J. exp. Biol. 108, 137-149 (1984)
trinted in Great Britain © The Company of Biologists Limited 1984
137
NERVE NETS AND CONDUCTING SYSTEMS IN SEA
ANEMONES: TWO PATHWAYS EXCITE TENTACLE
CONTRACTIONS IN CALLIACTIS PARASITICA
BY IAN D. McFARLANE
Department of Zoology, University of Hull, Hull HU6 7RX, U.K.
Accepted 2 June 1983
SUMMARY
1. Single shocks to the column sometimes evoke tentacle contractions,
ranging from slight movement of a few scattered tentacles to rapid bending
or shortening of all the tentacles. Some individuals are more responsive than
others. Complex bursts of electrical activity follow single shocks, but only
in tentacles that contract.
2. These single shocks excite pulses in two conducting systems - the
through-conducting nerve net (TCNN) and the ectodermal slow conduction system (SSI). When a single shock evokes contractions and bursts of
electrical activity, these usually follow the SSI pulse, rarely the TCNN
pulse. Stimulation of the SSI alone causes tentacle contraction in responsive
anemones.
3. Fast tentacle contractions always follow the second of two closelyspaced TCNN pulses: the TCNN shows facilitation (Pantin, 1935a). An
SSI pulse, however, does not facilitate subsequent pulses in either the SSI
or TCNN.
4. There are two pathways for activation of tentacle contractions. The
TCNN pathway is mechano-sensitive and normally requires facilitation.
The SSI pathway is mechano- and chemosensitive, only requires a single
SSI pulse to evoke contraction, but is very labile. It is proposed that the
TCNN and the SSI do not excite the ectodermal muscles directly, but via
a multipolar nerve net.
INTRODUCTION
Multiple conducting systems coordinate the behaviour of sea anemones. There are
at least four separate systems (McFarlane, 1982). Pulses from three of these (the
through-conducting nerve net, TCNN, the ectodermal slow system, SSI, and the
endodermal slow system, SS2) can be recorded extracellularly from tentacles.
The tentacles show both feeding movements and protective reflexes. Their contractions range from local movements after gentle stimulation, to rapid symmetrical
contractions after strong stimulation anywhere on the body. Tentacles have an
ectodermal longitudinal muscle layer (responsible for most local and symmetrical
movements) and a weak endodermal circular muscle layer. They have a well-developed
ectodermal nerve net but few, if any, endodermal nerve cells (Van Marie, 1977).
Key words: Nerve net, contraction, sea anemone.
138
I. D.
MCFARLANE
Fast contractions in Calliactisparasitica are coordinated by a specialized nerve net,
the TCNN. A single TCNN pulse does not normally evoke fast muscle contraction
but does facilitate the action of a subsequent pulse (Pantin, 1935a). Josephson (1966)
recorded muscle action potentials preceding fast tentacle contractions in C. polypus.
Single shocks to the column of Calliactis parasitica sometimes make the tentacles
contract. Pantin (1935a) noted that, 'Light stroking of the column may also produce
occasional slight upward contractions of individual tentacles scattered round the disc'.
When describing the results of electrical stimulation of the column, he stated that,
'Again, in responsive animals, a single stimulus may produce a reaction in the form
of a slight waving of tentacles scattered round the disc'. Davenport (1962) suggested
this showed that TCNN pulses can sometimes elicit tentacle contractions without
facilitation.
I show in this paper that tentacle contractions in response to single shocks are
usually coordinated by the SSI, not by the TCNN. The tentacle muscles may receive
dual excitatory innervation or the TCNN and SSI may act via a single interposed
conducting system. These results further extend the list of known SSI-coordinated
actions: pedal disc detachment, excitation of circular muscles, and activation of
TCNN pacemakers in Calliactis parasitica (McFarlane, 19696, 1976, 1983), inhibition of inherent contractions of oral disc muscles in Urticina eques (McFarlane
& Lawn, 1972), and activation of swimming pacemakers in Stomphia coccinea
(Lawn, 1976).
MATERIALS
AND
METHODS
Calliactis parasitica (pedal disc diameters, 2-4 cm) were supplied by the Plymouth
Marine Laboratory. They were left attached to Buccinum shells, kept at 16-20°C in
a 70-1 tank of artificial sea water, and fed weekly. Three separate batches of ten animals
were used; each batch was replaced after 4 weeks.
Recordings were made with polyethylene suction electrodes attached to tentacles.
