Correlation between uncoupled conductance-based integrate-and-fire neurons due to common and synchronous presynaptic firing

We investigate the firing characteristics of conductance-based integrate-and-fire neurons and the correlation of firing for uncoupled pairs of neurons as a result of common input and synchronous firing of multiple synaptic inputs. Analytical approximations are derived for the moments of the steady state potential and the effective time constant. We show that postsynaptic firing barely depends on the correlation between inhibitory inputs; only the inhibitory firing rate matters. In contrast, both the degree of synchrony and the firing rate of excitatory inputs are relevant. A coefficient of variation CV > 1 can be attained with low inhibitory firing rates and (Poisson-modulated) synchronized excitatory synaptic input, where both the number of presynaptic neurons in synchronous firing assemblies and the synchronous firing rate should be sufficiently large. The correlation in firing of a pair of uncoupled neurons due to common excitatory input is initially increased for increasing firing rates of independent inhibitory inputs but decreases for large inhibitory firing rates. Common inhibitory input to a pair of uncoupled neurons barely induces correlated firing, but amplifies the effect of common excitation. Synchronous firing assemblies in the common input further enhance the correlation and are essential to attain experimentally observed correlation values. Since uncorrelated common input (i.e., common input by neurons, which do not fire in synchrony) cannot induce sufficient postsynaptic correlation, we conclude that lateral couplings are essential to establish clusters of synchronously firing neurons.     

Theory of input spike auto- and cross-correlations and their effect on the response of spiking neurons

Spike correlations between neurons are ubiquitous in the cortex, but their role is not understood. Here we describe the firing response of a leaky integrate-and-fire neuron (LIF) when it receives a temporarily correlated input generated by presynaptic correlated neuronal populations. Input correlations are characterized in terms of the firing rates, Fano factors, correlation coefficients, and correlation timescale of the neurons driving the target neuron. We show that the sum of the presynaptic spike trains cannot be well described by a Poisson process. In fact, the total input current has a nontrivial two-point correlation function described by two main parameters: the correlation timescale (how precise the input correlations are in time) and the correlation magnitude (how strong they are). Therefore, the total current generated by the input spike trains is not well described by a white noise gaussian process. Instead, we model the total current as a colored gaussian process with the same mean and two-point correlation function, leading to the formulation of the problem in terms of a Fokker-Planck equation. Solutions of the output firing rate are found in the limit of short and long correlation timescales. The solutions described here expand and improve on our previous results (Moreno, de la Rocha, Renart, & Parga, 2002) by presenting new analytical expressions for the output firing rate for general IF neurons, extending the validity of the results for arbitrarily large correlation magnitude, and by describing the differential effect of correlations on the mean-driven or noise-dominated firing regimes. Also the details of this novel formalism are given here for the first time. We employ numerical simulations to confirm the analytical solutions and study the firing response to sudden changes in the input correlations. We expect this formalism to be useful for the study of correlations in neuronal networks and their role in neural processing and information transmission.     

Integrate-and-fire neurons driven by correlated stochastic input

Neurons are sensitive to correlations among synaptic inputs. However, analytical models that explicitly include correlations are hard to solve analytically, so their influence on a neuron's response has been difficult to ascertain. To gain some intuition on this problem, we studied the firing times of two simple integrate-and-fire model neurons driven by a correlated binary variable that represents the total input current. Analytic expressions were obtained for the average firing rate and coefficient of variation (a measure of spike-train variability) as functions of the mean, variance, and correlation time of the stochastic input. The results of computer simulations were in excellent agreement with these expressions. In these models, an increase in correlation time in general produces an increase in both the average firing rate and the variability of the output spike trains. However, the magnitude of the changes depends differentially on the relative values of the input mean and variance: the increase in firing rate is higher when the variance is large relative to the mean, whereas the increase in variability is higher when the variance is relatively small. In addition, the firing rate always tends to a finite limit value as the correlation time increases toward infinity, whereas the coefficient of variation typically diverges. These results suggest that temporal correlations may play a major role in determining the variability as well as the intensity of neuronal spike trains.     

