Computational Neuroscience: Hippocampus

  • Reference work entry
  • First Online:
Neuroscience in the 21st Century

Abstract

Extensive computational neuroscience research has addressed the functional role of the hippocampus and associated cortical structures. In this field, computational models of the hippocampus have simulated physiological phenomena ranging from single cell membrane potential dynamics to the spiking activity of neurons relative to network field potential oscillations. Other models have focused on simulating specific behavioral functions of the hippocampus including episodic memory, classical conditioning, and spatial memory. Starting with influential papers by Marr and by McNaughton and Morris, many studies have focused on basic functions of hippocampus including pattern separation in the dentate gyrus and pattern completion in region CA3. This theoretical framework has been the focus of a number of experimental tests over the years, including neurophysiological studies of patterns of neuronal activity in behaving rats. Research has also addressed network dynamics in the hippocampus including theta rhythm oscillations, theta phase precession, and the patterns of grid cell firing in entorhinal cortex.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
GBP 19.95
Price includes VAT (United Kingdom)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
GBP 449.99
Price includes VAT (United Kingdom)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
GBP 449.99
Price includes VAT (United Kingdom)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Agster KL, Fortin NJ, Eichenbaum H (2002) The hippocampus and disambiguation of overlap** sequences. J Neurosci 22:5760–5768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alvarez P, Squire LR (1994) Memory consolidation and the medial temporal lobe: a simple network model. Proc Natl Acad Sci U S A 91:7041–7045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amit DJ, Gutfreund H, Sompolinsky H (1987) Information storage in neural networks with low levels of activity. Phys Rev A 35:2293–2303

    Article  CAS  Google Scholar 

  • Anderson JA (1972) A simple neural network generating an interactive memory. Math Biosci 14:197–220

    Article  Google Scholar 

  • Arleo A, Gerstner W (2000) Spatial cognition and neuro-mimetic navigation: a model of hippocampal place cell activity. Biol Cybern 83:287–299

    Article  CAS  PubMed  Google Scholar 

  • Barry C, Lever C, Hayman R, Hartley T, Burton S, O’Keefe J, Jeffery K, Burgess N (2006) The boundary vector cell model of place cell firing and spatial memory. Rev Neurosci 17:71–97

    Article  PubMed  PubMed Central  Google Scholar 

  • Battaglia FP, Treves A (1998) Stable and rapid recurrent processing in realistic autoassociative memories. Neural Comput 10:431–450

    Article  CAS  PubMed  Google Scholar 

  • Becker S (2005) A computational principle for hippocampal learning and neurogenesis. Hippocampus 15:722–738

    Article  PubMed  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bliss TV, Lømo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Brankack J, Stewart M, Fox SE (1993) Current source density analysis of the hippocampal theta rhythm: associated sustained potentials and candidate synaptic generators. Brain Res 615:310–327

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Burgess N (2008) Grid cells and theta as oscillatory interference: theory and predictions. Hippocampus 18:1157–1174

    Article  PubMed  PubMed Central  Google Scholar 

  • Burgess N, Donnett JG, Jeffery KJ, O’Keefe J (1997) Robotic and neuronal simulation of the hippocampus and rat navigation. Philos Trans R Soc Lond B Biol Sci 352:1535–1543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burgess N, Barry C, O’Keefe J (2007) An oscillatory interference model of grid cell firing. Hippocampus 17:801–812

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Buzsaki G, Leung LW, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287:139–171

    Article  CAS  PubMed  Google Scholar 

  • Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI (2009) Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462:353–357

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Doboli S, Minai AA, Best PJ (2000) Latent attractors: a model for context-dependent place representations in the hippocampus. Neural Comput 12:1009–1043

    Article  CAS  PubMed  Google Scholar 

  • Eichenbaum H, Cohen NJ (2003) From conditioning to conscious recollection. Oxford University Press, New York

    Google Scholar 

  • Foster D, Morris RG, Dayan P (2000) Models of hippocampally dependent navigation using the temporal difference learning rule. Hippocampus 10:1–16

    Google Scholar 

  • Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440:680–683

    Article  CAS  PubMed  Google Scholar 

  • Fuhs MC, Touretzky DS (2006) A spin glass model of path integration in rat medial entorhinal cortex. J Neurosci 26:4266–4276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gerstner W, Abbott LF (1997) Learning navigational maps through potentiation and modulation of hippocampal place cells. J Comput Neurosci 4:79–94

