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First published online October 17, 2008
Journal of Experimental Biology 211, 3467-3477 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.018952

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Control of swimming in the hydrozoan jellyfish Aequorea victoria: subumbrellar organization and local inhibition

Richard A. Satterlie

Department of Biology and Marine Biology and Center for Marine Science, University of North Carolina, Wilmington, NC 28409, USA

View larger version (13K): [in this window] [in a new window]   Fig. 1. Diagram of an intact medusa and a `reduced preparation' consisting of three adjacent segments (viewed from the subumbrellar side). S, stomach; V, velum; G, gonad; SS, subumbrellar segment; RC, radial canal; MC, marginal canal; INR, inner nerve ring.

View larger version (142K): [in this window] [in a new window]   Fig. 2. Ultrastructure of the ectodermal muscle in a subumbrellar segment. Both A and B are radial sections, with the radial muscle (RM) cut longitudinally and the circular (swim) muscle (CM) in cross section. Note that the radial muscle cells are superficial to the circular muscle. In both A and B, neurites (N) are present, and contain dense core vesicles. The neurite in A is superficial to the radial muscle, whereas the neurite in B is between the radial and circular muscle processes. In both panels, the subumbrellar cavity is to the top left.

View larger version (91K): [in this window] [in a new window]   Fig. 3. Ultrastructure of the ectodermal muscle in a subumbrellar segment. In A, the circular muscle (CM) is cut longitudinally to show its striated nature. It also abuts the mesoglea (M). The radial muscle (RM) is cut in cross section, and shows a lack of regular organization of thick and thin filaments. In B, the end-to-end junction of two circular muscle cells show a desmosome (D) adjacent to a gap junction (GJ).

View larger version (127K): [in this window] [in a new window]   Fig. 4. Intercellular junctions between muscle cells. (A) Circular muscle cells (CM) have laterally positioned gap junctions (GJ) with other circular muscle cells. (B) Radial muscle (RM) cells have gap junctions (GJ) near the apical surface of the cells (they are also present deeper in the ectoderm – not shown).

View larger version (185K): [in this window] [in a new window]   Fig. 5. In cross section, the striated circular muscle cells have an ordered arrangement of thick and thin filaments.

View larger version (4K): [in this window] [in a new window]   Fig. 6. Intracellular recordings from subumbrellar muscle cells approximately 2–2.5 mm from the nerve ring. (A) A double recording from a radial muscle cell (top trace) and a circular muscle cell (bottom trace). An initial spontaneous swim produced a full action potential (with initial junctional potential) in the circular muscle cell, but only a `field effect' in the radial cell. When electrical stimuli were delivered to the segment with a suction electrode, both a junctional potential (circular muscle cell) and an action potential (radial muscle cell) were triggered. The small `blip' before each event is the stimulus artifact. (B) Variability in the shape and amplitude of circular muscle action potentials. Each event is initiated by a single junctional potential. All were spontaneously generated in a reduced preparation that showed varying contractions. This recording was from a small medusa, 3 cm bell diameter, so the action potentials are of a shorter duration. (C) Complex electrical event from a circular muscle cell in a segment in which a radial response was triggered by a mechanical stimulus (light touch with a glass micropipette electrode) delivered to the velum in the region of that segment. The contraction in that segment was weaker than in the adjacent segments on each side.

View larger version (7K): [in this window] [in a new window]   Fig. 7. Dual recording from a pair of circular muscle cells within 3 mm of the inner nerve ring. All muscle action potentials were spontaneous. The break in the traces represents a time break in the record. In the first segment, a single hyperpolarizing current (approximately 1 nA) was injected into the cell represented by the lower trace. The small hyperpolarization in the top trace (arrow) indicates the cells were electrically coupled. In the second segment, two current pulses were injected into the cell represented by the top trace. Again, small hyperpolarizations in the other cell (arrows) demonstrated similar coupling in the opposite direction.

