Neuronal coordination of motile cilia in locomotion and feeding

Philos Trans R Soc Lond B Biol Sci. 2020 Feb 17;375(1792):20190165. doi: 10.1098/rstb.2019.0165. Epub 2019 Dec 30.

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.

Publication types

  • Research Support, Non-U.S. Gov't
  • Review

MeSH terms

  • Animals
  • Cilia / physiology*
  • Feeding Behavior / physiology
  • Invertebrates / physiology*
  • Larva / growth & development
  • Larva / physiology
  • Locomotion / physiology
  • Polychaeta / growth & development
  • Polychaeta / physiology
  • Serotonergic Neurons / physiology*
  • Swimming / physiology