Structure of Cell Networks Critically Determines Oscillation Regularity

Abstract

Biological rhythms are generated by pacemaker organs, such as the heart pacemaker organ (the sinoatrial node) and the master clock of the circadian rhythms (the suprachiasmatic nucleus), which are composed of a network of autonomously oscillatory cells. Such biological rhythms have notable periodicity despite the internal and external noise present in each cell. Previous experimental studies indicate that the regularity of oscillatory dynamics is enhanced when noisy oscillators interact and become synchronized. This effect, called the collective enhancement of temporal precision, has been studied theoretically using particular assumptions. In this study, we propose a general theoretical framework that enables us to understand the dependence of temporal precision on network parameters including size, connectivity, and coupling intensity; this effect has been poorly understood to date. Our framework is based on a phase oscillator model that is applicable to general oscillator networks with any coupling mechanism if coupling and noise are sufficiently weak. In particular, we can manage general directed and weighted networks. We quantify the precision of the activity of a single cell and the mean activity of an arbitrary subset of cells. We find that, in general undirected networks, the standard deviation of cycle-to-cycle periods scales with the system size $N$ as $1/\sqrt{N}$, but only up to a certain system size $N^*$ that depends on network parameters. Enhancement of temporal precision is ineffective when $N>N^*$. We also reveal the advantage of long-range interactions among cells to temporal precision.