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


The arrangement of sensilla The tip of the head of C. elegans is shown en face in the scanning electron micrograph, figure 1. There are six symmetrical lips surrounding the triangular opening of the mouth. Each lip is surmounted by a papilla which is the ending of the inner labial sensillum. The lateral lips contain an inpocketing of the cuticle which is the opening of the amphid. Each sub-dorsal and sub-ventral lip has a pair of bumps and the lateral lip has a single bump visible. These are the endings of the cephalic and outer labial sensilla.
All of the cells found in the anterior 10 um of C. elegans' head are summarized in table 1. The non-neuronal cells were identified easily by their positions and morphology. The neurons were identified by synaptic connections in the central nervous system. Most of the neurons can also be recognized just by the fine structure of their anterior terminals.
The types of neurons in the tip of the head are summarized in table 2. (The labels given in this table will be used throughout this paper.) There are a total of 58 neurons arranged in bilateral, or apparent four and six-fold symmetries. This symmetry reduces the types of neurons to 21. With two possible exceptions (see below) all of the neurons appear to be sensory. Figure 2 is a micrograph of a transverse section cut 1 um from the tip of the head which shows the arrangement of the sensilla. Each of the six lips contains one inner labial and one outer labial sensillum. The sub-dorsal and sub-ventral lips each contain a cephalic sensillum. The lateral lips each contain an amphid. This arrangement of sensilla is summarized by figure 3 which shows diagrammatically all the sensilla and all the neurons in the head. The structure of each of these sensilla will be presented in the following sections.

Figure 1

Fig. 1 En face scanning electron micrograph. The six papillae surmounting the lips are the endings of the inner labial sensilla. Other sensilla endings are the small bumps and the inpocketing of the amphids which are labeled as indicated in table 2. This picture was taken by Mr. Len Christianson and Dr. Peter Andrews and kindly provided by Dr. David Hirsh. Magnification, x8,000.

TABLE 1: Cells in the anterior 10um of C. elegans
Cell type Number
Muscle 8
Hypodermal 8

Sheath 18
Socket 18
Neuron 58
Total cells 125

The hypodermal cells ring the circumference of the nematode and secrete the cuticle. The muscles lie longitudinally just under the hypodermis. The labial epidermal cells form the divisions of the six lips. The arcade cells line the esophagus: three syncytial anterior cells overlap six syncytial posterior cells. The nuclei of all the above cells lie 50-100 um from the tip of the head. The sheath, socket cells and the neurons make up the sensilla.

