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Models and Theoretical Frameworks for Hippocampal and Entorhinal Cortex Function in Memory and Navigation

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Analysis and Modeling of Coordinated Multi-neuronal Activity

Abstract

The hippocampus and related medial temporal lobe structures subserve both navigation and memory. These seemingly disparate functions have been characterized extensively at the cellular, network, and systems levels, leading to models of the hippocampus at different levels of abstraction. Mechanistic models relating neural activity to spatial and/or mnemonic function often rely on representations of individual neurons, synapses, or network structure, while theoretical models of the hippocampus incorporate and attempt to reconcile aspects of the hippocampal codes for space and/or past experience. In this chapter we first provide a brief introduction to the research history and concepts relating the hippocampus to memory and navigation, incorporating an overview of some of the influential models and theories that have been proposed to capture aspects of the hippocampus’s role in mnemonic or spatial processing. We then describe the anatomy of the hippocampal-entorhinal circuit, emphasizing the rough division of labor across hippocampal subregions and entorhinal cortex related to the computational demands of navigation and episodic memory. Next, we discuss the role of oscillations and cross-frequency coupling in coordinating neural activity to encode spatially and temporally sequenced information about ongoing or remembered experience. Finally, we discuss an important conceptual framework that links numerous experimental observations of hippocampal spatial and mnemonic function based on commonalities between map-based and self-motion-based navigation strategies on the one hand and semantic and episodic memory on the other.

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References

  1. Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Pychiatry. 1957;20:11–21.

    CAS  Google Scholar 

  2. Zola-Morgan S, Squire LR, Amaral DG. Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci. 1986;6(10):2950–67.

    CAS  PubMed  Google Scholar 

  3. Eichenbaum H, Cohen NJ. From conditioning to conscious recollection. New York: Oxford University Press; 2003.

    Google Scholar 

  4. Corkin S. What’s new with the amnesic patient HM? Nat Rev Neurosci. 2002;3(2):153–60.

    CAS  PubMed  Google Scholar 

  5. Corkin S. Acquisition of motor skill after bilateral medial temporal lobe excision. Neuropsychologia. 1968;6(3):255–65.

    Google Scholar 

  6. Schacter DL, Tulving E. Memory systems 1994. Boston, MA: MIT Press; 1994. 415 p.

    Google Scholar 

  7. Graf P, Squire LR, Mandler G. The information that amnesic patients do not forget. J Exp Psychol Learn Mem Cogn. 1984;10(1):164–78.

    CAS  PubMed  Google Scholar 

  8. Kesner RP, Gilbert PE, Barua LA. The role of the hippocampus in memory for the temporal order of a sequence of odors. Behav Neurosci. 2002;116(2):286–90.

    PubMed  Google Scholar 

  9. Agster KL, Fortin NJ, Eichenbaum H. The hippocampus and disambiguation of overlapping sequences. J Neurosci. 2002;22(13):5760–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  10. Takehara K, Kawahara S, Kirino Y. Time-dependent reorganization of the brain components underlying memory retention in trace eyeblink conditioning. J Neurosci. 2003;23(30):9897–905.

    CAS  PubMed  Google Scholar 

  11. Hasselmo ME, Wyble BP. Free recall and recognition in a network model of the hippocampus: simulating effects of scopolamine on human memory function. Behav Brain Res. 1997;89(1–2):1–34.

    CAS  PubMed  Google Scholar 

  12. Norman KA, O’Reilly RC. Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach. Psychol Rev. 2003;110(4):611–46.

    PubMed  Google Scholar 

  13. Jensen O, Lisman JE. Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn Mem. 1996;3:279–87.

    CAS  PubMed  Google Scholar 

  14. Tsodyks MV, Skaggs WE, Sejnowski TJ, McNaughton BL. Population dynamics and theta rhythm phase precession of hippocampal place cell firing: a spiking neuron model. Hippocampus. 1996;6(3):271–80.

    CAS  PubMed  Google Scholar 

  15. Wallenstein GV, Hasselmo ME. GABAergic modulation of hippocampal population activity: sequence learning, place field development, and the phase precession effect. J Neurophysiol. 1997;78(1):393–408.

