The sensory neurones and sensilla in the abdomen and thorax of the blowfly larva ByM. P ...

17 Pages·2006·1.99 MB·English

227
The sensory neurones and sensilla in the abdomen and
thorax of the blowfly larva
ByM. P. OSBORNE
(From the Department of Zoology and Comparative Physiology, The University,
Birmingham, 15)
With 2 plates (figs. 10 and 11)
Summary
The peripheral nervous system in the Phormia larva consists of bipolar neurones that
end in specialized sensilla, and bipolar or multipolar neurones with ramifying distal
processes. The former are associated with the cuticular sensilla and chordotonal
organs. The latter (a) constitute a sub-epidermal nerve-plexus with processes that
occasionally run over skeletal muscles, (b) innervate specifically orientated strands of
connective tissue, the longitudinal, vertical, and ventral stretch receptors, and (c)
innervate the tracheal epithelium, imaginal buds and associated pedicels, and the
nerve-sheaths.
Introduction
A SUB-EPIDERMAL nerve-plexus of multipolar neurones was first described
in insects by Viallanes (1882 a, b) in the dipteran larvae Stratiomys, Eristalis,
and Musca. A similar plexus has been described in cerambycid beetles
(Monti, 1893, 1894), in the caterpillar Sphinx lingustri (Holmgren, 1896), in
the silkworm larva (Bombyx mori) (Hilton, 1902), and in the larva of Melolontha
vulgaris (Zawarzin, 19126). Multipolar neurones associated with the body-
wall, muscles, and joint membranes of various insects have been reported by
other workers (Cajal, 1890; Zawarzin, 1912a; Rogosina, 1928; Tonner, 1936;
Josting, 1942; Meyer, 1955; Barbier, 1961; Hamon, 1961). Zawarzin (1916)
and Orlov (1924) have described multipolar neurones associated with the
muscles and epithelia of the insect gut.
Zawarzin (19126) and Monti (1893, 1894) are confident that the dendrites
from adjacent neurones do not anastomose, but other authors, for instance
Viallanes (1882 a, b), Holmgren (1896), and Hilton (1902), believe that the
dendrites from different neurones fuse to form a 'nerve-net'.
The structure and function of the sub-epidermal nerve-plexus in insects has
been reviewed by Snodgrass (1926). The terminal branches of the sub-
epidermal plexus are believed to end freely on the basement membrane. It is
suggested that these neurones are sensitive to mechanical stimuli or perhaps
changes in temperature, although they may receive general sensations such as
pain.
Welsh (1937) reported two clusters of multipolar neurones in the prothorax
of dipteran larvae and thought that they were photoreceptors. Bolwig (1946)
proved the dipteran photoreceptors to be located on the head, but stated
emphatically that there were no multipolar neurones associated with the
[Quart. J. micr. Sci., Vol. 104, pt. 2, pp. 227-41, 1963.]
228 Osborne—The sensory neurones and sensilla in the
epidermis, and suggested that the multipolar neurones described by Viallanes
and Welsh were tracheal end-cells. Hertweck (1931) described in detail the
nervous system and sense organs of Drosophila melanogaster but did not refer
to any multipolar neurones innervating the epidermis. He even saw the longi-
tudinal stretch receptor strands (Seitenstrdnge) but did not describe their
innervation by sensory neurones.
Thus there appears to be considerable controversy in the literature about
the occurrence of a multipolar nerve-plexus beneath the epidermis of dipteran
larvae, and whether the dendrites from different nerve-cells anastomose. It
was noticed during the investigation of dipteran stretch receptors that many
multipolar nerve cells were associated with the epidermis of the blowfly
larva. In view of the difference of opinion which exists between earlier
workers, it was decided to reinvestigate the sub-epidermal nerve-plexus in the
dipteran larva.
Material and methods
Large larvae of Phormia terrae-novae were used for this work. The peri-
pheral nervous system was stained supravitally with methylene blue by the
technique described in a previous paper (Osborne and Finlayson, 1962).