table 2

The inner labial sensilla The structure of an inner labial sensilIum is diagrammed in figure 4. Electron micrographs of transverse sections of this sensillum are shown in figures 5-13, and a longitudinal section in figure 15. Two sensory neurons innervate each sensillum. The ending of inner labial neuron 2 penetrates through a small opening in the cuticle at the tip of a papilla (figs. 4, 5, 6). The other neuron ends embedded in the cuticle approximately 0.5 um below this opening (figs. 4, 7). Both neuron processes then pass back through a channel in the cuticle and sub-cuticle. This channel is lined by extra-cellular material and bends inward before being encased by a specialized non-neuronal cell, the socket cell. The socket cell wraps around the channel approximately 1 um from the ending and seals to itself with a tight junction (figs. 28-30 for similar junctions). The extracellular material lining the channel ends where the socket cell forms a tight junction to another specialized non-neuronal cell, the sheath cell.
The sheath cell is goblet-shaped and surrounds the nerve channel. The neurons penetrate through the base of the sheath cell to reach the inside of the channel with tight junctions sealing the channel from the pseudo-coelom. The sheath cell membrane (the inner surface of the goblet) is deeply invaginated into lamellae below the region where the neurons penetrate the sheath cell. The spaces between lamellae are continuous with the sensory neuron channel, as drawn in figure 4 and shown in figure 10, 11 and 12.
The endings of the two inner labial sensory neurons have characteristic fine structure. Sensory neuron 1 has a basal body with seven doublet microtubles. These extend various distances up the nerve in a ciliary ring, some reaching the tip and fusing with an electron dense material This neuron also has a striated ciliary rootlet extending posteriorly from its basal body for about 7 um as shown in figure 15. There are one to four vesicles in this nerve just below its basal body. In glutaraldehyde fixed preparations the vesicles range in diameter from 250-900 Å and do not contain electron dense material.
Inner labial neuron 2 is exposed to the outside at its tip. It has a basal body with five to seven doublet-microtubules about 2.5 um. from its tip. These doublet tubules become singlets as they extend toward the tip, and two of them extend to the very end of the neuron. There is no ciliary rootlet.
Figure 4 shows an unciliated accessory neuron ending adjacent to a socket cell. A cell of this type is found invariably associated with the sub-ventral sensilla. In some animals this cell has a branch to the lateral sensilla as well. These accessory neurons sometimes end embedded in the socket cell but do not have specialized junctions at their endings. The dorsal sensilla have a similar neuron associated with them but this dorsal neuron is a branch of the lateral accessory neuron m discussed below.
The lateral inner labial sensillum has two additional ciliated accessory neuron labeled m and n. These neurons wrap around a branch of the lateral inner labial socket cell just below the region where the socket cell surrounds the neurons (fig. 2). Each contains a basal body near its ending containing nine doublet microtubules which extend anteriorly for about 1 um. The neuron m also has a short ciliary rootlet.

Figure 2

Fig. 2 Transverse section 1 um from the tip of the head. Sensilla and neurons are labeled as in table 2. The right sub-ventral side is more anterior than the left sub-dorsal. The specimen was prefixed in glutaraldehyde. Magnification, x 13,000

Figure 3

Fig. 3 Summary of the arrangement of neurons and sensilla in the head. All of the sensilla are shown as neurons surrounded by sheath cells (lightly shaded) with socket cells (darkly shaded) adjacent. Ciliatcd neurons are black, unciliated neurons are unshaded. Labeling is as in table 2.

Figure 4

Fig. 4 Inner labial sensillum. A right sub-ventral sensillum is shown diagrammatically in longitudinal and transverse section. The six inner labial sensilla have identical structure except for the accessory neuron. The outlines of the cells were simplified slightly from actual tracings and the number of membrane invagination in the sheath cell was reduced for clarity. The blackened junctions between cells represent tight junctions. Vesicles are shown near the basal body of neuron 1. The socket cell and the anterior part of the sheath cell are surrounded by a labial epidermal cell to which the socket cells make additional tight junctions. This cell is visible in figure 8 and 9.

Figure 5   Figure 6

Figs. 5,6 Tip of the inner labial sensillum. The very tip of the papilla is shown in transverse section, revealing that the inner labial neuron 2 opens to the outside through a channel in the cuticle. Figure 5 is a right sub-dorsal sensillum and figure 6 is a right sub-ventral sensillum from different animals. Magnification, x 21,000.

Figure 7

Fig. 7 Transverse section 0.5 um from the tip of an inner labial sensillum. This electronmicrograph shows the ending of the inner labial neuron 1. Magnification, x 21,000.

