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Nature Neuroscience
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Replay of rule-learning related neural patterns in the prefrontal cortex during sleep

Nature Neurosciencevolume 12, pages919–926 (2009)Cite this article

Abstract

Slow-wave sleep (SWS) is important for memory consolidation. During sleep, neural patterns reflecting previously acquired information are replayed. One possible reason for this is that such replay exchanges information between hippocampus and neocortex, supporting consolidation. We recorded neuron ensembles in the rat medial prefrontal cortex (mPFC) to study memory trace reactivation during SWS following learning and execution of cross-modal strategy shifts. In general, reactivation of learning-related patterns occurred in distinct, highly synchronized transient bouts, mostly simultaneous with hippocampal sharp wave/ripple complexes (SPWRs), when hippocampal ensemble reactivation and cortico-hippocampal interaction is enhanced. During sleep following learning of a new rule, mPFC neural patterns that appeared during response selection replayed prominently, coincident with hippocampal SPWRs. This was learning dependent, as the patterns appeared only after rule acquisition. Therefore, learning, or the resulting reliable reward, influenced which patterns were most strongly encoded and successively reactivated in the hippocampal/prefrontal network.

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Figure 1: Signal components and their behavioral correlates.
Figure 2: Time course of memory replay.
Figure 3: Memory replay, SPWRs and cell activity in a rest session.
Figure 4: Example of reactivation strength peaks coinciding with hippocampal SPWR.
Figure 5: Prefrontal memory replay is enhanced during hippocampal SPWRs.
Figure 6: Reactivation strength relative to mPFC LFP events.
Figure 7: Replayed activity during SPWRs is correlated to rule acquisition.

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References

  1. Malenka, R.C. & Nicoll, R.A. Long-term potentiation-a decade of progress?Science285, 1870–1874 (1999).

    Article CAS  Google Scholar 

  2. Marr, D. Simple memory: a theory for archicortex.Phil. Trans. R. Soc. Lond. B262, 23–81 (1971).

    Article CAS  Google Scholar 

  3. McClelland, J.L., McNaughton, B.L. & O'Reilly, R.C. 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 (1995).

    Article  Google Scholar 

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

    Article  Google Scholar 

  5. 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 

  6. Moscovitch, M., Nadel, L., Winocur, G., Gilboa, A. & Rosenbaum, R.S. The cognitive neuroscience of remote episodic, semantic and spatial memory.Curr. Opin. Neurobiol.16, 179–190 (2006).

    Article CAS  Google Scholar 

  7. Winocur, G., Moscovitch, M. & Sekeres, M. Memory consolidation or transformation: context manipulation and hippocampal representations of memory.Nat. Neurosci.10, 555–557 (2007).

    Article CAS  Google Scholar 

  8. Tse, D. et al. Schemas and memory consolidation.Science316, 76–82 (2007).

    Article CAS  Google Scholar 

  9. Marshall, L., Helgadóttir, H., Mölle, M. & Born, J. Boosting slow oscillations during sleep potentiates memory.Nature444, 610–613 (2006).

    Article CAS  Google Scholar 

  10. Walker, M.P. & Stickgold, R. Sleep, memory, and plasticity.Annu. Rev. Psychol.57, 139–166 (2006).

    Article  Google Scholar 

  11. Wagner, U., Gais, S., Haider, H., Verleger, R. & Born, J. Sleep inspires insight.Nature427, 352–355 (2004).

    Article CAS  Google Scholar 

  12. Wilson, M.A. & McNaughton, B.L. Reactivation of hippocampal ensemble memories during sleep.Science265, 676–679 (1994).

    Article CAS  Google Scholar 

  13. Nádasdy, Z., Hirase, H., Czurko, 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 

  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.Science297, 2070–2073 (2002).

    Article CAS  Google Scholar 

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

    Article CAS  Google Scholar 

  17. Euston, D.R., Tatsuno, M. & McNaughton, B.L. Fast-forward playback of recent memory sequences in prefrontal cortex during sleep.Science318, 1147–1150 (2007).

    Article CAS  Google Scholar 

  18. 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).

