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Consistent with the low phylogenetic status of nematodes, the neuropil of the nerve ring of C. elegans is exceedingly simple. It possesses none of the characteristics of fiber organization commonly associated with central ganglia of higher invertebrates such as distinctive glomeruli, stratifications, or giant fibers (Bullock and Horridge, '65). No doubt this is a reflection of the small number of neurons, each of which except for symmetry may be unique in function. It has been stated (Hyman, '51) that the nerve ring is more like a commisure connecting the lateral ganglia, which themselves correspond to the cerebral ganglia of other Protostomia. This seems not to be the case in C. elegans. Although the nerve ring does, in overall structure, have a commisural appearance in that its fibers travel largely in a circumferential direction, it is also the location of numerous synaptic interactions and the terminations of some identified sensory neurons. Since the lateral ganglia of C. elegans have no neuropil, it is apparent that from a functional point of view the nerve ring itself is the cerebral ganglion.
Fig. 22 - Schematic perpendicular section taken just behind the fibers of the nerve ring showing the entry of the eight muscles of one subdorsal cephalic bundle into the CNS. Muscle cell identification as in figure 21.
Fig. 23 - Electron micrograph at a level corresponding to figure 22. Arrow designates the very thin (350 nm) connection of two (MP1, MP2) of the posterior four muscle cells of the bundle.
Fig. 24 - Sagittal view of the entire dorsal nerve ring, sufficiently lateral of the vertical midplane to show the entry into the ring of some of the subdorsal muscle cells. Together with figure 26 this shows the plate-like nature of the muscle processes within the ring. Muscle cells are coded as in figure 21. DR: dorsal nerve ring fibers.
Fig. 25 - Perpendicular section through part of a subdorsal quadrant posterior to the nerve ring, showing the innervation processes of the MP1 psoterior muscle cell of a subdorsal bundle into the dorsal cord (DC). Muscle cells coded as in figure 21.
Fig. 26 - Ventral muscle plate, tangential section. Clustering of vesicles in the two symmetrically lacated presynaptic fibers on the midline can be seen, as well as a number of synapses onto muscle sheet processes. Some of the presynaptic darkenings show the more characteristic point-synapse structure on neighboring sections, and all, especially those onto the smallest sheet processes, are highly lacalized, spanning a distance no greater than that occupied by the postsynaptic muscle process. At the center of the plate the muscle processes become so convoluted and branched that they can only be identified in a long series of micrographs. M, the four entering muscle sheets from the medial muscles of the two subventral bundles in order from the oesophagus outward: MA1, MA2, MP1, MP2; 60: the subventral 60-fibers slightly anterior to their cell bodies. Beginnings of the granular, vacuolated cytoplasm characteristic of these cells can be seen. Inset: higher magnification of a different section showing the gap junction formed between the two homologous MA1 cells of the two subventral muscle groups (long arrow).
Fig. 27 - Longitudinal section taken near the midline showing a sagittal view of the ventral muscle plate (region enclosed by arrows, MP).
The most obvious deviation from a purely commisural nature of the ring occurs in its participation in the integration of sensory input and cephalic muscle motor output. Primary input is effected by synapses formed by the posterior processes of the bipolar papillary neurons whose cell hody locations have been described. The entry of these fibers into the ring is shown in the three parts of figure 28. In figure 28A the subdorsal papillary fibers are grouped as a bundle outside of the circumferential fibers of the nerve ring, but nonetheless within the thin glial sheath formed by the four LSM pocket cell bodies. In figure 28B at the posterior edge of the ring they are seen to turn from a longitudinal to a radial dIrection and plunge into the center of the circumferential fibers. At the level of figure 28C, taken anterior to figure 28A, all fibers except for those of the 60- and C-cells have completed a U-turn (the subdorsal LSM and 3-fibers accomplish this by branching and by multipolarity respectively as described) and again travel longitudinally but in an anterior dIrection. Shortly anterior to the U-turn all fibers diverge separately. The fibers may travel as much as 90° circumferentially and have aggregations of vesicles in presynaptic swellings which are large compared to the diameters of other circumferential ring fibers (fig 33, ILR).
A sagittal section through the entire dorsal extremity of the nerve ring, which consists of only about 100 fiber profiles (fig 29), shows a complete absence of penetration by the thin glial cytoplasm into the neuropil. Some organization is apparent. Most prominent is the anterior muscle plate region already described. It consists of a highly branched tangle of outward directed processes of the muscle sheets and is separated from the remainder of the neuropil by a slightly widened extracellular space which is occasionally seen to be filled with a slightly electron dense material (fig 30). All chemical synapses between ring and muscle fibers occur at the periphery of this delimited region, and no ring fibers penetrate into it. Numerous gap junctions are observed among the muscle processes themselves within the plate (fig 26, inset). Also apparent is a grouping of smaller, vesicle free fibers in the anterior ring region. Serial section analysis reveals few synaptic contacts within this cord of small fibers. This is in marked contrast to the surrounding neuropil consisting of larger diameter fibers which are densely packed with vesicles and form numerous synapses.
