AMFR. ZOOLOGIST, 5:483-490 (1965).
THE COORDINATION OF POTENTIAL PACEMAKERS
IN THE HYDROID TUBULARIA
ROBERT K. JOSEPHSON
Department of Zoology, University of Minnesota, Minneapolis
SYNOPSIS. Sectioning experiments and electrical recording indicate that there are
many potential pacemakers in polyps of the hydroid Tubularia. Functionally the
pacemakers are organized primarily into pacemaker systems, groups within which
there is tight coupling. The different pacemaker systems of a polyp are loosely coupled
to one another. There are two principal systems in Tubularia, one in the polyp neck
(the NP system) and one in the hydranth (the HP system). In addition, there are pacemakers controlling activities of individual tentacles. Activity in the NP system is usually
not associated with observable polyp behavior. HP system activity is correlated with
behavioral responses termed concerts. Concerts are probably digestive activities; they
result in the mixing of food being digested and the distribution of the products of this
digestion. The NP systems of polyps on a colony are loosely coupled to one another
through one of the three conducting systems found in Tubularia stalks. The loose
coupling between NP systems of polyps on a colony and the loose coupling between
NP and HP systems within single polyps results in there being some coordination of
concert activity throughout a colony.
Pieces removed from a coelenterate, if
large enough, are often spontaneously active. For example, a piece of a scyphozoan
medusae containing a marginal ganglion
(e.g., Romanes, 1877), a ring of column
from the anemone Metridium (Batham
and Pantin, 1954), or an isolated tentacle
from the hydroid Tubularia all show spontaneous contractions. It might be thought
that such activity is due to excitation
caused by the isolation procedure and the
exposure of cut tissue to the surrounding
medium; but the responses are so like those
seen in the intact animals, often both in
kind and frequency, that it seems more
likely that the activity is due to internal
pacemakers. The fact that many pieces cut
from a single animal will all show spontaneous activity indicates that there are
often many potential pacemakers in coelenterate tissue. But different parts of an
intact coelenterate do not act as completely
autonomous units; their activities are often
integrated so that the animal behaves as a
coordinated whole. The principal question
which I would like to consider here is how
are the many potential pacemakers of a
coelenterate coordinated to give unified
behavior.
Probably the simplest type of coordinaAuthor's present address: Dept. of Biologj, Western Reserve University, Cleveland, Ohio.
tion between potential pacemakers is found
in those cases where the pacemakers are
acted on by or are part of a common conducting system, and where the firing of any
one of the pacemakers resets them all. The
pacemakers of the several marginal ganglia
of scyphomedusae and the connecting giantfiber nerve-net represent an example of this
sort of pacemaker interaction (Pantin and
Vianna Dias, 1952; Horridge, 1959). Superimposed on this coordination, however, are
accelerating or inhibiting influences exerted by the diffuse nerve-net (Horridge,
1956). A tightly coupled group of potential
pacemakers and the conducting system linking them, such as the marginal ganglia pacemakers and giant-fiber nerve-net of scyphomedusae, here will be termed a pacemaker
system. Recent work has shown that there
are a number of pacemaker systems in
polyps of Tubularia and Hydra. The rest
of this paper will briefly describe the pacemaker systems of Tubularia, the behavioral
activities which they control, and the ways
in which activities of different pacemaker
systems are coordinated. Only a brief outline can be given here; more extensive accounts have been or will be published elsewhere (Josephson, 1962, 1965; Josephson
and Mackie, 1965). A large part of the work
which I will describe was done in collaboration with Dr. G. O. Mackie. McCullough (1965), presented some similar re-
(483)
'184
ROBERT K. JO.SEPHSON
teron canal in the more proximal stalk. The
endodermal cushion acts as a valve between
the two chambers and is usually closed in
quiescent polyps.
Unstimulated Tubularia polyps are spontaneously active. Most of the activity consists of local, non-rhythmic movements:
oral flexion of single proximal tentacles or
small groups of tentacles with slow return
to rest position, oral or aboral flexion of
single distal tentacles or small groups of
tentacles, and slow contractions of portions
of the musculature of the neck or proboscis
causing small postural changes. Periodically, twice a minute or so, all the proximal
tentacles synchronously flex orally. This
response is called a concert, after the concerted nature of the tentacle activity. Often
the distal tentacles also flex orally during a
concert. A few seconds after the onset of
the proximal tentacle movement, a peristaltic contraction sweeps down the probosFIG. I. A Tubularia polyp.
cis, beginning at the base of the distal tentacles. The concerts of a polyp are graded;
in
some the tentacle movements are brief
suits which she and Passano have obtained
and
stop when the tentacles are only parwith Hydra. I will ignore the very real
tially
elevated, in others the tentacle moveproblem of identifying the cellular elements
ments
are vigorous and the tentacles are
involved in the pacemaker and conduction
brought
up so that they completely envelop
activities. Evidence on these points for
the
proboscis.
