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Synaptic shot noise and conductance fluctuations affect the membrane voltage with equal significance

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Richardson, Magnus J. E. and Gerstner, Wulfram (2005) Synaptic shot noise and conductance fluctuations affect the membrane voltage with equal significance. Neural Computation, Vol.17 (No.4). pp. 923-947. ISSN 0899-7667

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Official URL: http://dx.doi.org/10.1162/0899766053429444

Abstract

The subthresholdmembranevoltage of a neuron in active cortical tissue is a fluctuating quantity with a distribution that reflects the firing statistics of the presynaptic population. It was recently found that conductancebased synaptic drive can lead to distributions with a significant skew. Here it is demonstrated that the underlying shot noise caused by Poissonian spike arrival also skews the membrane distribution, but in the opposite sense. Using a perturbative method, we analyze the effects of shot noise on the distribution of synaptic conductances and calculate the consequent voltage distribution. To first order in the perturbation theory, the voltage distribution is a gaussian modulated by a prefactor that captures the skew. The gaussian component is identical to distributions derived using current-based models with an effective membrane time constant. The well-known effective-time-constant approximation can therefore be identified as the leading-order solution to the full conductance-based model. The higher-order modulatory prefactor containing the skew comprises terms due to both shot noise and conductance fluctuations. The diffusion approximation misses these shot-noise effects implying that analytical approaches such as the Fokker-Planck equation or simulation with filtered white noise cannot be used to improve on the gaussian approximation. It is further demonstrated that quantities used for fitting theory to experiment, such as the voltage mean and variance, are robust against these non-Gaussian effects. The effective-time-constant approximation is therefore relevant to experiment and provides a simple analytic base on which other pertinent biological details may be added.

