Collective is Different: Information Exchange and Speed-Accuracy Trade-Offs in Self-Organized Patterning

Abstract

During development, highly ordered structures emerge as cells collectively coordinate with each other. While recent advances have clarified how individual cells process and respond to external signals, understanding collective cellular decision making remains a major challenge. Here, we introduce a minimal, analytically tractable model of cell patterning via local cell-cell communication. Using this framework, we identify a trade-off between the speed and accuracy of collective pattern formation and, by adapting techniques from stochastic chemical kinetics, quantify how information flows between cells during patterning. Our analysis reveals counterintuitive features of collective patterning: globally optimized solutions do not necessarily maximize intercellular information transfer and individual cells may appear suboptimal in isolation. Moreover, the model predicts that instantaneous information shared between cells can be nonmonotonic in time as patterning occurs. An analysis of recent experimental data from lateral inhibition in Drosophila pupal abdomen finds a qualitatively similar effect.