Tuning network dynamics from criticality to an asynchronous state

Abstract

Author summary What is the dynamical state of cerebral cortex? Are neurons mostly uncorrelated, firing independently of each other? Or are neurons more coordinated, firing in sync with each other? The answers to these questions have fundamental implications for how the cortical neural population encodes and processes information. Here we show that two possible scenarios-criticality and asynchronous dynamics-that are typically considered incompatible can be attained in the same network by maintaining a certain kind of balance, while tuning the strength of inhibition relative to excitation along with the average synaptic strength. According to many experimental observations, neurons in cerebral cortex tend to operate in an asynchronous regime, firing independently of each other. In contrast, many other experimental observations reveal cortical population firing dynamics that are relatively coordinated and occasionally synchronous. These discrepant observations have naturally led to competing hypotheses. A commonly hypothesized explanation of asynchronous firing is that excitatory and inhibitory synaptic inputs are precisely correlated, nearly canceling each other, sometimes referred to as 'balanced' excitation and inhibition. On the other hand, the 'criticality' hypothesis posits an explanation of the more coordinated state that also requires a certain balance of excitatory and inhibitory interactions. Both hypotheses claim the same qualitative mechanism-properly balanced excitation and inhibition. Thus, a natural question arises: how are asynchronous population dynamics and critical dynamics related, how do they differ? Here we propose an answer to this question based on investigation of a simple, network-level computational model. We show that the strength of inhibitory synapses relative to excitatory synapses can be tuned from weak to strong to generate a family of models that spans a continuum from critical dynamics to asynchronous dynamics. Our results demonstrate that the coordinated dynamics of criticality and asynchronous dynamics can be generated by the same neural system if excitatory and inhibitory synapses are tuned appropriately.