Hippocampal place cells take part in sequenced patterns of reactivation after behavioral experience, known as replay. Since replay was first reported, nearly 20 years ago, many new results have been found, necessitating revision of the original interpretations. We review some of these results with a focus on the phenomenology of replay.

Keyword(s): hippocampusmemoryplace cellreplay

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Literature Cited

  1. Altimus C, Harrold J, Jaaro-Peled H, Sawa A, Foster DJ. 2015. Disordered ripples are a common feature of genetically distinct mouse models relevant to schizophrenia. Mol. Neuropsychiatry 1:52–59 [Google Scholar]
  2. Ambrose RE, Pfeiffer BE, Foster DJ. 2016. Reverse replay of hippocampal place cells is uniquely modulated by changing reward. Neuron 91:1124–36 [Google Scholar]
  3. Andersen P, Morris R, Amaral D, Bliss T, O'Keefe J. 2007. The Hippocampus Book Oxford, UK: Oxford Univ. Press
  4. Ben-Yishai R, Hansel D, Sompolinsky H. 1997. Traveling waves and the processing of weakly tuned inputs in a cortical network module. J. Comput. Neurosci. 4:57–77 [Google Scholar]
  5. Bi GQ, Poo MM. 1998. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18:10464–72 [Google Scholar]
  6. Buckner RL, Andrews-Hanna JR, Schacter DL. 2008. The brain's default network: anatomy, function, and relevance to disease. Ann. N. Y. Acad. Sci. 1124:1–38 [Google Scholar]
  7. Buzsaki G. 1989. Two-stage model of memory trace formation: a role for “noisy” brain states. Neuroscience 31:551–70 [Google Scholar]
  8. Buzsaki G. 2015. Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus 25:1073–188 [Google Scholar]
  9. Carr MF, Jadhav SP, Frank LM. 2011. Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat. Neurosci. 14:147–53 [Google Scholar]
  10. Carr MF, Karlsson MP, Frank LM. 2012. Transient slow gamma synchrony underlies hippocampal memory replay. Neuron 75:700–13 [Google Scholar]
  11. Csicsvari J, O'Neill J, Allen K, Senior T. 2007. Place-selective firing contributes to the reverse-order reactivation of CA1 pyramidal cells during sharp waves in open-field exploration. Eur. J. Neurosci. 26:704–16 [Google Scholar]
  12. Davidson TJ, Kloosterman F, Wilson MA. 2009. Hippocampal replay of extended experience. Neuron 63:497–507 [Google Scholar]
  13. Diba K, Buzsaki G. 2007. Forward and reverse hippocampal place-cell sequences during ripples. Nat. Neurosci. 10:1241–42 [Google Scholar]
  14. Dolan RJ, Dayan P. 2013. Goals and habits in the brain. Neuron 80:312–25 [Google Scholar]
  15. Dragoi G, Tonegawa S. 2011. Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469:397–401 [Google Scholar]
  16. Dragoi G, Tonegawa S. 2013a. Development of schemas revealed by prior experience and NMDA receptor knock-out. eLife 2:e01326 [Google Scholar]
  17. Dragoi G, Tonegawa S. 2013b. Distinct preplay of multiple novel spatial experiences in the rat. PNAS 110:9100–5 [Google Scholar]
  18. Dupret D, O'Neill J, Pleydell-Bouverie B, Csicsvari J. 2010. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat. Neurosci. 13:995–1002 [Google Scholar]
  19. Epsztein J, Brecht M, Lee AK. 2011. Intracellular determinants of hippocampal CA1 place and silent cell activity in a novel environment. Neuron 70:109–20 [Google Scholar]
  20. Feng T, Silva D, Foster DJ. 2015. Mechanisms contributing to experience-dependent changes in the structure of hippocampal replay sequences Presented at Soc. Neurosci., Oct. 17–21 Chicago:
  21. Foster DJ, Knierim JJ. 2012. Sequence learning and the role of the hippocampus in rodent navigation. Curr. Opin. Neurobiol. 22:294–300 [Google Scholar]
  22. Foster DJ, Morris RGM, Dayan P. 2000. A model of hippocampally dependent navigation, using the temporal difference learning rule. Hippocampus 10:1–16 [Google Scholar]
