Evolutionary Constraints on Connectivity Patterns in the Mammalian Suprachiasmatic Nucleus

Abstract

The mammalian suprachiasmatic nucleus (SCN) comprises about 20,000 interconnected oscillatory neurons that create and maintain a robust circadian signal which matches to external light cues. Here, we use an evolutionary game theoretic framework to explore how evolutionary constraints can influence the synchronization of the system under various assumptions on the connection topology, contributing to the understanding of the structure of interneuron connectivity. Our basic model represents the SCN as a network of agents each with two properties—a phase and a flag that determines if it communicates with its neighbors or not. Communication comes at a cost to the agent, but synchronization of phases with its neighbors bears a benefit. Earlier work shows that when we have “all-to-all” connectivity, where every agent potentially communicates with every other agent, there is often a simple trade-off that leads to complete communication and synchronization of the system: the benefit must be greater than twice the cost. This trade-off for all-to-all connectivity gives us a baseline to compare to when looking at other topologies. Using simulations, we compare three plausible topologies to the all-to-all case, finding that convergence to synchronous dynamics occurs in all considered topologies under similar benefit and cost trade-offs. Consequently, sparser, less biologically costly topologies are reasonable evolutionary outcomes for organisms that develop a synchronizable oscillatory network. Our simulations also shed light on constraints imposed by the time scale on which we observe the SCN to arise in mammals. We find two conditions that allow for a synchronizable system to arise in relatively few generations. First, the benefits of connectivity must outweigh the cost of facilitating the connectivity in the network. Second, the game at the core of the model needs to be more cooperative than antagonistic games such as the Prisoner’s Dilemma. These results again imply that evolutionary pressure may have driven the system towards sparser topologies, as they are less costly to create and maintain. Last, our simulations indicate that models based on the mutualism game fare the best in uptake of communication and synchronization compared to more antagonistic games such as the Prisoner’s Dilemma.