Recording and display apparatus consisted of Isleworth Electronics A103 preamplifiers, a Telequipment D1011 oscilloscope, a Datalab DL902 transient recorder,
and a Linseis LY1700 plotter. Stimuli (1 ms duration) were given through a suction
electrode on the column. Experiments were performed under dim light.
Direct mechanical records of tentacle contractions were not made as most movements were too weak to be detected by the available equipment. Instead, times of
contraction were determined from cine"filmsmade on Eastman 4-X negative film. The
bright lights used did not appear to modify contractions. Each stimulus triggered an
electronic flash to mark the event on the film. Film speed was 24 or 32 frames per
second; this provided sufficient accuracy to determine whether contractions followed
TCNN pulses or SSI pulses.
RESULTS
Contractions following column stimulation
A single shock anywhere on the column sometimes evoked tentacle movements i d
responsive animals, regardless of whether or not a recording electrode was attache*
Tentacle contractions in Calliactis
125
Fig. 1. Single shocks to the column may elicit tentacle movements - either an 'early' contraction after
a through-conducting nerve net (TCNN) pulse or a 'delayed' contraction after an ectodermal slow
conduction system (SS1) pulse. Drawings were traced from single frames of a cin6 film; numbers refer
to time (in ms) since stimulus. As film speed was 24 frames per second the times shown have an error
range of ± 40 ms. (A) Two superimposed drawings showing an early contraction. These five outer
cycle tentacles did not shorten until 170 ms after the shock. At a nearby tentacle the TCNN pulse
came 1 IS ms after the shock (shortly before the contraction). The SSI pulse came 705 ms after the
shock (after the contraction). (B) Three superimposed drawings of a delayed contraction (an outward
sweep) in a single outer cycle tentacle. Movement began 920 ms after the shock and it ended 1-5 s after
stimulation. Nearby, the TCNN pulse delay was 105 ms, much less than the contraction delay,
whereas the SSI pulse delay was 770 ms. (C) Two superimposed drawings of a delayed contraction
(an inward sweep) of two inner cycle tentacles. Movement started at 840 ms, the TCNN pulse delay
was 95 ms, and the SSI pulse delay was 680ms.
to a tentacle. The response ranged from a barely detectable twitch of a few tentacles,
through to a large fast contraction of all the tentacles. Contractions appeared to fall
into two groups. In one, movement closely followed the stimulus (an 'early' contraction), in the other it came 0-5-1 s after the shock (a 'delayed' contraction). This
subjective distinction between early and delayed contractions was very clear and was
later supported by analysis of cine"films.Fig. 1 shows that an early contraction follows
a single TCNN pulse whereas a delayed contraction follows a single SSI pulse.
Early contractions appeared to involve more or less simultaneous contraction of all
tentacles. The movement was often barely visible and was seen in less than 25 % of
individuals tested and it followed less than 10 % of shocks applied. The tentacles did
not bend in this response, but just shortened slightly (Fig. 1A).
Delayed contractions were more variable in extent and strength, but they were
more common than early contractions: they were seen at some time in more than 90 %
of individuals. Members of a group of 10 anemones were stimulated daily for 2 weeks
with three test shocks (10 V, lms) 3 min apart. Each day between three and six
anemones (mean 4-9) showed delayed contractions (to at least one of the test shocks),
although generally the contraction was slight and detectable only as an inward movement of the inner cycle of tentacles. Only one anemone responded every day and one
never reacted at all. Individual variations in responsiveness were not obviously related
to nutritional state. No way was found to make unresponsive anemones respond.
The strength of the delayed response, and the number of tentacles involved, varied
considerably. When the nature of the contraction could be determined, it was generally a bending movement (Fig. 1B, C). The commonest movement (50 % of observed
'esponses) was an inward sweep of the inner cycle tentacles. An outward movement
140
I. D. MCFARLANE
of the outer cycle tentacles occurred in 15 % of observed responses. Rarely (less than'
3 % of responses) the contraction was powerful and produced marked shortening of
all tentacles. The contraction in the remaining cases was too small to be clearly
defined; sometimes only a few scattered tentacles moved, sometimes all tentacles gave
a barely perceptible twitch. In less than 2% of all responses the shock elicited both
an early and a delayed contraction.
