CA1 pyramidal cell: I_NaP and I_M contributions to somatic bursting (Golomb et al 2006)

 Download zip file 
Help downloading and running models
Accession:66268
To study the mechanisms of bursting, we have constructed a conductance-based, one-compartment model of CA1 pyramidal neurons. In this neuron model, reduced [Ca2+]o is simulated by negatively shifting the activation curve of the persistent Na+ current (INaP), as indicated by recent experimental results. The neuron model accounts, with different parameter sets, for the diversity of firing patterns observed experimentally in both zero and normal [Ca2+]o. Increasing INaP in the neuron model induces bursting and increases the number of spikes within a burst, but is neither necessary nor sufficient for bursting. We show, using fast-slow analysis and bifurcation theory, that the M-type K+ current (IM) allows bursting by shifting neuronal behavior between a silent and a tonically-active state, provided the kinetics of the spike generating currents are sufficiently, though not extremely, fast. We suggest that bursting in CA1 pyramidal cells can be explained by a single compartment *square bursting* mechanism with one slow variable, the activation of IM. See paper for more and details.
Reference:
1 . Golomb D, Yue C, Yaari Y (2006) Contribution of persistent Na+current and M-type K+ current to somatic bursting in CA1 pyramidal cells: combined experimental and modeling study J Neurophysiol 96(4):1912-26 [PubMed]
Model Information (Click on a link to find other models with that property)
Model Type: Neuron or other electrically excitable cell;
Brain Region(s)/Organism:
Cell Type(s): Hippocampus CA1 pyramidal cell;
Channel(s): I Na,p; I Na,t; I A; I K; I M;
Gap Junctions:
Receptor(s):
Gene(s):
Transmitter(s):
Simulation Environment: XPP;
Model Concept(s): Bursting; Bifurcation;
Implementer(s): Golomb, David [golomb at bgu.ac.il];
Search NeuronDB for information about:  Hippocampus CA1 pyramidal cell; I Na,p; I Na,t; I A; I K; I M;
  
/
ca1_model_db
README.HTML
casup.pdf
nca.ode
ncaScreenShot.jpg
zca.ode
zcaScreenShot.jpg
                            

Golomb D, Yue C, Yaari Y (2006) Contribution of persistent Na+current and M-type K+ current to somatic bursting in CA1 pyramidal cells: combined experimental and modeling study J Neurophysiol 96(4):1912-26[PubMed]

References and models cited by this paper

References and models that cite this paper

Azouz R, Jensen MS, Yaari Y (1996) Ionic basis of spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. J Physiol 492 ( Pt 1):211-23 [PubMed]

Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ (2004) Potassium model for slow (2-3 Hz) in vivo neocortical paroxysmal oscillations. J Neurophysiol 92:1116-32 [Journal] [PubMed]

Bertram R, Butte MJ, Kiemel T, Sherman A (1995) Topological and phenomenological classification of bursting oscillations. Bull Math Biol 57:413-39 [PubMed]

Borg-graham L (1999) Interpretations of data and mechanisms for hippocampal pyramidal cell models Cerebral Cortex cortical Models, Jones E:Ulinski P:Peters A, ed. pp.19

Brown BS, Yu SP (2000) Modulation and genetic identification of the M channel. Prog Biophys Mol Biol 73:135-66 [PubMed]

Cantrell AR, Ma JY, Scheuer T, Catterall WA (1996) Muscarinic modulation of sodium current by activation of protein kinase C in rat hippocampal neurons. Neuron 16:1019-26 [PubMed]

Chao TI, Alzheimer C (1995) Effects of phenytoin on the persistent Na+ current of mammalian CNS neurones. Neuroreport 6:1778-80 [PubMed]

Chen S, Yue C, Yaari Y (2005) A transitional period of Ca2+-dependent spike afterdepolarization and bursting in developing rat CA1 pyramidal cells. J Physiol 567:79-93 [PubMed]