The neck musculature often
Tubularia is as yet inconclusive. Mackie
contracts
during
the tentacle flexion of a
(1965) presented compelling evidence for
vigorous
concert.
Contraction of the neck
non-nervous conducting mechanisms in
usually
forces
fluid
from the neck chamber
some coclenterates, so it can no longer be
through
the
endodermal
valve into the proassumed that a coelenterate conducting .sysboscis chamber, causing the proboscis to
tem is nervous until proven otherwise.
swell appreciably. The peristaltic wave following the concert forces an approximately
POLYP BEHAVIOR
equal volume of fluid downward through
A Tubularia polyp has two sets of ten- the valve, reinflating the neck. Thus, in
tacles, the long proximal tentacles which concerts with neck contraction there is
circle the base of the hydranth, and the usually a tidal exchange of fluid between
smaller distal tentacles which surround the the two enteron chambers of a polyp. The
mouth (Fig. 1). The distal tentacles and valve usually remains shut during peristalmouth are borne on a mobile proboscis. tic contractions following concerts without
T h e stalk, just below the h\dranth, is modi- neck contraction, and no fluid is transferred
fied into a contractile neck region. A thick between the two chambers.
cushion of endoderm protrudes into the
The concert acthities of a polyp seem to
entcron at the base of the proximal ten- be primarily digesthe lmnemcnts. Thc\
tacles and divides the enteron into two result in the mixing of the contents ol the
(hainbeis, a distal chamber in the proboscis proboscis cavity where the initial lood diand a proximal chamber in the nerk. The gestion occurs (all concerts), and partial
neck < hambi'i is continuous with the cii- tianslcnal oi the pioriucts ol this dii^t stinn
PACEMAKER COORDINATION IN
Tubularia
485
0.2 mV
2mV
5 sec
FIG. 2. Spontaneous electrical activity in a polyp. The small potential from the neck is an
HP, the larger ones are NP's. The large potentials from the proboscis are HP's, XP's are
barely visible at this amplification.
to the neck and more proximal stalk (concerts with neck contraction). In mature
polyps, gonophores are borne on hollow
racemes which arise from the proboscis
wall in the intertentacular region. The
pressure changes in the proboscis cavity
caused by the concerts force fluid to and
fro in the racemes, and presumably aid in
supplying nutrients to the developing gonophores.
PACEMAKER SYSTEMS IN THE POLYP
An electrode anywhere in or on the hydranth or neck of Tubidaria records brief,
spontaneous electrical potentials. The potentials recorded from the distal polyp, excluding the tentacles, fall into two classes.
Potentials of one class are large in the neck
and are greatly attenuated in the hydranth
or more proximal stalk. These potentials
are termed neck pulses (XP's). The potentials of the second class are large in the
proboscis, but can usually be recorded as
smaller potentials in the distal stalk as
well. These potentials are termed hydranth
pulses (HP's). The proboscis and neck
respond in a unitary manner with regard to
the production of HP's and XP's. HP's
appear nearly simultaneously from each of
two electrodes on the proboscis, and an HP
is never seen from just one of the pair.
Similarly, NP activity throughout the neck
is everywhere nearly coincident.
XP's and HP's appear to result from activity in two distinct pacemaker systems.
From the size of the pulses, it seems safe to
assume that the XP system is found principally in the neck and the HP system in
the more distal hydranth. There is some
evidence indicating that there are many potential pacemakers within each system, but
the evidence for multiple pacemakers in the
systems of Tubidaria is not yet as conclusive
as it is for the similar systems of Hydra
(Passano and McCullough, 1964, 1965). In
Hydra it has been clearly shown that there
are many potential pacemakers, that the
initiating locus can shift from pulse to
pulse, and that firing of one pacemaker
resets the others.
Figure 2 illustrates some of the properties of the two pacemaker systems of Txibularia. XP's typically appear in a pattern of
repeating single pulses, interrupted at intervals by bursts of three or more pulses.
