Abstract

The spiking activity of single neurons can be well described by a nonlinear integrate-and-fire model that includes somatic adaptation. When exposed to fluctuating inputs sparsely coupled populations of these model neurons exhibit stochastic collective dynamics that can be effectively characterized using the Fokker-Planck equation. This approach, however, leads to a model with an infinite-dimensional state space and non-standard boundary conditions. Here we derive from that description four simple models for the spike rate dynamics in terms of low-dimensional ordinary differential equations using two different reduction techniques: one uses the spectral decomposition of the Fokker-Planck operator, the other is based on a cascade of two linear filters and a nonlinearity, which are determined from the Fokker-Planck equation and semi-analytically approximated. We evaluate the reduced models for a wide range of biologically plausible input statistics and find that both approximation approaches lead to spike rate models that accurately reproduce the spiking behavior of the underlying adaptive integrate-and-fire population. Particularly the cascade-based models are overall most accurate and robust, especially in the sensitive region of rapidly changing input. For the mean-driven regime, when input fluctuations are not too strong and fast, however, the best performing model is based on the spectral decomposition. The low-dimensional models also well reproduce stable oscillatory spike rate dynamics that are generated either by recurrent synaptic excitation and neuronal adaptation or through delayed inhibitory synaptic feedback. The computational demands of the reduced models are very low but the implementation complexity differs between the different model variants. Therefore we have made available implementations that allow to numerically integrate the low-dimensional spike rate models as well as the Fokker-Planck partial differential equation in efficient ways for arbitrary model parametrizations as open source software. The derived spike rate descriptions retain a direct link to the properties of single neurons, allow for convenient mathematical analyses of network states, and are well suited for application in neural mass/mean-field based brain network models.

Highlights

  • There is prominent evidence that information in the brain, about a particular stimulus for example, is contained in the collective neuronal spiking activity averaged over populations of neurons with similar properties [1, 2]

  • As an alternative to this expensive procedure we propose efficient models that describe the network activity in terms of a few ordinary differential equations

  • We build upon two research lines on which substantial efforts have been exerted in the last two decades: (i) the development of single neuron models of reduced complexity that can accurately reproduce a large repertoire of observed neuronal behavior, and (ii) different approaches to approximate the Fokker-Planck equation that represents the collective dynamics of large neuronal networks

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Summary

Introduction

There is prominent evidence that information in the brain, about a particular stimulus for example, is contained in the collective neuronal spiking activity averaged over populations of neurons with similar properties (population spike rate code) [1, 2]. A popular choice of single cell description for this purpose are two-variable integrate-and-fire models [5, 6] which describe the evolution of the fast (somatic) membrane voltage and an adaptation variable that represents a slowly-decaying potassium current. These models are computationally efficient and can be successfully calibrated using electrophysiological recordings of real cortical neurons and standard stimulation protocols [5, 7,8,9,10] to accurately reproduce their subthreshold and spiking activity. The choice of such (simple) neuron models, does not imply reasonable (short enough) simulation durations for a recurrent network, especially when large numbers of neurons and synaptic connections between them are considered

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