Locomotion and neuromuscular system of Aglantha digitale

Aglantha digitale swims in two ways: a slow rhythmical swim typical of hydromedusae in general and a sudden rapid movement that appears to be an escape response. The swimming musculature is an extremely well developed striated circular muscle layer that possesses a sarcoplasmic reticulum. The nervous system of this species can be divided into three units: an inner nerve ring and an outer nerve ring, which are joined by unusually large transmesogleal pathways, a group of giant axons that extends over the surface of the swimming muscle, and the radial canal. Well developed ciliated sensory cells are located on the exumbrellar surface of the margin. Consideration of these properties of the organisation of this species suggests that normal slow swimming is controlled by a mechanism similar to that found in other medusae, while the escape response is the result of the action of the giant axons.     

Nerves in the endodermal canals of hydromedusae and their role in swimming inhibition

N eoturris breviconis (Anthomedusae) has a nerve plexus in the walls of its endodermal canals. The plexus is distinct from the ectodermal nerve plexuses supplying the radial and circular muscles in the ectoderm and no connections have been observed between them. Stimulation of the endodermal plexus evokes electrical events recorded extracellularly as “E” potentials. These propagate through all areas where the plexus has been shown by immunohistology to exist and nowhere else. When Neoturris is ingesting food, trains of “E” potentials propagate down the radial canals to the margin and cause inhibition of swimming. This response is distinct from the inhibition of swimming associated with contractions of the radial muscles but both may play a part in feeding and involve chemoreceptors. Preliminary observations suggest that the “E” system occurs in other medusae including Aglantha digitale (Trachymedusae) where the conduction pathway was previously thought to be an excitable epithelium.     

Control of swimming in the hydrozoan jellyfish Aequorea aequorea: direct activation of the subumbrella

The epithelial cells that overlie the inner nerve ring of the hydrozoan jellyfish Aequorea aequorea were investigated ultrastructurally and electrophysiologically. The structurally unspecialized epithelial cells are interconnected by gap junctions and are electrically active during swimming as a single, long-duration action potential was recorded during each swim contraction. Intercellular electrical- and dye-coupling was demonstrated within the epithelial region extending into the velum and subumbrellar regions. Excitatory post-synaptic potentials were recorded from epithelial cells following swim motorneuron spikes with a short latency. Psps were up to 60 mV in amplitude and, when triggered in bursts, showed summation provided the interpulse interval was less than 25-35 ms. The initial gap in each of a series of bursts showed facilitation with the first few swim contractions following a period of inactivity. In actively swimming medusae, psp amplitude was relatively constant. The reversal potential for epithelial psp was estimated at between 0 and +20 mV. Spontaneous psps spread throughout the epithelial region electronically, but the amplitude decrease with conducting distance was less than that for current pulses injected into individual epithelial cells. This presumably represents the effect of widespread synaptic activation of epithelial cells via multiple input sites throughout the inner nerve ring as opposed to point-source input in current injection experiments. During a radial response, action potential amplitude was decreased and rise time increased due to decremental conduction through the inhibited region. It is postulated that conduction of a full action potential requires that electrotonic current spread from adjacent, active epithelial cells occur in synchrony with synaptic input from swim motoneurons.     

Effects of site of tactile stimulation on the escape swimming responses of hatchling Xenopus laevis embryos

Hatchling Xenopus laevis embryos usually swim when the skin is touched with a fine hair. Less common are small, local V-flexions and more general C-flexions. Simple flexions or the initial flexion at the start of swimming occur predominantly on the opposite side to the stimulus to direct the animal away from the stimulus. Strokes to the midline lead to random sidedness of responses.
The reliability of the sidedness of flexions and the first flexions of swimming decreases the more rostrally the stimuli are given. The range of directions of swimming paths are larger with more rostral stimuli so responses to head stimuli are unpredictable in direction.
In animals immobilized in α-bungarotoxin, strokes to the skin produce electrically recorded motor output which corresponds to: V-flexions, C-flexions and swimming. Fictive activity generally starts on the side opposite to the stimulus. The fictive responses suggest that the three basic behaviour patterns observed can be generated entirely within the central nervous system without any sensory feedback.
We discuss possible mechanisms for the generation of 'protean' responses to head stimulation which are unpredictable in direction.     