View larger version (63K): [in this window] [in a new window]   Fig. 8. (A) Lucifer Yellow fill of a circular muscle approximately one-third of the way from the margin in a subumbrellar segment, showing widespread dye coupling. The injected cell was in the middle of the bright spot. The small bright dots in the filled cells are nuclei. (B) Lucifer Yellow fill of a radial muscle cell roughly in the middle of a subumbrellar segment. The dye spread to the surface cells (radial muscle cells) throughout the epithelial tissue but not the underlying circular muscle cells. Again, the nuclei show up as bright dots. The scale bar applies to both A and B.

View larger version (5K): [in this window] [in a new window]   Fig. 9. Sequential experiment in which a single electrode was placed in a circular muscle cell (at the site marked R in the diagram), and a stimulating suction electrode was moved to the sites marked A, B and C. For trace A, the stimulus was delivered in the same segment as the recording site (stimulus site A), and a junctional potential was triggered with a short latency. Three spontaneous action potentials were also recorded, and each was initiated by a junctional potential of similar size to those electrically stimulated (note the slight inflection on the rising phase of the action potentials). When the stimulating electrode was moved over one segment (stimulus site B and trace B), junctional potentials were triggered by three of the four stimuli, but with a longer latency than in trace A. Following the second and fourth stimuli, weak contractions were initiated. The electrode was then moved over one more segment (stimulus site C and trace C). Electrical stimuli sufficient to produce weak contractions in the stimulated segment did not initiate junctional potentials in the recorded segment (two segments over). A few junctional potentials were recorded during these experiments (one is shown in this trace), however, they showed no regular relationship to imposed stimuli. It appears these are spontaneous events. Delivery of stimuli is marked by the stimulus artifacts (arrows). The recording site was 2.5 mm from the top of the nerve ring.

View larger version (127K): [in this window] [in a new window]   Fig. 10. FMRFamide immunoreactivity in a subumbrellar segment of Aequorea shows a diffuse nerve net with a definite oral–aboral orientation of neurites (direction indicated by arrow). The region was about one-third of the segment length up from the margin.

View larger version (144K): [in this window] [in a new window]   Fig. 11. Double-label immunohistochemistry using -tubulin (green) and FMRFamide (red) antibodies. In A, a dual filter shows the two colours together. The small arrows indicate FMRFamide cell bodies and neurites, and the large arrows indicate some of the tubulin-stained cell bodies. B and C are from identical areas (no change in focus) with a change from a FITC filter (B) to a TRITC filter (C). Note the neuron indicated by the arrow in B is not present in C indicating it was immunoreactive to the tubulin antibody, but not to FMRFamide antibody. This suggests the presence of two distinct neuronal types in the subumbrellar segments of Aequorea.

View larger version (5K): [in this window] [in a new window]   Fig. 12. Double recordings from a swim motor neuron in the inner nerve ring (top traces of each pair) and a circular muscle cell approximately 0.5 mm from the neuron recording site (bottom traces). In A, a spontaneous radial response occurred between the first and second swim. Note the inhibition of neuronal action potential burst and the smaller muscle event with a slow rise time. In the third swim, the preparation had partially recovered from the inhibition, and it was fully recovered by the fourth swim. (B) Another radial response from the same preparation produced total inhibition of the neuronal burst in the second swim (which occurs after a long delay), a single neuronal spike in the third swim, and full recovery on the fourth. Note the changes in the muscle action potentials during the inhibition.

View larger version (24K): [in this window] [in a new window]   Fig. 13. Schematic of the neuromuscular organization of the subumbrella of Aequorea. The arrows represent excitatory chemical connections and the bars, inhibitory connections. The resistor symbols represent electrical coupling, as do the dotted lines within the radial and circular muscle boxes. FMRF, FMRFamide-immunoreactive nerve net of the subumbrella; MNN, motor nerve net of the subumbrella;???, unknown pathway responsible for activation of the FMRFamide-immunoreactive nerve net following mechanical stimulation of the margin. The circular and radial muscle sheets refer to the musculature from a single subumbrellar segment.

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