scholarly journals Excitation of the nerve-muscle system in Crustacea

The nature of the action potential and the mechanical response of crustacean muscle is investigated. If electric shocks of sufficient intensity are applied to the muscle, graded local contractions occur at the cathode. If the intensity of the stimuli is further increased, propagated action potentials, up to 40 mV, are recorded, accompanied by vigorous twitches of the active fibres. The conduction velocity of the muscle impulse is about 20 cm./sec., at 20° C, and its wavelength about 2—3 mm. The mechanical and electrical responses of the muscle to motor nerve stimulation are local or propagated, depending upon the number and frequency of the nerve impulses. With single, or low-frequency, motor nerve impulses a negative potential change is recorded in the vicinity of the nerve endings. It spreads decrementally 2-3 mm. along the muscle fibres, and at 17° C rises to a peak in 3 msec, and falls to one half in about 6 msec. Because of its analogy to the junctional potential of curarized vertebrate muscle it will be referred to as 'end-plate potential’ (e. p. p.). The spatial characteristics of the e. p. p. provide evidence for a discrete ‘focal’ innervation of crustacean muscle fibres, similar to that in vertebrates. In many muscles, with repetitive stimulation, successive e. p. p.’s continue to grow in amplitude for 0⋅3-0⋅5 sec. The degree and time course of this ‘facilitation’ varies greatly in different muscles; depending upon initial size and rate of growth of successive e. p. p.’s, ‘fast’ and ‘slow ’ systems can be distinguished. At high frequencies (above 100 per sec.), e. p. p.’s sum to a plateau of several times their individual height. When the e. p. p.’s have grown or summed to a ‘threshold’ level, propagated spikes are set up. Spikes in individual fibres are usually asynchronous and occur at a lower rate than e. p. p.’s. If the e. p. p. is slightly below ‘threshold’, abortive spikes are observed. A prolonged series of e. p. p.’s is associated with a relatively slow maintained contraction of the junctional region. Propagated spikes, on the other hand, are accompanied by quick twitches of the active muscle fibres. This difference is seen clearly by direct inspection of the exposed muscle fibres, but not by recording the overall tension of the muscle. In many muscles, local junctional responses account for more than 50% of the maximum observed tension. Electric recording on the intact animal shows that a good deal of the normal limb muscle activity is based on e. p. p.’s and local contractions. Propagated muscle spikes were seen only during fast and powerful reactions. The rate of contraction varies with the frequency of motor impulses as a higher than second power function. This relation, and especially the origin of the very slow contraction at low frequency, is discussed. Recruitment of individual muscle fibres plays only a minor role; the main factor is the rate of summation of the local mechanical activation process at the junction. A further factor influencing the speed of contraction is the spatial spread of the active region, which controls the extent of internal elastic shortening of the muscle. The various links of the neuro-muscular transmission chain are discussed and compared with the analogous processes in vertebrates.

While it has been recognized for many years that different limb muscles belonging to the same mammal may have markedly differing contractile characteristics, it is only comparatively recently that it has been demonstrated that these differences depend upon the motor innervation. By appropriately changing the peripheral nerve innervating a mammalian skeletal muscle, it is possible to change dramatically the contractile behaviour of the reinnervated muscle. The manner by which the motor innervation determines the nature of a muscle fibre’s contractile machinery is not completely understood, but it appears that the number and pattern of motor nerve impulses reaching the muscle play an important role. The biochemical changes occurring within muscle fibres whose contractile properties have been modified by altered motor innervation include the synthesis of different contractile proteins.


