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Theta phase precession emerges from a hybrid computational model of a CA3 place cell

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Abstract

The origins and functional significance of theta phase precession in the hippocampus remain obscure, in part, because of the difficulty of reproducing hippocampal place cell firing in experimental settings where the biophysical underpinnings can be examined in detail. The present study concerns a neurobiologically based computational model of the emergence of theta phase precession in which the responses of a single model CA3 pyramidal cell are examined in the context of stimulation by realistic afferent spike trains including those of place cells in entorhinal cortex, dentate gyrus, and other CA3 pyramidal cells. Spike-timing dependent plasticity in the model CA3 pyramidal cell leads to a spatially correlated associational synaptic drive that subsequently creates a spatially asymmetric expansion of the model cell’s place field. Following an initial training period, theta phase precession can be seen in the firing patterns of the model CA3 pyramidal cell. Through selective manipulations of the model it is possible to decompose theta phase precession in CA3 into the separate contributing factors of inheritance from upstream afferents in the dentate gyrus and entorhinal cortex, the interaction of synaptically controlled increasing afferent drive with phasic inhibition, and the theta phase difference between dentate gyrus granule cell and CA3 pyramidal cell activity. In the context of a single CA3 pyramidal cell, the model shows that each of these factors plays a role in theta phase precession within CA3 and suggests that no one single factor offers a complete explanation of the phenomenon. The model also shows parallels between theta phase encoding and pattern completion within the CA3 autoassociative network.

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References

  • Amaral DG, Ishizuka N, Claiborne B (1990) Neurons, numbers and the hippocampal network. Prog Brain Res 83:1–11

    Article  PubMed  CAS  Google Scholar 

  • Best PJ, White AM, Minai A (2001) Spatial processing in the brain: the activity of hippocampal place cells. Annu Rev Neurosci 24:459–486

    Article  PubMed  CAS  Google Scholar 

  • Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18:10464–10472

    PubMed  CAS  Google Scholar 

  • Bose A, Booth V, Recce M (2001) A temporal mechanism for generating the phase precession of hippocampal place cells. J Comput Neurosci 5:9–30

    Google Scholar 

  • Bose A, Reece M (2001) Phase precession and phase-locking of hippocampal pyramidal cells. Hippocampus 11:204–215

    Article  PubMed  CAS  Google Scholar 

  • Buzsáki G (2002) Theta oscillations in the hippocampus. Neuron 33:325–340

    Article  PubMed  Google Scholar 

  • Debanne D, Gähwiler BH, Thompson SM (1998) Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J Physiol 507:237–247

    Article  PubMed  CAS  Google Scholar 

  • Dittman JS, Kreitzer AC, Regehr WG (2000). Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J Neurosci 20:1374–1385

    PubMed  CAS  Google Scholar 

  • Fisher NI (1995) Statistical analysis of circular data. Cambridge University Press, New York

    Google Scholar 

  • Fox SE, Wolfson S, Ranck JB Jr (1986) Hippocampal theta rhythm and firing of neurons in walking and urethane anesthetized rats. Exp Brain Res 62:495–508

    Article  PubMed  CAS  Google Scholar 

  • Fyhn M, Molden S, Witter MP, Moser EI, Moser MB (2004) Spatial representation in the entorhinal cortex. Science 305:1258–1264

    Article  PubMed  CAS  Google Scholar 

  • Giovannini MG, Rakovska A, Benton RS, Pazzagli M, Bianchi L, Pepeu G (2001) Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats. Neuroscience 106(1):43–53

    Article  PubMed  CAS  Google Scholar 

  • Gluck MA, Myers CE (2001) Gateway to memory. MIT Press, Cambridge, MA

    Google Scholar 

  • Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005). Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–806

    Article  PubMed  CAS  Google Scholar 

  • Hafting T, Fyhn MH, Moser M, Moser EI (2006) Phase precession and phase locking in entorhinal grid cells. Program No. 68.8. 2006 Neuroscience Meeting Planner. Society for Neuroscience, Atlanta, GA

  • Harris KD, Henze DA, Hirase H, Leinekugel X, Dragoi G, Czurkó A, Buzsáki G (2002) Spike train dyamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417:738–741

    Article  PubMed  CAS  Google Scholar 

  • Hasselmo ME (2005) What is the function of the hippocampal theta rhythm?—Linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus 15:936–949

    Article  PubMed  Google Scholar 

  • Hasselmo ME, Schnell E, Barkai E (1995) Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3. J Neurosci 15:5249–5262

    PubMed  CAS  Google Scholar 

  • Henze DA, Wittner L, Buzsáki G (2002) Single granule cell reliably discharge targets in the CA3 hippocampal network in vivo. Nat Neurosci 5(8):790–795

    PubMed  CAS  Google Scholar 

  • Huxter J, Burgess N, O’Keefe J (2003) Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425:828–832

    Article  PubMed  CAS  Google Scholar 

  • Jensen O, Lisman JE (1996) Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn Mem 3:279–287

    Article  PubMed  CAS  Google Scholar 

  • Johnston D, Amaral DG (1998) Hippocampus. In: Shepherd GM (ed) The synaptic organization of the brain, 4th edn. Oxford University Press, New York

    Google Scholar 

  • Jones MW, Wilson MA (2005) Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm. Hippocampus 15:867–873

    Article  PubMed  Google Scholar 

  • Káli S, Dayan P (2000) The involvement of recurrent connections in area CA3 in establishing the properties of place fields: a model. J Neurosci 20:7463–7477

    PubMed  Google Scholar 

  • Kamondi A, Ascády L, Wang XJ, Buzsáki G (1998) Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 8:244–261

