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Central circuitry in the jellyfish Aglantha digitale IV. Pathways coordinating feeding behaviour

G. O. Mackie^1,*, R. M. Marx¹ and R. W. Meech²

¹ Biology Department, University of Victoria, Victoria, British Columbia, V8W 3N5, Canada
² Department of Physiology, University Walk, Bristol BS8 1TD, UK

View larger version (38K): [in a new window]   Fig. 1. Feeding in Aglantha digitale. (A) A specimen floating upside down in feeding posture, tentacles extended (photograph by Claus Nielsen). (B) Cyclical sink-fishing of Aglantha. The animal sinks passively, tentacles extended (i); at the bottom of the cycle swimming ensues (ii); the animal swims upwards with tentacles contracted (iii); then it stops swimming, turns over and starts sinking again (after Mackie, 1980).

View larger version (38K): [in a new window]   Fig. 2. Conduction pathways involved in feeding in Aglantha digitale. (A) Vertical section, apex of bell upwards, showing general structural relationships and distribution of neural elements having FMRFamide-like immunoreactivity (after Mackie et al., 1985). (B) Diagram of a transverse section through a subumbrellar radial strand showing the relationship between the radial canal, the small axon bundle and the giant axon.

View larger version (87K): [in a new window]   Fig. 3. Food capture, ingestion and digestion. (A) Ciliary beating drives water orally past the extended tentacles (arrows) and causes the animal to glide slowly through the water, bringing the tentacles into contact with a copepod. (B) Tentacular contraction and flexion brings the prey to the margin while the manubrium points across to it with flared lips. (C) Peduncle (p) and manubrium (m) of an unfed animal at rest. (D) Lateral flexion (pointing) to a site where food is held by the tentacles. (E,F) Changes in the diameter of the manubrium during peristalsis in a fed animal. (G) Lip flaring evoked by a shock from a stimulating electrode (s) on a peduncular radial canal.

View larger version (22K): [in a new window]   Fig. 4. Analysis of pointing pathways. (A) The manubrium (m) is at rest. (B) It points to a stimulus (s) located at the junction of a radial strand with the margin. (C) The stimulus was delivered interradially. (D) After cutting all radial strands, stimuli cease to evoke pointing. (E) After cutting six adjacent strands, stimuli cause pointing to the closest intact radius. (F) After cutting five adjacent strands, leaving two strands equidistant from the stimulus, pointing may be to either of the two equidistant radii.

View larger version (23K): [in a new window]   Fig. 5. Inhibition of rhythmic swimming by manubrial stimulation. (A) Portions of a chart recording from one animal in which swims were recorded electromyographically using a suction pipette attached to the velum. Each swim was registered as a large downward deflection; shocks to the manubrium appear as small stimulus artefacts (downward in top series of traces, upward in bottom trace). Stimulus pulse trains were delivered at 3 Hz. The top traces show that a stimulus train containing two or more pulses caused a perceptible increase in the interval between successive swims. In the bottom trace, inhibition outlasted the 10.5 s stimulus by at least 6 s. (The swim deflections have been enhanced to improve clarity). (B) Relationship between the stimulus duration and the time interval from the end of the stimulus to the first post-stimulus swim; each data point was normalized by dividing it by the average pre-stimulus swim interval (N=3). The line drawn through the points was fitted by linear regression (slope, 1.3 of control swim interval/second of stimulus; y-intercept, 0.40 of control swim interval). (C) Relationship between the stimulus duration and the time interval between the first and second post-stimulus swim; data points were normalized as above. The line drawn through the points was fitted by linear regression (slope, 0.06 of control swim interval/second of stimulus; y-intercept, taken as 1.0 of control swim interval).

View larger version (14K): [in a new window]   Fig. 6. External recording of propagated events evoked by radial strand stimulation. (A) A single shock (asterisk) evoked three propagated events: the first, G, (artificially enhanced for improved clarity) corresponds to the overshooting action potential in the motor giant axon; the second, E, corresponds to a propagating impulse in the endodermal epithelial conduction pathway; the third, F, corresponds to propagating impulses in the bundle of small-axons. Inset: experimental arrangement with stimulating (S) and recording (R) electrodes located on an intact radial strand (RS), subumbrella surface upwards. The stimulating electrode is near the velum (v). The dotted lines represent tissues containing one or more radial and circular conduction pathways as described in the text. (B) Recording showing E and F events in a peduncular radial strand close to its junction with the manubrium. Average of three responses evoked by single stimuli (asterisk) delivered to the same strand approximately 5 mm away.

View larger version (11K): [in a new window]   Fig. 7. Circular propagation of E impulses at the margin. (A) Representation of a quartered, splayed preparation with the stimulating electrode (S) located on a radial strand in the peduncle (p) and the recording electrode (R1) on another peduncular radial strand. A second recording electrode (R2) was located on the stimulated strand close to the margin. This strand was cut between S and R2 at site a. A second cut at site b went through the ectoderm only, leaving the radial canal intact. RS, radial strand; v, velum; m, manubrium. The dotted lines represent tissues containing one or more radial and circular conduction pathways as described in the text. (B) A stimulus (asterisk) evoked both E and F events at R1 although only the E event arrived at R2. Thus the E impulse must propagate down one radial canal, around the margin and up other canals.