The HP system itself produces single pulses
or short bursts of two or three pulses. When
the XP system fires in a burst, it usually
drives the HP system to fire concurrently.
During an NP burst, an electrode on the
proboscis typically records a number of
small NP's which facilitate slightly and are
suddenly obscured by the appearance of the
much larger HP's. Driving of the HP system by the NP system, when the latter fires
in a burst, is the principal but not the only
type of interaction between the two systems. Single NP firing sometimes triggers
HP's, and independent firing of the HP system sometimes triggers NP's. Thus the
interaction between the two systems is twoway and not just uni-directional.
Activity of the NP system usually is re;-
486
ROBERT K. JOSEPHSON
fleeted only indirectly in polyp behavior.
In a few polyps, XP's are associated with
slow, slight, neck-straightening; but in most
polyps single NP's or NP bursts which fail
to excite the HP system have no behavioral
correlate. HP's, on the other hand, are
quantitatively correlated with concerted
tentacle elevation. Brief, twitch-like concerts generally appear with one or a few
HP's, vigorous concerts appear with longer
HP bursts, those that occur when the HP
system is driven by the NP system firing in
a burst. The exact relation between number of HP's and concert intensity varies
somewhat from polyp to polyp, but after a
polyp has been observed for a while and
"calibrated," the concerted activity of the
proximal tentacles can be predicted quite
accurately by observing a recording channel
displaying HP's. The relation between electrical activity and contraction of the polyp
neck region is not so clear. Neck contraction of the sort leading to tidal exchange
occurs during long NP bursts when both
the NP and HP systems are active. Single
NP's, NP bursts which fail to excite the
HP system, independent HP's, or short NPHP bursts usually have no associated neck
contraction. The precise relation between
pacemaker activity and neck contraction is
one of the many problems waiting to be
solved in Tubularia.
The above observations apply to freshly
collected Tubularia larynx. Mackie (personal communication) has succeeded in
growing T. crocea in the laboratory, and
has found some interesting differences in
the behavior of his cultured polyps as compared to field-collected T. larynx. In well
fed, laboratory-grown polyps, the NP bursts
are longer and more regular, the concerts
almost always have an associated neck contraction component, and there is essentially
no independent HP activity.
The concerts of a Tubularia polyp, which
represent a large fraction of its spontaneous behavior, appear to result from activity
in two interacting pacemaker systems; the
HP system, which is directly related to
concerts, and the NP -A stun, uhkh is related to concerts through its ability to dri\e
the HP system. 1 lie spontaneous ik\-
100 msec
, 100/uV
FIG. 3. Electrical potentials from two of the three
conducting systems in the stalk. The small potentials (marked by the dots) are from the DOS, the
large potentials from the SS. The SS has fired twice
in this record.
ions of single tentacles or small groups of
tentacles indicate that there are pacemakers
controlling independent tentacle activity in
addition to the two principal pacemaker
systems. The tentacles synchronously flex
during concerts, indicating that the HP
system, when it fires, can drive the mechanisms controlling muscular contraction in
the tentacles.
CONDUCTING SYSTEMS IN THE STALK
Three, non-polarized conducting systems
have been identified in the stalk of Tubularia. Electrical potentials from two of the
three are shown in Figure 3. The very small
potentials are from a conducting system
termed the distal opener system (DOS) because activating it causes synchronous
aboral flexion (opening) of the distal
tentacles. The DOS conducts at about 15
cm/sec (19°C). The larger potentials are
from a conducting system termed the slow
system (SS). The SS conducts at about 6
cm/sec. The SS often fires repetitively to
supra-threshold stimuli; in Figure 3 it has
fired twice. The SS is very labile and can
only predictably be demonstrated in a fresh,
pre\iously unstimulated polyp. SS activity
has no known behavioral correlate, nor does
it appear to affect spontaneous electrical
activity in the distal polyp.
Although electrical correlates of its activity have not yet been recorded, the presence of a third conducting system in the
stalk can be inferred from the lact that
stimulation ol the pioxinul stalk ran trig-
PACF.MAKFR COORDINATION IN Tubulnria
S $ £
(Tl
W
10
0
05
10
487
The low sensitivity to triggering in the
first 0.2 sec after NP firing is presumably
due in part to a refractory period in the
NP system. The sensitivity pattern for NP
triggering by independent HP firing is
quite different from that found with stalk
stimulation. An HP is most likely to trigger
an NP if it comes long after the last NP,
that is, late in the NP cycle. This difference
suggests that different mechanisms are operative in NP triggering by stalk stimulation and by HP firing.
