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

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Table of contents  -  Abstract  -   Introduction  -   Materials & Methods  -   Results  -   Discussion  -   References


C. elegans has at least three sensory responses: chemical, mechanical and thermal (Ward, '73; Dusenberry, '73; Ward, unpublished). The chemical sense includes detection of at least four classes of attractants: cyclic nucleotides, anions, cations and hydroxyl ions (Ward, '73). The nematode is also repelled by acid, some form of carbonate ions, and aromatic compounds (Dusenberry, '74; Brenner and Ward, unpublished). From the altered chemotaxis of head-defective mutants, Ward ('73) concluded that the receptors detecting the attractants must be located on the head.
The structures of the sensilla on the head suggest which of them could detect these attractants, Chemoreceptive neurons must either directly contact the environment surrounding the nematode or contact another specialized cell which then contacts the surround. All of the neurons in the amphid meet these criteria, as does the inner labial neuron 2. Eight of the amphidial neurons, e-l, reach nearly to the opening in the cuticle of the amphidial channel. The three neurons a-c also contact the open channel further down. The neuron d has only a small branch reaching the open channel; however, it has a large surface area adja- cent to the sheath cell which bounds the channel, and therefore it might be a secondary sensory neuron such as is found in the mammalian taste bud (e.g., Murray and Murray, '70).
Amphids in other nematodes have been assumed to be chemoreceptors because they open to the outside, but no more direct evidence of their function has been presented (deConinck, '65; Bird, '71; Croll, '70). How- ever, the recent isolation of non-chemotactic C. elegans mutants which are defective in their amphidial neurons supports the interpretation that the amphid is a chemoreceptor (J. Lewis, personal communication).
The function of the amphidial sheath cell remains unknown. The large golgi apparatus with its forming face facing the amphidial channel suggests that it secretes material into the channel (Revel, '71). Presumably this material is stored in the large sheath cell vesicles and released into the channel, The sheath cell has been identified as a gland cell in other nematodes and esterase activities have been detected in the amphidial channel (Bird, '71; McLaren, '72). Its secretions may include mucus to protect the exposed neuron terminals or secretions which might be involved directly in neuron specificity or function.
The sheath cells surrounding all of the sensilla except the amphids have striking lamellar membrane invaginations which increase enormously the surface area of sheath cell membrane in contact with the neuron channels. Such membrane specialization might be for ion uptake and secretion so that these cells could regulate the ionic environment surrounding the sensory neurons thus affecting their sensitivity. The role of the socket cells appears to be support, but they may secrete the extracellular material lining the neuron channels.
The four additional sensory processes in the male cephalic sensilla are likely to be chemoreceptive because they contact the outside directly. A likely function for such a neuron would be to detect a sexual attractant released by a hermaphrodite. Sexual attractants have been described for several dioecious nematode species (Greet, '64; Green, '66; Cheng and Samoiloff, '71) but no evidence for asexual attractant in C. eleganshas been reported yet.
The mechanical and temperature sensitivity of C. elegans has not been studied extensively, but one can observe easily that a worm touched on the head backs up. Since we do not know how mechanical deformations are propagated along the cuticle we cannot predict which sensilla mediate this response. The inner labial, outer labial and cephalic sensilla are all candidates for mechanoreceptors because they have neurons ending embedded in the cuticle. They might also function as proprioreceptors since the fine structure of the cephalic sensilla resembles that of the proprioreceptive campaniform sensilla in insects (Moran et al., '72). Isolation of mutants altered in mechanosensitivity and identification of their anatomical defects might help to specify the function of these sensilla.

