Abstract

Networks of neurons produce diverse patterns of oscillations, arising from the network's global properties, the propensity of individual neurons to oscillate, or a mixture of the two. Here we describe noisy limit cycles and quasi-cycles, two related mechanisms underlying emergent oscillations in neuronal networks whose individual components, stochastic spiking neurons, do not themselves oscillate. Both mechanisms are shown to produce gamma band oscillations at the population level while individual neurons fire at a rate much lower than the population frequency. Spike trains in a network undergoing noisy limit cycles display a preferred period which is not found in the case of quasi-cycles, due to the even faster decay of phase information in quasi-cycles. These oscillations persist in sparsely connected networks, and variation of the network's connectivity results in variation of the oscillation frequency. A network of such neurons behaves as a stochastic perturbation of the deterministic Wilson-Cowan equations, and the network undergoes noisy limit cycles or quasi-cycles depending on whether these have limit cycles or a weakly stable focus. These mechanisms provide a new perspective on the emergence of rhythmic firing in neural networks, showing the coexistence of population-level oscillations with very irregular individual spike trains in a simple and general framework.

Highlights

  • Networks of the central nervous system display oscillations at many frequencies and scales of organization

  • We show that noisy limit cycle oscillations persist in sparse networks, whose frequency varies with parameters for synaptic weights and sparseness of connectivity as well as the single-neuron parameters

  • The firing of individual neurons has an even weaker phase relationship with a quasi-cycle population oscillation than to a noisy limit cycle oscillation, to the extent where the population oscillation is undetectable from the spike trains of single neurons in the network

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Summary

Introduction

Networks of the central nervous system display oscillations at many frequencies and scales of organization. The third case includes the delay-driven models of Brunel et al [9,10] and most models based on Hodgkin-Huxley neurons [11,12,13] In both the first and third category we may have exact synchronous firing, where each neuron fires once per population cycle, or ‘‘cluster states’’ where neurons fire together in groups at some fixed multiple of the population frequency [14]. Noisy versions of such models may produce sparse or irregular firing, so that neurons skip beats, i.e. do not fire in every cycle of the network oscillation; but generally the spike times have a narrow distribution of phases within the network cycle

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