Microanatomy of the subumbrellar motor innervation inAglantha digitale (Hydromedusae: Trachylina)

Summary The hydrozoan medusaAglantha digitale (Müller 1776) has eight syncytical giant motor axons, up to 40 m in diameter, running from the margin, up the inside of the bell towards the apex. Giant motor axons injected with Lucifer Yellow CH are connected with lateral neurons running circumferentially across the subumbrellar muscle. These processes fill with the dye. Bundles of 20 to 50 small dye-coupled neurons extend circumferentially along the margin for up to 0.85mm. Giant motor axons injected with horseradish peroxidase divide into a few short branches on entering the inner nerve ring. Here the giant motor axon forms both chemical synapses and gap junctions with neurons that also send their axons into the inner nerve ring. In this region the inner and outer nerve ringe are connected by axons passing through openings in the intervening mesoglea.     

Properties of central motor neurons exciting locomotory cilia inTritonia diomedea

Summary A pair of large, identifiable neurons (Pd 21), one in each pedal ganglion, can excite previously inactive locomotory cilia on the sole of the foot ofTritonia diomedea (Audesirk, 1978; Fig. 3). These neurons exert their effect via axons which innervate the foot and are probably central motor neurons for pedal cilia. IntactTritonia are stimulated to crawl by the application of 1.5 M NaCl to the tail, and conversely usually stop crawling when the chemosensitive oral veil is touched with food (sea whip,Virgularia sp.). The Pd 21 neurons are excited by 1.5 M NaCl applied externally to the tail, and are inhibited by sea whip touch to the oral veil (Figs. 4 and 5). When aTritonia performs its escape swim, the cilia move strongly, and the Pd 21 neurons fire bursts of spikes in phase with dorsal flexions (Figs. 6 and 7). After a swim, aTritonia rapidly crawls along the substrate; during this time the spiking rate of the Pd 21s is greatly accelerated. Interneurons thought to drive swim bursts produce monosynaptic EPSPs in the Pd 21s (Fig. 8). The Pd 21s are coordinated in their spike activity by synaptic activity which is synchronous in the two neurons regardless of the site of external stimulation, and by electrical coupling between the two cells via axons in a pedal commissure (Figs. 9 and 10). The coupling coefficient for passively conducted potentials is quite high, about 0.15, despite an axon 8 to 12 mm long separating the two cells.Abbreviations BPSP biphasic postsynaptic potential - SW sea water     

The Tentacle Cilia of Aglantha digitale (Hydrozoa: Trachylina) and their Control

The tentacles of Aglantha have ciliary bands along the sides. Metachronal waves pass along these bands. The strong ciliary currents produced propel water past the tentacles, increasing the probability of prey capture. The ciliated cells are unusual in having many (up to about 500) cilia per cell, where most cnidarian ciliated cells have only one. The cells are also peculiar in containing numerous axonemes without membrane coverings, lying loose in the cytoplasm. Tentacles show independent, rhythmic, slow flexions in the oral direction and groups of tentacles show coordinated, slow flexions as part of a regularly repeated fishing cycle. In both cases, these slow, graded movements are mediated by a slowly conducting system, probably the network of small neurons present in the ectoderm, and are accompanied by ciliary arrests. Much faster, more powerful, coordinated contractions of the tentacles occur in the context of escape behaviour; these are mediated by giant axons which run down the tentacles and are also accompanied by ciliary arrest. Ciliary and muscle effectors evidently share a common motor innervation. Electron microscopy shows that the giant and non-giant nerves both synapse with muscle cells. The latter are joined to the ciliated cells by gap junctions, and it is suggested that whenever the muscles are excited depolarizations spread to the ciliated cells through the gap junctions and cause ciliary arrests. Neuronal control of ciliary activity has not previously been reported in the Hydrozoa.     

