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Learning-Induced Sequence Reactivation During Sharp-Wave Ripples: A Computational Study

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Abstract

During sleep, memories formed during the day are consolidated in a dialogue between cortex and hippocampus. The reactivation of specific neural activity patterns—replay—during sleep has been observed in both structures and is hypothesized to represent a neuronal substrate of consolidation. In the hippocampus, replay happens during sharp-wave ripple complexes (SWR), when short bouts of excitatory activity in area CA3 induce high-frequency oscillations in area CA1. In particular, recordings of hippocampal cells which spike at a specific location (“place cells”) show that recently learned trajectories are reactivated during CA1 ripples in the following sleep period. Despite the importance of sleep replay, its underlying neural mechanisms are still poorly understood.

We used a previously developed model of sharp-wave ripples activity, to study the effects of learning-induced synaptic changes on spontaneous sequence reactivation during CA3 sharp waves. In this study, we implemented a paradigm including three epochs: Pre-sleep, learning, and Post-sleep activity. We first tested the effects of learning on the hippocampal network activity through changes in a minimal number of synapses connecting selected pyramidal cells. We then introduced an explicit trajectory-learning task to the learning portion of the paradigm, to obtain behavior-induced synaptic changes. Our analysis revealed that recently learned trajectories were reactivated during sleep more often than other trajectories in the training field. This study predicts that the gain of reactivation rate during sleep following vs sleep preceding learning for a trained sequence of pyramidal cells depends on Pre-sleep activation of the same sequence, and on the amount of trajectory repetitions included in the training phase.

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References

  1. S. Mednick, K. Nakayama, R. Stickgold, Sleep-dependent learning: a nap is as good as a night. Nat. Neurosci. 6(7), 697–698 (2003)

    Article  Google Scholar 

  2. S.C. Mednick, D.J. Cai, T. Shuman, S. Anagnostaras, J.T. Wixted, An opportunistic theory of cellular and systems consolidation. Trends Neurosci. 34(10), 504–514 (2011)

    Article  Google Scholar 

  3. S.C. Mednick, T. Makovski, D.J. Cai, Y.V. Jiang, Sleep and rest facilitate implicit memory in a visual search task. Vis. Res 49, 2557 (2009)

    Article  Google Scholar 

  4. B. Rasch, J. Born, About sleep’s role in memory. Physiol. Rev. 93(2), 681–766 (2013)

    Article  Google Scholar 

  5. I. Wilhelm, S. Diekelmann, I. Molzow, A. Ayoub, M. Mölle, J. Born, Sleep selectively enhances memory expected to be of future relevance. J. Neurosci. 31(5), 1563–1569 (2011)

    Article  Google Scholar 

  6. L. Marshall, H. Helgadottir, M. Molle, J. Born, Boosting slow oscillations during sleep potentiates memory. Nature 444(7119), 610–613 (2006)

    Article  Google Scholar 

  7. E.A. McDevitt, K.A. Duggan, S.C. Mednick, REM sleep rescues learning from interference. Neurobiol. Learn. Mem. 122, 51 (2014)

    Article  Google Scholar 

  8. S.C. Mednick, E.A. McDevitt, J.K. Walsh, E. Wamsley, M. Paulus, J.C. Kanady, S.P. Drummond, The critical role of sleep spindles in hippocampal-dependent memory: a pharmacology study. J. Neurosci. 33(10), 4494–4504 (2013)

    Article  Google Scholar 

  9. C.V. Latchoumane, H.V. Ngo, J. Born, H.S. Shin, Thalamic spindles promote memory formation during sleep through triple phase-locking of cortical, thalamic, and hippocampal rhythms. Neuron 95, 424 (2017)

    Article  Google Scholar 

  10. B.P. Staresina, T.O. Bergmann, M. Bonnefond, R. van der Meij, O. Jensen, L. Deuker, C.E. Elger, N. Axmacher, J. Fell, Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep. Nat. Neurosci. 18(11), 1679–1686 (2015)

