Muscle length affects the architecture and pattern of innervation differently in leg muscles of mouse, guinea pig, and rabbit compared to those of human and monkey muscles

The innervation pattern and fascicular anatomy of muscles of different lengths in mouse, guinea pig, rabbit, macaque monkey and human legs were analyzed. Neuromuscular junctions, muscle tendon junctions and ends of intrafascicularly terminating fibers were stained for acetylcholinesterase, and fascicle lengths measured. A high correlation between increasing fascicle length and increasing number of neuromuscular junctions was found, with non-primate (mouse, guinea pig, rabbit) and primate (macaque monkey, human) muscles forming two discrete groups. In non-primates, muscles with a single endplate band, fascicles were always shorter than 35 mm, fixing the limit of fiber length served by one neuromuscular junction. Muscles with fascicles longer than this had multiple discrete bands of motor endplates crossing their width at regular intervals. An increase in muscle length across or within species corresponded to an equivalent, standard increase of 10-12 mm fascicle length per motor endplate band. All human and monkey leg muscles, with the exception of gracilis and sartorius, were singly innervated and all muscle fibers ran the full distance from tendon to tendon. Singly innervated primate muscle fibers were up to 140 mm long whereas the mean distance between endplate bands in the two multiply innervated muscles was also considerably greater than in non-primates. These data indicate that allometric effects of increasing fascicle length, are distinct in common laboratory animals and two primates, when architecture and pattern of innervation are compared.     

Multifocal innervation and muscle length

Summary The dependence of the inner organisation and innervation of a skeletal muscle on its size was studied at the level of single muscle fiber architecture and motor endplate topography in muscles of different size, all of them lacking a tendinous scaffolding. The muscles evaluated in this study were: Mm. sternomastoideus, gracilis and latissimus dorsi of the rat and the M. sternocephalicus of the horse. In these muscles a subdivision into two or more innervation-compartments becomes obvious in fascicles reaching a certain length. This provides the possibility of an almost synchronous activation of the entire muscle by its nerve. At the level of single muscle fiber elements, large numbers of myo-myonal junctions were discernible in many sites. However, unequivocal multiple innervation was found, with several endplates per single muscle fiber, without the interposition of any junctional structure.Myo-myonal junctions, combined with a characteristic branching pattern of many muscle fibers, and scattered innervation sites, obviously play an important role in the architecture of fan-like muscles lacking a tendinous scaffolding.     

Reparative myogenesis in long-term denervated skeletal muscles of adult rats results in a reduction of the satellite cell population

This study, conducted on 25-month denervated rat hindlimb muscles, was directed toward elucidating the basis for the poor regeneration that is observed in long-term denervated muscles. Despite a approximately 97.6% loss in mean cross-sectional area of muscle fibers, the muscles retained their fascicular arrangement, with the fascicles containing approximately 1.5 times more fibers than age-matched control muscles. At least three distinct types of muscle fibers were observed: degenerating, persisting (original), and newly formed (regenerated) fibers. A majority of newly formed fibers did not appear to undergo complete maturation, and morphologically they resembled myotubes. Sites of former motor end-plates remained identifiable in persisting muscle fibers. Nuclear death was seen in all types of muscle fibers, especially in degenerating fibers. Nevertheless, the severely atrophic skeletal muscles continued to express developmentally and functionally important proteins, such as MyoD, myogenin, adult and embryonic subunits of the nicotinic acetylcholine receptor, and neural-cell adhesion molecule. Despite the prolonged period of denervation, slow and fast types of myosin were found in surviving muscle fibers. The number of satellite cells was significantly reduced in long-term denervated muscles, as compared with age-matched control muscles. In 25-month denervated muscle, satellite cells were only attached to persisting muscle fibers, but were never seen on newly formed fibers. Our data suggest that the absence of satellite cells in a population of immature newly formed muscle fibers that has arisen as a result of continuous reparative myogenesis may be a crucial, although not necessarily the only, factor underlying the poor regenerative ability of long-term denervated muscle.     

