Short-term synaptic plasticity can enhance weak signal detectability in nonrenewal spike trains

We study the encoding of weak signals in spike trains with interspike interval (ISI) correlations and the signals' subsequent detection in sensory neurons. Motivated by the observation of negative ISI correlations in auditory and electrosensory afferents, we assess the theoretical performance limits of an individual detector neuron receiving a weak signal distributed across multiple afferent inputs. We assess the functional role of ISI correlations in the detection process using statistical detection theory and derive two sequential likelihood ratio detector models: one for afferents with renewal statistics; the other for afferents with negatively correlated ISIs. We suggest a mechanism that might enable sensory neurons to implicitly compute conditional probabilities of presynaptic spikes by means of short-term synaptic plasticity. We demonstrate how this mechanism can enhance a postsynaptic neuron's sensitivity to weak signals by exploiting the correlation structure of the input spike trains. Our model not only captures fundamental aspects of early electrosensory signal processing in weakly electric fish, but may also bear relevance to the mammalian auditory system and other sensory modalities.     

Including long-range dependence in integrate-and-fire models of the high interspike-interval variability of cortical neurons

Many different types of integrate-and-fire models have been designed in order to explain how it is possible for a cortical neuron to integrate over many independent inputs while still producing highly variable spike trains. Within this context, the variability of spike trains has been almost exclusively measured using the coefficient of variation of interspike intervals. However, another important statistical property that has been found in cortical spike trains and is closely associated with their high firing variability is long-range dependence. We investigate the conditions, if any, under which such models produce output spike trains with both interspike-interval variability and long-range dependence similar to those that have previously been measured from actual cortical neurons. We first show analytically that a large class of high-variability integrate-and-fire models is incapable of producing such outputs based on the fact that their output spike trains are always mathematically equivalent to renewal processes. This class of models subsumes a majority of previously published models, including those that use excitation-inhibition balance, correlated inputs, partial reset, or nonlinear leakage to produce outputs with high variability. Next, we study integrate-and-fire models that have (nonPoissonian) renewal point process inputs instead of the Poisson point process inputs used in the preceding class of models. The confluence of our analytical and simulation results implies that the renewal-input model is capable of producing high variability and long-range dependence comparable to that seen in spike trains recorded from cortical neurons, but only if the interspike intervals of the inputs have infinite variance, a physiologically unrealistic condition. Finally, we suggest a new integrate-and-fire model that does not suffer any of the previously mentioned shortcomings. By analyzing simulation results for this model, we show that it is capable of producing output spike trains with interspike-interval variability and long-range dependence that match empirical data from cortical spike trains. This model is similar to the other models in this study, except that its inputs are fractional-gaussian-noise-driven Poisson processes rather than renewal point processes. In addition to this model's success in producing realistic output spike trains, its inputs have long-range dependence similar to that found in most subcortical neurons in sensory pathways, including the inputs to cortex. Analysis of output spike trains from simulations of this model also shows that a tight balance between the amounts of excitation and inhibition at the inputs to cortical neurons is not necessary for high interspike-interval variability at their outputs. Furthermore, in our analysis of this model, we show that the superposition of many fractional-gaussian-noise-driven Poisson processes does not approximate a Poisson process, which challenges the common assumption that the total effect of a large number of inputs on a neuron is well represented by a Poisson process.     

Information encoding and computation with spikes and bursts

Neurons compute and communicate by transforming synaptic input patterns into output spike trains. The nature of this transformation depends crucially on the properties of voltage-gated conductances in neuronal membranes. These intrinsic membrane conductances can enable neurons to generate different spike patterns including brief, high-frequency bursts that are commonly observed in a variety of brain regions. Here we examine how the membrane conductances that generate bursts affect neural computation and encoding. We simulated a bursting neuron model driven by random current input signal and superposed noise. We consider two issues: the timing reliability of different spike patterns and the computation performed by the neuron. Statistical analysis of the simulated spike trains shows that the timing of bursts is much more precise than the timing of single spikes. Furthermore, the number of spikes per burst is highly robust to noise. Next we considered the computation performed by the neuron: how different features of the input current are mapped into specific output spike patterns. Dimensional reduction and statistical classification techniques were used to determine the stimulus features triggering different firing patterns. Our main result is that spikes, and bursts of different durations, code for different stimulus features, which can be quantified without a priori assumptions about those features. These findings lead us to propose that the biophysical mechanisms of spike generation enables individual neurons to encode different stimulus features into distinct spike patterns.     

