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Nerve Net Pacemakers and Phases of Behaviour in the Sea Anemone Calliactis Parasitica

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Nerve Net Pacemakers and Phases of Behaviour in the Sea Anemone Calliactis Parasitica J. exp. Biol. 104, 231-246 (1983) 231 Erinted in Great Britain © The Company of Biologists Limited 1983 NERVE NET PACEMAKERS AND PHASES OF BEHAVIOUR IN THE SEA ANEMONE CALLIACTIS PARASITICA BY IAN D. McFARLANE Department of Zoology, University of Hull, Hull HU6 7RX (Received 9 November 1982 —Accepted 31 January 1983) SUMMARY Bursts of through-conducting nerve net (TCNN) pulses, 20—45 min apart, were recorded from Calliactis attached to shells. Within 15—25 min of the anemones being detached the TCNN bursts suddenly became more frequent (only 4—11 min apart). Such bursts continued for several hours if re-attachment was prevented. In an attached anemone simultaneous electrical stimulation of the TCNN and ectodermal slow system (SSI) with 20-30 shocks at one every 5 s also led to more frequent TCNN bursts, whether or not detachment took place. If, however, the anemone remained attached, the intervals between bursts returned to the normal resting dura- tion after about 90 min. In all cases the decay of the 4—11 min interval TCNN bursts involved a reduction in pulse number, not an increase in burst interval. Partial activation of the TCNN pacemakers followed stimulation of the SSI alone. It is suggested that in sea anemones the change from one behavioural phase to another is associated with a change in the patterned output of nerve net pacemakers. INTRODUCTION The most obvious behavioural response of a sea anemone is that it contracts when touched. These fast contractions are triggered by a through-conducting nerve net (TCNN), (e.g. Pantin, 1935a; Josephson, 1966; Pickens, 1969). Other more com- plex, but still obvious, behavioural responses such as swimming in Stomphia coccinea and shell climbing in Stomphia and Calliactis parasitica involve additional conduct- ing systems, the slow systems SSI and SS2 (Lawn, 1976a; Lawn& McFarlane, 1976; McFarlane, 1976). These complex behaviour patterns are also evoked by external stimuli. Far less noticeable are the slow, rhythmical, spontaneous shape changes shown by all species of sea anemone. These contractions are important as they may be the basic primitive form of neuromuscular activity in anemones (Ross, 1957) and components of these rhythms are incorporated into the complex behaviour patterns. Slow contrac- tions have received less attention than the fast reflexes because the time scale is so much longer. Techniques such as kymograph or time-lapse cine' recording have shown that a particular sequence of muscular contractions (a phase) may be repeated for words: Pacemakers, nerve net, sea anemone. 232 I. D. MCFARLANE several hours but even a brief stimulus can trigger a new phase that may persist several more hours (Batham & Pantin, 1950). The responses to stimuli may v according to the phase the animal is in. The only neurophysiological analysis of the coordination of slow contractions to date has shown that bursts of TCNN pulses in half-animal preparations of Calliactis parasitica are followed by a sequence of parietal and circular muscle contractions (McFarlane, 1974a). In this paper, neurophysiological evidence is presented for a change in behavioural phase in intact Calliactis. It is shown that detachment of the pedal disc leads to a long-lasting activation of TCNN bursts. MATERIALS AND METHODS Calliactis parasitica, attached to Buccinum shells, were supplied by the Plymouth Marine Laboratory and kept at 15-19 °C. They were starved for a week before use. Animals were detached from the shells by being gently pulled. The pedal disc of a detached anemone will quickly re-attach to any object it touches, so to prevent this the anemone was suspended free of such contact by a large diameter suction electrode attached to the mid-column region. Recordings were made with polyethylene suction electrodes attached to tentacles. To minimize mechanical stimulation, only one recording electrode was used. This made pulse identification difficult (previous studies always compared pulses at two electrodes) and required selection of in- dividuals where all pulse types were clearly recognizable. Electrodes sometimes remained attached for several hours but usually there was a gradual deterioration in signal size, presumably due to tissue damage, after about 1 h. Consequently the electrode had to be moved periodically and this caused a short break in the record as a few minutes must elapse before pulses can again be confidently identified. Pulse identification was facilitated by connecting the pre-amplifier output to the oscilloscope via a Datalab DL902 transient recorder in the roll mode with a sample rate of 1 KHz. This gave a 2s period in which to identify each