- About this Journal ·
- Abstracting and Indexing ·
- Aims and Scope ·
- Annual Issues ·
- Article Processing Charges ·
- Author Guidelines ·
- Bibliographic Information ·
- Citations to this Journal ·
- Contact Information ·
- Editorial Board ·
- Editorial Workflow ·
- Free eTOC Alerts ·
- Publication Ethics ·
- Recently Accepted Articles ·
- Reviewers Acknowledgment ·
- Submit a Manuscript ·
- Subscription Information ·
- Table of Contents
Computational and Mathematical Methods in Medicine
Volume 2012 (2012), Article ID 595398, 16 pages
The Effect of Neural Noise on Spike Time Precision in a Detailed CA3 Neuron Model
1Department of Physiology, First Medical Faculty, Charles University in Prague, Albertov 5, 12800 Praha 2, Czech Republic
2Department of Pathological Physiology, Medical Faculty, Charles University in Prague, U nemocnice 5, 12853 Praha 2, Czech Republic
3Faculty of Biomedical Engineering, Czech Technical University in Prague, Nam. Sitna 3105, 27201 Kladno, Czech Republic
Received 30 September 2011; Revised 21 December 2011; Accepted 23 January 2012
Academic Editor: Reinoud Maex
Copyright © 2012 Eduard Kuriscak et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- E. D. Adrian and Y. Zotterman, “The impulses produced by sensory nerve endings—part 2. The response of a single end organ,” Journal of Physiology, vol. 61, pp. 151–171, 1926.
- W. Bialek, F. Rieke, R. R. de Ruyter van Steveninck, and D. Warland, “Reading a neural code,” Science, vol. 252, no. 5014, pp. 1854–1857, 1991.
- M. N. Shadlen and W. T. Newsome, “The variable discharge of cortical neurons: implications for connectivity, computation, and information coding,” Journal of Neuroscience, vol. 18, no. 10, pp. 3870–3896, 1998.
- M. Carandini, “Amplification of trial-to-trial response variability by neurons in visual cortex,” PLoS Biology, vol. 2, no. 9, article E264, 2004.
- D. MacKay and W. McCulloch, “The limiting information capacity of a neuronal link,” Bulletin of Mathematical Biophysics, vol. 14, no. 2, pp. 127–135, 1952.
- B. N. Lundstrom and A. L. Fairhall, “Decoding stimulus variance from a distributional neural code of interspike intervals,” Journal of Neuroscience, vol. 26, no. 35, pp. 9030–9037, 2006.
- R. Rieke, D. Warland, R. de Ruyter van Steveninck, and W. Bialek, Spikes: Exploring the Neural Code, Massachusetts Institute of Technology Press, Cambridge, Mass, USA, 1997.
- W. Bair and C. Koch, “Temporal precision of spike trains in extrastriate cortex of the behaving macaque monkey,” Neural Computation, vol. 8, no. 6, pp. 1185–1202, 1996.
- R. C. de Charms and A. Zador, “Neural representation and the cortical code,” Annual Review of Neuroscience, vol. 23, pp. 613–647, 2000.
- B. Gutkin, G. B. Ermentrout, and M. Rudolph, “Spike generating dynamics and the conditions for spike-time precision in cortical neurons,” Journal of Computational Neuroscience, vol. 15, no. 1, pp. 91–103, 2003.
- J. Kretzberg, M. Egelhaaf, and A. K. Warzecha, “Membrane potential fluctuations determine the precision of spike timing and synchronous activity: a model study,” Journal of Computational Neuroscience, vol. 10, no. 1, pp. 79–97, 2001.
- L. Cathala, S. Brickley, S. Cull-Candy, and M. Farrant, “Maturation of EPSCs and intrinsic membrane properties enhances precision at a cerebellar synapse,” Journal of Neuroscience, vol. 23, no. 14, pp. 6074–6085, 2003.
- M. C. van Rossum, B. J. O'Brien, and R. G. Smith, “Effects of noise on the spike timing precision of retinal ganglion cells,” Journal of Neurophysiology, vol. 89, no. 5, pp. 2406–2419, 2003.
- K. Diba, C. Koch, and I. Segev, “Spike propagation in dendrites with stochastic ion channels,” Journal of Computational Neuroscience, vol. 20, no. 1, pp. 77–84, 2006.
- S. E. Street and P. B. Manis, “Action potential timing precision in dorsal cochlear nucleus pyramidal cells,” Journal of Neurophysiology, vol. 97, no. 6, pp. 4162–4172, 2007.
- V. J. Uzzell and E. J. Chichilnisky, “Precision of spike trains in primate retinal ganglion cells,” Journal of Neurophysiology, vol. 92, no. 2, pp. 780–789, 2004.
