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Extracting Information from the Power Spectrum of Synaptic Noise

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Abstract

In cortical neurons, synaptic “noise” is caused by the nearly random release of thousands of synapses. Few methods are presently available to analyze synaptic noise and deduce properties of the underlying synaptic inputs. We focus here on the power spectral density (PSD) of several models of synaptic noise. We examine different classes of analytically solvable kinetic models for synaptic currents, such as the “delta kinetic models,” which use Dirac delta functions to represent the activation of the ion channel. We first show that, for this class of kinetic models, one can obtain an analytic expression for the PSD of the total synaptic conductance and derive equivalent stochastic models with only a few variables. This yields a method for constraining models of synaptic currents by analyzing voltage-clamp recordings of synaptic noise. Second, we show that a similar approach can be followed for the PSD of the the membrane potential (V m ) through an effective-leak approximation. Third, we show that this approach is also valid for inputs distributed in dendrites. In this case, the frequency scaling of the V m PSD is preserved, suggesting that this approach may be applied to intracellular recordings of real neurons. In conclusion, using simple mathematical tools, we show that V m recordings can be used to constrain kinetic models of synaptic currents, as well as to estimate equivalent stochastic models. This approach, therefore, provides a direct link between intracellular recordings in vivo and the design of models consistent with the dynamics and spectral structure of synaptic noise.

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References

  • Bernander Ö, Douglas RJ, Martin KAC, Koch C (1991) Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc. Natl. Acad. Sci. USA 88: 11569–11573.

    Google Scholar 

  • Brunel N, Chance FS, Fourcaud N, Abbott LF (2001) Effects of synaptic noise and filtering on the frequency response of spiking neurons. Phys. Rev. Lett. 86: 2186–2189.

    Google Scholar 

  • Brunel N, Wang XJ (2001) Effects of neuromodulation in a cortical network model of object working memory dominated by recurrent inhibition. J. Comput. Neurosci. 11: 63–85.

    Google Scholar 

  • Campbell N (1909) The study of discontinuous phenomena. Proc. Cambr. Phil. Soc. 15: 117–136.

    Google Scholar 

  • Chance FS, Abbott LF, Reyes AD (2002). Gain modulation from background synaptic input. Neuron. 35: 773–782.

    Google Scholar 

  • Clements JD (1996). Transmitter time course in the synaptic cleft: Its role into central synaptic function. Trends Neurosci. 19: 163–171.

    Google Scholar 

  • Cragg BG (1967) The density of synapses and neurones in the motor and visual areas of the cerebral cortex. J. Anat. 101: 639–654.

    Google Scholar 

  • Dayan P, Abbott LF (2001). Theoretical Neuroscience. MIT Press, Cambridge, MA.

    Google Scholar 

  • DeFelipe J, Fariñas I (1992) The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs. Prog. Neurobiol. 39: 563–607.

    Google Scholar 

  • DeFelipe J, Alonso-Nanclares L, Arellano JI (2002) Microstructure of the neocortex: Comparative aspects. J. Neurocytol. 31: 299–316.

    Google Scholar 

  • Evarts EV (1964) Temporal patterns of discharge of pyramidal tract neurons during sleep and waking in the monkey. J. Neurophysiol. 27: 152–171.

    Google Scholar 

  • Destexhe A, Mainen ZF, Sejnowski TJ (1994) Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. J. Comput. Neurosci. 1: 195–230.

    Google Scholar 

  • Destexhe A, Paré D(1999) Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J. Neurophysiol. 81: 1531–1547.

    Google Scholar 

  • Destexhe A, Rudolph M, Fellous J-M, Sejnowski TJ (2001) Fluctuating synaptic conductances recreate in-vivo-like activity in neocortical neurons. {Neuroscience} 107: 13–24.

    Google Scholar 

  • Doiron B, Longtin A, Berman N, Maler L (2000) Subtractive and divisible inhibition: Effect of voltage-dependent inhibitory conductances and noise. Neural Comput. 13: 227–248.

    Google Scholar 

  • Fellous J-M, Rudolph M, Destexhe A, Sejnowski TJ (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.

    Google Scholar 

  • Gerstner W, Kistler W (2002) Spiking Neuron Models. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Hanson FB, Tuckwell HC (1983) Diffusion approximation for neuronal activity including reversal potentials. J. Theor. Neurobiol. 2: 127–153.

