The Nerve Ring of the Nematode Caenorhabditis elegans: Sensory Input and Motor Output

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Table of contents   -   Abstract   -    Mat. & Methods   -    Observations   -    Discussion & Acknowledgments

Abstract

The general organization and structure of the nerve ring, the main mass of central nervous system neuropil, in the small soil nematode Caenorhabditis elegans is described. The nerve ring receives sensory input from the anterior tip of the animal by means of six nerve bundles, all nerve fibers of which have centrally located cell bodies. The anterior sensory structures are classically divided into two types, papilIary and amphidial, and are assumed responsible for mechano- and chemoreception, respectively. Papillary fibers enter dIrectly into the nerve ring, whereas amphidial fibers enter the ventral ganglion, a posterior extension of the nerve ring, in a circuitous, manner which is not discussed in detail. Of those papillary fibers which project into the nerve ring neuropil, 22 end in easily characterized sensory structures whereas 14 terminate distally near sensory organs but have no function which can be deduced on the basis of comparative morphology. After entering the ring the fiber, maintain their identity and do not anastamose with one another. Cell bodies of each papillary sensory neuron have been mapped around the nerve ring. The cephalic musculature is shown to consist of 32 muscle cells which form four longitudinal submedial groups of eight muscles each. Innervation of this musculature occurs wholly within the CNS by means of processes of the muscle cells which are sent centrally. The anterior 16 cephalic muscle cells are innervated by the ring only, in well delimited regions termed muscle plates. The posterior 16 are dually innervated by means of processes sent both to the nerve ring plates and to theIr nearest medial longtitudinal nerve cord. The nerve ring neuropil is characterized as having fibers containing one of four morphologically distinct vesicle types. Gap junction contacts are observed within the main neuropil involving one of these fiber types and within the muscle plate regions among muscle processes, which do not contain vesicles. An evolutionarily primitive sensory-motor synapse within the nerve ring is described from an identified sensory neuron onto an identified cephalic muscle cell process. Comparisons are made with the nervous system of Ascaris lumbricoides, the only other nematode to be extensively studied, to ilIustrate the conservativeness of the nemic nervous system.

A number of different approaches have been used in attempts to elucidate the nature of the rules of growth which lead to the observed high degree of specificity of neuronal connections. The most dIrect is simply to follow the growth of nerve fibers during embryogenesis (Waddington and Perry, '69; Hanson, '72; Trujillo-Cenoz and Melamed, '73; LoPresti et al., '73). Inferences have also been derived from neurophysiological investigations of connectivities in adult animals following regeneration of severed nerves or after surgical intervention during development (Sperry, '65; Jacobsen, '70; Yoon, '73) and by characterizing irregularities in the special case of a regular repeated adult structure (Horridge and Meinertzhagen, '70; Meinertzhagen, '72). It has been proposed (Benzer, '67) that the analysis of animals with single gene mutations leading to behavioral alterations can serve this same purpose, with the additional advantage that there is the possibility of analyzing the nature of the mutation biochemically.

Study of nematodes has appeared promising to a number of workers because, in spite of forming an extraordinarily widespread class adapted to live in many varied ecological niches, their varied structures represent fundamentally small variations on the same overall scheme. The central nervous system, in particular, consists of approximately the same number of cells in roughly the same arrangements from the smallest free living forms (less than 1 mm in length) to the very large mammalian parasites (up to 50 cm in length). This similarity may well prove to be useful in comparing the ultrastructure of some members of the group, necessarily the smaller ones, with electrophysiological results obtained from the larger ones.

The small soil nematode C. elegans is an excellent candidate for both mutational and ultrastructural studies. Extensive genetic analyses involving this organism have recently been reported by Brenner ('74) and have been related to DNA content by Sulston and Brenner ('74). Anatomical alterations in mutants have also been described (Brenner, '73). Mutational studies involving chemotactic behavior have been reported by Dusenbery ('73, '74), Ward ('73j and Dusenbery et al. ('75) indicating that mutants with quantifiable behavioral abnormalities can be obtained. Of particular interest for the work reported here, the central nervous system, consisting of about 200 cells, is sufficiently small to enable extensive reconstruction at the level of the electron microscope with an acceptable amount of effort. Because the number of neurons is small and, according to our results, the presence of each is invariant, it is likely that the proper connectivities of everyone is essential for the normal functioning of the animal. Thus one can hope to correlate an observed behavioral alteration with a particular morphologicai alteration in the CNS. In addition, it may be possible to use the analysis of mutants exhibiting partial expressivity to gain some insight into the mechanism of fiber growth and recognition which, in the normal animal produces a stereotyped nervous system with nearly 100% reproducibility.

We report here some results of the necessary first step in using the mutational approach to the study of neurogenesis, that is, the determination of the fundamental features of the wild type structure. These features will be used as a basis for the analysis of our existing chemotaxis, thermotaxis, and head muscle-defective mutants. In what follows we will discuss (i) the fine structure of the various anterior sensory organs and their projections to the central nervous system; (ii) the locations of the anterior sensory cell neurons around the nerve ring, the main part of the central nervous system, as revealed by complete three-dimensional reconstruction; (iii) the general layout and innervation of the cephalic musculature; (iv) the general structure of the neuropil of the nerve ring.


Web adaptation, Thomas Boulin, for Wormatlas, 2002