  23. Foster DJ, Wilson MA. 2006. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440:680–83 [Google Scholar]
  24. Frank LM, Brown EN, Wilson M. 2000. Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27:169–78 [Google Scholar]
  25. Georgopoulos AP, Lurito JT, Petrides M, Schwartz AB, Massey JT. 1989. Mental rotation of the neuronal population vector. Science 243:234–36 [Google Scholar]
  26. Gerrard JL, Burke SN, McNaughton BL, Barnes CA. 2008. Sequence reactivation in the hippocampus is impaired in aged rats. J. Neurosci. 28:7883–90 [Google Scholar]
  27. Gerrard JL, Kudrimoti H, McNaughton BL, Barnes CA. 2001. Reactivation of hippocampal ensemble activity patterns in the aging rat. Behav. Neurosci. 115:1180–92 [Google Scholar]
  28. Gomperts SN, Kloosterman F, Wilson MA. 2015. VTA neurons coordinate with the hippocampal reactivation of spatial experience. eLife 4:e05360 [Google Scholar]
  29. Grosmark AD, Buzsaki G. 2016. Diversity in neural firing dynamics supports both rigid and learned hippocampal sequences. Science 351:1440–43 [Google Scholar]
  30. Gupta AS, van der Meer MAA, Touretzky DS, Redish AD. 2010. Hippocampal replay is not a simple function of experience. Neuron 65:695–705 [Google Scholar]
  31. Guzowski JF, McNaughton BL, Barnes CA, Worley PF. 1999. Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat. Neurosci. 2:1120–24 [Google Scholar]
  32. Harvey CD, Collman F, Dombeck DA, Tank DW. 2009. Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461:941–46 [Google Scholar]
  33. Hopfield JJ. 1982. Neural networks and physical systems with emergent collective computational abilities. PNAS 79:2554–58 [Google Scholar]
  34. Jadhav SP, Kemere C, German PW, Frank LM. 2012. Awake hippocampal sharp-wave ripples support spatial memory. Science 336:1454–58 [Google Scholar]
  35. Jadhav SP, Rothschild G, Roumis DK, Frank LM. 2016. Coordinated excitation and inhibition of prefrontal ensembles during awake hippocampal sharp-wave ripple events. Neuron 90:113–27 [Google Scholar]
  36. Johnson A, Fenton AA, Kentros C, Redish AD. 2009. Looking for cognition in the structure within the noise. Trends Cogn. Sci. 13:55–64 [Google Scholar]
  37. Johnson A, Redish AD. 2007. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 27:12176–89 [Google Scholar]
  38. Karlsson MP, Frank LM. 2009. Awake replay of remote experiences in the hippocampus. Nat. Neurosci. 12:913–18 [Google Scholar]
  39. Kennerley SW, Behrens TE, Wallis JD. 2011. Double dissociation of value computations in orbitofrontal and anterior cingulate neurons. Nat. Neurosci. 14:1581–89 [Google Scholar]
  40. Kentros C, Hargreaves E, Hawkins RD, Kandel ER, Shapiro M, Muller RV. 1998. Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science 280:2121–26 [Google Scholar]
  41. Klausberger T, Somogyi P. 2008. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321:53–57 [Google Scholar]
  42. Kleinfeld D. 1986. Sequential state generation by model neural networks. PNAS 83:9469–73 [Google Scholar]
  43. Kudrimoti HS, Barnes CA, McNaughton BL. 1999. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J. Neurosci. 19:4090–101 [Google Scholar]
  44. Lansink CS, Goltstein PM, Lankelma JV, McNaughton BL, Pennartz CM. 2009. Hippocampus leads ventral striatum in replay of place-reward information. PLOS Biol 7:e1000173 [Google Scholar]
  45. Lee AK, Wilson MA. 2002. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36:1183–94 [Google Scholar]
  46. Lisman JE. 1999. Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 22:233–42 [Google Scholar]
  47. Lisman JE, Talamini LM, Raffone A. 2005. Recall of memory sequences by interaction of the dentate and CA3: a revised model of the phase precession. Neural Netw 18:1191–201 [Google Scholar]