Central generation of swimming activity in the hydrozoan jellyfish Aequorea aequorea

Swimming in Aequorea is controlled by a network of electrically coupled neurons (swim motorneurons) located in the inner nerve ring. The network is made up of the largest neurons in the ring, up to 22 microns in diameter. Intracellular recordings from swim motorneurons reveal slow membrane potential oscillations and a superimposed barrage of synaptic "noise." The synaptic noise, but not the slow oscillations, is eliminated in seawater containing an elevated Mg++ concentration. The swim motorneurons produce a rapid burst of two to eight action potentials preceding each contraction of the subumbrella. Spontaneous bursting persists in high-Mg++ seawater. Injected ramp currents indicated a "bursty" character of the swim motorneurons as suprathreshold depolarizations produced repetitive bursting with an increasing burst frequency with increased depolarization. Hyperpolarizing currents locally blocked spiking in swim motorneurons. Intercellular coupling was demonstrated with Lucifer Yellow injection and dual electrode recordings. In dye fills, only the large neurons of the inner nerve ring were dye-coupled. Two pieces of evidence suggest that swim motorneurons activate the overlying epithelial cells via chemical synapses. First, direct synaptic connections have been noted in ultrastructural examination of the inner nerve ring region. Second, dual recordings from a swim motorneuron and an epithelial cell reveal a 1:1 correspondence between neuron spikes and epithelial synaptic potentials. The synaptic potentials occur with a latency as short as 3 ms which is constant in any one recording session. The results suggest that the swim motorneuron network of Aequorea not only performs a motorneuron function, but also serves as the pattern generator for swimming activity.     

Behavioral plasticity and central regeneration of locomotor reflexes in the freshwater oligochaete, Lumbriculus variegatus. I: Transection studies

Abstract. Access to the ventral nerve cord in living specimens of Lumbriculus variegatus , an aquatic oligochaete, is normally impossible because surgical invasion induces segmental autotomy (self-fragmentation). We show here that nicotine is a powerful paralytic agent that reversibly immobilizes worms, blocks segmental autotomy, and allows experimental access to the nerve cord. Using nicotine-treated worms, we transected the ventral nerve cord and used non-invasive electrophysiological recordings and behavioral analyses to characterize the functional recovery of giant nerve fibers and other reflex pathways. Initially, after transection, medial giant fiber (MGF) and lateral giant fiber (LGF) spikes conducted up to, but not across, the transection site. Reestablishment of MGF and LGF through-conduction across the transection site occurred as early as 10 h (usually by 20 h) after transection. Analyses of non-giant-mediated behavioral responses (i.e., helical swimming and body reversal) were also made following nerve cord transection. Immediately after transection, functional reorganization of touch-evoked locomotor reflexes occurred, so that the two portions of the worm anterior and posterior to the transection site were independently capable of helical swimming and body reversal responses. Similar reorganization of responses occurred in amputated body fragments. Reversion back to the original whole-body pattern of swimming and reversal occurred as early as 8 h after transection. Thus, functional restoration of the non-giant central pathways appeared slightly faster than giant fiber pathways. The results demonstrate the remarkable plasticity of locomotor reflex behaviors immediately after nerve cord transection or segment amputation. They also demonstrate the exceptional speed and specificity of regeneration of the central pathways that mediate locomotor reflexes.     

A theory of oscillatory instability in two-state systems in relation to nerve excitation

The oscillatory aspect in a system having two steady states is studied theoretically using a model of excitable nerve membrane. The condition for the occurrence of oscillatory instability is discussed on the basis of the kinetic picture of nerve excitation in consideration of the non-Markoffian effect caused by ion transport in the system. Small oscillations around a steady state as well as a giant fluctuation between two states are obtained. Results are compared with experiments carried out with squid giant axons perfused intracellularly.     

