1932

Abstract

The hippocampus is critical for memory and spatial navigation. The ability to map novel environments, as well as more abstract conceptual relationships, is fundamental to the cognitive flexibility that humans and other animals require to survive in a dynamic world. In this review, we survey recent advances in our understanding of how this flexibility is implemented anatomically and functionally by hippocampal circuitry, during both active exploration (online) and rest (offline). We discuss the advantages and limitations of spike timing–dependent plasticity and the more recently discovered behavioral timescale synaptic plasticity in supporting distinct learning modes in the hippocampus. Finally, we suggest complementary roles for these plasticity types in explaining many-shot and single-shot learning in the hippocampus and discuss how these rules could work together to support the learning of cognitive maps.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-102423-100258
2024-08-08
2024-12-12
Loading full text...

Full text loading...

/deliver/fulltext/neuro/47/1/annurev-neuro-102423-100258.html?itemId=/content/journals/10.1146/annurev-neuro-102423-100258&mimeType=html&fmt=ahah

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:(1):5259
    [Google Scholar]
  2. Ambrose RE, Pfeiffer BE, Foster DJ. 2016.. Reverse replay of hippocampal place cells is uniquely modulated by changing reward. . Neuron 91:(5):112436
    [Crossref] [Google Scholar]
  3. Andersen P, Morris R, Amaral DG, Bliss T, O'Keefe J, eds. 2007.. The Hippocampus Book. New York:: Oxford Academic
    [Google Scholar]
  4. Andrychowicz M, Wolski F, Ray A, Schneider J, Fong R, et al. 2017.. Hindsight experience replay. . Adv. Neural Inform. Proc. Syst. 30:. https://proceedings.neurips.cc/paper_files/paper/2017/file/453fadbd8a1a3af50a9df4df899537b5-Paper.pdf
    [Google Scholar]
  5. Aronov D, Nevers R, Tank DW. 2017.. Mapping of a non-spatial dimension by the hippocampal–entorhinal circuit. . Nature 543:(7647):71922
    [Crossref] [Google Scholar]
  6. Baraduc P, Duhamel JR, Wirth S. 2019.. Schema cells in the macaque hippocampus. . Science 363:(6427):63539
    [Crossref] [Google Scholar]
  7. Behrens TE, Muller TH, Whittington JC, Mark S, Baram AB, et al. 2018.. What is a cognitive map? Organizing knowledge for flexible behavior. . Neuron 100:(2):490509
    [Crossref] [Google Scholar]
  8. Bendor D, Wilson MA. 2012.. Biasing the content of hippocampal replay during sleep. . Nat. Neurosci. 15:(10):143944
    [Crossref] [Google Scholar]
  9. Benna MK, Fusi S. 2021.. Place cells may simply be memory cells: Memory compression leads to spatial tuning and history dependence. . PNAS 118:(51):e2018422118
    [Crossref] [Google Scholar]
  10. Berners-Lee A, Feng T, Silva D, Wu X, Ambrose ER, et al. 2022.. Hippocampal replays appear after a single experience and incorporate greater detail with more experience. . Neuron 110:(11):182942
    [Crossref] [Google Scholar]
  11. Bezaire MJ, Raikov I, Burk K, Vyas D, Soltesz I. 2016.. Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit. . eLife 5::e18566
    [Crossref] [Google Scholar]
  12. Bezaire MJ, Soltesz I. 2013.. Quantitative assessment of CA1 local circuits: knowledge base for interneuron-pyramidal cell connectivity. . Hippocampus 23:(9):75185
    [Crossref] [Google Scholar]
  13. Bi GQ, Poo MM. 1998.. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. . J. Neurosci. 18:(24):1046472
    [Crossref] [Google Scholar]
  14. Bittner KC, Grienberger C, Vaidya SP, Milstein AD, Macklin JJ, et al. 2015.. Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons. . Nat. Neurosci. 18:(8):113342
    [Crossref] [Google Scholar]
  15. Bittner KC, Milstein AD, Grienberger C, Romani S, Magee JC. 2017.. Behavioral time scale synaptic plasticity underlies CA1 place fields. . Science 357:(6355):103336
    [Crossref] [Google Scholar]
  16. Bowler JC, Losonczy A. 2023.. Direct cortical inputs to hippocampal area CA1 transmit complementary signals for goal-directed navigation. . Neuron 111:(24):407185.e6
    [Crossref] [Google Scholar]
  17. Branco T, Clark BA, Hausser M. 2010.. Dendritic discrimination of temporal input sequences in cortical neurons. . Science 329:(5999):167175
    [Crossref] [Google Scholar]
  18. Buzsáki G. 2015.. Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. . Hippocampus 25:(10):1073188
    [Crossref] [Google Scholar]
  19. Buzsáki G, Draguhn A. 2004.. Neuronal oscillations in cortical networks. . Science 304:(5679):192629
    [Crossref] [Google Scholar]
  20. Buzsáki G, Logothetis N, Singer W. 2013.. Scaling brain size, keeping timing: evolutionary preservation of brain rhythms. . Neuron 80:(3):75164
    [Crossref] [Google Scholar]
