Muscle Receptor Organs in the Abdomen of Homarus vulgaris and Palinurus vulgaris

40 Pages·2006·2.55 MB·English

i63
Muscle Receptor Organs in the Abdomen of Homarus
vulgaris and Palinurus vulgaris
By J. S. ALEXANDROWICZ
{From the Laboratory of the Marine Biological Association, Plymouth)
With three plates
SUMMARY
I . In the abdomen and thorax of some groups of Crustacea (Stomatopoda, Deca-
poda Macrura, and Anomura) ganglion cells have been found with ramifications into
special muscle-fibres. It is assumed that these are organs for response to stimuli re-
sulting from muscular activity and therefore the name 'muscle receptor organs' has
been adopted for them. Each muscle receptor unit consists of (a) a thin muscle, (6)
one ganglion cell connected with this muscle by means of numerous dendritic proces-
ses, and (c) various nerves supplying the muscle and entering into connexion with
ganglion cells.
This paper describes the results of a study of these organs in the abdomen of Homarus
vulgaris and Palinurus vulgaris.
2. In each of the six abdominal segments of these animals there are two muscle
receptor units on each side lying close to one another at the level of the superficial
dorsal muscles. Their muscle components are quite distinct from the neighbouring
muscles and preserve their individuality throughout their whole course and at their
attachments. Moreover, the two muscles of the same side exhibit differences in their
length, their attachments, and even their histological structure. Each muscle in about
the middle of its length has a region made up of connective tissue fibres which may
be regarded as an intercalated tendon.
3. Situated near to and in connexion with each of these muscle units is one large
nerve-cell; there are, therefore, four such cells in each segment and a total of twenty-
four in the abdomen. The cells are multipolar in shape with a variable number of short
dendritic processes abundantly ramifying in the intercalated tendinous region of the
muscle. The long processes, the axons, join the dorsal branch of the nerve supplying
the extensor muscles and run in it towards the ganglionic cord.
4. In preparations made from embryonic lobsters it has been possible to establish
that these axons bifurcate after entering the ganglionic cord, and the resulting branches
run in opposite directions. Associating with similar fibres from other segments they
form a tract situated in the nerve-cord near to its median line and running through all
the ganglia of the abdominal and thoracic segments.
5. It has been found that in addition to the ganglion cells, at least three kinds of
nerves take part in the innervation of the muscle receptors. They have been described
under the names of: (a) motor nerves, (b) thick accessory nerve, and (c) thin accessory
nerve.
6. Special means for protecting the muscle receptor organs are present. The nerve-
cells are encapsuled and encircled by several layers of thin membranous tissue. The
muscles are surrounded by connective tissue fibres and a special arrangement of these
fibres supports the muscles in position.
7. As regards the function of these organs, the hypothesis is put forward that they
might come into action during vigorous movements of the abdomen in the escape
[Quarterly Journal of Microscopical Science, Vol. 92, part 2, June 1951.]
164 Alexandrowicz—Muscle Receptor Organs in the
reaction of the animal. If this be so, they may perhaps convey inhibitory impulses to
the elements causing the rapid contractions of the flexor muscles. As these contractions
are governed by the giant fibre system it might be expected that the neurons of the
receptor organs enter into relation with some elements of that system.
CONTENTS
PAGE
INTRODUCTION . . . . . . . . . . . . .164
METHODS . . . . . . . . . . . . .. 165
RESULTS 167
Muscle Elements of the Recepto^ Organs . • • • • • . .167
Topography of the Muscles of the Receptor Organs . . . . . .167
Structure of the Muscles of the Receptor Organs . . . . . . 175
Nerve-cells . . . . . . . • . . . . .180
Nerve-fibres . . . . . . . - - . . • -183
Motor Nerves . . . . . . . . . . . . 183
Thick Accessory Nerve . . . • • • • • • .187
Thin Accessory Nerve . . . • • • • • • .187
Elements of Muscle Receptors in the Embryonic Lobster . . . .. 192
DISCUSSION . . . . . . . . . . . .. 194
REFERENCES . . . . . . . . . . . .. 198
EXPLANATION OF PLATES . . . . . " . . - . . 198
INTRODUCTION
IN the course of investigations made on the innervation of the heart of
Squilla mantis many years ago, I became aware that some muscle-fibres in
the dorsal part of the body of this animal have a peculiar nerve-supply: there
are ganglion cells that ramify in the muscle with numerous short branches.
