Non-giant Tailflips Research Articles

Projection and local interneurons in the sixth abdominal ganglion of the sand crab Emerita analoga (Hippidae)

Hippid crabs are adapted for life in the surf zone of exposed sandy beaches, and their tailfan differs from the tailfans of other crustaceans with respect to morphology and motor control and in having nonspiking stretch receptors (NSR). To investigate how these crabs' mechanosensory systems are adapted to this turbulent environment, I used axonal back-filling and intracellular recording with dye-filled microelectrodes to describe afferent projections from the telson and morphologies and physiological responses of intersegmental and local neurons in abdominal ganglion 6 (A6) in Emerita analoga, then compared them with descriptions of corresponding neurons in A6 of crayfish. The density of afferent terminals and the proportion of projection neuron somata is lower in anterior A6 of E. analoga than in crayfish, perhaps correlated with a reduction in hydrodynamic setae. Many interneurons responded to afferent nerve stimulation and displayed activity correlated with levels of A6 motor output. NSR stretch depolarizes unilateral local neurons and terminals of axons entering A6 from the connective and hyperpolarizes bilateral local and projection neurons. The timing and duration of this inhibition would suppress mechanosensory input from the telson during uropod beating (homologue of crayfish's nongiant tail-flipping). Suppression of reafference during uropod beating may have been pivotal for evolution of hippids' ability to move rapidly across the water-sand interface in the slosh zone of sandy beaches. Homologies between A6 neurons in E. analoga and crayfish, suggested by morphological and physiological similarities, indicate that the NSRs connect to a neuronal network regulating exteroceptive input that was inherited from their tail-flipping ancestors.

Loss of escape responses and giant neurons in the tailflipping circuits of slipper lobsters, Ibacus spp. (Decapoda, Palinura, Scyllaridae)

In many decapod crustaceans, escape tailflips are triggered by lateral giant (LG) and medial giant (MG) interneurons, which connect to motor giant (MoG) abdominal flexor neurons. Several decapods have lost some or all of these giant neurons, however. Because escape-related giant neurons have not been documented in palinurans, I examined tailflipping and abdominal nerve cords for giant neurons in two scyllarid lobster species, Ibacus peronii and Ibacus alticrenatus. Unlike decapods with giant neurons, Ibacus do not tailflip in response to sudden taps. Ibacus can perform non-giant tailflipping: the frequency of tailflips during swimming is adjusted by altering the gap between each individual tailflip. Abdominal nerve cord sections show no LG or MG interneurons. Backfilling nerve 3 of abdominal ganglia revealed no MoG neurons, and the fast flexor motor neuron population is otherwise identical to that described for crayfish. The loss of giant neurons in Ibacus represents an independent deletion of these cells compared to other reptantian decapods known to have lost these giant neurons. This loss is correlated with the normal posture in scyllarids, in which the last two abdominal segments are flexed, and an alternative defensive strategy, concealment by digging into sand.

An Analysis of Field Potentials During Different Tailflip Behaviours in Crayfish

Crayfish tailflips have been intensively studied to reveal the decision-making processes and neural organisation underlying a stereotyped escape behaviour. Three behaviours mediated by different neural pathways have been well described: medial giant, lateral giant and non-giant tailflips. It has proved difficult to distinguish between the three without invasive or restrictive experimental manipulation. We report unambiguous differences between the signals generated by the crayfish Cherax destructor during the three types of tailflip when recorded by bath electrodes placed in the holding aquarium. Using our ability to distinguish between the different behaviours in freely moving animals we examined the relationship between the type of tailflip evoked by stimulation to different parts of the body. The transition zone between medial and lateral giant tailflips is the thoracic-abdominal border but it is not absolute and some stimuli produce responses that cannot be unambiguously assigned to either behavioural category. We examined the latency between stimulation at different points down the length of the body and the appearance of the electrical signal accompanying escape for both medial and lateral tailflips. We used two methods to estimate the proportion of the latency accounted for by giant fibre conduction velocity. The results support current views of the differences between the activation sites of the two giant fibre systems and suggest why stimulation in the transition zone results in ambiguous outcomes.

Tailflipping ofMunida quadrispina (Galatheidae): conservation of behavior and underlying musculature with loss of anterior contralateral flexor motoneurons and motor giant