    CAS  PubMed  Google Scholar 

  16. Lisman JE. Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron. 1999;22(2):233–42.

    CAS  PubMed  Google Scholar 

  17. Hasselmo ME. A model of episodic memory: mental time travel along encoded trajectories using grid cells. Neurobiol Learn Mem. 2009;92(4):559–73.

    PubMed Central  PubMed  Google Scholar 

  18. Alvarez P, Squire LR. Memory consolidation and the medial temporal lobe: a simple network model. Proc Natl Acad Sci U S A. 1994;91(15):7041–5.

    CAS  PubMed Central  PubMed  Google Scholar 

  19. McClelland JL, McNaughton BL, O'Reilly RC. 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. 1995;102(3):419–57.

    CAS  PubMed  Google Scholar 

  20. Teyler TJ, Discenna P. The hippocampal memory indexing theory. Behav Neurosci. 1986;100(2):147–54.

    CAS  PubMed  Google Scholar 

  21. Teyler TJ, Rudy JW. The hippocampal indexing theory and episodic memory: updating the index. Hippocampus. 2007;17(12):1158–69.

    PubMed  Google Scholar 

  22. Ribot T. Diseases of the memory: an essay in the positive psychology. New York, NY: D. Appleton and Company; 1882. 209 p.

    Google Scholar 

  23. O’Keefe J, Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971;34:171–5.

    PubMed  Google Scholar 

  24. O’Keefe J, Nadel L. The hippocampus as a cognitive map. Oxford, UK: Oxford University Press; 1978.

    Google Scholar 

  25. Moser EI, Kropff E, Moser MB. Place cells, grid cells, and the brain’s spatial representation system. Annual review of neuroscience. vol. 31. Palo Alto: Annual Reviews; 2008. pp. 69–89.

    Google Scholar 

  26. O’Keefe J, Burgess N. Geometric determinants of the place fields of hippocampal neurons. Nature. 1996;381:425–8.

    PubMed  Google Scholar 

  27. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB. Path integration and the neural basis of the “cognitive map”. Nat Rev Neurosci. 2006;7(8):663–78.

    CAS  PubMed  Google Scholar 

  28. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. Microstructure of a spatial map in the entorhinal cortex. Nature. 2005;436(7052):801–6.

    CAS  PubMed  Google Scholar 

  29. Domnisoru C, Kinkhabwala AA, Tank DW. Membrane potential dynamics of grid cells. Nature. 2013;495(7440):199–204.

    CAS  PubMed Central  PubMed  Google Scholar 

  30. Schmidt-Hieber C, Hausser M. Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nat Neurosci. 2013;16(3):325–31.

    CAS  PubMed  Google Scholar 

  31. Hasselmo ME, Brandon MP. A model combining oscillations and attractor dynamics for generation of grid cell firing. Front Neural Circuits. 2012;6:13.

    Google Scholar 

  32. Bush D, Burgess N. A hybrid oscillatory interference/continuous attractor network model of grid cell firing. J Neurosci. 2014;34(14):5065–79.

    CAS  PubMed Central  PubMed  Google Scholar 

  33. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser MB, et al. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science. 2006;312(5774):758–62.

    CAS  PubMed  Google Scholar 

  34. Taube JS, Muller RU, Ranck Jr JB. Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J Neurosci. 1990;10(2):436–47.

    CAS  PubMed  Google Scholar 

  35. Taube JS, Muller RU, Ranck Jr JB. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci. 1990;10(2):420–35.

    CAS  PubMed  Google Scholar 

  36. Cho J, Sharp PE. Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. Behav Neurosci. 2001;115(1):3–25.

    CAS  PubMed  Google Scholar 

  37. Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP, Moser EI, et al. Grid cells in pre- and parasubiculum. Nat Neurosci. 2010;13(8):987–94.

    CAS  PubMed  Google Scholar 

  38. Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI. Representation of geometric borders in the entorhinal cortex. Science. 2008;322(5909):1865–8.