Later on, during a visit to Naples in 1939, I examined various species of
crustaceans on this point and was able to establish the presence of similar
cells on the dorsal side of the abdominal segments in the stomatopods and all
decapod Macrura and Anomura examined. There were four cells in each
segment, two on each side. It became evident that these cells and the muscle-
bundle with which they are connected constitute an unknown neuro-
muscular organ endowed most probably with some receptor function. More
detailed observations on the structure of these elements were then made in
Squilla mantis and Pagurus striatus, but unfortunately during the war years
all my preparations and notes were lost. It only became possible to return
to these interrupted investigations again in 1949, at the Laboratory of the
Marine Biological Association in Plymouth. I would like to express my most
cordial thanks to the Director of the Laboratory, Mr. F. S. Russell, F.R.S.,
for having given me the opportunity of working there and for the great
interest he has taken in my work.
Owing to the rarity of stomatopods off Plymouth the investigations have
been continued with Homarus vulgaris, which is available in, sufficient
numbers. Some data have also been obtained from Palinurus vulgafis. In both
Abdomen of Homarus vulgaris and Palinurus vulgaris 165
species the organs in question could be found in the six abdominal segments
and, moreover, in certain thoracic muscles. The present paper is concerned
with observations on the abdominal segments only. Those relating to the
thoracic muscles will be dealt with in a further contribution.
METHODS
The results described below were obtained by means of methylene blue
staining. In both the lobster and the rock-lobster the nerves in the organs
under examination stain on the whole very satisfactorily, so that no prepara-
tion is ever a complete failure, though, of course, all are not of equal value.
The staining was achieved either by immersing the tissues in the methylene
blue solution (10-15 drops of 0-5 per cent, solution in distilled water to 100 c.c.
of sea-water), or by injection of the dye into the living animal (1 volume of
methylene blue, 0-5 per cent, aq., with 2-5 volumes of sodium chloride,
1-5 per cent, aq.), or by combining the two processes, i.e. staining the tissue in
the solution as above, after the animal had been previously injected. Dissection
of the specimens was performed 1-4 hours after injection. The last method
was often used in order to correct the staining when it was unsatisfactory
after injection.
Fixation. The preparations were fixed with solutions of ammonium molybd-
ate. The following formulae were used:
1. Ammonium molybdate, 8 per cent. . . .. go c.c.
Platinum chloride, i per cent. . . . .. 3 c.c.
Osmium tetroxide, 2 per cent. . . . .. 3 drops
2. In one of my previous papers in which this formula was recommended
(Alexandrowicz, 1932), the addition of cane sugar (saccharose) to the ammon-
ium molybdate solution was suggested, so as to make it isotonic for marine
invertebrates. In the present series of experiments it was found that the shape
of the ganglion cells in the receptor organs was preserved better when the
quantity of saccharose amounted to about half that needed to make the solu-
tion isotonic:
Ammonium molybdate 10 per cent. . . .. 100 c.c.
Saccharose . . . . . . .. 17 gm.
To this platinum chloride and osmium tetroxide may also be added.
3. The mixture with glycerine and hydrochloric acid, as recommended
by E. C. Cole (1934), was also tried and it was found that for my purpose it
was advisable to make the mixture with less glycerine and acid. This modified
formula was as follows:
Ammonium molybdate . . . . . . 12 gm.
Glycerine . . . . . . .. 25 c.c.
Dist. water . . . . . . .. 75 c.c.
HC1, sp. gr. 1-124 . . . . . .. 15 drops
The solution of ammonium molybdate to which saccharose or glycerine
has been added becomes blue when exposed to light. It was noticed in the
i()(» Alexandrowicz—Muscle Receptor Organs in the
earlier experiments that this colour disappeared when the bottle was put in a
shaded place, and also after addition of platinum chloride and osmium
tetroxide. In the course of the recent work it was found that a similar solution,
probably owing to some different properties of the sample of ammonium
molybdate used, became very dark blue and that it did not even turn colour-
less if kept in brown bottles. What is worse, the tissues of the preparations
may retain a greyish-blue coloration.