    Article  Google Scholar 

  11. G. Buzsaki, Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus 25(10), 1073–1188 (2015)

    Article  Google Scholar 

  12. G. Buzsaki, D.L. Buhl, K.D. Harris, J. Csicsvari, B. Czeh, A. Morozov, Hippocampal network patterns of activity in the mouse. Neuroscience 116(1), 201–211 (2003)

    Article  Google Scholar 

  13. C.D. Schwindel, B.L. McNaughton, Hippocampal-cortical interactions and the dynamics of memory trace reactivation. Prog. Brain Res. 193, 163–177 (2011)

    Article  Google Scholar 

  14. J. Csicsvari, H. Hirase, A. Czurko, A. Mamiya, G. Buzsaki, Fast network oscillations in the hippocampal CA1 region of the behaving rat. J. Neurosci. 19(16), Rc20 (1999)

    Article  Google Scholar 

  15. J. Csicsvari, H. Hirase, A. Czurko, A. Mamiya, G. Buzsaki, Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J. Neurosci. 19(1), 274–287 (1999)

    Article  Google Scholar 

  16. J. Csicsvari, H. Hirase, A. Mamiya, G. Buzsáki, Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28(2), 585–594 (2000)

    Article  Google Scholar 

  17. A. Ylinen, A. Bragin, Z. Nadasdy, G. Jando, I. Szabo, A. Sik, G. Buzsaki, Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 15(1 Pt 1), 30–46 (1995)

    Article  Google Scholar 

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

    Article  Google Scholar 

  19. J.M. O’Keefe, L. Nadel, The Hippocampus as a Cognitive Map (Clarendon Press/Oxford University Press, Oxford/New York, 1978)

    Google Scholar 

  20. J. O’Neill, T. Senior, J. Csicsvari, Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron 49(1), 143–155 (2006)

    Article  Google Scholar 

  21. W.E. Skaggs, B.L. McNaughton, Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271(5257), 1870–1873 (1996)

    Article  Google Scholar 

  22. G.R. Sutherland, B. McNaughton, Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr. Opin. Neurobiol. 10(2), 180–186 (2000)

    Article  Google Scholar 

  23. M.A. Wilson, B.L. McNaughton, Reactivation of hippocampal ensemble memories during sleep. Science 265(5172), 676–679 (1994)

    Article  Google Scholar 

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

    Article  Google Scholar 

  25. H.S. Kudrimoti, C.A. Barnes, B.L. McNaughton, Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J. Neurosci. 19(10), 4090–4101 (1999)

    Article  Google Scholar 

  26. Z. Nádasdy, H. Hirase, A. Czurkó, J. Csicsvari, G. Buzsáki, Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 19(21), 9497–9507 (1999)

    Article  Google Scholar 

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

    Google Scholar 

  28. G. Girardeau, K. Benchenane, S.I. Wiener, G. Buzsaki, M.B. Zugaro, Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 12(10), 1222–1223 (2009)

    Article  Google Scholar 

  29. A.D. Grosmark, G. Buzsaki, Diversity in neural firing dynamics supports both rigid and learned hippocampal sequences. Science 351(6280), 1440–1443 (2016)

    Article  Google Scholar 

  30. G. Bi, M. Poo, Synaptic modification by correlated activity: Hebb’s postulate revisited. Annu. Rev. Neurosci. 24, 139–166 (2001)

    Article  Google Scholar 

  31. M.S. Rioult-Pedotti, D. Friedman, J.P. Donoghue, Learning-induced LTP in neocortex. Science 290(5491), 533–536 (2000)

    Article  Google Scholar 

  32. J.H. Sadowski, M.W. Jones, J.R. Mellor, Sharp-wave ripples orchestrate the induction of synaptic plasticity during reactivation of place cell firing patterns in the hippocampus. Cell Rep. 14(8), 1916–1929 (2016)

    Article  Google Scholar 

  33. P. Malerba, A. Fodder, M. Jones, M. Bazhenov, Modeling of coordinated sequence replay in CA3 and CA1 during sharp wave-ripples, in Society for Neuroscience Annual Meeting San Diego, CA, 2016 Neuroscience Meeting Planner (2016)

