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.
Highlights
In Platynereis larvae, regular arrests are triggered by bursts of spikes that can be recorded from the ciliary band cells (Conzelmann et al 2011; Tosches et al 2014)
We can exclude a role for cholinergic neurons in rhythm generation since blocking cholinergic transmission did not eliminate the rhythmic activation of the MC neuron
The function of the rhythmically active ciliomotor circuitry is to trigger the coordinated arrests of all cilia in the body and likely to trigger the coordinated resumption of beating
Summary
Metachronal beating (Osterman and Vilfan 2011; Gueron and Levit-Gurevich 1999). Metachronal coordination requires the orientation of ciliary beating planes during development (Mitchell et al 2007; Park et al 2008; Mitchell et al 2009; Guirao et al 2010; Vladar et al 2012; Kunimoto et al 2012). Changes in ciliary beat frequency are coordinated to regulate flow rates. Annelid larvae show regular and coordinated arrests of the entire prototroch ciliary band (Conzelmann et al 2011). Such coordinated changes in ciliary activity, often triggered throughout the whole body, require neuronal control. We used whole-body connectomics, transgenic neuron labelling, and calcium imaging to reconstruct and functionally analyse the entire ciliomotor system in Platynereis larvae. We identified a ciliomotor system consisting of interconnected catecholaminergic, cholinergic, and serotonergic ciliomotor neurons These neurons form a pacemaker system responsible for the whole-body coordination of alternating episodes of ciliary arrests and ciliary beating to regulate larval swimming
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