  21. Caillard O, Ben-Ari Y, Gaiarsa JL. 1999a.. Long-term potentiation of GABAergic synaptic transmission in neonatal rat hippocampus. . J. Physiol. 518:(1):10919
    [Crossref] [Google Scholar]
  22. Caillard O, Ben-Ari Y, Gaarsa JL. 1999b.. Mechanisms of induction and expression of long-term depression at GABAergic synapses in the neonatal rat hippocampus. . J. Neurosci. 19:(17):756877
    [Crossref] [Google Scholar]
  23. Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, et al. 2013.. Ultrasensitive fluorescent proteins for imaging neuronal activity. . Nature 499:(7458):295300
    [Crossref] [Google Scholar]
  24. Chevaleyre V, Castillo PE. 2003.. Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. . Neuron 38:(3):46172
    [Crossref] [Google Scholar]
  25. Constantinescu AO, O'Reilly JX, Behrens TE. 2016.. Organizing conceptual knowledge in humans with a gridlike code. . Science 352:(6292):146468
    [Crossref] [Google Scholar]
  26. D'amour JA, Froemke RC. 2015.. Inhibitory and excitatory spike-timing-dependent plasticity in the auditory cortex. . Neuron 86:(2):51428
    [Crossref] [Google Scholar]
  27. Dan Y, Poo MM. 2006.. Spike timing-dependent plasticity: from synapse to perception. . Physiol. Rev. 86:(3):103348
    [Crossref] [Google Scholar]
  28. Dragoi G, Buzsáki G. 2006.. Temporal encoding of place sequences by hippocampal cell assemblies. . Neuron 50:(1):14557
    [Crossref] [Google Scholar]
  29. Dragoi G, Tonegawa S. 2014.. Selection of preconfigured cell assemblies for representation of novel spatial experiences. . Philos. Trans. R. Soc. B 369:(1635):20120522
    [Crossref] [Google Scholar]
  30. Dudok B, Klein PM, Hwaun E, Lee BR, Yao Z, et al. 2021a.. Alternating sources of perisomatic inhibition during behavior. . Neuron 109:(6):9971012
    [Crossref] [Google Scholar]
  31. Dudok B, Szoboszlay M, Paul A, Klein PM, Liao Z, et al. 2021b.. Recruitment and inhibitory action of hippocampal axo-axonic cells during behavior. . Neuron 109:(23):383850
    [Crossref] [Google Scholar]
  32. Ecker A, Bagi B, Vértes E, Steinbach-Németh O, Karlócai MR, et al. 2022.. Hippocampal sharp wave-ripples and the associated sequence replay emerge from structured synaptic interactions in a network model of area CA3. . eLife 11::e71850
    [Crossref] [Google Scholar]
  33. Ego-Stengel V, Wilson MA. 2010.. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. . Hippocampus 20:(1):110
    [Crossref] [Google Scholar]
  34. Eichenbaum H. 2000.. A cortical-hippocampal system for declarative memory. . Nat. Rev. Neurosci. 1:(1):4150
    [Crossref] [Google Scholar]
  35. Eichenbaum H. 2014.. Time cells in the hippocampus: a new dimension for mapping memories. . Nat. Rev. Neurosci. 15:(11):73244
    [Crossref] [Google Scholar]
  36. Ekstrom A, Meltzer J, McNaughton B, Barnes C. 2001.. NMDA receptor antagonism blocks experience-dependent expansion of hippocampal “place fields. .” Neuron 31:(4):63138
    [Crossref] [Google Scholar]
  37. Eliav T, Maimon SR, Aljadeff J, Tsodyks M, Ginosar G, et al. 2021.. Multiscale representation of very large environments in the hippocampus of flying bats. . Science 372:(6545):eabg4020
    [Crossref] [Google Scholar]
  38. Engel J. 1996.. Excitation and inhibition in epilepsy. . Can. J. Neurol. Sci. 23:(3):16774
    [Crossref] [Google Scholar]
  39. Euston DR, Tatsuno M, McNaughton BL. 2007.. Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. . Science 318:(5853):114750
    [Crossref] [Google Scholar]
  40. Eysenbach B, Salakhutdinov RR, Levine S. 2019.. Search on the replay buffer: bridging planning and reinforcement learning. . Adv. Neural Inform. Proc. Syst. 32:. https://proceedings.neurips.cc/paper_files/paper/2019/file/5c48ff18e0a47baaf81d8b8ea51eec92-Paper.pdf
    [Google Scholar]
  41. Fan LZ, Kim DK, Jennings JH, Tian H, Wang PY, et al. 2023.. All-optical physiology resolves a synaptic basis for behavioral timescale plasticity. . Cell 186:(3):54359.e19
    [Crossref] [Google Scholar]
  42. Fauth MJ, Van Rossum MC. 2019.. Self-organized reactivation maintains and reinforces memories despite synaptic turnover. . eLife 8::e43717
    [Crossref] [Google Scholar]
  43. Fei-Fei L, Fergus R, Perona P. 2006.. One-shot learning of object categories. . IEEE Trans. Pattern Anal. Mach. Intel. 28:(4):594611
    [Crossref] [Google Scholar]
  44. FeldmanHall O, Montez DF, Phelps EA, Davachi L, Murty VP. 2021.. Hippocampus guides adaptive learning during dynamic social interactions. . J. Neurosci. 41:(6):134048
    [Crossref] [Google Scholar]
  45. Fernandez-Ruiz A, Oliva A, Fermino de Oliveira E, Rocha-Almeida F, Tingley D, Buzsáki G. 2019.. Long-duration hippocampal sharp wave ripples improve memory. . Science 364:(6445):108286
    [Crossref] [Google Scholar]