Dynamics of the firing probability of noisy integrate-and-fire neurons

Cortical neurons in vivo undergo a continuous bombardment due to synaptic activity, which acts as a major source of noise. Here, we investigate the effects of the noise filtering by synapses with various levels of realism on integrate-and-fire neuron dynamics. The noise input is modeled by white (for instantaneous synapses) or colored (for synapses with a finite relaxation time) noise. Analytical results for the modulation of firing probability in response to an oscillatory input current are obtained by expanding a Fokker-Planck equation for small parameters of the problem - when both the amplitude of the modulation is small compared to the background firing rate and the synaptic time constant is small compared to the membrane time constant. We report here the detailed calculations showing that if a synaptic decay time constant is included in the synaptic current model, the firing-rate modulation of the neuron due to an oscillatory input remains finite in the high-frequency limit with no phase lag. In addition, we characterize the low-frequency behavior and the behavior of the high-frequency limit for intermediate decay times. We also characterize the effects of introducing a rise time to the synaptic currents and the presence of several synaptic receptors with different kinetics. In both cases, we determine, using numerical simulations, an effective decay time constant that describes the neuronal response completely.     

Modified firing-rate model reproduces synchronization of a neuronal population receiving complex input

Synchronization plays important role in generation of brain activity patterns. Experimental data show that neurons demonstrate more reproducible activity for noise-like input than for constant current injection, and that effect can not be reproduced by standard oversimplified Firing-Rate (FR) models. The paper proposes a modification of FR model which reproduces these kinds of activity. The FR model approximates the firing rate of an infinite number of leaky integrate-and-fire neurons, considered as a population, and in contrary to conventional models it accounts for not only a steady-state firing regime but a fast rising excitation as well. Comparison of our simulations with the experimental data shows that the synchronous firing of the neuronal population strongly depends on the synchrony of neuronal states just before spiking. This effect is reproduced by the proposed FR model in contrary to the conventional FR models and is in agreement with the direct Monte-Carlo simulation of individual neurons.     

Gain control by concerted changes in I(A) and I(H) conductances

Stability of intrinsic electrical activity and modulation of input-output gain are both important for neuronal information processing. It is therefore of interest to define biologically plausible parameters that allow these two features to coexist. Recent experiments indicate that in some biological neurons, the stability of spontaneous firing can arise from coregulated expression of the electrophysiologically opposing I(A) and I(H) currents. Here, I show that such balanced changes in I(A) and I(H) dramatically alter the slope of the relationship between the firing rate and driving current in a Hodgkin-Huxley-type model neuron. Concerted changes in I(A) and I(H) can thus control neuronal gain while preserving intrinsic activity.     

Higher-order statistics of input ensembles and the response of simple model neurons

Pairwise correlations among spike trains recorded in vivo have been frequently reported. It has been argued that correlated activity could play an important role in the brain, because it efficiently modulates the response of a postsynaptic neuron. We show here that a neuron's output firing rate critically depends on the higher-order statistics of the input ensemble. We constructed two statistical models of populations of spiking neurons that fired with the same rates and had identical pairwise correlations, but differed with regard to the higher-order interactions within the population. The first ensemble was characterized by clusters of spikes synchronized over the whole population. In the second ensemble, the size of spike clusters was, on average, proportional to the pairwise correlation. For both input models, we assessed the role of the size of the population, the firing rate, and the pairwise correlation on the output rate of two simple model neurons: a continuous firing-rate model and a conductance-based leaky integrate-and-fire neuron. An approximation to the mean output rate of the firing-rate neuron could be derived analytically with the help of shot noise theory. Interestingly, the essential features of the mean response of the two neuron models were similar. For both neuron models, the three input parameters played radically different roles with respect to the postsynaptic firing rate, depending on the interaction structure of the input. For instance, in the case of an ensemble with small and distributed spike clusters, the output firing rate was efficiently controlled by the size of the input population. In addition to the interaction structure, the ratio of inhibition to excitation was found to strongly modulate the effect of correlation on the postsynaptic firing rate.     

