Interleaving asynchronous and synchronous activity in balanced cortical networks with short-term synaptic depression

Cortical populations are in a broadly asynchronous state that is sporadically interrupted by brief epochs of coordinated population activity. Cortical models are at a loss to explain this combination of states. At one extreme are network models where recurrent inhibition dynamically stabilizes an asynchronous low activity state. While these networks are widely used, they cannot produce the coherent population-wide activity that is reported in a variety of datasets. At the other extreme are models in which strong recurrent excitation that is quickly tamed by short term synaptic depression between excitatory neurons leads to short epochs of population-wide activity. However, in these networks, inhibition plays only a perfunctory role in network stability, which is at odds with many reports across cortex. In this study we analyze spontaneously active in vitro preparations of primary auditory cortex that show dynamics that are emblematic of this mixture of states. To capture this complex population activity we use firing rate-based networks as well as biologically realistic networks of spiking neuron models where large excitation is balanced by recurrent inhibition, yet we include short-term synaptic depression dynamics of the excitatory connections. These models give very rich nonlinear behavior that mimics the core features of the in vitro data, including the possibility of low frequency (2-12 Hz) rhythmic dynamics within population events. In these networks, synaptic depression enables activity fluctuations to induce a weakening of inhibitory recruitment, which in turn triggers population events. In sum, our study extends balanced network models to account for nonlinear, population-wide correlated activity, thereby providing a critical step in a mechanistic theory of realistic cortical activity.