Skip to main content

Hippocampus, Model Excitatory Cells

  • Living reference work entry
  • First Online:
  • 229 Accesses

Definition

Hippocampus, model excitatory cells refer to mathematical models of neurons that are designed to represent excitatory neurons in hippocampus. Here, we focus on biophysically motivated models of excitatory cells in the hippocampus proper (specifically the CA1 and CA3 pyramidal cells) and the granule cells of the dentate gyrus (DG). This article discusses some common motives for constructing these models and describes a few frequently used models in more detail.

Detailed Description

Introduction

Three principal hippocampal excitatory cell types are CA1 pyramidal cells, CA3 pyramidal cells, and granule cells of the DG (Fig. 1). These cells depolarize their postsynaptic targets through glutamatergic transmission of three main types of ionotropic receptors: α-amino-3-hydroxy-5-methyl-isoxazole-propionic acid (AMPA), kainate, and N-methyl-d-aspartate (NMDA). This is in contrast to hippocampal interneurons, which inhibit their postsynaptic targets through γ-aminobutyric acid...

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

References

  • Adams PR, Constanti A, Brown DA, Clark RB (1982) Intracellular Ca2+ activates a fast voltage-sensitive K+ current in vertebrate sympathetic neurones. Nature 296:746–749

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571–591

    Article  CAS  PubMed  Google Scholar 

  • Aradi I, Holmes WR (1999) Role of multiple calcium and calcium-dependent conductances in regulation of hippocampal dentate granule cell excitability. J Comput Neurosci 6:215–235

    Article  CAS  PubMed  Google Scholar 

  • Ashhad S, Narayanan R (2013) Quantitative interactions between the A-type K+ current and inositol trisphosphate receptors regulate intraneuronal Ca2+ waves and synaptic plasticity. J Physiol (Lond) 591:1645–1669

    Article  CAS  Google Scholar 

  • Baker JL, Olds JL (2007) Theta phase precession emerges from a hybrid computational model of a CA3 place cell. Cogn Neurodyn 1:237–248

    Article  PubMed Central  PubMed  Google Scholar 

  • Baker JL, Perez-Rosello T, Migliore M, Barrionuevo G, Ascoli GA (2011) A computer model of unitary responses from associational/commissural and perforant path synapses in hippocampal CA3 pyramidal cells. J Comput Neurosci 31:137–158

    Article  PubMed  Google Scholar 

  • Bianchi D, Marasco A, Limongiello A, Marchetti C, Marie H, Tirozzi B, Migliore M (2012) On the mechanisms underlying the depolarization block in the spiking dynamics of CA1 pyramidal neurons. J Comput Neurosci 33:207–225

    Article  PubMed  Google Scholar 

  • Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol (Berl) 82:239–259

    Article  CAS  Google Scholar 

  • Bruton CJ (1988) The neuropathology of temporal lobe epilepsy. Oxford University Press, Oxford

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cash S, Yuste R (1999) Linear summation of excitatory inputs by CA1 pyramidal neurons. Neuron 22:383–394

    Article  CAS  PubMed  Google Scholar 

  • Claiborne BJ, Amaral DG, Cowan WM (1986) A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus. J Comp Neurol 246:435–458

    Article  CAS  PubMed  Google Scholar 

  • Colgin LL, Moser EI (2010) Gamma oscillations in the hippocampus. Physiology 25:319–329

    Article  PubMed  Google Scholar 

  • Cutsuridis V, Cobb S, Graham BP (2010) Encoding and retrieval in a model of the hippocampal CA1 microcircuit. Hippocampus 20:423–446

    CAS  PubMed  Google Scholar 

  • Deuchars J, Thomson AM (1996) CA1 pyramid-pyramid connections in rat hippocampus in vitro: dual intracellular recordings with biocytin filling. Neuroscience 74:1009–1018

    CAS  PubMed  Google Scholar 

  • Dur-e-Ahmad M, Nicola W, Campbell SA, Skinner FK (2012) Network bursting using experimentally constrained single compartment CA3 hippocampal neuron models with adaptation. J Comput Neurosci 33:21–40

    Article  PubMed  Google Scholar 

  • Dyhrfjeld-Johnsen J, Morgan RJ, Földy C, Soltesz I (2008) Upregulated H-current in hyperexcitable CA1 dendrites after febrile seizures. Front Cell Neurosci 2:2. doi:10.3389/neuro.03.002.2008

    Article  PubMed Central  PubMed  Google Scholar 

  • Ferguson K, Campbell SA (2009) A two compartment model of a CA1 pyramidal neuron. Canad Appl Math Quart 17:293–307