Bayesian spiking neurons I: inference

We show that the dynamics of spiking neurons can be interpreted as a form of Bayesian inference in time. Neurons that optimally integrate evidence about events in the external world exhibit properties similar to leaky integrate-and-fire neurons with spike-dependent adaptation and maximally respond to fluctuations of their input. Spikes signal the occurrence of new information-what cannot be predicted from the past activity. As a result, firing statistics are close to Poisson, albeit providing a deterministic representation of probabilities.     

The relationship between synchronization among neuronal populations and their mean activity levels.

In the past decade the importance of synchronized dynamics in the brain has emerged from both empirical and theoretical perspectives. Fast dynamic synchronous interactions of an oscillatory or nonoscillatory nature may constitute a form of temporal coding that underlies feature binding and perceptual synthesis. The relationship between synchronization among neuronal populations and the population firing rates addresses two important issues: the distinction between rate coding and synchronization coding models of neuronal interactions and the degree to which empirical measurements of population activity, such as those employed by neuroimaging, are sensitive to changes in synchronization. We examined the relationship between mean population activity and synchronization using biologically plausible simulations. In this article, we focus on continuous stationary dynamics. (In a companion article, Chawla (forthcoming), we address the same issue using stimulus-evoked transients.) By manipulation parameters such as extrinsic input, intrinsic noise, synaptic efficacy, density of extrinsic connections, the voltage-sensitive nature of postsynaptic mechanisms, the number of neurons, and the laminar structure within the populations, we were able to introduce variations in both mean activity and synchronization under a variety of simulated neuronal architectures. Analyses of the simulated spike trains and local field potentials showed that in nearly every domain of the model's parameter space, mean activity and synchronization were tightly coupled. This coupling appears to be mediated by an increase in synchronous gain when effective membrane time constants are lowered by increased activity. These observations show that under the assumptions implicit in our models, rate coding and synchrony coding in neural systems with reciprocal interconnections are two perspectives on the same underlying dynamic. This suggests that in the absence of specific mechanisms decoupling changes in synchronization from firing levels, indexes of brain activity that are based purely on synaptic activity (e.g., functional magnetic resonance imaging) may also be sensitive to changes in synchronous coupling.     

An invariance principle for maintaining the operating point of a neuron

Sensory neurons adapt to changes in the natural statistics of their environments through processes such as gain control and firing threshold adjustment. It has been argued that neurons early in sensory pathways adapt according to information-theoretic criteria, perhaps maximising their coding efficiency or information rate. Here, we draw a distinction between how a neuron's preferred operating point is determined and how its preferred operating point is maintained through adaptation. We propose that a neuron's preferred operating point can be characterised by the probability density function (PDF) of its output spike rate, and that adaptation maintains an invariant output PDF, regardless of how this output PDF is initially set. Considering a sigmoidal transfer function for simplicity, we derive simple adaptation rules for a neuron with one sensory input that permit adaptation to the lower-order statistics of the input, independent of how the preferred operating point of the neuron is set. Thus, if the preferred operating point is, in fact, set according to information-theoretic criteria, then these rules nonetheless maintain a neuron at that point. Our approach generalises from the unimodal case to the multimodal case, for a neuron with inputs from distinct sensory channels, and we briefly consider this case too.     

Rate limitations of unitary event analysis

Unitary event analysis is a new method for detecting episodes of synchronized neural activity (Riehle, Grün, Diesmann, & Aertsen, 1997). It detects time intervals that contain coincident firing at higher rates than would be expected if the neurons fired as independent inhomogeneous Poisson processes; all coincidences in such intervals are called unitary events (UEs). Changes in the frequency of UEs that are correlated with behavioral states may indicate synchronization of neural firing that mediates or represents the behavioral state. We show that UE analysis is subject to severe limitations due to the underlying discrete statistics of the number of coincident events. These limitations are particularly stringent for low (0-10 spikes/s) firing rates. Under these conditions, the frequency of UEs is a random variable with a large variation relative to its mean. The relative variation decreases with increasing firing rate, and we compute the lowest firing rate, at which the 95% confidence interval around the mean frequency of UEs excludes zero. This random variation in UE frequency makes interpretation of changes in UEs problematic for neurons with low firing rates. As a typical example, when analyzing 150 trials of an experiment using an averaging window 100 ms wide and a 5 ms coincidence window, firing rates should be greater than 7 spikes per second.     