Since the end of the 1939-45 war, the task of someone trying to understand muscular contraction has become in some respects easier, and in others more difficult. On the credit side, straightforward explanations are now available—and well established—for the main events in neuromuscular transmission, propagation of the action potential, the inward spread of an activating process, chemical activation of the myofibrils, and the sliding filament process of length change. On the other side new properties, new structures and new substances have turned up which cannot yet be fitted into any comprehensive scheme. Further, we are still totally in the dark about the actual molecular processes involved even in those steps for which clear explanations are available at the electrophysiological or electronmicroscopical level. Yet another complication is the extraordinary variety of muscle types that are being discovered, even among such thoroughly studied groups of animals as amphibians and mammals. I have been repeatedly struck by cases where the investigation of muscle has been held up by a false assumption based on the supposition that different kinds of contractile materials must work in the same way. For example, it has often been argued that smooth muscle and striated muscle are essentially similar, and therefore the striations are of only minor importance; this argument was given, for example, by Bernstein (1901, p. 284). The still more general argument that the nature of the ‘contractility’ of muscle should be looked for in the supposedly simpler processes of protoplasmic movement had been the main theme of a book by Verworn (1892). This attitude was, I am sure, one of the main reasons for the almost complete disregard of the striations by physiologists and biochemists between about 1910 and 1950. Again, the elucidation of the slow motor system of certain striated muscle fibres, present in probably all vertebrates, was delayed for many years by the discovery that in mammals even the slow postural activity of limb and trunk muscles is accompanied by propagated action potentials characteristic of fast motor systems. It was widely assumed on this basis that ‘tonic’ contractions in all vertebrate striated muscles consisted of asynchronous twitches or unfused tetani in scattered motor units, and most physiologists came to disregard the numerous indications—physiological and pharmacological (Langley 1913; Sommerkamp 1928; Wachholder & von Ledebur 1930) as well as histological (see Krüger (1952) for references both to his own work in the thirties and to other work)—of the existence of a second, slow, system in skeletal muscles of the frog. The very slow contractions elicited in the familiar gastrocnemius muscle of the frog by stimulating small-diameter motor-nerve fibres (Tasaki & Kano 1942; Tasaki & Mizutani 1944; Tasaki & Tsukagoshi 1944) came as a complete surprise to most physiologists, and received little attention until the matter was taken up by Kufiler and his colleagues (e.g. Kuffler & Vaughan Williams 1953). The astonishing range of structural diversity that becomes apparent when one looks at the arthropods as well as the vertebrates has recently been emphasized by Hoyle (1967).


1936 ◽  
Vol 13 (1) ◽  
pp. 111-130
Author(s):  
C. F. A. PANTIN

1. The response of certain limb muscles in Carcinus maenas to stimuli of different frequencies and intensities has been analysed. The precautions necessary to obtain reproducible results in crustacean muscle are recorded. The material must be fresh; the duration of stimulation short; and each individual shock must be less than the true chronaxie, to prevent multiple excitation of the nerve. 2. A single stimulus produces a microscopic response or none at all. A succession of shocks, however, causes a contraction, the rate of which increases with the frequency, till this reaches the high values of 300-400 shocks per sec. The rate of contraction varies absolutely continuously with the frequency from 300 per sec. down to the microscopic response observed at less than 10 per sec. The rate of contraction increases very rapidly indeed between frequencies of 50 and 200 per sec, so that this range includes almost all rates of contraction. 3. The limiting frequency of 300-400 per sec. is close to the refractory period. For pairs of stimuli, the absolute refractory period is about 1σ at 18° C. This is followed by a relative refractory phase and sometimes by a supernormal phase. The excitability has returned to normal after about 4σ. In repetitive stimulation the absolute refractory period lengthens. 4. With stimuli of increasing intensity, the responses of both flexor and extensor muscles show first a threshold for excitation of the motor nerve, and, at a higher intensity, a threshold for inhibition. At very high intensities (10-20 times the true threshold) large contractions may be obtained owing to repetitive excitation. 5. With suitable precautions it can be shown that between the threshold of excitation and the threshold of inhibition there is great independence between the response and the intensity of the stimulus. The system behaves as a single excitable system and possibly in some cases a single axon supplies the entire muscle. 6. The chronaxie of the nerve to single shocks and to repetitive stimulation is of the order of 0.2-0.4σ. Single shocks of high intensity give multiple excitation, and the thresholds for this simulate a chronaxie curve. False chronaxies up to 30σ can be obtained in this way. 7. There is no evidence of a double excitable system in the muscles of the walking leg of Carcinus such as has sometimes been recorded in crustacean claws. There is no doubling of intensity-duration or refractory period curves. 8. All the effects observed are explicable in terms of neuromuscular facilitation. The response is governed entirely by the frequency and number of stimuli. Each shock in a series brings more and more muscle fibres into action. With increasing frequency of stimulation, not only are there more contraction increments in a given time, but the increment following each shock is larger. 9. At low and moderate frequencies the rate of development of tension is governed by the rate at which impulses reach the muscle. At the highest frequencies a limit is set to the rate of contraction by the physical properties of the muscle. 10. There is a close analogy between the neuromuscular mechanism disclosed here and the neuromuscular mechanism of the Coelenterata. In both there is a tendency for an entire effector to behave as a single system in which the response is governed by the number and frequency of impulses received by the muscle. This system is distinguished sharply from that of vertebrate skeletal muscle in which gradation of response is brought about through the multiplicity of motor units.