View larger version (9K): [in a new window]   Fig. 8. E pulses evoked by crushed amphipod juice applied to the manubrium. (A) Amphipod juice was applied to the manubrium at the time indicated by the arrow. A train of E pulses was evoked, recorded with electrodes on the manubrium itself and on the marginal nerve ring. (B) A single E event on an expanded time scale. All E events in the train appeared in the manubrium first and were conducted to the margin.

View larger version (9K): [in a new window]   Fig. 9. Circular propagation of E and F events at the margin. (A) In a quartered, splayed preparation a stimulating electrode (S) was placed on one radial strand while a recording electrode (R) was placed on another near its junction with the manubrium (m). A cut through the radial strand (RS) at site a blocked that pathway to the manubrium. The dotted lines represent tissues containing one or more radial and circular conduction pathways as described in the text. p, peduncle; v, velum. (B) Upper trace (B1) shows propagation of both E and F events to the manubrium via a route that includes a circular component at the margin. Lower trace (B2) shows blockage of E events by cutting the circular (ring) canal at site b. This cut also went through the inner nerve ring, showing that F impulses can propagate circularly in the outer nerve ring.

View larger version (13K): [in a new window]   Fig. 10. Evocation of F events by food juices and their propagation to the manubrium. (A) In a quartered, splayed preparation recording electrodes (R) were placed on two radial strands within the peduncle equidistant from a stimulating electrode (S) on a third radial strand in a flap of body wall. Tentacles (T) were left intact. The dotted lines represent tissues containing one or more radial and circular conduction pathways as described in the text. (B) A control shock was used to establish the characteristic waveforms of E and F events so that they could be recognized in subsequent experiments. Differences in waveform at the two recording sites were attributed to differences in tissue volume and composition drawn into the suction pipette. (C) After application of food juice to the margin on the left flap, trains of F pulses were recorded at both recording electrodes, appearing first on the left electrode.

View larger version (145K): [in a new window]   Fig. 11. Transmission electron micrographs of radial nerve pathways. (A) Transverse section across a radial strand as in Fig. 6. The scale bar lies within the lumen of the radial canal. The inset shows a gap junction in the endoderm of the radial canal. (B) Enlarged portion of A to show small axon bundle (sab). (C) Transverse section through a longitudinal muscle bundle in the ectoderm of the manubrium. ec, ectoderm; en, endoderm; ga, giant axon; lmb, longitudinal muscle bundle; mes, mesogloea; sab, small axon bundle; sm striated swimming muscle.

View larger version (102K): [in a new window]   Fig. 12. Confocal overlays showing immunolabelled radial nerve pathways. Nerves showing FMRFamide-like immunoreactivity (FaIR) are green, other nerves red (antitubulin). (A) Subumbrellar radial strand showing the giant axon and the small axon bundle. (B) Peduncular radial strand showing small axon bundle and non-FaIR elements. (C) Manubrium, showing small axon bundle whose axons are now spread out, and underlying, non-FaIR plexus.

View larger version (65K): [in a new window]   Fig. 13. Nerves associated with the outer nerve ring showing FMRFamide-like immunoreactivity (FaIR). (A) Outer nerve ring (onr) with tracts (t) leading to tentacles. (B) Monopolar sensory cells with their neurites running into the outer nerve ring. The inset shows sensory cilia (arrow) at the tips of these cells.

View larger version (103K): [in a new window]   Fig. 14. Nerves and muscles in the manubrium. Nerves are labelled with anti-FMRFamide, muscles with phalloidin. (A) One of the four manubrial lips (l) with FMRFamide-like immunoreactivity (FaIR) in a nerve tract (t) running aborally. This tract becomes the small axon bundle that goes to the margin. (B) Sensory cells at the lip edge. (C) Longitudinal (horizontal) and circular myofibrils in the wall of the manubrium. The longitudinal muscles are concentrated into longitudinal muscle bands (lmb) that underlie the FaIR nerve tracts shown in A.

View larger version (27K): [in a new window]   Fig. 15. The principal pathways involved in locomotion, the control of tentacle contractions and food manipulation. Three of the eight longitudinal muscle bands lying in the wall of the peduncle and manubrium are shown. The diagram is based on Mackie and Meech, (2000), but includes two new pathways, the flexion system (F) that mediates the pointing responses seen during feeding, and the endodermal, epithelial system (EN) that mediates lip flaring and swimming inhibition (via the swimming pacemakers system, P). The exumbrellar epithelial conduction system (EX) also inhibits swimming, but impulses do not pass between it and EN, so the two are shown as functionally separate systems. The cells in these epithelial pathways are coupled by gap junctions, shown as incomplete membrane partitions, and conduction in them is unpolarized. Impulses spread in all directions in EX while in EN they spread laterally along the ring canal and up or down all eight radial canals (not shown). EX is not the subject of this paper and in the text `E' simply refers to EN. MG, motor giant axon; RG, ring giant axon; TF, tentacle nerves that feed into the F system. The experimental basis for other components of the nervous system, the carrier system (C), the nitric oxide pathway (NO), the relay system (R), the rootlet interneurone system (RI) and the tentacle systems (TG, TS), are given in Mackie and Meech (1995a,b, 2000).