The collective dynamics of frustrated biological neuron networks

To maintain normal functionality, it is necessary for a multicellular organism to generate robust responses to external temporal signals. However, the underlying mechanisms to coordinate the collective dynamics of cells remain poorly understood. Here we study the calcium activity of micropatterned biological neuron networks excited by periodic ATP stimuli. Combining quantitative experiments, physical and biological manipulation of cells, as well as mathematical modeling, we show that isolated cells in a network become more synchronized at longer period of stimuli through noise cancellation. However, slowly varying external signal also increases gap junction coupling between connected nodes in the network; and gap junction mediated communication may destroy network synchronization due to special nonlinear bifurcations exhibited by the excitable dynamics of neuronal cells. Based on our results, we propose that a biological neuron network supported by gap junctional communication encodes external temporal signals in its network dynamics. A sparely connected network approaches synchronization as input signal slows down, whereas a highly connected network enters dynamic frustration in the same situation.