From Spiking Neuron Models to Linear-Nonlinear Models

Neurons transform time-varying inputs into action potentials emitted stochastically at a time dependent rate. The mapping from current input to output firing rate is often represented with the help of phenomenological models such as the linear-nonlinear (LN) cascade, in which the output firing rate is estimated by applying to the input successively a linear temporal filter and a static non-linear transformation. These simplified models leave out the biophysical details of action potential generation. It is not a priori clear to which extent the input-output mapping of biophysically more realistic, spiking neuron models can be reduced to a simple linear-nonlinear cascade. Here we investigate this question for the leaky integrate-and-fire (LIF), exponential integrate-and-fire (EIF) and conductance-based Wang-Buzsáki models in presence of background synaptic activity. We exploit available analytic results for these models to determine the corresponding linear filter and static non-linearity in a parameter-free form. We show that the obtained functions are identical to the linear filter and static non-linearity determined using standard reverse correlation analysis. We then quantitatively compare the output of the corresponding linear-nonlinear cascade with numerical simulations of spiking neurons, systematically varying the parameters of input signal and background noise. We find that the LN cascade provides accurate estimates of the firing rates of spiking neurons in most of parameter space. For the EIF and Wang-Buzsáki models, we show that the LN cascade can be reduced to a firing rate model, the timescale of which we determine analytically. Finally we introduce an adaptive timescale rate model in which the timescale of the linear filter depends on the instantaneous firing rate. This model leads to highly accurate estimates of instantaneous firing rates

Identification of linear and nonlinear sensory processing circuits from spiking neuron data

Inferring mathematical models of sensory processing systems directly from input-output observations, while making the fewest assumptions about the model equations and the types of measurements available, is still a major issue in computational neuroscience. This letter introduces two new approaches for identifying sensory circuit models consisting of linear and nonlinear filters in series with spiking neuron models, based only on the sampled analog input to the filter and the recorded spike train output of the spiking neuron. For an ideal integrate-and-fire neuron model, the first algorithm can identify the spiking neuron parameters as well as the structure and parameters of an arbitrary nonlinear filter connected to it. The second algorithm can identify the parameters of the more general leaky integrate-and-fire spiking neuron model, as well as the parameters of an arbitrary linear filter connected to it. Numerical studies involving simulated and real experimental recordings are used to demonstrate the applicability and evaluate the performance of the proposed algorithms

Stimulus-dependent maximum entropy models of neural population codes

Neural populations encode information about their stimulus in a collective fashion, by joint activity patterns of spiking and silence. A full account of this mapping from stimulus to neural activity is given by the conditional probability distribution over neural codewords given the sensory input. To be able to infer a model for this distribution from large-scale neural recordings, we introduce a stimulus-dependent maximum entropy (SDME) model---a minimal extension of the canonical linear-nonlinear model of a single neuron, to a pairwise-coupled neural population. The model is able to capture the single-cell response properties as well as the correlations in neural spiking due to shared stimulus and due to effective neuron-to-neuron connections. Here we show that in a population of 100 retinal ganglion cells in the salamander retina responding to temporal white-noise stimuli, dependencies between cells play an important encoding role. As a result, the SDME model gives a more accurate account of single cell responses and in particular outperforms uncoupled models in reproducing the distributions of codewords emitted in response to a stimulus. We show how the SDME model, in conjunction with static maximum entropy models of population vocabulary, can be used to estimate information-theoretic quantities like surprise and information transmission in a neural population.Comment: 11 pages, 7 figure

Multivariate Autoregressive Modeling and Granger Causality Analysis of Multiple Spike Trains

Recent years have seen the emergence of microelectrode arrays and optical methods allowing simultaneous recording of spiking activity from populations of neurons in various parts of the nervous system. The analysis of multiple neural spike train data could benefit significantly from existing methods for multivariate time-series analysis which have proven to be very powerful in the modeling and analysis of continuous neural signals like EEG signals. However, those methods have not generally been well adapted to point processes. Here, we use our recent results on correlation distortions in multivariate Linear-Nonlinear-Poisson spiking neuron models to derive generalized Yule-Walker-type equations for fitting ‘‘hidden” Multivariate Autoregressive models. We use this new framework to perform Granger causality analysis in order to extract the directed information flow pattern in networks of simulated spiking neurons. We discuss the relative merits and limitations of the new method

