1. The prothoracic flexor tibialis muscle of Carausius morosus consists of two lateral rows of pinnately arranged muscle units. Motor nerve endings of the ‘Doyére-cone’ type are distributed at intervals of approximately 60 p 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 50 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.

Insect muscles are innervated by relatively few motor axons. Some or all of these axons may evoke different electrical and mechanical responses in the muscle fibres they innervate (see Hoyle, 1957 a). Only one full analysis of the neuromuscular mechanisms of an insect muscle has been made, on the jumping muscle of the locust (Hoyle, 1955 a, b). Hoyle found that this muscle was innervated by three different kinds of axons which could elicit four distinct types of electrical response in the muscle fibres. He designated these ‘fast’ and ‘slow’, following crustacean terminology. Other studies of insect neuromuscular mechanisms have either been restricted to descriptions of ‘fast’ responses (Hagiwara, 1953; Hagiwara & Watanabe, 1954); or were made with techniques incapable of revealing the finer details (Pringle, 1939; Roeder & Weiant, 1950). Hoyle (1957a) has criticized in certain respects Wilson’s (1954) description of the neuromuscular mechanisms of the cockroach.

The purpose of this account is to present information about the electrical and mechanical responses of a normal walking muscle, the prothoracic flexor tibialis of the stick insect, Carausius morosus Br., obtained by modern methods.

The flexor tibialis muscle is similar in organization in all three legs. Like the metathoracic extensor tibialis muscle of the locust (Hoyle, 1955 a) it is composed of bundles of fibres, or ‘muscle units’, arranged pinnately with their origin on a central apodeme and their insertion on the lateral cuticle (Fig. 1). The muscle is much less bulky, and therefore has fewer muscle units and fewer fibres per muscle unit, than in the locust. There are about seventeen pairs of muscle units, each unit containing ten to twelve fibres, in the prothoracic muscle.

Fig. 1.

Slightly ventro-lateral view of the prothoracic femur of Carausiut. Cuticle partly removed to show some of the muscle units of the flexor tibialis, and two muscle units removed to show the position of the apodeme.

Fig. 1.

Slightly ventro-lateral view of the prothoracic femur of Carausiut. Cuticle partly removed to show some of the muscle units of the flexor tibialis, and two muscle units removed to show the position of the apodeme.

The muscle is innervated solely by the crural nerve. As this nerve passes into the femur, it divides to send branches to the extensor tibialis and retractor unguis muscles, but the body of the nerve continues through the femur adjacent to the flexor tibialis muscle. The body of the nerve gives off branches at intervals on either side, each branch innervating a pair of adjacent muscle units on the same side of the femur. The main body of the nerve proceeds into the tibia, and is presumed to carry sensory fibres from tibial and tarsal receptors.

Each motor nerve branch which innervates a single muscle unit passes to the centre of the unit and there divides to send finer branches between and along the individual muscle fibres. These ultimately terminate in a number of motor nerve endings distributed at intervals of about 60 μ along the muscle fibre they innervate. The main branch of the crural nerve contains a large number of axons of many different sizes, while the side branches to muscle units run obliquely and their detailed contents are therefore not very clear in transverse section. But in some cases two axons have been observed in the fine branches to individual nerve endings, and these presumably correspond to the two types of physiological response described in this paper. The motor endings are of the ‘Doyère-cone’ type, and in general appearance resemble the motor nerve endings in the locust (Hoyle, 1955 a).

Hoyle (1955b) measured the tension developed under conditions of natural stimulation by the jumping muscle of the locust and concluded that it was about 1000 g./cm.2 in terms of unit area of cross-section of individual fibres. This figure is similar to that for frog muscle, although the pinnate arrangement confers a much higher tension : weight ratio for the whole muscle, than in frog muscle and other vertebrate muscles where the muscle fibres are parallel.

The mechanical performance of the prothoracic flexor tibialis muscle of Carausius has been similarly examined. When lying ventral surface uppermost with its tarsi free in the air, as in the preparation used in this work, Carausius is very passive, and difficult to excite by natural stimulation. Stimuli were therefore applied to the crural nerve in the thorax at a frequency of about 20/sec. when testing mechanical performance. This frequency of stimulation produced a rapid tetanic contraction in the flexor. Weights were applied to the tip of the tibia by means of cotton thread, and the maximum weight which could be lifted during such a contraction was determined.

