Small modifications to network topology can induce stochastic bistable spiking dynamics in a balanced cortical model

Directed random graph models frequently are used successfully in modeling the population dynamics of networks of cortical neurons connected by chemical synapses. Experimental results consistently reveal that neuronal network topology is complex, however, in the sense that it differs statistically from a random network, and differs for classes of neurons that are physiologically different. This suggests that complex network models whose subnetworks have distinct topological structure may be a useful, and more biologically realistic, alternative to random networks. Here we demonstrate that the balanced excitation and inhibition frequently observed in small cortical regions can transiently disappear in otherwise standard neuronal-scale models of fluctuation-driven dynamics, solely because the random network topology was replaced by a complex clustered one, whilst not changing the in-degree of any neurons. In this network, a small subset of cells whose inhibition comes only from outside their local cluster are the cause of bistable population dynamics, where different clusters of these cells irregularly switch back and forth from a sparsely firing state to a highly active state. Transitions to the highly active state occur when a cluster of these cells spikes sufficiently often to cause strong unbalanced positive feedback to each other. Transitions back to the sparsely firing state rely on occasional large fluctuations in the amount of non-local inhibition received. Neurons in the model are homogeneous in their intrinsic dynamics and in-degrees, but differ in the abundance of various directed feedback motifs in which they participate. Our findings suggest that (i) models and simulations should take into account complex structure that varies for neuron and synapse classes; (ii) differences in the dynamics of neurons with similar intrinsic properties may be caused by their membership in distinctive local networks; (iii) it is important to identify neurons that share physiological properties and location, but differ in their connectivity.