Network events on multiple space and time scales in cultured neural networks and in a stochastic rate model

TL;DR

This study unifies the understanding of diverse neural network events across scales using a probabilistic framework and a rate model, revealing their regulation by oscillatory instability and excitation-inhibition balance.

Contribution

It introduces a common probabilistic definition of network events and demonstrates how various phenomena emerge from a single rate model near oscillatory instability.

Findings

Network events co-occur and follow distinct statistical distributions.

Emergence of events is regulated by proximity to oscillatory instability.

Cultured networks show multiple fatigue time scales, indicating diverse fatigue mechanisms.

Abstract

Cortical networks, in-vitro as well as in-vivo, can spontaneously generate a variety of collective dynamical events such as network spikes, UP and DOWN states, global oscillations, and avalanches. Though each of them have been variously recognized in previous works as expressions of the excitability of the cortical tissue and the associated nonlinear dynamics, a unified picture of their determinant factors (dynamical and architectural) is desirable and not yet available. Progress has also been partially hindered by the use of a variety of statistical measures to define the network events of interest. We propose here a common probabilistic definition of network events that, applied to the firing activity of cultured neural networks, highlights the co-occurrence of network spikes, power-law distributed avalanches, and exponentially distributed `quasi-orbits', which offer a third type of collective behavior. A rate model, including synaptic excitation and inhibition with no imposed topology, synaptic short-term depression, and finite-size noise, accounts for all these different, coexisting phenomena. We find that their emergence is largely regulated by the proximity to an oscillatory instability of the dynamics, where the non-linear excitable behavior leads to a self-amplification of activity fluctuations over a wide range of scales in space and time. In this sense, the cultured network dynamics is compatible with an excitation-inhibition balance corresponding to a slightly sub-critical regime. Finally, we propose and test a method to infer the characteristic time of the fatigue process, from the observed time course of the network's firing rate. Unlike the model, possessing a single fatigue mechanism, the cultured network appears to show multiple time scales, signalling the possible coexistence of different fatigue mechanisms.