    CAS  PubMed  Google Scholar 

  39. Lever C, Burton S, Jeewajee A, O’Keefe J, Burgess N. Boundary vector cells in the subiculum of the hippocampal formation. J Neurosci. 2009;29(31):9771–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  40. Nitz DA. Spaces within spaces: rat parietal cortex neurons register position across three reference frames. Nat Neurosci. 2012;15(10):1365–7.

    CAS  PubMed  Google Scholar 

  41. Derdikman D, Whitlock JR, Tsao A, Fyhn M, Hafting T, Moser MB, et al. Fragmentation of grid cell maps in a multicompartment environment. Nat Neurosci. 2009;12(10):1325–32.

    CAS  PubMed  Google Scholar 

  42. Dickinson JR, Weible AP, Rowland DC, Deblander L, Wu H, Kentros CG. Transgenic activation of the same entorhinal inputs leads to the same hippocampal network response. Soc Neurosci Abstr. 2012;397(22).

    Google Scholar 

  43. Yanovich Y, Weible A, Deblander L, Roth BL, Kentros CG. Inactivation of layer II neurons in the medial entorhinal cortex causes remapping of CA1 place fields. Soc Neurosci Abstr. 2012;293:08.

    Google Scholar 

  44. Koenig J, Linder AN, Leutgeb JK, Leutgeb S. The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science. 2011;332(6029):592–5.

    CAS  PubMed  Google Scholar 

  45. Brandon MP, Koenig J, Hasselmo ME, Leutgeb JK, Leutgeb S. Septal inactivation eliminates grid cell spatial periodicity and causes instability of hippocampal place cells in novel environments. Soc Neurosci Abstr. 2012;203(05).

    Google Scholar 

  46. Brandon Mark P, Koenig J, Leutgeb Jill K, Leutgeb S. New and distinct hippocampal place codes are generated in a new environment during septal inactivation. Neuron. 2014;82(4):789–96.

    CAS  PubMed  Google Scholar 

  47. Bonnevie T, Dunn B, Fyhn M, Hafting T, Derdikman D, Kubie JL, et al. Grid cells require excitatory drive from the hippocampus. Nat Neurosci. 2013;16(3):309–17.

    CAS  PubMed  Google Scholar 

  48. Muller RU, Stead M. Hippocampal place cells connected by Hebbian synapses can solve spatial problems. Hippocampus. 1996;6:709–19.

    CAS  PubMed  Google Scholar 

  49. Touretzky DS, Redish AD. Theory of rodent navigation based on interacting representations of space. Hippocampus. 1996;6(3):247–70.

    CAS  PubMed  Google Scholar 

  50. Burgess N, Donnett JG, Jeffery KJ, O’Keefe J. Robotic and neuronal simulation of the hippocampus and rat navigation. Philos Trans R Soc Lond B Biol Sci. 1997;352(1360):1535–43.

    CAS  PubMed Central  PubMed  Google Scholar 

  51. Redish AD, Touretzky DS. The role of the hippocampus in solving the Morris water maze. Neural Comput. 1998;10(1):73–111.

    CAS  PubMed  Google Scholar 

  52. Foster DJ, Morris RG, Dayan P. A model of hippocampally dependent navigation, using the temporal difference learning rule. Hippocampus. 2000;10(1):1–16.

    CAS  PubMed  Google Scholar 

  53. Hasselmo ME, Eichenbaum H. Hippocampal mechanisms for the context-dependent retrieval of episodes. Neural Netw. 2005;18(9):1172–90.

    PubMed Central  PubMed  Google Scholar 

  54. Johnson A, Redish AD. Hippocampal replay contributes to within session learning in a temporal difference reinforcement learning model. Neural Netw. 2005;18(9):1163–71.

    PubMed  Google Scholar 

  55. Foster DJ, Wilson MA. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature. 2006;440(7084):680–3.

    CAS  PubMed  Google Scholar 

  56. Sharp PE. Computer simulation of hippocampal place cells. Psychobiology. 1991;19:103–15.

    Google Scholar 

  57. Arleo A, Gerstner W. Spatial cognition and neuro-mimetic navigation: a model of hippocampal place cell activity. Biol Cybern. 2000;83(3):287–99.