Reparative myogenesis in long‐term denervated skeletal muscles of adult rats results in a reduction of the satellite cell population

This study, conducted on 25‐month denervated rat hindlimb muscles, was directed toward elucidating the basis for the poor regeneration that is observed in long‐term denervated muscles. Despite a ～97.6% loss in mean cross‐sectional area of muscle fibers, the muscles retained their fascicular arrangement, with the fascicles containing ～1.5 times more fibers than age‐matched control muscles. At least three distinct types of muscle fibers were observed: degenerating, persisting (original), and newly formed (regenerated) fibers. A majority of newly formed fibers did not appear to undergo complete maturation, and morphologically they resembled myotubes. Sites of former motor end‐plates remained identifiable in persisting muscle fibers. Nuclear death was seen in all types of muscle fibers, especially in degenerating fibers. Nevertheless, the severely atrophic skeletal muscles continued to express developmentally and functionally important proteins, such as MyoD, myogenin, adult and embryonic subunits of the nicotinic acetylcholine receptor, and neural‐cell adhesion molecule. Despite the prolonged period of denervation, slow and fast types of myosin were found in surviving muscle fibers. The number of satellite cells was significantly reduced in long‐term denervated muscles, as compared with age‐matched control muscles. In 25‐month denervated muscle, satellite cells were only attached to persisting muscle fibers, but were never seen on newly formed fibers. Our data suggest that the absence of satellite cells in a population of immature newly formed muscle fibers that has arisen as a result of continuous reparative myogenesis may be a crucial, although not necessarily the only, factor underlying the poor regenerative ability of long‐term denervated muscle. Anat Rec 263:139–154, 2001. © 2001 Wiley‐Liss, Inc.     

Decreasing the cortical response to monocular deprivation need not decrease cell shrinkage in cat lateral geniculate nucleus

Summary Mammalian optic nerve axons are organised within a fascicular framework. This pattern changes between the eye and the chiasm. For most of the length of the nerve fascicular patterns are apparent, but close to the chiasm, in a region of major fibre rearrangement, the fascicular configuration is lost. It is not known how this change occurs, or whether there are less obvious systematic changes in the number of fascicles or their geometry along the length of the nerve. In this study these questions have been addressed at successive locations along the length of the cat optic nerve.The number of fascicles varied depending upon the location examined. A relatively high number were found behind the eye. The number declined in the mid-orbital portion before increasing again in the region of the optic canal. Further caudally there was a progressive change in the pattern of fasciculation, with a loss of fascicular structure medially. The remaining fascicles became concentrated around the inferotemporal periphery of the nerve. There was no fascicular organisation at the point at which the two nerves fused at the chiasm. Although the number of fascicles varied along the length of the nerve their geometric pattern did not change.     

Force-length characteristics of the in vivo human gastrocnemius muscle

In this study, the force-length characteristics of the in vivo medial (GM) and lateral (GL) heads of the human gastrocnemius muscle were estimated from measurements in eight healthy male subjects. This involved: 1) dynamometry-based measurements of the moment generated during maximal isometric plantar flexion; 2) ultrasound-based measurements of fascicular length and pennation angle; and 3) ultrasound-based calculations of moment arm lengths. All measurements were taken over the ankle angle range from 20 degrees of dorsiflexion to 30 degrees of plantar flexion. Tendon forces were calculated by dividing the moments recorded by the muscle moment arm lengths, and fascicular forces were calculated by dividing the tendon forces estimated by the cosine of pennation angle. In the transition from 30 degrees of plantar flexion to 20 degrees of dorsiflexion, the GM muscle fascicular length and force increased linearly from 24 to 39 mm and from 222 to 931 N, respectively. Over the same ankle angle range, the GL muscle fascicular length and force increased linearly from 30 to 47 mm and from 139 to 393 N, respectively. Estimates of the sarcomeric lengths corresponding to the fascicular lengths measured indicated that the two muscles operated in the range 1.4-2.2 microm, below the optimal length region for force generation according to the cross-bridge mechanism of contraction. These results indicate that the force-length relation of the in vivo human gastrocnemius muscle is limited to the ascending limb of the bell-shaped force-length curve obtained from experiments on isolated material.     

