribution of frame duration, within-frame multiunit firing rate per tetrode, and within frame active cell firing rate between replaying and non-replaying candidate frames in either the visual cortex or the hippocampus. (PDF 22 kb)

Supplementary Fig. 9

Shuffling procedure to determine significance (p value) of the overlapping replaying frame pairs. (PDF 65 kb)

Supplementary Fig. 10

Temporal relationship between cortical and hippocampal sequence replays. (PDF 69 kb)

Supplementary Fig. 11

Sleep stage classification. (PDF 38 kb)

Supplementary Fig. 12

Frame boundary determination. (PDF 69 kb)

Supplementary Table 1

Minimum matching indices (I) required for significant frame sequences, given the number of cells in a frame. (PDF 26 kb)

Supplementary Table 2

Comparison in replaying frame ratio between PRE and POST in the visual cortex for each of the 12 trajectories. (PDF 19 kb)

Supplementary Table 3

Comparison in replaying frame ratio between PRE and POST in the hippocampus for each of the 15 trajectories. (PDF 19 kb)

Supplementary Methods (PDF 53 kb)

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Ji, D., Wilson, M. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10, 100–107 (2007). https://doi.org/10.1038/nn1825

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