Tuning network dynamics from criticality to an asynchronous state

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.