INTERVAL BETWEEN STIMULUS AND PRECEDING NP (SECS)
FIG. 4. The proportion of stalk stimuli which
triggered NP's as a function of the intervals between the stimuli and the preceding spontaneous
NP's. B is an expansion of the 0-1 sec portion of
A. Further explanation in text.
COMMUNICATION BETWEEN POLYPS
Often polyps can be found in a cluster
of Tubularia which appear to branch from
a common stalk. In some cases there is a
ger NP's in the polyp neck even if the stimu- partition of perisarc across the junction and
lus intensity is below threshold for the two hence no continuity of the inner coenosarc
recordable conducting systems. This third tissue. Such branching has presumably
conducting system is termed the triggering arisen through the settling and subsequent
system (TS). The TS conduction velocity, development of a larval Tubularia upon
determined from changes in the stimulus an existent stalk. In other cases, however,
to triggered NP interval with changes in there is coenosarc continuity at the juncthe position of the stimulating electrodes tion, the enteron canals in the stalks of
the two polyps are continuous, and the stalk
on the stalk, is about 17 cm/sec.
In a few polyps almost every stalk stimu- conducting systems of the two polyps are
lus of appropriate strength triggers the NP continuous across the junction. There is
system to fire; but with most polyps not some coordination between pacemaker sysall stimuli trigger NP's, and the probability tems of such connected polyps. This is
that a stimulus will trigger an NP depends most clearly seen for NP bursts. NP bursts
on when the stimulus is given with respect in two connected polyps on a Y stalk almost
to the last NP firing. The NP sensitivity always occur simultaneously (Fig. 5), and
to triggering at different times in the spon- only infrequently is there an NP burst in
taneous NP cycle is shown in Figure 4. just one of the two. There is also interThis figure is based on recordings of NP's action between single NP's in connected
from the necks of polyps made while the polyps; firing of an NP by one polyp somepolyp stalks were being stimulated regu- times triggers an NP in a connected polyp,
larly at one shock each 10 sec. In analyzing but interaction between single NP's is less
the records, the interval between each shock obvious than that for NP bursts.
and the preceding NP was measured, and
Communication between the NP systems
it was noted whether that stimulus did or of connected polyps appears to be mediated
did not trigger an NP. Only stimuli which through the TS in the stalk. Potentials of
followed single, spontaneous NP's are in- the sorts associated with activity in the
cluded in Figure 4; stimuli which followed other two conducting systems are not seen
triggered NP's or NP's of NP bursts have during inter-polyp triggering. The interval
been omitted. Figure 4 includes data between an NP in one polyp and its trigpooled from several polyps.
gered counterpart in a connected polyp is
A stalk stimulus is most likely to trigger usually about what should be expected from
an NP if it comes within a few seconds after the TS conduction velocity and the distance
NP firing, that is, early in the NP cycle. between the two polyps (a puzzling excep-
488
ROBERT K. JOSEPHSON
A
|OlmV
0.2 mV
ImV
•|lmV
30 sec
FIG. 5. A. XP's in two connected polyps. The occasional appearance of pahs of pulses in either
channel is a result of inter-polyp triggering, li. HP's from the same colony.
tion to this is discussed below). And the
rules for NP-triggering between connected
polyps are the same as those for triggering
NP's in a polyp by stalk stimulation. Firing of an NP in one polyp is most likely
to trigger an NP in a connected polyp if
the connected polyp has just fired an XP.
Triggered NP's are usually the second NP
of a distinct pair, and follow an NP in a
connected polyp by a short and reasonably
constant interval. Thus it appears that
each time a polyp spontaneously produces
an NP it also activates the TS system, and
this TS activity can trigger NP's in any
connected polyps which are in sensitive
portions of their own spontaneous cycles.
T h e interaction between polyps results in
the NP patterns of connected polyps being
less regular than those of isolated polyps.
T h e sensitivity pattern of the NP system
to triggering by TS activity results in there
being relatively little interaction between
single NP's in connected polyps, at least in
the small two-polyp colonies which ha\e
been im estimated. Most single NP's produced by a polyp do not occur during the
stiisithe jjLiiod of a connected JJ<)I\p. But
the sensitivity pattern does allow rather
effective communication during NP bursts.