    Article  PubMed  CAS  Google Scholar 

  • Klausberger T, Magill PJ, Márton LF, Roberts JDB, Cobden PM, Buzsáki G, Somogyi P (2003) Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844–848

    Article  PubMed  CAS  Google Scholar 

  • Klausberger T, Márton LF, Baude A, Roberts JDB, Magill PJ, Somogyi P (2004) Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat Neurosci 7:41–47

    Article  PubMed  CAS  Google Scholar 

  • Marr D (1971) Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci 262(841):23–81

    Article  PubMed  CAS  Google Scholar 

  • Mascagni MV, Sherman AS (1998) Numerical methods in neuronal modeling. In: Koch C, Segev I (eds) Methods in neuron modeling: from ions to networks, 2nd edn. MIT Press, Cambridge, MA

    Google Scholar 

  • Matsumoto M, Nishimura T (1998) Mersenne twister: a 623-dimensionally equidistributed uniform pseudorandom number generator. ACM Trans. Model Comput Simulat 8:3–30. http://www.math.sci.hiroshima-u.ac.jp/∼m-mat/MT/emt.html. Cited 23 July 2004

  • Mehta MR, Barnes CA, McNaughton BL (1997) Experience-dependent, asymmetric expansion of hippocampal place fields. Proc Natl Acad Sci USA 94:8918–8921

    Article  PubMed  CAS  Google Scholar 

  • Mehta MR, Lee AK, Wilson MA (2002) Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417:741–746

    Article  PubMed  CAS  Google Scholar 

  • Mehta MR, Quirk MC, Wilson MA (2000) Experience-dependent asymmetric shape of hippocampal receptive fields. Neuron 25:707–715

    Article  PubMed  CAS  Google Scholar 

  • Muller R (1996) A quarter of a century of place cells. Neuron 17:813–822

    Article  PubMed  CAS  Google Scholar 

  • O’Keefe J, Burgess N (2005) Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells. Hippocampus 15:853–866

    Article  PubMed  Google Scholar 

  • O’Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171–175

    Article  PubMed  CAS  Google Scholar 

  • O’Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3(3):317–330

    Article  PubMed  CAS  Google Scholar 

  • O’Reilly RC, McClelland JL (1994) Hippocampal conjunctive encoding, storage and recall: avoiding a trade-off. Hippocampus 4:661–682

    Article  PubMed  CAS  Google Scholar 

  • Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1992) Numerical recipes in C. 2nd edn. Cambridge University Press, New York

    Google Scholar 

  • Quirk GJ, Muller RU, Kubie JL, Ranck JB Jr (1992) The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells. J Neurosci 12:1945–1963

    PubMed  CAS  Google Scholar 

  • Rolls ET, Treves A (1998) Neural networks and brain function. Oxford University Press, New York

    Google Scholar 

  • Samsonovich A, McNaughton BL (1997) Path integration and cognitive mapping in a continuous attractor neural network model. J Neurosci 17:5900–5920

    PubMed  CAS  Google Scholar 

  • Segev I, Burke RE (1998) Compartmental models of complex neurons. In: Koch C, Segev I (eds) Methods in neuron modeling: from ions to networks, 2nd edn. MIT Press, Cambridge, MA

    Google Scholar 

  • Sjöström PJ, Turrigiano GG, Nelson SB (2001) Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32:1149–1164

    Article  PubMed  Google Scholar 

  • Skaggs WE, McNaughton BL, Wilson MA, Barnes CA (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149–172

    Article  PubMed  CAS  Google Scholar 

  • Stewart M, Quirk GJ, Barry M, Fox SE (1992) Firing relations of medial entorhinal neurons to the hippocampal theta rhythm in urethane anesthetized and walking rats. Exp Brain Res 90:21–28

    Article  PubMed  CAS  Google Scholar 

  • Tsodyks MV, Skaggs WE, Sejnowski TJ, McNaughton BL (1996) Population dynamics and theta rhythm phase precession of hippocampal place cell firing: a spiking neuron model. Hippocampus 6:271–280

    Article  PubMed  CAS  Google Scholar 

  • Turner DA, Li XG, Pyapali GK, Ylinen A, Buzsáki G (1995) Morphometric and electrical properties of reconstructed hippocampal CA3 neurons recorded in vivo. J Comp Neurol 356:580–594. http://neuron.duke.edu/cells/. Cited 7 April 2004

    Google Scholar 

  • Vazdarjanova A, Guzowski JF (2004) Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J Neurosci 24:6489–6496

    Article  PubMed  CAS  Google Scholar 

  • Wagatsuma H, Yamaguchi Y (2007) Neural dynamics of the cognitive map in the hippocampus. Cogn Neurodyn (in press) DOI 10.1007/s11571-006-9013-6

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

    PubMed  CAS  Google Scholar 

  • Weast RC (ed.) (1964) C.R.C. Standard mathematical tables, 13th edn. The Chemical Rubber Co., Cleveland, OH

  • Wilson MA, McNaughton BL (1993) Dynamics of the hippocampal ensemble code for space. Science 261(5124):1055–1058

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi Y (2003) A theory of hippocampal memory based on theta phase precession. Biol Cybern 89:1–9

    PubMed  Google Scholar 

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Acknowledgments

We would like to thank Professors Kim Blackwell, Giorgio Ascoli, and James Gentle for the advice they generously provided during the conduct of this research. We also gratefully acknowledge the suggestions of multiple anonymous reviewers. JLB was supported by a fellowship from the Krasnow Institute of Advanced Study.

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Correspondence to James L. Olds.

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Baker, J.L., Olds, J.L. Theta phase precession emerges from a hybrid computational model of a CA3 place cell. Cogn Neurodyn 1, 237–248 (2007). https://doi.org/10.1007/s11571-007-9018-9

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