Ciliary band innervation in the bipinnaria larva of Pisaster ochraceus

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Abstract
Characteristic features of ciliary band organization and neurociliary innervation in Pisaster ochraceus larvae are described at the ultrastructural level. Serial reconstructions of selected parts of the band are used to identify the main nerve cell types and trace their fibres. The band has an intraepithelial plexus of fibres near its base and a ciliary nerve that runs along the aboral margin of the plexus. Three nerve cell types occur within the band: sensory cells, which lie along the oral margin of the band; bipolar cells, which lie along the ciliary nerve; and multipolar cells, which are more generally distributed in the band between the other two types. The sensory and bipolar cells are similar in appearance. Both contain dense-core vesicles and have slender basal processes that run lengthways along the plexus. The multipolar cells have extensive local arrays of basal processes filled with clear vesicles, and unusual apical processes that run across the apical surface of the band between the bases of its cilia. The ciliary nerve consists predominantly of a separate fibre type that originates outside the band, probably in the oral region. Behavioural tests show that the larvae are capable of modulating ciliary beat, but coordinated reversals and arrests like those seen in other echinoderm larva do not occur. The modulatory effect operates over the long term, in response to culture conditions and nutritional state, and is involved in the larval response to contact. The latter has both neurociliary and neuromuscular aspects. There is a momentary pause in swimming and coincident backward flexure of the preoral hood. Sustained ciliary effects and flexures are induced by cholinergic agonists, notably nicotine, and transitory effects occur in response to catecholamines. Serotonin inhibits the neuromuscular response. Assessment of the cell types, their position, morphology and contents, suggests that the sensory and bipolar cells are catecholamine-containing. The former probably have a sensory function. We suggest that the multipolar cells are cholinergic effector neurons that act directly to control ciliary beat. There are two phylogenetic aspects of interest: (1) the echinoderm system represents an improvement on the condition seen in more primitive larval bands, which have fewer identifiable nerve cell types and more limited behavioural capabilities; (2) the bipinnaria provides an example of neural organization in a dipleurula-type larva. According to Garstang, the first chordates may have evolved from such a larva. Comparing our results on cell types, their relative positions and probable functions, with basic features of the chordate central nervous system (CNS), provides at least provisional support for this proposal.