After staining and fixing, the skeletal muscles were carefully removed so as to
expose the nerves innervating the epidermis. The material was then dehy-
drated and mounted in dammar. Photomicrographs of preparations were
taken on Ilford Pan F 3 5-mm film with a Zeiss photomicroscope.
Results
Throughout this work only the thoracic and abdominal segments 1 to 7 were
investigated. The topography of the peripheral neurones and sense-organs is
different in each thoracic segment (figs. 1, 2) but similar in all abdominal
segments (fig. 3). For the sake of clarity only the main dendrites of the
multipolar neurones are shown. The peripheral nerve-cells are classified
according to Zawarzin (1912a).
Type I cells are always bipolar and are associated with the cuticular sensilla
and chordotonal organs. Type II cells are multipolar or bipolar, and include
the stretch receptor neurones, the neurones innervating the epidermis, and
certain cells to be described later which have a type of innervation not
previously reported.
Type I cells
Two types of epidermal sensilla were found in the thorax and abdomen.
The more numerous are campaniform sensilla (figs. 4, A; 10, B, E), of symmet-
rical form. Twenty-two have been found in each abdominal segment, 20 in
the meso- and metathorax, and 22 in the prothorax. Their positions on the
cuticle are remarkably constant. In the mesothorax, metathorax, and abdominal
segments they are arranged roughly in an annulus round the centre of the
abdomen and thorax of the blowfly larva 229
segment (figs. 1, 2, 3). In the prothorax (fig. 1) they are arranged in a ring on
the ventral and lateral sides, but in the dorsal region they form a cluster.
The second type of sensillum consists of 3 neurones, the dendrites of which
extend into a fine channel running through the cuticle and terminate beneath
a small pore on the surface of the cuticle (figs. 4, B; 10, F). Only 4 of this type
of sensillum are found in each segment. In the prothorax 2 are found in
FIG. 1. Lateral view (from inside) of the right half of the pro- and mesothorax of a Phormia
larva, to show the topography of the sensory neurones and sensilla. cam, campaniform
sensillum; cs, cuticular sensillum (possibly a chemoreceptor); co, chordotonal organ; Ir,
longitudinal stretch receptor; mn, multipolar neurone; sp, spiracle.
the dorsal region and 1 on each ventro-lateral area, while in the meso- and
metathorax they are found on the lateral and ventral surfaces. In the
abdominal segments they are arranged in similar manner to those in the
prothorax.
The topography and structure of the chordotonal organs in the abdomen of
Phormia are exactly the same as those described by Hertweck (1931) in
Drosophila larva. There are, however, fewer chordotonal organs in the thorax
of Phormia than in Drosophila.
There are 8 chordotonal organs in abdominal segments 1 to 7. In each
segment there are 2 on each side of the ventral mid-line, 1 in each lateral
region, and 1 on each side of the dorsal mid-line (fig. 3). The ven-
tral chordotonal organs all have a single scolopidium and are orientated
230 Osborne—The sensory neurones and sensilla in the
transversely. Each lateral organ has 5 scolopidia (fig. io, G) and is orientated
obliquely. The dorsal chordotonal organs are orientated transversely and each
has a single scolopidium. In both the meso- and metathorax (figs. 1, 2) there
are only 2 chordotonal organs, one on each side of the dorsal mid-line. Each is
Obmrn
FIG. 2. Lateral view (from inside) of the right half of the metathorax of a Phormia larva to
show the topography of the sensory neurones and sensilla. cam, campaniform sensillum; cs,
cuticular sensillum; co, chordotonal organ; Ir, longitudinal stretch receptor; mn, multipolar
neurone.
orientated transversely and has 3 scolopidia. Four chordotonal organs are
found in the prothorax (fig. 1). There is 1 on each side of the dorsal mid-line
and 1 in each lateral region. All have 2 scolopidia. The axons from the lateral
chordotonal organ join the main segmental nerve of the mesothorax, unlike
the other chordotonal organs whose axons join the segmental nerves of the
segments in which they are located.
abdomen and thorax of the blowfly larva 231
Type II cells
The sub-epidermal nerve-plexus is composed of multipolar neurones (figs.