- E. Arabzadeh, S. Panzeri, and M. E. Diamond, “Deciphering the spike train of a sensory neuron: counts and temporal patterns in the rat whisker pathway,” Journal of Neuroscience, vol. 26, no. 36, pp. 9216–9226, 2006.
- R. C. Liu, S. Tzonev, S. Rebrik, and K. D. Miller, “Variability and information in a neural code of the cat lateral geniculate nucleus,” Journal of Neurophysiology, vol. 86, no. 6, pp. 2789–2806, 2001.
- R. A. DiCaprio, C. P. Billimoria, and B. C. Ludwar, “Information rate and spike-timing precision of proprioceptive afferents,” Journal of Neurophysiology, vol. 98, no. 3, pp. 1706–1717, 2007.
- A. Rokem, S. Watzl, T. Gollisch, M. Stemmler, A. V. Herz, and I. Samengo, “Spike-timing precision underlies the coding efficiency of auditory receptor neurons,” Journal of Neurophysiology, vol. 95, no. 4, pp. 2541–2552, 2006.
- J. A. Simmons, N. Neretti, N. Intrator, R. A. Altes, M. J. Ferragamo, and M. I. Sanderson, “Delay accuracy in bat sonar is related to the reciprocal of normalized echo bandwidth, or Q,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 10, pp. 3638–3643, 2004.
- M. I. Sanderson and J. A. Simmons, “Target representation of naturalistic echolocation sequences in single unit responses from the inferior colliculus of big brown bats,” Journal of the Acoustical Society of America, vol. 118, no. 5, pp. 3352–3361, 2005.
- D. A. Butts, C. Weng, J. Jin et al., “Temporal precision in the neural code and the timescales of natural vision,” Nature, vol. 449, no. 7158, pp. 92–95, 2007.
- A. A. Faisal, L. P. J. Selen, and D. M. Wolpert, “Noise in the nervous system,” Nature Reviews Neuroscience, vol. 9, no. 4, pp. 292–303, 2008.
- M. Frerking, J. Schulte, S. P. Wiebe, and U. Stäubli, “Spike timing in CA3 pyramidal cells during behavior: implications for synaptic transmission,” Journal of Neurophysiology, vol. 94, no. 2, pp. 1528–1540, 2005.
- J. M. Fellous, M. Rudolph, A. Destexhe, and T. J. Sejnowski, “Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity,” Neuroscience, vol. 122, no. 3, pp. 811–829, 2003.
- V. M. Rodriguez-Molina, A. Aertsen, and D. H. Heck, “Spike timing and reliability in cortical pyramidal neurons: effects of EPSC kinetics, input synchronization and background noise on spike timing,” PLoS ONE, vol. 2, no. 3, article no. E319, 2007.
- D. Paré, E. Shink, H. Gaudreau, A. Destexhe, and E. J. Lang, “Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons in vivo,” Journal of Neurophysiology, vol. 79, no. 3, pp. 1450–1460, 1998.
- J. M. Bekkers and C. F. Stevens, “Quantal analysis of EPSCs recorded from small numbers of synapses in hippocampal cultures,” Journal of Neurophysiology, vol. 73, no. 3, pp. 1145–1156, 1995.
- V. N. Murthy, T. J. Sejnowski, and C. F. Stevens, “Heterogeneous release properties of visualized individual hippocampal synapses,” Neuron, vol. 18, no. 4, pp. 599–612, 1997.
- J. M. Bekkers, G. Richerson, and C. F. Stevens, “Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 14, pp. 5359–5362, 1990.
- G. Liu, S. Choi, and R. W. Tsien, “Variability of neurotransmitter concentration and nonsaturation of postsynaptic AMPA receptors at synapses in hippocampal cultures and slices,” Neuron, vol. 22, no. 2, pp. 395–409, 1999.
- L. J. Defelice, Introduction to Membrane Noise, Plenum Press, New York, NY, USA, 1981.
- J. A. White, J. T. Rubinstein, and A. R. Kay, “Channel noise in neurons,” Trends in Neurosciences, vol. 23, no. 3, pp. 131–137, 2000.
- E. Schneidman, B. Freedman, and I. Segev, “Ion channel stochasticity may be critical in determining the reliability and precision of spike timing,” Neural Computation, vol. 10, no. 7, pp. 1679–1703, 1998.
- R. C. Cannon, C. O'Donnell, and M. F. Nolan, “Stochastic ion channel gating in dendritic neurons: morphology dependence and probabilistic synaptic activation of dendritic spikes,” PLoS Computational Biology, vol. 6, no. 8, Article ID E1000886, 2010.
- E. Kuriscak, S. Trojan, and Z. Wünsch, “Model of spike propagation reliability along the myelinated axon corrupted by axonal intrinsic noise sources,” Physiological Research, vol. 51, no. 3, pp. 205–215, 2002.