    Google Scholar 

  34. P. Malerba, G.P. Krishnan, J.M. Fellous, M. Bazhenov, Hippocampal CA1 ripples as inhibitory transients. PLoS Comput. Biol. 12(4), e1004880 (2016)

    Article  Google Scholar 

  35. G.M. Shepherd, The Synaptic Organization of the Brain (Oxford University Press, Oxford, 2004)

    Book  Google Scholar 

  36. J. Deuchars, A.M. Thomson, CA1 pyramid-pyramid connections in rat hippocampus in vitro: dual intracellular recordings with biocytin filling. Neuroscience 74(4), 1009–1018 (1996)

    Google Scholar 

  37. P. Andersen, R. Morris, D. Amaral, T. Bliss, J. O'Keefe, The Hippocampus Book (Oxford University Press, New York, 2006)

    Book  Google Scholar 

  38. K. Mizuseki, S. Royer, K. Diba, G. Buzsáki, Activity dynamics and behavioral correlates of CA3 and CA1 hippocampal pyramidal neurons. Hippocampus 22(8), 1659–1680 (2012)

    Article  Google Scholar 

  39. D. Sullivan, J. Csicsvari, K. Mizuseki, S. Montgomery, K. Diba, G. Buzsáki, Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity. J. Neurosci. 31(23), 8605–8616 (2011)

    Article  Google Scholar 

  40. P. Malerba, M. Bazhenov, Circuit mechanisms of hippocampal reactivation during sleep. Neurobiol. Learn. Mem. 2018. https://doi.org/10.1016/j.nlm.2018.04.018

  41. J. Patel, E.W. Schomburg, A. Berenyi, S. Fujisawa, G. Buzsaki, Local generation and propagation of ripples along the septotemporal axis of the hippocampus. J. Neurosci. 33(43), 17029–17041 (2013)

    Article  Google Scholar 

  42. N. Rebola, M. Carta, C. Mulle, Operation and plasticity of hippocampal CA3 circuits: implications for memory encoding. Nat. Rev. Neurosci. 18(4), 208–220 (2017)

    Article  Google Scholar 

  43. L.F. Cobar, L. Yuan, A. Tashiro, Place cells and long-term potentiation in the hippocampus. Neurobiol. Learn. Mem. 138, 206–214 (2017)

    Article  Google Scholar 

  44. R.A. Nicoll, A brief history of long-term potentiation. Neuron 93(2), 281–290 (2017)

    Article  Google Scholar 

  45. D. Manahan-Vaughan, Learning-related hippocampal long-term potentiation and long-term depression A2, in Learning and Memory: A Comprehensive Reference, 2nd edn., ed. By J.H. Byrne (Academic Press, Oxford, 2017), pp. 585–609

    Chapter  Google Scholar 

  46. C. Pinar, C.J. Fontaine, J. Trivino-Paredes, C.P. Lottenberg, J. Gil-Mohapel, B.R. Christie, Revisiting the flip side: long-term depression of synaptic efficacy in the hippocampus. Neurosci. Biobehav. Rev. 80, 394–413 (2017)

    Article  Google Scholar 

  47. K. Mizuseki, G. Buzsaki, Preconfigured, skewed distribution of firing rates in the hippocampus and entorhinal cortex. Cell Rep. 4(5), 1010–1021 (2013)

    Article  Google Scholar 

  48. Y. Omura, M.M. Carvalho, K. Inokuchi, T. Fukai, A lognormal recurrent network model for burst generation during hippocampal sharp waves. J. Neurosci. 35(43), 14585–14601 (2015)

    Article  Google Scholar 

  49. D.A. McCormick, Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog. Neurobiol. 39, 337–388 (1992)

    Article  Google Scholar 

  50. D.A. McCormick, H.C. Pape, A. Williamson, Actions of norepinephrine in the cerebral cortex and thalamus: implications for function of the central noradrenergic system. Prog. Brain Res. 88, 293–305 (1991)