    Article CAS  Google Scholar 

  19. Siapas, A.G. & Wilson, M.A. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep.Neuron21, 1123–1128 (1998).

    Article CAS  Google Scholar 

  20. Sirota, A., Csicsvari, J., Buhl, D. & Buzsáki, G. Communication between neocortex and hippocampus during sleep in rodents.Proc. Natl. Acad. Sci. USA100, 2065–2069 (2003).

    Article CAS  Google Scholar 

  21. 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 

  22. Isomura, Y. et al. Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations.Neuron52, 871–882 (2006).

    Article CAS  Google Scholar 

  23. Hahn, T.T., 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 

  24. Buzsáki, G. Two-stage model of memory trace formation: a role for 'noisy' brain states.Neuroscience31, 551–570 (1989).

    Article  Google Scholar 

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

    Article  Google Scholar 

  26. Steriade, M., Nuñez, 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 

  27. Frankland, P.W. & Bontempi, B. The organization of recent and remote memories.Nat. Rev. Neurosci.6, 119–130 (2005).

    Article CAS  Google Scholar 

  28. Gais, S. et al. Sleep transforms the cerebral trace of declarative memories.Proc. Natl. Acad. Sci. USA104, 18778–18783 (2007).

    Article CAS  Google Scholar 

  29. Jay, T.M. & Witter, M.P. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport ofPhaseolus vulgaris leucoagglutinin.J. Comp. Neurol.313, 574–586 (1991).

    Article CAS  Google Scholar 

  30. Jay, T.M., Burette, F. & Laroche, S. NMDA receptor–dependent long-term potentiation in the hippocampal afferent fibre system to the prefrontal cortex in the rat.Eur. J. Neurosci.7, 247–250 (1995).

    Article CAS  Google Scholar 

  31. Takashima, A. et al. Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study.Proc. Natl. Acad. Sci. USA103, 756–761 (2006).

    Article CAS  Google Scholar 

  32. Floresco, S.B., Braaksma, D.N. & Phillips, A.G. Thalamic-cortical-striatal circuitry subserves working memory during delayed responding on a radial arm maze.J. Neurosci.19, 11061–11071 (1999).

    Article CAS  Google Scholar 

  33. Jones, M.W. & Wilson, M.A. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task.PLoS Biol.3, e402 (2005).

    Article  Google Scholar 

  34. Pasupathy, A. & Miller, E.K. Different time courses of learning-related activity in the prefrontal cortex and striatum.Nature433, 873–876 (2005).

    Article CAS  Google Scholar 

  35. Baeg, E.H. et al. Learning-induced enduring changes in functional connectivity among prefrontal cortical neurons.J. Neurosci.27, 909–918 (2007).

    Article CAS  Google Scholar 

  36. Birrell, J.M. & Brown, V.J. Medial frontal cortex mediates perceptual attentional set shifting in the rat.J. Neurosci.20, 4320–4324 (2000).

    Article CAS  Google Scholar 

  37. Beggs, J.M. & Plenz, D. Neuronal avalanches are diverse and precise activity patterns that are stable for many hours in cortical slice cultures.J. Neurosci.24, 5216–5229 (2004).

    Article CAS  Google Scholar 

  38. Mongillo, G., Barak, O. & Tsodyks, M. Synaptic theory of working memory.Science319, 1543–1546 (2008).

    Article CAS  Google Scholar 

  39. Dégenètais, E., Thierry, A.M., Glowinski, J. & Gioanni, Y. Synaptic influence of hippocampus on pyramidal cells of the rat prefrontal cortex: anin vivo intracellular recording study.Cereb. Cortex13, 782–792 (2003).

    Article  Google Scholar 

  40. Amzica, F. & Steriade, M. Electrophysiological correlates of sleep delta waves.Electroencephalogr. Clin. Neurophysiol.107, 69–83 (1998).

    Article CAS  Google Scholar 

  41. Steriade, M. Neuronal substrates of spike-wave seizures and hypsarrhythmia in corticothalamic systems.Adv. Neurol.97, 149–154 (2006).

