AMFR. ZOOLCM.IST, r>:-)03-H0 (1965).
SOME ASPECTS OF THE STRUCTURE OF THE NERVOUS
SYSTEM IN THE ANEMONE CALLIACTIS
ELAINE A. ROBSON
Dept. of Zoology, University of Cambridge, England
SYNOPSIS. In the light of existing work on tbe behavioral physiology of this anemone,
the structure of parts of the neuroimiscular system has been examined in detail. In
the sphincter region, the morphological basis for rapid through-conduction and motor
innervation is a network of bipolar nerve cells, which is connected to the similar
retractor nerve-nets of mesenteries. Sphincter muscle fibers are arranged at the periphery of tubes, which form a meshwork within the mesogloea. Bipolar nerve cells
appear to run in these tubes. Neurites also reach the sphincter from the endodermal
nerve-net by penetrating the mesogloea directly. The nerve-net over the circular
muscle is richer than in other parts of the column, but shows similar features. It
includes small multipolar cells of unknown function.
Coordination between different parts of the anemone is discussed in terms of possible
pathways for the transmission of excitation. For example, bundles of retractor and
parietobasilar muscle fibers continue from both surfaces of mesenteries into the mesogloea of the pedal disk, suggesting a possible route for neurites passing to or from
the ectoderm. If confirmed, the existence of this route could throw light on a number
of sequences of behavior.
Although much is already known about
the behavioral physiology of Calliactis parasilica, the anatomical pathways responsible
for coordination of activity in this anemone
have not yet been examined in detail. Some
relevant features of the sphincter and pedal
disk, regions essential to many common
sequences of behavior, will be described.
faces. Morphological connections with
muscle fibers, and also with the processes
of sense cells, are readily observed. Similar
observations have been made on Calliactis
(Robson, 1961b) and on Mimetridium cryptum (Batham, 1965). The innervation of
the sphincter muscle, however, has not yet
been examined in any species and will be
discussed.
When adequate mechanical stimuli are
ANALYSIS OF BEHAVIOR
applied to the column or to the crown,
The anemone (Fig. 1) withdraws from the anemone withdraws symmetrically. But
a mechanical stimulus. The reflex is me- local stimuli can also produce local rediated by through-conducting pathways in sponses. Contractions of tentacles or of
the nervous system, which possess the prop- muscles affecting the rim of the oral disc
erties of ordinary nerve (Pantin, 1935a, b,
c, d). These paths conduct especially rapidly, and innervate the sphincter and retractor muscles. Whereas most anemone
muscles contract slowly, these two sets of
muscles can give rapid facilitated contractions as well, a feature which depends on
motor innervation in a manner not yet
understood. The afferent side of the reHex
has also been examined (Passano and
Pantin, 1955).
Histological work on mesenteries of Metridiitrn senile (Pantin, 1952; Batham, Pantin, and Robson, 1960) shows that the rapid
paths supplying the retractor and sphinc- FIG. 1. Calliactis parasitica (Couch), Mediterranean
ter muscles correspond to a well-developed specimens with n a b Dardanus arrosor. (After
synaptic nerve-net over the retractor sur- Krunelli. 1913.;
(403)
404
ELAINE A. ROBSON
SPHINCTER
RETRACTOR
A
O5 CM
CALLIACTIS PARASITICA
B
FIG. 2. General structure of Calliactis. A. Vertically divided anemone. B. Transverse section at
mid-column level.
may spread round the circumference with
apparent decrement due, as Pantin (1935b)
suggested, to interneural facilitation. There
is, however, through-conduction in a radial
direction. The crown is a very interesting
region, but the most complete study of its
nervous anatomy in Calliactis is still that
of the Hertwigs (1879). In this anemone
it is the only region where ectodermal as
well as endodermal muscle is developed,
and as yet it is not known how the contractions of the two layers are coordinated,
as they evidently are in feeding and other
activities.