Once a polyp fires during an NP burst of
a connected polyp, its sensitive period overlaps the next burst NP, and the polyps
continue for a while firing NP's together
but slightly out of step. If the polyp which
is initially the leader slows down, the other
polyp can take over and be the leader for
the remainder of the burst (Fig. 6). The
NP system of a polyp acts as though it were
joined to NP systems of connected polyps
through a peculiar sort of high pass filter,
such that it responds only occasionally to
single NP's in connected polyps but quite
regularly to the higher frequency NP bursts.
In some connected polyps, NP bursts are
occasionally recorded in which the delay
between corresponding burst-pulses in the
two polyps is far shorter than can be accounted for on the basis of TS conduction
time. The coordinating mechanism for
these bursts with short inter-polyp delav
is unknown. A possible explanation is that
during the short delay bursts the NP systems of both polyps are being driven
tinf>ugh the TS In pacemakers in the proxi-
PACEMAKER COORDINATION IN
489
Tubuhnia
4-t-
0.2 mV
0.1 mV
I sec
FIG. 6. An XP burst in two connected pol)ps. The clots above the upper channel mark the
onsets of NP's in the lower channel. Note the leadership change, the lower pol)p leading early
in the burst and following at the end of the burst.
nial stalk rather than the usual neck pacemakers. According to this explanation, the
time difference between correspondingpulses in each polyp would result from different conduction times between the two
polyp NP systems and the common driving
jjacemaker. If the common pacemaker were
equidistant from the two polyps, the interval between corresponding pulses could be
vanishingly small. From this hypothesis
changing leadership would not be expected
during short delay bursts, and in fact none
is seen.
The relation between HP's in connected
polyps is as would be predicted from the
loose coupling between the NP systems of
connected polyps and the loose coupling
between NP and HP systems within single
polyps. Single HP's or short HP bursts
are not coordinated between connected
polyps, while the longer HP bursts, those
that occur in conjunction with NP bursts,
are usually coincident in connected polyps.
The behavioral consequences of the interpolyp communication arc again as would
be predicted. Weak concerts, those that
occur with independent HP activity, are
not synchronous in connected polyps; while
vigorous concerts, those that occur when
the HP system is driven by the NP system
during an NP burst, are generally synchronous in connected polyps. Neck contraction leading to tidal exchange, which is
associated with vigorous concerts, is thus
also usually synchronous in connected
polyps.
A functional significance for the coordination between polyps can be suggested if
it is assumed that the function of concerts
with neck contraction is to transfer fluid
and partially digested food between the
two enteron chambers of a polyp. Were
neck contractions of connected polyps not
coordinated, sometimes one polyp would
contract its neck while a connected polyp
would be relaxing following such contraction. In this case, neck contraction would
force fluid down the stalk toward the relaxing polyp rather than distally into the
oral enteron chamber, and there would be
no tidal exchange between the two enteron
chambers of the contracting polyp. As it
is, neck contractions are synchronized
throughout a colony, the pressure in the
connected neck and stalk compartments
must increase throughout the colony during
concerts, and the passage of fluid into the
oral chambers of polyps throughout the
colony is facilitated.
CONCLUSION
The question raised early in this paper
was how are the many potential pacemakers
of a coelenterate coordinated to give unified behavior. The beginning of an answer
can be given for the hydroid Tubularin,
and a quite similar picture has come from
recent work on Hydra (McCullough, 1965).
Pacemakers are primarily organized in
groups within which there is tight coupling.
These groups are here termed pacemaker
systems. The different pacemaker systems
of a polyp are loosely coupled together so
that their activities are to some degree coordinated. Figure 7 shows some of the
490
ROBERT K. JOSE.PHSON
distal tentac'e openers
Foundation (No. G23822 R) and the
National Institute of Neurological Diseases and Blindness, U.S.P.H.S. (No. NB
05263-01).
REFERENCES
{ggggg
neck musculature
conducting system
o
pacemaker system
a
muscle group
FIG. 7. Some of the interactions between pacemaker systems, stalk conducting systems, and effectors found in Tubularia.
interactions between pacemaker systems,
stalk conducting systems, and effectors
which have been so far identified in Tubularia. The pacemaker systems of individuals on a colony are loosely coupled, so that
some activities of connected polyps are coordinated in a functionally meaningful
way. The quantification of the interactions
between loosely coupled pacemaker systems
and the elucidation of the mechanisms of
this interaction are challenging problems
for present and future students of coelenterate behavior.
ACKNOWLEDGMENT
Original investigations have been supported by grants from the National Science
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