Fast drum strokes: Novel and convergent features of sonic muscle ultrastructure,innervation, and motor neuron organization in the pyramid butterflyfish (hemitaurichthys polylepis)

Sound production that is mediated by intrinsic or extrinsic swim bladder musculature has evolved multiple times in teleost fishes. Sonic muscles must contract rapidly and synchronously to compress the gas‐filled bladder with sufficient velocity to produce sound. Muscle modifications that may promote rapid contraction include small fiber diameter, elaborate sarcoplasmic reticulum (SR), triads at the A–I boundary, and cores of sarcoplasm. The diversity of innervation patterns indicate that sonic muscles have independently evolved from different trunk muscle precursors. The analysis of sonic motor pathways in distantly related fishes is required to determine the relationships between sonic muscle evolution and function in acoustic signaling. We examined the ultrastructure of sonic and adjacent hypaxial muscle fibers and the distribution of sonic motor neurons in the coral reef Pyramid Butterflyfish (Chaetodontidae: Hemitaurichthys polylepis) that produces sound by contraction of extrinsic sonic muscles near the anterior swim bladder. Relative to adjacent hypaxial fibers, sonic muscle fibers were sparsely arranged among the endomysium, smaller in cross‐section, had longer sarcomeres, a more elaborate SR, wider t‐tubules, and more radially arranged myofibrils. Both sonic and non‐sonic muscle fibers possessed triads at the Z‐line, lacked sarcoplasmic cores, and had mitochondria among the myofibrils and concentrated within the peripheral sarcoplasm. Sonic muscles of this derived eutelost possess features convergent with other distant vocal taxa (other euteleosts and non‐euteleosts): small fiber diameter, a well‐developed SR, and radial myofibrils. In contrast with some sonic fishes, however, Pyramid Butterflyfish sonic muscles lack sarcoplasmic cores and A–I triads. Retrograde nerve label experiments show that sonic muscle is innervated by central and ventrolateral motor neurons associated with spinal nerves 1–3. This restricted distribution of sonic motor neurons in the spinal cord differs from many euteleosts and likely reflects the embryological origin of sonic muscles from hypaxial trunk precursors rather than occipital somites. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.     

粘虫蛾飞行肌超微结构的研究

应用电子显微镜对粘虫雌蛾Mythimna separata(Walker)飞行(背纵)肌的研究结果表明,其肌原纤维由500-700根肌球蛋白丝(粗丝)组成,每根粗丝由6根肌动蛋白丝(细丝)环绕排列成六角形,每根细丝精确地位于两根粗丝间1/2处,从而使粗丝和细丝的比为1：3。肌节较短,长度约2.2-2.6μm。肌原纤维之间充满着线粒体和横管。每个肌节约有线粒体三个,横管二根。线粒体约占肌纤维体积的40%,而横管为7%。每根横管准确地位于肌节的1/4、3/4处,或Z线和中膈的中央,并与肌质网交接形成二位体(dyads)或三位体(triads)。肌质网相当不发达,约占肌纤维体积的2.5%。但其分布很有特色,即除了紧贴于肌原纤维周围的由单层液泡组成的肌质网以外,在中膈处还有一层横穿于肌原纤维的肌质网。和其它同步飞行肌的结构和功能分析比较的结果还表明,粘虫蛾飞行肌具有较善于飞行的结构。     

The primary body-wall musculature in the arrow-worm Sagitta setosa (Chaetognatha): An ultrastructural study

The primary musculature of Sagitta is mainly made up of two kinds of alternating fibers, A and B. These fibers differ markedly in their localization in the muscular tissue, by the development of their SR and their mitochondria, and the shape of their myofibrils. Their contractile apparatus is similar and possesses myofibrils of regular thickness with very short I bands, flanked by invaginations which are large compartments communicating with the extracellular space. This fiber diversity appears and is maintained in the presence of an apparent common innervation. Nerve endinglike structures are scattered in the epidermis against the basement membrane and there are no nerves beneath this. The presence of at least two kinds of fibers in the primary musculature and the presence of the secondary musculature would suggest that the displacements of sagitta may be more complex than is generally admitted. The specializations of the trunk musculature underline the degree of specialization in the Chaetognatha phylum.     