The slow circular and parietal muscles
of the column can produce both local responses and changes in shape of the whole
animal (Needier and Ross, 1958; and see
Batham and Pantin, 1950, 1954). Speed of
conduction in the nerve-net of the column
is only about one-tenth of that in the mesenteries, and the number of nerve cells is
correspondingly small (Pantin 1935b;
Batham, Pantin, and Robson, 1960). But
the coordination of column movements is
not a simple matter. Batham and Pantin
(1954) suggested for Metridium that peristalsis in the circular muscle might be conducted in the muscle-field itself, and also
that circular and parietal muscles showed
reciprocal inhibition. Both suggestions are
valid for Calliactis. The studies of Needier
and Ross (1958) and of Ewer (1960) show
that in whole Calliactis or in rings prepared
from the column, activity spreads from the
subsphincter or pedal zones rather than
from the mid-column. The same appears
to be true for Metridium (Batham and
Pantin, 1954), but in neither case are the
morphological pathways for excitation or
for inhibition of column muscles accurately known.
All parts of the anemone may be involved
in long sequences of slow beha-vior, such as
that by which Calliactis characteristically
transfers to a new shell. Analysis of this
behavior (Ross, 1960; Ross and Stitton,
1961 a,b) draws attention to striking coordination of reciprocal activity in the
crown and pedal disk, and to the movements of the pedal disk as it detaches, reattaches, and performs creeping movements.
All of this is still problematical in terms of
possible activity in the nervous system, and
even the sequence in which different pedal
muscles contract is not well known in any
anemone. The anatomy of the pedal region
will be mentioned briefly.
THE SPHINCTER REGION
Figure 2 shows the general structure of
Calliactis and the position of the retractor
and sphincter muscles. It will be recalled
that these muscles produce rapid withdrawal, and are excited hy rhrongh-rondurtion tracts in the nervous system. As in
Metridium, the retractor face of a mesentery
shows a rich network of bipolar nerve cells
(Robson, 1961b). This tract must transmit
excitation not only to the retractor muscle
fibers, but also to and from the sphincter
NKRVOI'S SYSTEM OF
CALLIACTIS BPLSASITICA
FIG. 3. The through-conduction tract between a
mesentery and the sphincter is shown as broken
line.
region. As the two sets of muscles are supplied by the same through-conduction system (Pantin 1935a), the retractor nerve-net
may be expected to connect with a histologically similar nerve-net in the sphincter
legion. This now appears to be the case.
A mesenteric through-conduction route to
the sphincter is depicted (Fig. 3) in order
to clarify the description which follows.
The nerve-net represented by the broken
line in fact extends across most of the
mesentery, and also connects with the processes of a large population of sense cells
situated in the angles between septum and
column.
The sphincter of Calliactis is quite a
large muscle, occupying a zone at the top
of the column, perhaps 1 cm deep in an
anemone with a column 3 cm in diameter.
Muscle fibers are arranged in groups within
the mesogloea (Fig. 4). These groups are
hollow tubes, the muscle fibers being disposed at the periphery of cylindrical
bundles. As in other anemone muscles,
each fiber is therefore attached to the mesogloea along one surface only, and is not
completely surrounded by connective tissue
(Pantin, 1960). Most of the fibers have no
connection with the epithelium, and their
nuclei are to be seen within the tubes. The
organization of the sphincter can be understood in tenns of a musculo-epithelium
which has sunk into the mesogloea (Hertwig and Hertwig, 1879): but in fact, the
morphogenetic process by which the meshwork of muscle tubes develops and grows
has never been examined.
Callinrlis
405
Pending a study of its development, the
sphincter muscle of Calliactis may be regarded as a derivative of the circular muscle
of the column. Endodermal circular muscle
(a true musculo-epithelium) lines the column, pedal disk, oral disk, and tentacles.
Although hollow tubes resembling those of
the sphincter are formed when circular
fibers pass into the mesogloea beneath the
insertions of mesenteries (Robson, 1957),
sections suggest that the circular muscle
adjacent to the sphincter remains quite
distinct from it. Figure 4 shows that in
average-sized Calliactis the sphincter and
circular muscles are separated by mesogloea
at least 100 ^ thick. It is possible that a
few muscle strands may connect the two
systems, but it would not be surprising
if they functioned independently.