Colbert CM, Pan E (2002) Ion channel properties underlying axonal action potential initiation in pyramidal neurons. Nat Neurosci 5:533-8 [PubMed]

Ermentrout GB (2002) Simulating, Analyzing, and Animating Dynamical System: A Guide to XPPAUT for Researchers and Students Society for Industrial and Applied Mathematics (SIAM)

Fleidervish IA, Friedman A, Gutnick MJ (1996) Slow inactivation of Na+ current and slow cumulative spike adaptation in mouse and guinea-pig neocortical neurones in slices. J Physiol 493 ( Pt 1):83-97 [PubMed]

French CR, Sah P, Buckett KJ, Gage PW (1990) A voltage-dependent persistent sodium current in mammalian hippocampal neurons. J Gen Physiol 95:1139-57 [PubMed]

Gasparini S, Magee JC (2002) Phosphorylation-dependent differences in the activation properties of distal and proximal dendritic Na+ channels in rat CA1 hippocampal neurons. J Physiol 541:665-72 [PubMed]

Gilles N, Blanchet C, Shichor I, Zaninetti M, Lotan I, Bertrand D, Gordon D (1999) A scorpion alpha-like toxin that is active on insects and mammals reveals an unexpected specificity and distribution of sodium channel subtypes in rat brain neurons. J Neurosci 19:8730-9 [PubMed]

Golomb D, Amitai Y (1997) Propagating neuronal discharges in neocortical slices: computational and experimental study. J Neurophysiol 78:1199-211 [Journal] [PubMed]

Gu N, Vervaeke K, Hu H, Storm JF (2005) Kv7-KCNQ-M and HCN-h, but not KCa2-SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells. J Physiol 566:689-715 [PubMed]

Halliwell JV, Adams PR (1982) Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res 250:71-92 [PubMed]

Hammarstrom AK, Gage PW (2002) Hypoxia and persistent sodium current. Eur Biophys J 31:323-30 [PubMed]

Harris KD, Hirase H, Leinekugel X, Henze DA, Buzsaki G (2001) Temporal interaction between single spikes and complex spike bursts in hippocampal pyramidal cells. Neuron 32:141-9 [PubMed]

Heinemann U, Lux HD, Gutnick MJ (1977) Extracellular free calcium and potassium during paroxsmal activity in the cerebral cortex of the cat. Exp Brain Res 27:237-43 [PubMed]

Hoffman DA, Magee JC, Colbert CM, Johnston D (1997) K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387:869-75 [PubMed]

Hoppensteadt FC, Izhikevich EM (1997) Weakly Connected Neural Networks :90

Izhikevich EM (2000) Neural excitability, spiking and bursting Int J Bifurcat Chaos Appl Sci Eng 10:1171-1266

Izhikevich EM (2007) Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting [Journal]

   Artificial neuron model (Izhikevich 2003, 2004, 2007) [Model]

Izhikevich EM, Desai NS, Walcott EC, Hoppensteadt FC (2003) Bursts as a unit of neural information: selective communication via resonance. Trends Neurosci 26:161-7 [PubMed]

Jensen MS, Azouz R, Yaari Y (1994) Variant firing patterns in rat hippocampal pyramidal cells modulated by extracellular potassium. J Neurophysiol 71:831-9 [Journal] [PubMed]

Jung HY, Staff NP, Spruston N (2001) Action potential bursting in subicular pyramidal neurons is driven by a calcium tail current. J Neurosci 21:3312-21 [PubMed]

Karst H, Joa Low-threshold calcium current in dendrites of the adult rat hippocampus. Neurosci Lett 164:154-8 [PubMed]

Kay AR, Sugimori M, Llinas R (1998) Kinetic and stochastic properties of a persistent sodium current in mature guinea pig cerebellar Purkinje cells. J Neurophysiol 80:1167-79 [Journal] [PubMed]

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 392:603-16 [PubMed]