- A. A. Faisal and S. B. Laughlin, “Stochastic simulations on the reliability of action potential propagation in thin axons,” PLoS Computational Biology, vol. 3, no. 5, article E79, 2007.
- A. Manwani and C. Koch, “Detecting and estimating signals in noisy cable structures, I: neuronal noise sources,” Neural Computation, vol. 11, no. 8, pp. 1797–1829, 1999.
- I. Oren, E. O. Mann, O. Paulsen, and N. Hájos, “Synaptic currents in anatomically identified CA3 neurons during hippocampal gamma oscillations in vitro,” Journal of Neuroscience, vol. 26, no. 39, pp. 9923–9934, 2006.
- J. J. Lawrence, Z. M. Grinspan, J. M. Statland, and C. J. McBain, “Muscarinic receptor activation tunes mouse stratum oriens interneurones to amplify spike reliability,” Journal of Physiology, vol. 571, no. 3, pp. 555–562, 2006.
- K. Vervaeke, H. Hu, L. J. Graham, and J. F. Storm, “Contrasting effects of the persistent Na+ current on neuronal excitability and spike timing,” Neuron, vol. 49, no. 2, pp. 257–270, 2006.
- C. Koch, Biophysics of Computation: Information Processing in Single Neurons, Oxford University Press, New York, NY, USA, 1999.
- J. M. Bower and C. Koch, “Experimentalists and modelers: can we all just get along?” Trends in Neurosciences, vol. 15, no. 11, pp. 458–461, 1992.
- J. M. Bower and D. Beeman, The Book of GENESIS: Exploring Realistic Neural Models with the General Neural Simulation System, Springer, New York, NY, USA, 1995.
- R. D. Traub, J. G. Jefferys, R. Miles, M. A. Whittington, and K. Tóth, “A branching dendritic model of a rodent CA3 pyramidal neurone,” Journal of Physiology, vol. 481, no. 1, pp. 79–95, 1994.
- E. D. Menschik and L. H. Finkel, “Neuromodulatory control of hippocampal function: towards a model of Alzheimer's disease,” Artificial Intelligence in Medicine, vol. 13, no. 1-2, pp. 99–121, 1998.
- A. Kapur, R. A. Pearce, W. W. Lytton, and L. B. Haberly, “GABA(A)-mediated IPSCs in piriform cortex have fast and slow components with different properties and locations on pyramidal cells,” Journal of Neurophysiology, vol. 78, no. 5, pp. 2531–2545, 1997.
- M. Rapp, Y. Yarom, and I. Segev, “Modeling back propagating action potential in weakly excitable dendrites of neocortical pyramidal cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 21, pp. 11985–11990, 1996.
- S. Bertrand and J. C. Lacaille, “Unitary synaptic currents between lacunosum-moleculare interneurones and pyramidal cells in rat hippocampus,” Journal of Physiology, vol. 532, no. 2, pp. 369–384, 2001.
- R. E. Fisher, R. Gray, and D. Johnston, “Properties and distribution of single voltage-gated calcium channels in adult hippocampal neurons,” Journal of Neurophysiology, vol. 64, no. 1, pp. 91–104, 1990.
- J. C. Magee and D. Johnston, “Characterization of single voltage-gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons,” Journal of Physiology, vol. 487, no. 1, pp. 67–90, 1995.
- J. Kang, J. R. Huguenard, and D. A. Prince, “Voltage-gated potassium channels activated during action potentials in layer V neocortical pyramidal neurons,” Journal of Neurophysiology, vol. 83, no. 1, pp. 70–80, 2000.
- P. A. Lima and N. V. Marrion, “Mechanisms underlying activation of the slow AHP in rat hippocampal neurons,” Brain Research, vol. 1150, no. 1, pp. 74–82, 2007.
- B. Lancaster, R. A. Nicoll, and D. J. Perkel, “Calcium activates two types of potassium channels in rat hippocampal neurons in culture,” Journal of Neuroscience, vol. 11, no. 1, pp. 23–30, 1991.
- X. Chen and D. Johnston, “Properties of single voltage-dependent K+ channels in dendrites of CA1 pyramidal neurones of rat hippocampus,” Journal of Physiology, vol. 559, no. 1, pp. 187–203, 2004.
- D. Linaro, M. Storace, and M. Giugliano, “Accurate and fast simulation of channel noise in conductance-based model neurons by diffusion approximation,” PLoS Computational Biology, vol. 2, no. 3, article e1001102, 17 pages, 2011.
- B. Hille, Ionic Channels of Excitable Membranes, Sinauer Associates, Sunderland, Mass, USA, 2nd edition, 1992.