    Article  CAS  PubMed  Google Scholar 

  • Giocomo LM, Hasselmo ME (2009) Knock-out of HCN1 subunit flattens dorsal-ventral frequency gradient of medial entorhinal neurons in adult mice. J Neurosci 29:7625–7630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giocomo LM, Zilli EA, Fransen E, Hasselmo ME (2007) Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science 315:1719–1722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gluck MA, Myers CE (1993) Hippocampal mediation of stimulus representation: a computational theory. Hippocampus 3:491–516

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Green JD, Arduini AA (1954) Hippocampal electrical activity and arousal. J Neurophysiol 17:533–557

    Article  CAS  PubMed  Google Scholar 

  • Grossberg S, Schmajuk NA (1989) Neural dynamics of adaptive timing and temporal discrimination during associative learning. Neural Netw 2:79–102

    Article  Google Scholar 

  • Harvey CD, Collman F, Dombeck DA, Tank DW (2009) Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461(7266):941–946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasselmo ME (1999) Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci 3:351–359

    Article  CAS  PubMed  Google Scholar 

  • Hasselmo ME (2008) Grid cell mechanisms and function: contributions of entorhinal persistent spiking and phase resetting. Hippocampus 18:1213–1229

    Article  PubMed  PubMed Central  Google Scholar 

  • Hasselmo ME (2009) A model of episodic memory: mental time travel along encoded trajectories using grid cells. Neurobiol Learn Mem 92:559–573

    Article  PubMed  PubMed Central  Google Scholar 

  • Hasselmo ME, Eichenbaum H (2005) Hippocampal mechanisms for the context-dependent retrieval of episodes. Neural Netw 18:1172–1190

    Article  PubMed  PubMed Central  Google Scholar 

  • Hasselmo ME, Schnell E (1994) Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology. J Neurosci 14:3898–3914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasselmo ME, Bodelon C, Wyble BP (2002) A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput 14:793–817

    Article  PubMed  Google Scholar 

  • Holmes WR, Levy WB (1990) Insights into associative long-term potentiation from computational models of NMDA receptor-mediated calcium influx and intracellular calcium concentration changes. J Neurophysiol 63:1148–1168

    Article  CAS  PubMed  Google Scholar 

  • Izhikevich EM (2003) Simple model of spiking neurons. IEEE Trans Neural Netw 14:1569–1572

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jensen O, Lisman JE (1996b) Novel lists of 7+/−2 known items can be reliably stored in an oscillatory short-term memory network: interaction with long-term memory. Learn Mem 3:257–263

    Article  CAS  PubMed  Google Scholar 

  • Johnson A, Redish AD (2005) Hippocampal replay contributes to within session learning in a temporal difference reinforcement learning model. Neural Netw 18:1163–1171

    Article  PubMed  Google Scholar 

  • Kamondi A, Acsady L, Wang XJ, Buzsaki 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  CAS  PubMed  Google Scholar 

  • Kelso SR, Ganong AH, Brown TH (1986) Hebbian synapses in hippocampus. Proc Natl Acad Sci U S A 83:5326–5330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kesner RP, Gilbert PE, Barua LA (2002) The role of the hippocampus in memory for the temporal order of a sequence of odors. Behav Neurosci 116:286–290

    Article  PubMed  Google Scholar 

  • Kohonen T (1972) Correlation matrix memories. IEEE Trans Comput C-21:353–359

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Lengyel M, Szatmary Z, Erdi P (2003) Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing. Hippocampus 13:700–714

    Article  PubMed  Google Scholar 

  • Leung L-WS (1984) Model of gradual phase shift of theta rhythm in the rat. J Neurophysiol 52:1051–1065

    Article  CAS  PubMed  Google Scholar 

  • Lever C, Burton S, Jeewajee A, O’Keefe J, Burgess N (2009) Boundary vector cells in the subiculum of the hippocampal formation. J Neurosci 29:9771–9777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levy WB (1996) A sequence predicting CA3 is a flexible associator that learns and uses context to solve hippocampal-like tasks. Hippocampus 6:579–590

    Article  CAS  PubMed  Google Scholar 

  • Levy WB, Steward O (1983) Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus. Neuroscience 8:791–797

    Article  CAS  PubMed  Google Scholar 

  • Lisman JE (1989) A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proc Natl Acad Sci U S A 86:9574–9578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lisman JE (1999) Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 22:233–242

    Article  CAS  PubMed  Google Scholar 

  • Marr D (1971) Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci B262:23–81