Lancaster B, Adams PR (1986) Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons. J Neurophysiol 55:1268-82 [Journal] [PubMed]

Larkum ME, Zhu JJ, Sakmann B (1999) A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398:338-41 [PubMed]

Li Z, Hatton GI (1996) Oscillatory bursting of phasically firing rat supraoptic neurones in low-Ca2+ medium: Na+ influx, cytosolic Ca2+ and gap junctions. J Physiol 496 ( Pt 2):379-94 [PubMed]

Lisman JE (1997) Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20:38-43 [PubMed]

Maccaferri G, McBain CJ (1996) The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J Physiol 497 ( Pt 1):119-30 [PubMed]

Madison DV, Nicoll RA (1984) Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. J Physiol 354:319-31 [PubMed]

Magee JC (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18:7613-24 [PubMed]

Magee JC, Carruth M (1999) Dendritic voltage-gated ion channels regulate the action potential firing mode of hippocampal CA1 pyramidal neurons. J Neurophysiol 82:1895-901 [Journal] [PubMed]

Magistretti J, Ragsdale DS, Alonso A (2003) Kinetic diversity of single-channel burst openings underlying persistent Na(+) current in entorhinal cortex neurons. Biophys J 85:3019-34 [PubMed]

Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382:363-6 [Journal] [PubMed]

   [2 reconstructed morphologies on NeuroMorpho.Org]
   Pyramidal Neuron Deep, Superficial; Aspiny, Stellate (Mainen and Sejnowski 1996) [Model]

Mandelblat Y, Etzion Y, Grossman Y, Golomb D (2004) Period doubling of calcium spike firing in a model of a Purkinje cell dendrite. J Comput Neurosci 11:43-62 [Journal] [PubMed]

Martina M, Jonas P (1997) Functional differences in Na+ channel gating between fast-spiking interneurones and principal neurones of rat hippocampus. J Physiol 505 ( Pt 3):593-603 [PubMed]

Martina M, Schultz JH, Ehmke H, Monyer H, Jonas P (1998) Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus. J Neurosci 18:8111-25 [PubMed]

Metz AE, Jarsky T, Martina M, Spruston N (2005) R-type calcium channels contribute to afterdepolarization and bursting in hippocampal CA1 pyramidal neurons. J Neurosci 25:5763-73 [PubMed]

Mickus T, Jung H, Spruston N (1999) Properties of slow, cumulative sodium channel inactivation in rat hippocampal CA1 pyramidal neurons. Biophys J 76:846-60 [PubMed]

Pinsky PF, Rinzel J (1994) Intrinsic and network rhythmogenesis in a reduced Traub model for CA3 neurons. J Comput Neurosci 1:39-60 [Journal] [PubMed]

   CA3 pyramidal cell: rhythmogenesis in a reduced Traub model (Pinsky, Rinzel 1994) [Model]

Pumain R, Menini C, Heinemann U, Louvel J, Silva-Barrat C (1985) Chemical synaptic transmission is not necessary for epileptic seizures to persist in the baboon Papio papio. Exp Neurol 89:250-8 [PubMed]

Ranck JB (1973) Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp Neurol 41:461-531 [PubMed]

Rinzel J, Ermentrout B (1998) Analysis of neural excitability and oscillations. Methods In Neuronal Modeling 2nd Edition, Segev I, Koch C, ed. pp.251

Rush ME, Rinzel J (1995) The potassium A-current, low firing rates and rebound excitation in Hodgkin-Huxley models. Bull Math Biol 57:899-929 [PubMed]

Sah P, Gibb AJ, Gage PW (1988) Potassium current activated by depolarization of dissociated neurons from adult guinea pig hippocampus. J Gen Physiol 92:263-78 [PubMed]

Sah P, Gibb AJ, Gage PW (1988) The sodium current underlying action potentials in guinea pig hippocampal CA1 neurons. J Gen Physiol 91:373-98 [PubMed]