A study of the fine structure of the accessory muscle of the horseshoe crab,Tachypleus gigas

The accessory muscle of the walking leg of the horseshoe crab, Tachypleus gigas, was examined electron microscopically. The muscle fibers vary in size but are small in diameter, when compared with other arthropod skeletal muscles. They are striated with A, I, Z and poorly defined H bands. The sarcomere length ranges from 3-10 μm with most sarcomeres in the range of about 6 μm. The myofilaments are arranged in lamellae in larger fibers and less well organized in the smaller ones. Each thick filament is surrounded by 9-12 thin filaments which overlap. The SR is sparse but well organized to form a fenestrated collar around the fibrils. Individual SR tubules are also seen among the myofibrils. Long transverse tubules extend inward from the sarcolemma to form dyads or triads with the SR at the A-I junction. Both dyads and triads coexist in a single muscle fiber, a feature believed to have evolutionary significance. The neuromuscular relationship is unique. In the region of synaptic contact, the sarcolemma is usually elevated to form a large club-shaped structure containing no myofilaments and few other organelles. The axons or axon terminals and glial elements penetrate deep into the club-shaped sarcoplasm and form synapses with the fiber. As many as 13 terminals have been observed within a single section. Synaptic vesicles of two types are found in the axon terminals.     

Fine structure of the drum muscles of the piranha (serrasalminae,characidae)

Summary The anterior and the posterior drum muscles of the piranha resemble each other in all essential fine structural aspects: myofibrils are slender; sarcomeres are short compared with those of other drum muscles; mitochondria, located in the periphery of the fibers, are numerous and show an irregular internal structure; and the sarcoplasmic reticulum is abundant. Triads appear at the level of the Z lines. The drum muscles have many motor endplates, which, however, lack the characteristic junctional-fold apparatus. No lipid substances could be demonstrated in these muscles. In the posterior drum muscle the fibers depart from their orderly longitudinal arrangement at irregular intervals.     

Fiber‐type composition in the perivertebral musculature of lizards: Implications for the evolution of the diapsid trunk muscles

The perivertebral musculature of lizards is critical for the stabilization and the mobilization of the trunk during locomotion. Some trunk muscles are also involved in ventilation. This dual function of trunk muscles in locomotion and ventilation leads to a biomechanical conflict in many lizards and constrains their ability to breathe while running (“axial constraint”) which likely is reflected by their high anaerobic scope. Furthermore, different foraging and predator‐escape strategies were shown to correlate with the metabolic profile of locomotor muscles in lizards. Because knowledge of muscle's fiber‐type composition may help to reveal a muscle's functional properties, we investigated the distribution pattern of muscle fiber types in the perivertebral musculature in two small lizard species with a generalized body shape and subjected to the axial constraint (Dipsosaurus dorsalis, Acanthodactylus maculatus) and one species that circumvents the axial constraint by means of gular pumping (Varanus exanthematicus). Additionally, these species differ in their predator‐escape and foraging behaviors. Using refined enzyme‐histochemical protocols, muscle fiber types were differentiated in serial cross‐sections through the trunk, maintaining the anatomical relationships between the skeleton and the musculature. The fiber composition in Dipsosaurus and Acanthodactylus showed a highly glycolytic profile, consistent with their intermittent locomotor style and reliance on anaerobic metabolism during activity. Because early representatives of diapsids resemble these two species in several postcranial characters, we suggest that this glycolytic profile represents the plesiomorphic condition for diapsids. In Varanus, we found a high proportion of oxidative fibers in all muscles, which is in accordance with its high aerobic scope and capability of sustained locomotion. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.     

Morphometry of muscle fibre types in the carp (Cyprinus carpio L.)