  46. Foster DJ. 2017.. Replay comes of age. . Annu. Rev. Neurosci. 40::581602
    [Crossref] [Google Scholar]
  47. Foster DJ, Knierim JJ. 2012.. Sequence learning and the role of the hippocampus in rodent navigation. . Curr. Opin. Neurobiol. 22:(2):294300
    [Crossref] [Google Scholar]
  48. Foster DJ, Wilson MA. 2006.. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. . Nature 440:(7084):68083
    [Crossref] [Google Scholar]
  49. Foster DJ, Wilson MA. 2007.. Hippocampal theta sequences. . Hippocampus 17:(11):109399
    [Crossref] [Google Scholar]
  50. Froemke RC, Poo MM, Dan Y. 2005.. Spike-timing-dependent synaptic plasticity depends on dendritic location. . Nature 434:(7030):22125
    [Crossref] [Google Scholar]
  51. Gaiarsa JL, Caillard O, Ben-Ari Y. 2002.. Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance. . Trends Neurosci. 25:(11):56470
    [Crossref] [Google Scholar]
  52. Geiller T, Sadeh S, Rolotti SV, Blockus H, Vancura B, et al. 2022.. Local circuit amplification of spatial selectivity in the hippocampus. . Nature 601:(7891):1059
    [Crossref] [Google Scholar]
  53. Geiller T, Vancura B, Terada S, Troullinou E, Chavlis S, et al. 2020.. Large-scale 3D two-photon imaging of molecularly identified CA1 interneuron dynamics in behaving mice. . Neuron 108:(5):96883.e9
    [Crossref] [Google Scholar]
  54. Gelfand AE, Smith AF. 1990.. Sampling-based approaches to calculating marginal densities. . J. Am. Stat. Assoc. 85:(410):398409
    [Crossref] [Google Scholar]
  55. Gillespie AK, Astudillo Maya DA, Denovellis EL, Liu DF, Kastner DB, et al. 2021.. Hippocampal replay reflects specific past experiences rather than a plan for subsequent choice. . Neuron 109:(19):314963.e6
    [Crossref] [Google Scholar]
  56. Girardeau G, Benchenane K, Wiener SI, Buzsáki G, Zugaro MB. 2009.. Selective suppression of hippocampal ripples impairs spatial memory. . Nat. Neurosci. 12:(10):122223
    [Crossref] [Google Scholar]
  57. Gonzalez KC, Losonczy A, Negrean A. 2022.. Dendritic excitability and synaptic plasticity in vitro and in vivo. . Neuroscience 489::16575
    [Crossref] [Google Scholar]
  58. Gonzalez KC, Negrean A, Liao Z, Polleux F, Losonczy A. 2023.. Synaptic basis of behavioral timescale plasticity. . bioRxiv 2023.10.04.560848. https://doi.org/10.1101/2023.10.04.560848
  59. Grenier F, Timofeev I, Steriade M. 2001.. Focal synchronization of ripples (80–200 Hz) in neocortex and their neuronal correlates. . J. Neurophysiol. 86:(4):188498
    [Crossref] [Google Scholar]
  60. Grienberger C, Magee JC. 2022.. Entorhinal cortex directs learning-related changes in CA1 representations. . Nature 611:(7936):55462
    [Crossref] [Google Scholar]
  61. Grieves RM, Jedidi-Ayoub S, Mishchanchuk K, Liu A, Renaudineau S, et al. 2021.. Irregular distribution of grid cell firing fields in rats exploring a 3D volumetric space. . Nat. Neurosci. 24:(11):156773
    [Crossref] [Google Scholar]
  62. Grill-Spector K, Malach R. 2004.. The human visual cortex. . Annu. Rev. Neurosci. 27::64977
    [Crossref] [Google Scholar]
  63. Grosmark AD, Buzsáki G. 2016.. Diversity in neural firing dynamics supports both rigid and learned hippocampal sequences. . Science 351:(6280):144043
    [Crossref] [Google Scholar]
  64. Grosmark AD, Sparks FT, Davis MJ, Losonczy A. 2021.. Reactivation predicts the consolidation of unbiased long-term cognitive maps. . Nat. Neurosci. 24:(11):157485
    [Crossref] [Google Scholar]
  65. Gubellini P, Ben-Ari Y, Gaarsa JL. 2001.. Activity- and age-dependent GABAergic synaptic plasticity in the developing rat hippocampus. . Eur. J. Neurosci. 14:(12):193746
    [Crossref] [Google Scholar]
  66. Gupta AS, Van Der Meer MA, Touretzky DS, Redish AD. 2010.. Hippocampal replay is not a simple function of experience. . Neuron 65:(5):695705
    [Crossref] [Google Scholar]
  67. Hadjiabadi D, Lovett-Barron M, Raikov IG, Sparks FT, Liao Z, et al. 2021.. Maximally selective single-cell target for circuit control in epilepsy models. . Neuron 109:(16):255672
    [Crossref] [Google Scholar]
  68. Hassabis D, Kumaran D, Summerfield C, Botvinick M. 2017.. Neuroscience-inspired artificial intelligence. . Neuron 95:(2):24558
    [Crossref] [Google Scholar]
  69. Hebb DO. 1949.. The Organization of Behavior: A Neuropsychological Theory. London:: Psychol. Press
    [Google Scholar]
  70. Huszar R, Zhang Y, Blockus H, Buzsáki G. 2022.. Preconfigured dynamics in the hippocampus are guided by embryonic birthdate and rate of neurogenesis. . Nat. Neurosci. 25:(9):120112
    [Crossref] [Google Scholar]
  71. Jablonowski J, Taesler P, Fu Q, Rose M. 2018.. Implicit acoustic sequence learning recruits the hippocampus. . PLOS ONE 13:(12):e0209590
    [Crossref] [Google Scholar]