Information geometry of interspike intervals in spiking neurons

An information geometrical method is developed for characterizing or classifying neurons in cortical areas, whose spike rates fluctuate in time. Under the assumption that the interspike intervals of a spike sequence of a neuron obey a gamma process with a time-variant spike rate and a fixed shape parameter, we formulate the problem of characterization as a semiparametric statistical estimation, where the spike rate is a nuisance parameter. We derive optimal criteria from the information geometrical viewpoint when certain assumptions are added to the formulation, and we show that some existing measures, such as the coefficient of variation and the local variation, are expressed as estimators of certain functions under the same assumptions.     

Attractor reliability reveals deterministic structure in neuronal spike trains

When periodic current is injected into an integrate-and-fire model neuron, the voltage as a function of time converges from different initial conditions to an attractor that produces reproducible sequences of spikes. The attractor reliability is a measure of the stability of spike trains against intrinsic noise and is quantified here as the inverse of the number of distinct spike trains obtained in response to repeated presentations of the same stimulus. High reliability characterizes neurons that can support a spike-time code, unlike neurons with discharges forming a renewal process (such as a Poisson process). These two classes of responses cannot be distinguished using measures based on the spike-time histogram, but they can be identified by the attractor dynamics of spike trains, as shown here using a new method for calculating the attractor reliability. We applied these methods to spike trains obtained from current injection into cortical neurons recorded in vitro. These spike trains did not form a renewal process and had a higher reliability compared to renewal-like processes with the same spike-time histogram.     

Modeling synaptic plasticity in conjuction with the timing of pre- and postsynaptic action potentials

We present a spiking neuron model that allows for an analytic calculation of the correlations between pre- and postsynaptic spikes. The neuron model is a generalization of the integrate-and-fire model and equipped with a probabilistic spike-triggering mechanism. We show that under certain biologically plausible conditions, pre- and postsynaptic spike trains can be described simultaneously as an inhomogeneous Poisson process. Inspired by experimental findings, we develop a model for synaptic long-term plasticity that relies on the relative timing of pre- and post-synaptic action potentials. Being given an input statistics, we compute the stationary synaptic weights that result from the temporal correlations between the pre- and postsynaptic spikes. By means of both analytic calculations and computer simulations, we show that such a mechanism of synaptic plasticity is able to strengthen those input synapses that convey precisely timed spikes at the expense of synapses that deliver spikes with a broad temporal distribution. This may be of vital importance for any kind of information processing based on spiking neurons and temporal coding.     

Synchronization of the neural response to noisy periodic synaptic input.

The timing information contained in the response of a neuron to noisy periodic synaptic input is analyzed for the leaky integrate-and-fire neural model. We address the question of the relationship between the timing of the synaptic inputs and the output spikes. This requires an analysis of the interspike interval distribution of the output spikes, which is obtained in the gaussian approximation. The conditional output spike density in response to noisy periodic input is evaluated as a function of the initial phase of the inputs. This enables the phase transition matrix to be calculated, which relates the phase at which the output spike is generated to the initial phase of the inputs. The interspike interval histogram and the period histogram for the neural response to ongoing periodic input are then evaluated by using the leading eigenvector of this phase transition matrix. The synchronization index of the output spikes is found to increase sharply as the inputs become synchronized. This enhancement of synchronization is most pronounced for large numbers of inputs and lower frequencies of modulation and also for rates of input near the critical input rate. However, the mutual information between the input phase of the stimulus and the timing of output spikes is found to decrease at low input rates as the number of inputs increases. The results show close agreement with those obtained from numerical simulations for large numbers of inputs.     

