Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva

Abstract

Ciliated surfaces harbouring synchronously beating cilia can generate fluid flow or drive locomotion. In ciliary swimmers, ciliary beating, arrests, and changes in beat frequency are often coordinated across extended or discontinuous surfaces. To understand how such coordination is achieved, we studied the ciliated larvae of Platynereis dumerilii, a marine annelid. Platynereis larvae have segmental multiciliated cells that regularly display spontaneous coordinated ciliary arrests. We used whole-body connectomics, activity imaging, transgenesis, and neuron ablation to characterize the ciliomotor circuitry. We identified cholinergic, serotonergic, and catecholaminergic ciliomotor neurons. The synchronous rhythmic activation of cholinergic cells drives the coordinated arrests of all cilia. The serotonergic cells are active when cilia are beating. Serotonin inhibits the cholinergic rhythm, and increases ciliary beat frequency. Based on their connectivity and alternating activity, the catecholaminergic cells may generate the rhythm. The ciliomotor circuitry thus constitutes a stop-and-go pacemaker system for the whole-body coordination of ciliary locomotion.DOI: http://dx.doi.org/10.7554/eLife.26000.001

Serotonin in Animal Cognition and Behavior

“…5-HT is a major neuromodulator of motor behaviors ( Figure 1A) in many species belonging to different invertebrate phyla. This includes flatworms [58], cnidarians [59], nematodes [60], annelids [61,62], arthropods (insects and crustaceans, [63][64][65]), and mollusks [66][67][68][69]. Part of our knowledge comes from studies investigating the ecological/toxicological consequences of SSRIs used as antidepressants, released in sanitary water, and finally spread in rivers [63,65,[70][71][72].…”

On the unity and diversity of cilia

“…For example, at the size and complexity scale of marine larvae, this swimming-feeding trade-off becomes particularly significant. New insights into the pathways and control architectures used by marine organisms for regulating the activity of extended ciliated bands and surfaces have been made possible by detailed reconstructions of whole-organism neurocircuitry by serial EM [41]. Delving deeper into the developmental and molecular diversity of cilia and basal bodies may help us understand how different types of cilia came to be specialized for different functions, even within the same organism [42].…”

“…Eichele et al [59] detail the types, alignment and putative transport functions of cilia existing in the ependyma. Over the course of evolution, nervous systems arose to coordinate ciliary locomotion over even longer distances, adding a new dimension to controlling ciliated structures [41,60]. Marinkovic et al [61] review the anatomy, ciliomotor circuitry and feeding systems in marine invertebrates, focusing on the neurons that innervate ciliated cells, and the diverse physiological cues that modulate ciliary activity through the release of neurotransmitters and neuropeptides.…”

Neuronal coordination of motile cilia in locomotion and feeding

“…In some cases, large neurons known as ciliomotor neurons that innervate multiple ciliated cells are used to coordinate ciliary activity throughout an organism. The recently characterized whole-body ciliomotor circuit of the marine annelid Platynereis dumerilii [12] highlights the sophistication of a dedicated ciliomotor circuit. In Platynereis larvae, large biaxonal neurons form a morphologically and functionally distinct ciliomotor nervous system coordinating whole-body ciliary activity.…”