    Google Scholar 

  • Ferrante M, Migliore M, Ascoli GA (2009) Feed-forward inhibition as a buffer of the neuronal input-output relation. Proc Natl Acad Sci U S A 106:18004–18009

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Frick A, Magee J, Koester HJ, Migliore M, Johnston D (2003) Normalization of Ca2+ signals by small oblique dendrites of CA1 pyramidal neurons. J Neurosci 23:3243–3250

    CAS  PubMed  Google Scholar 

  • Gloveli T, Dugladze T, Rotstein HG, Traub RD, Monyer H, Heinemann U, Whittington MA, Kopell NJ (2005) Orthogonal arrangement of rhythm-generating microcircuits in the hippocampus. Proc Natl Acad Sci U S A 102:13295–13300

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Golarai G, Greenwood AC, Feeney DM, Connor JA (2001) Physiological and structural evidence for hippocampal involvement in persistent seizure susceptibility after traumatic brain injury. J Neurosci 21:8523–8537

    CAS  PubMed  Google Scholar 

  • Hemond P, Epstein D, Boley A, Migliore M, Ascoli GA, Jaffe DB (2008) Distinct classes of pyramidal cells exhibit mutually exclusive firing patterns in hippocampal area CA3b. Hippocampus 18:411–424

    Article  PubMed  Google Scholar 

  • Hoffman DA, Magee JC, Colbert CM, Johnston D (1997) K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387:869–875

    Article  CAS  PubMed  Google Scholar 

  • Huang C-W, Huang C-C, Cheng J-T, Tsai J-J, Wu S-N (2007) Glucose and hippocampal neuronal excitability: role of ATP-sensitive potassium channels. J Neurosci Res 85:1468–1477

    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 

  • Jaffe DB, Ross WN, Lisman JE, Lasser-Ross N, Miyakawa H, Johnston D (1994) A model for dendritic Ca2+ accumulation in hippocampal pyramidal neurons based on fluorescence imaging measurements. J Neurophysiol 71:1065–1077

    CAS  PubMed  Google Scholar 

  • Kay AR, Wong RK (1986) Isolation of neurons suitable for patch-clamping from adult mammalian central nervous systems. J Neurosci Methods 16:227–238

    Article  CAS  PubMed  Google Scholar 

  • Kay AR, Wong RK (1987) Calcium current activation kinetics in isolated pyramidal neurones of the Ca1 region of the mature guinea-pig hippocampus. J Physiol (Lond) 392:603–616

    CAS  Google Scholar 

  • Kim M, Huang T, Abel T, Blackwell KT (2010) Temporal sensitivity of protein kinase a activation in late-phase long term potentiation. PLoS Comput Biol 6:e1000691. doi:10.1371/journal.pcbi.1000691

    Article  PubMed Central  PubMed  Google Scholar 

  • Knowles WD, Schwartzkroin PA (1981) Axonal ramifications of hippocampal Ca1 pyramidal cells. J Neurosci 1:1236–1241

    CAS  PubMed  Google Scholar 

  • Lipowsky R, Gillessen T, Alzheimer C (1996) Dendritic Na+ channels amplify EPSPs in hippocampal CA1 pyramidal cells. J Neurophysiol 76:2181–2191

    CAS  PubMed  Google Scholar 

  • Lømo T (1966) Frequency potentiation of excitatory synaptic activity in the dentate area of the hippocampal formation. Acta Physiol Scand 68:128

    Google Scholar 

  • Lynch M, Sutula T (2000) Recurrent excitatory connectivity in the dentate gyrus of kindled and kainic acid-treated rats. J Neurophysiol 83:693–704

    CAS  PubMed  Google Scholar 

  • Magee J, Hoffman D, Colbert C, Johnston D (1998) Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. Annu Rev Physiol 60:327–346

    Article  CAS  PubMed  Google Scholar 

  • Major G, Larkman AU, Jonas P, Sakmann B, Jack JJ (1994) Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices. J Neurosci 14:4613–4638

    CAS  PubMed  Google Scholar 

  • Migliore M, Cook EP, Jaffe DB, Turner DA, Johnston D (1995) Computer simulations of morphologically reconstructed CA3 hippocampal neurons. J Neurophysiol 73:1157–1168

    CAS  PubMed  Google Scholar 

  • Migliore M, Ferrante M, Ascoli GA (2005) Signal propagation in oblique dendrites of CA1 pyramidal cells. J Neurophysiol 94:4145–4155

    Article  PubMed Central  PubMed  Google Scholar 

  • Migliore M, Messineo L, Ferrante M (2004) Dendritic Ih selectively blocks temporal summation of unsynchronized distal inputs in CA1 pyramidal neurons. J Comput Neurosci 16:5–13