  72. Jacobacci F, Armony JL, Yeffal A, Lerner G, Amaro E Jr., et al. 2020.. Rapid hippocampal plasticity supports motor sequence learning. . PNAS 117:(38):23898903
    [Crossref] [Google Scholar]
  73. Jadhav SP, Kemere C, German PW, Frank LM. 2012.. Awake hippocampal sharp-wave ripples support spatial memory. . Science 336:(6087):145458
    [Crossref] [Google Scholar]
  74. Jahnke S, Timme M, Memmesheimer RM. 2015.. A unified dynamic model for learning, replay, and sharp-wave/ripples. . J. Neurosci. 35:(49):1623658
    [Crossref] [Google Scholar]
  75. Ji D, Wilson MA. 2007.. Coordinated memory replay in the visual cortex and hippocampus during sleep. . Nat. Neurosci. 10:(1):1007
    [Crossref] [Google Scholar]
  76. Jia H, Rochefort NL, Chen X, Konnerth A. 2010.. Dendritic organization of sensory input to cortical neurons in vivo. . Nature 464:(7293):130712
    [Crossref] [Google Scholar]
  77. Jun JJ, Steinmetz NA, Siegle JH, Denman DJ, Bauza M, et al. 2017.. Fully integrated silicon probes for high-density recording of neural activity. . Nature 551:(7679):23236
    [Crossref] [Google Scholar]
  78. Karlsson MP, Frank LM. 2008.. Network dynamics underlying the formation of sparse, informative representations in the hippocampus. . J. Neurosci. 28:(52):1427181
    [Crossref] [Google Scholar]
  79. Kaufman AM, Geiller T, Losonczy A. 2020.. A role for the locus coeruleus in hippocampal CA1 place cell reorganization during spatial reward learning. . Neuron 105:(6):101826
    [Crossref] [Google Scholar]
  80. Kay K, Chung JE, Sosa M, Schor JS, Karlsson MP, et al. 2020.. Constant sub-second cycling between representations of possible futures in the hippocampus. . Cell 180:(3):55267
    [Crossref] [Google Scholar]
  81. Khodagholy D, Gelinas JN, Buzsáki G. 2017.. Learning-enhanced coupling between ripple oscillations in association cortices and hippocampus. . Science 358:(6361):36972
    [Crossref] [Google Scholar]
  82. Kim YJ, Ujfalussy BB, Lengyel M. 2023.. Parallel functional architectures within a single dendritic tree. . Cell Rep. 42:(4):112386
    [Crossref] [Google Scholar]
  83. King C, Henze DA, Leinekugel X, Buzsáki G. 1999.. Hebbian modification of a hippocampal population pattern in the rat. . J. Physiol. 521:(1):15967
    [Crossref] [Google Scholar]
  84. Kolibius L, Roux F, Parish G, Ter Wal M, Van Der Plas M, et al. 2023.. Hippocampal neurons code individual episodic memories in humans. . Nat. Hum. Behav. 7:(11):196879
    [Crossref] [Google Scholar]
  85. Kullmann DM, Lamsa KP. 2007.. Long-term synaptic plasticity in hippocampal interneurons. . Nat. Rev. Neurosci. 8:(9):68799
    [Crossref] [Google Scholar]
  86. Lake BM, Salakhutdinov RR, Tenenbaum J. 2013.. One-shot learning by inverting a compositional causal process. . Adv. Neural Inform. Proc. Syst. 26:. https://papers.nips.cc/paper_files/paper/2013/file/52292e0c763fd027c6eba6b8f494d2eb-Paper.pdf
    [Google Scholar]
  87. Lenck-Santini PP, Scott RC. 2015.. Mechanisms responsible for cognitive impairment in epilepsy. . Cold Spring Harb. Perspect. Med. 5:(10):a022772
    [Crossref] [Google Scholar]
  88. Li Y, Briguglio J, Romani S, Magee JC. 2023.. Mechanisms of memory storage and retrieval in hippocampal area CA3. . bioRxiv 2023.05.30.542781. https://doi.org/10.1101/2023.05.30.542781
  89. Liao Z, Gonzalez KC, Li DM, Yang CM, Holder D, . 2024.. Functional architecture of intracellular oscillations in hippocampal dendrites. . bioRxiv 2024.02.12.579750. https://doi.org/10.1101/2024.02.12.579750
  90. Liao Z, Hadjiabadi DH, Terada S, Soltesz I, Losonczy A. 2022.. An inhibitory plasticity mechanism for world structure inference by hippocampal replay. . bioRxiv 2022.11.02.514897. https://doi.org/10.1101/2022.11.02.514897
  91. Lillicrap TP, Hunt JJ, Pritzel A, Heess N, Erez T, et al. 2015.. Continuous control with deep reinforcement learning. . arXiv:1509.02971 [cs.LG]
  92. Liotta A, Çalɪşkan G, ul Haq R, Hollnagel JO, Rösler A, et al. 2011.. Partial disinhibition is required for transition of stimulus-induced sharp wave–ripple complexes into recurrent epileptiform discharges in rat hippocampal slices. . J. Neurophysiol. 105:(1):17287
    [Crossref] [Google Scholar]
  93. Liu AA, Henin S, Abbaspoor S, Bragin A, Buffalo EA, et al. 2022.. A consensus statement on detection of hippocampal sharp wave ripples and differentiation from other fast oscillations. . Nat. Commun. 13:(1):6000
    [Crossref] [Google Scholar]
  94. Liu Z, Lu X, Villette V, Gou Y, Colbert KL, et al. 2022.. Sustained deep-tissue voltage recording using a fast indicator evolved for two-photon microscopy. . Cell 185:(18):340825.e29
    [Crossref] [Google Scholar]
  95. Losonczy A, Magee JC. 2006.. Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. . Neuron 50:(2):291307
