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. Inhibitory stabilized networks reproduce a low activity asynchronous regime but cannot generate population events. In contrast, synaptic depression stabilized excitatory networks create transient surges of activity, yet give inhibition only a perfunctory role. We analyzed spontaneously active in vitro mouse auditory cortex slices that show both regimes, including slow (2–12 Hz) oscillations within some events. We built firing rate and biophysically realistic spiking models in which excitation is balanced by recurrent inhibition, yet all excitatory synapses undergo short term depression. In our model a depression of synaptic excitation onto inhibition neurons initiates events, while depression of excitation onto excitatory neurons shapes rhythmicity of the events, reproducing the full repertoire observed experimentally. Our work unifies balanced and depression stabilized theories and provides a mechanistic framework for nonlinear, population wide correlations in cortex.