Unlike early contractions, delayed contractions could be seen to spread around the
oral disc as waves of tentacle movements. Clearly the conducting systems coordinating the two responses conduct at different rates or have different pathways. At 18 °C,
the TCNN in the oral disc conducts at 60-100cms" 1 (Pantin, 19356) whereas the
SSI conducts at 15cms" 1 (McFarlane, 1969a).
Electrical activity associated with delayed contractions
Electrical events that accompany tentacle contractions will be termed Tentacle
Contraction Pulses (TCPs), regardless of whether they follow TCNN or SS1 activity.
The nature of these potentials is not known, they are simply taken as evidence for
contraction at the recording site.
A single, low-intensity, shock to the column elicited a TCNN pulse and an SSI
Rl-
Rl-
R2-
R2-
-j-f
j0(M
I
A
D
w
R2
y*-—-4VHJ|M
J^I
Rl-
R2
Fig. 2. Delayed tentacle contractions to single shocks were associated with potentials (Tentacle
Contraction Pulses, TCPs) that closely followed the SSI pulse. Two recording electrodes (Rl, R2)
on inner face of inner cycle tentacles, 1 cm apart. Each record is the response to a single shock: at least
2min rest was allowed between shocks. The electrodes were not moved between trials hence the
different results are due to variations in responsiveness. (A) No delayed contraction seen — no activity
recorded after the SS 1 pulse. (B) Slight inward sweeping movement of the inner cycle tentacles noted
— TCPs seen after the SSI pulse. (C) Noticeable twitching of all tentacles. (D) Maximal response (a
marked shortening of all tentacles) - large TCPs follow the SSI pulse. Symbols: O, stimulus; |,
TCNN pulse; A, SSI pulse. Time scale, 500ms; amplitude scale, 10/iV.
Tentacle contractions in Calliactis
141
pulse. If no delayed contraction was evoked then the recorded SSI pulse had no
detectable afterpotentials (Fig. 2A). When delayed contractions did occur, electrodes
picked up pulses shortly after the SSI pulse (Fig. 2B, C, D), but only from tentacles
that moved. These TCPs came 0-150 ms after the SSI pulse, they never preceded it
when delayed contractions were seen. The TCPs in Fig. 2B were associated with an
inward sweep of the inner cycle of tentacles. The recording electrode was later moved
to a tentacle in another cycle; no TCPs were recorded when only the inner cycle
tentacles moved. Fig. 2D shows large TCPs, recorded from the same site as in Fig.
2B, but when all the tentacles gave a large contraction. Fig. 2B and 2D represent the
extremes of the SSI-associated contractions.
There was considerable variation in both TCP amplitude and in the delay between
the SSI pulse and the TCPs. These variations occurred between recording sites and
also between recordings at the same site. In Fig. 2C the delay was short at recording
site 2 but long at site 1, whereas only 3min later this situation was reversed (Fig.
2D). At site 1 the TCPs were small in Fig. 2C but only 3 min later they were large
(Fig. 2D).
Electrical activity associated with early contractions
When early contractions were seen it was found that the TCPs closely followed the
TCNN pulse, not the SSI pulse. Fig. 3A shows three consecutive stimuli recorded
at one site. The first shock gave no response, the second evoked a delayed contraction,
and the third gave an early contraction. With the delayed contraction TCPs followed
the SSI pulse. With the early contraction TCPs followed the TCNN pulse. Rarely
the early contraction was large and then the TCPs after the TCNN pulse were also
large (Fig. 3B). Large early contractions may result from the facilitating effect of a
preceding spontaneous TCNN pulse. Fig. 3B shows one of the rare occasions when
a single shock evoked both early and delayed contractions. Two recording electrodes
were used, on different tentacles. At one recording site the early TCPs were larger
than the delayed TCPs, at the other site the opposite was true. It is not known if this
reciprocal relationship is a common feature.
Fig. 3. Electrical activity associated with early and delayed contractions. (A) Three separate shocks,
2min apart, with three different results. Upper trace: no contraction seen. Middle trace: delayed
contraction seen. A burst of TCPs follows the SSI pulse. Here for some reason the stimulus failed
to excite the TCNN. Lower trace: early contraction seen. A burst of TCPs comes after the TCNN
pulse. (B) Record from two electrodes (Rl, R2) on tentacles 2 cm apart when a single shock evoked
both an early and a delayed contraction. Unusually, the early contraction gave TCPs at only one of
the electrodes. Symbols as in Fig. 1. Time scale, 500ms; amplitude scale, 10/iV.