  48. Louie K, Wilson MA. 2001. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29:145–56 [Google Scholar]
  49. Maier NRF. 1929. Reasoning in white rats. Comp. Psychol. Monogr. 6:1–93 [Google Scholar]
  50. Maier NRF, Schneirla TC. 1935. Principles of Animal Psychology New York: McGraw-Hill
  51. McClelland JL, McNaughton BL, O'Reilly RC. 1995. 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. 102:419–57 [Google Scholar]
  52. McHugh TJ, Blum KI, Tsien JZ, Tonegawa S, Wilson MA. 1996. Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice. Cell 87:1339–49 [Google Scholar]
  53. McNamara CG, Tejero-Cantero A, Trouche S, Campo-Urriza N, Dupret D. 2014. Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence. Nat. Neurosci. 17:1658–60 [Google Scholar]
  54. Mehta MR, Lee AK, Wilson MA. 2002. Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417:741–46 [Google Scholar]
  55. Morris RGM. 2013. NMDA receptors and memory encoding. Neuropharmacology 74:32–40 [Google Scholar]
  56. Morris RGM, Anderson E, Lynch GS, Baudry M. 1986. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319:774–76 [Google Scholar]
  57. Moser EI, Kropff E, Moser MB. 2008. Place cells, grid cells, and the brain's spatial representation system. Annu. Rev. Neurosci. 31:69–89 [Google Scholar]
  58. Nadasdy Z, Hirase H, Czurko A, Csicsvari J, Buzsaki G. 1999. Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 19:9497–507 [Google Scholar]
  59. O'Keefe J, Dostrovsky J. 1971. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171–75 [Google Scholar]
  60. O'Keefe J, Nadel L. 1978. The Hippocampus as a Cognitive Map London: Clarendon
  61. O'Neill J, Pleydell-Bouverie B, Dupret D, Csicsvari J. 2010. Play it again: reactivation of waking experience and memory. Trends Neurosci 33:220–29 [Google Scholar]
  62. Parr R, Russell S. 1997. Reinforcement learning with hierarchies of machines. Adv. Neural Inf. Process. Syst. 10:1043–49 [Google Scholar]
  63. Pavlides C, Winson J. 1989. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J. Neurosci. 9:2907–18 [Google Scholar]
  64. Pennartz CM, Lee E, Verheul J, Lipa P, Barnes CA, McNaughton BL. 2004. The ventral striatum in off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples. J. Neurosci. 24:6446–56 [Google Scholar]
  65. Pfeiffer BE, Foster DJ. 2013a. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497:74–79 [Google Scholar]
  66. Pfeiffer BE, Foster DJ. 2013b. Place-cell sequences depict behaviorally relevant trajectories during sleep Presented at Soc. Neurosci., Nov. 9–13 San Diego:
  67. Pfeiffer BE, Foster DJ. 2015. Autoassociative dynamics in the generation of sequences of hippocampal place cells. Science 349:180–83 [Google Scholar]
  68. Redish AD. 2016. Vicarious trial and error. Nat. Rev. Neurosci. 17:147–59 [Google Scholar]
  69. Roesch MR, Singh T, Brown PL, Mullins SE, Schoenbaum G. 2009. Ventral striatal neurons encode the value of the chosen action in rats deciding between differently delayed or sized rewards. J. Neurosci. 29:13365–76 [Google Scholar]
  70. Romani S, Tsodyks M. 2015. Short-term plasticity based network model of place cells dynamics. Hippocampus 25:94–105 [Google Scholar]
  71. Schultz W, Dayan P, Montague PR. 1997. A neural substrate of prediction and reward. Science 275:1593–99 [Google Scholar]
  72. Schwindel CD, McNaughton BL. 2011. Hippocampal-cortical interactions and the dynamics of memory trace reactivation. Prog. Brain Res. 193:163–77 [Google Scholar]
  73. Seol GH, Ziburkus J, Huang S, Song L, Kim IT. et al. 2007. Neuromodulators control the polarity of spike-timing-dependent synaptic plasticity. Neuron 55:919–29 [Google Scholar]
  74. Shallice T. 1988. From Neuropsychology to Mental Structure Cambridge, UK: Cambridge Univ. Press