    [Crossref] [Google Scholar]
  96. Losonczy A, Makara JK, Magee JC. 2008.. Compartmentalized dendritic plasticity and input feature storage in neurons. . Nature 452:(7186):43641
    [Crossref] [Google Scholar]
  97. Losonczy A, Zemelman BV, Vaziri A, Magee JC. 2010.. Network mechanisms of theta related neuronal activity in hippocampal CA1 pyramidal neurons. . Nat. Neurosci. 13:(8):96772
    [Crossref] [Google Scholar]
  98. Madar A, Dong C, Sheffield M. 2023.. BTSP, not STDP, drives shifts in hippocampal representations during familiarization. . bioRxiv 2023.10.17.562791. https://doi.org/10.1101/2023.10.17.562791
  99. Magee JC, Grienberger C. 2020.. Synaptic plasticity forms and functions. . Annu. Rev. Neurosci. 43::95117
    [Crossref] [Google Scholar]
  100. Malerba P, Bazhenov M. 2019.. Circuit mechanisms of hippocampal reactivation during sleep. . Neurobiol. Learn. Mem. 160::98107
    [Crossref] [Google Scholar]
  101. Marafiga JR, Pasquetti MV, Calcagnotto ME. 2020.. GABAergic interneurons in epilepsy: more than a simple change in inhibition. . Epilepsy Behav. 121::106935
    [Crossref] [Google Scholar]
  102. Markram H, Lübke J, Frotscher M, Sakmann B. 1997.. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. . Science 275:(5297):21315
    [Crossref] [Google Scholar]
  103. Mattar MG, Daw ND. 2018.. Prioritized memory access explains planning and hippocampal replay. . Nat. Neurosci. 21:(11):160917
    [Crossref] [Google Scholar]
  104. 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:(3):41957
    [Crossref] [Google Scholar]
  105. McEchron MD, Bouwmeester H, Tseng W, Weiss C, Disterhoft JF. 1998.. Hippocampectomy disrupts auditory trace fear conditioning and contextual fear conditioning in the rat. . Hippocampus 8:(6):63846
    [Crossref] [Google Scholar]
  106. McKenzie S. 2018.. Inhibition shapes the organization of hippocampal representations. . Hippocampus 28:(9):65971
    [Crossref] [Google Scholar]
  107. McMahon LL, Kauer JA. 1997.. Hippocampal interneurons express a novel form of synaptic plasticity. . Neuron 18:(2):295305
    [Crossref] [Google Scholar]
  108. Mehta MR, Barnes CA, McNaughton BL. 1997.. Experience-dependent, asymmetric expansion of hippocampal place fields. . PNAS 94:(16):891821
    [Crossref] [Google Scholar]
  109. Milner B, Corkin S, Teuber HL. 1968.. Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M. . Neuropsychologia 6:(3):21534
    [Crossref] [Google Scholar]
  110. Milstein AD, Li Y, Bittner KC, Grienberger C, Soltesz I, et al. 2021.. Bidirectional synaptic plasticity rapidly modifies hippocampal representations. . eLife 10::e73046
    [Crossref] [Google Scholar]
  111. Milstein AD, Tran S, Ng G, Soltesz I. 2023.. Offline memory replay in recurrent neuronal networks emerges from constraints on online dynamics. . J. Physiol. 601:(15):324164
    [Crossref] [Google Scholar]
  112. Mishra RK, Kim S, Guzman SJ, Jonas P. 2016.. Symmetric spike timing-dependent plasticity at CA3–CA3 synapses optimizes storage and recall in autoassociative networks. . Nat. Commun. 7:(1):11552
    [Crossref] [Google Scholar]
  113. Morris RG, Garrud P, Rawlins JN, O'Keefe J. 1982.. Place navigation impaired in rats with hippocampal lesions. . Nature 297:(5868):68183
    [Crossref] [Google Scholar]
  114. Moser EI, Moser MB. 2003.. One-shot memory in hippocampal CA3 networks. . Neuron 38:(2):14748
    [Crossref] [Google Scholar]
  115. Muessig L, Lasek M, Varsavsky I, Cacucci F, Wills TJ. 2019.. Coordinated emergence of hippocampal replay and theta sequences during post-natal development. . Curr. Biol. 29:(5):83440
    [Crossref] [Google Scholar]
  116. Neves G, Cooke SF, Bliss TV. 2008.. Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. . Nat. Rev. Neurosci. 9:(1):6575
    [Crossref] [Google Scholar]
  117. Nguyen ND, Lutas A, Amsalem O, Fernando J, Ahn AY-E, et al. 2024.. Cortical reactivations predict future sensory responses. . Nature 625::11018
    [Crossref] [Google Scholar]
  118. Nicola W, Clopath C. 2017.. Supervised learning in spiking neural networks with force training. . Nat. Commun. 8:(1):2208
    [Crossref] [Google Scholar]
  119. Nicola W, Clopath C. 2019.. A diversity of interneurons and Hebbian plasticity facilitate rapid compressible learning in the hippocampus. . Nat. Neurosci. 22:(7):116881
    [Crossref] [Google Scholar]
  120. Nieh EH, Schottdorf M, Freeman NW, Low RJ, Lewallen S, et al. 2021.. Geometry of abstract learned knowledge in the hippocampus. . Nature 595:(7865):8084
    [Crossref] [Google Scholar]
  121. Noguchi A, Huszar R, Morikawa S, Buzsáki G, Ikegaya Y. 2022.. Inhibition allocates spikes during hippocampal ripples. . Nat. Commun. 13:(1):1280
    [Crossref] [Google Scholar]