2020 ◽  
Vol 223 (24) ◽  
pp. jeb233494
Author(s):  
Tigran P. Norekian ◽  
Robert W. Meech

ABSTRACTAlthough the bell-shaped nectophores of the siphonophore Nanomia bijuga are clearly specialized for locomotion, their complex neuroanatomy described here testifies to multiple subsidiary functions. These include secretion, by the extensively innervated ‘flask cells' located around the bell margin, and protection, by the numerous nematocytes that line the nectophore's exposed ridges. The main nerve complex consists of a nerve ring at the base of the bell, an adjacent column-shaped matrix plus two associated nerve projections. At the top of the nectophore the upper nerve tract appears to have a sensory role; on the lower surface a second nerve tract provides a motor input connecting the nectophore with the rest of the colony via a cluster of nerve cells at the stem. N. bijuga is capable of both forward and backward jet-propelled swimming. During backwards swimming the water jet is redirected by the contraction of the Claus' muscle system, part of the muscular velum that fringes the bell aperture. Contractions can be elicited by electrical stimulation of the nectophore surface, even when both upper and lower nerve tracts have been destroyed. Epithelial impulses elicited there, generate slow potentials and action potentials in the velum musculature. Slow potentials arise at different sites around the bell margin and give rise to action potentials in contracting Claus’ muscle fibres. A synaptic rather than an electrotonic model more readily accounts for the time course of the slow potentials. During backward swimming, isometrically contracting muscle fibres in the endoderm provide the Claus' fibres with an immobile base.


1953 ◽  
Vol 30 (3) ◽  
pp. 433-439
Author(s):  
P. FATT

1. The importance of the spatial distribution of motor nerve endings in crustacean muscle is discussed. 2. The spread of the ‘end-plate potential’ (e.p.p.) has been mapped out in individual crustacean muscle fibres using intracellular recording. 3. The e.p.p. is distributed over the whole length of the fibre with relatively small variations of its local amplitude. In any one of fourteen individual fibres, the size of the e.p.p. varied by less than a factor of two along 5-6 mm. of fibre length, the average range of variation being 1.4. A sharp focal e.p.p. was only seen in a partially ‘denervated’ muscle fibre. 5. These experiments support the view that motor nerve endings are widely distributed along the length of crustacean muscle fibres.


1939 ◽  
Vol 16 (2) ◽  
pp. 121-133
Author(s):  
A. VAN HARREVELD ◽  
C. A. G. WIERSMA

The functions of the five fibres innervating the flexor muscle of the carpopodite was investigated in Panulirus interruptus. The four thicker fibres were found to be motor axons, each eliciting a contraction with different characteristics. These four contractions were accompanied by four different types of action currents. The thinnest fibre when stimulated simultaneously with any of the four motor fibres caused inhibition of the contraction. It is concluded that all four contractions take place in all the muscle fibres and that the conception of the mechanism of crustacean nerve muscle system developed before is enlarged to include the new results. The possible biological significance of the quintuple innervation is discussed.


1981 ◽  
Vol 92 (1) ◽  
pp. 13-22
Author(s):  
DAISUKE YAMAMOTO ◽  
HIROSHI WASHIO

Two components of outward currents were investigated under voltage clamp conditions in Tenebrio muscle fibres. The instantaneous current-voltage relation for the transient outward current showed outward rectification. The tail currents for the delayed outward currents were made up of either one or two exponential components. The activation process for the delayed current was analysed using positive tails that decayed with a simple exponential time course. The delayed current was half-activated at about + 35 mV. Two rate constants for activation are both monotonic functions of membrane potential. The reversal potential for the delayed current was only partially dependent on the external K-concentration. The role of the two outward currents in the production of the action potential was discussed.