Analysis of spike statistics in neuronal systems with continuous attractors or multiple, discrete attractor States

Attractor networks are likely to underlie working memory and integrator circuits in the brain. It is unknown whether continuous quantities are stored in an analog manner or discretized and stored in a set of discrete attractors. In order to investigate the important issue of how to differentiate the two systems, here we compare the neuronal spiking activity that arises from a continuous (line) attractor with that from a series of discrete attractors. Stochastic fluctuations cause the position of the system along its continuous attractor to vary as a random walk, whereas in a discrete attractor, noise causes spontaneous transitions to occur between discrete states at random intervals. We calculate the statistics of spike trains of neurons firing as a Poisson process with rates that vary according to the underlying attractor network. Since individual neurons fire spikes probabilistically and since the state of the network as a whole drifts randomly, the spike trains of individual neurons follow a doubly stochastic (Poisson) point process. We compare the series of spike trains from the two systems using the autocorrelation function, Fano factor, and interspike interval (ISI) distribution. Although the variation in rate can be dramatically different, especially for short time intervals, surprisingly both the autocorrelation functions and Fano factors are identical, given appropriate scaling of the noise terms. Since the range of firing rates is limited in neurons, we also investigate systems for which the variation in rate is bounded by either rigid limits or because of leak to a single attractor state, such as the Ornstein-Uhlenbeck process. In these cases, the time dependence of the variance in rate can be different between discrete and continuous systems, so that in principle, these processes can be distinguished using second-order spike statistics.     

Estimating the temporal interval entropy of neuronal discharge

To better understand the role of timing in the function of the nervous system, we have developed a methodology that allows the entropy of neuronal discharge activity to be estimated from a spike train record when it may be assumed that successive interspike intervals are temporally uncorrelated. The so-called interval entropy obtained by this methodology is based on an implicit enumeration of all possible spike trains that are statistically indistinguishable from a given spike train. The interval entropy is calculated from an analytic distribution whose parameters are obtained by maximum likelihood estimation from the interval probability distribution associated with a given spike train. We show that this approach reveals features of neuronal discharge not seen with two alternative methods of entropy estimation. The methodology allows for validation of the obtained data models by calculation of confidence intervals for the parameters of the analytic distribution and the testing of the significance of the fit between the observed and analytic interval distributions by means of Kolmogorov-Smirnov and Anderson-Darling statistics. The method is demonstrated by analysis of two different data sets: simulated spike trains evoked by either Poissonian or near-synchronous pulsed activation of a model cerebellar Purkinje neuron and spike trains obtained by extracellular recording from spontaneously discharging cultured rat hippocampal neurons.     

Differences in spiking patterns among cortical neurons

Spike sequences recorded from four cortical areas of an awake behaving monkey were examined to explore characteristics that vary among neurons. We found that a measure of the local variation of interspike intervals, L(V), is nearly the same for every spike sequence for any given neuron, while it varies significantly among neurons. The distributions of L(V) values for neuron ensembles in three of the four areas were found to be distinctly bimodal. Two groups of neurons classified according to the spiking irregularity exhibit different responses to the same stimulus. This suggests that neurons in each area can be classified into different groups possessing unique spiking statistics and corresponding functional properties.     

Finding the event structure of neuronal spike trains

Neurons in sensory systems convey information about physical stimuli in their spike trains. In vitro, single neurons respond precisely and reliably to the repeated injection of the same fluctuating current, producing regions of elevated firing rate, termed events. Analysis of these spike trains reveals that multiple distinct spike patterns can be identified as trial-to-trial correlations between spike times (Fellous, Tiesinga, Thomas, & Sejnowski, 2004 ). Finding events in data with realistic spiking statistics is challenging because events belonging to different spike patterns may overlap. We propose a method for finding spiking events that uses contextual information to disambiguate which pattern a trial belongs to. The procedure can be applied to spike trains of the same neuron across multiple trials to detect and separate responses obtained during different brain states. The procedure can also be applied to spike trains from multiple simultaneously recorded neurons in order to identify volleys of near-synchronous activity or to distinguish between excitatory and inhibitory neurons. The procedure was tested using artificial data as well as recordings in vitro in response to fluctuating current waveforms.     