  122. Norimoto H, Makino K, Gao M, Shikano Y, Okamoto K, et al. 2018.. Hippocampal ripples down-regulate synapses. . Science 359:(6383):152427
    [Crossref] [Google Scholar]
  123. Norman Y, Yeagle EM, Khuvis S, Harel M, Mehta AD, Malach R. 2019.. Hippocampal sharp-wave ripples linked to visual episodic recollection in humans. . Science 365:(6454):eaax1030
    [Crossref] [Google Scholar]
  124. Nour MM, Liu Y, Arumuham A, Kurth-Nelson Z, Dolan RJ. 2021.. Impaired neural replay of inferred relationships in schizophrenia. . Cell 184:(16):431528
    [Crossref] [Google Scholar]
  125. Nusser Z, Hajos N, Somogyi P, Mody I. 1998.. Increased number of synaptic GABAA receptors underlies potentiation at hippocampal inhibitory synapses. . Nature 395:(6698):17277
    [Crossref] [Google Scholar]
  126. O'Hare JK, Gonzalez KC, Herrlinger SA, Hirabayashi Y, Hewitt VL, et al. 2022.. Compartment-specific tuning of dendritic feature selectivity by intracellular CA2+ release. . Science 375:(6586):eabm1670
    [Crossref] [Google Scholar]
  127. 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::17175
    [Crossref] [Google Scholar]
  128. O'Keefe J, Nadel L. 1978.. The Hippocampus as a Cognitive Map. Oxford, UK:: Clarendon
    [Google Scholar]
  129. Ólafsdóttir HF, Bush D, Barry C. 2018.. The role of hippocampal replay in memory and planning. . Curr. Biol. 28:(1):R3750
    [Crossref] [Google Scholar]
  130. Ólafsdóttir HF, Carpenter F, Barry C. 2017.. Task demands predict a dynamic switch in the content of awake hippocampal replay. . Neuron 96:(4):92535
    [Crossref] [Google Scholar]
  131. Oliva A, Fernández-Ruiz A, Leroy F, Siegelbaum SA. 2020.. Hippocampal CA2 sharp-wave ripples reactivate and promote social memory. . Nature 587:(7833):26469
    [Crossref] [Google Scholar]
  132. Payne HL, Lynch GF, Aronov D. 2020.. Precise spatial representations in the hippocampus of a food-caching bird. . bioRxiv 2020.11.27.399444. https://doi.org/10.1101/2020.11.27.399444
  133. Paz JT, Huguenard JR. 2015.. Microcircuits and their interactions in epilepsy: Is the focus out of focus?. Nat. Neurosci. 18:(3):35159
    [Crossref] [Google Scholar]
  134. Penfield W, Milner B. 1958.. Memory deficit produced by bilateral lesions in the hippocampal zone. . AMA Arch. Neurol. Psychiatry 79:(5):47597
    [Crossref] [Google Scholar]
  135. Peyrache A, Khamassi M, Benchenane K, Wiener SI, Battaglia FP. 2009.. Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. . Nat. Neurosci. 12:(7):91926
    [Crossref] [Google Scholar]
  136. Pfeiffer BE, Foster DJ. 2013.. Hippocampal place-cell sequences depict future paths to remembered goals. . Nature 497:(7447):7479
    [Crossref] [Google Scholar]
  137. Poirazi P, Brannon T, Mel BW. 2003.. Pyramidal neuron as two-layer neural network. . Neuron 37:(6):98999
    [Crossref] [Google Scholar]
  138. Poirazi P, Papoutsi A. 2020.. Illuminating dendritic function with computational models. . Nat. Rev. Neurosci. 21:(6):30321
    [Crossref] [Google Scholar]
  139. Poldrack RA, Rodriguez P. 2003.. Sequence learning: What's the hippocampus to do?. Neuron 37:(6):89193
    [Crossref] [Google Scholar]
  140. Priestley JB, Bowler JC, Rolotti SV, Fusi S, Losonczy A. 2022.. Signatures of rapid plasticity in hippocampal CA1 representations during novel experiences. . Neuron 110:(12):197892
    [Crossref] [Google Scholar]
  141. Quiroga RQ, Reddy L, Kreiman G, Koch C, Fried I. 2005.. Invariant visual representation by single neurons in the human brain. . Nature 435:(7045):11027
    [Crossref] [Google Scholar]
  142. Reddy L, Self MW, Zoefel B, Poncet M, Possel JK, et al. 2021.. Theta-phase dependent neuronal coding during sequence learning in human single neurons. . Nat. Commun. 12:(1):4839
    [Crossref] [Google Scholar]
  143. Reid IC, Stewart CA. 1997.. Seizures, memory and synaptic plasticity. . Seizure 6:(5):35159
    [Crossref] [Google Scholar]
  144. Rolnick D, Ahuja A, Schwarz J, Lillicrap T, Wayne G. 2019.. Experience replay for continual learning. . Adv. Neural Inform. Proc. Syst. 32:. https://papers.nips.cc/paper_files/paper/2019/file/fa7cdfad1a5aaf8370ebeda47a1ff1c3-Paper.pdf
    [Google Scholar]
  145. Rolotti SV, Ahmed MS, Szoboszlay M, Geiller T, Negrean A, et al. 2022a.. Local feedback inhibition tightly controls rapid formation of hippocampal place fields. . Neuron 110:(5):78394.e6
    [Crossref] [Google Scholar]
  146. Rolotti SV, Blockus H, Sparks FT, Priestley JB, Losonczy A. 2022b.. Reorganization of CA1 dendritic dynamics by hippocampal sharp-wave ripples during learning. . Neuron 110:(6):97791
    [Crossref] [Google Scholar]
  147. Rothschild G, Eban E, Frank LM. 2017.. A cortical-hippocampal-cortical loop of information processing during memory consolidation. . Nat. Neurosci. 20:(2):25159