In a typical case the flexor of an adult insect was able to lift up to 2 g. At the latter weight flexion could be maintained only for about 1 sec., after which a period of rest was necessary before the muscle could again be stimulated to lift the weight. This weight was therefore taken as the maximum load which the muscle was capable of lifting. The muscle weighed 9 mg., and the lengths of the tibia and femur were 1·8 and 1·85 cm respectively. Longitudinal sections showed the attachment of the apodeme to the head of the tibia to be about 0·3 mm. from the fulcrum. The lever factor was therefore approximately 60:1 and the peak tension developed by the muscle in lifting 2 g. was about 13,000 g./g. muscle weight, compared with 20,000 g./g. in the locust (Hoyle, 1955b). In terms of mean crosssection area of individual fibres the figure is about 800 g./cm.a, compared with 1000 g./cm.2 in frog and locust (Hoyle, 1955b). Variation between individuals might lessen the difference between figures for the two animals, but would be unlikely to abolish it.

The tetanus:twitch ratio was measured by a simple lever system. It was found to be over 25:1.

The electrical responses of the muscle fibres were studied by means of glass capillary intracellular microelectrodes. The preparation and procedure have been described previously (Wood, 1957). Mechanical responses were recorded with a simple electromechanical transducer (see Hoyle, 1955b). The output from the transducer was fed to the Y-plates of the oscillograph.

The two types of axons in the crural nerve were stimulated independently of one another by means of the anodal blocking technique of Kuffler & Vaughan Williams (1953). Impulses passing down the crural nerve were monitored from time to time, using tapered silver wire electrodes and an a.c. mains amplifier, also connected to the Y-plates of the oscillograph.

A single stimulus applied to the ‘fast’ (F) axon at above threshold level produced a quick twitch of the flexor tibialis muscle. This was accompanied by flexion of the tibia which, although brisk, was very slight in extent (Fig. 2A) and in most cases below the recording level of the mechanical transducer. Where recording was achieved increased tibial flexion was observed when the stimulus intensity was raised very gradually from threshold level, suggesting a recruitment of fibres of different thresholds. The increase in stimulus intensity and the increase in the mechanical response were so small that it is impossible to state with certainty the number of similar fibres present; but there appear to be at least four.

Fig. 2.

Mechanical records of F responses. A, single twitches; B, tetanus resulting from repetitive stimulation at 20 stimuli per second. The time-scale refers to A, which is magnified by about 2 × as compared with B.

Fig. 2.

Mechanical records of F responses. A, single twitches; B, tetanus resulting from repetitive stimulation at 20 stimuli per second. The time-scale refers to A, which is magnified by about 2 × as compared with B.

In the locust del Castillo, Hoyle & Machne (1953) found that when single shocks of high intensity were applied to the F axon they were followed by a tetanic contraction of the extensor tibialis muscle. This effect has not been observed in Carausius, in which a single shock of any intensity applied to the F axon results in a single twitch of the muscle.

The F electrical response has been described previously (Wood, 1957) and is shown in Fig. 3. In the insect’s own haemolymph, containing 18 m. equiv. potassium ions/litre, Wood (1957) found that the resting potential of six fibres averaged 41 mV. ± 1·5 (S.E.) and the action potential of the same fibres averaged 39 mV. ± 2·2. The action potential shows greater variation in magnitude from fibre to fibre than the resting potential. The rising phase occupies about 6 msec, and the rate of rise is about 5–7 V./sec. It is followed by a long decay phase of about 100–150 msec. The rising phase is composed of two components, the end-plate or junctional potential and the spike or active membrane response. In many cases small overshoots of the active membrane response above the zero potential line are recorded. These never exceed about 8 mV. in size, and the majority are only a few mV. above the zero potential line.

Fig. 3.

Two examples, on different time bases, of F responses from two separate fibres of the same muscle.

Fig. 3.

Two examples, on different time bases, of F responses from two separate fibres of the same muscle.

Paired stimulation of the F axon

Stimuli were applied to the F axon in pairs, the interval between the two members of each pair being progressively reduced in successive experiments. The results are shown in Fig. 4. In Fig. 4A the stimuli were sufficiently apart in time for each to evoke a separate action potential. In Fig. 4B–D the second stimulus was applied at various times during the decay phase of the first response, and the second stimulus continued to elicit a second response, although the second action potential decreased in size as it approached the peak of the first action potential. In Fig. 4E-F the second stimulus was applied during the upper part of the rising phase of the first response, and in G–J during the lower part of its rising phase. In Fig. 4E–F the second response still falls in the decay phase of the first and continues to diminish in size as it approaches the peak of the latter. There may be a very small remnant in Fig. 4G but in H and J the second response has disappeared as a separate entity. However, in H and J the second stimulus was applied at or below the small inflexion which is presumed to mark the junction between the junctional potential and the active membrane response; and although there is no separate second response the single action potential observed is larger in size than those resulting from single shocks. The single shock responses in Fig. 4A–F have a magnitude of about 42 mV., whereas the response in G measures about 53 mV., and in H and J about 60 mV. Judging by the position of the inflexion in the rising phase, the active membrane response remained constant in size, or nearly so, at about 20 mV. throughout the experiment. In H and J, and presumably in G, it is the junctional potential which increases in size.