142
I. D.
MCFARLANE
c
D
B
f
f
/
(
A
Fig. 4. (A) Tentacle contractions can, in responsive anemones, be elicited by stimulation of the SSI
alone. Here five consecutive single shocks were applied, at 1 min intervals. TCPs and contractions
followed the first two shocks but subsequent shocks did not evoke contraction. Small potentials here
follow the third and fourth SSI pulses but their significance is not known. (B-D) Effects of repetitive
stimulation. Ten shocks were applied at stimulus intervals of 3 min (B), 2min (C), and 1 min (D).
Only the first five responses are shown in B and the first seven in D ; the responses not shown involved
no contraction. Note temporary recovery of the contraction response in C and D. Symbols as in Fig.
1. Time scale, 500ms; amplitude scale, 20[iV.
Stimulation of the SSI alone can elicit tentacle contractions
The SSI has a higher threshold than the TCNN but can, however, be stimulated
alone via a shallow ectodermal flap cut in the column (McFarlane, 196%). Flap
stimulation at intensities below SSI threshold never evoked delayed contractions or
TCPs. Stimuli at, or above, SSI threshold evoked delayed contractions in responsive
animals (Fig. 4A). The second shock in Fig. 4A produced a rare event, the apparent
reflection of a contraction wave. Here the delayed contraction began, as usual, as two
waves of tentacle movement that spread in opposite directions around the oral disc.
Then, the waves did not cancel out but passed each other and this gave the impression
of a reflected wave. The waves stopped when they collided on meeting again at their
point of origin on the disc. The recording shows a second SSI pulse and following
TCPs, presumably associated with the second contraction.
Although, as in the case of the double contraction described above, two SSIactivated contractions can occur close together, there is normally a marked decline in
responsiveness with repetitive stimulation (Fig. 4B—D). The effect of repetitive stimulation varied considerably from animal to animal and from time to time in the samj
animal.
Tentacle contractions in Calliactis
143
Comparison of evoked and spontaneous tentacle contractions
Tentacle contractions may be evoked by TCNN or SSI pulses, but tentacles can
also contract spontaneously, without preceding TCNN or SSI activity. Such contractions involve single tentacles: they do not spread. They occur regardless of whether
or not an electrode is attached to the tentacle. Fig. 5 shows recordings made with two
electrodes on the same tentacle. Both electrically-stimulated and 'spontaneous' SSI
pulses may cause contractions and TCPs (Fig. 5A, B). The SSI is probably not
spontaneously active (McFarlane, 1973): the 'spontaneous' SSI pulses may arise from
mechanical stimulation. The tentacles did, however, sometimes contract in the absence of SSI pulses (Fig. 5C, D) and the movement was accompanied by TCP-like
electrical events. Note that these spontaneous events spread, comparatively slowly,
from tip to base of tentacle. The conduction velocity of the SSI pulses recorded in
Fig. 5B, and hence the rate of spread of evoked contractions, is about 18cms ~\
whereas the spontaneous events in Fig. 5C and 5D appear to spread at Terns"1 and
2 cm s~' respectively. The latter value may be an underestimate as it is difficult in Fig.
5D to say where the TCP in R2 begins.
Lack of interaction between SSI and TCNN pathways
The SSI and TCNN pathways to the tentacle ectodermal muscles have different
properties. The TCNN pathway normally requires facilitation whereas the SSI pathway operates in response to a single pulse, not to the second of two closely spaced
pulses.
A single TCNN pulse rarely causes tentacle contraction but does facilitate the
action of a closely-following TCNN pulse (Pantin, 1935a). Pantin believed that this
facilitation occurred at the neuromuscular junction. TCPs always follow the second
RlR2-
C
RI
D
,
uLv^w^-^,—.
,
- Rl
>
Fig. 5. Evoked and spontaneous contractions recorded by two electrodes on the same tentacle - Rl
near tentacle tip, R2 on mid tentacle - about S mm apart. (A) Single shock to the column elicited a
delayed contraction and an SSI pulse followed by TCEs recorded at Rl and R2. Note that the SSI
pulses and TCPs spread distally, towards the tentacle tip. (B) 'Spontaneous' SSI pulse followed by
tentacle contraction. (C, D) Spontaneous tentacle twitch; note absence of SSI pulses before the
TCPs. The pulses spread proximaJly from the tentacle tip. Symbols as in Fig. 1. Time scale, 500 m»;
