Abstract

Efficient ciliary locomotion and transport require the coordination of motile cilia. Short-range coordination of ciliary beats can occur by biophysical mechanisms. Long-range coordination across large or disjointed ciliated fields often requires nervous system control and innervation of ciliated cells by ciliomotor neurons. The neuronal control of cilia is best understood in invertebrate ciliated microswimmers, but similar mechanisms may operate in the vertebrate body. Here, we review how the study of aquatic invertebrates contributed to our understanding of the neuronal control of cilia. We summarize the anatomy of ciliomotor systems and the physiological mechanisms that can alter ciliary activity. We also discuss the most well-characterized ciliomotor system, that of the larval annelid Platynereis. Here, pacemaker neurons drive the rhythmic activation of cholinergic and serotonergic ciliomotor neurons to induce ciliary arrests and beating. The Platynereis ciliomotor neurons form a distinct part of the larval nervous system. Similar ciliomotor systems likely operate in other ciliated larvae, such as mollusc veligers. We discuss the possible ancestry and conservation of ciliomotor circuits and highlight how comparative experimental approaches could contribute to a better understanding of the evolution and function of ciliary systems.This article is part of the Theo Murphy meeting issue ‘Unity and diversity of cilia in locomotion and transport’.

Highlights

  • Ciliary locomotion occurs in the majority of unicellular eukaryotes [1,2] and is widespread in animals

  • There is a great diversity in the mode of movement, the type of ciliation and the tissue-scale dynamics of cilia

  • Flow-based hydrodynamic coupling of adjacent cilia of the same ciliary band or the same ciliated epithelium contributes to the generation of metachronal waves

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Summary

Introduction

Ciliary locomotion occurs in the majority of unicellular eukaryotes [1,2] and is widespread in animals. There are several other contexts where ciliated fields and the flows they generate are important for animal physiology, including the establishment of symbiosis in squid [9], mixing the boundary layer in corals [10] or the movement of cerebrospinal fluid in the vertebrate brain [11]. In Platynereis larvae, large biaxonal neurons form a morphologically and functionally distinct ciliomotor nervous system coordinating whole-body ciliary activity. Future comparative studies could test the hypothesis that ciliomotor nervous systems have a unique evolutionary history with potentially deep origin in animal evolution [13,14]

Types of ciliary locomotor and feeding systems in invertebrates
Ciliary coordination by biophysical and cellular mechanisms
Neuronal and paracrine mechanisms of ciliary coordination
Innervation of ciliary bands
The ciliomotor circuit in the Platynereis dumerilii larva
The evolution of ciliomotor cell types and circuits
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