    Article  Google Scholar 

  51. M. Vassalle, Contribution of the Na+/K+-pump to the membrane potential. Experientia 43(11-12), 1135–1140 (1987)

    Article  Google Scholar 

  52. F.F. Offner, Ion flow through membranes and the resting potential of cells. J. Membr. Biol. 123(2), 171–182 (1991)

    Article  Google Scholar 

  53. Y. Burak, I.R. Fiete, Accurate path integration in continuous attractor network models of grid cells. PLoS Comput. Biol. 5(2), e1000291 (2009)

    Article  MathSciNet  Google Scholar 

  54. L.M. Giocomo, M.B. Moser, E.I. Moser, Computational models of grid cells. Neuron 71(4), 589–603 (2011)

    Article  Google Scholar 

  55. E. Kropff, A. Treves, The emergence of grid cells: intelligent design or just adaptation? Hippocampus 18(12), 1256–1269 (2008)

    Article  Google Scholar 

  56. B. Jones, E. Bukoski, L. Nadel, J.M. Fellous, Remaking memories: reconsolidation updates positively motivated spatial memory in rats. Learn. Mem. 19(3), 91–98 (2012)

    Article  Google Scholar 

  57. B.J. Jones, S.M. Pest, I.M. Vargas, E.L. Glisky, J.M. Fellous, Contextual reminders fail to trigger memory reconsolidation in aged rats and aged humans. Neurobiol. Learn. Mem. 120, 7–15 (2015)

    Article  Google Scholar 

  58. L.A. Atherton, D. Dupret, J.R. Mellor, Memory trace replay: the shaping of memory consolidation by neuromodulation. Trends Neurosci. 38(9), 560–570 (2015)

    Article  Google Scholar 

  59. M.R. Mehta, From synaptic plasticity to spatial maps and sequence learning. Hippocampus 25(6), 756–762 (2015)

    Article  Google Scholar 

  60. V. Cutsuridis, M. Hasselmo, Spatial memory sequence encoding and replay during modeled theta and ripple oscillations. Cogn. Comput. 4(3), 554–574 (2011)

    Article  Google Scholar 

  61. M. Bazhenov, I. Timofeev, M. Steriade, T.J. Sejnowski, Model of thalamocortical slow-wave sleep oscillations and transitions to activated states. J. Neurosci. 22(19), 8691–8704 (2002)

    Article  Google Scholar 

  62. G.P. Krishnan, S. Chauvette, I.S. Shamie, S. Soltani, I. Timofeev, S.S. Cash, E. Halgren, M. Bazhenov, Cellular and neurochemical basis of sleep stages in thalamocortical network. Elife 5, e18607 (2016)

    Article  Google Scholar 

  63. Y. Wei, G. Krishnan, M. Bazhenov. Synaptic mechanisms of memory consolidation during NREM sleep. Society for Neuroscience. San Diego, CA. Program No. 82.01 (2016)

    Google Scholar 

  64. Y. Wei, G.P. Krishnan, M. Bazhenov, Synaptic mechanisms of memory consolidation during sleep slow oscillations. J. Neurosci. 36(15), 4231–4247 (2016)

    Article  Google Scholar 

  65. N. Kopell, C. Börgers, D. Pervouchine, P. Malerba, A. Tort, Gamma and theta rhythms in biophysical models of hippocampal circuits, in Hippocampal Microcircuits (Springer, New York, 2010), pp. 423–457

    Chapter  Google Scholar 

  66. P. Malerba, M. W. Jones, M. Bazhenov, Defining the synaptic mechanisms that tune CA3-CA1 reactivation during sharp-wave ripples. bioRxiv (2017). https://doi.org/10.1101/164699

  67. P. Malerba, N. F. Rulkov, M. Bazhenov, Large time step discrete-time modeling of sharp wave activity in hippocampal area CA3. bioRxiv (2018). https://doi.org/10.1101/303917

  68. T. Broicher, P. Malerba, A.D. Dorval, A. Borisyuk, F.R. Fernandez, J.A. White, Spike phase locking in CA1 pyramidal neurons depends on background conductance and firing rate. J. Neurosci. 32(41), 14374–14388 (2012)

