Spontaneous and stimulus-induced coherent states of critically balanced neuronal networks

TL;DR

This study explores how balanced excitation and inhibition in neuronal networks at criticality generate spontaneous and stimulus-induced coherent states, revealing a new mechanism for multiscale neural information processing.

Contribution

It introduces a novel mean-field theory for critically balanced networks, demonstrating how microscopic fluctuations amplify to produce macroscopic coherence and information read-out.

Findings

Balanced networks exhibit spontaneous irregular rhythms.

External inputs can entrain whole-network dynamics.

Coherent states enable state-dependent information read-out.

Abstract

How the information microscopically processed by individual neurons is integrated and used in organizing the behavior of an animal is a central question in neuroscience. The coherence of neuronal dynamics over different scales has been suggested as a clue to the mechanisms underlying this integration. Balanced excitation and inhibition may amplify microscopic fluctuations to a macroscopic level, thus providing a mechanism for generating coherent multiscale dynamics. Previous theories of brain dynamics, however, were restricted to cases in which inhibition dominated excitation and suppressed fluctuations in the macroscopic population activity. In the present study, we investigate the dynamics of neuronal networks at a critical point between excitation-dominant and inhibition-dominant states. In these networks, the microscopic fluctuations are amplified by the strong excitation and inhibition to drive the macroscopic dynamics, while the macroscopic dynamics determine the statistics of the microscopic fluctuations. Developing a novel type of mean-field theory applicable to this class of interscale interactions, we show that the amplification mechanism generates spontaneous, irregular macroscopic rhythms similar to those observed in the brain. Through the same mechanism, microscopic inputs to a small number of neurons effectively entrain the dynamics of the whole network. These network dynamics undergo a probabilistic transition to a coherent state, as the magnitude of either the balanced excitation and inhibition or the external inputs is increased. Our mean-field theory successfully predicts the behavior of this model. Furthermore, we numerically demonstrate that the coherent dynamics can be used for state-dependent read-out of information from the network. These results show a novel form of neuronal information processing that connects neuronal dynamics on different scales.