    Google Scholar 

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

    Google Scholar 

  • Johannesma PIM (1968) Diffusion models of the stochastic activity of neurons. In: Caianello ER (ed.), Neural Networks. Springer, Berlin, pp. 116–144.

    Google Scholar 

  • Koch C (1999) Biophysics of Computation. Oxford University Press, Oxford, UK.

    Google Scholar 

  • Lánský P, Lánská V(1987) Diffusion approximation of the neuronal model with synaptic reversal potentials. Biol. Cybern. 56: 19–26.

    Google Scholar 

  • Lánský P, Rodriguez R (1999) Two-compartment stochastic model of a neuron. Physica D. 132: 267–286.

    Google Scholar 

  • Lánský P, Rospars JP (1995) Ornstein-Uhlenbeck model neuron revisited. Biol. Cybern. 72: 397–406.

    Google Scholar 

  • Lowen SB and Teich MC (1990) Power-law shot noise. IEEE Trans. Inform. Theory 36: 1302–1318.

    Google Scholar 

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

    Google Scholar 

  • Matsumura M, Cope T, Fetz EE (1988) Sustained excitatory synaptic input to motor cortex neurons in awake animals revealed by intracellular recording of membrane potentials. Exp. Brain Res. 70: 463–469.

    Google Scholar 

  • Mattia M, Del Giudice P. (2000) Efficient event-driven simulation of large networks of spiking neurons and dynamical synapses. Neural Comput. 12: 2305–2329.

    Google Scholar 

  • Papoulis A (1991) Probability, Random Variables, and Stochastic Processes. McGraw-Hill, Boston, MA.

  • Prescott SA, De Koninck Y (2003) Gain control of firing rate by shunting inhibition: Roles of synaptic noise and dendritic saturation. Proc. Natl. Acad. Sci. USA 100: 2076–2081.

    Google Scholar 

  • Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1986) Numerical Recipes. The Art of Scientific Computing. Cambridge University Press, Cambridge, MA.

  • Rapp M, Yarom Y, Segev I (1992) The impact of parallel fiber background activity on the cable properties of cerebellar purkinje cells. Neural Comput. 4: 518–533.

    Google Scholar 

  • Ricciardi LM (1976) On the transformation of diffusion processes into the Wiener process. J. Math. Analysis Appl. 54: 185–199.

    Google Scholar 

  • Rudolph M, Destexhe A (2003a) A fast-conducting, stochastic integrative mode for neocortical dendrites in vivo. J. Neurosci. 23: 2466–2476.

    Google Scholar 

  • Rudolph M, Destexhe A(2003b) The discharge variability of neocortical neurons during high-conductance states. Neuroscience 119: 855–87

  • 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.

    Google Scholar 

  • Steriade M (1978) Cortical long-axoned cells and putative interneurons during the sleep-waking cycle. Behav. Brain Sci. 3: 465–514.

    Google Scholar 

  • Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: A view from inside neocortical neurons. J. Neurophysiol. 85: 1969–1985.

    Google Scholar 

  • Szentagothai J (1965) The use of degeneration in the investigation of short neuronal connections. In: M Singer, JP Shade, (eds.) Progress in Brain Research, vol. 14. Elsevier Science Publishers, Amsterdam, pp. 1-32.

    Google Scholar 

  • Tiesinga PHE, José JV, Sejnowski TJ (2000) Comparison of current-driven and conductance-driven neocortical model neurons with Hodgkin-Huxley voltage-gated channels. Phys. Rev. E 62: 8413–8419.

    Google Scholar 

  • Tuckwell HC, Wan FYM, Rospars JP (2002) A spatial stochastic neuronal model with Ornstein-Uhlenbeck input current. Biol. Cybern. 86: 137–145.

    Google Scholar 

  • Uhlenbeck GE, Ornstein LS (1930). On the theory of the Brownian motion. Phys. Rev. 36: 823–841.

    Google Scholar 

  • van Rossum MCW (2001) The transient precision of integrate and fire neurons: Effect of background activity and noise. J. Comput. Neurosci. 10: 303–311.

    Google Scholar 

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Destexhe, A., Rudolph, M. Extracting Information from the Power Spectrum of Synaptic Noise. J Comput Neurosci 17, 327–345 (2004). https://doi.org/10.1023/B:JCNS.0000044875.90630.88

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