The effect of NMDA receptors on gain modulation

The ability of individual neurons to modulate the gain of their input-output function is important for information processing in the brain. In a recent study, shunting inhibition was found to modulate the gain of cerebellar granule cells subjected to simulated currents through AMPA receptor synapses. Here we investigate the effect on gain modulation resulting from adding the currents mediated by NMDA receptors to a compartmental model of the granule cell. With only AMPA receptors, the changes in gain induced by shunting inhibition decreased gradually with the average firing rate of the afferent mossy fibers. With NMDA receptors present, this decrease was more rapid, therefore narrowing the bandwidth of mossy fiber firing rates available for gain modulation. The deterioration of gain modulation was accompanied by a reduced variability of the input current and saturation of NMDA receptors. However, when the output of the granule cell was plotted as a function of the average input current instead of the input firing frequency, both models showed very similar response curves and comparable gain modulation. We conclude that NMDA receptors do not directly impair gain control by shunting inhibition, but the effective bandwidth decreases as a consequence of the increased total charge transfer.     

The dynamics of integrate-and-fire: mean versus variance modulations and dependence on baseline parameters

The leaky integrate-and-fire (LIF) is the simplest neuron model that captures the essential properties of neuronal signaling. Yet common intuitions are inadequate to explain basic properties of LIF responses to sinusoidal modulations of the input. Here we examine responses to low and moderate frequency modulations of both the mean and variance of the input current and quantify how these responses depend on baseline parameters. Across parameters, responses to modulations in the mean current are low pass, approaching zero in the limit of high frequencies. For very low baseline firing rates, the response cutoff frequency matches that expected from membrane integration. However, the cutoff shows a rapid, supralinear increase with firing rate, with a steeper increase in the case of lower noise. For modulations of the input variance, the gain at high frequency remains finite. Here, we show that the low-frequency responses depend strongly on baseline parameters and derive an analytic condition specifying the parameters at which responses switch from being dominated by low versus high frequencies. Additionally, we show that the resonant responses for variance modulations have properties not expected for common oscillatory resonances: they peak at frequencies higher than the baseline firing rate and persist when oscillatory spiking is disrupted by high noise. Finally, the responses to mean and variance modulations are shown to have a complementary dependence on baseline parameters at higher frequencies, resulting in responses to modulations of Poisson input rates that are independent of baseline input statistics.     

Analytic expressions for rate and CV of a type I neuron driven by white gaussian noise

We study the one-dimensional normal form of a saddle-node system under the influence of additive gaussian white noise and a static "bias current" input parameter, a model that can be looked upon as the simplest version of a type I neuron with stochastic input. This is in contrast with the numerous studies devoted to the noise-driven leaky integrate-and-fire neuron. We focus on the firing rate and coefficient of variation (CV) of the interspike interval density, for which scaling relations with respect to the input parameter and noise intensity are derived. Quadrature formulas for rate and CV are numerically evaluated and compared to numerical simulations of the system and to various approximation formulas obtained in different limiting cases of the model. We also show that caution must be used to extend these results to the Theta neuron model with multiplicative gaussian white noise. The correspondence between the first passage time statistics for the saddle-node model and the Theta neuron model is obtained only in the Stratonovich interpretation of the stochastic Theta neuron model, while previous results have focused only on the Ito interpretation. The correct Stratonovich interpretation yields CVs that are still relatively high, although smaller than in the Ito interpretation; it also produces certain qualitative differences, especially at larger noise intensities. Our analysis provides useful relations for assessing the distance to threshold and the level of synaptic noise in real type I neurons from their firing statistics. We also briefly discuss the effect of finite boundaries (finite values of threshold and reset) on the firing statistics.     