The outer labial and cephalic sensilla The six outer labial and four cephalic sensilla end beneath the cuticle and have similar structures. The lateral pair of outer labial sensilla differ somewhat from the sub-dorsal and sub-ventral pairs. The sub-ventral cephalic and outer labial sensilla are shown diagrammatically in figure 14. Figure 8-13 are electron micrographs of transverse sections through these sensilla.
In each sensillum a single neuron passes through a close-fitting channel about 1.5 microns long through the cuticle and sub-cuticular matrix and ends embedded in the cuticle. The neuron channel widens slightly where the socket cell wraps around it and seals to itself. Like the inner labial socket cells, the socket cell abuts onto a sheath cell with a tight junction. The sheath cell is again goblet-shaped with the neuron penetrating into the channel through its base. The channel is sealed from the pseudocoelom with tight junctions between the neuron and the sheath cell. Both the outer labial and the cephalic sheath cells have deeply invaginated membrane lamellae separated by spaces which are continuous with the channel surrounding the neuron.
The cephalic and outer labial neurons differ from each other in size and in the fine structure of their tips. Each cephalic neuron has a basal body with six to eight doublet microtubules which extend toward the tip for about a micron in a ciliary ring. The neuron widens just above where it enters the subcuticular matrix, and its microtubules are joined by other tubules organized in groups around an amorphous electron dense core. These tubules extend to the end of the neuron. The neuron has no ciliary rootlet.
The sub-dorsal and sub-ventral outer labial neurons have basal bodies with five to seven doublet microtubules. Apparent singlet tubules extend anteriorly from the basal body in a characteristic joined diamond pattern, which reaches almost to the end of the neuron (fig. 10). A striated rootlet 3 um long extends posteriorly from the basal body of the sub-dorsal and sub-ventral neurons. Both the cephalic and outer labial neurons have a small electron dense branch which extends to a bump in the cuticle without penetrating through the cuticle. This bump is visible in the scanning elec- tron micrograph, figure 1.
The lateral outer labial sensilla have a neuron, sheath and socket cell arrangement similar to the sub-dorsal and sub-ventral sensilla, but the fine structure is different. The neurons end about 0.5 um less anteriorly than the other outer labial sensilla. Their endings are shorter and smaller and are electron dense. These endings resemble the small electron-dense bump of the other outer labial neurons without the anterior extension. Their basal body is within 1 um of the endings and does not have a striated rootlet connecting to it. Because of these differences in fine structure, the designation of these lateral sensilla as outer labial is based on other similarities to the sub-dorsal and sub-ventral sensilla: the positions of their cell bodies; the similarity of then arrangement in the nerve cords; and the position and morphology of their sheath cells.

Figure 8   Figure 9   Figure 10   Figure 11   Figure 12   Figure 13  

Figs. 8-13 Series of transverse sections through the inner labial, outer labial and cephalic sensilla. The series is through a right sub-dorsal lip of a single animal fixed only with osmium. Labeling is as in table 2 and in addition. So, socket: Sh, sheath: Cu, cuticle. The sections are approximately 0.5 um apart and correspond roughly to the transverse sections diagrammed in figure 4 and figure 14. Unlabeled processes are branches of non-neuronal cells or of the right amphid. Magnification, x 26,000.

Figure 14

Fig. 14 Outer Iabial and cephalic sensilla. The left sub-ventral outer labial and cephalic sensilla are shown in longitudinal and transverse section in a manner similar to figure 4.

Figure 15

Fig. 15 Longitudinal section of an inner labial sensillum. The section is cut longitudinally tangential to the cuticle. The electron-dense tip of the papilla is shown. Below that, the section crosses the subcuticular endings of the outer labial and cephalic sensilla. The junction between the socket and sheath cells is indicated by arrows. The striated ciliary rootlet in neuron 1 shows clearly. The average spacing of striations is 750 Å. Magnification, x 14,000.

General structure The amphids are two large lateral sensilla each containing 12 sensory neurons and a sheath and socket cell. The amphid structure is shown diagrammatically in figure 18. Various aspects of the structure can be seen in figure 16-27 and figure 31 and figure 32. The general arrangement of neurons, sheath and socket cells shown in figure 18 is similar to that of the other sensilla. Eight of the neurons end in a channel which opens to the outside through the cuticle. This opening is formed by an infolding of the cuticle. The socket cell wraps around the channel and seals to itself as do the socket cells of the other sensilla. The socket cell is shown clearly in the longitudinal section, figure 17. The socket cell surrounds a sheath cell and joins to it with a tight junction (fig. 27). The neuron channel formed by the sheath cell is lined for part of its length by a densely staining extracellular material.

