The nervous anatomy of the body segments of nereid polychaetes

Abstract

The nerve cord of nereid polychaetes consists of intersegmental ganglia linked by narrower connectives. Each ganglion gives rise to four pairs of peripheral nerves designated in their order of origin IV, I, II and III, but numbered I-IV in their segmental succession. Nerve I arises from the cord immediately behind the intersegmental septum, II (the parapodial nerve) and III leave the posterior end of the ganglion near the middle of the segment and IV originates from the anterior (preseptal) part of the succeeding ganglion at the posterior margin of the segment. Nerves I and IV cross the floor of the body wall transversely and terminate in the dorsal integument, II supplies the parapodium and III links ipsilaterally with homologous nerves of other segments through a lateral nerve which runs longitudinally in the ventral body wall adjacent to the bases of the parapodia. Nerves II are the largest, IV are next in size while I and III are very fine and visible only after staining. All the nerves are mixed and contain relatively few fibres. Each, on the afferent side, supplies a determinable region of the integument, I and IV between them drawing on integumentary receptors over the greater part of the ventral and the whole of the dorsal surface. Nerve II alone receives excitation from the parapodial integument and III is primarily proprioceptive, fibres entering the nerve from the surface of the dorsal and ventral longitudinal muscles. Sensory cells are most numerous in the parapodia, particularly in the cirri, and are present in large number in the ventral body wall. There are very few in the dorsal integument. Almost all are bipolar, usually single but occasionally grouped. Two morphological types of sensory cell are described. The internal (centrifugal) fibres of the sensory cells either run directly into the segmental nerves or, more frequently, discharge excitation into the nerve through tracts of a lattice-like subepithelial plexus made up of fibres of multipolar association cells. Excitation originating in scattered receptors thus appears to be canalized into the few fibres of the main nerves by way of the plexus. The internuncial systems of the cord through which the afferent (and efferent) fibres make their central connexion are of two kinds, (1) giant-fibres and (2) fine-fibres. The paired lateral and paramedial giant-fibres and the single median dorsal giant-fibre have a similar arrangement and distribution in Platynereis dumerilii and Nereis diversicolor to that described by Hamaker (1898) in Neanthes virens . The fine-fibre internuncial neurons are of two types: (1) with short, richly branching axons forming an extensive network in the dorsal neuropile and (2) with long axons, possessed of few collateral processes, forming six longitudinal tracts extending suprasegmentally as dorso-lateral, dorso-medial and ventral tracts disposed symmetrically about the midline. Within the ganglion internuncially transmitted excitation is carried, by virtue of the orientation of the fibres, ventrodorsally within the neuropile. Afferent fibres connect directly with one or other of the six fine-fibre longitudinal tracts. Proprioceptor fibres probably discharge into the dorso-medial region of the ganglion, exteroceptor fibres into its dorso-lateral area. In addition, afferent fibres, of unknown sensory connexion, enter the ventral fine-fibre tracts from nerves II and IV but not from I and III. Incoming afferent fibres, except perhaps in this latter instance where the ventral tract is adjacent to the lateral giant-fibre, appear never to excite giant-fibres directly. The latter are considered to be indirectly excited through the diffuse pathways of the neuropile. Motor axons arise, as do internuncial fibres, from cell bodies in the crescentic cell cortex of the ganglion. Every segmental nerve contains at least one motor axon which crosses the dorsal neuropile of the ganglion from a contralateral cell body, the axon giving off longitudinally alined collateral branches which connect directly with one or more of the dorsal fine-fibre tracts. Synapses between the dorsally crossing motor axons and the giant-fibres have not been observed, though a motor fibre of ventral emergence in nerve IV is synaptically connected with the lateral giant-fibre. The probable significance of these direct and indirect neuron interrelationships is discussed in relation to the responses of nereids and to previously described properties of the giant-fibres. Each segmental nerve contains, at its root, from one to four motor fibres. There is evidence of multiplication of the fibres at the periphery of the nerve, not by branching, but by the interpolation into the motor tracts of relay neurons. In one instance (the parapodial nerve distal to its ganglion) second-order motor neurons contribute additional fibres to the branches. These in turn connect with third-order neurons supplying the muscles. The terminal motor innervation has, however, been seen only in a few places. The peripheral connexions, both on their afferent and efferent sides, thus embody relay neurons, and it is considered that the arrangement may permit of the short-circuiting of excitation and of the possibility of extensive local control of movement. Evidence is presented to show that nerve IV may be mainly concerned with the innervation of the longitudinal muscles of the body wall through the contraction of which locomotory flexures are developed. Nerve II is responsible for the motor innervation of the parapodium. The occurrence of peripheral nervous connexions between the two nerves further suggests that the co-ordination of body flexures and parapodial movements may not be entirely dependent on central nervous linkages.