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A Simple Mechanism for Beyond-Pairwise Correlations in Integrate-and-Fire Neurons.

ABSTRACT: The collective dynamics of neural populations are often characterized in terms of correlations in the spike activity of different neurons. We have developed an understanding of the circuit mechanisms that lead to correlations among cell pairs, but little is known about what determines the population firing statistics among larger groups of cells. 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 this leads to strong beyond-pairwise correlations-that is, correlations that cannot be captured by maximum entropy models that extrapolate from pairwise statistics-as for earlier work with discrete threshold crossing (dichotomous Gaussian) models. Moreover, we find that the same is true for another widely used, doubly stochastic model of neural spiking, the linear-nonlinear cascade. We demonstrate the strong connection between the collective dynamics produced by integrate-and-fire and dichotomous Gaussian models, and show that the latter is a surprisingly accurate model of the former. Our conclusion is that beyond-pairwise correlations can be both broadly expected and possible to describe by simplified (and tractable) statistical models.

SUBMITTER: Leen DA

PROVIDER: S-EPMC4554967 | biostudies-other | 2015 Dec

REPOSITORIES: biostudies-other

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A Simple Mechanism for Beyond-Pairwise Correlations in Integrate-and-Fire Neurons.

Leen David A DA Shea-Brown Eric E

Journal of mathematical neuroscience 20150901 1

The collective dynamics of neural populations are often characterized in terms of correlations in the spike activity of different neurons. We have developed an understanding of the circuit mechanisms that lead to correlations among cell pairs, but little is known about what determines the population firing statistics among larger groups of cells. Here, we examine this question for a simple, but ubiquitous, circuit feature: common fluctuating input arriving to spiking neurons of integrate-and-fir ...[more]

PMID: 26265217

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Project description:The ability of spiking neurons to synchronize their activity in a network depends on the response behavior of these neurons as quantified by the phase response curve (PRC) and on coupling properties. The PRC characterizes the effects of transient inputs on spike timing and can be measured experimentally. Here we use the adaptive exponential integrate-and-fire (aEIF) neuron model to determine how subthreshold and spike-triggered slow adaptation currents shape the PRC. Based on that, we predict how synchrony and phase locked states of coupled neurons change in presence of synaptic delays and unequal coupling strengths. We find that increased subthreshold adaptation currents cause a transition of the PRC from only phase advances to phase advances and delays in response to excitatory perturbations. Increased spike-triggered adaptation currents on the other hand predominantly skew the PRC to the right. Both adaptation induced changes of the PRC are modulated by spike frequency, being more prominent at lower frequencies. Applying phase reduction theory, we show that subthreshold adaptation stabilizes synchrony for pairs of coupled excitatory neurons, while spike-triggered adaptation causes locking with a small phase difference, as long as synaptic heterogeneities are negligible. For inhibitory pairs synchrony is stable and robust against conduction delays, and adaptation can mediate bistability of in-phase and anti-phase locking. We further demonstrate that stable synchrony and bistable in/anti-phase locking of pairs carry over to synchronization and clustering of larger networks. The effects of adaptation in aEIF neurons on PRCs and network dynamics qualitatively reflect those of biophysical adaptation currents in detailed Hodgkin-Huxley-based neurons, which underscores the utility of the aEIF model for investigating the dynamical behavior of networks. Our results suggest neuronal spike frequency adaptation as a mechanism synchronizing low frequency oscillations in local excitatory networks, but indicate that inhibition rather than excitation generates coherent rhythms at higher frequencies.

Project description: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.

Dataset Information

A Simple Mechanism for Beyond-Pairwise Correlations in Integrate-and-Fire Neurons.

Publications

A Simple Mechanism for Beyond-Pairwise Correlations in Integrate-and-Fire Neurons.

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