Summary Ultrastructural parameters of muscle fibre types of the carp (Cyprinus carpio L.) were measured and compared with their contractile properties. In red fibres, which are slower than pink fibres, the relative length of the junction between the T system and the sarcoplasmic reticulum (T-SR junction) is smaller and the Z lines are thicker than in pink fibres. Pink fibres have a smaller relative length of T-SR junction than white fibres from the axial muscles. The two types of red fibres present in carp muscle also differ in their relative lengths of T-SR junction. Significant differences in the relative areas of the SR were not found.The relative volume of myofibrils in red fibres is two-thirds that in pink fibres, a difference that is not reflected in the maximal isometric tetanic tensions of these types. Red fibres, which are less easily fatigued than pink fibres, have larger relative volumes of subsarcolemmal and intermyofibrillar mitochondria. Small pink fibres have a larger relative volume of subsarcolemmal mitochondria than large pink fibres, but have a similar relative volume of intermyofibrillar mitochondria. Small and large pink fibres differ in the relative volumes of their membrane systems, but have similar relative lengths of T-SR junction.     

The membrane systems of the cardiac muscle cell of Meganychtiphanes norvegica (M. Sars), euphauciacea,crustacea

Summary The membrane systems of cardiac muscle cells of the euphausiacean Meganychtiphanes norvegica are described. Transverse tubules are found both at the Z-band level (T_z-tubules) and at the H-band level (T_h-tubules). Within the sarcomere narrow longitudinal tubules branch off from the T_z-tubules. At the H-band level these tubules expand forming flattened cisternae in dyadic and triadic couplings with the sarcoplasmic reticulum (SR). Adjacent myofibrils are separated by a well developed SR. Modifications of the SR are seen at the H-band level where junctional cisternae are formed.     

High -resolution scanning electron-microscopic studies on the three-dimensional structure of mitochondria and sarcoplasmic reticulum in the different twitch muscle fibers of the frog

Summary The three-dimensional structure of the mitochondria and sarcoplasmic reticulum (SR) in the three types of twitch fibers, i.e., the red, white and intermediate skeletal muscle fibers, of the vastus lateralis muscle of the Japanese meadow frog (Rana nigromaculata nigromaculata Hallowell) was examined by high resolution scanning electron microscopy, after removal of the cytoplasmic matrices.The small red fibers have numerous mitochondrial columns of large diameter, while the large white fibers have a small number of mitochondrial columns of small diameter. In the medium-size intermediate fibers, the number and diameter of the mitochondrial columns are intermediate between those of the red and white fibers.In all three types of fibers, the terminal cisternae and transverse tubules form triads at the level of each Z-line. The thick terminal cisternae continue into much thinner flat intermediate cisternae, through a transitional part where a row of tiny indentations can be observed. Numerous slender longitudinal tubules originating from the intermediate cisternae, extend longitudinally or obliquely and form elongated oval networks of various sizes in front of the A-band, then fuse to form the H-band collar (fenestrated collar) around the myofibrils. On the surface of the H-band collar, small fenestrations as well as tiny hollows are seen. The three-dimensional structure of SR is basically the same in all three muscle fiber-types. However, the SR is sparse on the surface of mitochondria, so the mitochondria-rich red fiber has a smaller total volume of SR than the mitochondria-poor white fiber. The volume of SR of the intermediate fiber is intermediate between other the two.     

Scanning electron-microscopic studies on the three-dimensional structure of mitochondria in the mammalian red,white and intermediate muscle fibers