Item Type: Journal Item
Subjects: Q Science > QP Physiology
Divisions: Faculty of Science > Centre for Systems Biology
Library of Congress Subject Headings (LCSH): Neurons -- Mathematical models, Neural transmission -- Mathematical models, Cerebral cortex, Cell membranes
Journal or Publication Title: Neural Computation
Publisher: MIT Press
ISSN: 0899-7667
Date: April 2005
Volume: Vol.17
Number: No.4
Page Range: pp. 923-947
Identification Number: 10.1162/0899766053429444
Status: Peer Reviewed
Access rights to Published version: Restricted or Subscription Access
References: Brunel, N., Chance, F. S., Fourcaud, N., & Abbott, L. F. (2001). Effects of synaptic noise and filtering on the frequency response of spiking neurons. Phys. Rev. Lett., 86, 2186–2189. Burkitt, A. N. (2001). Balanced neurons: Analysis of leaky integrate-and-fire neurons with reversal potentials Biol. Cybern., 85, 247–255. Burkitt, A. N., & Clark, G. M. (1999). New technique for analyzing integrate and fire neurons. Neurocomputing, 26–27, 93–99. Burkitt A. N., Meffin, H., & Grayden, D. B. (2003). Study of neuronal gain in a conductance-based leaky integrate-and-fire neuron model with balanced excitatory and inhibitory synaptic input. Biol. Cybern., 89, 119–125. Chance, F. S., Abbott, L. F., & Reyes, A. D. (2002). Gain modulation from background synaptic input. Neuron, 35, 773–782. Destexhe, A., & Par´e, D. (1999). Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J. Neurophysiol., 81, 1531–1547. Destexhe, A., Rudolph, M., Fellous, J.-M., & Sejnowski, T. J. (2001). Fluctuating synaptic conductances recreate in vivo–like activity in neocortical neurons. Neuroscience, 107, 13–24. Destexhe, A., Rudolph, M., & Par´e, D. (2003). The high-conductance state of neocortical neurons in vivo. Nature Rev. Neurosci., 4, 739–751. Fellous, J.-M., Rudolph, M., Destexhe, A., & Sejnowski T. J. (2003). Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity. Neuroscience, 122, 811–829. Fourcaud, N., & Brunel, N. (2002). Dynamics of the firing probability of noisy integrate-and- fire neurons. Neural Comput., 14, 2057–2110. Gilbert, E. N.,&Pollak, H. O. (1960). Amplitude distributions of shot noise. Bell. Syst. Tech. J., 39, 333–350. Grande, L. A., Kinney, G. A., Miracle G. L., & SpainW. J. (2004). Dynamic influences on coincidence detection in neocortical pyramidal neurons. J. Neurosci., 24, 1839– 1851. Hahnloser, R. H. R. (2003). Stationary transmission distribution of random spike trains by dynamical synapses. Phys. Rev. E, 67, 022901. Hohn, N., & Burkitt, A. N. (2001). Shot noise in the leaky integrate-and-fire neuron. Phys. Rev. E, 63, 031902. Holmgren, C., Harkany, T., Svennenfors, B., & Zilberter, Y. (2003). Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J. Physiol. London., 551, 139–153. Johannesma, P. I. M. (1968). Diffusion models for the stochastic activity of neurons. In E. R. Caianello (Ed.), Neural networks (pp. 116–144). New York: Springer. Jolivet, R., Lewis, T. J., & Gerstner,W. (2004). Generalized integrate-and-fire models of neuronal activity approximate spike trains of a detailed model to a high degree of accuracy. J. Neurophysiol., 92, 959–976. KamondiA., Acsady, L.,Wang, X.-J.,&Buzsaki, G. (1998). Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: Activity-dependent phaseprecession of action potentials. Hippocampus, 8, 244–261. Kuhn, A., Aertsen, A., & Rotter, S. (2003). Higher-order statistics of input ensembles and the response of simple model neurons. Neural Comp., 15, 67–101. Kuhn, A., Aertsen, A., & Rotter, S. (2004). Neuronal integration of synaptic input in the fluctuation-driven regime. J. Neurosci., 24, 2345–2356. La Camera, G., Senn, W., & Fusi, S. (2004). Comparison between networks of conductance and current-driven neurons: Stationary spike rates and subthreshold depolarization. Neurocomputing, 58–60, 253–258. Lansky, P., & Lanska, V. (1987). Diffusion approximation of the neuronal model with synaptic reversal potentials. Biol. Cybern., 56, 19–26. Manwani, A., & Koch, C. (1999). Detecting and estimating signals in noisy cable structures, I: Neuronal noise sources. Neural Comp., 11, 1797–1829. Meffin, H., Burkitt, A. N.,&Grayden, D. B. (2004). An analytical model for the “large, fluctuating synaptic conductance state” typical of neocortical neurons in vivo. J. Comput. Neurosci., 16, 159–175. Monier, C., Chavane, F., Baudot, P., Graham, L. J., & Fr´egnac, Y. (2003). Orientation and direction selectivity of synaptic inputs in visual cortical neurons: A diversity of combinations produces spike tuning. Neuron, 37, 663–680. Prescott, S. A., & De Koninck, Y. (2003). Gain control of firing rate by shunting inhibition: Roles of synaptic noise and dendritic saturation. P. Natl. Acad. Sci., 100, 2076–2081. Rauch, A., La Camera, G., L¨ uscher, H.-R., Senn, W., & Fusi, S. (2003). Neocortical pyramidal cells respond as integrate-and-fire neurons to in vivo–like input currents. J. Neurophysiol., 90, 1598–1612. Richardson,M.J. E. (2004). Effects of synaptic conductance on the voltage distribution and firing rate of spiking neurons. Phys. Rev. E, 69, 051918. Risken, H. (1996). The Fokker-Planck equation. New York: Springer-Verlag. Rodriguez, M. A., Pesquera, L., San Miguel, M., & Sancho, J. M. (1985). Master equation description of external Poisson white noise in finite systems. J. Stat. Phys., 40, 669–724. Rubin, J., Lee, D. D., & Sompolinsky,H. (2001). Equilibrium properties of temporally asymmetric Hebbian plasticity. Phys. Rev. Lett., 86, 364–367. Rudolph, M., & Destexhe, A. (2003). Characterization of subthreshold voltage fluctuations in neuronal membranes. Neural Comput., 15, 2577–2618. Rudolph, M., Piwkowska Z., Badoual, M., Bal, T., & Destexhe, A. (2004). A method to estimate synaptic conductances from membrane potential fluctuations. J. Neurophysiol., 91, 2884–2896. Sanchez-Vives, M. V.,&McCormick, D. A. (2000). Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci., 3, 1027–1034. Silberberg, G.,Wu,C. Z.,&Markram, H. (2004). Synaptic dynamics control the timing of neuronal excitation in the activated neocortical microcircuit. J. Physiol-London, 556, 19–27. Stein, R. B. (1965). A theoretical analysis of neuronal activity. Biophys. J., 5, 173–193. Stein, R. B. (1967). Some models of neuronal variability. Biophys. J., 7, 37–68. Stroeve, S., & Gielen, S. (2001). Correlation between uncoupled conductance-based integrate-and-fire neurons due to common and synchronous presynaptic firing. Neural. Comp., 13, 2005–2029. Tiesinga, P. H. E., Jos´e, J. V., & Sejnowski, T. J. (2000). Comparison of currentdriven and conductance-driven neocortical model neurons with Hodgkin-Huxley voltage-gated currents. Phys. Rev. E, 62, 8413–8419. Tuckwell, H. C. (1979). Synaptic transmission in a model for stochastic neural activity. J. Theor. Biol., 77, 65–81. Tuckwell, H. C. (1989). Stochastic processes in the neurosciences. Philadelphia: SIAM. van Rossum, M. C.W., Bi, G. Q., & Turrigiano, G. C. (2000). Stable Hebbian learning from spike timing-dependent plasticity. J. Neurosci., 20, 8812–8821. Wan, F. Y. M.,&Tuckwell, H. C. (1979). The response of a spatially distributed neuron to white noise current injection. Biol. Cybern., 33, 39–55. Wilbur, W. J., & Rinzel, J. (1983). A theoretical basis for large coefficient of variation and bimodality in neuronal interspike distribution. J. Theor. Biol., 105, 345–368.
URI: http://wrap.warwick.ac.uk/id/eprint/34561

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