1958 ◽  
Vol 35 (4) ◽  
pp. 850-861
Author(s):  
D. W. WOOD

1. The prothoracic flexor tibialis muscle of Carausius morosus consists of two lateral rows of pinnately arranged muscle units. Motor nerve endings of the ‘Doyère-cone’ type are distributed at intervals of approximately 60 µ along each fibre. Each motor ending is probably innervated by two axons. 2. Two types of responses have been found in the muscle fibres: (i) ‘fast’ electrical responses resembling the action potential of vertebrate muscles, associated with twitch-type contractions of the fibres; (ii) ‘slow’ readily facilitating responses resembling end-plate potentials, associated with slow, smooth contractions of the muscle, and with the maintenance of tonus. There is no evidence of peripheral motor inhibition. 3. The muscle bathed in haemolymph is capable of developing a tetanus tension of 800 g./cm.2 cross-sectional area of individual muscle fibres. The tetanus:twitch ratio is over 25:1. 4. Pharmacological substances which affect excitable tissues of other animals have no effect on the fast response. 5. Progressively lowered temperatures lengthen the time course and reduce the amplitude of the fast response, but an active membrane response remains at 5°C. 6. Refractoriness is evident near the peak of the fast response. The junctional potentials will summate if sufficiently close in time. 7. It is suggested that the process underlying the fast response in Carausius is similar to that in the locust and in vertebrates; but neuromuscular transmission does not appear to be cholinergic.


1936 ◽  
Vol 13 (2) ◽  
pp. 148-158
Author(s):  
C. F. A. PANTIN

1. The cases where there appears to exist a "quick" and "slow" contractile system in the same crustacean muscle are reviewed. 2. Blaschko, Cattell and Kahn (1931) showed that in the claws of Maia a stimulus of very low frequency produced a scarcely perceptible response. But the interjection of a single stimulus during such low-frequency excitation brought about a sudden rapid contraction which was subsequently maintained by the low-frequency stimulus. This effect is to be found in other muscles, including the flexor of the dactylopodite of the walking leg of Carcinus. 3. The effect is not due to the presence of a second excitable element in the neuromuscular system. The flexor in Carcinus leg can be shown to behave as though there were only one excitable element present. The effect is due to neuromuscular facilitation. The low-frequency excitation is unable to reach the majority of the muscle fibres; but it leaves their neuromuscular junctions in a condition in which the transmission of an interjected impulse by momentarily increasing the frequency, is so greatly facilitated that it reaches almost all the muscle fibres. Once the conduction path has been established between nerve and muscle in this way, the low-frequency excitation is sufficient to maintain it. 4. The most certain evidence for the existence of a double excitable mechanism in any crustacean limb muscle is that of Keith Lucas on the claws of lobster and of Astacus. These are highly specialised, and further are differentiated into cutter and crusher claws in Carcinus and many decapods. The muscles of the cutter claw show the same behaviour as the muscles of the walking leg. The muscle behaves as a single excitable unit when the nerve is excited near the base of the limb. 5. The adductor of the crusher claw and this muscle alone exhibits a double excitable system. Two distinct types of response are obtained at different thresholds. Two intensity-duration curves can be traced. The systems show very different rates of contraction. The whole system behaves as though there were two distinct muscles. The "slow" system has a lower threshold than the "quick" system. 6. The "quick" system differs sharply from the "slow" in the frequency of stimulation required to bring it into action. The frequency range of stimulation required to activate the "slow" system of the crusher claw is identical with the range for the whole adductor of the cutter claw and the flexor and extensor muscles of the dactylopodite of the walking leg. The "quick" system, on the other hand, is brought into action at a much lower frequency range. Apart from this, the behaviour of both systems is the same as that of all the other muscles investigated. Over their own characteristic ranges, the higher the frequency the more rapid the contraction. 7. The crusher adductor is equivalent to two units physiologically differentiated. The unit corresponding to the slow system is used in the normal movements of the crab, while the unit corresponding to the quick system is used when great tensions are suddenly required for the crushing of hard objects. The differentiation thus has a decided functional significance.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Gotthold Fläschner ◽  
Cosmin I. Roman ◽  
Nico Strohmeyer ◽  
David Martinez-Martin ◽  
Daniel J. Müller

AbstractUnderstanding the viscoelastic properties of living cells and their relation to cell state and morphology remains challenging. Low-frequency mechanical perturbations have contributed considerably to the understanding, yet higher frequencies promise to elucidate the link between cellular and molecular properties, such as polymer relaxation and monomer reaction kinetics. Here, we introduce an assay, that uses an actuated microcantilever to confine a single, rounded cell on a second microcantilever, which measures the cell mechanical response across a continuous frequency range ≈ 1–40 kHz. Cell mass measurements and optical microscopy are co-implemented. The fast, high-frequency measurements are applied to rheologically monitor cellular stiffening. We find that the rheology of rounded HeLa cells obeys a cytoskeleton-dependent power-law, similar to spread cells. Cell size and viscoelasticity are uncorrelated, which contrasts an assumption based on the Laplace law. Together with the presented theory of mechanical de-embedding, our assay is generally applicable to other rheological experiments.


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