Schnee ME, Brown BS (1998) Selectivity of linopirdine (DuP 996), a neurotransmitter release enhancer, in blocking voltage-dependent and calcium-activated potassium currents in hippocampal neurons. J Pharmacol Exp Ther 286:709-17 [PubMed]

Schwartzkroin PA (1975) Characteristics of CA1 neurons recorded intracellularly in the hippocampal in vitro slice preparation. Brain Res 85:423-36 [PubMed]

Sharp AA, O'Neil MB, Abbott LF, Marder E (1993) The dynamic clamp: artificial conductances in biological neurons. Trends Neurosci 16:389-94 [PubMed]

Shuai J, Bikson M, Hahn PJ, Lian J, Durand DM (2003) Ionic mechanisms underlying spontaneous CA1 neuronal firing in Ca2+-free solution. Biophys J 84:2099-111 [PubMed]

Spadoni F, Hainsworth AH, Mercuri NB, Caputi L, Martella G, Lavaroni F, Bernardi G, Stefani A (2002) Lamotrigine derivatives and riluzole inhibit INa,P in cortical neurons. Neuroreport 13:1167-70 [PubMed]

Spain WJ, Schwindt PC, Crill WE (1987) Anomalous rectification in neurons from cat sensorimotor cortex in vitro. J Neurophysiol 57:1555-76 [Journal] [PubMed]

Stocker M, Krause M, Pedarzani P (1999) An apamin-sensitive Ca2+-activated K+ current in hippocampal pyramidal neurons. Proc Natl Acad Sci U S A 96:4662-7 [PubMed]

Storm JF (1987) Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J Physiol 385:733-59 [PubMed]

Su H, Alroy G, Kirson ED, Yaari Y (2001) Extracellular calcium modulates persistent sodium current-dependent burst-firing in hippocampal pyramidal neurons. J Neurosci 21:4173-82 [PubMed]

Tatulian L, Delmas P, Abogadie FC, Brown DA (2001) Activation of expressed KCNQ potassium currents and native neuronal M-type potassium currents by the anti-convulsant drug retigabine. J Neurosci 21:5535-45 [PubMed]

Terman D (1992) The transition from bursting to continuous spiking in excitable membrane models J Nonlinear Sci 2:135-182

Thompson SM, Wong RK (1991) Development of calcium current subtypes in isolated rat hippocampal pyramidal cells. J Physiol 439:671-89 [PubMed]

Traub RD, Jefferys JG, Miles R, Whittington MA, Toth K (1994) A branching dendritic model of a rodent CA3 pyramidal neurone. J Physiol 481 ( Pt 1):79-95 [PubMed]

Traub RD, Miles R (1991) Neuronal Networks Of The Hippocampus

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 66:635-50 [Journal] [PubMed]

Urbani A, Belluzzi O (2000) Riluzole inhibits the persistent sodium current in mammalian CNS neurons. Eur J Neurosci 12:3567-74 [PubMed]

Vasilyev DV, Barish ME (2002) Postnatal development of the hyperpolarization-activated excitatory current Ih in mouse hippocampal pyramidal neurons. J Neurosci 22:8992-9004 [PubMed]

Vervaeke K, Hu H, Graham LJ, Storm JF (2006) Contrasting effects of the persistent Na+ current on neuronal excitability and spike timing. Neuron 49:257-70 [PubMed]

Wang HS, Pan Z, Shi W, Brown BS, Wymore RS, Cohen IS, Dixon JE, McKinnon D (1998) KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 282:1890-3 [PubMed]

Warman EN, Durand DM, Yuen GL (1994) Reconstruction of hippocampal CA1 pyramidal cell electrophysiology by computer simulation. J Neurophysiol 71:2033-45 [Journal] [PubMed]

Wickenden AD, Yu W, Zou A, Jegla T, Wagoner PK (2000) Retigabine, a novel anti-convulsant, enhances activation of KCNQ2-Q3 potassium channels. Mol Pharmacol 58:591-600 [PubMed]