amplitude scale,
I. D.
MCFARLANE
D
Fig. 6. (A) Facilitation in the TCNN pathway to the tentacle muscles. Three shock pairs, with shock
intervals of 500, 800, and 1000 ms, applied to the column. The TCNN pulses after the first shocks
are not visible, but they had a facilitating effect as the second shocks evoked fast contraction. (B, C)
The SSI pathway to the muscles cannot be facilitated by SSI or TCNN pulses. (B) Two shocks,
500 ms apart, to a column flap evoked two SSI pulses, neither of which was followed by TCPs. (C)
Two shocks, 400ms apart, the first (O) to a flap excited an SSI pulse only, the second (O1) at low
intensity to the column excited a TCNN pulse only. Thus the SSI pulse could be made to follow
closely the TCNN pulse at the recording site. Although the TCNN pulse facilitates the TCNN
pathway, the SSI pulse was not followed by TCPs. (D, E) The SSI does not facilitate the TCNN
pathway. (D) Two shocks, 1000 ms apart, to TCNN only. (E) Two minutes later two shocks, 1000 ms
apart, to the TCNN and SSI. The size of TCPs following the second shock was unaffected by the
presence of an SSI pulse. Symbols as in Fig. 1. Time scale, 500ms; amplitude scale, 10/iV.
of two TCNN pulses 100—1500 ms apart: the amplitude and duration of the TCPs is
related to the interval between stimuli (Fig. 6A). When the interval was short, TCPs
were mainly single large biphasic or triphasic potentials similar to the pulses that
accompany fast sphincter muscle contraction (Josephson, 1966). At longer intervals,
the TCPs were less synchronous and resembled the pulses seen during SSI-evoked
contractions.
There was no evidence for heterofacilitation between the SS1 and TCNN pathways
to the muscle. A single SSI pulse did not facilitate the action of a closely-following
SSI pulse (Fig. 6B). Although a single TCNN pulse facilitated the TCNN pathway
(Pantin, 1935a), it did not enable a subsequent SSI pulse to evoke contraction (Fig.
6C). Again, a single SSI pulse did not facilitate the TCNN pathway to the muscle
(Fig. 6D, E).
DISCUSSION
Lability and variability of the response
The likelihood that a single SSI pulse will elicit a contraction declines with repeated
stimulation. This is not due to sensory adaptation as the stimuli are electric shocks.
It is not due to muscular fatigue as the muscle can still be activated via the TCNN.
It is an activity-dependent decline in responsiveness, presumably at a site somewhere
between the SSI and the muscle. Habituation occurs in Anthopleura elegantissima
(Logan, 1975) but it is not known which conducting system is involved.
Individual Calliactis parasitica differed considerably in their responses to single
stimuli. Fleure & Walton (1907) commented on differences in responsiveness between different individuals of several actinian species and mentioned that captivity
may modify characteristic activities. Perhaps the delayed contraction is less labile and
less variable in freshly-caught animals.
Tentacle contractions in Calliactis
145
Function of the response
A single SSI pulse can cause contraction of tentacles, a movement at times so small
as to be without obvious significance. At other times, a strong inward sweep of the
inner cycle tentacles, or an outward flourish of the outer cycle tentacles, may aid in
food gathering. The SSI can be excited by both touch, especially of the lower column,
and by dissolved food substances (McFarlane & Lawn, 1972), so such tentacle movements might allow the capture of nearby food. A few seconds after food is held above
the oral disc, out of reach of the tentacles, the tentacles begin to twitch. Some movements are uncoordinated, and may involve direct stimulation of individual tentacles,
but some are waves of contraction, presumably coordinated by the SSI.
Well-developed tentacle contractions occur in Boloceroides mcmurrichi, an
anemone that swims by lashing its tentacles. Lawn & Ross (1982) recorded bursts of
pulses (tentacle burst pulses - TBPs) associated with each tentacle flexion. They
found no SSI but their recordings clearly show a small SSI-like pulse (flexion trigger
pulse - FTP) just preceding each TBP burst. The FTP system is probably the SSI,
here again eliciting tentacle movements. Their records show a 100-200ms delay
between FTPs and TBPs, comparable with the 0—150ms delay seen between SSI
pulses and TCPs in Calliactis parasitica.
