The Croonian Lecture, 1967: The activation of striated muscle and its mechanical response

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).

Author(s):  
R. M. A. P. Ridge

This paper is concerned with a re-examination of the pattern of nerve activity from receptors in ray fin muscles in response to stretch applied to the muscles. In earlier work receptors have been found in the fin muscles of elasmobranchs, those in rays being described in a recent paper by Bone & Chubb (1975 - which see for references to earlier anatomical work) and physiologically by Fessard & Sand (1937). The receptors are supplied by myelinated axons, and the endings take the form of beaded nerve strands associated with congregations of connective tissue lying between muscle fibres. In the pectoral fin muscles these structures lie between small-diameter muscle fibres, with multiple motor nerve endings, which occur superficially in the muscle. Most of these muscle fibres show a positive staining reaction for succinic dehydrogenase (SDH) and lipid, though some are negative for SDH. They contrast with the larger fibres, which show negative staining reactions for SDH and lipid, andhave focal motor innervation. The latter make up the bulk of the muscle (Bone & Chubb, 1975). It seems very likely that most of the small fibres are slow contracting (possibly with no propagated action potential in the muscle fibre), and the large fibres are of a twitch type. This would parallel the arrangement in dogfish myotomes (Bone, 1966). Bone & Chubb consider the coupling between the endings and the muscle fibres to be generally loose, although they also describe occasional sites of much tighter coupling. Such small muscle fibres are particularly concentrated in a superficial and rather discrete part of the muscle, here called the tonic bundle and used in the present experiments as an isolated preparation.


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.


Author(s):  
Quentin Bone

Observations are described upon the innervation of striated muscles, the innervation of the slime glands, and the subcutaneous innervation in the hagfish, Myxine glutinosa L. It is shown that the two types of striated muscle fibre receive different types of motor innervation. Presumed sensory endings are described from above the striated muscle fibres of the ventral part of the body, and are similar to those endings near to the dorsal root ganglia whichcan be traced to their cells of origin within the ganglia. It is suggested that these endings are proprioceptive in function. Other endings within the outer edge of the myosepta are described, which may possibly also have a proprioceptive function. A rich plexus of neurons is described upon the capsule of the slime glands, and these neurons, like those of the subcutaneous plexus, receive pericellular terminations from the axons of central cells. It is suggested that they are motor to smooth muscle fibres, in the slime-gland plexus being related to the expulsion of slime (together with the action of striated muscle fibres), and in the subcutaneous plexus playing some role in the control of the venous blood in the subcutaneous sinuses.


2012 ◽  
Vol 51 (No. 10) ◽  
pp. 485-489 ◽  
Author(s):  
K. Besoluk ◽  
E. Eken ◽  
E. Sur

The aim of this study is to reveal the morphology of the lyssa in the cat and dog. Eight heads of adult healthy cats and eight heads of dogs of both sexes were used as materials. In the cat the lyssa, yellow coloured, had a helical appearance and its edge facing the oral cavity became sharp; in the dog the lyssa, pinkish white coloured, was more or less J-shaped. The whole body of the cat’s lyssa was buried among the intrinsic lingual muscles. In the dog, although aboral, two thirds of the lyssa were squeezed among the intrinsic lingual muscles, its cranial third was placed just under the mucosa to protrude slightly into the oral cavity. In both species, the whole body of the lyssa was determined to have been formed by the nearly adipose tissue in which occasional striated muscles existed. Moreover, in the middle third of the dog’s lyssa, dense striated muscle fibres were seen dorsally to the adipose tissue, and we also noticed with interest that the lyssa sheath embracing this part contained few muscle spindle-like structures. It was of interest that in the cat a pyramidal rod encircled by a fine capsule of connective tissue was attached to the ventral edge of the cranial third of the lyssa.


1995 ◽  
Vol 73 (12) ◽  
pp. 2259-2265 ◽  
Author(s):  
M. N. Fernandes ◽  
S. A. Perna

The structural organization of the interbranchial septum of the gill arch of the air-breathing loricariid fish Hypostomus plecostomus was examined using light and electron microscopy. In the middle of the interbranchial septum, an extensive interconnection was found between the afferent primary arteries from successive and opposing primary lamellae. The blood circulates among numerous trabeculae consisting of connective tissue, smooth muscle cells, and collagen fibres. A sheet of smooth muscle cells is localized at the borders of these interconnected primary arteries and joins the cartilage rod from one primary lamella to the adjacent one on the same hemibranch. The adductor muscles are restricted to the distal end of the interbranchial septum and consist of transverse and oblique striated muscle fibres fixed to the cartilage rod from the primary lamella of opposite hemibranchs. The arrangement of these muscle fibres suggests a double movement of adduction: approximation of the tips of the primary lamellae of opposing hemibranchs and reduction of the space between adjacent primary lamellae of the same hemibranch. The action of both smooth and striated muscles reduces the interconnecting vascular septal space between the primary arteries, which may allow fine adjustment of vascular perfusion of the distal part of the filaments as an adaptation for better blood flow under hypoxic conditions.


