Abstract

Experimental and numerical studies have revealed that isolated populations of oscillatory neurons can spontaneously synchronize and generate periodic bursts involving the whole network. Such a behavior has notably been observed for cultured neurons in rodent's cortex or hippocampus. We show here that a sufficient condition for this network bursting is the presence of an excitatory population of oscillatory neurons which displays spike-driven adaptation. We provide an analytic model to analyze network bursts generated by coupled adaptive exponential integrate-and-fire neurons. We show that, for strong synaptic coupling, intrinsically tonic spiking neurons evolve to reach a synchronized intermittent bursting state. The presence of inhibitory neurons or plastic synapses can then modulate this dynamics in many ways but is not necessary for its appearance. Thanks to a simple self-consistent equation, our model gives an intuitive and semi-quantitative tool to understand the bursting behavior. Furthermore, it suggests that after-hyperpolarization currents are sufficient to explain bursting termination. Through a thorough mapping between the theoretical parameters and ion-channel properties, we discuss the biological mechanisms that could be involved and the relevance of the explored parameter-space. Such an insight enables us to propose experimentally-testable predictions regarding how blocking fast, medium or slow after-hyperpolarization channels would affect the firing rate and burst duration, as well as the interburst interval.

Highlights

  • Network bursting is an intermittent collective behavior that occurs spontaneously in neuronal populations

  • Our model provides a predictive framework which allows us to determine how this bursting behavior is affected by changes in the individual properties of the neurons

  • We suggest how adaptation-channel blockers may affect the dynamics when applied on a bursting neuronal culture

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Summary

Introduction

Network bursting is an intermittent collective behavior that occurs spontaneously in neuronal populations It is characterized by long quiet periods, with almost no spike emission, punctuated by brief periods of intense spiking activity, where the whole network displays high firing rates—most neurons emit at least 2 closely-packed spikes. This particular pattern is repeated, with varying regularity, over long time intervals Such periodic and synchronized activity has been observed as an emergent phenomenon in large neuronal populations, both in brain regions (Meister et al, 1991; Blankenship and Feller, 2009; Rybak et al, 2014) and unperturbed neuronal cultures (Wagenaar et al, 2006; Stegenga et al, 2008; Penn et al, 2016). It has been investigated as a plausible candidate for rhythmogenesis (Ramirez et al, 2004), and in various disorders such as epilepsy (Derchansky et al, 2008) or Parkinson’s disease.

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