Neurobiology of Stomotoca. I. Action systems

The layout of nerves, muscles, and conducting epithelia is described for the simple hydrozoan medusa Stomotoca. Comparisons are drawn with Sarsia and other recently studied forms. The major action systems are those responsible for swimming, crumpling (protective involution), tentacle posture, pointing (unilateral reciprocal flexions of the manubrium and margin), and visceral movements (barely mentioned). Crumpling is a simple summating response in this species. Crumpling and pointing are considered to use the same effectors but different conduction pathways. New histological results include the demonstration of a nerve plexus running through the endodermal canal system and a nerve plexus in the ectoderm encircling the peduncle. Special attention is given to the distribution of synapses and gap junctions, as possible trasmission pathways in behavioral responses. Some details are included on organization within the marginal nerve rings.     

Neurobiology of Polyorchis. I. Function of effector systems.

The electrical correlates of activity in the effector systems responsible for swimming, crumpling and postural changes have been recorded in the anthomedusan Polyorchis penicillatus. Motor spikes (pre-swim pulses), that initiate swimming contractions, appear without delay at distant sites on the inner nerve-ring in unstimulated preparations. Levels of Mg++ anaesthesia which block the neuromuscular junctions between PSP giant neurons and swimming muscle do not affect PSP activity. Swimming muscle potentials can be recorded from subumbrella and velar muscle sheets using extra- and intracellular electrodes. These action potentials have a distinct plateau and are propagated in a myoid fashion. Resting potentials average -70 mV with spikes overshooting zero by some 62 mV. The effects of repetitive stimulation are described. Extracellular recordings indicate that neuronal pathways may play a major role in mediating crumpling, unlike many other species where epithelial pathways are more important. Endodermal spikes recorded intracellularly from the radial and ring canals have amplitudes of some 92 mV arising from resting potentials that average -55 mV. Repetitive stimulation causes a decrease in amplitude and increase in duration of epithelial action potentials. Tentacle length is controlled by a pacemaker system located in both nerve rings. The frequency of spikes (PTPs) generated by this system determines the length and tonus of tentacles. The neuromuscular junctions between the motor neurons and tentacle muscle are Mg++ sensitive and show facilitating properties.     

The Role of the Escape Swim Motor Network in the Organization of Behavioral Hierarchy and Arousal in Pleurobranchaea

The escape swimming pattern generator of the notaspid opisthobranchPleurobranchaea drives a high threshold, override behavior.The pattern generator is integrated with neural networks ofother behaviors so as to coordinate unitary behavioral expressionand to promote general behavioral arousal. These functions areseparately produced by different swim network elements. Oneset of swim premotor neurons, the A1/A10 ensemble, A3 and I_VS,generate the swim pattern and, through corollary activity, suppresspotentially conflicting feeding behavior by exerting broad inhibitionat major feeding network interneurons. A second set of swimneurons, the serotonergic As1–4 neurons, provides intrinsicneuromodulatory excitation to the swim pattern generator thatsustains the escape swim episode through multiple cycles. TheAs1–4 also provide neuromodulatory excitation to importantmodulatory, serotonergic cells in the feeding motor networkand locomotor network, and may have a general regulatory rolein the distributed serotonergic arousal network of the mollusk.The As1–4 appear to be also necessary to both avoidanceand orienting turning, and are therefore likely to be critical,multi-functional components upon which much of the organizationof the animal's behavior rests.     

Defensive strategies in planktonic coelenterates

Some planktonic coelenterates respond to potentially harmful stimulation by protective involution, others by escape behaviour. Examples of protective involution are seen in the ‘crumpling’ behaviour of various hydrome‐dusae (Sarsia, Euphysa) and of siphonophores such as Hippopodius. Involution may be accompanied by striking visual displays e.g. light emission in Euphysa, light emission and blanching in Hippopodius. These displays probably serve to startle or blind interlopers. In Hippopodius, light emission in the dark would have the same effect as blanching in the light, an example of behavioural self‐mimicry.

Animals employing escape locomotion include the ctenophore Euplokamis, the siphonophore Nanomia and the rhopalonematid medusa Aglantha. All of these forms have evolved giant axons that facilitate escape by reducing response time. The central nervous circuitry underlying locomotion in Aglantha is reviewed.

