Relevance of network topology for the dynamics of biological neuronal networks

Abstract

Complex random networks provide a powerful mathematical framework to study high-dimensional physical and biological systems. Several features of network structure (e.g. degree correlation, average path length, clustering coefficient) are correlated with descriptors of network dynamics and function. However, it is not clear which features of network structure relate to the dynamics of biological neuronal networks (BNNs), characterized by non-linear nodes with high in- and out degrees, but being weakly connected and communicating in an event-driven manner, i.e. only when neurons spike. To better understand the structure-dynamics relationship in BNNs, we analysed the structure and dynamics of > 9, 000 BNNs with different sizes and topologies. In addition, we also studied the effect of network degeneration on neuronal network structure and dynamics. Surprisingly, we found that the topological class (random, small-world, scale-free) was not an indicator of the BNNs activity state as quantified by the firing rate, network synchrony and spiking regularity. In fact, we show that different network topologies could result in similar activity dynamics. Furthermore, in most cases, the network activity changes did not depend on the rules according to which neurons or synapses were pruned from the networks. The analysis of dynamics and structure of the networks we studied revealed that the effective synaptic weight (ESW) was the most crucial feature in predicting the statistics of spiking activity in BNNs. ESW also explained why different synapse and neuron pruning strategies resulted in almost identical effects on the network dynamics. Thus, our findings provide new insights into the structure-dynamics relationships in BNNs. Moreover, we argue that network topology and rules by which BNNs degenerate are irrelevant for BNN activity dynamics. Beyond neuroscience, our results suggest that in large networks with non-linear nodes, the effective interaction strength among the nodes, instead of the topological network class, may be a better predictor of the network dynamics and information flow.