Embodied behavioural complexity in a ciliated microorganism

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Abstract Most animals coordinate behaviour using neural computations. Yet, single-celled organisms also exhibit stimulus-responsive, even cognitive, actions. To understand how a single cell can coordinate and drive complex behaviours without any neural encoding, we study an algal protist – a motile cell with four extremely long cilia. The organism displays a surprisingly rich locomotor repertoire, emerging from the intricate dynamics of the cilia, which form a tight bundle when swimming. We use high-speed quantitative live imaging to extract the spectrum of possible ciliary beating patterns and derive a dispersion relation coupling the temporal frequency and spatial wavelength of cilia oscillations. We further reconstruct the manifold embedded in the behavioural space, showing that despite the range and complexity of ciliary beating modes, the underlying behavioural manifold is intrinsically low-dimensional with non-trivial topological structure. Dynamic transitions in motility patterns are encoded as trajectories in this space, thus reducing the macroscopic behavioural states to the underlying microscopic dynamics of the cilia.

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