With each of the above formulae satisfactory fixation may be obtained.
The preparations were left in the fixing fluid for 6-18 hours, washed out for
about the same time in distilled water, then dehydrated in absolute alcohol,
transferred to xylene and mounted in xylene dammar.
Although the staining and fixing of these organs proved comparatively
easy, there were difficulties that had to be overcome. Chief among these was
to ensure the access of the dye to the nervous elements during staining.
Methylene blue has a low penetrating capacity so that a small fold or some
overlapping parts of the tissue may hinder the staining of the nerves. It is
therefore very important to get the nerves exposed on the surface of well-
stretched preparations. To do this I use the method already recommended
(Alexandrowicz, 1932); i.e. the portion removed from the animal is pinned to
paraffin-wax plates with hedgehog spines. When the preparations have been
thus fixed in a fully stretched state, all manipulations on them are much
easier. In my investigation it was necessary to remove as much of the surface
connective tissue and blood-vessels as possible. This is a very delicate opera-
tion and needs to be done when, after some minutes, the staining has advanced
so far that the different tissues are becoming differentiated. Sometimes pieces
of muscle have to be pushed aside and fixed to the plate or even removed.
Unfortunately, operations in which the muscles are squashed or cut often
have an unfavourable influence on the staining of the adjoining nerves. The
preparations are left attached to the paraffin plates during staining and fixa-
tion ; it is also better to keep them for some time on these plates while washing
in water, since after treatment with ammonium molybdate some tissues have
a tendency to shrink and others to swell. After detaching them it is advisable
to remove all superfluous parts. The muscle layer can be thinned by removal
with scissors from the underside. Before transferring into alcohol the prepara-
tions should be put on the slide and as much water as possible sucked away
with blotting-paper. If some regions are still too thick, they can be reduced
further when in alcohol or xylene by scraping or by cutting out parts of them.
In all these manipulations the muscle receptor organs, as a rule, remained in
connexion with the neighbouring dorsal muscles and with the soft chitinous
parts to which they were attached. It is, however, possible to isolate them.
This can be done before staining, but the final results are much better if it is
done when the preparations are in water after fixation or even when they have
been transferred to xylene.
It is not particularly difficult, when the preparations are in water, to cut out
the receptor organs, viz. the muscle-bundles with their nerve elements, the
Abdomen of Homarus vulgaris and Palinurus vulgaris 167
latter in connexion with the main dorsal nerve-trunk. The whole should be
put on the cover-glass, stretched properly, passed into alcohol, &c. When the
separation has to be made after the pieces have been brought into xylene, the
isolation of the required parts can be done by teasing off small pieces of
the adjoining muscles. Caution is needed as the muscles and nerves are brittle
and there is always some risk of damaging the preparations at the important
spot, but after some practice not many of them become lost in that way.
These processes for reducing the thickness of the preparations or separating
some parts of them are applicable also to those which have been mounted for
a long time: after keeping them some hours in xylene the cover-glass can be
removed, the desired improvements effected, and the preparations mounted
again.
Some hints on dissecting the animal in order to expose the muscle receptor
organs are given later (p. 174) as they can be better understood after a detailed
account of the situation of these organs has been given.
RESULTS
The symbol MRO will be used in this paper as an abbreviation for muscle
receptor organ.
In Homarus (Text-fig. 1) MRO appears on the dorsal surface of each of the
six abdominal segments as a very thin muscle-bundle, approximately equal in
length to the superficial dorsal muscles and situated at the level of these
muscles. Two largish ganglion cells lying quite near to this muscle-bundle
send short branches to it while their axons, starting from the opposite poles,
join the nerve-trunk running transversely on the superficial dorsal muscles
and supplying these muscles; the same trunk carries also several nerve-fibres
destined for the MRO. We have therefore to consider three components of
this organ, viz. (a) muscle elements, (b) nerve-cells, and (c) nerve-fibres.