    Article  CAS  PubMed  Google Scholar 

  • Narayanan R, Johnston D (2007) Long-term potentiation in rat hippocampal neurons is accompanied by spatially widespread changes in intrinsic oscillatory dynamics and excitability. Neuron 56:1061–1075

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nettleton JS, Spain WJ (2000) Linear to supralinear summation of AMPA-mediated EPSPs in neocortical pyramidal neurons. J Neurophysiol 83:3310–3322

    CAS  PubMed  Google Scholar 

  • Numann RE, Wadman WJ, Wong RK (1987) Outward currents of single hippocampal cells obtained from the adult guinea-pig. J Physiol (Lond) 393:331–353

    CAS  Google Scholar 

  • Penttonen M, Kamondi A, Sik A, Acsády L, Buzsáki G (1997) Feed-forward and feed-back activation of the dentate gyrus in vivo during dentate spikes and sharp wave bursts. Hippocampus 7:437–450

    Article  CAS  PubMed  Google Scholar 

  • Pinsky PF, Rinzel J (1994) Intrinsic and network rhythmogenesis in a reduced Traub model for CA3 neurons. J Comput Neurosci 1:39–60

    Article  CAS  PubMed  Google Scholar 

  • Poirazi P, Brannon T, Mel BW (2003) Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell. Neuron 37:977–987

    Article  CAS  PubMed  Google Scholar 

  • Regehr WG, Connor JA, Tank DW (1989) Optical imaging of calcium accumulation in hippocampal pyramidal cells during synaptic activation. Nature 341:533–536

    Article  CAS  PubMed  Google Scholar 

  • Royeck M, Horstmann M-T, Remy S, Reitze M, Yaari Y, Beck H (2008) Role of axonal NaV1.6 sodium channels in action potential initiation of CA1 pyramidal neurons. J Neurophysiol 100:2361–2380

    Article  CAS  PubMed  Google Scholar 

  • Rusakov DA, Stewart MG, Korogod SM (1996) Branching of active dendritic spines as a mechanism for controlling synaptic efficacy. Neuroscience 75:315–323

    Article  CAS  PubMed  Google Scholar 

  • Sah P, Gibb AJ, Gage PW (1988) Potassium current activated by depolarization of dissociated neurons from adult guinea pig hippocampus. J Gen Physiol 92:263–278

    Article  CAS  PubMed  Google Scholar 

  • Santhakumar V, Aradi I, Soltesz I (2005) Role of mossy fiber sprouting and mossy cell loss in hyperexcitability: a network model of the dentate gyrus incorporating cell types and axonal topography. J Neurophysiol 93:437–453

    Article  PubMed  Google Scholar 

  • Santhakumar V, Bender R, Frotscher M, Ross ST, Hollrigel GS, Toth Z, Soltesz I (2000) Granule cell hyperexcitability in the early post-traumatic rat dentate gyrus: the “irritable mossy cell” hypothesis. J Physiol (Lond) 524(Pt 1):117–134

    Article  CAS  Google Scholar 

  • Santhakumar V, Ratzliff AD, Jeng J, Toth Z, Soltesz I (2001) Long-term hyperexcitability in the hippocampus after experimental head trauma. Ann Neurol 50:708–717

    Article  CAS  PubMed  Google Scholar 

  • Schmidt-Hieber C, Jonas P, Bischofberger J (2007) Subthreshold dendritic signal processing and coincidence detection in dentate gyrus granule cells. J Neurosci 27:8430–8441

    Article  CAS  PubMed  Google Scholar 

  • Schwartzkroin PA (1978) Secondary range rhythmic spiking in hippocampal neurons. Brain Res 149:247–250

    Article  CAS  PubMed  Google Scholar 

  • Skinner F (2006) Conductance-based models. Scholarpedia 1:1408. doi:10.4249/scholarpedia.1408

    Article  Google Scholar 

  • Spruston N, Johnston D (1992) Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. J Neurophysiol 67:508–529

    CAS  PubMed  Google Scholar 

  • Spruston N, McBain C (2007) Chap 5. Structural and functional properties of hippocampal neurons. In: Andersen P, Morris R, Amaral D, Bliss T, O’Keefe J (eds) The hippocampus book. Oxford University Press, New York, pp 133–201

    Google Scholar 

  • Staley KJ, Otis TS, Mody I (1992) Membrane properties of dentate gyrus granule cells: comparison of sharp microelectrode and whole-cell recordings. J Neurophysiol 67:1346–1358

    CAS  PubMed  Google Scholar 

  • Taxidis J, Coombes S, Mason R, Owen MR (2012) Modeling sharp wave-ripple complexes through a CA3-CA1 network model with chemical synapses. Hippocampus 22:995–1017