Sheath cell The ending of the amphidial sheath cell is a large bilobed structure as shown in figure 19. The longitudinal section shown in figure 18 is drawn as if cut along the radial axis of the nematode parallel to the line of view of the sheath cell shown in figure 19. Figure 18 shows that the neurons enter the sheath cell at the base of its channel with tight junctions sealing their entry. Unlike the sheath cells of the other sensilla the amphidial sheath cell does not have deeply invaginated membrane lamellae opening into the neuron channel. Instead, it has a large golgi apparatus giving rise to many large vesicles along its concave face facing the channel (figs. 17, 18, 25).

Figure 16

Fig. 16 Tangential section through an amphid. This section shows the seam of the socket ceII particularly clearly, as well as clustering of the neuron endings (N) as they pass into the socket cell channel. Vesicles (v) inside thc sheath cell adjacent to the channel boundary are also evident. Magnification, x 14,000.

Figure 17

Fig. 17 Radial section through an amphid. The opening of the amphid through the cuticle is shown with the neurons passing up the amphidial channel. The large white-ish vesicles (v) on the right are inside the amphidial sheath cell. Magnification, x 14,000.

Neurons Reconstructions of the endings of 12 sensory neurons which innervate the amphid are shown in figure 20 and 21. They all contain basal bodies with nine outer doublet microtubules located in the relative positions shown. They also contain 2-6 central singlet microtubules. In the endings e-l, the doublet tubules extend anteriorly in a ciliary ring nearly to the tip of each neuron and become singlet tubules near their endings (figs. 26, 27). Although the neuron endings e and g-k appear similar in morphology, each can be identified uniquely by the relative position of its basal body, its point of entry into the sheath cell, and, most importantly, its relative position in the sheath cell channel. This positioning will be described below. The eight cells e-l all pass up the amphidial channel nearly to its opening, as indicated in figure 18 and shown in figure 17. Because cells f and l are branched there are a total of ten ciliated processes passing up the amphidial channel.
The unusually shaped neuron endings a-d do not run all the way up the amphidial channel. Cells a-c run in the sheath cell channel up to their basal bodies but above this they poke their way into the sheath cell itself, like hands into a balloon, ending surrounded by the sheath cell. Cell d also pokes into the sheath cell but does so from outside of the sheath channel. It sends into the channel a small branch which is sealed off at its base by tight junctions to the sheath cell. None of these four neurons makes gap junction synapses to the sheath cell membrane; nevertheless, their shape creates an enormous surface area of membrane adjacent to the sheath cell membrane. There is always a 75-150 Å space between the two membranes. For cells a-c this space is continuous with the sheath cell channel. For cell d it is separated from the channel and the pseudo-coelom by tight junctions.
The arrangement of the four neurons (a-d) in the sheath cell is indicated in figure 18, 31 and 32. The cell with finger-like projections, d, is always dorsal; the branched cell a is dorso-lateral (it is the cell shown poking into the sheath in fig. 18); cell c has its wings extending both dorsally and ventrally; cell b has its wing ventral and the small branch dorsal in the channel.
Tracings of the cell positions at three different levels in the amphids are shown in figure 31; in figure 32 the arrangement of neurons in the left amphid of different adult animals is compared. The arrangement is identical in these four animals and is the same in males and juveniles. This invariant arrangement makes it possible to identify each amphidial neuron by its position in a single transverse section.

Other neurons There are six neurons in the tip of the head which are not intimately associated with sensilla. Two of these neurons end in unciliated large bulbs, located between the sub-dorsal cephalic sheath cell and the amphidial sheath cell. These are labeled x in figure 3, 12 and 13. Four other unciliated neurons end in thin sheet-like structures. The ventral pair extends on the ventral side of the sub-ventral inner and outer labial sheath cells just below their anterior endings. The dorsal pair extends similarly between the dorsal inner and outer labial sheath cells. They are labeled y in figures 3, 12 and 13. These cells may be homologous to Goldschmidt's ('03) four "Faserzellen" in Ascaris.