Summary The three-dimensional structure and arrangement of mitochondria in the red, white and intermediate striated muscle fibers of the rat were examined under a field-emission type scanning electron microscope after removal of cytoplasmic matrices by means of the Osmium-DMSO-Osmium procedure.Beneath the sarcolemma, spherical or ovoid subsarcolemmal mitochondria show accumulations. The mitochondria are numerous and large in size in the red fibers, intermediate in the intermediate fibers, and few and small in the white fibers. Paired, slender I-band-limited mitochondria were located on both sides of the Z-line and partly embraced the myofibrils at the I-band level; they occurred in all three types of fibers. In the intermyofibrillar spaces, numerous mitochondria formed mitochondrial columns. These columns were classified into two types: 1) thick mitochondrial columns, formed by multiple mitochondria each with an intermyofibrillar space corresponding to one sarcomere in length, and 2) thin mitochondrial columns, established by single mitochondria corresponding to one sarcomere in length. In the red fibers mitochondrial columns were abundant and the ratio of the thick and thin columns was almost the same, while in the intermediate fibers most of the columns belonged to the thin type. The white fibers displayed rare, very thin columns.     

An electron microscope study of myofibril formation in embryonic rabbit skeletal muscle

Trunk and limb muscles from fetal and newborn rabbits were investigated by means of light and electron microscopes. At 14 days gestation, the presumptive myoblasts migrate away from the myotome to form the anlage of the muscle of the trunk and limb. Among the population of undifferentiated cells, the myoblasts were recognized due to the presence of actin and myosin filaments. The aggregates of thin and thick filaments appear at the periphery of the cells. There is a great variety of filament assembly. The presence of Z band material appears to be essential for sarcomere formation. At 14 days of gestation the myotubes are more numerous in the limb than in the trunk. The presence of unmaturated fibrils with absence of the M line in the sarcomeres was observed. By day 18 of gestation the myotubes are wider and aggregate to form small bundles. The myofibrils were more numerous and the vesicles of the SR precursor, partly incrustated with ribosomes were dispersed among them. At day 22 of gestation the myotubes are thicker because of the myofibrils which are far more numberous. The sarcomeres were more fully developed, with the M line present. At day 28 of gestation and 3 days after delivery the already developed myofibers were present with a well organized SR system and fully developed sarcomeres.     

Rattlesnake shaker muscle: I. A light microscopic and histochemical study

Rattlesnake body and shaker muscles were studied using light microscopy and histochemistry. Five myofiber types are distinguishable in the body musculature. The majority are large diameter fast twitch fibers with high alkaline-stable ATPase activity and few mitochondria. In the shaker muscle the major fiber differs from all body fibers in that myofibrils do not entirely fill the fibers. The myofibrils branch repeatedly with one another, which leaves large areas of sarcoplasm devoid of filaments and gives the fibers a characteristic mottled appearance. Mitochondria and glycogen deposits are very numerous. Shaker fibers have high alkaline stable ATPase activity and, in addition, stain intensely for NADH-TR and _αGPD. Myofibers of the shaker muscle are unusual in that they are extremely fast contracting yet are highly fatigue resistant.     

FINE STRUCTURE OF RAT INTRAFUSAL MUSCLE FIBERS : The Polar Region

An ultrastructural comparison of the two types of intrafusal muscle fibers in muscle spindles of the rat was undertaken. Discrete myofibrils with abundant interfibrillar sarcoplasm and organelles characterize the nuclear chain muscle fiber, while a continuous myofibril-like bundle with sparse interfibrillar sarcoplasm distinguishes the nuclear bag muscle fiber. Nuclear chain fibers possess well-defined and typical M bands in the center of each sarcomere, while nuclear bag fibers contain ill-defined M bands composed of two parallel thin densities in the center of the pseudo-H zone of each sarcomere. Mitochondria of nuclear chain fibers are larger and more numerous than they are in nuclear bag fibers. Mitochondria of chain fibers, in addition, often contain conspicuous dense granules, and they are frequently intimately related to elements of the sarcoplasmic reticulum (SR). Striking differences are noted in the organization and degree of development of the sarcotubular system. Nuclear bag fibers contain a poorly developed SR and T system with only occasional junctional couplings (dyads and triads). Nuclear chain fibers, in contrast, possess an unusually well-developed SR and T system and a variety of multiple junctional couplings (dyads, triads, quatrads, pentads, septads). Greatly dilated SR cisternae are common features of nuclear chain fibers, often forming intimate associations with T tubules, mitochondria, and the sarcolemma. Such dilatations of the SR were not encountered in nuclear bag fibers. The functional significance of these structural findings is discussed.     