Wong RK, Prince DA (1981) Afterpotential generation in hippocampal pyramidal cells. J Neurophysiol 45:86-97 [Journal] [PubMed]

Yaari Y, Beck H (2002) fiEpileptic neuronsfi in temporal lobe epilepsy. Brain Pathol 12:234-9 [PubMed]

Yue C, Remy S, Su H, Beck H, Yaari Y (2005) Proximal persistent Na+ channels drive spike afterdepolarizations and associated bursting in adult CA1 pyramidal cells. J Neurosci 25:9704-20 [PubMed]

Yue C, Yaari Y (2004) KCNQ-M channels control spike afterdepolarization and burst generation in hippocampal neurons. J Neurosci 24:4614-24 [PubMed]

Yue C, Yaari Y (2006) Axo-somatic and apical dendritic Kv7-M channels differentially regulate the intrinsic excitability of adult rat CA1 pyramidal cells. J Neurophysiol 95:3480-95 [Journal] [PubMed]

Zador AM, Agmon-Snir H, Segev I (1995) The morphoelectrotonic transform: a graphical approach to dendritic function. J Neurosci 15:1669-82 [PubMed]

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. 33:207-25 [Journal] [PubMed]

   CA1 pyramidal neuron: depolarization block (Bianchi et al. 2012) [Model]

Chambers JD, Bornstein JC, Gwynne RM, Koussoulas K, Thomas EA (2014) A detailed, conductance based computer model of intrinsic sensory neurons of the gastrointestinal tract. Am J Physiol Gastrointest Liver Physiol 307:G517-G532 [Journal] [PubMed]

   Intrinsic sensory neurons of the gut (Chambers et al. 2014) [Model]

Harish O, Golomb D (2010) Control of the Firing Patterns of Vibrissa Motoneurons by Modulatory and Phasic Synaptic Inputs: a Modeling Study. J Neurophysiol 103:2684-2699 [Journal] [PubMed]

   Control of vibrissa motoneuron firing (Harish and Golomb 2010) [Model]

Hayut I, Fanselow EE, Connors BW, Golomb D (2011) LTS and FS Inhibitory Interneurons, Short-Term Synaptic Plasticity, and Cortical Circuit Dynamics PLoS Comput Biol 7(10):e1002248 [Journal]

   Rate model of a cortical RS-FS-LTS network (Hayut et al. 2011) [Model]

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(4):411-24 [Journal] [PubMed]

   CA3 pyramidal neuron: firing properties (Hemond et al. 2008) [Model]

Morse TM, Carnevale NT, Mutalik PG, Migliore M, Shepherd GM (2010) Abnormal excitability of oblique dendrites implicated in early Alzheimer's: a computational study Front. Neural Circuits 4:16 [Journal] [PubMed]

   Amyloid beta (IA block) effects on a model CA1 pyramidal cell (Morse et al. 2010) [Model]

Royeck M, Horstmann MT, 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 [Journal] [PubMed]

   Axonal NaV1.6 Sodium Channels in AP Initiation of CA1 Pyramidal Neurons (Royeck et al. 2008) [Model]

Stefanescu RA, Shivakeshavan RG, Khargonekar PP, Talathi SS (2013) Computational Modeling of Channelrhodopsin-2 Photocurrent Characteristics in Relation to Neural Signaling. Bull Math Biol 75(11):2208-2240 [Journal] [PubMed]

   Computational modelling of channelrhodopsin-2 photocurrent characteristics (Stefanescu et al. 2013) [Model]

Xu J, Clancy CE (2008) Ionic mechanisms of endogenous bursting in CA3 hippocampal pyramidal neurons: a model study. PLoS ONE 3:e2056 [Journal] [PubMed]

   Ionic mechanisms of bursting in CA3 pyramidal neurons (Xu and Clancy 2008) [Model]

(88 refs)