Nonperiodic synchronization in heterogeneous networks of spiking neurons

Neural synchronization is of wide interest in neuroscience and has been argued to form the substrate for conscious attention to stimuli, movement preparation, and the maintenance of task-relevant representations in active memory. Despite a wealth of possible functions, the mechanisms underlying synchrony are still poorly understood. In particular, in vitro preparations have demonstrated synchronization with no apparent periodicity, which cannot be explained by simple oscillatory mechanisms. Here, we investigate the possible origins of nonperiodic synchronization through biophysical simulations. We show that such aperiodic synchronization arises naturally under a simple set of plausible assumptions, depending crucially on heterogeneous cell properties. In addition, nonperiodicity occurs even in the absence of stochastic fluctuation in membrane potential, suggesting that it may represent an intrinsic property of interconnected networks. Simulations capture some of the key aspects of population-level synchronization in spontaneous network spikes (NSs) and suggest that the intrinsic nonperiodicity of NSs observed in reduced cell preparations is a phenomenon that is highly robust and can be reproduced in simulations that involve a minimal set of realistic assumptions. In addition, a model with spike timing-dependent plasticity can overcome a natural tendency to exhibit nonperiodic behavior. After rhythmic stimulation, the model does not automatically fall back to a state of nonperiodic behavior, but keeps replaying the pattern of evoked NSs for a few cycles. A cluster analysis of synaptic strengths highlights the importance of population-wide interactions in generating this result and describes a possible route for encoding temporal patterns in networks of neurons.