Analysis and modelling of variability and covariability of population spike trains across multiple time scales

As multi-electrode and imaging technology begin to provide us with simultaneous recordings of large neuronal populations, new methods for modelling such data must also be developed. We present a model of responses to repeated trials of a sensory stimulus based on thresholded Gaussian processes that allows for analysis and modelling of variability and covariability of population spike trains across multiple time scales. The model framework can be used to specify the values of many different variability measures including spike timing precision across trials, coefficient of variation of the interspike interval distribution, and Fano factor of spike counts for individual neurons, as well as signal and noise correlations and correlations of spike counts across multiple neurons. Using both simulated data and data from different stages of the mammalian auditory pathway, we demonstrate the range of possible independent manipulations of different variability measures, and explore how this range depends on the sensory stimulus. The model provides a powerful framework for the study of experimental and surrogate data and for analyzing dependencies between different statistical properties of neuronal populations.     

Parameters of spike trains observed in a short time window

We study the estimation of statistical moments of interspike intervals based on observation of spike counts in many independent short time windows. This scenario corresponds to the situation in which a target neuron occurs. It receives information from many neurons and has to respond within a short time interval. The precision of the estimation procedures is examined. As the model for neuronal activity, two examples of stationary point processes are considered: renewal process and doubly stochastic Poisson process. Both moment and maximum likelihood estimators are investigated. Not only the mean but also the coefficient of variation is estimated. In accordance with our expectations, numerical studies confirm that the estimation of mean interspike interval is more reliable than the estimation of coefficient of variation. The error of estimation increases with increasing mean interspike interval, which is equivalent to decreasing the size of window (less events are observed in a window) and with decreasing the number of neurons (lower number of windows).     

Reliability of spike timing is a general property of spiking model neurons

The responses of neurons to time-varying injected currents are reproducible on a trial-by-trial basis in vitro, but when a constant current is injected, small variances in interspike intervals across trials add up, eventually leading to a high variance in spike timing. It is unclear whether this difference is due to the nature of the input currents or the intrinsic properties of the neurons. Neuron responses can fail to be reproducible in two ways: dynamical noise can accumulate over time and lead to a desynchronization over trials, or several stable responses can exist, depending on the initial condition. Here we show, through simulations and theoretical considerations, that for a general class of spiking neuron models, which includes, in particular, the leaky integrate-and-fire model as well as nonlinear spiking models, aperiodic currents, contrary to periodic currents, induce reproducible responses, which are stable under noise, change in initial conditions and deterministic perturbations of the input. We provide a theoretical explanation for aperiodic currents that cross the threshold.     

A neuromorphic depth-from-motion vision model with STDP adaptation

We propose a simplified depth-from-motion vision model based on leaky integrate-and-fire (LIF) neurons for edge detection and two-dimensional depth recovery. In the model, every LIF neuron is able to detect the irradiance edges passing through its receptive field in an optical flow field, and respond to the detection by firing a spike when the neuron's firing criterion is satisfied. If a neuron fires a spike, the time-of-travel of the spike-associated edge is transferred as the prediction information to the next synapse-linked neuron to determine its state. Correlations between input spikes and their timing thus encode depth in the visual field. The adaptation of synapses mediated by spike-timing-dependent plasticity is used to improve the algorithm's robustness against inaccuracy caused by spurious edge propagation. The algorithm is characterized on both artificial and real image sequences. The implementation of the algorithm in analog very large scale integrated (aVLSI) circuitry is also discussed.     

A novel spiking neural network of receptive field encoding with groups of neurons decision

Human information processing depends mainly on billions of neurons which constitute a complex neural network, and the information is transmitted in the form of neural spikes. In this paper, we propose a spiking neural network (SNN), named MD-SNN, with three key features: (1) using receptive field to encode spike trains from images; (2) randomly selecting partial spikes as inputs for each neuron to approach the absolute refractory period of the neuron; (3) using groups of neurons to make decisions. We test MD-SNN on the MNIST data set of handwritten digits, and results demonstrate that: (1) Different sizes of receptive fields influence classification results significantly. (2) Considering the neuronal refractory period in the SNN model, increasing the number of neurons in the learning layer could greatly reduce the training time, effectively reduce the probability of over-fitting, and improve the accuracy by 8.77%. (3) Compared with other SNN methods, MD-SNN achieves a better classification; compared with the convolution neural network, MD-SNN maintains flip and rotation invariance (the accuracy can remain at 90.44% on the test set), and it is more suitable for small sample learning (the accuracy can reach 80.15% for 1000 training samples, which is 7.8 times that of CNN).     