Figure 18

Fig. 18 Amphid. A right amphid is shown in radial and transverse section in the manner of figures 4 and 14. The shapes of the cells were simplified slightly for clarity. Dense vesicles are shown near the basal bodies of the neurons. A large golgi apparatus and mitochondria are shown in the base of the sheath cell. The scale of the transverse sections is one half that shown for the longitudinal sections.

Figure 19   Figure 20

Fig.19 Amphidial sheath cell. This drawing views a right amphidial sheath cell from the outside of a vertical nematode. The drawing was based on a computer reconstruction of cell outlines from series of transverse sections.
Fig. 20 Amphidial neurons a-d. The neurons are shown viewed from the side as for figure 19. They are based on computer reconstruction of transverse cell outlines. The rings of doublets indicate the position of the basal bodies.

Figure 21

Fig. 21 Amphidial neurons e-l. The neurons are shown as in figure 20.

Figure 22   Figure 23   Figure 24   Figure 25

Figs. 22-25 Transverse serial sections through an amphid. The series is through a right amphid of an animal fixed only with osmium. The neurons can be identified by comparison with figure 31. The sections are at approximately 1 um intervals. Magnification, x 18,000.

Figure 26   Figure 27

Figs. 26, 27 Fine structure of the amphidial neurons. High magnification electronmicrographs of transverse sections of the amphidial neurons of a glutaraldehyde-fixed specimen. (26) 3 um from the amphidial opening. Magnification, x 31,000. (27) 1 umm from the opening. Magnification, x 45,000.

Figure 28   Figure 29   Figure 30  

Figs. 28,29, 30 Cell junctions. High magnification pictures of the junctions between cells of a glutaraldehyde-fixed specimen. (30) A socket cell junction to itself. (29) A sheath-socket celljunction. (28) A sheath-epidermal cell junction. E, epidermal cell. Magnification, x 45,000.

Figure 31

Fig. 31 Arrangement of amphidial neurons. Tracings of transverse sections of the left and right amphids of a single animal are shown. The neurons are labeled as in figure 20 and 21.

Figure 32

Fig. 32 Comparison of the arrangements of amphidial neurons in different animals. The arrangement of neurons identified by their fine structure, shape and position is shown for three different animals. The left amphids are shown as in figure 31 at a level corresponding to the middle tracing in figure 31.

Males Series of transverse serial sections through the tip of the head of three adult male worms have been examined. The arrangement of sensory cells is identical with that of the hermaphrodite except that there is an additional sensory process in the channel of each of the cephalic sensilla. This process is a modified cilium but is smaller than the cephalic nerve ending. It penetrates the cuticle of the male, opening to the outside through a small papilla as shown in figure 33. This opening is continuous with the cephalic nerve channel so that in the male the entire channel appears to open to the outside.
These four extra processes exit posteriorly from the sheath cell channel with tight junctions to the sheath cell, as do the cephalic neurons. It is not yet known whether they represent four additional neurons or are extra branches of neurons also found in the hermaphrodite.

Figure 33

Fig. 33 Male. The additional process which is in the male cephalic sensilla is shown ending exposed to the environment in the channel of an extra male papilla. This is a right sub-dorsal lip with the endings of the cephalic and outer labial neurons shown. Magnification, x 32,000.

Deirids The deirids are a pair of lateral, cervical, sub-cuticular sensilla located about 70 um from the tip of the head. The ending of one of them is shown in figure 34. Like the other sensilla they have a ciliated sensory neuron in a channel surrounded by a socket cell and an invaginated sheath cell. The neuron channel does not penetrate the cuticle but ends longitudinally in the subcuticle, dorso-laterally. The fine structure of the ending closely resembles the endings of the cephalic sensilla showing many microtubules clustered around electron-dense material. Fluorescence microscopy of formaldehyde-treated worms shows that both the deirid and cephalic cell bodies and processes contain catecholamines and these six cells are the only anterior cells which do so (J. Sulston, personal communication).