Extraocular muscles in the lamprey, Lampetra fluviatilis L. I. Muscle fibres

Six extraocular muscles of the river lamprey, Lampetra fluviatilis L., were studied with the light and electron microscope. On the basis of morphology and histochemistry three types of muscle fibres were distinguished: thin, thick mitochondria-rich and thick multifibrillar fibres. In the thin fibres, 2.8-22.4 microns in diameter, myofibrils are distributed peripherally and show strong ATPase activity. The mitochondria are located paraxially. In the thick mitochondria-rich fibres, 19.4-31.0 microns in diameter, myofibrils are also located peripherally, whereas the central part of the fibre is densely packed with very numerous mitochondria possessing tubular cristae. Thick multifibrillar fibres, with a diameter similar to that of the former type, contain thin myofibrils scattered over the entire cross-section of the fibre. The activity of myofibrillar ATPase is lower in both types of thick fibres than in the thin ones. The tubules of the T system were observed frequently only in the thick multifibrillar fibres. The extraocular muscles of the lamprey are composed of large quantities of muscle fibres. Thin and thick fibres do not form separate layers, but are more or less uniformly distributed throughout the muscle. Many muscle fibres show structural features suggesting their degeneration.     

Muscular architecture of <Emphasis Type="Italic">Milnesium tardigradum </Emphasis>and <Emphasis Type="Italic">Hypsibius </Emphasis>sp. (Eutardigrada,Tardigrada) with some data on <Emphasis Type="Italic">Ramazottius oberhaeuseri</Emphasis>

The architecture of the musculature of the eutardigrade species Milnesium tardigradum Doyère, 1840, Hypsibius sp. and Ramazzottius oberhaeuseri (Doyère in Ann Sci Nat Zool Sér 2(14):269–369, 1840) is investigated by phalloidin staining and confocal laser scanning microscopy. There are methodological problems in staining eutardigrades due to physiological alterations under stress (anhydrobiosis) and due to penetration problems of the cuticle. It is helpful to fix specimens in the state of asphyxy, where animals are stretched following an oxygen shortage in their environment. The musculatures of all three species correspond in their general architecture, but differ in detail, such as in the number of muscles. All muscles are isolated muscle strands. There are on each body side two dorsal and one ventral muscle strands, in addition to a system of dorsoventral, lateral and lateroventral muscles. Seven median ventral attachment points give rise to dorsoventral, ventrolateral and appendage muscles. The appendages receive several muscles originating dorsally and ventrally. The number of muscles and the arrangement differ in each appendage. The fourth appendage shows the greatest differences with a far smaller number of muscles compared to other species. The musculature shows comparably few strict segmental patterns, for example, the musculature of each appendage differs from the other ones. By comparison with literature data on the same species and data of Macrobiotus hufelandi it can be shown that eutardigrades have a roughly comparable muscular architecture, but that there are several differences in detail. Dedicated to Professor Westheide on the occasion of his 70th birthday.     

Structural and functional development of cricket ring muscles

The sizes of the unifunctional dorsal longitudinal (DLM) and bifunctional subalar (SA) metathoracic flight muscles of the cricket Teleogryllus oceanicus increase by more than an order of magnitude between the second instar before the terminal molt and the tenth day of adult life. During the same developmental period isometric twitch duration (onset to 50% relaxation, 25 degrees C) varies little, while muscle mitochondrial content increased by a factor of ten as measured by stereological analysis of electron micrographs and citrate synthase activity (mumoles citrate . min-1 . gm protein-1, 25 degrees C). The wing muscles of adults have abundant sarcoplasmic reticulum (SR), narrow myofibrils, and a high volume density of mitochondria. At two molts from adulthood muscles that will later be used in flight behavior also have narrow myofibrils and abundant SR, but unlike muscles at later stages, nymphal muscles have a low volume density of mitochondria. At the terminal molt muscles have at least as much SR as is seen in muscles at the tenth day of adult life, and the myofibrils are also more narrow at the earlier stage. Since there is significant variation in muscle structure and little change in twitch duration during late development, the efficacy of the SR in releasing and resequestering CA2+ is seemingly lower in muscles at the terminal molt, a time of rapid muscle growth.     

