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Stochastic Ion Channel Gating and Probabilistic Computation in Dendritic Neurons

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The Computing Dendrite

Part of the book series: Springer Series in Computational Neuroscience ((NEUROSCI,volume 11))

Abstract

The electrical signals underlying neural computations are mediated by membrane ion channels. Although these ion channels are well known to operate stochastically, most computational models of dendritic neurons instead make the approximation that ionic conductances are deterministic. We review the basic mathematical considerations underlying this approximation and new efficient simulation tools that allow it to be evaluated systematically. We show how this approximation breaks down for dendritic neurons, with the relative functional influence of stochastic ion channel gating likely to depend strongly on neuron type. An important consequence of stochastic gating of ion channels may be that it causes dendritic neurons to integrate synaptic inputs probabilistically, rather than in the all or nothing fashion predicted by deterministic models.

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References

  • Bhalla US (2004a) Signaling in small subcellular volumes. I. Stochastic and diffusion effects on individual pathways. Biophys J 87(2):733–744

    Article  PubMed  CAS  Google Scholar 

  • Bhalla US (2004b) Signaling in small subcellular volumes. II. Stochastic and diffusion effects on synaptic network properties. Biophys J 87(2):745–753

    Article  PubMed  CAS  Google Scholar 

  • Bittner KC, Andrasfalvy BK, Magee JC (2012) Ion channel gradients in the apical tuft region of CA1 pyramidal neurons. PLoS One 7(10):e46652

    Article  PubMed  CAS  Google Scholar 

  • Bruce IC (2009) Evaluation of stochastic differential equation approximation of ion channel gating models. Ann Biomed Eng 37(4):824–838

    Article  PubMed  Google Scholar 

  • Buesing L, Bill J, Nessler B, Maass W (2011) Neural dynamics as sampling: a model for stochastic computation in recurrent networks of spiking neurons. PLoS Comput Biol 7(11):e1002211

    Article  PubMed  CAS  Google Scholar 

  • Cannon RC, O’Donnell C, Nolan MF (2010) Stochastic ion channel gating in dendritic neurons: morphology dependence and probabilistic synaptic activation of dendritic spikes. PLoS Comput Biol 6(8)

    Google Scholar 

  • Cao Y, Gillespie DT, Petzold LR (2006) Efficient step size selection for the tau-leaping simulation method. J Chem Phys 124(4):044109

    Article  PubMed  Google Scholar 

  • Chen X, Johnston D (2004) Properties of single voltage-dependent K+ channels in dendrites of CA1 pyramidal neurones of rat hippocampus. J Physiol 559(Pt 1):187–203

    Article  PubMed  CAS  Google Scholar 

  • Chow CC, White JA (1996) Spontaneous action potentials due to channel fluctuations. Biophys J 71(6):3013–3021

    Article  PubMed  CAS  Google Scholar 

  • DeFelice LJ (1981) Introduction to membrane noise. Plenum, New York

    Book  Google Scholar 

  • Diba K, Lester HA, Koch C (2004) Intrinsic noise in cultured hippocampal neurons: experiment and modeling. J Neurosci 24(43):9723–9733

    Article  PubMed  CAS  Google Scholar 

  • Diba K, Koch C, Segev I (2006) Spike propagation in dendrites with stochastic ion channels. J Comput Neurosci 20(1):77–84

    Article  PubMed  Google Scholar 

  • Dorval AD Jr, White JA (2005) Channel noise is essential for perithreshold oscillations in entorhinal stellate neurons. J Neurosci 25(43):10025–10028

    Article  PubMed  CAS  Google Scholar 

  • Dudman JT, Nolan MF (2009) Stochastically gating ion channels enable patterned spike firing through activity-dependent modulation of spike probability. PLoS Comput Biol 5(2):e1000290

    Article  PubMed  Google Scholar 

  • Engel D, Jonas P (2005) Presynaptic action potential amplification by voltage-gated Na+ channels in hippocampal mossy fiber boutons. Neuron 45(3):405–417

    Article  PubMed  CAS  Google Scholar 

  • Faisal AA, White JA, Laughlin SB (2005) Ion-channel noise places limits on the miniaturization of the brain’s wiring. Curr Biol 15(12):1143–1149

    Article  PubMed  CAS  Google Scholar 

  • Faisal AA, Selen LP, Wolpert DM (2008) Noise in the nervous system. Nat Rev Neurosci 9(4):292–303

    Article  PubMed  CAS  Google Scholar 

  • Fiser J, Berkes P, Orban G, Lengyel M (2010) Statistically optimal perception and learning: from behavior to neural representations. Trends Cogn Sci 14(3):119–130