The linear electrical properties of muscle fibres have been examined using intracellular electrodes for a. c. measurements and analyzing observations on the basis of cable theory. The measurements have covered the frequency range 1 c/s to 10 kc/s. Comparison of the theory for the circular cylindrical fibre with that for the ideal, one-dimensional cable indicates that, under the conditions of the experiments, no serious error would be introduced in the analysis by the geometrical idealization. The impedance locus for frog sartorius and crayfish limb muscle fibres deviates over a wide range of frequencies from that expected for a simple model in which the current path between the inside and the outside of the fibre consists only of a resistance and a capacitance in parallel. A good fit of the experimental results on frog fibres is obtained if the inside-outside admittance is considered to contain, in addition to the parallel elements R m = 3100 Ωcm 2 and C m = 2.6 μF/cm 2 , another path composed of a resistance R e = 330 Ωcm 2 in series with a capacitance C e = 4.1 μF/cm 2 , all referred to unit area of fibre surface. The impedance behaviour of crayfish fibres can be described by a similar model, the corresponding values being R m = 680 Ωcm 2 , C m = 3.9 μF/cm 2 , R e = 35 Ωcm 2 , C e = 17 μF/cm 2 . The response of frog fibres to a step-function current (with the points of voltage recording and current application close together) has been analyzed in terms of the above two-time constant model, and it is shown that neglecting the series resistance would have an appreciable effect on the agreement between theory and experiment only at times less than the halftime of rise of the response. The elements R m and C m are presumed to represent properties of the surface membrane of the fibre. R e and C e are thought to arise not at the surface, but to be indicative of a separate current path from the myoplasm through an intracellular system of channels to the exterior. In the case of crayfish fibres, it is possible that R e (when referred to unit volume) would be a measure of the resistivity of the interior of the channels, and C e the capacitance across the walls of the channels. In the case of frog fibres, it is suggested that the elements R e , C e arise from the properties of adjacent membranes of the triads in the sarcoplasmic reticulum . The possibility is considered that the potential difference across the capacitance C e may control the initiation of contraction.


1992 ◽  
Vol 282 (1) ◽  
pp. 237-242 ◽  
Author(s):  
A Jakubiec-Puka ◽  
C Catani ◽  
U Carraro

The myosin heavy-chain (MHC) isoform pattern was studied by biochemical methods in the slow-twitch (soleus) and fast-twitch (gastrocnemius) muscles of adult rats during atrophy after tenotomy and recovery after tendon regeneration. The tenotomized slow muscle atrophied more than the tenotomized fast muscle. During the 12 days after tenotomy the total MHC content decreased by about 85% in the slow muscle, and only by about 35% in the fast muscle. In the slow muscle the ratio of MHC-1 to MHC-2A(2S) remained almost unchanged, showing that similar diminution of both isoforms occurs. In the fast muscle the MHC-2A/MHC-2B ratio decreased, showing the loss of MHC-2A mainly. After tendon regeneration, the slow muscle recovered earlier than the fast muscle. Full recovery of the muscles was not observed until up to 4 months later. The embryonic MHC, which seems to be expressed in denervated adult muscle fibres, was not detected by immunoblotting in the tenotomized muscles during either atrophy or recovery after tendon regeneration. The influence of tenotomy and denervation on expression of the MHC isoforms is compared. The results show that: (a) MHC-1 and MHC-2A(2S) are very sensitive to tenotomy, whereas MHC-2B is much less sensitive; (b) expression of the embryonic MHC in adult muscle seems to be inhibited by the intact neuromuscular junction.


2002 ◽  
Vol 205 (15) ◽  
pp. 2189-2201 ◽  
Author(s):  
Fred Schachat ◽  
Margaret M. Briggs

SUMMARY Extraocular muscle exhibits higher-velocity and lower-tension contractions than other vertebrate striated muscles. These distinctive physiological properties are associated with the expression of a novel extraocular myosin heavy chain (MYH). Encoded by the MYH13 gene, the extraocular myosin heavy chain is a member of the fast/developmental MYH gene cluster on human chromosome 17 and the syntenic MYH cluster on mouse chromosome 11. Comparison of cDNA sequences reveals that MYH13 also encodes the atypical MYH identified in laryngeal muscles, which have similar fast contractile properties. Comparing the MYH13 sequence with the other members of the fast/developmental cluster, the slow/cardiac MYH genes and two orphan skeletal MYH genes in the human genome provides insights into the origins of specialization in striated muscle myosins. Specifically, these studies indicate (i) that the extraocular myosin is not derived from the adult fast skeletal muscle myosins, but was the first member of the fast/developmental MYH gene cluster to diverge and specialize, (ii) that the motor and rod domains of the MYH13 have evolved under different selective pressures and (iii) that the MYH13 gene has been largely insulated from genomic events that have shaped other members of the fast/developmental cluster. In addition, phylogenetic footprinting suggests that regulation of the extraocular MYH gene is not governed primarily by myogenic factors, but by a hierarchical network of regulatory factors that relate its expression to the development of extraocular muscles.


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