1. We analyzed tailflipping behavior, motor patterns, underlying musculature and flexor motoneurons inMunida quadrispina (Galatheidae) and compared them with these parameters in crayfish to reveal evolutionary changes in the nervous system which might have occurred in conjunction with loss of giant interneurons and change in body form and posture. 2. The form of tailflipping (videoanalysis) varies with respect to abdomen extension angle, amount of uropod promotion, and pereopod positioning (Fig. 1). In ‘full’ tailflips, the uropods are maximally promoted throughout active flexion; the first 3 pairs of pereopods are held forward. In ‘truncated’ tailflips, abdominal segments 4–6 do not extend, uropods do not promote and pereopods either move actively or trail passively. Flexion latency (=extension duration) covaries with extension period, but does not vary systematically with extension amplitude (Fig. 3C, D). 3. Flexor-burst latencies (electromyograms) in segments 2–4 vary independently of extensor-burst period; in segment 5 they covary with period (Figs. 2, 3 A, C). 4. M. quadrispina has slow flexor motoneurons identical to those in crayfish but lacks homologs of the motor giants and of any FAC motoneurons (Figs. 4, 5; Table 1). 5. Quantitative comparison of the relative sizes of fast flexor and extensor musculatures inM. quadrispina and in crayfish revealed only one significant difference between the 2 animals: the extensor muscles are approximately the same size in all segments in crayfish whereas inM. quadrispina they are largest in segment 5 (Fig. 6; Table 2). 6. The major conclusion is that whereas nongiant tailflipping behavior (overt behavior and motor pattern) and underlying musculature were conserved in evolution ofM. quadrispina, flexor motoneurons underwent reductions compared with crayfish (andGalathea strigosa). Loss of FAC motoneurons perhaps resulted from chance loss of certain neuroblasts which was tolerated because other motoneurons still innervated the affected muscles.

Further Studies of Crayfish Escape Behaviour : I. The Role of the Appendages and the Stereotyped Nature of Non-Giant Escape Swimming

ABSTRACT High-speed cinematography of the escape behaviour of freelymoving crayfish showed that the thoracic and abdominal appendages exhibit stereotyped movements in giant axon-mediated tail flips and in non-giant flips. Three distinct classes of non-giant tail flips were recognized in this study: linear, pitching and twisting flips. In medial giant flips and linear non-giant flips the chelipeds and pereiopods were promoted and extended in a manner which minimized the hydrodynamic resistance of the animal. The exopodites of the uropods were promoted. In lateral giant flips and pitching non-giant flips the thoracic appendages moved only passively. The uropod protopodites were promoted but the exopodites remained remoted. When giant axon-mediated tailflips were elicited with natural stimuli they were followed by sequences of non-giant flips which appeared quite stereotyped.

Plasticity of non-giant flexion circuitry in chronically cut abdominal nerve cords of the crayfish, Procambarus clarkii.

We have investigated the pattern of neuronal activity involved in the gradual return of sensory-evoked abdominal flexions in crayfish with chronically transected nerve cords. Recordings were made from eight types of identified neurone that mediate phasic abdominal movements, in a preparation consisting of the isolated abdominal nerve cord and tailfan. Responses of the cells to pinches and dorsiflexions of the tailfan were compared in two groups of animals: animals whose cords had been cut at the thoracic-abdominal junction 4-17 weeks earlier (chronic preparations), and animals whose cords had been cut at the same site either just before the experiment or up to 6 days earlier (acute preparations). Sensory stimuli produced bursts of spikes in 73% of the fast flexor motoneurones impaled in chronic preparations, but never fired these neurones in acute preparations. However, fast flexor motoneurones in both preparations were fired with approximately equal frequency by single impulses in the giant axons, suggesting that the firing thresholds of these motoneurones had not changed. Sensory stimuli also caused spiking in the extensor inhibitor and the flexor inhibitor in chronic preparations; in contrast, responses in the fast extensor motoneurones were always subthreshold and occasionally hyperpolarizing. None of these cells was fired by similar stimuli in acute preparations. Neurones restricted to the giant axon pathways (lateral, medial, segmental and motor giants) were silent during sensory-evoked flexor discharges in chronically transected cords. Flexor discharges were accompanied by intense activity in non-giant axons recorded from the dorsal cord. Two identified, non-giant interneurones with axons in the dorsal cord were substantially depolarized but never fired by sensory input in chronic preparations. Sensory-evoked firing in the fast flexor motoneurones was not abolished by removal of the posterior stump of the nerve cord at the transection site. About 20% of chronic preparations generated cyclic motor output in response to unpatterned sensory stimulation. The pattern of motor activity that develops in chronically transected cords resembles that seen in normal crayfish during non-giant tailflips. Because cord transection permanently isolates the abdomen from rostral neural centres normally required for the generation of such tailflips, the return of co-ordinated motor output in chronically cut cords may result from the sensory activation of non-giant circuitry within the abdominal nervous system.

Crayfish escape behavior: production of tailflips without giant fiber activity.