Muscle Elements of the Receptor Organs
Topography of the Muscle Receptor Organs
The situation of the muscle components of MRO can be best understood in
relation to the superficial dorsal muscles. The latter were described in
Homarus by Milne Edwards (1834) and mentioned by W. Schmidt (1915),
who, in his monograph of the muscle system of the common crayfish, gives
some particulars regarding the lobster. Daniel (1930) investigated the muscle
system of various crustaceans and among them that of the lobster, but from
his diagrammatic figures one can hardly get an idea of what these muscles look
like when seen from the dorsal side. The only illustration representing them
which could be found was that of Milne Edwards, but it is not quite exact.
Some remarks about the general topography of this region may therefore not
be superfluous.
168 Akxandrowicz—Muscle Receptor Organs in the
In Homarus vulgaris, to which the following description refers, the super-
ficial dorsal muscles form in the 2nd to 5th abdominal segments two distinct
portions; both originate at the forward edge of one segment and run forward
as thin band-like muscle units; they have their attachments to the integument
TEXT-FIG, I. Homarus vulgaris. A. Muscle receptor organs in the 2nd abdominal segment
(left side). The receptor organs have been a little displaced in dissection from the edge of the
lateral superficial dorsal muscle for the sake of clarity .A certain amount of connective tissue
has been left surrounding the organs, B. Muscle receptor organs in the ist abdominal segment
(right side).
of the next segment not far from its anterior edge. As is shown in Text-fig. 2A
(representing the 2nd segment with the adjoining parts of the ist and the
3rd), the fibres of the median portion run parallel to the longitudinal axis
while those of the lateral portion take an oblique course. In the resulting gap
parts of the deeper thicker layer of the dorsal muscles lying immediately
beneath the superficial ones become exposed to view. These deeper muscles
also come into view between the median borders of the superficial ones. There
are also in this region tiny muscle units attached to the interarticular mem-
brane (Text-fig. 2A).
Abdomen of Homanis vulgaris and Palinurus vulgaris 169
f^^-STz
••:- \ -»•
D
TEXT FIG. 2. Homanis vulgaris. Diagrams showing the situation of the muscle receptor
organs in the 2nd abdominal segment from (A) the dorsal and (B) the ventral side. c. Sections
through the same segment in the plane of the receptor organs; the muscle-fibres are diagram-
matically represented as if they were lying with their insertions in the same plane. In Fig. c the
abdomen is in a bent position, in D it is straightened. •
170 Alexandrowicz—Muscle Receptor Organs in the
The general arrangement of the muscles is the same in the segments 2-5.
There are only certain differences in the anterior attachments of the lateral
portion, which in each succeeding segment is situated a little farther back
than in the one next in front of it. Consequently the oblique portion becomes
gradually shorter. In the 4th and especially the 5th segment the gap between
the two portions appears comparatively large.
In the 1st segment the median portion takes an oblique course, too, and
thus the fibres of the whole superficial muscle run approximately parallel with
each other. The gap between them is closed and the two portions may appear
as one muscle, although by more careful examination they can be distinguished
as two units.
In the 6th segment the superficial dorsal muscles are not divided into two
portions and are greatly reduced both in width and length. They begin at the
forward edge of the telson and run for a short distance, occupying only about
one-third of the length of the segment.
The situation of the muscle-bundle of MRO may be roughly defined as
being between the two portions of the superficial muscles but more or less
close to the lateral portion. On microscopic examination it may be seen that
this thin muscle-bundle actually consists of two muscle units of about 150/A in
diameter; though closely associated in the middle part of their course, they
preserve their individuality throughout. They are, moreover, not of the same
length and they have different points of attachment, and they also show a
difference in their histological structure. For the convenience of the descrip-
tion that muscle which has the more superficial attachments will be called
RM 1 and the other RM 2. The following description refers to the 2nd seg-
ment which is represented in Text-fig. 2.
The muscle RM 1, the shorter of the two, has its posterior insertion at the
point where the fibres of the two superficial dorsal muscles meet at an acute
angle and it may therefore be most easily recognized at this spot. In its forward
course it runs at first along the edge of the lateral superficial muscle but soon
departs from it and comes to lie in the triangular space between the two por-
tions of the superficial muscles and on the bundles of the deeper dorsal
muscles. Bending slightly inwards and dorsalwards it usually divides into a
few bundles of fibrils which are attached to the integument at the point
between the two superficial muscles and a good deal behind their anterior
insertions.