Multiplicative Auditory Spatial Receptive Fields Created by a Hierarchy of Population Codes

A multiplicative combination of tuning to interaural time difference (ITD) and interaural level difference (ILD) contributes to the generation of spatially selective auditory neurons in the owl's midbrain. Previous analyses of multiplicative responses in the owl have not taken into consideration the frequency-dependence of ITD and ILD cues that occur under natural listening conditions. Here, we present a model for the responses of ITD- and ILD-sensitive neurons in the barn owl's inferior colliculus which satisfies constraints raised by experimental data on frequency convergence, multiplicative interaction of ITD and ILD, and response properties of afferent neurons. We propose that multiplication between ITD- and ILD-dependent signals occurs only within frequency channels and that frequency integration occurs using a linear-threshold mechanism. The model reproduces the experimentally observed nonlinear responses to ITD and ILD in the inferior colliculus, with greater accuracy than previous models. We show that linear-threshold frequency integration allows the system to represent multiple sound sources with natural sound localization cues, whereas multiplicative frequency integration does not. Nonlinear responses in the owl's inferior colliculus can thus be generated using a combination of cellular and network mechanisms, showing that multiple elements of previous theories can be combined in a single system

Integration of continuous-time dynamics in a spiking neural network simulator

Contemporary modeling approaches to the dynamics of neural networks consider two main classes of models: biologically grounded spiking neurons and functionally inspired rate-based units. The unified simulation framework presented here supports the combination of the two for multi-scale modeling approaches, the quantitative validation of mean-field approaches by spiking network simulations, and an increase in reliability by usage of the same simulation code and the same network model specifications for both model classes. While most efficient spiking simulations rely on the communication of discrete events, rate models require time-continuous interactions between neurons. Exploiting the conceptual similarity to the inclusion of gap junctions in spiking network simulations, we arrive at a reference implementation of instantaneous and delayed interactions between rate-based models in a spiking network simulator. The separation of rate dynamics from the general connection and communication infrastructure ensures flexibility of the framework. We further demonstrate the broad applicability of the framework by considering various examples from the literature ranging from random networks to neural field models. The study provides the prerequisite for interactions between rate-based and spiking models in a joint simulation

A simple mechanism for higher-order correlations in integrate-and-fire neurons

The collective dynamics of neural populations are often characterized in terms of correlations in the spike activity of different neurons. Open questions surround the basic nature of these correlations. In particular, what leads to higher-order correlations -- correlations in the population activity that extend beyond those expected from cell pairs? Here, we examine this question for a simple, but ubiquitous, circuit feature: common fluctuating input arriving to spiking neurons of integrate-and-fire type. We show that leads to strong higher-order correlations, as for earlier work with discrete threshold crossing models. Moreover, we find that the same is true for another widely used, doubly-stochastic model of neural spiking, the linear-nonlinear cascade. We explain the surprisingly strong connection between the collective dynamics produced by these models, and conclude that higher-order correlations are both broadly expected and possible to capture with surprising accuracy by simplified (and tractable) descriptions of neural spiking

Nonlinear Hebbian learning as a unifying principle in receptive field formation

The development of sensory receptive fields has been modeled in the past by a variety of models including normative models such as sparse coding or independent component analysis and bottom-up models such as spike-timing dependent plasticity or the Bienenstock-Cooper-Munro model of synaptic plasticity. Here we show that the above variety of approaches can all be unified into a single common principle, namely Nonlinear Hebbian Learning. When Nonlinear Hebbian Learning is applied to natural images, receptive field shapes were strongly constrained by the input statistics and preprocessing, but exhibited only modest variation across different choices of nonlinearities in neuron models or synaptic plasticity rules. Neither overcompleteness nor sparse network activity are necessary for the development of localized receptive fields. The analysis of alternative sensory modalities such as auditory models or V2 development lead to the same conclusions. In all examples, receptive fields can be predicted a priori by reformulating an abstract model as nonlinear Hebbian learning. Thus nonlinear Hebbian learning and natural statistics can account for many aspects of receptive field formation across models and sensory modalities