Calculation of Interspike Intervals for Integrate-and-Fire Neurons with Poisson Distribution of Synaptic Inputs

We present a new technique for calculating the interspike intervals of integrate-and-fire neurons. There are two new components to this technique. First, the probability density of the summed potential is calculated by integrating over the distribution of arrival times of the afferent post-synaptic potentials (PSPs), rather than using conventional stochastic differential equation techniques. A general formulation of this technique is given in terms of the probability distribution of the inputs and the time course of the postsynaptic response. The expressions are evaluated in the gaussian approximation, which gives results that become more accurate for large numbers of small-amplitude PSPs. Second, the probability density of output spikes, which are generated when the potential reaches threshold, is given in terms of an integral involving a conditional probability density. This expression is a generalization of the renewal equation, but it holds for both leaky neurons and situations in which there is no time-translational invariance. The conditional probability density of the potential is calculated using the same technique of integrating over the distribution of arrival times of the afferent PSPs. For inputs with a Poisson distribution, the known analytic solutions for both the perfect integrator model and the Stein model (which incorporates membrane potential leakage) in the diffusion limit are obtained. The interspike interval distribution may also be calculated numerically for models that incorporate both membrane potential leakage and a finite rise time of the postsynaptic response. Plots of the relationship between input and output firing rates, as well as the coefficient of variation, are given, and inputs with varying rates and amplitudes, including inhibitory inputs, are analyzed. The results indicate that neurons functioning near their critical threshold, where the inputs are just sufficient to cause firing, display a large variability in their spike timings.

[1]  Christof Koch,et al.  Cortical Cells Should Fire Regularly, But Do Not , 1999, Neural Computation.

[2]  Shigeru Tanaka,et al.  Stochastic resonance in a model neuron with reset , 1996, physics/9611014.

[3]  J. Jack,et al.  Electric current flow in excitable cells , 1975 .

[4]  Haim Sompolinsky,et al.  Chaotic Balanced State in a Model of Cortical Circuits , 1998, Neural Computation.

[5]  Henry C. Tuckwell,et al.  Introduction to theoretical neurobiology , 1988 .

[6]  W. Press,et al.  Numerical Recipes in Fortran: The Art of Scientific Computing.@@@Numerical Recipes in C: The Art of Scientific Computing. , 1994 .

[7]  H. Sompolinsky,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 1996, Science.

[8]  R. Stein A THEORETICAL ANALYSIS OF NEURONAL VARIABILITY. , 1965, Biophysical journal.

[9]  W. Gerstner,et al.  Time structure of the activity in neural network models. , 1995, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[10]  Wulfram Gerstner,et al.  Reduction of the Hodgkin-Huxley Equations to a Single-Variable Threshold Model , 1997, Neural Computation.

[11]  H. Tuckwell Introduction to Theoretical Neurobiology: Linear Cable Theory and Dendritic Structure , 1988 .

[12]  H C Tuckwell,et al.  Firing rates of neurons with random excitation and inhibition. , 1979, Journal of theoretical biology.

[13]  Michael N. Shadlen,et al.  Noise, neural codes and cortical organization , 1994, Current Opinion in Neurobiology.

[14]  William Bialek,et al.  Reliability and information transmission in spiking neurons , 1992, Trends in Neurosciences.

[15]  J. J. Hopfield,et al.  Pattern recognition computation using action potential timing for stimulus representation , 1995, Nature.

[16]  G M Clark,et al.  Intracellular responses of the rat cochlear nucleus to sound and its role in temporal coding , 1997, Neuroreport.

[17]  Kazuyuki Aihara,et al.  Pulse propagation networks: A neural network model that uses temporal coding by action potentials , 1993, Neural Networks.

[18]  Henry C. Tuckwell,et al.  Stochastic processes in the neurosciences , 1989 .

[19]  R. Douglas,et al.  Opening the grey box , 1991, Trends in Neurosciences.

[20]  Marius Usher,et al.  The Effect of Synchronized Inputs at the Single Neuron Level , 1994, Neural Computation.

[21]  W. S. Rhode,et al.  Encoding timing and intensity in the ventral cochlear nucleus of the cat. , 1986, Journal of neurophysiology.

[22]  Terrence J. Sejnowski,et al.  RAPID STATE SWITCHING IN BALANCED CORTICAL NETWORK MODELS , 1995 .

[23]  Moshe Abeles,et al.  Corticonics: Neural Circuits of Cerebral Cortex , 1991 .

