535
The nerve-net of a swimming anemone, Stomphia
coccinea
By ELAINE A. ROBSON
(From the Department of Zoology, Downing St., Cambridge)
With one plate (fig. 2)
Summary
The nervous system of this anemone has been examined in an attempt to study the
pacemaker system, previously thought to be localized in the median zone of the
column. No clear-cut nerve-ring has been found. The whole column, however, is
characterized by the presence of large multipolar nerve-cells in the endoderm, to
which pacemaker activity is provisionally attributed. There are several thousand of
these cells and their neurites connect with those of other nerve-cells and sense-cells
in the column, and with the mesenteric nerve-nets. The column nerve-net, of which
the multipolars form part, conducts slowly and fatigues easily. Present physiological
evidence from Stomphia and other coelenterates does not invalidate the suggestion
that the multipolar cells may also function as a pacemaker system.
Other features of the nervous and sensory systems are very like those of other
anemones (e.g. Calliactis, Metridium). The column, mesenteries, and oral and pedal
disks are briefly described; much information is still lacking. As expected, sense-cells
are aggregated along the angles of the mesenteries except in the pharynx. Their
neurites connect with the column nerve-net, and with the mesenteric nerve-nets.
A well-developed network of bipolar nerve-cells on the retractor surface may be
regarded as a rapid through-conduction tract. As in Metridium and Calliactis the
radial nerve-net on the opposite face of the mesentery is similar but much sparser.
The ectodermal surface of the oral disk, as described by the Hertwigs, shows a crisscross network of bipolar nerve-cells together with radial rows of small multipolar
nerve-cells above the septa. These might perhaps have a proprioceptive function.
In the endoderm of the pedal disk, sense-cells are numerous but nerve-cells few.
These features are discussed only in so far as they may be related to the swimming
behaviour of Stomphia.
Introduction
T H E swimming behaviour of this sea-anemone has already been described
several times (Yentsch and Pierce, 1955; Sund, 1958; Wilson, 1959; Hoyle,
i960; Robson, 1961 a, b). Stomphia coccinea Miiller swims on contact with
the predatory nudibranch Aeolidia papillosa L., or with the starfish
Dermasterias imbricata Grube, Hippasteria phrygiana Parelius, H. spinosa
Verrill. It has been shown that aqueous extracts of the first two of these animals
have the same effect (Ward, 1958, 1962; Robson, 19616). Swimming can
also be produced by electrical stimulation (Yentsch and Pierce; Sund). Once
detached from its substrate the anemone expands markedly and shows
a series of abrupt bending movements, which may be interpreted as
contractions of parieto-basilar muscles in the mesenteries. The irregular
sequence of contractions continues with declining frequency for several
minutes, and after a resting phase the anemone re-attaches itself.
[Quart. J. micr. Sci., Vol. 104, pt. 4, pp. 535-49, 1963.]
536
Robson—Nerve-net of swimming anemone
Rapid rhythmical activity is unusual in sea-anemones. In this case, although
contractions tend to occur at alternating radii, their sites are not constant and
a sequence may rotate slowly round the column (Robson, 1961a). As pieces
of vertically divided anemones show all the features of swimming behaviour,
the neuromuscular elements involved must be radially equivalent. It seems
likely that a pacemaker system is situated in the column. Since cutting
experiments show that swimming contractions continue only where the
median zone of the column remains intact, it was suggested that the pacemaker
might be restricted to this region (Robson, 19616). The present study began
as an attempt to detect specialization in the structure of the nerve-net which
might be correlated with pacemaker activity.
Although the histology of parts of the nervous system has been examined
with this possibility in mind, no evidence for a specialized equatorial zone
in the nerve-net of the column has been found. The column is characterized
as a whole, however, by the presence of relatively large multipolar nerve-cells
not seen elsewhere in the anemone. The results reported here are considered
in relation to features of nervous organization in other coelenterates.
Methods
Most of the work was done at the Marinbiologisk Laboratorium, Helsingor.