    Article  PubMed  Google Scholar 

  • Fox RF (1997) Stochastic versions of the Hodgkin–Huxley equations. Biophys J 72(5):2068–2074

    Article  PubMed  CAS  Google Scholar 

  • Fox RF, Lu Y (1994) Emergent collective behavior in large numbers of globally coupled independently stochastic ion channels. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 49(4):3421–3431

    Article  PubMed  CAS  Google Scholar 

  • Franks KM, Stevens CF, Sejnowski TJ (2003) Independent sources of quantal variability at single glutamatergic synapses. J Neurosci 23(8):3186–3195

    PubMed  CAS  Google Scholar 

  • Gillespie DT (1977) Exact stochastic simulation of coupled chemical-reactions. Abstr Paper Am Chem Soc 173:128

    Google Scholar 

  • Gillespie DT (2001) Approximate accelerated stochastic simulation of chemically reacting systems. J Chem Phys 115(4):1716–1733

    Article  CAS  Google Scholar 

  • Golding NL, Mickus TJ, Katz Y, Kath WL, Spruston N (2005) Factors mediating powerful voltage attenuation along CA1 pyramidal neuron dendrites. J Physiol 568(Pt 1):69–82

    Article  PubMed  CAS  Google Scholar 

  • Goldwyn JH, Shea-Brown E (2011) The what and where of adding channel noise to the Hodgkin–Huxley equations. PLoS Comput Biol 7(11):e1002247

    Article  PubMed  CAS  Google Scholar 

  • Goldwyn JH, Imennov NS, Famulare M, Shea-Brown E (2011) Stochastic differential equation models for ion channel noise in Hodgkin-Huxley neurons. Phys Rev E Stat Nonlin Soft Matter Phys 83:041908

    Article  PubMed  Google Scholar 

  • Hille B (2001) Ion channels of excitable membranes, 3rd edn. Sinauer, Sunderland, MA

    Google Scholar 

  • Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9(6):1179–1209

    Article  PubMed  CAS  Google Scholar 

  • Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117(4):500–544

    PubMed  CAS  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(6636):869–875

    Article  PubMed  CAS  Google Scholar 

  • Jacobson GA, Diba K, Yaron-Jakoubovitch A, Oz Y, Koch C, Segev I, Yarom Y (2005) Subthreshold voltage noise of rat neocortical pyramidal neurones. J Physiol 564:145–160

    Article  PubMed  CAS  Google Scholar 

  • Jarsky T, Roxin A, Kath WL, Spruston N (2005) Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat Neurosci 8:1667–1676

    Article  PubMed  CAS  Google Scholar 

  • Johansson S, Arhem P (1994) Single-channel currents trigger action potentials in small cultured hippocampal neurons. Proc Natl Acad Sci USA 91(5):1761–1765

    Article  PubMed  CAS  Google Scholar 

  • Johnston D, Narayanan R (2008) Active dendrites: colorful wings of the mysterious butterflies. Trends Neurosci 31(6):309–316

    Article  PubMed  CAS  Google Scholar 

  • Johnston D, Christie BR, Frick A, Gray R, Hoffman DA, Schexnayder LK, Watanabe S, Yuan LL (2003) Active dendrites, potassium channels and synaptic plasticity. Philos Trans R Soc Lond B Biol Sci 358(1432):667–674

    Article  PubMed  CAS  Google Scholar 

  • Koch C (1999) Biophysics of computation: information processing in single neurons. Computational neuroscience. Oxford University Press, New York

    Google Scholar 

  • Kole MH, Hallermann S, Stuart GJ (2006) Single Ih channels in pyramidal neuron dendrites: properties, distribution, and impact on action potential output. J Neurosci 26:1677–1687

    Article  PubMed  CAS  Google Scholar 

  • Lecar H, Nossal R (1971) Theory of threshold fluctuations in nerves. II. Analysis of various sources of membrane noise. Biophys J 11(12):1068–1084

    Article  PubMed  CAS  Google Scholar 

  • Linaro D, Storace M, Giugliano M (2011) Accurate and fast simulation of channel noise in conductance-based model neurons by diffusion approximation. PLoS Comput Biol 7(3):e1001102

    Article  PubMed  CAS  Google Scholar 

  • Lindner B, Garcia-Ojalvo J, Neiman A, Schimansky-Geier L (2004) Effects of noise in excitable systems. Phys Rep 392(6):321–424

    Article  Google Scholar 

  • Lisman JE, Raghavachari S, Tsien RW (2007) The sequence of events that underlie quantal transmission at central glutamatergic synapses. Nat Rev Neurosci 8(8):597–609

    Article  PubMed  CAS  Google Scholar 

  • Lorincz A, Notomi T, Tamas G, Shigemoto R, Nusser Z (2002) Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci 5:1185–1193