[24]  I. Miller Probability, Random Variables, and Stochastic Processes , 1966 .

[25]  Anthony N. Burkitt,et al.  Analysis of Integrate-and-Fire Neurons: Synchronization of Synaptic Input and Spike Output , 1999, Neural Computation.

[26]  W. Singer Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[27]  M. Abeles Local Cortical Circuits: An Electrophysiological Study , 1982 .

[28]  A. Hill The Basis of Sensation: the Action of the Sense Organs , 1929, Nature.

[29]  Christof Koch,et al.  Coding of Time-Varying Signals in Spike Trains of Integrate-and-Fire Neurons with Random Threshold , 1999, Neural Computation.

[30]  Wolfgang Maass,et al.  Lower Bounds for the Computational Power of Networks of Spiking Neurons , 1996, Neural Computation.

[31]  B Gluss,et al.  A model for neuron firing with exponential decay of potential resulting in diffusion equations for probability density. , 1967, The Bulletin of mathematical biophysics.

[32]  Anthony N. Burkitt,et al.  Synchronization of the Neural Response to Noisy Periodic Synaptic Input , 2001, Neural Computation.

[33]  B. Mandelbrot,et al.  RANDOM WALK MODELS FOR THE SPIKE ACTIVITY OF A SINGLE NEURON. , 1964, Biophysical journal.

[34]  John H. R. Maunsell,et al.  On the relationship between synaptic input and spike output jitter in individual neurons. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[35]  H C Tuckwell,et al.  Synaptic transmission in a model for stochastic neural activity. , 1979, Journal of theoretical biology.

[36]  H C Tuckwell Onstochastic models of the activity of single neurons. , 1977, Journal of theoretical biology.

[37]  Shin Ishii,et al.  Gaussian Process Approach to Spiking Neurons for Inhomogeneous Poisson Inputs , 2001, Neural Computation.

[38]  William R. Softky,et al.  Sub-millisecond coincidence detection in active dendritic trees , 1994, Neuroscience.

[39]  P Lánský,et al.  On approximations of Stein's neuronal model. , 1984, Journal of theoretical biology.

[40]  R. Stein Some models of neuronal variability. , 1967, Biophysical journal.

[41]  Catherine E. Carr,et al.  Evolution of Time Coding Systems , 1999, Neural Computation.

[42]  D. Snodderly,et al.  Response Variability of Neurons in Primary Visual Cortex (V1) of Alert Monkeys , 1997, The Journal of Neuroscience.

[43]  G. M. Clark,et al.  input and spike output in neural systems , 1998 .

[44]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[45]  William R. Softky,et al.  The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  W. Singer,et al.  Temporal coding in the visual cortex: new vistas on integration in the nervous system , 1992, Trends in Neurosciences.

[47]  Christof Koch,et al.  Biophysics of Computation: Information Processing in Single Neurons (Computational Neuroscience Series) , 1998 .

[48]  A. Burkitt,et al.  Temporal processing from the auditory nerve to the medial nucleus of the trapezoid body in the rat , 2001, Hearing Research.

[49]  D. Georgescauld Local Cortical Circuits, An Electrophysiological Study , 1983 .

[50]  Kenneth D. Miller,et al.  Physiological Gain Leads to High ISI Variability in a Simple Model of a Cortical Regular Spiking Cell , 1997, Neural Computation.

[51]  William H. Press,et al.  Numerical Recipes in FORTRAN - The Art of Scientific Computing, 2nd Edition , 1987 .

[52]  P Lánský,et al.  On the interspike intervals calculated from diffusion approximations of Stein's neuronal model with reversal potentials. , 1994, Journal of theoretical biology.

[53]  Satish Iyengar,et al.  Modeling neural activity using the generalized inverse Gaussian distribution , 1997, Biological Cybernetics.

[54]  Athanasios Papoulis,et al.  Probability, Random Variables and Stochastic Processes , 1965 .

[55]  H. Tuckwell,et al.  Accuracy of neuronal interspike times calculated from a diffusion approximation. , 1980, Journal of theoretical biology.

[56]  H C Tuckwell,et al.  Neuronal interspike time histograms for a random input model. , 1978, Biophysical journal.

[57]  Anthony N. Burkitt Balanced neurons: analysis of leaky integrate-and-fire neurons with reversal potentials , 2001, Biological Cybernetics.

[58]  M. Abeles Role of the cortical neuron: integrator or coincidence detector? , 1982, Israel journal of medical sciences.