Hydrodynamic synchronization of elastic cilia: How surface effects determine the characteristics of metachronal waves

Cilia are hairlike microactuators whose cyclic motion is specialized to propel extracellular fluids at low Reynolds numbers. Clusters of these organelles can form synchronized beating patterns, called metachronal waves, which presumably arise from hydrodynamic interactions. We model hydrodynamically interacting cilia by microspheres elastically bound to circular orbits, whose inclinations with respect to a no-slip wall model the ciliary power and recovery stroke, resulting in an anisotropy of the viscous flow. We derive a coupled phase-oscillator description by reducing the microsphere dynamics to the slow timescale of synchronization and determine analytical metachronal wave solutions and their stability in a periodic chain setting. In this framework, a simple intuition for the hydrodynamic coupling between phase oscillators is established by relating the geometry of flow near the surface of a cell or tissue to the directionality of the hydrodynamic coupling functions. This intuition naturally explains the properties of the linear stability of metachronal waves. The flow near the surface stabilizes metachronal waves with long wavelengths propagating in the direction of the power stroke and, moreover, metachronal waves with short wavelengths propagating perpendicularly to the power stroke. Performing simulations of phase-oscillator chains with periodic boundary conditions, we indeed find that both wave types emerge with a variety of linearly stable wave numbers. In open chains of phase oscillators, the dynamics of metachronal waves is fundamentally different. Here the elasticity of the model cilia controls the wave direction and selects a particular wave number: At large elasticity, waves traveling in the direction of the power stroke are stable, whereas at smaller elasticity waves in the opposite direction are stable. For intermediate elasticity both wave directions coexist. In this regime, waves propagating towards both ends of the chain form, but only one wave direction prevails, depending on the elasticity and initial conditions.