    Article  CAS  PubMed  Google Scholar 

  • Tort ABL, Rotstein HG, Dugladze T, Gloveli T, Kopell NJ (2007) On the formation of gamma-coherent cell assemblies by oriens lacunosum-moleculare interneurons in the hippocampus. Proc Natl Acad Sci U S A 104:13490–13495

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Traub RD (1982) Simulation of intrinsic bursting in CA3 hippocampal neurons. Neuroscience 7:1233–1242

    Article  CAS  PubMed  Google Scholar 

  • Traub RD, Knowles WD, Miles R, Wong RK (1984) Synchronized after discharges in the hippocampus: simulation studies of the cellular mechanism. Neuroscience 12:1191–1200

    Article  CAS  PubMed  Google Scholar 

  • Traub RD, Llinás R (1979) Hippocampal pyramidal cells: significance of dendritic ionic conductances for neuronal function and epileptogenesis. J Neurophysiol 42:476–496

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Vetter P, Roth A, Häusser M (2001) Propagation of action potentials in dendrites depends on dendritic morphology. J Neurophysiol 85:926–937

    CAS  PubMed  Google Scholar 

  • Warman EN, Durand DM, Yuen GL (1994) Reconstruction of hippocampal CA1 pyramidal cell electrophysiology by computer simulation. J Neurophysiol 71:2033–2045

    CAS  PubMed  Google Scholar 

  • West MJ, Slomianka L, Gundersen HJG (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482–497

    Article  CAS  PubMed  Google Scholar 

  • Wilson HR, Cowan JD (1972) Excitatory and inhibitory interactions in localized populations of model neurons. Biophys J 12:1–24

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wong RKS, Prince DA (1978) Participation of calcium spikes during intrinsic burst firing in hippocampal neurons. Brain Res 159:385–390

    Article  CAS  PubMed  Google Scholar 

  • Wong RKS, Prince DA (1981) After potential generation in hippocampal pyramidal cells. J Neurophysiol 45:86–97

    CAS  PubMed  Google Scholar 

  • Yuen GL, Durand D (1991) Reconstruction of hippocampal granule cell electrophysiology by computer simulation. Neuroscience 41:411–423

    Article  CAS  PubMed  Google Scholar 

Further Reading

  • Izhikevich EM (ed) (2007) Dynamical systems in neuroscience: the geometry of excitability and bursting. The MIT Press, London

    Google Scholar 

  • Migliore M, Ascoli GA, Jaffe DB (2010) CA3 cells: detailed and simplified pyramidal cell models. In: Cutsuridis V, Graham B, Cobb S, Vida I (eds) Hippocampal microcircuits. Springer, New York, pp 353–374

    Chapter  Google Scholar 

  • Morgan RJ, Soltesz I (2010) Microcircuit model of the dentate gyrus in epilepsy. In: Cutsuridis V, Graham B, Cobb S, Vida I (eds) Hippocampal microcircuits. Springer, New York, pp 495–525

    Chapter  Google Scholar 

  • Nicolas B, Hakim V (2009) Neuronal dynamics. In: Meyers RA (ed) Encyclopedia of complexity and systems science. Springer, New York, pp 6099–6116. doi:10.1007/978-0-387-30440-3_359

    Google Scholar 

  • Poirazi P, Pissadaki E-K (2010) The making of a detailed CA1 pyramidal neuron model. In: Cutsuridis V, Graham B, Cobb S, Vida I (eds) Hippocampal microcircuits. Springer, New York, pp 317–352

    Chapter  Google Scholar 

  • Vida I (2010) Morphology of hippocampal neurons. In: Cutsuridis V, Graham B, Cobb S, Vida I (eds) Hippocampal microcircuits. Springer, New York, pp 27–67

    Chapter  Google Scholar 

Download references

Acknowledgments

We would like to thank Natural Sciences and Engineering Research Council of Canada (NSERC) for their ongoing support as well as an Ontario Graduate Scholarship (OGS) to KAF.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Katie A. Ferguson .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this entry

Cite this entry

Ferguson, K.A., Skinner, F.K. (2013). Hippocampus, Model Excitatory Cells. In: Jaeger, D., Jung, R. (eds) Encyclopedia of Computational Neuroscience. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7320-6_28-1

Download citation

  • DOI: https://doi.org/10.1007/978-1-4614-7320-6_28-1

  • Received:

  • Accepted:

  • Published:

  • Publisher Name: Springer, New York, NY

  • Online ISBN: 978-1-4614-7320-6

  • eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences

Publish with us

Policies and ethics