The nervous system of this part of the
column has been studied in whole mounts
fixed after staining with methylene blue
(Robson, 1961b). From the examination of
a large number of preparations, it is clear
that a nerve-net of the type associated with
through-conduction tracts in the mesenteries is also found in the sphincter region.
In this zone there are abundant bipolar
nerve cells running over the circular muscle
at the surface, of the same order of size
as those in the mesenteric nerve-net. As in
other parts of the column of Metridium or
Calliactis, the processes of bipolar nerve
cells also pass from mesenteries onto the
circular muscle, and there is similarly some
tendency to follow the direction of circular
muscle fibers or the angles of mesenteries.
The sphincter zone, however, is noticeably
richer in bipolar cells than are other parts
of the column.
The sphincter muscle, which is of course
separated from the circular muscle by mesogloea (Fig. 4C), has similar bipolar nerve
cells of its own which probably run within
the muscle tubes. It is supplied as well by
the processes of bipolar cells situated at
the surface. Processes originating from the
nerve-net above the circular muscle or from
the retractor nerve-net of a mesentery appear to pass directly through the mesogloea
to the sphincter muscle beneath. The neurites may penetrate a depth of 100 p. even
406
ELAINE A. ROBSON
circular
muscle
r
P
i.
If.
sphincter
muscle
FIG. 4. Vertical section of the sphincter region.
A. Drawing to show position of sphincter. Mesogloea is black. B, C. Photographs from a different
preparation at levels indicated on A. ect, ecto-
derm; end, endoderin; tmt, longitudinal muscle of
tentacle. Arrow indicates thin mesogloea between
this muscle and the top of the sphincter (see text).
in stretched preparations, and thus probably reach most parts of the sphincter.
Some pursue an erratic- course of rightangled bends, as if they passed from one
muscle bundle to another. Although nerve
terminations on actual muscle fibers have
not yet been seen, it seems probable that
nerve cells which appear to end in the
sphincter do so.
The superficial appearance of these preparations is depicted in the upper part of
Figure 5 (5A); in the diagram the innervation of the deeper-lying sphincter muscle
is only suggested. As some of the nerve-net
supplying the sphincter runs over the circular muscle, the presumably different roles
of the two muscles in this region would be
worth further study._ For the, moment^
physiological evidence that the same
through-conduction system supplies both
sphincter and retractor muscles is confirmed. The density of nerve-cells in the
sphincter zone appears adequate to account
for a conduction speed of 100 cm/sec (Pan-
tin, 1935b; Batharn, Pantin, and Robson,
1960), and there is some tendency for nerve
processes to run parallel to the muscle
fibers.
In some methylene blue preparations
where bipolar nerve cells have failed to
stain, a population of small multipolar
nerve cells may nevertheless appear quite
clearly. This system is shown in the lower
part of Figure 5 (5B). The cells are from
10 to 15 f». in diameter and have from three
tofivefineprocesses usually exceeding 500 p.
in length. These cells have already been
seen in the column (Robson, 1961b), and
are situated above the circular muscle.
Their processes connect with those of bipolar nerve cells and of sense cells, but
Temain superfietirt~fiKl"«lo Tiol "pen€BfSIe 16
the sphincter muscle. They are uniformly
distributed in the sphincter region and
there may be 50 to 100 per mm2 in fixed
preparations. They are not strictly comparable to the much larger multipolar
XERVOIS SYSTKM OF
A.
Calliaclis
407
bipolar nerve cells
FIG. 5. Histological appearance of nerve-net in whole mounts of sphincter region stained with
methylene blue (see text). Photographs A and B are at different magnifications.
nerve cells in the column of the anemone
Stomphia coccinea which probably act as
a pacemaker system during swimming (Robson, 1963). It is too early to say whether
multipolar cells in Calliactis may be concerned with autonomous activity or not.