The giant interneurons of the crayfish nerve cord are well-known mediators of fast tail flexions, "tailflips," that propel animals through the water away from danger. More recent studies have revealed an additional nongiant generator of tailflips. In contrast to giant tailflips, which are stereotyped, nongiant tailflips have variable form. The operating principles and portions of the neural circuitry governing nongiant tailflips were here investigated. Whereas fast flexor motor neurons (FFs) receive excitatory postsynaptic potentials (EPSPs) with large unitary components just prior to giant tailflips, excitation of the FFs during nongiant tailflips is due to summation of many small EPSPs, and these build up for about 60 ms prior to the tailflip; we call the period of excitation prior to FF firing the preflexion phase and the period during which FFs fire, the flexion phase of the tailflip. Even FFs that will not fire during a given tailflip become depolarized during preflexion and flexion periods. Throughout the preflexion and flexion periods there is activity in dorsal nerve cord axons (DCAs) that lie below the giants. Many DCAs are interneurons that excite FFs at short latency. Some DCAs fire uniquely during the preflexion phase, while some fire only during the flexion phase. Which DCAs fire is highly variable, and in some cases firing of particular DCAs can be correlated with particular forms of tailflips. Two identified DCAs, 12 and 13, that fire during the flexion phase were studied. These interneurons originate and receive their synaptic input in the second and third abdominal ganglia, respectively, and project to the last ganglion exciting FFs caudal to their ganglion of origin en route. Their pattern of synaptic input prior to and during nongiant tailflips is indistinguishable from that of FFs. Their input to FFs is weak, but when they fire they tend to promote intersegmental synchrony of FFs in the segments they feed. It appears likely to us that nongiant tailflips are synthesized from a small library of component tailflip movements that can be combined to produce a variety of complete tailflips and that the component movements are produced by a limited group of premotor interneurons, of which 12 and 13 are members.(ABSTRACT TRUNCATED AT 400 WORDS)

Interneurons between giant axons and motoneurons in crayfish escape circuitry

1. Crayfish giant fibers are generally believed to generate tailflip movements by means of direct connections to two classes of phasic flexor muscle motoneurons, the motor giants (MoGs) and the nongiant fast flexor motoneurons (FFs). It is shown here that the giants also stimulate a network of interneurons that make connections with the FFs. 2. This network includes an intraganglionic neuron, the segmental giant (SG), in each abdominal hemisegment and a number of intersegmental neurons, two of which (I2 and I3) were studied in detail. 3. The SGs are driven reliably by the giant fibers and they in turn drive the FFs of their hemisegment about as effectively as do the giant fibers themselves; it is possible that the giant fibers excite the FFs mainly by way of the SGs. The SGs also have an efferent first root axon whose peripheral targets we have been unable to determine. 4. I2 and I3 originate in the second and third abdominal ganglia, respectively, and descend to the last ganglion. In their ganglia of origin they are reliably driven by the giant fibers and by the SGs. In addition, I2 weakly excites I3 and both receive weak, apparently direct, excitatory input from FFs as well as less direct excitatory and inhibitory input from unidentified afferent sources. Both weakly excite most FFs in ganglia behind the one in which they originate. This excitation adds to that produced directly by giant fibers and SGs and, we believe, is sometimes decisive in causing FF firing. Their firing also causes inhibition involved in suppressing effects of reafference, as do the giant fibers themselves. 5. I3 strongly excites the motoneurons of certain tail fan muscles (the ventral and posterior telson flexors). However, the contraction of these muscles would be maladaptive during some giant fiber-mediated tailflips. Accordingly, when the giant fibers, which always recruit I3, fire, they cause an inhibition of the motoneurons that nullifies the excitatory input from I3. At a formal level this means that the giants, viewed as command neurons, not only drive but also alter or modulate the subordinate motor pattern-generating network that they control. 6. Tailflips that are less stereotyped than those mediated by giant fibers are known to occur without participation of the giants. It is suggested that the presence of complex circuitry mediating between giant fibers and FFs may be related to the use of portions of this circuitry as well as the FFs themselves in production of nongiant tailflips.

Crayfish escape behavior: Neurobehavioral analysis of phasic extension reveals dual systems for motor control

1. Electromyograms (EMGs) from phasic abdominal muscles of unrestrained and variously restrained crayfish were used to study the involvement of sensory information in phasic abdominal extension during escape behavior. 2. Lateral giant neuron impulses (escape commands), elicited either with natural stimuli or via direct shocks, caused a flexion which was followed at short and near-constant latency by extension (Figs. 1 and 2). 3. Extension produced as above was termed ‘postgiant’ extension and had the following properties: it was labile (Figs. 3 and 4), it was eliminated when flexion was prevented, and it was reduced or eliminated if flexion was hampered (Fig. 5 and Table 1). 4. The above observations, which suggest sensory involvement in post-giant extension, are complemented by the observation that phasic extensor activity could be evoked without prior flexion by rapid water displacements over the abdomen or by taps to the abdomen (Fig. 7). 5. In addition to post-giant extension the extensors were active during many kinds of non-giant tailflips. During swimming, non-giant extensionpreceded flexion at short and constant latency (Fig. 9) and persisted after flexor root section (Fig. 10) or during restraint. Non-giant extension was not labile (Fig. 11), and it depended on the integrity of the rostral nervous system. 6. Animals frequently initiate escape with a giantmediated tailflip followed by non-giant swimming. When this occurred our most common observation was consistent with the interpretation that both postgiant and non-giant extension occurred between the first two flexions (Figs. 13 and 14). 7. We interpret our results to mean that extension occurs as a chained reflex following giant-mediated flexion, with subsequent control of the extensors passing to a central pattern generator.