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Mind the Last Spike -- Firing Rate Models for Mesoscopic Populations of Spiking Neurons

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 Added by Tilo Schwalger
 Publication date 2019
  fields Biology
and research's language is English




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The dominant modeling framework for understanding cortical computations are heuristic firing rate models. Despite their success, these models fall short to capture spike synchronization effects, to link to biophysical parameters and to describe finite-size fluctuations. In this opinion article, we propose that the refractory density method (RDM), also known as age-structured population dynamics or quasi-renewal theory, yields a powerful theoretical framework to build rate-based models for mesoscopic neural populations from realistic neuron dynamics at the microscopic level. We review recent advances achieved by the RDM to obtain efficient population density equations for networks of generalized integrate-and-fire (GIF) neurons -- a class of neuron models that has been successfully fitted to various cell types. The theory not only predicts the nonstationary dynamics of large populations of neurons but also permits an extension to finite-size populations and a systematic reduction to low-dimensional rate dynamics. The new types of rate models will allow a re-examination of models of cortical computations under biological constraints.



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The macroscopic dynamics of large populations of neurons can be mathematically analyzed using low-dimensional firing-rate or neural-mass models. However, these models fail to capture spike synchronization effects of stochastic spiking neurons such as the non-stationary population response to rapidly changing stimuli. Here, we derive low-dimensional firing-rate models for homogeneous populations of general renewal-type neurons, including integrate-and-fire models driven by white noise. Renewal models account for neuronal refractoriness and spike synchronization dynamics. The derivation is based on an eigenmode expansion of the associated refractory density equation, which generalizes previous spectral methods for Fokker-Planck equations to arbitrary renewal models. We find a simple relation between the eigenvalues, which determine the characteristic time scales of the firing rate dynamics, and the Laplace transform of the interspike interval density or the survival function of the renewal process. Analytical expressions for the Laplace transforms are readily available for many renewal models including the leaky integrate-and-fire model. Retaining only the first eigenmode yields already an adequate low-dimensional approximation of the firing-rate dynamics that captures spike synchronization effects and fast transient dynamics at stimulus onset. We explicitly demonstrate the validity of our model for a large homogeneous population of Poisson neurons with absolute refractoriness, and other renewal models that admit an explicit analytical calculation of the eigenvalues. The here presented eigenmode expansion provides a systematic framework for novel firing-rate models in computational neuroscience based on spiking neuron dynamics with refractoriness.
We derive analytical formulae for the firing rate of integrate-and-fire neurons endowed with realistic synaptic dynamics. In particular we include the possibility of multiple synaptic inputs as well as the effect of an absolute refractory period into the description.
Finite-sized populations of spiking elements are fundamental to brain function, but also used in many areas of physics. Here we present a theory of the dynamics of finite-sized populations of spiking units, based on a quasi-renewal description of neurons with adaptation. We derive an integral equation with colored noise that governs the stochastic dynamics of the population activity in response to time-dependent stimulation and calculate the spectral density in the asynchronous state. We show that systems of coupled populations with adaptation can generate a frequency band in which sensory information is preferentially encoded. The theory is applicable to fully as well as randomly connected networks, and to leaky integrate-and-fire as well as to generalized spiking neurons with adaptation on multiple time scales.
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. [...] 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. [...] The low-dimensional models also well reproduce stable oscillatory spike rate dynamics that is generated by recurrent synaptic excitation and neuronal adaptation. [...] 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.
Fast-spiking (FS) interneurons in the brain are self-innervated by powerful inhibitory GABAergic autaptic connections. By computational modelling, we investigate how autaptic inhibition regulates the firing response of such interneurons. Our results indicate that autaptic inhibition both boosts the current threshold for action potential generation as well as modulates the input-output gain of FS interneurons. The autaptic transmission delay is identified as a key parameter that controls the firing patterns and determines multistability regions of FS interneurons. Furthermore, we observe that neuronal noise influences the firing regulation of FS interneurons by autaptic inhibition and extends their dynamic range for encoding inputs. Importantly, autaptic inhibition modulates noise-induced irregular firing of FS interneurons, such that coherent firing appears at an optimal autaptic inhibition level. Our result reveal the functional roles of autaptic inhibition in taming the firing dynamics of FS interneurons.
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