In some methylene blue preparations
both bipolar and multipolar nerve cells
stain, and the histological appearance of
the sphincter region could then be represented by superimposing the upper over
the lower diagram in Figure 5.
PATHWAYS THROUGH MESOGLOEA
In the Anthozoa, nerve processes usually
run above a muscle field and do not pass
into the mesogloea. The direct passage of
neurites to the sphincter which has been
described is an exception whose interpretation will be clearer once it is known how
this muscle develops. The occasions on
which primarily subepithelial nerve processes penetrate mesogloea are interesting
and functionally significant (Pantin, 1960,
1965). It has been mentioned that an outstanding problem in the interpretation of
behavior in anemones is how the activities
of different muscles are coordinated. It is
possible that when different muscles are
adjacent to the extent of being separated
by very little or no mesogloea, connections
may develop between their respective nervenets. In Mimetridiurn there are connections between the ectodermal nerve-net of
the oral disk and the retractor nerve-net
of the mesenteries (Batham, 1965). Similar pathways through the disk in Calliactis,
if present, might similarly account for
communication between the sphincterretractor system and the crown. It may
possibly be relevant here that the uppermost part of the sphincter muscle in Calliactis (Fig. 4B) is separated from the ectodermal longitudinal muscle of tentacles by
a particularly thin lamina of mesogloea,
and it would not be altogether surprising
if neurites were found to cross through at
this point. As yet, however, there is no
evidence for or against this suggestion.
408
ELAINE A. ROBSON
A
mesentery
parietobasilar m.
basilarm.
r
circular m.
mesogloea
of pedal disk
ectodermal
epithelium
FIG. 8. Structure of pedal dUk in vertical sections, disk. Approximate position of photographs ii indiA. Drawing to allow orientation. B, C. Muade fibers cated by arrow in A. r, retractor musde fibers,
from mesenteries penetrating mesogloea of pedal
NF.RVOI'S SYSTEM OF
THE PEDAL DISK
Another possible route by which ectoderm
and endoderm might be connected has been
found in the pedal disk. In Calliactis this is
of particular interest in view of the potentially complex behavior of the pedal disk in
relation to external stimuli (Ross and Sutton, 1961a). In the endoderm there are
circular and basilar muscles, the latter
placed radially at the angles of each mesentery with the pedal disk. The muscles of
the mesenteries are exactly as in Melridium
(Batham and Pantin, 1951, Fig. 8): endocoelic retractors and exocoelic parietobasilars fan out towards their insertion at the
base. Vertical sections (Fig. 6) show that
the fibers of both these muscles continue
downwards into the mesogloea of the pedal
disk as tubular bundles on each side of the
mesentery. The muscle fibers peter out but
a few seem to extend almost if not quite
to the pedal ectoderm. This feature would
seem to offer ready-made pathways for the
neurites of nerve cells or sense cells to pass
between the ectoderm and any of the endoclermal muscles. It must be emphasized
that whether or not neurites follow this
route through the mesogloea has not yet
been ascertained: the possibility is of current interest. Cinclides, present in Calliactis, offer another possible but less relevant connection between ectoderm and
endoderm. The penetration of pedal disk
mesogloea by muscle tubes is similar in
Slomphia which has no cinclides (Robson,
1961a).
CONCLUSION
Conclusions from this study are brief and
are largely summarized in Figure 3. It may
yet prove possible to trace morphologically
as well as physiologically the means by
which the behavior of this anemone is coordinated, a far from simple matter when
one considers how reciprocal activities of
the crown, foot, and column are integrated
in relation to the environment.
ACKNOWLEDGMENTS
I wish to thank the Director and Staff of
CrilHactis
400
the Marine Laboratory, Plymouth, where
some of this work was carried out, and
particularly Mr. A. C. G. Best and Miss J.
Kibble for most of the sections illustrated.
REFERENCES
Batham, E. J. 1965. The neural architecture of the
sea anemone Mimetridium cryptum. Am. Zoologist 5:395-402.
Balham, E. J., and C. F. A. Pantin. 1950. Muscular
and h)drostatic action in the sea-anemone, Metridium senile (L.). J. Exptl. Biol. 27:264-289.