    Article  Google Scholar 

  69. F.R. Fernandez, T. Broicher, A. Truong, J.A. White, Membrane voltage fluctuations reduce spike frequency adaptation and preserve output gain in CA1 pyramidal neurons in a high-conductance state. J. Neurosci. 31(10), 3880–3893 (2011)

    Article  Google Scholar 

  70. R. Brette, W. Gerstner, Adaptive exponential integrate-and-fire model as an effective description of neuronal activity. J. Neurophysiol. 94(5), 3637–3642 (2005)

    Article  Google Scholar 

  71. J. Touboul, R. Brette, Dynamics and bifurcations of the adaptive exponential integrate-and-fire model. Biol. Cybern. 99(4-5), 319–334 (2008)

    Article  MathSciNet  Google Scholar 

  72. G.E. Uhlenbeck, L.S. Ornstein, On the theory of the Brownian motion. Phys. Rev. 36(5), 823 (1930)

    Article  Google Scholar 

  73. A. Roxin, N. Brunel, D. Hansel, G. Mongillo, C. van Vreeswijk, On the distribution of firing rates in networks of cortical neurons. J. Neurosci. 31(45), 16217–16226 (2011)

    Article  Google Scholar 

  74. X.G. Li, P. Somogyi, A. Ylinen, G. Buzsáki, The hippocampal CA3 network: an in vivo intracellular labeling study. J. Comp. Neurol. 339(2), 181–208 (1994)

    Article  Google Scholar 

  75. J. Taxidis, S. Coombes, R. Mason, M.R. Owen, Modeling sharp wave-ripple complexes through a CA3-CA1 network model with chemical synapses. Hippocampus 22(5), 995–1017 (2012)

    Article  Google Scholar 

  76. B.V. Atallah, M. Scanziani, Instantaneous modulation of gamma oscillation frequency by balancing excitation with inhibition. Neuron 62(4), 566–577 (2009)

    Article  Google Scholar 

  77. M. Bartos, I. Vida, M. Frotscher, A. Meyer, H. Monyer, J.R. Geiger, P. Jonas, Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc. Natl. Acad. Sci. U. S. A. 99(20), 13222–13227 (2002)

    Article  Google Scholar 

  78. V. Cutsuridis, B. Graham, S. Cobb, I. Vida, Hippocampal Microcircuits: A Computational Modeler’s Resource Book (Springer, New York, 2010)

    Book  Google Scholar 

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Acknowledgments

This work was supported by MURI grant (MURI: N000141612829 and N000141612415) to MB.

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Authors and Affiliations

  1. Department of Medicine, University of California San Diego, San Diego, CA, USA

    Paola Malerba & Maxim Bazhenov

  2. University of California San Diego, San Diego, CA, USA

    Katya Tsimring

Authors
  1. Paola Malerba
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  2. Katya Tsimring
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  3. Maxim Bazhenov
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Corresponding author

Correspondence to Paola Malerba .

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Editors and Affiliations

  1. Center for Communications Res, San Diego, CA, USA

    Alyson Deines

  2. Department of Mathematics, Texas State University, San Marcos, TX, USA

    Daniela Ferrero

  3. Bryn Mawr College, Ardmore, PA, USA

    Erica Graham

  4. United States Military Academy, New York, NY, USA

    Mee Seong Im

  5. Los Alamos National Laboratory, Los Alamos, NM, USA

    Carrie Manore

  6. Department of Mathematics, University of San Diego, San Diego, CA, USA

    Candice Price

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Malerba, P., Tsimring, K., Bazhenov, M. (2018). Learning-Induced Sequence Reactivation During Sharp-Wave Ripples: A Computational Study. In: Deines, A., Ferrero, D., Graham, E., Im, M., Manore, C., Price, C. (eds) Advances in the Mathematical Sciences. AWMRS 2017. Association for Women in Mathematics Series, vol 15. Springer, Cham. https://doi.org/10.1007/978-3-319-98684-5_11

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