  75. Silva D, Feng T, Foster DJ. 2015. Trajectory events across hippocampal place cells require previous experience. Nat. Neurosci. 18:1772–79 [Google Scholar]
  76. Singer AC, Carr MF, Karlsson MP, Frank LM. 2013. Hippocampal SWR activity predicts correct decisions during the initial learning of an alternation task. Neuron 77:1163–73 [Google Scholar]
  77. Singer AC, Frank LM. 2009. Rewarded outcomes enhance reactivation of experience in the hippocampus. Neuron 64:910–21 [Google Scholar]
  78. Singh SP. 1992. Reinforcement learning with a hierarchy of abstract models. Proc. Tenth Natl. Conf. Artif. Intell., San Jose, CA, July 12–16202–7 Menlo Park, CA: AAAI Press [Google Scholar]
  79. Skaggs WE, McNaughton BL. 1996. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271:1870–73 [Google Scholar]
  80. Solstad T, Moser EI, Einevoll GT. 2006. From grid cells to place cells: a mathematical model. Hippocampus 16:1026–31 [Google Scholar]
  81. Sompolinsky H, Kanter I. 1986. Temporal association in asymmetric neural networks. Phys. Rev. Lett. 57:2861–64 [Google Scholar]
  82. Squire LR. 1992. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99:195–231 [Google Scholar]
  83. Squire LR, Genzel L, Wixted JT, Morris RG. 2015. Memory consolidation. Cold Spring Harb. Perspect. Biol. 7:a021766 [Google Scholar]
  84. Suh J, Foster DJ, Davoudi H, Wilson MA, Tonegawa S. 2013. Impaired hippocampal ripple-associated replay in a mouse model of schizophrenia. Neuron 80:484–93 [Google Scholar]
  85. Sutton RS, Barto AG. 1998. Reinforcement Learning: An Introduction Cambridge, MA: MIT Press
  86. Sutton RS, Precup D, Singh S. 1999. Between MDPs and semi-MDPs: a framework for temporal abstraction in reinforcement learning. Artif. Intell. 112:181–211 [Google Scholar]
  87. Tobler PN, Fiorillo CD, Schultz W. 2005. Adaptive coding of reward value by dopamine neurons. Science 307:1642–45 [Google Scholar]
  88. Tolman EC. 1948. Cognitive maps in rats and men. Psychol. Rev. 55:189–208 [Google Scholar]
  89. Tolman EC. 1949. Purposive Behavior in Animals and Men Berkeley: Univ. Calif. Press
  90. Tolman EC, Honzik CH. 1930. “Insight” in rats. Univ. Calif. Publ. Psychol. 4:215–32 [Google Scholar]
  91. Tulving E. 2002. Episodic memory: from mind to brain. Annu. Rev. Psychol. 53:1–25 [Google Scholar]
  92. van der Meer MAA, Redish AD. 2009. Covert expectation-of-reward in rat ventral striatum at decision points. Front. Integr. Neurosci. 3:1 [Google Scholar]
  93. van der Meer MAA, Redish AD. 2011. Theta phase precession in rat ventral striatum links place and reward information. J. Neurosci. 31:2843–54 [Google Scholar]
  94. Wilson MA, McNaughton BL. 1993. Dynamics of the hippocampal ensemble code for space. Science 261:1055–58 [Google Scholar]
  95. Wilson MA, McNaughton BL. 1994. Reactivation of hippocampal ensemble memories during sleep. Science 265:676–79 [Google Scholar]
  96. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H. 2000. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27:623–33 [Google Scholar]
  97. Wu X, Foster DJ. 2014. Hippocampal replay captures the unique topological structure of a novel environment. J. Neurosci. 34:6459–69 [Google Scholar]
  98. York LC, van Rossum MC. 2009. Recurrent networks with short term synaptic depression. J. Comput. Neurosci. 27:607–20 [Google Scholar]
  99. Zhang JC, Lau PM, Bi GQ. 2009. Gain in sensitivity and loss in temporal contrast of STDP by dopaminergic modulation at hippocampal synapses. PNAS 106:13028–33 [Google Scholar]
  100. Zhang K, Ginzburg I, McNaughton BL, Sejnowski TJ. 1998. Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. J. Neurophysiol. 79:1017–44 [Google Scholar]

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