    Article  PubMed  Google Scholar 

  • Magee JC (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18:7613–7624

    PubMed  CAS  Google Scholar 

  • Magee JC (2000) Dendritic integration of excitatory synaptic input. Nat Rev Neurosci 1(3):181–190

    Article  PubMed  CAS  Google Scholar 

  • Magee JC, Johnston D (1995) Characterization of single voltage-gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. J Physiol 487:67–90

    PubMed  CAS  Google Scholar 

  • Magistretti J, Ragsdale DS, Alonso A (1999) Direct demonstration of persistent Na+ channel activity in dendritic processes of mammalian cortical neurones. J Physiol 521:629–636

    Article  PubMed  CAS  Google Scholar 

  • Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382(6589):363–366

    Article  PubMed  CAS  Google Scholar 

  • Manwani A, Koch C (1999) Detecting and estimating signals in noisy cable structure, I: neuronal noise sources. Neural Comput 11:1797–1829

    Article  PubMed  CAS  Google Scholar 

  • Mino H, Rubinstein JT, White JA (2002) Comparison of algorithms for the simulation of action potentials with stochastic sodium channels. Ann Biomed Eng 30:578–587

    Article  PubMed  Google Scholar 

  • Neher E (1998) Usefulness and limitations of linear approximations to the understanding of Ca++ signals. Cell Calcium 24:345–357

    Article  PubMed  CAS  Google Scholar 

  • Neher E, Sakmann B (1976) Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature 260(5554):799–802

    Article  PubMed  CAS  Google Scholar 

  • Nolan MF, Malleret G, Dudman JT, Buhl DL, Santoro B, Gibbs E, Vronskaya S, Buzsaki G, Siegelbaum SA, Kandel ER, Morozov A (2004) A behavioral role for dendritic integration: HCN1 channels constrain spatial memory and plasticity at inputs to distal dendrites of CA1 pyramidal neurons. Cell 119(5):719–732

    PubMed  CAS  Google Scholar 

  • Nusser Z (2009) Variability in the subcellular distribution of ion channels increases neuronal diversity. Trends Neurosci 32(5):267–274

    Article  PubMed  CAS  Google Scholar 

  • Raj A, van Oudenaarden A (2008) Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135(2):216–226

    Article  PubMed  CAS  Google Scholar 

  • Rall W (1959) Branching dendritic trees and motoneuron membrane resistivity. Exp Neurol 1:491–527

    Article  PubMed  CAS  Google Scholar 

  • Rall W (1962) Theory of physiological properties of dendrites. Ann N Y Acad Sci 96:1071–1092

    Article  PubMed  CAS  Google Scholar 

  • Reyes A (2001) Influence of dendritic conductances on the input–output properties of neurons. Annu Rev Neurosci 24:653–675

    Article  PubMed  CAS  Google Scholar 

  • Robinson RB, Siegelbaum SA (2003) Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol 65:453–480

    Article  PubMed  CAS  Google Scholar 

  • Schneidman E, Freedman B, Segev I (1998) Ion channel stochasticity may be critical in determining the reliability and precision of spike timing. Neural Comput 10:1679–1703

    Article  PubMed  CAS  Google Scholar 

  • Skaugen E, Walloe L (1979) Firing behaviour in a stochastic nerve membrane model based upon the Hodgkin–Huxley equations. Acta Physiol Scand 107(4):343–363

    Article  PubMed  CAS  Google Scholar 

  • Spruston N (2008) Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 9:206–221

    Article  PubMed  CAS  Google Scholar 

  • van Rossum MC, O’Brien BJ, Smith RG (2003) Effects of noise on the spike timing precision of retinal ganglion cells. J Neurophysiol 89:2406–2419

    Article  PubMed  Google Scholar 

  • Wahl-Schott C, Biel M (2009) HCN channels: structure, cellular regulation and physiological function. Cell Mol Life Sci 66:470–494

    Article  PubMed  CAS  Google Scholar 

  • White JA, Budde T, Kay AR (1995) A bifurcation analysis of neuronal subthreshold oscillations. Biophys J 69:1203–1217

    Article  PubMed  CAS  Google Scholar 

  • White JA, Klink R, Alonso A, Kay AR (1998) Noise from voltage-gated ion channels may influence neuronal dynamics in the entorhinal cortex. J Neurophysiol 80:262–269

    PubMed  CAS  Google Scholar 

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Correspondence to Matthew F. Nolan .

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O’Donnell, C., Nolan, M.F. (2014). Stochastic Ion Channel Gating and Probabilistic Computation in Dendritic Neurons. In: Cuntz, H., Remme, M., Torben-Nielsen, B. (eds) The Computing Dendrite. Springer Series in Computational Neuroscience, vol 11. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8094-5_24

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