Four morphologically distinct vesicle types have been observed (fig 31). Whether these can be broken down further on the basis of histochemical properties remains to be seen. Most numerous are the typical small clear round vesicles 40 nm in diameter (fig 31A). These are the only vesicles observed at the synaptic darkenings at the muscle plates, and are observed in the central processes of the bipolar papillary sensory neurons. Nearly as numerous are slightly larger but much more irregular clear vesicles 55 nm in diameter (fig 31B). Dense core vesicles 65 nm in diameter, often mixed with clear vesicles, occur more infrequently and are associated particularly with fibers entering as part of the amphidial connective (fig 31C), never with papillary sensory fibers. Finally, we have observed that there are only two fibers, one on either side of the ventral midline, which possess neurosecretory-like vesicles of very large but non-uniform diameter (fig. 31D). The terminal swellings of these fibers occur just posterior to the ventral muscle plate and are connected to cell bodies in the region of tile ventral ganglion.
Fig. 28 - A, B, C. Three perpendicular views of a papillary bundle (DN) undergoing its U-turn entry into the nerve ring at its posterior edge. See text for explanation. The lateral papillary nerve (LN), containing both lateral papillary and amphidial fibers can also be seen in this section, as well as the large process of the amphidial pocket cell (A.P1 D. Schematic of the enclosed region in figure 28A identifying papillary components of the U-turn. l: LSM; m: MSM; n: ILN; r: ILR. Outside the nerve ring (upper left) the positioning of the papillary fibers is similar but not always the same in different animals. Within the ring (lower right), however, each fiber always has its same relative position with corrections occurring at the bend of the turn.
Fig. 29 - Sagittal section through the entire dorsal ring at the midline. Co: region of the small cord of fibers discussed in the text.
Fig. 30 - Higher magnification sagittal view of the dorsal muscle plate region (delimited by arrows, MP) taken near the midline showing the widened extracellular space separating it from the remainder of the nerve ring fibers.
Fig. 31 - A, B. Sagittal sections of the dorsal nerve ring near the midline illustrating the small clear and irregular clear vesicle types described in the text. C, D. Sagittal sections of the ventral nerve ring near the midline illustrating the dark core and neurosecretory-like vesicle types described in the text.
Fig. 32 - A. Point-type synapses from an unidenrified neuron onto an identified cell of the region of the ventrall ganglion. Inset: view of the same identified synapse taken in a perpendicular direction. N: nucleus of the postsynaptic cell. B. Serial point-synapse onto the dorsal muscle plate from unidentified fibers. C. Gap junction contact between two fibers of the irregular clear vesicle type in the dorsal ring. Inset: Higher magnification view of the same contact. D. A long en-passant synapse from an unidentified fiber onto several muscle sheet processes in the dorsal muscle plate.
By far the most common type of synaptic contacts are mediated by the so-called point synapses (fig 32A,B) which occur along the length of fibers and are not necessarily associated with a swelling of the presynaptic fiber. These are characterized by a very electron-dense presynaptic band usually packed with vesicles and forming a distinct convex protrusion from the presynaplic neuron. That the synapses are in fact highly localized can be seen in the two parts of figure 32A, which shows the same identified axosomatic synapses as cut in two perpendicular directions in different animals. Serial section analysis of junctions of this type in other regions of the neuropil has similarly verified their limited extend. Occasionally, both within the ring and at the muscle plate (fig. 32D), longer enpassant synapses without a membrane convexity are observed, although until preparative techniques have improved we cannot rule out the possibility that they are a series of point synapses. Both of these synapse types have the small clear round vesicles on the presynaptic side. Gap junctlon contacts are frequently seen (fig 32C). Invariably at least one, and usually both, of the participating fibers are of the irregular clear vesicle type. These fibers have never been observed to be presynaptic with a point synapse.
In addition to the highly unusual axosomatic synapse, we have also identified sensory motor synapse, which is of the point type, between the ILR fiber and the MPL muscle process (fig 33). This occurs not at the usual interior muscle plate region, but much more posteriorly, just after the entry of this muscle fiber into the ring. It is accompanied by a very large and terminal swelling of the ILR fiber which is nearly completely packed with vesicles. Serial section analysis of a number of these junctions has shown that they are composed of two point synapses, one slightly anterior to the other.
Fig. 33 - Sensory-motor synapses from the ILR sensory cell onto a projection of the sub-dorsal MA1 muscle cell sheet, perpendicular section.
Web adaptation, Thomas Boulin, for Wormatlas, 2002