Anemones were obtained by dredging at Knahaken in the Danish Sound
(Bratstromm, 1941) and were kept under circulation or in bowls at temperatures between io° and 13° C. Methylene blue was used as a vital stain for the
nervous system: the following procedure proved suitable even for small
specimens 1 cm or less in diameter.
Anemones were stimulated electrically, and as soon as they began to swim
they were transferred to an anaesthetizing medium consisting of equal
volumes of sea-water and 7-^% MgCl 2 .6H 2 O. After 15 to 20 min, depending
on the size of the anemone, this fluid was run slowly into the coelenteron
through a hypodermic needle in the column for an equivalent length of time
(Batham, Pantin, and Robson, i960). Reduced0-5% methylene blue, diluted
3 or 4 times with sea-water, was then injected through the pedal disk at several
radii. Usually after f h the specimen was dissected and pieces of the column
and other tissues were pinned out on wax for examination. They were fixed
in 10% ammonium molybdate, usually with a drop or two of 2% osmium
tetroxide solution (Alexandrowicz, i960) for about 24 h at 2° C, washed, and
taken through ethyl and butyl alcohols to liquid paraffin. Successful preparations were later mounted in depex (Kirkpatrick and Lendrum, 1939).
A few whole mesenteries and sections of anemones fixed in picro-formol
were stained with Batham-Holmes's silver method (Batham, Pantin, and
Robson, i960).
Most of these preparations were not flat enough to give satisfactory photographs, and drawings were made with the help of a camera lucida and tracings
from negatives.
Robson—Nerve-net of swimming anemone
537
The nerve-net and sensory system
The anatomy of the anemone is shown diagrammatically in fig. 1.
The processes of sense-cells are so interconnected with the nerve-net that
it is best to consider these systems together. It is unfortunate that the
material available is restricted to certain regions of the anemone, and in particular that little can be said about the innervation of the parieto-basilar and
sphincter muscles.
pharynx
retractor muscle
(endocoelic)
parieto-basilar
muscle (exocoelic)
• pedal disk
FIG. 1. Diagram showing the main anatomical features. The anemones available
were from I to 3 cm in diameter.
The column
The following features are common also to Metridium and Calliactis
Pantin, 1952; Batham, Pantin, and Robson, i960; Robson, 1961c). In the
column, relatively small bipolar nerve-cells form a sparse background network. Their processes run in no preferred direction but may accompany
orientated structures. Some run beneath the mesenteries alongside bundles
of circular muscle-fibres, others pass from the column on to a septum, and
others run wholly or partly along the angles between mesenteries and column.
As might be expected from previous studies, an aggregation of sense cells
is found on each side of a mesentery where it joins the column (and also at
the oral and pedal disks, but not the pharynx—see below). In Stomphia the
538
Robson—Nerve-net of swimming anemone
majority of sense-cells in this position have either one or two processes
(figs. 2 D; 3). These neurites are less than 1 /z in diameter and taper away so
that it is impossible to see how they end. As in Metridium and Calliactis,
sensory neurites may connect with neurites of the bipolar nerve-cells noted
above (fig. 4, A) and often show a similar distribution. That is to say, sensory
processes may run with circular muscle-fibres, either diving beneath mesenteries or passing on to the column (fig. 6, B) ; or they may run on to the septa,
connecting with the nerve-net there; or they may run vertically, contributing
to the usual plexus of fine neurites in the angle of the mesentery (fig. 2, D).
The sense-cells thus show the same histological connexions with the nerve-net
of the column and of the mesenteries as in other anemones. Scattered sensecells are likewise quite numerous over the general surface of the column
endoderm (fig. 4, A).
In Stomphia many column preparations also show large multipolar nervecells of the kind shown in figs. 2, A, B, c; 3; 4; and 5, A; an earlier record is
now confirmed (Robson, 1961a). Stellate cells occur rarely in the column of
Calliactis and have so far not been observed in Metridium. Their diameter
does not exceed 30 p. Each cell has up to a dozen processes, some of which
may fork once or twice. The neurites radiate in all directions and it is not
possible to distinguish a main axon. The processes are fine, comparable to
those of sense cells, and like them taper to invisibility. Since they can be
followed for at least 200 p it may be supposed that the average cell spans an
area possibly up to 1 mm in diameter.
