Neuronal coordination of motile cilia in locomotion and feeding

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'.

Keywords: Platynereis; calcium; ciliary band; ciliary swimming; evolution; marine larva.

Figure 1.

The diversity of ciliated larvae. (a) Nematostella vectensis uniformly ciliated planula (cnidarian), (b) Mueller's larva of the flatworm Maritigrella crozieri, uniformly ciliated, (c) annelid trochophore with ciliary bands, (d) annelid trochophore with ciliary bands (P. dumerilii), (e) larva of the brachiopod Terebratalia transversa, (f) Aplysia californica, mollusc veliger with ciliary bands, (g) Lineus longissimus, nemertean pilidium larva, (h) starfish bipinnaria larva, (i) echinoderm 8-arm-larva (sea urchin), (j) phoronid actinotroch larva, (k) amphioxus chordate larva and (l) Schizocardium californicum hemichordate tornaria.

Figure 2.

Mono- and multiciliated surfaces. (a) Annelid multiciliated cells of the ciliary band (P. dumerilii). (b) Multiciliated cells on a hemichordate larva. (c) Multiciliated cells on a nemertean pilidium larva. (d) Monociliated epithelium in the planula of N. vectensis. (e) Monociliated cells on echinoderm larval arms. (f) Monociliated cells in an amphioxus larva.

Figure 3.

Types of metachrony. (a) Side view of a row of beating cilia. Symplectic metachronal waves (i) propagate in the same, while antiplectic waves (ii) propagate in the direction opposite to the direction of the effective stroke. (b) Top view of a bundle of cilia. Metachronal waves can propagate orthogonally to the beat plane. Laeoplectic waves propagate to the left, and dexioplectic to the right relative to the effective stroke of the cilia. Based on [19].

Figure 4.

The ciliomotor circuit of the Platynereis larva. (a) SEM of a Platynereis nectochaete (3 days old) larva with ciliary bands labelled. Scale bar 50 µm. (b) serial scanning transmission electron microscopy (ssTEM)-based reconstructions of one of three catecholaminergic neurons (anterior view) and (c) of the closure-inducing cholinergic MC neuron (anterior view) in the Platynereis ciliomotor circuit. Ciliated cells are shown in grey. (d) Reconstruction of the serotonergic Ser-tr1 and (e) cholinergic Loop ciliomotor neurons (ventral views). (f) Synaptic connectivity graph of all ciliomotor neurons and ciliary band cells.

Figure 5.

Types of invertebrate ciliary systems and their control. Blue squares indicate presence, and red squares absence of a trait. Squares with no available data are crossed out. Phylogeny is based on [–117]. *Nemerteans show brief arrests coupled with muscle contractions upon contact with food particles. **Only motile cilia on the body surface (anuran larvae) are considered.