In a few cases (e.g. Aglantha and possibly Nanomia), the responses described can be seen as defensive against predators, but in the majority of cases, the responses probably serve primarily to reduce the risk of damage due to accidental contact with other organisms.     

Neurobiology of Polyorchis. I. Function of effector systems

The electrical correlates of activity in the effector systems responsible for swimming, crumpling and postural changes have been recorded in the anthomedusan Polyorchis penicillatus. Motor spikes (pre-swim pulses), that initiate swimming contractions, appear without delay at distant sites on the inner nerve-ring in unstimulated preparations. Levels of Mg⁺⁺ anaesthesia which block the neuromuscular junctions between PSP giant neurons and swimming muscle do not affect PSP activity. Swimming muscle potentials can be recorded from subumbrella and velar muscle sheets using extra- and intracellular electrodes. These action potentials have a distinct plateau and are propagated in a myoid fashion. Resting potentials average ?70 mV with spikes overshooting zero by some 62 mV. The effects of repetitive stimulation are described. Extracellular recordings indicate that neuronal pathways may play a major role in mediating crumpling, unlike many other species where epithelial pathways are more important. Endodermal spikes recorded intracellularly from the radial and ring canals have amplitudes of some 92 mV arising from resting potentials that average ?55 mV. Repetitive stimulation causes a decrease in amplitude and increase in duration of epithelial action potentials. Tentacle length is controlled by a pacemaker system located in both nerve rings. The frequency of spikes (PTPs) generated by this system determines the length and tonus of tentacles. The neuromuscular junctions between the motor neurons and tentacle muscle are Mg⁺⁺ sensitive and show facilitating properties.     

In situ time budgets of the scyphomedusae Aurelia aurita, Cyanea sp., and Chrysaora quinquecirrha

The in situ behavior of three scyphomedusan species was videorecorded by scuba divers in natural daytime lighting with minimalinterference to the medusae. The mean percentage of time thatindividual medusae spent swimming ranged from 93 to 100%. Therewere no significant differences in the percent time spent swimmingbetween life stages of a species (ephyra, adult) or betweenspecies. The predominance of swimming activity by medusae indicatesthat swimming, and hence the creation of fluid motions responsiblefor prey entrainment and capture, plays a widespread functionalrole in feeding by scyphomedusae.     

Swimming behavior of the nudibranch Melibe leonina

Swimming in the nudibranch Melibe leonina consists of five types of movements that occur in the following sequence: (1) withdrawal, (2) lateral flattening, (3) a series of lateral flexions, (4) unrolling and swinging, and (5) termination. Melibe swims spontaneously, as well as in response to different types of aversive stimuli. In this study, swimming was elicited by contact with the tube feet of the predatory sea star Pycnopodia helianthoides, pinching with forceps, or application of a 1 M KCl solution. During an episode of swimming, the duration of swim cycles (2.7 +/- 0.2 s [mean +/- SEM], n = 29) and the amplitude of lateral flexions remained relatively constant. However, the latency between the application of a stimulus and initiation of swimming was more variable, as was the duration of an episode of swimming. For example, when touched with a single tube foot from a sea star (n = 32), the latency to swim was 7.0 +/- 2.4 s, and swimming continued for 53.7 +/- 9.4 s, whereas application of KCl resulted in a longer latency to swim (22.3 +/- 4.5 s) and more prolonged swimming episodes (174.9 +/- 32.1 s). Swimming individuals tended to move in a direction perpendicular to the long axis of the foot, which propelled them laterally when they were oriented with the oral hood toward the surface of the water. The results of this study indicate that swimming in Melibe, like that in several other molluscs, is a stereotyped fixed action pattern that can be reliably elicited in the laboratory. These characteristics, along with the large identifiable neurons typical of many molluscs, make swimming in this nudibranch amenable to neuroethological analyses.     