Fig. 4.

The effect of paired stimuli on the F response. From A to J, the interval between the two stimuli was progressively reduced. Stimulus artifacts appear as small downward strokes.

Fig. 4.

The effect of paired stimuli on the F response. From A to J, the interval between the two stimuli was progressively reduced. Stimulus artifacts appear as small downward strokes.

Repetitive stimulation of the F axon

When the F axon is stimulated repetitively at frequencies above approximately 5/sec. a tetanic contraction is observed. At 5/sec. the tetanus is only partial, and individual twitches are clearly marked. Progressive fusion of these occurs up to a frequency of about 25 stimuli/sec.: a recording at 20 stimuli/sec. is shown in Fig. 2B. Above 25 stimuli/sec. the contraction is smooth. At this frequency the electrical responses are still discrete, and fusion of them does not begin until frequencies of about 50/sec. are approached. There is no evidence of facilitation while the electrical responses remain separate. Summation at high frequencies might be expected, in view of the experiments with paired stimuli; but this is offset by the tendency to fatigue at frequencies of about 20/sec. and above. This is shown by a progressive decrease in the ability to lift weights, and is often accompanied by a progressive diminution in size of the action potential (see Fig. 8).

Effect of temperature on the F response

Action potentials were recorded from muscle fibres bathed in salines at temperatures between 5° and 30° C. The electrode was kept in the same fibre throughout the experiment. As the temperature was lowered, the time course of the action potential lengthened, and the response became somewhat smaller in amplitude (Fig. 5). At the same time the latent period between the stimulus artifact and the onset of the action potential increased.

Fig. 5.

Records of the F response at A, 5°; B, 10°; C, 15° ; D, 20°; and E, 30° C.

Fig. 5.

Records of the F response at A, 5°; B, 10°; C, 15° ; D, 20°; and E, 30° C.

As the temperature was lowered progressively an inflexion appeared in the rising phase of the action potential (Fig. 5). This inflexion appears to mark the junction between the junctional potential and the active membrane response (Wood, 1957). The rate of rise of the two components changes at a comparable rate in the different temperatures. The inflexion therefore probably results from an increase in the time taken for the initiation of the active membrane response when the junctional potential reaches a critical threshold level, due to the decreasing rate of rise of the junctional potential as the temperature is lowered.

Effect of drugs on the F response

In an attempt to identify a possible neuromuscular transmitter, substances known to affect the excitability of nerves and muscles of other groups of animals were added to the bathing medium in concentrations effective in these animals, and the F responses were recorded. The test salines were allowed to bathe the muscle for at least 30 min. and in some cases for several hours. Substances tested in this way were atropine, sodium azide, 5-hydroxytryptamine, reserpine, chlorpromazine (given by Messrs May and Baker) strophanthin, histamine, acetylcholine, physostigmine, and noradrenalin. In the experiments involving the three latter drugs either ‘hyalase’ (a commercial preparation of hyaluronidase given by Messrs Bengers) or trypsin was added to the salines at concentrations of 1000 units/ml. and 0·1 % by weight respectively.

No significant alteration in the size or time course of the action potential occurred in any of these experiments.

The ‘slow’ response

Spontaneous activity is rare in this preparation but occasionally spontaneous movements of the tibiae, accompanied by electrical activity and contraction in the flexor muscle, have been observed. Some of these movements were brisk and appear from the records to have been due to F responses ; but others were slower and smoother in character. Such slow, smooth movements were found to be associated with a second type of mechanical and electrical response, termed here the ‘slow’ (S) response. Whether spontaneous or evoked by single shock stimulation of the S axon (Fig. 6) the S electrical responses vary between 5 and 20 mV. in magnitude. In appearance they are very similar to junctional potentials and have an exponential decay phase. Their rate of rise is 1–1·5 V./sec., and although they may rise above the threshold level of the junctional response at which an active membrane response is normally initiated in the case of the F response, no inflexion has been observed in the rising phase of the largest S responses. This does not, of course, prove that no active component is present.

Fig. 6.

Single S responses recorded : A, during spontaneous activity ; B, during stimulation of the S axon.

Fig. 6.

Single S responses recorded : A, during spontaneous activity ; B, during stimulation of the S axon.