Comparison to nematodes and other invertebrates
The arrangement of nematode sensilla has been studied extensively with the light microscope because of its taxonomic importance (Chitwood and Wehr, '34; Chitwood and Chitwood, '38; DeConinck, '65). Chitwood and Wehr proposed that the primitive ancestral pattern of labial sense organs should consist of three sensilla per lip plus the amphids. They could arrange the phylogeny of various species so that it reflected modifications of this basic plan. They noted with chagrin, however (and this is confirmed by DeConinck ('65)), that no nematode has been discovered with three sensilla (excluding the amphids) on its lateral lips. Because the dorso-lateral sensilla is invariably absent, DeConinck proposed a different symmetry arrangement for the ancestral nematode: an inner ring of six; one outer ring of six; and an outer ring of four sensilla plus the two amphids. DeConinck proposed that the outer ring of four reflected the bilateral symmetry of the body rather than the hexaradiate symmetry of the head.
The arrangement of cephalic sensilla in the head of C. elegans conforms to the general nematode plan with no dorso-lateral sensillum. However, the cervical deirid is located dorso-laterally; it is similar in fine structure to the cephalic sensilla and like the cephalic neurons the deirid neurons contain catecholamines. Therefore, the deirid could be regarded as homologous to the cephalic sensilla. Thus, these sensilla would have a hexaradiate arrangement, with the lateral member displaced, supporting the model proposed by Chitwood and Wehr.
The structure of individual sensilla in C. elegans resembles sensilla in other nematodes, Goldschmidt ('03) first described that two accessory cells were associated with most of the sensilla. Goldschmidt found only one associated with the amphid but this was later corrected by Hoepli ('25). The resolution of the electron microscope has allowed us to describe the topology of these cells more accurately and we have renamed the cell which corresponds to Goldschmidt's Geleitezelle (accompanying or escort cell) the socket cell, and the cell corresponding to the Stützelle (support cell) the sheath cell. One reason for introducing this new terminology is that Goldschmidt's missing the Geleitezelle for the amphid has caused a subsequent confusion in terminology for the two cells found associated with amphids in other nematodes. In addition the terms "accompanying" and "support" cells have been used differently by different authors and some reviewers have confused them with labial cells.
Ciliated endings of nematode sensory neurons have been described for several species (for references, see McLaren, '72) and the complete structure of amphids from electron micrographs has been described recently by McLaren ('70) for Dipetalonema viteae, and by Storch and Riemann ('73) for Tobrilus aberrans. The amphid in D. viteae is similar in structure to that of C. elegans and has accessory cells corresponding to the sheath and socket cells. The accessory cells appear to be present in T. aberrans as well from the electronmicrographs shown, but they are not described as part of the amphid. In both cases, neurons with modified cilia pass out through a channel open to the outside. Other neurons ending in the sheath cell were not described but are found in other nematodes (Burr and Webster, '71).
As has been noted before (Lee, '65), the sensilla in nematodes resemble those in other invertebrates, especially arthropods (e.g. Slifter, '70; Hayes, '71; Harris and Mill, '73). They all have ciliated sensory neurons surrounded by specialized accessory cells. This similarity probably reflects evolution of convergent solutions to the problem of how to get a sensory neuron into or through an exoskeleton. Nonetheless, the possibility that the similarities in structure reflect a common primitive invertebrate ancestor with specialized sense organs should not be automatically dismissed.

The sensory-motor neuron
The finding that all six of the inner labial neurons 1 make direct chemical synapses to muscle arms establishes that these cells are sensory-motor neurons. Direct sensory-motor neurons have been postulated as intermediates in the evolution of nervous systems. Coggeshall ('71) described a possible sensory-motor neuron in the sea hare Aplysia, and a possible sensory-secretory neuron has been described in Trichuroid nematodes (Wright and Chan, '73). Interestingly, Goldschmidt ('08) proposed that one of the anterior sensory neurons in Ascarismight make a direct neuromuscular connection, but he could not be certain of this connectivity using only the light microscope. Our results suggest that Goldschmidt was correct so that sensory-motor cells may be common in nematodes. Since the nematode is a primitive invertebrate, such cells may indeed represent an important stage of the evolution of complex nervous systems.

Invariance and symmetry
The detailed comparison of the sensory terminals of several worms reveals little anatomical variation. The shape and position of the ciliated neuron endings and the arrangement of sheath and socket cells were identical in all animals examined. This invariance is also reflected by the symmetry of the sensilla, The animals are exactly bilaterally symmetric. The striking hexaradiate symmetry is not exact. The lateral pair of each type of sensilla are distinct from the sub-dorsal and sub-ventral pairs: the outer labial have smaller terminals, the inner labial have additional accessory neurons, the "lateral cephalics," the deirids, are displaced caudally. In addition, the inner labial sensilla do not have a medio-lateral plane of symmetry because in all sensilla the neuron 1 is most dorsal. These variations might indicate the influence of position on the development of sensilla specified identically genetically.
Four of the accessory neurons (the ventral inner labial accessory and the neuron m) vary both between and within animals in the number and length of their terminal branches. However, since the branches are absent in juvenile animals the growth of these processes may be age dependent and the variations found to be due to slight differences in age of the animals sectioned. There is also slight variation in the fine structure within the terminals of some of the neurons: the number of doublet microtubules in the neurons of the inner, outer and cephalic sensilla is variable and the presence of vesicles in the region of the basal bodies varies from animal to animal. This variation probably reflects the "noise level" in the developmental pathways specifying these structures. Since the animals were grown under identical conditions and are likely to be isogenic (Brenner, '74).
Although individual worms are not precise replicas of each other down to the finest details they are remarkably exact copies. By a combination of properties each individual cell and its processes may be uniquely identified in different animals. This is clearly essential for the ultimate interpretation of the anatomical findings in terms of function, but it is also important because it allows small anatomical changes to be reliably recognized in sensory mutants without complete reconstruction. A number of non-chemotactic mutants have alrcady been isolated (J. Lewis, personal communication and S. Ward and P. St. John, unpublished) and other sensory-defective phenotypes are being sought. These will be useful to further probe the structure and function of the nematode's sensory nervous system.

Web adaptation, Thomas Boulin, for Wormatlas, 2002