    PubMed  Google Scholar 

  42. Baeg, E.H. et al. Dynamics of population code for working memory in the prefrontal cortex.Neuron40, 177–188 (2003).

    Article CAS  Google Scholar 

  43. Seamans, J.K., Floresco, S.B. & Phillips, A.G. D1 receptor modulation of hippocampal-prefrontal cortical circuits integrating spatial memory with executive functions in the rat.J. Neurosci.18, 1613–1621 (1998).

    Article CAS  Google Scholar 

  44. Lee, I. & Kesner, R.P. Differential contribution of NMDA receptors in hippocampal subregions to spatial working memory.Nat. Neurosci.5, 162–168 (2002).

    Article CAS  Google Scholar 

  45. Steriade, M. Grouping of brain rhythms in corticothalamic systems.Neuroscience137, 1087–1106 (2006).

    Article CAS  Google Scholar 

  46. Harris, K.D., Henze, D.A., Csicsvari, J., Hirase, H. & Buzsáki, G. Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements.J. Neurophysiol.84, 401–414 (2000).

    Article CAS  Google Scholar 

  47. Hazan, L., Zugaro, M. & Buzsáki, G. Klusters, NeuroScope, NDManager: a free software suite for neurophysiological data processing and visualization.J. Neurosci. Methods155, 207–216 (2006).

    Article  Google Scholar 

  48. Marčenko, V.A. & Pastur, L.A. Distribution of eigenvalues for some sets of random matrices.Math USSR SB1, 457–483 (1967).

    Article  Google Scholar 

  49. Sengupta, A.M. & Mitra, P.P. Distributions of singular values for some random matrices.Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics60, 3389–3392 (1999).

    CAS PubMed  Google Scholar 

  50. Fitzpatrick, S. & Scott, A. Quick simultaneous confidence intervals for multinomial proportions.J. Am. Stat. Assoc.82, 875–878 (1987).

    Article  Google Scholar 

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Acknowledgements

We thank P. Tierney for valuable discussions and help with the surgical procedures, J.-M. Deniau, Y. Gioanni, A.-M. Thierry, M.B. Zugaro, M. Cencini and A. Aubry for interesting discussions, S. Doutremer for histology, D. Hopkins and N. Quenech'du for the anatomical reconstructions, V. Douchamps for help with the experiments, K. Gothard, K. Hoffman and A. Treves for critical readings of an earlier version of the manuscript, and A Berthoz for support throughout the project. This work was supported by Fondation Fyssen (F.P.B.), Fondation pour la Recherche Medicale (A.P.), and European Community contracts FP6-IST 027819 (Integrating Cognition, Emotion and Autonomy), FP6-IST-027140 (Bayesian Approach to Cognitive Systems) and FP6-IST-027017 (NeuroProbes).

Author information

Authors and Affiliations

  1. Laboratoire de Physiologie de la Perception et de l'Action, Collège de France, Centre National de la Recherche Scientifique, Paris, France

    Adrien Peyrache, Mehdi Khamassi, Karim Benchenane, Sidney I Wiener & Francesco P Battaglia

  2. Institut des Systèmes Intelligents et de Robotique, Université Pierre et Marie Curie – Paris 6, Centre National de la Recherche Scientifique, Paris, France

    Mehdi Khamassi

  3. Center for Neuroscience, Swammerdam Institute for Life Sciences, Faculty of Science, Universiteit van Amsterdam, Amsterdam, The Netherlands

    Francesco P Battaglia

Authors
  1. Adrien Peyrache

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  2. Mehdi Khamassi

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  4. Sidney I Wiener

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Contributions

S.I.W., F.P.B. and M.K. designed the experiment, F.P.B., M.K. and A.P. performed the experiments, A.P., F.P.B. and K.B. designed the analysis techniques, A.P. analyzed the data, and F.P.B., A.P. and S.I.W. wrote the paper.

Corresponding author

Correspondence toSidney I Wiener.

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Supplementary Figures 1–13, Supplementary Table 1 and Supplementary Discussion (PDF 9430 kb)

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Peyrache, A., Khamassi, M., Benchenane, K.et al. Replay of rule-learning related neural patterns in the prefrontal cortex during sleep.Nat Neurosci12, 919–926 (2009). https://doi.org/10.1038/nn.2337

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