Batham, E. J., and C. F. A. Pantin. 1951. The organization of the muscular system of Metridium
senile (L.). Quart. J. Microscop. Sci. 92:27-54.
Batham, E. J., and C. F. A. Pantin. 1954. Slow contraction and its relation to spontaneous activity
in the sea-anemone Metridium senile (L.). J.
Exptl. Biol. 31:84-103.
Batham, E. J., C. F. A. Pantin, and E. A. Robson.
1960. The nerve-net o£ the sea anemone Metridium senile (L.): the mesenteries and column.
Quart. J. Microscop. Sci. 101:487-510.
Brunelli, G. 1913. Ricerche etologiche. Osservazioni ed esperienze sulla simbiosi dei Paguridi e
delle attinie. Zool. Jahrb. Abt. Allgem. Zool.
Physiol. Tiere 34:1-26.
Ewer, D. W. 1960. Inhibition and rhythmic activity of the circular muscles of Calliactis parasitica (Couch). J. Exptl. Biol. 37:812-831.
Hertwig, O., and R. Hertwig. 1879. Studien zur
Blattertheories. Heft. 1. Die Actinien, Gustav
Fischer, Jena.
Needier, M., and D. M. Ross. 1958. Neuromuscular
activity in sea anemone Calliactis parasitica
(Couch). J. Mar. Biol. Assoc. U. K. 37:789-805.
Pantin, C. F. A. 1935a. The nene-net of the Actinozoa. I. Facilitation. J. Exptl. Biol. 12:119138.
Pantin, C. F. A. 1935b The nerve-net of the Actinozoa. II. Plan of the nerve net. J. Exptl. Biol.
12:139-155.
Pantin, C. F. A. 1935c. The nerve-net of the Actinozoa. III. Polarity and after-dischaige. J.
Exptl. Biol. 12:156-164.
Pantin, C. F. A. 1935d. The nerve-net of the
Actinozoa. IV. Facilitation and the "staircase."
J. Exptl. Biol. 12:389-396.
Pantin, C. F. A. 1952. The elementary nervous
system. Proc. Roy. Soc. (London), B, 140:147-168.
Pantin, C. F. A. 1960. Diploblastic animals. Proc.
Linnean Soc. London 171:1-14.
Pantin, C. F. A. 1965. The capabilities of the coelenterate behaviour machine. Am. Zoologist 5:
581-589.
Passano, L. M., and C. F. A. Pantin. 1955. Mechanical stimulation in the sea-anemone Calliactis
parasitica. Proc. Roy. Soc. (London), B, 143:
226-238.
ELAINE A. ROBSON
Robson, E. A. 1957. Structure and hydromechanics Ross, D. M. I960. The association between the
of the lnusculo-ephhelhim in Metridium. Quart.
hermit crab Eupagurus bernhardus (L.) and the
J. Microscop. Sci. 98:265-278.
sea anemone Calliaclis parasitica (Couch). Proc.
Robson, E. A. 196)a. Some observations on the
Zool. Soc. (London), B, 134:43-57.
swimming behaviour of the anemone Stomphiu Ross, D. M., and L. Sutton. 1961a. The response of
coccinea. J. Exptl. Biol. 38:343-363.
the sea anemone Calliaclis parasitica to shells of
Robson, E. A. 1961b. A comparison of the nervous
the hermit crab Pagtmis bernhardus. Proc. Roy.
systems of two sea-anemones, Calliactis parasilica
Soc. (London), B, 155:266-281.
and Metridium senile. Quart. J. Microscop. Sci. Ross, D. M., and L. Sutton. 1961b. The association
102:319-326.
between the hermit crab Dardanus arrosor
Robson, E. A. 1963. The nerve-net of a swimming
(Herbst) and the sea anemone Calliaclis parasitica
anemone, Stomphia coccinea. Quart. J. Microscop.
(Couch). Proc. Roy. Soc. (London), B, 155:282Sci. 104:535-549.
291.
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