Repetitive stimulation of the S axon

If a single shock is applied to the S axon the muscle fibres can be seen to give a very faint twitch, but no movement of the tibia is detected. Several successive stimuli are necessary before a contraction occurs which will move the tibia.

When the S axon is stimulated at a sufficiently high frequency the S electrical responses show a marked tendency toward facilitation (Fig. 7 A). At frequencies of about 10·15 sec. these responses begin to fuse together (Fig. 7B). As the frequency of stimulation is raised, the extent and speed of contraction of the muscle increases. This may be coupled with an increase in depolarization of the membrane.

Fig. 7.

Repetitive stimulation of the S axon. A, facilitation at about 10 stimuli/sec. ; B, summation of responses at 50 stimuli/sec. Upper trace, tension ; lower trace, electrical responses (B only).

Fig. 7.

Repetitive stimulation of the S axon. A, facilitation at about 10 stimuli/sec. ; B, summation of responses at 50 stimuli/sec. Upper trace, tension ; lower trace, electrical responses (B only).

Occurrence of F and S responses

It is evident, both from observations made during spontaneous activity and from electrical stimulation of the crural nerve, that F and S responses can occur together in the same muscle fibre. When this happens, F responses are simply superimposed upon the S depolarization (Fig. 8).

Fig. 8.

Stimulation of the S axon, followed by simultaneous stimulation of the F axon, both at 40 stimuli/sec. Note the progressive decline of the F response at this frequency. Upper trace, tension ; lower trace, electrical responses.

Fig. 8.

Stimulation of the S axon, followed by simultaneous stimulation of the F axon, both at 40 stimuli/sec. Note the progressive decline of the F response at this frequency. Upper trace, tension ; lower trace, electrical responses.

Over sixty experimental animals have been examined and over 4000 separate muscle fibres have been impaled at random during the course of this work, about 1000 in the metathoracic leg, and over 3000 in the prothoracic leg. Many of these fibres were superficial fibres in which the F responses only were studied, in connexion with previous work (Wood, 1957). F and S responses have been looked for at all positions and depths of the flexor muscles of different animals in only about 1000 fibres. This is an insufficient sample for definite conclusions to be drawn. Nevertheless, F responses have been found in every fibre impaled, and S responses in every fibre in which they have been looked for. It may therefore be tentatively concluded that all fibres of the flexor tibialis muscle are innervated by both F and S axons.

The resting potential of the muscle fibres of Carausius at 41 mV. is at the lower level of the normal range for insect muscle fibres. In insects, the highest value so far reported has been 60 mV. in Locusta and Schistocera (Hoyle, 1957 a) and in Gampsocleis and Platypleura (Hagiwara & Watanabe, 1954); and the lowest value the figure of 42 mV. recorded by the latter authors in Mecopoda and Graptosaltria.

In the muscles of Acrididae the size of the action potential appears to be related to that of the resting potential, and there is less likelihood of an overshoot of zero potential in muscle fibres with low resting potentials (Hoyle, 1957 a). Nevertheless such overshoots, although small in size, often occur in Carausius; and Wood (1957) found that they might persist in this insect even in potassium concentrations sufficient to reduce the resting potential to 20 mV. Hoyle (1957a) has shown that there is evidence that the extent of contraction of an insect muscle is related to the degree of depolarization of the muscle fibre membrane. Herbivorous insects typically have a high blood potassium concentration related to their diet (Boné, 1955; Duchâteau, Florkin & Leclerq, 1953) and Hoyle (1954) inferred that such insects might be condemned to sluggish movement owing to the resulting low resting potential. This view was based on experiments with the locust, an herbivorous insect which, however, is anomalous in having blood ion ratios typical of carnivorous insects (Hoyle, 1955 c). The presence of overshoots in Carausius muscle fibres suggests the possibility that some degree of adaptation to low resting potentials may be present in the process responsible for the active membrane response in herbivorous insects, though its probable basis is obscure. It is also possible that the coupling of contraction to membrane depolarization is not a direct one in insects : Hoyle (1957b) has presented evidence that in crustaceans it is not. A complex coupling mechanism could quite possibly possess properties which would allow adaptations resulting in increased activation of the contractile mechanism by smaller depolarization. The mechanical performance of Carausius muscle is of interest in this connexion. The tension developed by fibres of its prothoracic flexor tibialis is four-fifths of that developed by fibres of the locust jumping muscle (both muscles in their natural media). Yet the action potential in Carausius is only a little over one-half that of the locust in size (see Hoyle, 1955 c).

The very high tetanus/twitch ratio in Carausius lends support to the suggestion made by Hoyle (1955 b) that in arthropods the contractile material is not fully activated by a single muscle depolarization, however complete, but that more than one is required for full activation.