These stellate nerve-cells extend in one plane between the circular muscle
and endodermal epithelium. They occur throughout the column and available preparations suggest that they are evenly scattered. Two or three may
occur together as in fig. 3, but they do not appear to form any regional aggregations. An anemone 2 cm in diameter might by the crudest calculation be
supposed to have more than 10,000 of them. They appear to be fully interconnected with the ordinary endodermal system of the column: that is to say,
multipolar neurites show connexions with the background network of bipolar
nerve-cells (fig. 4, A), with processes of sense-cells (figs. 3; 4, A, C), and with
neurites of other multipolar cells (figs. 2, A; 3). The processes of multipolar
cells sometimes pass beneath the septa like those of other elements (fig. 6, A).
They are also linked to the mesenteric nerve-net, either passing on to the
septa themselves or connecting with bipolar mesenteric nerve-cells which run
Fie. 2 (plate). From fixed methylene blue preparations.
A, B, c, multipolar nerve-cells from the column. Circular muscle fibres (out of focus) run
vertically. A shows neurites from sense-cells and other nerve-cells. B shows oval nucleus and
nucleolus. In c, arrow indicates possible junction between adjacent neurites.
D, E, sense-cells at the base of mesenteries. Circular muscle-fibres (out of focus) run horizontally. D, junction of a mesentery (clear left-hand strip) and the column (granular area to
the right), showing a few of the many sense cells and their processes (compare fig. 3). E, pedal
disk, showing neurites of a bipolar sense-cell passing beneath a mesentery (the grey band left
of centre). A few other sense-cells have stained.
•t
•i
1
Robson—Nerve-net of swimming anemone
539
on to the column. A few cases have also been seen in which adjacent neurites
of the same cell appear to form a junction (figs. 2, c; 6, A). Further unorthodoxy is provided by an occasional neurite which seems to arise from the lower
surface of a cell and to pass into the mesogloea towards the ectoderm. The
last two observations require confirmation, for it is difficult to estimate the
FIG. 3. Multipolar nerve-cells and sense-cells from the column. Sense-cells are aligned at the
base of a mesentery (not shown, but compare fig. 2, D), which runs parallel to the lower edge
of the drawing. The arrow shows direction of circular muscle-fibres.
degree of artifact in fixed methylene blue preparations and unfortunately
silver preparations of the column have not yet been obtained.
The middle zone of the column does not appear to differ from the rest, and
the pacemaker system clearly does not reside in a 'nerve-ring'. The possibility
that the multipolar cells are concerned is discussed on p. 546. It may be noted
here that all the processes of nerve-cells and sense-cells in the column are fine
and short, compared to the much thicker and longer ones of most bipolar cells
in the mesenteries and oral disk. It is consistent that the rate of conduction
round the column is relatively slow, not exceeding 25 cm/sec. Comparable
values in Calliactis and Metridium are 15 and 10 cm/sec respectively (Pantin,
19356; Robson, 1961c). The multipolar nerve-cells of Stomphia certainly do
not conduct very rapidly. They may have a motor function but so far actinian
54°
Robson—Nerve-net of swimming anemone
nerve-endings have only been seen in the retractor nerve-net of Metridium
(Pantin, 1952; Batham, Pantin, and Robson, i960).
10//
FIG. 4. Multipolar nerve-cells fromfixedmethylene blue preparations of the column. Possible
connexions with neurites of a bipolar nerve-cell are shown in A, and with those of sense-cells
in A and c. Circular muscle-fibres run parallel to arrows.
The mesenteries
The main mesenteries carry 3 different muscles: there is a well-developed
retractor on the endocoelic surface, while on the exocoelic side there is radial
muscle in part covered by the parieto-basilar muscle. This originates from
the parietal region of the mesentery as a fold of vertical fibres, and extends
as a triangle from the base of the septum to a point below the tentacles.
