Collective gradient sensing with limited positional information.

Abstract

Eukaryotic cells sense chemical gradients to decide where and when to move. Clusters of cells can sense gradients more accurately than individual cells by integrating measurements of the concentration made across the cluster. Is this gradient-sensing accuracy impeded when cells have limited knowledge of their position within the cluster, i.e., limited positional information? We apply maximum likelihood estimation to study gradient-sensing accuracy of a cluster of cells with finite positional information. If cells must estimate their location within the cluster, this lowers the accuracy of collective gradient sensing. We compare our results with a tug-of-war model where cells respond to the gradient by polarizing away from their neighbors without relying on their positional information. As the cell positional uncertainty increases, there is a trade-off where the tug-of-war model responds more accurately to the chemical gradient. However, for sufficiently large cell clusters or sufficiently shallow chemical gradients, the tug-of-war model will always be suboptimal to one that integrates information from all cells, even if positional uncertainty is high.