Carlgren (1942) considered the tribe Boloceroidaria (e.g. Boloceroides mcmurrichi)
to be more primitive than the tribe Thenaria (e.g. Calliactis parasitica). SSIactivation of tentacle contractions may be a primitive feature, one that is much
reduced and of little functional significance in Calliactis. Recordings from the two
species in the primitive actinian suborder, Protantheae, should be revealing: Gonactiniaprolifera also swims by tentacle flexions (Robson, 1971) and Protanthea simplex
reacts to various stimuli with violent twitching or lashing of the tentacles (Manuel,
1981).
Organization of the ectodermal 'nerve plexus'
The nervous structure of anthozoan ectoderm is not clearly understood. Hertwig
& Hertwig (1879-80) described a 'nerve plexus' formed from sensory cell branches
and from ganglion cells. Electronmicrographs show this plexus is 10 'neurites' thick
(Kawaguti, 1964; Van Marie, 1977). As the mean neurite diameter is less than 1 ptxn,
and the fibres appear tightly packed, there must be around 100000 profiles in a
transverse section of a 3 mm diameter tentacle. Such a neuronal abundance surely
exceeds requirements for behavioural coordination and contrasts sharply with the
smaller number of bipolar and multipolar nerve cells seen in methylene blue stained
whole mounts (Robson, 1963). The status of the plexus has been questioned. Vandermeulen (1974) suggests the layer is a concentration of basal ramifications from the
supporting cells. Van Marie (1977) says the plexus contains both nervous elements
and supporting cell branches but that when profiles are empty (without vesicles) one
cannot determine their nature.
I will consider two recent descriptions of neural structure — Peteya (1973) on
Ceriantheopsis americanus and Van Marie (1977) on four anthozoans — and try to
late them to the physiological findings. In Ceriantheopsis the plexus contains
fibre types (A, B, C, D) in the ratios 4000:4000:4: 1 and with diameters of
146
I. D. MCFARLANE
.-.-.-•-•
-,-.-.-.-.-.-.-.-.-.-.-.-.-.-.-.-.-.-.-.........-.....-.-..............-..-...........]E
1
Fig. 7. Model for arrangement of conducting systems in Calliactis parasitica. Multipolar nerve cells
(m), some possibly pacemakers, may excite ectodermal longitudinal muscle cells (lm) and endodermal circular muscle cells (cm). Activity in the multipolar net probably only spreads a short distance.
This nerve net's activity may be coordinated by three through-conducting systems: the throughconducting nerve net (TCNN), and ectodermal and endodermal slow systems (SSI & SS2). Arrows
show sensory input to all conducting systems. The multipolar nerve cells may drive behaviour directly
by acting as pattern-generating motoneurones (McFarlane, 1983). The TCNN, SSI and SS2 may
act as interneuronal systems that distribute sensory information (from internal and external sources)
that modifies behavioural programmes being executed by the multipolar cells. The TCNN action
tends to be immediate, exciting fast or slow contractions that override current spontaneous activity.
The SSI and SS2, whilst having some immediate effects (for example the SS1 -activated contractions
described in this paper), may be more involved in switching the pacemaker output from one phase
of spontaneous activity to another (McFarlane, 1983). Symbols: —|, excitatory junction; - O , inhibitory junction; -\ (-, unpolarized excitatory junction.
0-3-1 ^m: 0-1-0-3 /im: 4-6 /xm: 10-20 /im. Peteya believes C and D fibres to be axons
of bipolar neurones and A fibres to be axons of multipolar neurones respectively. A
fibre cell bodies are 5-10 /im in diameter and each carries 3-4 neurites. Only A fibres
bear neuromuscular synapses. Van Marie could not distinguish fibre classes by
diameter but he gave pharmacological evidence for two distinct nerve nets. One
employs a catecholamine transmitter and the other is purinergic; only the purinergic
system synapses with the muscles. The TCNN in Calliactis parasitica consists of
large bipolar nerve cells (Robson, 1965). These may correspond to Peteya's C and D
cells and Van Marie's catecholamine-containing cells. The multipolar nerve cells oJj
Calliactis (Hertwig & Hertwig, 1879-80; Robson, 1963) may be equivalent t™
Tentacle contractions in Calliactis
147
reteya's A cells and Van Marie's purinergic cells. I propose therefore that the TCNN
excites tentacle muscles indirectly by way of a multipolar nerve net. Robson (1971)
proposed such an arrangement in the primitive anemone Gonactiniaprolifera. In the
hydromedusan Polyorchis penicillatus a network of small multipolar neurones lies
between the swimming motoneurones and the epitheliomuscular cells (Singla, 1978;
Spencer, 1982).