The retractor surface has a rich network of bipolar nerve-cells, similar in
many respects to that described for Metridium and Calliactis (Pantin, 1952;
Batham, 1956; Batham, Pantin, and Robson, i960; Robson, 1961c). In
Robson—Nerve-net of swimming anemone
541
silver preparations the cell-bodies are 30 p or more long (fig. 7, c), and their
processes, initially 2 or 3 ^ wide, may each run for a few millimetres, crossing
many other neurites as they do so (fig. 7, A, D). Synaptic junctions resemble
those of Metridium (figs. 7, B, D). Since the retractor muscles can give quick,
facilitated contractions (Sund, 1958; Hoyle, i960), the retractor nerve-net
FIG. 5. A shows size range of multipolar nerve-cells in the column. The arrow indicates the
direction of circular muscle fibres, and a few epithelial cell-boundaries are indicated, B, a
multipolar nerve-cell from the pedal disk.
FIG. 6. A shows a multipolar nerve-cell in the column, two of whose processes pass under
a mesentery (stippled) and cross at the same focal level (compare fig. 2, c). B, sense cell with
four radiating neurites, one of which also follows the circular muscle beneath a mesentery
(stippled) where it joins the column (compare fig. 2, D, E).
may be regarded as a rapid through-conduction system (Pantin, 1935, 1952).
Its speed of conduction has not been measured but is much faster than in the
column. Fig. 7 A suggests that the density of cells and connexions is comparable to the retractor nerve-net in Metridium, where vertical conduction
speed is about 1 m/sec. Endings over the muscle have not yet been seen.
Processes from the retractor nerve-net may run out on to adjacent parts of
the column and oral and pedal disks, and make contact with a variety of
neurites there. As in other anemones, the retractor nerve-net is connected with the column system and with the rows of parietal sense cells. It is
worth mentioning here that excitation of the retractor and sphincter muscles
542
Robson—Nerve-net of swimming anemone
FIG. 7. The retractor nerve-net, from silver preparations of mesenteries. Retractor musclefibres all run parallel to the arrow in A. A, sketch of the main neurites in a representative area.
B, bipolar nerve-cell on the radial surface of the mesentery (stippled) has neurites comparable
to those of the retractor nerve-net (full line), c, a large bipolar cell-body from the retractor
surface. D shows its southern neurite a short distance away. It is unusually broad (ribboning
artifacts are common in silver preparations) and forms junctions with processes of several
other nerve-cells.
apparently inhibits parieto-basilar contractions, which depend on excitation in
the column (Robson, 1961a, see p. 547).
As to the exocoelic surface of the mesentery, it is unfortunate that nothing
Robson—Nerve-net of swimming anemone
543
can yet be said of a parieto-basilar nerve-net. The innervation of parietal
muscles in other anemones, with which these are probably homologous, is
also unknown. In Stomphia the parieto-basilars respond to single electric
shocks with a quick contraction which varies with intensity (Hoyle, i960).
During swimming each contraction is presumably caused by local firing of
the pacemaker system in the column, but appropriate histological pathways
have not yet been seen.
The other exocoelic muscle has radial (or transverse) fibres over which
a sparse network of bipolar nerve-cells can be seen, at least where it is not
covered by the parieto-basilar. Just as in Metridium and Calliactis the cells
show the same range of size as those on the retractor surface (fig. 7, B), but
are very much fewer in number.
The oral disk, tentacles, and pharynx
Features of the crown may be examined in methylene blue preparations
with both disk and column left intact. Little has yet been seen of the nervous
system in the endoderm here. Rows of sense-cells occur in the angles where
mesenteries join the disk, but they are not concentrated at junctions with the
pharynx. This is not surprising, as they would hardly function as efficient
mechano- or chemoreceptors there. The retractor nerve-nets of the mesenteries are presumably connected endodermally with the oral disk and tentacles
and with the sphincter muscle, but this part of the system has not been studied
and is not yet known in any actinian.