    CAS  PubMed  Google Scholar 

  58. Shapiro ML, Hetherington PA. A simple network model simulates hippocampal place fields: parametric analyses and physiological predictions. Behav Neurosci. 1993;107(1):34–50.

    CAS  PubMed  Google Scholar 

  59. Samsonovich A, McNaughton BL. Path integration and cognitive mapping in a continuous attractor neural network model. J Neurosci. 1997;17(15):5900–20.

    CAS  PubMed  Google Scholar 

  60. Redish AD. Beyond the cognitive map. Cambridge, MA: MIT Press; 1999.

    Google Scholar 

  61. Fuhs MC, Touretzky DS. A spin glass model of path integration in rat medial entorhinal cortex. J Neurosci. 2006;26(16):4266–76.

    CAS  PubMed  Google Scholar 

  62. Burgess N, Barry C, O’Keefe J. An oscillatory interference model of grid cell firing. Hippocampus. 2007;17(9):801–12.

    PubMed Central  PubMed  Google Scholar 

  63. Giocomo LM, Zilli EA, Fransen E, Hasselmo ME. Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science. 2007;315(5819):1719–22.

    CAS  PubMed Central  PubMed  Google Scholar 

  64. Kropff E, Treves A. The emergence of grid cells: Intelligent design or just adaptation? Hippocampus. 2008;18(12):1256–69.

    PubMed  Google Scholar 

  65. Solstad T, Moser EI, Einevoll GT. From grid cells to place cells: a mathematical model. Hippocampus. 2006;16(12):1026–31.

    PubMed  Google Scholar 

  66. O’Keefe J, Burgess N. Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells. Hippocampus. 2005;15(7):853–66.

    PubMed Central  PubMed  Google Scholar 

  67. Barry C, Lever C, Hayman R, Hartley T, Burton S, O’Keefe J, et al. The boundary vector cell model of place cell firing and spatial memory. Rev Neurosci. 2006;17(1–2):71–97.

    PubMed Central  PubMed  Google Scholar 

  68. Blum KI, Abbott LF. A model of spatial map formation in the hippocampus of the rat. Neural Comput. 1996;8(1):85–93.

    CAS  PubMed  Google Scholar 

  69. Mehta MR, Lee AK, Wilson MA. Role of experience and oscillations in transforming a rate code into a temporal code. Nature. 2002;417(6890):741–6.

    CAS  PubMed  Google Scholar 

  70. Lavenex P, Amaral DG. Hippocampal-neorcortical interaction: a hierarchy of associativity. Hippocampus. 2000;10:420–30.

    CAS  PubMed  Google Scholar 

  71. Marr D. Simple memory: a theory for archicortex. Phil Trans Roy Soc B. 1971;B262:23–81.

    Google Scholar 

  72. Rapp PR, Gallagher M. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc Natl Acad Sci U S A. 1996;93(18):9926–30.

    CAS  PubMed Central  PubMed  Google Scholar 

  73. West MJ, Slomianka L, Gundersen HJG. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec. 1991;231(4):482–97.

    CAS  PubMed  Google Scholar 

  74. McNaughton BL. Associative pattern completion in hippocampal circuits: new evidence and new questions. Brain Res Rev. 1991;16:193–220.

    Google Scholar 

  75. Treves A, Rolls ET. Computational analysis of the role of the hippocampus in memory. Hippocampus. 1994;4(3):374–91.

    CAS  PubMed  Google Scholar 

  76. O'Reilly RC, McClelland JL. Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus. 1994;4(6):661–82.

    PubMed  Google Scholar 

  77. Treves A, Tashiro A, Witter MP, Moser EI. What is the mammalian dentate gyrus good for? Neuroscience. 2008;154(4):1155–72.

    CAS  PubMed  Google Scholar 

  78. Becker S. A computational principle for hippocampal learning and neurogenesis. Hippocampus. 2005;15(6):722–38.

    PubMed  Google Scholar 

  79. Aimone JB, Wiles J, Gage FH. Computational influence of adult neurogenesis on memory encoding. Neuron. 2009;61(2):187–202.

