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


General description - Detailed structure of the organs in C. elegans - Cephalic musculature - Neuropil

Cephalic musculature

Only much more general information is available concerning the pattern of nematode muscle innervation, which has been known from the work of Schneider (1860) to be peculiar in that the muscles send processes to the CNS rather than vice versa. The structure of the muscle cell itself has been investigated for over a century (reviewed by Debell, 65) and has been shown to consist of three parts an outer contractile portion apposed longitudinally just inside the cuticle; an intermediate "belly," containing the nucleus, other cellular organelles, and large supplies of glycogen; and an inner fiber portion which projects into the CNS (nerve ring or cords, depending on its location). The organization of the myofilaments in the contractile portion of the cell was investigated by Rosenbluth ('65a; 67) who found that they are arranged so as to produce an obliquely striated muscle as has been observed in a number of invertebrates. In this type of muscle the rectangular sarcomere typical of vertebrate striated muscle is in effect sheared along a plane parallel to the filaments, with the continuous Z-band plate being replaced by discrete posts which serve as points of attachment for the thin filaments.

As is generally true with the smaller terrestrial nematodes, somatic musculature in C. elegans is of the meromyarian-platymyarian type (Bird, '71), in which there is a single layer of sarcomeres beneath the cuticle (fig 19). When cut perpendicular to the body axis (fig 20A) the filaments of a muscle cell are seen to be grouped into from one to five sarcomeres. Each extends nearly the length of the cell and is separated from its neighbors by the Z-plane, into which the electron dense attachment posts are inserted at approximately one micron intervals along the animal. A higher magnification perpendicular view of a single sarcomere (fig 20B) reveals the expected banding pattern, a narrow central region in which only thick filaments are present (H band), two surrounding broader regions (A-bands) in which both thick and thin are present, and outside of them the two narrow regions consisting only of thin filaments (I bands). A longitudinal section through several sarcomeres of this muscle (fig 20C) illustrates the shear required to produce the oblique striated pattern from the striated one.

Several observations indicate thai in C. elegans body and cephalic somatic muscles may comprise two developmentally different muscle systems (i) body muscles send their innervation processes only to the nerve cords, whereas the processes from the cephalic muscle cells within each quadrant form a bundle of fibers which enter the nerve ring and there form chemical synapses directly with primary sensory cells as well as with unidentified interneurons; (ii) we possess a number of independently isolated, presumably point mutants in which body musculature is apparently normal but in which there is a defect in some or all of the cephalic musculature in the adult animal leading to partial or complete paralysis of the cephalic region. In such animals the volume normally occupied by the muscle cells is partially taken over by the very characteristically appearing hypodermal cells; (iii) we have isolated one example of a complementary mutant in which the cephalic region is fully active but in which the body muscles fail to function in the adult.

Figure 19

Fig. 19 - Schematic of a perpendicular section taken slightly anterior to the nerve ring neuropil. Only seven of the eight muscles in each cephalic bundle (M) are observed, the eigth originating slightly posterior. OeG: oesophageal gland; H, HN: hypodermal cell cytoplasm, nuclei; EC: excretory canal. Other abbreviations as in Abbreviations.

The cephalic region of C. elegans contains 32 muscle cells arranged into four submedial groups of eight (figs 19, 21). The positioning of the cells, nuclei, contractile portions, and innervation processes within any group represents a mirror reflection of the neighboring group, consistent with the basically bilateral symmetry of the animal observed both in the sensory organs and in their innervations of the nerve ring. The cells of each group of eight can be divided according to the locations of their contractile portions into an anterior four and a posterior four, or alternatively into a more medial four and a more lateral four. Although there is overlap, these divisions are always unambiguous, and they have a significance which is revealed in the way the muscles receive their innervation in the nerve ring (figs 22-27). Each muscle cell sends a process radially toward the oesophagus just behind the neuropil of the nerve ring. This process spreads out into a very thin sheet which extends circumferentially and longitudinally forward and is inserted between the 60-fiber sheets and nerve ring. Synapses from ring nerve fibers occur on small projections which are sent up toward the ring from the edge of this sheet in one case at the point of entry (fig 33), but mainly in the terminal medial and lateral regions (figs 26,27, 29, 32D).

Figure 20

Fig. 20 - A. Perpendicular section through part of a cephalic muscle bundle showing the contractile and non-contractile portions of some of its muscle cells. B. Higher magnification view of a single sarcomere. C. Longitudinal section through two neighboring muscle cells of a cephalic bundle. A: A-band, consisting of both thick and surrounding thin filaments; C: muscle cell cytoplasm; H: H-band, consisting of only thick filaments; I-band, consisting of only thin filaments; Z: z-posts.

The entry pattern of each fiber of the group is symmetric in all quadrants and identical in all animals studied. The four more medial cells expand their sheets medially around the oesophagus, the four more lateral cells laterally (figs, 22, 23). The division of the group of eight cells into four anterior and four posterior is also significant. The sheets themselves are stacked in order so that the more anterior muscle of the four has its sheet nearest the oesophagus, the more posterior just under the nerve ring. The four anterior muscles of the bundle have large swellings immediately before the formation of their sheets behind the nerve ring (figs, 22, 23). These swellings contain no mitochondria or other organelles, but are densely packed with glycogen granules (Rosenbluth '65b). The four more posterior cells on the other hand possess exceedingly slender processes (350 nm) before the formation of theIr sheets, which by electron microscopy seem to contain only small if any amounts of glycogen. These cells have a second pro- jection into the CNS, more posterior into their respective medial cords (fig 25). At these locations the entering processes are much broader and do possess a dense homogeneous glycogen content.

Figure 21

Fig. 21 - Diagram of the distribution of the contractile portions of the cephalic muscle cells representing a worm as if cut along its ventral midline and flattened into a plane, posterior end up. Positions of nuclei are indicated by circles. The column of labels to the left represents our identification of muscle cells within a bundle. M, broken lines: medial muscles; L, solid lines: lateral muscles; A: anterior; P: posterior.

At the medial and lateral poles where the sheets from two of the neighboring groups of eight meet there is formed a very characteristic synaptic region termed the muscle plate (figs. 26, 27). It is largely in this region that the muscle fibers send projections up toward the neuropil, and depending on the muscle cell, branch characteristically to receive theIr synaptic contacts. As has been described by Rosenbluth ('65b) for the innervation of the body somatic musculature by the ventral cord in Ascaris, the synapses do not have the appearance of vertebrate myoneuronal junctions but appear more like highly localized neuroneuronal synapses. Those homologous muscles which we have compared in different animals have shown the same course and branching pattern. Synapses onto the muscles come mainly from the motoneurons. Different muscle cells synapse with different numbers of motoneurons. Although none of the motoneurons has yet been traced to its cell body, the configuration of the neuropil is sufficiently reproducible from animal to animal to permit the conclusion that corresponding muscle cells in different animals are postsynaptic to the same set of fibers. Within the plates homologous muscle cells from the two neighboring quadrants have also been seen to contact one another by means of what appear to be gap junctions (fig 26, inset). We have also identified one case in which a primary sensory cell, the rootleted ciliary cell of the internal labial papilla, synapses dIrectly onto a muscle cell (fig 33, ILR synapsing onto muscle MA1), thus forming an evolutionarily primitive sensory motor synapse.

Web adaptation, Thomas Boulin, for Wormatlas, 2002