The ectoderm of the oral disk shows an extensive nerve-net. Bipolar cells
of fairly uniform size run obliquely to the radii or along them, forming a crisscross system of large neurites over the whole surface (fig. 8, A, B). There is
some suggestion that they may be concentrated peripherally, and that they
may run on to the tentacles. Connected to this system and in the same plane
of focus, smaller nerve-cells form rows situated just above the insertion of the
mesenteries (fig. 8, c, D). These nerve-cells are multipolar, having usually
3 or 4 processes, and are distinct from the smaller sense-cells (fig. 8, c). (Sensecells are scattered over the whole disk, and their processes as usual connect
with the nerve-net.) The rows of small multipolar cells may tail off centrally,
at least above incomplete septa. Their distribution suggests a means by which
the disk and mesenteries might be co-ordinated. In an expanded anemone
they might perhaps function as ectodermal proprioceptors whenever the
mesenteric retractors contracted (Passano and Pantin, 1955), and bring about
contractions of the radial muscle in the disk and tentacles.
A similar ectodermal system was described by the Hertwigs (1879) f° r t n e
disk of Sagartiaparasitica {Calliactis (Stephenson, 1935)) and other anemones,
and it seems unlikely that many of its features are peculiar to Stomphia. The
network of bipolar nerve-cells has been seen in Metridium (Batham, Pantin,
and Robson, unpublished observations). In Calliactis, as noted by the
Hertwigs, disk nerve-cells of the bipolar type include many with 3 or 4 long
neurites. As the oral disk of Calliactis shows most interneural facilitation in
544
Robson—Nerve-net of swimming anemone
a radial direction (Pantin, 1935 a, b), it is possible that this property is associated with radially aligned small nerve-cells. Further work is needed for
it is not even clear how the ectodermal muscle of the crown is innervated.
FIG. 8. Ectodermal nerve-net of the oral disk, from methylene blue preparations, A, diagram
of oral disk (after Stephenson, 1935) to show situation of B. B, network of bipolar nerve-cells
(incomplete) on upper surface of the disk. The position of two mesenteries and of two
tentacles is indicated by stippling, c, drawing of another preparation showing numerous
small multipolar nerve-cells in a row above the insertion of a mesentery (stippled). The
processes of bipolar nerve-cells run across the field, and a sense-cell (arrow) is included for
comparison. D, small multipolar nerve-cells from another preparation, oriented as in c.
In Stomphia sense-cells are numerous throughout the ectoderm or disk and
tentacles, and are very abundant in the pharynx. They have a short cilium
and 1, 2, or 3 neurites.
As specimens of Stomphia show swimming behaviour after the whole of
the crown has been removed, this region cannot be essential to the pacemaker
system.
Robson—Nerve-net of swimming anemone
545
The pedal disk
Only the endodermal surface of the pedal disk has been examined. It
seems to have few nerve-cells running on to it from the septa, and those seen
are small. Bipolar cells form a sparse general network but seem to be even
fewer than those in the column. Multipolar nerve-cells occur very occasionally (fig. s, B).
Sense-cells, on the other hand, are numerous. The usual aggregation lines
the basal angles of each mesentery, and there are scattered sense-cells over the
whole pedal surface. Some of these look unusually large, but this may be due
to the ease with which preparations can be stretched. They normally have
two or more processes, which often follow the circular muscle fibres (fig. 2, E).
They are smaller than most nerve-cells but might be hard to distinguish from
them were it not for their cilia. There is, of course, no reason why their
functions should not be similar (compare Grundfest, 1961). Even if the circular and basilar muscles of the pedal disk require little innervation, it seems
odd that so few nerve-cells should be present, and until more evidence is
forthcoming, Parker's suggestion (1919) that sensory neurites might supply
muscle fibres directly still seems a sensible one. The problem cannot be
solved until electron microscopy or histochemistry provides a means of
tracing hitherto invisible endings.
Nervous elements which might function as pacemakers seem to be absent
from the pedal disk. Another feature of the swimming response is of interest
here: the speed with which a closed anemone may react to brief contact with
Aeolidia suggests that conducting pathways exist between ectoderm and
endoderm. In the foot, retractor muscle-fibres of the mesenteries pass into
the mesogloea and may reach the ectoderm (Robson, 1961a). In methylene
blue preparations a few stained processes resembling those of nerve-cells
have now been seen penetrating the pedal mesogloea, usually near the septa.