pulse. When a pulse was seen a contact was made which deflected a slow moving plotter pen. Different pulse types were indicated by different sized deflections. SSI pulses are relatively large (around 10-30/iV) and easily recognized. TCNN pulses have a distinctive shape but during a TCNN burst they usually become smaller and some may have been missed. SS2 pulses are small (often only 5 fiV) and are often lost in background activity (Fig. 1). The results are based upon more than 160h of recording from 10 anemones. RESULTS Detachment causes frequent nerve net bursts: a pre-settling phase The spontaneous electrical activity of an anemone attached to a shell could gener- ally be predicted by the anemone's appearance. If it was 'alert' (i.e. well expanded with tentacles outstretched) a typical recording was as shown in Fig. 2A. This record shows the distribution of electrical activity in the three conducting systems (TCNN, SSI and SS2). For this, and subsequent Figures, the activities of the systems are sum- marized in Table 1. Nerve net pacemakers in Calliactis 233 Fig. 1. Single suction electrode recordings from a tentacle of Calliactis. The first deflection in each record is the stimulus artefact. (A) Single shock (40 V, lms) to base of column elicits through- conducting nerve net (TCNN) pulse (•), probably a muscle action potential, an ectodermal slow conduction system (SSI) pulse (A), and an endodermal slow conduction system (SS2) pulse (A). (B) Same size shock, 30s later, evokes same pulses but the SS2 pulse is lost in a burst of complex pulses. Such complex activity is usually localized and associated with a twitch contraction of the tentacle. The SS2 pulse often has an amplitude of only 5 fiV and many may be missed during continuous monitoring of spontaneous activity, particularly during and just after TCNN bursts, when complex activity is common. Time scale: 500 ms. SSI pulses were rarely detected in an attached, unstimulated anemone. Generally SS2 activity was at a low frequency — about one pulse every 25 s. There were also occasional short bursts of TCNN activity, usually 20-45 min apart and rarely contain- ing more than seven pulses. The pulse frequency in the bursts was about one pulse every 4 s. A small, slow sphincter muscle contraction was visible after most bursts. The pattern of electrical activity recorded from an unstimulated, attached anemone will be termed 'resting phase' activity in this paper. Occasionally, anemones looked 'limp' with flaccid tentacles. Recordings then showed a much higher level of SS2 activity — around one pulse every 8 s. TCNN bursts were rarely detected (less than 1 h"1). This is atypical and such anemones were not used in the experiments described below. Electrical stimulation of the SS2 can cause a similar loss of muscle tone (McFarlane, 1976). When an anemone was detached by being pulled off the shell there was a marked change in TCNN activity. After a delay of 15—20 min, the widely-spaced TCNN bursts seen in the attached anemone were suddenly replaced by more frequent bursts, often only 5 min apart (Fig. 2B) and rarely as much as 11 min apart (Fig. 2C). The bursts contained more pulses than resting phase bursts; containing 9-12 pulses on average in different anemones (Table 1). A wide range of pulse intervals was seen n the bursts (3—6 s). There was rarely any noticeable change in the overall level I. D. MCFARLANE I 1 I I I I I L J I 1 I I I 1 I I 1 I: -SS2 TCNN M ir ,, , ,1, KLIILILL i in i ft I ft .11 L.llllllll , JJUI i c 1 i i n i n i i i—i i mi 1 1 1 1 n 1 1 . 1, . .-. Illllll Illlll.L.m r—in i I 1 1 1 1 n n i 1 | 1 11 in m flr- 1 , i • I • n. | i I, 1 i 1 | lillUJJLI1 _J L Fig. 2. Electrical activity patterns of attached and detached Calhactis. In each section the records are continuous and each line of the record covers 260 s. Pulses are shown by different-sized deflections of the plotter pen: TCNN > SSI > SS2. Periods of complex activity, sufficiently large to mask SS2 pulses, are shown by long-duration marks at SS2 amplitude. The long-duration marks at TCNN amplitude show where fast contractions occurred. A break in the record signifies a period when electrode contact was lost. (A) Resting phase: activity in an anemone attached to a shell. Two short- duration TCNN bursts are shown. The spontaneous activity of the resting phase is characterized by widely-spaced TCNN bursts and regular firing of the SS2. (B) Pre-settlement phase: activity in an anemone pulled off a shell 10 mm before the start of the record. Note the frequent TCNN bursts that in this case start 17min after detachment. (C) Another detached anemone, showing TCNN bursts some 11 min apart. This record starts 20min after detachment. Time scale: 1 min. of SS2 activity but there were always more SSI pulses (Table 1), probably caused by mechanical stimulation of the detached pedal disc margin (McFarlane, 1976).
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