脉冲神经元的信息处理

介绍累积放电脉冲神经元的数学描述;讨论脉冲神经元如何将激励信号转化为脉冲序列;讨论脉冲神经元如何将输入脉冲序列转化为输出脉冲序列。实验结果表明脉冲神经元具有很好的信息表示能力、信号鉴别能力和图像信号重构能力。给出利用脉冲神经网络进行图像信号处理的方法。     

Dynamical constraints on using precise spike timing to compute in recurrent cortical networks

Several recent models have proposed the use of precise timing of spikes for cortical computation. Such models rely on growing experimental evidence that neurons in the thalamus as well as many primary sensory cortical areas respond to stimuli with remarkable temporal precision. Models of computation based on spike timing, where the output of the network is a function not only of the input but also of an independently initializable internal state of the network, must, however, satisfy a critical constraint: the dynamics of the network should not be sensitive to initial conditions. We have previously developed an abstract dynamical system for networks of spiking neurons that has allowed us to identify the criterion for the stationary dynamics of a network to be sensitive to initial conditions. Guided by this criterion, we analyzed the dynamics of several recurrent cortical architectures, including one from the orientation selectivity literature. Based on the results, we conclude that under conditions of sustained, Poisson-like, weakly correlated, low to moderate levels of internal activity as found in the cortex, it is unlikely that recurrent cortical networks can robustly generate precise spike trajectories, that is, spatiotemporal patterns of spikes precise to the millisecond timescale.     

Interspike interval statistics in the stochastic Hodgkin-Huxley model: coexistence of gamma frequency bursts and highly irregular firing

When the classical Hodgkin-Huxley equations are simulated with Na- and K-channel noise and constant applied current, the distribution of interspike intervals is bimodal: one part is an exponential tail, as often assumed, while the other is a narrow gaussian peak centered at a short interspike interval value. The gaussian arises from bursts of spikes in the gamma-frequency range, the tail from the interburst intervals, giving overall an extraordinarily high coefficient of variation--up to 2.5 for 180,000 Na channels when I approximately 7 microA/cm(2). Since neurons with a bimodal ISI distribution are common, it may be a useful model for any neuron with class 2 firing. The underlying mechanism is due to a subcritical Hopf bifurcation, together with a switching region in phase-space where a fixed point is very close to a system limit cycle. This mechanism may be present in many different classes of neurons and may contribute to widely observed highly irregular neural spiking.     

What can a neuron learn with spike-timing-dependent plasticity?

Spiking neurons are very flexible computational modules, which can implement with different values of their adjustable synaptic parameters an enormous variety of different transformations F from input spike trains to output spike trains. We examine in this letter the question to what extent a spiking neuron with biologically realistic models for dynamic synapses can be taught via spike-timing-dependent plasticity (STDP) to implement a given transformation F. We consider a supervised learning paradigm where during training, the output of the neuron is clamped to the target signal (teacher forcing). The well-known perceptron convergence theorem asserts the convergence of a simple supervised learning algorithm for drastically simplified neuron models (McCulloch-Pitts neurons). We show that in contrast to the perceptron convergence theorem, no theoretical guarantee can be given for the convergence of STDP with teacher forcing that holds for arbitrary input spike patterns. On the other hand, we prove that average case versions of the perceptron convergence theorem hold for STDP in the case of uncorrelated and correlated Poisson input spike trains and simple models for spiking neurons. For a wide class of cross-correlation functions of the input spike trains, the resulting necessary and sufficient condition can be formulated in terms of linear separability, analogously as the well-known condition of learnability by perceptrons. However, the linear separability criterion has to be applied here to the columns of the correlation matrix of the Poisson input. We demonstrate through extensive computer simulations that the theoretically predicted convergence of STDP with teacher forcing also holds for more realistic models for neurons, dynamic synapses, and more general input distributions. In addition, we show through computer simulations that these positive learning results hold not only for the common interpretation of STDP, where STDP changes the weights of synapses, but also for a more realistic interpretation suggested by experimental data where STDP modulates the initial release probability of dynamic synapses.