    CAS  PubMed Central  PubMed  Google Scholar 

  80. Doboli S, Minai AA, Best PJ. Latent attractors: a model for context-dependent place representations in the hippocampus. Neural Comput. 2000;12(5):1009–43.

    CAS  PubMed  Google Scholar 

  81. McNaughton BL, Morris RGM. Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci. 1987;10:408–15.

    Google Scholar 

  82. Levy WB. A sequence predicting CA3 is a flexible associator that learns and uses context to solve hippocampal-like tasks. Hippocampus. 1996;6(6):579–90.

    CAS  PubMed  Google Scholar 

  83. Treves A, Rolls ET. Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus. 1992;2(2):189–99.

    CAS  PubMed  Google Scholar 

  84. Hasselmo ME, Schnell E, Barkai E. Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3. J Neurosci. 1995;15(7 Pt 2):5249–62.

    CAS  PubMed  Google Scholar 

  85. Amit DJ, Gutfreund H, Sompolinsky H. Information storage in neural networks with low levels of activity. Phys Rev A. 1987;35(5):2293–303.

    PubMed  Google Scholar 

  86. Battaglia FP, Treves A. Attractor neural networks storing multiple space representations: a model for hippocampal place fields. Phys Rev E. 1998;58(6):7738–53.

    CAS  Google Scholar 

  87. Burak Y, Fiete IR. Accurate path integration in continuous attractor network models of grid cells. PLoS Comput Biol. 2009;5(2):e1000291.

    PubMed Central  PubMed  Google Scholar 

  88. Treves A. Computational constraints between retrieving the past and predicting the future, and the CA3-CA1 differentiation. Hippocampus. 2004;14(5):539–56.

    PubMed  Google Scholar 

  89. Gray JA. The neuropsychology of anxiety: an enquiry into the functions of the septo-hippocampal system. Oxford, UK: Oxford University Press; 1982.

    Google Scholar 

  90. Hasselmo ME, Schnell E. Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology. J Neurosci. 1994;14(6):3898–914.

    CAS  PubMed  Google Scholar 

  91. Sharp PE. Multiple spatial/behavioral correlates for cells in the rat postsubiculum: multiple regression analysis and comparison to other hippocampal areas. Cereb Cortex. 1996;6(2):238–59.

    CAS  PubMed  Google Scholar 

  92. Rolls ET, Treves A. Neural networks and brain function. New York: Oxford University Press; 1998.

    Google Scholar 

  93. Burgess N. Grid cells and theta as oscillatory interference: theory and predictions. Hippocampus. 2008;18(12):1157–74.

    PubMed Central  PubMed  Google Scholar 

  94. Hasselmo ME, Giocomo LM, Zilli EA. Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons. Hippocampus. 2007;17(12):1252–71.

    PubMed Central  PubMed  Google Scholar 

  95. Giocomo LM, Hasselmo ME. Time constants of h current in layer II stellate cells differ along the dorsal to ventral axis of medial entorhinal cortex. J Neurosci. 2008;28(38):9414–25.

    CAS  PubMed Central  PubMed  Google Scholar 

  96. Giocomo LM, Hasselmo ME. Knock-out of HCN1 subunit flattens dorsal-ventral frequency gradient of medial entorhinal neurons in adult mice. J Neurosci. 2009;29(23):7625–30.

    CAS  PubMed Central  PubMed  Google Scholar 

  97. Jeewajee A, Barry C, O’Keefe J, Burgess N. Grid cells and theta as oscillatory interference: electrophysiological data from freely moving rats. Hippocampus. 2008;18(12):1175–85.

    CAS  PubMed Central  PubMed  Google Scholar 

  98. Navratilova Z, Giocomo LM, Fellous JM, Hasselmo ME, McNaughton BL. Phase precession and variable spatial scaling in a periodic attractor map model of medial entorhinal grid cells with realistic after-spike dynamics. Hippocampus. 2012;22(4):772–89.

    PubMed  Google Scholar 

  99. Hasselmo ME. Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci. 1999;3(9):351–9.

    PubMed  Google Scholar 

  100. Denham MJ, Borisyuk RM. A model of theta rhythm production in the septal-hippocampal system and its modulation by ascending brain stem pathways. Hippocampus. 2000;10(6):698–716.