To understand the course of the muscle RM 2 Text-fig. 2A should be
compared with 2B, in which the same segments are depicted as seen from the
ventral side with all the muscles removed except the superficial ones, so that
the whole muscle RM 2 is exposed to view; in Text-fig. 2A those parts of
RM 2 that are hidden from view are drawn in dotted lines.
The anterior attachment of RM 2 lies a little to the side of and much in
front of that of RM i, approximately at the level of the insertion of the
median bundles of the lateral superficial muscle. In its backward course RM 2
passes beneath RM 1 and runs alongside it in such a position that a good deal
Abdomen of Homarus vulgaris and Palinurns vulgaris 171
of RM 2 or even the whole of it may be seen on the median side of RM 1.
Held together by connective tissue the fibres run for a distance in close
association, but they separate again as RM 2 passes underneath the lateral
superficial muscle, crosses its fibres obliquely near to their insertion (Text-figs.
1 A, 2B) and runs so far backwards that its attachment takes place in the vicinity
of the superficial muscles (median portion) of the next following segment.
It ought to be noted, as this feature may have some importance for the
function of these muscles, that RM 2 looks in the preparations as if it were
more loose, so that even in its middle part the fibres of RM 2 may be often
distinguished from those of RM 1 by their undulating course.
The length of RM 2 in the 2nd and also in the 3rd segment is not much less
than twice that of RM 1. In the preparation which served as a basis for the
drawing of Text-fig. 2 the respective lengths were 19 and 10 mm. As to their
calibre, RM 2 appears a little stouter in that region where both muscles run
together. Moreover, each appears as if it were not. of uniform thickness
throughout its whole length, RM 1 looking thinner anteriorly and RM 2
thinner posteriorly. However, the evaluations of their calibre as seen during
dissection are not exact, as variations are also caused by deformations of the
cylindrical fibres, which are flattened in various directions by the neighbour-
ing organs.
As the muscle RM 1 approaches its anterior attachment it frequently
splits into several tiny bundles of fibrils which spread out fanwise. The
posterior end of this muscle and both ends of RM 2 only show an enlargement
due to a slight divergence of the fibrils.
The course of the muscles RM drawn to greater magnification is shown in
Text-fig. 3A. We see that they must cross each other twice, since in the middle
part RM 2 always lies nearer the median line than RM 1. It is to be emphasized
that at both crossings RM 2 always passes ventrally to RM 1.
In front of and behind the crossing RM 2 runs at a deeper level. These
points are made clear in the diagrammatic figures 2c and D; these represent
a dorso-ventral section of the same segments as 2A, made in the plane of
the muscles RM of the 2nd segment. In Text-fig. 2c the abdomen is supposed
to be in almost maximal flexion and consequently the muscles are stretched;
their longitudinal dimensions correspond in this state to those represented in
A. and B, which were drawn from preparations that had been stretched and
flattened, with, therefore, the muscles fixed in the stretched position. In the
living animal, when the abdomen becomes straightened, the points of attach-
ment of the muscles RM assume the position shown in 2D. Where they are
linked together in their middle parts, they do not deviate from a straight
course. Elsewhere they are bent; this applies especially to the posterior part
of RM 2, which has to turn round the edge of the following segment and,
moreover, is separated at this place from RM 1 by the thickness of the lateral
superficial muscle (not represented in this figure).
In Text-fig. 2c and D allowance must be made for the fact that the inser-
tions of both muscles are shown in the same plane, although this does not
172 Alexandrowicz—Muscle Receptor Organs in the
A W B
D
TEXT-FIG. 3. Homarus vulgaris. A. Muscle elements RM 1 and RM 2 of the receptor organs
in the. 2nd abdominal segment. B. Same of the 5th segment. C. One of the types of the inser-
tions of the muscle-fibres in the 5th segment. D. Diagram of the dorsal view of the abdomen
showing the positions of the receptor organs and of the superficial dorsal muscles by trans-
parency.