10, A; 11, A). The neurones and their main dendrites are surrounded by a
neurilemma sheath (fig. 10, c, j). Often dendrites or dendrites and axons
OS /7J/7J
FIG. 3. Lateral view (from inside) of the righthalf of the fourth abdominal segment of aPhormia
larva to show the topography of the sensory neurones and sensilla. cam, campaniform sensillum;
cs, cuticular sensillum; co, chordotonal organ; Ir, longitudinal stretch receptor; mn, multipolar
neurone; ven, ventral stretch receptor; vr, vertical stretch receptor.
from different neurones run in common sheaths (fig. 5). Connective-tissue
fibres sometimes join adjacent neural sheaths together, or anchor them to the
epidermis (figs. 5; 10, j). The main dendrites branch profusely, giving rise to
a plexus of exceedingly fine neural processes which have a characteristic
beaded appearance and are apparently without a neurilemma sheath (figs.
232 Osborne—The sensory neurones and sensilla in the
5; 11, A). The plexus forms a delicate interwoven meshwork that runs over
the basement membrane of the epidermal cells. I believe that this plexus
covers practically the entire epidermis of the blowfly larva. No dendrites were
seen to penetrate the basement membrane between the epidermal cells or
ramify beneath the cuticle. The vast majority of dendrites appeared to end on
the basement membrane of the epidermal cells although a few were found to
FIG. 4. Cuticular sensilla from the abdomen and thorax of the Phormia larva. A, campaniform
sensillum. B, possibly a chemoreceptor.
terminate on skeletal muscles. In no case has any anastomosis been seen
between the dendrites of different neurones, although processes from different
cells may run very close together. The number of neurones in each segment
is always the same, and there is little variation in their topography. There are
24 neurones constituting the nerve-plexus of the prothorax, 28 in both the
meso- and metathorax, and 30 in each abdominal segment (figs. 1, 2, 3).
Typically the neurones are arranged approximately in 6 main groups in all
segments. Two are located dorsally, 2 ventrally, and 1 in each lateral region.
The topography of the neurones in the dorsal groups of the mesothorax,
metathorax, and abdominal segments is similar. One of the neurones in the
dorsal group always has a cell-body that is about twice the diameter of that of
the other neurones (fig. 11, A). In the prothorax the anterior neurones of the
abdomen and thorax of the blowfly larva 233
dorsal plexus are grouped more closely together and are situated nearer to the
intersegmental fold than they are in other segments. A comparison of the
lateral groups shows that the neurones are distributed anteriorly in the pro-
thorax and abdomen, and in the middle of the segment in the meso- and meta-
thorax. The neurones constituting the ventral groups are arranged similarly
FIG. 5. Drawing of part of the multipolar nerve-plexus of a Phormia larva to show dendrites
and a dendrite and axon from different neurones running in common neurilemma sheaths, ax,
axon; con, connective tissue; d, dendrite; ns, neurilemma sheath.
in the thoracic segments. The neurones of the ventral groups in the abdomen
are more widely distributed laterally and anteriorly than they are in the thorax.
A number of neurones in the body-cavity are associated with strands of
connective tissue. These are the stretch receptors (Finlayson and Lowenstein,
1955; Slifer and Finlayson, 1956; Finlayson and Lowenstein, 1958; Osborne
and Finlayson, 1962).
In the larva of Phormia 3 pairs of stretch receptors have been located in
abdominal segments 1 to 7. Two are present above the dorsal musculature,
the longitudinal and vertical receptors, but the third is located amongst the
ventral musculature (fig. 6). These paired ventrally located receptors are con-
sequently termed 'ventral receptors'. The longitudinal and vertical receptors
234 Osborne—The sensory neurones and sensilla in the
lie above 2 layers of dorsal longitudinal muscles which run obliquely across
the segment.
The longitudinal receptor is suspended between the intersegmental folds and
07S/n/7?