Stable propagation of activity pulses in populations of spiking neurons

We investigate the propagation of pulses of spike activity in a neuronal network with feedforward couplings. The neurons are of the spike-response type with a firing probability that depends linearly on the membrane potential. After firing, neurons enter a phase of refractoriness. Spike packets are described in terms of the moments of the firing-time distribution so as to allow for an analytical treatment of the evolution of the spike packet as it propagates from one layer to the next. Analytical results and simulations show that depending on the synaptic coupling strength, a stable propagation of the packet with constant waveform is possible. Crucial for this observation is neither the existence of a firing threshold nor a sigmoidal gain function--both are absent in our model--but the refractory behavior of the neurons.     

Stochastic synchrony of chaos in a pulse-coupled neural network with both chemical and electrical synapses among inhibitory neurons

The synchronous firing of neurons in a pulse-coupled neural network composed of excitatory and inhibitory neurons is analyzed. The neurons are connected by both chemical synapses and electrical synapses among the inhibitory neurons. When electrical synapses are introduced, periodically synchronized firing as well as chaotically synchronized firing is widely observed. Moreover, we find stochastic synchrony where the ensemble-averaged dynamics shows synchronization in the network but each neuron has a low firing rate and the firing of the neurons seems to be stochastic. Stochastic synchrony of chaos corresponding to a chaotic attractor is also found.     

Rate and synchrony in feedforward networks of coincidence detectors: analytical solution

We provide an analytical recurrent solution for the firing rates and cross-correlations of feedforward networks with arbitrary connectivity, excitatory or inhibitory, in response to steady-state spiking input to all neurons in the first network layer. Connections can go between any two layers as long as no loops are produced. Mean firing rates and pairwise cross-correlations of all input neurons can be chosen individually. We apply this method to study the propagation of rate and synchrony information through sample networks to address the current debate regarding the efficacy of rate codes versus temporal codes. Our results from applying the network solution to several examples support the following conclusions: (1) differential propagation efficacy of rate and synchrony to higher layers of a feedforward network is dependent on both network and input parameters, and (2) previous modeling and simulation studies exclusively supporting either rate or temporal coding must be reconsidered within the limited range of network and input parameters used. Our exact, analytical solution for feedforward networks of coincidence detectors should prove useful for further elucidating the efficacy and differential roles of rate and temporal codes in terms of different network and input parameter ranges.     

Run-length chain coding and scalable computation of a shape''s moments using reconfigurable optical buses

The main contribution of this paper is the design of several efficient algorithms for modified run-length chain coding and for computing a shape's moments on arrays with reconfigurable optical buses. The proposed algorithms are based on the boundary representation of an object. Instead of using chain code, the boundary can be represented by a modified run-length chain code, where each entity represents a line segment (two adjacent corner pixels). The sequential nature of the chain code makes it difficult to be parallelized. We first propose two constant time algorithms for boundary extraction and run-length chain coding. To the authors' knowledge, these are the most time efficient algorithms yet published. Based on the modified run-length chain coding, and the advantages of both optical transmission and electronic computation, a constant time parallel algorithm for computing a shape's moments using N x N processors is proposed. Additionally, instead of using N x N processors, a scalable moment algorithm using r x r processors is also derived, where r < N. Based on the product of time and the number of processors used, both proposed parallel algorithms are time and cost optimal.     

Stability and synchronization of random brain networks with a distribution of connection strengths

The impact of stability and synchronization of electrical activity on the structure of random brain networks with a distribution of connection strengths is investigated using a physiological model of brain activity. Connection strength is measured by the gain of the connection, which describes the effect of changes in the firing rate of neurons in one component on the neurons of another component. The stability of a network is calculated from the eigenvalue spectrum of the network's matrix of gains. Using random matrix theory, we predict and numerically verify the eigenvalue spectrum of randomly connected networks with gain values determined by a probability distribution. From the eigenvalue spectrum, the probability that a network is stable is calculated and shown to constrain the structural and physiological parameters of the network. In particular, stability constrains the variance of the gains. The complex vector of component amplitudes, or mode, corresponding to each dispersion root is an eigenvector of the network's gain matrix and is used to calculate the synchronization of each component's electrical activity. Synchronization is shown to decrease as the variance of the connection gain increases and inhibitory connections become more likely. Brain networks with large gain variance are shown to have multiple eigenvalues close to the stability boundary and to be partially synchronized. Such a network would have multiple partially synchronized modes strongly excited by a stimulus.