    [Crossref] [Google Scholar]
  148. Royer S, Zemelman BV, Losonczy A, Kim J, Chance F, et al. 2012.. Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. . Nat. Neurosci. 15::76975
    [Crossref] [Google Scholar]
  149. Sadowski JH, Jones MW, Mellor JR. 2016.. Sharp-wave ripples orchestrate the induction of synaptic plasticity during reactivation of place cell firing patterns in the hippocampus. . Cell Rep. 14:(8):191629
    [Crossref] [Google Scholar]
  150. Samborska V, Butler JL, Walton ME, Behrens TE, Akam T. 2022.. Complementary task representations in hippocampus and prefrontal cortex for generalizing the structure of problems. . Nat. Neurosci. 25:(10):131426
    [Crossref] [Google Scholar]
  151. Schwartenbeck P, Baram A, Liu Y, Mark S, Muller T, et al. 2023.. Generative replay underlies compositional inference in the hippocampal-prefrontal circuit. . Cell 26::488597.e14
    [Crossref] [Google Scholar]
  152. Scoville WB, Milner B. 1957.. Loss of recent memory after bilateral hippocampal lesions. . J. Neurol. Neurosurg. Psychiatry 20::1121
    [Crossref] [Google Scholar]
  153. Silva D, Feng T, Foster DJ. 2015.. Trajectory events across hippocampal place cells require previous experience. . Nat. Neurosci. 18:(12):177279
    [Crossref] [Google Scholar]
  154. Singer AC, Frank LM. 2009.. Rewarded outcomes enhance reactivation of experience in the hippocampus. . Neuron 64:(6):91021
    [Crossref] [Google Scholar]
  155. Skaggs WE, McNaughton BL, Permenter M, Archibeque M, Vogt J, et al. 2007.. EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. . J. Neurophysiol. 98:(2):898910
    [Crossref] [Google Scholar]
  156. Smith SL, Smith IT, Branco T, Häusser M. 2013.. Dendritic spikes enhance stimulus selectivity in cortical neurons in vivo. . Nature 503:(7474):11520
    [Crossref] [Google Scholar]
  157. Sparks FT, Liao Z, Li W, Grosmark A, Soltesz I, Losonczy A. 2020.. Hippocampal adult-born granule cells drive network activity in a mouse model of chronic temporal lobe epilepsy. . Nat. Commun. 11:(1):6138
    [Crossref] [Google Scholar]
  158. Stachenfeld KL, Botvinick MM, Gershman SJ. 2017.. The hippocampus as a predictive map. . Nat. Neurosci. 20:(11):164353
    [Crossref] [Google Scholar]
  159. Steinmetz NA, Aydin C, Lebedeva A, Okun M, Pachitariu M, et al. 2021.. Neuropixels 2.0: a miniaturized high-density probe for stable, long-term brain recordings. . Science 372:(6539):eabf4588
    [Crossref] [Google Scholar]
  160. Stelzer A, Simon G, Kovacs G, Rai R. 1994.. Synaptic disinhibition during maintenance of long-term potentiation in the CA1 hippocampal subfield. . PNAS 91:(8):305862
    [Crossref] [Google Scholar]
  161. Stelzer A, Slater NT, Ten Bruggencate G. 1987.. Activation of NMDA receptors blocks GABAergic inhibition in an in vitro model of epilepsy. . Nature 326:(6114):698701
    [Crossref] [Google Scholar]
  162. Sugden AU, Zaremba JD, Sugden LA, McGuire KL, Lutas A, et al. 2020.. Cortical reactivations of recent sensory experiences predict bidirectional network changes during learning. . Nat. Neurosci. 23:(8):98191
    [Crossref] [Google Scholar]
  163. Suh J, Foster DJ, Davoudi H, Wilson MA, Tonegawa S. 2013.. Impaired hippocampal ripple-associated replay in a mouse model of schizophrenia. . Neuron 80:(2):48493
    [Crossref] [Google Scholar]
  164. Sun W, Advani M, Spruston N, Saxe A, Fitzgerald JE. 2023.. Organizing memories for generalization in complementary learning systems. . Nat. Neurosci. 26::143848
    [Crossref] [Google Scholar]
  165. Taxidis J, Coombes S, Mason R, Owen MR. 2012.. Modeling sharp wave-ripple complexes through a CA3–CA1 network model with chemical synapses. . Hippocampus 22:(5):9951017
    [Crossref] [Google Scholar]
  166. Terada S, Geiller T, Liao Z, O'Hare J, Vancura B, Losonczy A. 2022.. Adaptive stimulus selection for consolidation in the hippocampus. . Nature 601:(7892):24044
    [Crossref] [Google Scholar]
  167. Tolman EC. 1932.. Purposive Behavior in Animals and Men. London:: Century
    [Google Scholar]
  168. Tolman EC. 1948.. Cognitive maps in rats and men. . Psychol. Rev. 55:(4):189208
    [Crossref] [Google Scholar]
  169. Tulving E. 2002.. Episodic memory: from mind to brain. . Annu. Rev. Psychol. 53::125
    [Crossref] [Google Scholar]
  170. Turi GF, Li WK, Chavlis S, Pandi I, O'Hare J, et al. 2019.. Vasoactive intestinal polypeptide-expressing interneurons in the hippocampus support goal-oriented spatial learning. . Neuron 101:(6):115065.e8
    [Crossref] [Google Scholar]
  171. Turner G, Onysk J. 2022.. The hippocampus may support context retrieval in one-shot learning about pain. . J. Neurosci. 42:(10):188385
    [Crossref] [Google Scholar]