The observation needs to be confirmed.
Discussion
As far as the nervous system is concerned, Stomphia differs from some of the
anemones not showing swimming behaviour in possessing large multipolar
nerve-cells in the column. These elements are for the moment the only ones
with which a pacemaker system might be specifically associated. No difference
between the median zone of the column and the rest has yet been noticed.
Three kinds of multipolar nerve-cell have been seen and can to some extent
be recognized in other coelenterates. There are those situated among bipolar
nerve-cells and which differ from them only in having 3 or 4 neurites. In
Stomphia they are seen occasionally in the retractor and column nerve-nets.
They occur in other anemones (Anthea, = Anemonia (Stephenson, 1935);
Calliactis (Hertwigs, 1879); Metridium (Pantin, 1952)), and in medusae
(e.g. Amelia (Schafer, 1878), Carmarina (Geryonia), Cunina (Hertwigs, 1878);
Gonionemus (Hyde, 1902)). Tracts of large bipolar-type cells are associated
546
Robson—Nerve-net of swimming anemone
with rapid through-conduction and with a quick motor response. Their
action potentials have been studied only in medusae (Horridge, 1954; Passano,
I958).
Secondly there are smaller cells such as those forming rows on the oral disk.
They commonly have from 3 to 5 processes and although larger than sensecells may differ from them only in lacking cilia. Cells of this kind have been
supposed to represent a primitive condition (e.g. Parker, 1918) and occur in
most coelenterates. They characterize the nerve-net of Hydra and other
hydroids (e.g. Schneider, 1890; McConnell, 1932) and are found in any
medusa or anthozoan (e.g. Hertwigs, 1878, 1879). ft *s usually agreed that
they are able to conduct diffuse excitation (Bozler, 1927), but their functions
must depend on the distribution and density of neurites and of their connexions. Horridge (1956a, b) showed that in Cyanea, Cassiopeia, Nausithoe,
and the ephyra larva of Amelia a diffuse net produces motor activity distinct
from pulsations of the bell. This net contains small multipolar cells and has
many sensory connexions. It is able to excite and sometimes to inhibit the
marginal ganglia and thus also influences the locomotor rhythm. Passano
(1958) has recorded nerve action potentials in the diffuse nets of Cyanea and
Cassiopeia. His evidence that individual cells conduct excitation only intermittently supports the theory developed by Horridge (1957) for anthozoan
colonies. Two nerve-nets are also present in hydromedusae (Horridge, 1955).
Potentials provisionally attributed to the diffuse hydrozoan nerve-net have
been recorded in Hydra (Passano and McCullough, 1962), Cordylophora,
and Tubularia (Josephson, 1961, 1962).
The multipolar cells in the column of Stomphia have at least half a dozen
neurites and are regarded as a third group owing to their size. Such conspicuous stellate cells have not often been reported in coelenterates. Similar
but smaller ones which occur over the subumbrellar muscle of Carmarina
[Geryonia) (Hertwigs, 1878; Krasiriska, 1914), and Cyanea (von Ledenfeld,
1882) are probably part of the diffuse nerve-net.
From work on jellyfish it is not possible to suggest that one kind of nervecell is particularly associated with pacemaker activity. In scyphomedusae
impulses arise in the marginal ganglia (Horridge, 1959; Passano and
McCullough, i960), but these are not of uniform histological structure.
Horridge (1961) has discussed the key role of neuropile in the activity of
ganglia in general and has suggested that it may be important in Aurelia
(19566). In hydromedusae the pacemaker system is associated with one or
both nerve-rings but no further histological correlation is yet possible.
In Stomphia, however, the nerve-net of the column, where the pacemaker is
thought to be situated, differs from that in some non-swimming anemones in
possessing large multipolar cells. In the absence of physiological information
the function of these cells can only be elucidated by morphological comparison, and it is provisionally suggested that they constitute the pacemaker
system. When active this system would produce a relatively slow train of
impulses. The parieto-basilar muscles respond to single electric shocks
Robson—Nerve-net of swimming anemone
547
(Hoyle, i960) and it is reasonable to suppose that one impulse would precede
each swimming contraction. If impulses do arise in the column nerve-net, it
is difficult to understand the complete absence of retractor contractions
without supposing either that the retractor system is inhibited during
swimming, or that such impulses do not reach the retractors. Strong stimuli
which cause retraction interrupt swimming (Wilson, 1959). Reciprocal
inhibition between the parieto-basilar and retractor muscles would clearly
depend on the distribution of neurites where mesenteries join the column,
but the histological picture of this region is far from complete and requires
further study.