FIG. 6. Diagram of the right half of the sixth abdominal segment of a Phormia larva with
various muscles removed to show the location of the 3 stretch receptors. Ir, longitudinal
receptor; ven, ventral receptor; vr, vertical receptor.
consists of a multipolar neurone associated with a strand of connective tissue
(fig. 10, H). The neurone, which is contained in a fibrous capsule, is situated
near the centre of the strand. The connective-tissue fibres of the strand are
organized to form a tube, inside which run the dendritic processes (fig. 7, A).
These have been seen to extend as far as the regions where the connective-
tissue fibres fan out at the ends of the strand to make the attachments to the
abdomen and thorax of the blowfly larva 235
intersegmental folds (figs. 7, A; 10,1). Fine connective-tissue fibres anchor the
receptor to the main branch of the tergal nerve which runs between the second
and third bands of both layers of dorsal muscles to provide sensory innervation
for the tergal epidermis. The axon from the neurone joins this nerve.
The vertical receptor (fig. 8) consists of a bipolar neurone associated with a
strand of connective tissue. The strand is anchored at one end to the tergal
epidermis (fig. 6), and at the other to the motor branch of the tergal nerve
50//
FIG. 7. Diagram to show the structure and posterior attachments of the longitudinal, A, and
ventral, B, stretch receptors of the Phormia larva.
where it runs below the second and third dorsal muscle-bands. Some con-
nective-tissue fibres are also attached to these two muscles. The connective-
tissue fibres are more diffusely arranged than those of the longitudinal
receptor, with the result that the tubular structure is not so compact or well
defined. The neurone is situated on the epidermis and is enclosed within a
neurilemma capsule which is continuous with that of one of the epidermal
sensilla that have 3 neurones (fig. 8). The distal process runs inside the
connective-tissue strand as far as its attachment to the tergal nerve. The axon
runs with those of the other 3 neurones to join the main nerve innervating the
dorsal epidermis.
The ventral receptor is orientated longitudinally and has essentially the
same structure as the longitudinal receptor, consisting of a multipolar neurone
whose dendrites run inside a tube of connective tissue. It differs, however,
in its mode of anchorage. Posteriorly it is attached to the edge of a ventral
oblique muscle; anteriorly it is attached at two points to the ventral epidermis
and also to the edge of another ventral oblique muscle (fig. 6). At each attach-
ment to a ventral oblique muscle, a single muscle-fibre is seen to enter
the strand of connective tissue (figs. 7, B; 10, K). The receptor strand is
236 Osborne—The sensory neurones and sensilla in the
anchored to adjacent muscles, nerves and tracheae by connective-tissue
fibres.
The thorax has also been examined for stretch receptors. In the thorax
stretch receptors are restricted to the meso- and metathorax, but even in these
segments only the longitudinal receptors were found (figs. 1, 2).
A number of multipolar nerve-cells have been found in the lateral region of
FIG. 8. Schematic drawing of the structure of the vertical stretch receptor of the Phormia
larva. The neurones drawn in dotted lines represent those of a cuticular sensillum.
the abdomen which have a type of innervation not previously described (fig. 9).
The most anterior of these neurones (mm) is located in a capsule attached
to the posterior edge of the transverse intersegmental muscle. It is a tripolar
(fig. 11, E). One of its processes runs in a fine nerve which ultimately joins
one of the ventral unpaired nerves; another runs along the edge of the transverse
intersegmental muscle and enters a strand of connective tissue that anchors the
main longitudinal tracheal trunk to the body-wall. The third process, probably
the axon, runs into a nerve-branch supplying the ventro-lateral muscles. This
nerve-branch ultimately joins the main segmental nerve. The next neurone
(mm) is situated in a capsule adjoining the motor-nerve which the third
process from cell mm enters (fig. 11, D, E, G). One dendrite innervates the
pedicel and associated imaginal bud that is attached to a trachea. A second
innervates the epithelium of a trachea (fig. 11, B, C), a third runs into the