The F response in Carausius is similar to that observed in other insects (see Hoyle, 1957a) and to certain ‘fast’ responses found in crustaceans by Furshpan (1955). Detailed studies of insect fast responses have been confined to the locust (del Castillo et al. 1955 ; Hoyle, 1955b, c, 1957a) and to a lesser extent to the cockroach (Hoyle, 1955 c). In the locust, progressive lowering of the temperature results in a lengthening of the time course and a reduction in size of the response, and an inflexion becomes increasingly apparent in the rising phase. Below about 8° C. the active membrane response disappears. The F response in Carausius is affected by temperature variation in the same way, but to a lesser degree; for example, the active membrane response is still present at 5° C. This is surprising at first sight, because according to Chopard (1938) C. morosus is a strictly tropical insect from the Far East, where diurnal and seasonal temperatures remain at a fairly high and constant level. Some degree of accommodation may have resulted from continuous breeding in this country for many years.

The ability of the junctional potential to summate shows it to be a graded response. Summation could be due to the liberation of a further quantity of a transmitter substance by a subsequent stimulus. The active membrane response, on the other hand, exhibits refractoriness and does not appear to summate with a further active membrane response. This suggests an all-or-nothing process. In vertebrates Hodgkin (1951) has shown that refractoriness of the spike potential results from the high potassium conductance which occurs during this phase of the action potential, and to a lesser extent to the inactivation of the ‘sodium carrier’ by the intense depolarization of the propagated response. Wood (1957) obtained evidence that a specific ‘sodium carrier’ may not be present in Carausius, but that the process responsible for the production of the action potential could be explained on a similar general basis to that which produces the vertebrate action potential. The present results support this view. If it is correct, the nature of the neuromuscular transmitter is of interest. There is no direct evidence that a transmitter substance occurs in insects, but its presence in the locust and cockroach has been inferred by Hoyle (1955 c). The lack of any action of common pharmacological drugs suggests that neuromuscular transmission in Carausius is not cholinergic, nor is there any indication that the transmitter is any other well-known drug. The effects of some quaternary ammonium compounds other than acetylcholine are ambiguous (Wood, 1957), but do not encourage the view that they are involved. However, it is just possible that the diffusion barrier set up by the tracheolated connective tissue around the muscle fibres of Carausius and other insects (Hoyle, 1953 ; Wood,1957) could prevent an externally applied drug from reaching the junctional receptors in sufficient concentration to overcome the action of any destructive enzyme system which might be present. But if this was so, physostigmine might still be expected to exert some effect. The fact that it has none strengthens the probability that acetylcholine is not the transmitter. The possibility of a diffusion barrier effect of this kind is lessened, but not disproved, by the lack of effect of hyaluronidase and trypsin.

The S responses of Carausius muscle fibres are comparable with the S1 responses described by Hoyle (1955b) in the locust, and with the slow responses observed by Furshpan (1955) in the muscle fibres of Cambarus, although they more nearly resemble the latter in exhibiting no active membrane response. The alterations in speed and extent of contraction accompanying changes in the frequency of stimulation of the S axon show that very delicately graded movements of the muscle could be obtained naturally by the animal by this means. During spontaneous activity S responses have been observed which appear to hold the muscle at a particular level of contraction. There seems to be no need for a second slow response of the type described by Hoyle (1955 b) which in the locust is responsible for the performance of very slow movements and for the maintenance of tonus. The flexor tibialis of Carausius is innervated by a number of F axons which evoke similar responses. Control of fast activity could therefore be achieved by the animal both by altering the frequency of impulses passing down each F axon and by the typical vertebrate method of varying the number of axons operating at a given time. There is no evidence that there may be a similar duplication of S axons, but if it occurs the control of slow activity would be even finer.

Friedrich (1933) claimed to have demonstrated peripheral inhibition in the flexor of Carausius. He stimulated the flexor at an intensity just below that required for excitation and observed a slight further relaxation of the resting muscle. He also stimulated the muscle at a similar intensity while it was relaxing from a contraction and found that the rate of relaxation increased. Ripley and Ewer (1951) suggested that this effect could have been obtained from a loosely held preparation by contraction of the coxal muscles. Another possibility is that reflex slow contraction of the extensor muscle occurred through stimulation of afferent fibres in the crural nerve. The effects, as shown in Friedrich’s (1933) records, were in any case very slight. In the present work stimulation at different intensities, using the Kuffler & Vaughan Williams (1953) technique, has failed to reveal any evidence of the existence of an inhibitory axon; such histological evidence as there is, also argues against the presence of such an axon.

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