Figure 34

Fig. 34 Deirid. The ending of the right deirid is shown. This transverse section was cut about 80 um from the tip of the head. The projections of the cuticle are the lateral "treads". D, deirid neuron. Magnification, x 27,000.

Juveniles Figure 35 shows a complete section of a first or second stage juvenile. All of the sensilla are present and are identical with those in the adult hermaphrodite except that the sheath cells are not as extensive and none of the non-ciliated accessory neurons are branched.

Figure 35

Fig. 35 Juvenile. A complete transverse section about 0.5 um from the tip of the head of a juvenile is shown. Compare this figure to figure 2 and notice that the non-neuronal cells are much less extensive and that the sheath cells are smaller and less invaginated. Magnification, x 17,500.

Positions of cell bodies The cell bodies for all cells in the anterior tip of C. elegans lie further back in the head. The neurons, sheath and socket cells connect to their cell bodies by long, thin processes that run down the head in six cords reflecting the arrangement of sensilla in the lips. Sections of the nerve cords are shown in figures 38 and 39. Although the sheath and socket cells run as nerve-like processes down the cords to their cell bodies, they do not give or receive synapses to any other cell and are, therefore, not neurons. In addition to the processes from cells in the tip of the head, 14 other processes are found in the anterior nerve cords.
These terminate about 15 um from the tip of the head, Two are interneurons which innervate the pharynx, and these are described in a subsequent section. Six others (one in each cord) are tiny processes from glial cells which line the inside of the nerve ring. Another four (2 sub-dorsal, 2 sub-ventral) are tiny processes from neurons which synapse onto muscles in the ring. Two more are tiny lateral processes from other neurons in the ring.
The positions of the cell bodies for all the processes in the anterior are shown in figure 40. Note that the positions of sheath and socket cell nuclei are not perfectly bilaterally symmetrical. The significant alterations are in the position relative to the first bulb of the pharynx. In the left dorsal cord, the outer labial socket cell nucleus is adjacent to the inner labial, anterior to the bulb, whereas in the right dorsal cord this outer labial socket cell nucleus is displaced posteriorly. A similar displacement is observed for the inner labial sheath cell in the two lateral cords. However, in all cases the sequence of cell bodies within each cord and the dorso-ventral positions of the cell bodies relative to the cords are the same. Two identical dorsal motor neuron cell bodies are also not bilaterally symmetrical: they are in reverse order on the two sides. The above variations in symmetry may be trivial due only to mechanical displacement by the pharynx so that the cell body positions actually reflect the bilateral symmetry of the sensilla in the head exactly.
The additional four- and six-fold arrangements of sensilla in the head are reflected in cell body position also but not as precisely. For example, if one compares the dorsal to the ventral cords one finds the same anterior-posterior sequence of neuron cell bodies (inner labial two, inner labial one, outter labial, cephalic) but the spacings and dorso-ventral displacements of the nuclei differ. The dorsal cephalic cell bodies are, in fact, posterior to the nerve ring itself. The positions of the lateral outer labial neuron cell bodies are similar to those of the outer labials in the dorsal and ventral cords and are not as posterior as the cephalic cell bodies, This is evidence supporting the designation of the lateral sensilla as part of the outer labial symmetry group.

Pharyngeal innervation Two neurons found in the lateral cord enter the anterior end of the pharynx. This connection was described in Ascaris by Goldschmidt (Bullock, '65), and our attention was drawn to it in C. elegans by R. L. Russell (personal communication). Figures 36 and 37 show the extension of this neuron into the pharynx. The neuron ends in an electron-dense specialization adjacent to two pharyngeal neurons with a possible gap junction between them.
The two neurons entering the pharynx are interneurons which receive synaptic input in the ring and are afferent to the pharynx (White, Thomson and Brenner, unpublished). They are the only two neurons which connect the somatic nervous system to the pharynx.