    Google Scholar 

  • 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 102:419–457

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • McNaughton BL, Morris RGM (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408–415

    Article  Google Scholar 

  • McNaughton BL, Douglas RM, Goddard GV (1978) Synaptic enhancement in fascia dentata: cooperativity among coactive afferents. Brain Res 157:277–293

    Article  CAS  PubMed  Google Scholar 

  • McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser M-B (2006) Path integration and the neural basis of the ‘cognitive map’. Nat Rev Neurosci 7:663–678

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Muller RU, Stead M (1996) Hippocampal place cells connected by Hebbian synapses can solve spatial problems. Hippocampus 6:709–719

    Article  CAS  PubMed  Google Scholar 

  • Norman KA, O’Reilly RC (2003) Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach. Psychol Rev 110:611–646

    Article  PubMed  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  PubMed Central  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  Google Scholar 

  • O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, Oxford, UK

    Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Redish AD (1999) Beyond the cognitive map. MIT Press, Cambridge, MA

    Book  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez P, Levy WB (2001) A model of hippocampal activity in trace conditioning: where’s the trace? Behav Neurosci 115(6):1224–1238

    Article  CAS  PubMed  Google Scholar 

  • Rolls ET (1987) Information representation, processing and storage in the brain: analysis at the single neuron level. In: Changeux JP, Konishi M (eds) The neural and molecular bases of learning. Wiley, Chichester, pp 503–540

    Google Scholar 

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

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmajuk NA, DiCarlo JJ (1992) Stimulus configuration, classical conditioning, and the hippocampus. Psychol Rev 99:268–305

    Article  CAS  PubMed  Google Scholar 

  • Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sharp PE (1991) Computer simulation of hippocampal place cells. Psychobiology 19:103–115

    Article  Google Scholar 

  • Shouval HZ, Wang SS, Wittenberg GM (2010) Spike timing dependent plasticity: a consequence of more fundamental learning rules. Front Comput Neurosci 1:4

    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  CAS  PubMed  Google Scholar 

  • Solstad T, Moser EI, Einevoll GT (2006) From grid cells to place cells: a mathematical model. Hippocampus 16:1026–1031

    Article  PubMed  Google Scholar 

  • Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI (2008) Representation of geometric borders in the entorhinal cortex. Science 322:1865–1868

    Article  CAS  PubMed  Google Scholar 

  • Teyler TJ, DiScenna P (1986) The hippocampal memory indexing theory. Behav Neurosci 100:147–154

    Article  CAS  PubMed  Google Scholar 

  • Teyler TJ, Rudy JW (2007) The hippocampal indexing theory and episodic memory: updating the index. Hippocampus 17:1158–1169

    Article  PubMed  Google Scholar 

  • Touretzky DS, Redish AD (1996) Theory of rodent navigation based on interacting representations of space. Hippocampus 6:247–270

    Article  CAS  PubMed  Google Scholar 

  • Traub R, Wong RK, Miles R, Michelson H (1991) A model of a CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductance’s. J Neurophysiol 66:635–650

    Article  CAS  PubMed  Google Scholar 

  • Treves A (2004) Computational constraints between retrieving the past and predicting the future, and the CA3-CA1 differentiation. Hippocampus 14:539–556

    Article  PubMed  Google Scholar 

  • Treves A, Rolls ET (1992) Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 2:189–199

    Article  CAS  PubMed  Google Scholar 

  • Treves A, Rolls ET (1994) Computational analysis of the role of the hippocampus in memory. Hippocampus 4:374–391

    Article  CAS  PubMed  Google Scholar 

  • Treves A, Tashiro A, Witter ME, Moser EI (2008) What is the mammalian dentate gyrus good for? Neuroscience 154:1155–1172

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Tulving E (1984) Precis of Elements of Episodic Memory. Behav Brain Sci 7:223–268

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Zola-Morgan S, Squire LR, Amaral DG (1986) Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6:2950–2967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael E. Hasselmo .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2022 Springer Science+Business Media, LLC, part of Springer Nature

About this entry

Check for updates. Verify currency and authenticity via CrossMark

Cite this entry

Hasselmo, M.E., Hinman, J.R. (2022). Computational Neuroscience: Hippocampus. In: Pfaff, D.W., Volkow, N.D., Rubenstein, J.L. (eds) Neuroscience in the 21st Century. Springer, Cham. https://doi.org/10.1007/978-3-030-88832-9_175

Download citation

Publish with us

Policies and ethics

Navigation