    CAS  PubMed  Google Scholar 

  101. Brandon MP, Bogaard AR, Libby CP, Connerney MA, Gupta K, Hasselmo ME. Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science. 2011;332(6029):595–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  102. Yartsev MM, Witter MP, Ulanovsky N. Grid cells without theta oscillations in the entorhinal cortex of bats. Nature. 2011;479(7371):103–7.

    CAS  PubMed  Google Scholar 

  103. Heys JG, MacLeod KM, Moss CF, Hasselmo ME. Bat and rat neurons differ in theta-frequency resonance despite similar coding of space. Science. 2013;340(6130):363–7.

    CAS  PubMed  Google Scholar 

  104. Green JD, Arduini AA. Hippocampal electrical activity and arousal. J Neurophysiol. 1954;17:533–57.

    CAS  PubMed  Google Scholar 

  105. Leung L-WS. Model of gradual phase shift of theta rhythm in the rat. J Neurophysiol. 1984;52:1051–65.

    CAS  PubMed  Google Scholar 

  106. Bland BH. The physiology and pharmacology of hippocampal-formation theta rhythms. Progr Neurobiol. 1986;26:1–54.

    CAS  Google Scholar 

  107. Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G. Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci. 1995;15(1 pt 1):47–60.

    CAS  PubMed  Google Scholar 

  108. Vinogradova OS. Expression, control, and probable functional significance of the neuronal theta-rhythm. Prog Neurobiol. 1995;45(6):523–83.

    CAS  PubMed  Google Scholar 

  109. Vertes RP, Kocsis B. Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience. 1997;81(4):893–926.

    CAS  PubMed  Google Scholar 

  110. Buzsaki G. Theta oscillations in the hippocampus. Neuron. 2002;33(3):325–40.

    CAS  PubMed  Google Scholar 

  111. Mizuseki K, Sirota A, Pastalkova E, Buzsaki G. Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron. 2009;64(2):267–80.

    CAS  PubMed Central  PubMed  Google Scholar 

  112. Boyce R, Glasgow SD, Adamantidis AR, Williams S. Optogenetic investigation of septal GABAergic modulation of hippocampal theta rhythm. Soc Neurosci Abstr. 2012;339(01).

    Google Scholar 

  113. Amilhon B, Huh C, Manseau F, Jackson J, Ducharme G, Goutagny R, et al. Intrinsic theta oscillators of the hippocampus are differentially controlled by parvalbumin and somatostatin interneurons. Soc Neurosci Abstr. 2012;339(02).

    Google Scholar 

  114. Bernstein JG, Boyden ES. Optogenetic tools for analyzing the neural circuits of behavior. Trends Cogn Sci. 2011;15(12):592–600.

    PubMed Central  PubMed  Google Scholar 

  115. Fenno L, Yizhar O, Deisseroth K. The development and application of optogenetics. In: Hyman SE, Jessell TM, Shatz CJ, Stevens CF, Zoghbi HY, editors. Annual review of neuroscience, vol. 34. Palo Alto: Annual Reviews; 2011. p. 389–412.

    Google Scholar 

  116. Melloni L, Molina C, Pena M, Torres D, Singer W, Rodriguez E. Synchronization of neural activity across cortical areas correlates with conscious perception. J Neurosci. 2007;27(11):2858–65.

    CAS  PubMed  Google Scholar 

  117. Gray CM, Konig P, Engel AK, Singer W. Oscillatory responses in cat visual cortex exhibit intercolumnar synchronization which reflects global stimulus properties. Nature. 1989;338(6213):334–7.

    CAS  PubMed  Google Scholar 

  118. Rodriguez E, George N, Lachaux JP, Martinerie J, Renault B, Varela FJ. Perception’s shadow: long-distance synchronization of human brain activity. Nature. 1999;397(6718):430–3.

    CAS  PubMed  Google Scholar 

  119. Engel AK, Fries P, Singer W. Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci. 2001;2(10):704–16.

    CAS  PubMed  Google Scholar 

  120. Lisman JE, Idiart MA. Storage of 7 +/− 2 short-term memories in oscillatory subcycles. Science. 1995;267(5203):1512–5.