Ultrastructural alterations in extrinsic eye muscles induced by vincristine.

A comparative morphological analysis of the effects of vincristine on particular types of muscle fibres of the eye and selected trunk muscles of the mouse was performed. Great resistance of the mouse organism to the action of sublethal doses of vincristine has been found. Degenerative changes of great intensity (atrophy of myofibrils, disturbances of the Z line) and the appearance of new changes, not mentioned hitherto among the vincristine myopathies (megamitochondria, intermembranous inclusions, glycogen in mitochondria and very large vacuoles) were observed in the trunk muscles of mice. The eye muscles are seem to be more resistant to the action of vincristine. The intensity of changes in the eye muscles was connected with the types of muscle fibres. Red fibres, rich in mitochondria, underwent relatively greatest changes, whereas the smallest changes were found in tonic fibres, poor in mitochondria and sarcotubular system, i.e. these structures from which spheromembranous bodies, most characteristic of the pathogenic effects of vincristine arise.     

Structural organization of two fast,rhythmically active crustacean muscles

Summary The organization of the flagellum abductor muscle and of a scaphognathite levator muscle of the green crab, Carcinus maenas, has been compared quantitatively using light and electron microscopy. These muscles are rhythmically active at relatively high frequencies and for long durations. Fibers of both muscles are interconnected to form fascicles of 50 or more fibers within which there is cytoplasmic continuity. A single muscle is made up of 8–12 fascicles. Individual fibers consist of a peripheral rind of densely packed mitochondria, a thick region of glycogen granules, and myofibrils arranged into scattered central islands. Less than half the volume-density of these muscles is contractile material, the balance being largely mitochondria and glycogen. The fibers within a muscle are structurally similar. They have short sarcomeres (about 2 m), thin to thick filament ratios of about 3:1, and junctions between the sarcoplasmic reticulum and the transverse tubules at the M line. Sarcoplasmic reticulum occupies about 10% of the myofibrillar volume-density. A well developed sarcoplasmic reticulum appears to underlie the capacities of these two muscles for high frequency contraction; extensive mitochondria and glycogen stores should confer fatigue resistance under both aerobic and anaerobic conditions.     

The musculature of the electric fish Eigenmannia virescens (South American green knife fish) characterized with cytochrome oxidase staining

Using cytochrome C-oxidase staining, different types of somatic musculature were clearly distinguished in the gymnotoid fish Eigenmannia virescens. Except for a few thin fibres in the region of the horizontal septum, which stained faintly, no others in the trunk muscle stained. Strong staining appeared in the fibres of the anal fin muscles. According to the classification of fish musculature into white, intermediate and red, only the locomotory organ of this fish has red fibres, whereas the trunk muscles are white. The red muscles along the horizontal septum, found in all other fish which have been investigated in this respect, seem to be absent. This is noteworthy since the anal fin alone provides locomotion while the trunk muscles are responsible for posture only.     

The ultrastructure of locust pleuroaxillary "steering" muscles in comparison to other skeletal muscles

The ultrastructure of locust muscles with different function is examined: the pleuroaxillary flight steering muscle is compared with a typical flight (power muscle) and a typical leg muscle, in particular with respect to sarcomere length, tracheation, mitochondria, and sarcoplasmatic reticulum. The pleuroaxillary muscle exhibits some features characteristic of flight muscles but most of the ultrastructure resembles that of leg muscles. This is in agreement with the innervation of this muscle by an octopaminergic neuron, which also innervates leg muscles but no other flight muscles. It also supports the hypothesis that octopaminergic neurons are important metabolic regulators and that the above muscle types exhibit important differences in energy metabolism.