  172. Tzilivaki A, Tukker JJ, Maier N, Poirazi P, Sammons RP, Schmitz D. 2023.. Hippocampal GABAergic interneurons and memory. . Neuron 111:(20):315475
    [Crossref] [Google Scholar]
  173. Ujfalussy BB, Makara JK, Lengyel M, Branco T. 2018.. Global and multiplexed dendritic computations under in vivo-like conditions. . Neuron 100:(3):57992.e5
    [Crossref] [Google Scholar]
  174. Ulanovsky N, Moss CF. 2007.. Hippocampal cellular and network activity in freely moving echolocating bats. . Nat. Neurosci. 10:(2):22433
    [Crossref] [Google Scholar]
  175. Vaidya SP, Chitwood RA, Magee JC. 2023.. The formation of an expanding memory representation in the hippocampus. . bioRxiv 2023.02.01.526663. https://doi.org/10.1101/2023.02.01.526663
  176. Van Kesteren MT, Brown TI, Wagner AD. 2018.. Learned spatial schemas and prospective hippocampal activity support navigation after one-shot learning. . Front. Hum. Neurosci. 12::486
    [Crossref] [Google Scholar]
  177. Vancura B, Geiller T, Grosmark A, Zhao V, Losonczy A. 2023.. Inhibitory control of sharp-wave ripple duration during learning in hippocampal recurrent networks. . Nat. Neurosci. 26::78897
    [Crossref] [Google Scholar]
  178. Vaz AP, Inati SK, Brunel N, Zaghloul KA. 2019.. Coupled ripple oscillations between the medial temporal lobe and neocortex retrieve human memory. . Science 363:(6430):97578
    [Crossref] [Google Scholar]
  179. Villette V, Chavarha M, Dimov IK, Bradley J, Pradhan L, et al. 2019.. Ultrafast two-photon imaging of a high-gain voltage indicator in awake behaving mice. . Cell 179:(7):1590608.e23
    [Crossref] [Google Scholar]
  180. Vinyals O, Blundell C, Lillicrap T, Kavukcuoglu K, Wierstra D, et al. 2016.. Matching networks for one shot learning. . Adv. Neural Inform. Proc. Syst. 29:. https://proceedings.neurips.cc/paper_files/paper/2016/file/90e1357833654983612fb05e3ec9148c-Paper.pdf
    [Google Scholar]
  181. Vogels TP, Froemke RC, Doyon N, Gilson M, Haas JS, et al. 2013.. Inhibitory synaptic plasticity: spike timing-dependence and putative network function. . Front. Neural Circuits 7::119
    [Crossref] [Google Scholar]
  182. Vogels TP, Sprekeler H, Zenke F, Clopath C, Gerstner W. 2011.. Inhibitory plasticity balances excitation and inhibition in sensory pathways and memory networks. . Science 334:(6062):156973
    [Crossref] [Google Scholar]
  183. Wang M, Foster DJ, Pfeiffer BE. 2020.. Alternating sequences of future and past behavior encoded within hippocampal theta oscillations. . Science 370:(6513):24750
    [Crossref] [Google Scholar]
  184. Whittington JC, McCaffary D, Bakermans JJ, Behrens TE. 2022.. How to build a cognitive map. . Nat. Neurosci. 25:(10):125772
    [Crossref] [Google Scholar]
  185. Whittington JC, Muller TH, Mark S, Chen G, Barry C, et al. 2020.. The Tolman-Eichenbaum machine: unifying space and relational memory through generalization in the hippocampal formation. . Cell 183:(5):124963
    [Crossref] [Google Scholar]
  186. Widloski J, Foster DJ. 2022.. Flexible rerouting of hippocampal replay sequences around changing barriers in the absence of global place field remapping. . Neuron 110:(9):154758
    [Crossref] [Google Scholar]
  187. Wikenheiser AM, Redish AD. 2015.. Hippocampal theta sequences reflect current goals. . Nat. Neurosci. 18:(2):28994
    [Crossref] [Google Scholar]
  188. Wittkuhn L, Chien S, Hall-McMaster S, Schuck NW. 2021.. Replay in minds and machines. . Neurosci. Biobehav. Rev. 129::36788
    [Crossref] [Google Scholar]
  189. Wu Z, Lin D, Li Y. 2022.. Pushing the frontiers: tools for monitoring neurotransmitters and neuromodulators. . Nat. Rev. Neurosci. 23:(5):25774
    [Crossref] [Google Scholar]
  190. Xiao K, Li Y, Chitwood RA, Magee JC. 2023.. A critical role for CaMKII in behavioral timescale synaptic plasticity in hippocampal CA1 pyramidal neurons. . Sci. Adv. 9:(36):eadi3088
    [Crossref] [Google Scholar]
  191. Zaremba JD, Diamantopoulou A, Danielson NB, Grosmark AD, Kaifosh PW, et al. 2017.. Impaired hippocampal place cell dynamics in a mouse model of the 22q11.2 deletion. . Nat. Neurosci. 20:(11):161223
    [Crossref] [Google Scholar]
  192. Zhang Y, Rózsa M, Liang Y, Bushey D, Wei Z, et al. 2023.. Fast and sensitive GCaMP calcium indicators for imaging neural populations. . Nature 615:(7954):88491
    [Crossref] [Google Scholar]
  193. Zhao X, Hsu CL, Spruston N. 2022.. Rapid synaptic plasticity contributes to a learned conjunctive code of position and choice-related information in the hippocampus. . Neuron 110:(1):96108
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-neuro-102423-100258
Loading
/content/journals/10.1146/annurev-neuro-102423-100258
Loading

Data & Media loading...

Supplemental Materials

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error