- A. D. Coop, H. Cornelis, and F. Santamaria, “Dendritic excitability modulates dendritic information processing in a Purkinje cell model,” Frontiers in Computational Neuroscience, vol. 4, pp. 1–10, 2010.
- A. L. Hodgkin and A. F. Huxley, “A quantitative description of membrane current and its application to conduction and excitation in nerve,” Journal of Physiology, vol. 117, no. 4, pp. 500–544, 1952.
- W. H. Press, S. A. Teukolsky, W. T. Vetterling, and B. P. Flannery, Numerical Recipes in FORTRAN: The Art of Scientific Computing, Cambridge University Press, New York, NY, USA, 1992.
- R. J. MacGregor, Neural and Brain Modeling, Academic Press, New York, NY, USA, 1987.
- R. Halas and M. Jukl, “On Beck's coloring of posets,” Discrete Mathematics, vol. 309, no. 13, pp. 4584–4589, 2009.
- W. S. Cleveland, “Robust locally weighted regression and smoothing scatterplots,” Journal of the American Statistical Association, vol. 74, no. 368, pp. 829–836, 1995.
- A. K. McAllister and C. F. Stevens, “Nonsaturation of AMPA and NMDA receptors at hippocampal synapses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 11, pp. 6173–6178, 2000.
- S. Nurse and J. C. Lacaille, “Late maturation of GABA(B) synaptic transmission in area CA1 of the rat hippocampus,” Neuropharmacology, vol. 38, no. 11, pp. 1733–1742, 1999.
- E. Hanse and B. Gustafsson, “Quantal variability at glutamatergic synapses in area CA1 of the rat neonatal hippocampus,” Journal of Physiology, vol. 531, no. 2, pp. 467–480, 2001.
- Z. F. Mainen and T. J. Sejnowski, “Reliability of spike timing in neocortical neurons,” Science, vol. 268, no. 5216, pp. 1503–1506, 1995.
- G. T. Buracas, A. M. Zador, M. R. DeWeese, and T. D. Albright, “Efficient discrimination of temporal patterns by motion-sensitive neurons in primate visual cortex,” Neuron, vol. 20, no. 5, pp. 959–969, 1998.
- Y. Prut, E. Vaadia, H. Bergman, I. Haalman, H. Slovin, and M. Abeles, “Spatiotemporal structure of cortical activity: properties and behavioral relevance,” Journal of Neurophysiology, vol. 79, no. 6, pp. 2857–2874, 1998.
- M. N. Shadlen and W. T. Newsome, “Noise, neural codes and cortical organization,” Current Opinion in Neurobiology, vol. 4, no. 4, pp. 569–579, 1994.
- G. Buzsaki and J. J. Chrobak, “Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks,” Current Opinion in Neurobiology, vol. 5, no. 4, pp. 504–510, 1995.
- B. J. Richmond, M. W. Oram, and M. C. Wiener, “Response features determining spike times,” Neural Plasticity, vol. 6, no. 4, pp. 133–145, 1999.
- T. Weiss, R. W. Veh, and U. Heinemann, “Dopamine depresses cholinergic oscillatory network activity in rat hippocampus,” European Journal of Neuroscience, vol. 18, no. 9, pp. 2573–2580, 2003.
- J. E. Mikkonen, J. Huttunen, and M. Penttonen, “Contribution of a single CA3 neuron to network synchrony,” NeuroImage, vol. 31, no. 3, pp. 1222–1227, 2006.
- J. A. White, M. I. Banks, R. A. Pearce, and N. J. Kopell, “Networks of interneurons with fast and slow gamma-aminobutyric acid type A (GABA(A)) kinetics provide substrate for mixed gamma-theta rhythm,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 14, pp. 8128–8133, 2000.
- N. Axmacher and R. Miles, “Intrinsic cellular currents and the temporal precision of EPSP-action potential coupling in CA1 pyramidal cells,” Journal of Physiology, vol. 555, no. 3, pp. 713–725, 2004.
- Y. Yang, M. R. DeWeese, G. H. Otazu, and A. M. Zador, “Millisecond-scale differences in neural activity in auditory cortex can drive decisions,” Nature Neuroscience, vol. 11, no. 11, pp. 1262–1263, 2008.
- P. Maršálek, “Coincidence detection in the Hodgkin-Huxley equations,” BioSystems, vol. 58, no. 1–3, pp. 83–91, 2000.
- T. M. Hospedales, M. C. van Rossum, B. P. Graham, and M. B. Dutia, “Implications of noise and neural heterogeneity for vestibulo-ocular reflex fidelity,” Neural Computation, vol. 20, no. 3, pp. 756–778, 2008.
- A. Saarinen, M. L. Linne, and O. Yli-Harja, “Stochastic differential equation model for cerebellar granule cell excitability,” PLoS Computational Biology, vol. 4, no. 2, Article ID E1000004, 2008.