It is not impossible that the multipolar cells perform several functions.
Vigorous swimming contractions are associated with high tone of the circular
muscle (Robson, 1961a). It seems probable that the column nerve-net can
transmit excitation to the circular muscle, but it is difficult to estimate the
possible role of multipolar cells in this context as the endings of their neurites
have not been seen. There are several studies of actinian circular muscle
(Batham and Pantin, 1954; Ross, 1957, i960; Ewer, i960), but it is not yet
known how contractions are normally initiated or maintained.
As the multipolar cells are histologically interconnected with the column
nerve-net they may also conduct nervous excitation. It has been seen that
the column nerve-net conducts slowly (p. 539). In addition, it seems to fatigue
easily. When an isolated sector of anemone (fig. 1) is stimulated electrically
(Robson, 1961c), 10 shocks 1 sec. apart produce 9 facilitated retractor contractions. If the electrode is placed at the end of a strip of column attached
to the preparation so that excitation reaches the retractors after travelling
through the column nerve-net, contractions drop out towards the end of the
series and the total may be 7 or 8. Fatigue in the column nerve-net is a
possible interpretation of this result and it may help to explain why sites of
swimming contractions are so labile.
Further remarks about the operation of the pacemaker system are purely
speculative. The multipolar neurites show frequent connexions with other
nerve-cells and with sense-cells, and it would be possible for excitation in
any of these elements to interact. Passano and McCullough's recent studies
(i960, 1961) provide some information about the regulation of spontaneous
electrical activity in ganglia of Cassiopeia and Cyanea. It may prove that
coelenterate pacemakers are concerned only with separate propagated impulses. On the other hand, it may be suggested with due caution in the
absence of direct evidence, that it might be possible for electrotonic changes
to play some part in pacemaker activity, as seems to be the case in the crustacean heart ganglion (Bullock and Terzuolo, 1957; Watanabe and Bullock,
i960; Maynard, 1961). Pantin (1950, 1956) has suggested that graded
potentials may be significant in the nerve-net of Hydra, although Passano
and McCullough's evidence (1962) throws little light on this point. If action
potentials can be recorded from the actinian nerve-net it will be easier to discuss changes in threshold and 'spontaneous activity' in terms of depolarization
548
Robson—Nerve-net of swimming anemone
(e.g. Eyzaguirre, 1961), and to assess the role, if any, of non-propagated potentials. In this respect little is known either of the mode of action of
coelenterate receptors, or of whether sensory excitation always reaches the
nerve-net as separate impulses in sensory neurites. The problem might
perhaps be studied most easily in medusan sense organs (Yamashita, 1957).
Whether or not graded potentials occur and are of any significance, the
structure of the large multipolar cells in Stomphia suggests that any impulses
arising in the soma would be distributed by all the neurites. It might, however, be necessary for several neurites to be excited at once before such a cell
would discharge 'spontaneously' (see Tauc and Hughes, 1963). The local
geography of neurites and of their connexions would appear to allow of this,
but the physiological properties of such a system cannot be predicted from
histological observations alone. From existing evidence it is at least not
impossible that the multipolar network may show pacemaker activity when
excited to a critical level, and that when acting as a pacemaker it should be
influenced by further stimulation.
This work was carried out at the Marinbiologisk Laboratorium, Helsingor,
and was assisted by a grant for travelling expenses from the E. M. Musgrave
Fund of the University of Cambridge. It is a pleasure to thank Professor
Gunnar Thorson and his colleagues for their generous support during the
course of this study, and Dr. G. M. Hughes and Professor C. F. A. Pantin,
F.R.S., for very helpful discussion.
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