    CAS  PubMed  Google Scholar 

  121. Jensen O, Lisman JE. Theta/gamma networks with slow NMDA channels learn sequences and encode episodic memory: role of NMDA channels in recall. Learn Mem. 1996;3:264–78.

    CAS  PubMed  Google Scholar 

  122. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus. 1996;6:149–72.

    CAS  PubMed  Google Scholar 

  123. O’Keefe J, Recce ML. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus. 1993;3:317–30.

    PubMed  Google Scholar 

  124. Lengyel M, Szatmary Z, Erdi P. Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing. Hippocampus. 2003;13(6):700–14.

    PubMed  Google Scholar 

  125. Bose A, Booth V, Recce M. A temporal mechanism for generating the phase precession of hippocampal place cells. J Comput Neurosci. 2000;9(1):5–30.

    CAS  PubMed  Google Scholar 

  126. Hasselmo ME. Grid cell mechanisms and function: contributions of entorhinal persistent spiking and phase resetting. Hippocampus. 2008;18(12):1213–29.

    PubMed Central  PubMed  Google Scholar 

  127. Kamondi A, Acsady L, Wang XJ, Buzsaki G. Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus. 1998;8(3):244–61.

    CAS  PubMed  Google Scholar 

  128. Harvey CD, Collman F, Dombeck DA, Tank DW. Intracellular dynamics of hippocampal place cells during virtual navigation. Nature. 2009;461(7266):941–6.

    CAS  PubMed Central  PubMed  Google Scholar 

  129. Leung LWS, Dasilva FHL, Wadman WJ. Spectral characteristics of the hippocampal EEG in the freely moving rat. Electroencephalogr Clin Neurophysiol. 1982;54(2):203–19.

    CAS  PubMed  Google Scholar 

  130. Chrobak JJ, Buzsaki G. Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci. 1998;18(1):388–98.

    CAS  PubMed  Google Scholar 

  131. Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, et al. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature. 2009;462(7271):353–7.

    CAS  PubMed  Google Scholar 

  132. Tort AB, Komorowski RW, Manns JR, Kopell NJ, Eichenbaum H. Theta-gamma coupling increases during the learning of item-context associations. Proc Natl Acad Sci U S A. 2009;106(49):20942–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  133. Shirvalkar PR, Rapp PR, Shapiro ML. Bidirectional changes to hippocampal theta-gamma comodulation predict memory for recent spatial episodes. Proc Natl Acad Sci U S A. 2010;107(15):7054–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  134. Miller GA. The magical number 7, plus or minus 2, some limits on our capacity for processing information. Psychol Rev. 1956;63(2):81–97.

    CAS  PubMed  Google Scholar 

  135. Sternberg S. High-speed scanning in human memory. Science. 1966;153:652–4.

    CAS  PubMed  Google Scholar 

  136. Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger CE, Fell J. Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc Natl Acad Sci U S A. 2010;107(7):3228–33.

    CAS  PubMed Central  PubMed  Google Scholar 

  137. Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, et al. High gamma power is phase-locked to theta oscillations in human neocortex. Science. 2006;313(5793):1626–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  138. Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, Buzsaki G. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron. 2008;60(4):683–97.

    CAS  PubMed Central  PubMed  Google Scholar 

  139. Buzsaki G, Moser EI. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci. 2013;16(2):130–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  140. Pastoll H, Solanka L, van Rossum MC, Nolan MF. Feedback inhibition enables theta-nested gamma oscillations and grid firing fields. Neuron. 2013;77(1):141–54.

    CAS  PubMed  Google Scholar 

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Correspondence to Nathan W. Schultheiss Ph.D. .

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Schultheiss, N.W., Hinman, J.R., Hasselmo, M.E. (2015). Models and Theoretical Frameworks for Hippocampal and Entorhinal Cortex Function in Memory and Navigation. In: Tatsuno, M. (eds) Analysis and Modeling of Coordinated Multi-neuronal Activity. Springer Series in Computational Neuroscience, vol 12. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1969-7_12

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