Figure 36   Figure 37

Figs. 36, 37 Pharyngeal neuron. Figure 36 shows the pharyngeal neuron (IP) extending an electron-dense process into the pharynx. Figure 37 shows this process two sections later ending as a densely staining process with a possible gap junction to neuron (3) within the pharynx. The two neurons labeled 3 and 4 both may be associated with the ending of the pharyngeal neuron. They appear to be fused in figure 37, but successive sections show that this is not so: the membrane boundaries are not perpendicular to the plane of section figure 37. Both neurons 3 and 4 have cell bodies with the pharynx. Magnification, x 30,000.

Figure 38
Figure 39

Fig 38 Sub-dorsal and sub-lateral anterior nerve cords. A transverse section approximately 30 u from the tip of the head. The sub-dorsal cord is the cluster of small processes at the top left. The amphidial neurons are the larger processes below the amphidial socket cell body; the small processes are from the other lateral sensilla and from other lateral cells (see tect). Magnification, x 13,000.
Fig 39 Neuronal cell bodies. A transverse section approximately 50 u from the tip of the head showing some of the neuron cell bodies on the right sub-dorsal side. mn motor neuron. Magnification, x 15,000.

Figure 40

Fig 40 Anterior nerve cords and sensilla cell bodies. The nerve cords and cell bodies of all cells which have processes in the anterior nerve cords are shown. They are drawn as if projected radially onto a cylinder through the length of the worm and the cylinder were cut along the mid-dorsal line and unrolled. The positions of the first bulb of the pharynx and the nerve ring are noted on the side. In addition to previous labels, cells are labeled as follows: G, glia; mn, motor neuron; in, inter-neuron; P, pharyngeal neuron. Non-neuronal cells are shaded. Not all the cell bodies in this region are shown. The neurons changing cords in front of the pharynx bulb are m and I Ac.

Axonal projections For clarity the axonal projections of the sensory neurons are not shown in figure 40. The axons of the sensory neurons, except for 11 of the amphidial neurons and neuron m, enter the circumpharyngeal nerve ring. The axons first pass posteriorly outside the nerve ring remaining grouped in symmetrical cords. They then turn back to form the neuropil of the ring making both gap junctions and chemical synapses en passant as they course anteriorly. Eleven amphidial neuron axons enter the ventral ganglia through commissures passing ventrally between the muscles and hypodermis. The synaptic connections of all of the neurons from the head have been determined. With the exception of the pharyngeal neurons and the neurons x, all the neurons give synapses in the ring, consistent with their designation as sensory. The axonal processes from all six inner labial neurons 1 make direct chemical synapses to muscle arms from the thirty-two most anterior body muscle cells. One such synapse is shown in figure 41. Each neuron makes several such synapses. This synaptic connection to a muscle makes the inner labial neuron a direct sensory-motor neuron. However, these neurons also synapse onto interneurons, including the neuron which connects to the pharynx, and they have a peculiar synapse-like association with hypodermal cells. The details of these connections and the synapses of the other neurons will be described elsewhere.

Figure 41

Fig 41 Nerve ring. A transverse section of the right lateral and ventral regions of the nerve ring. The small processes labeled 1 and 2 to the lower left of center are the sub-ventral inner labial neurons as they pass posteriorly. After turning around they become larger and are the processes with vesicles labeled I-1 and I-2 which are passing anteriorly. The inner labial neuron 1 is also labeled at the top of the section. the arrow shows a synapse to a muscle process (M). The muscles in nematodes receive innervation by sending processes to the nerves; the process labeled M is from the most anterior head muscle. The synapse is recognized by its characteristic electron dense presynaptic specialization. It extends for several sections and this neuron makes four such synapses to the muscle. Magnification, x 17,000.

Web adaptation, Thomas Boulin, for Wormatlas, 2002