The proposed model (Fig. 7) positions a multipolar nerve net between the TCNN
and the muscles. From this the neuromuscular facilitation of tentacle muscles (Pantin, 1935a) may be reinterpreted as being interneural facilitation between the TCNN
and the multipolar nerve net. This may not, however, apply to the specialized fast
muscle — the sphincter — studied by Pantin. Indeed, only bipolar neurones, not
multipolar neurones, have been found immediately adjacent to sphincter muscle cells
(Robson, 1965). The model shows multipolar neurones linking the TCNN to the
endodermal circular muscles - a multipolar net overlies the circular muscles (Robson,
1965). The TCNN action on the endodermal multipolars may be both excitatory and
inhibitory; Ewer (1960) showed the TCNN has a dual action on circular muscle
contractions.
Some multipolar cells may be pacemakers. At times the pacemaker output may pass
directly to the innervated muscles, to excite the spontaneous contractions so obvious
in isolated preparations. Ross (1960) states that the evidence, on balance, supports a
neurogenic origin for such contractions. At other times the pacemakers may excite the
TCNN, giving rise to TCNN bursts that coordinate the activity of many muscle
groups (McFarlane, 1974a). Pacemaker—* TCNN connections may be absent in the
ectoderm (McFarlane, 1974a).
The model shows sensory input to all the conducting systems. The TCNN and SSI
both respond to touch (Pantin, 1935a; McFarlane, 19696), the SSI and SS2 respond
to dissolved food substances or to contact with shells (McFarlane, 1970, 1976), and
the SS2 may receive input from endodermal receptors that detect stress in endodermal
muscles (McFarlane, 1974a). Multipolar neurones may be directly excited by sensory
cells and thus cause local contractions in response to touch; this implies there is
limited spread of activity through the multipolar net. Local contractions could, however, involve spread of activity through the muscle field itself- the model shows links
between muscle cells.
Both slow conduction systems may connect with the multipolar neurones. Transmesogloeal links between the SSI and a multipolar net are suspected in Stomphia
coccinea (Lawn, 1980). SS2 activity inhibits spontaneous contractions of endodermal
muscles (McFarlane, 1974a) and inhibits TCNN pacemakers (McFarlane, 19746).
The SSI excites endodermal circular muscle contractions (McFarlane, 1976), inhibits spontaneous contractions of ectodermal muscles (McFarlane & Lawn, 1972),
activates TCNN pacemakers (McFarlane, 1983) and excites occasional tentacle
contractions (present work). The observed variability of delayed contractions may be
explained by regional and temporal changes in the functional state of the SSI connexions with the multipolar cells. The 0-150 ms delay between SSI pulses and TCPs
might be evidence for an indirect action of the SSI on the muscles. Alternatively, the
31 may not always activate the muscle at the recording site. The delay would then
suit from a slow spread of TCPs through the muscle sheet. Fig. 7 shows junctions
K
148
I. D.
MCFARLANE
between muscle cells. Coupling could be electrical or mechanical, but neither have yeP
been demonstrated.
Nature of the SSI
It is unlikely that the SSI is the multipolar nerve net. There are few nervous
elements, other than sense cells, in the column ectoderm (Hertwig & Hertwig,
1879—80), yet the SSI is present in this region. The SSI could, however, be a nerve
net formed by sensory cell branches.
Some hydrozoan conducting systems are nervous, but others are non-nervous and
involve cell-to-cell conduction in sheets of epithelial or epitheliomuscular cells
(Mackie, 1970). Non-nervous conduction has not been demonstrated in anemones;
the somata of the ectodermal supporting cells might form the SSI but they are tall and
thin whereas non-nervous systems invariably involve cells only a few microns high
(Anderson, 1980). Perhaps a network of supporting cell branches forms the conducting elements. Shelton (1982) made a similar suggestion, based on an unpublished
electron microscopic study of Calliactis parasitica. Such a 'fib1"*1 network', a form of
non-nervous conducting system, might be equivalent to Peteya's B fibres. Peteya,
however, thought that the B fibres of Ceriantheopsis americanus were part of an
effector system, a proposal supported by the finding that synapses were only found
from A fibres onto B fibres; none were seen between B fibres. Synapses between B
fibres would be necessary to form a conducting system and also as the basis for the
observation that SSI activity is abolished by excess magnesium ions (McFarlane,
1969a).
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