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Function
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unpublished).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(Dusenberry, '74; Brenner and Ward, unpublished).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