The senses of sea anemones: responses of the SS1 nerve net to chemical and mechanical stimuli

The ectodermal slow system (SS1) is one of 3 separate nerve nets in sea anemones. SS1 sensory responses coordinate swimming in Stomphia coccinea (escape response) and expansion to dissolved food substances in Urticina felina (pre-feeding response). Here we have studied Actinia equina, Anemonia viridis, and Anthopleura ballii. Although these anemones can escape from nudibranch predators, the SS1 response to attack by Aeolidia papillosa is probably evoked mechanically rather than chemically (cf. Stomphia). Multiple SS1 pulses to mechanical stimulation are described for the first time. Previous work has shown that in the pre-feeding response of Urticina the SS1 is excited by betaine; in Actinia however, the excitant is proline. The anemones studied can utilize the SS1 in 2 different behavioural responses (escape and pre-feeding/feeding) because the different receptors involved respond at different frequencies (at around 0.6 Hz in escape and 0.2 Hz in pre-feeding).     

Modulation of swimming in Tritonia: excitatory and inhibitory effects of serotonin

1. In the mollusc Tritonia escape swimming is produced by a network of central pattern generator (CPG) neurons. The purpose of this study was to determine which neurotransmitters might be involved in the swim system.
2. Injection of serotonin (5HT) into whole animals elicited swimming followed by a long-lasting inhibition of swimming. In isolated brain preparations, bath-applied 5HT elicited a swim pattern at short latency and also caused a long-lasting inhibition of the swim pattern. The activation of swimming by 5HT was associated with a tonic depolarization of cerebral cell 2 (C2) and the dorsal swim interneurons (DSI) which form part of the swim CPG network.
3. In isolated brain preparations, bath applied glycine, histamine, proctolin, and FMFRamide had no effect on the swim motor pattern elicited by electrical stimulation of a peripheral nerve. Aspartate, carbacol, dopamine, glutamate, octopamine, pilocarpine, and small cardioactive peptide-B (SCP_B) inhibited the activation of swimming by nerve stimulation.
4. The 5HT antagonists cyproheptidine, tryptamine, and 7-methyltryptamine had no effect on swimming, but methysergide and fenfluramine inhibited swimming to both normal sensory stimuli and exogenously applied 5HT.
5. Staining with a polyclonal antibody indicated that one class of CPG neurons, the dorsal swim interneurons (DSI), was immunoreactive for 5HT.
6. Taken together, the data suggest that pattern generator interneurons, particularly the DSIs, use 5HT as a neurotransmitter.

     

Behavioral plasticity and central regeneration of locomotor reflexes in the freshwater oligochaete, Lumbriculus variegatus. II: Ablation studies

Abstract. After 8–10 segments of posterior ventral nerve cord were ablated in Lumbriculus variegatus , touch-evoked locomotor responses were evident both in segments anterior and posterior to the ablation site. However, responses in these two regions were independent and uncoupled. During recovery, four outcomes were observed at the ablation site: (Group 1) recovery of normal functions with no growth of new segments; (Group 2) formation of a laterally protruding, multi-segmented, ectopic head; (Group 3) formation of a laterally protruding, amorphous, and multi-segmented outgrowth; and (Group 4) segmental autotomy. In Groups 1 and 2, touch-evoked swimming and body reversal were studied. In addition, sensory fields and conduction properties of giant nerve fibers were examined near the ablation site. In some Group 1 worms, clear-cut behavioral and electrical signs of recovery and reconnection were seen by 3 d after ablation. By 8 d, all worms had recovered and exhibited response patterns comparable to those of normal worms. In Group 2 worms, with an ectopic head, segments posterior to the ablation (together with those in the ectopic head), exhibited touch-evoked swimming and body reversal responses resembling those of a complete worm. Segments anterior to the ectopic head were independently capable of locomotor responses. Medial and lateral giant fiber sensory fields in worms with ectopic heads reflected a pattern expected for two worms. Thus, through apparent morphallactic reorganization, a medial giant fiber sensory field emerged which included the ectopic head and 10–15 adjacent posterior segments. In contrast, electrical recordings showed longitudinal through-conduction of giant fiber spikes, across the ablation site. Histological examination revealed that the giant nerve fibers in the ectopic head were complexly interconnected with those in the main body axis.