Early stages of myogenesis in a large mammal: Formation of successive generations of myotubes in sheep tibialis cranialis muscle

Summary The generation of myotubes was studied in the tibialis cranialis muscle in the sheep hindlimb from the earliest stage of primary myotube formation until a stage shortly before muscle fascicles began to segregate. Primary myotubes were first seen on embryonic day 32 (E32) and reached their maximum number by E38. Small numbers of secondary myotubes were first identified at E38, and secondary myotube numbers continued to increase during the period of study. The ratio of adult muscle fibre to primary myotube numbers was approximately 701, making it seem unlikely that every later generation myotube used a primary myotube as scaffold for its formation, as described in small mammals. By E62, some secondary myotubes were supporting the formation of a third generation of myotubes. Experiments with diffusible dye markers showed that primary myotubes extended from tendon to tendon of the muscle, whereas most adult fibres ran for only part of the muscle length, terminating with myo-myonal attachments to other muscle fibres in a series arrangement. Acetylcholinesterase (AChE) and acetylcholine receptor (AChR) aggregations appeared in multiple bands across the muscle shortly after formation of the primary generation of myotubes was complete. The number of bands and their pattern of distribution across the muscle as they were first formed was the same as in the adult. Primary myotubes teased from early muscles had multiple focal AChE and AChR deposits regularly spaced along their lengths. We suggest that the secondary generation of myotubes forms at endplate sites in a series arrangement along the length of single primary myotubes, and that tertiary and possibly later generations of myotubes in their turn use the earlier generation myofibres as a scaffold. Although the fundamental cellular mechanisms appear to be similar, the process of muscle fibre generation in large mammalian muscles is more complex than that described from previous studies in small laboratory rodents.     

Neuromuscular organization of the superior longitudinalis muscle in the human tongue. 1. Motor endplate morphology and muscle fiber architecture

Proper tongue function is essential for respiration and mastication, yet we lack basic information on the anatomical organization underlying human tongue movement. Here we use microdissection, acetylcholinesterase histochemistry, silver staining of nerves, alpha bungarotoxin binding and immunohistochemistry to describe muscle fiber architecture and motor endplate (MEP) distribution of the human superior longitudinalis muscle (SL). The human SL extends from tongue base to tongue tip and is composed of fiber bundles that range from 2.8 to 15.7 mm in length. Individual muscle fibers of the SL range from 1.2 to 17.3 mm in length (1.3-18.2% of muscle length). Seventy-one percent of SL fibers have blunt-blunt terminations; the remainder have blunt-taper terminations. Multiple MEPs are present along SL length and dual MEPs are present on some muscle fibers. These data demonstrate that the human SL is a muscle of "in-series" design. We suggest that SL motor units are organized to innervate specific regions of the tongue body and that activation of SL motor units according to anteroposterior location is one strategy employed by the nervous system to control tongue shape and tongue movement.     

Neuromuscular junctions in adult and developing fast and slow muscles

Functional changes that occur just before hatching in future fast muscles of the chicken are thought to be influenced by the pattern of innervation. We have compared the neuromuscular junctions of two fast muscles, the posterior latissimus dorsi (PLD) and the pectoralis, which differ in their myosin composition at 18 days in ovo. We have also presented new information on the neuromuscular junctions of the adult fast muscles and an adult slow muscle, the anterior latissimus dorsi (ALD). Both categories of adult muscles were heterogeneous, and there was little difference between endplates of the two fast muscles or between the fast and slow muscles. In contrast, there were significant structural differences between the two fast muscles during embryonic development. In early embryonic muscle fibers, which synthesize embryonic forms of myosin, individual motor endplates were contacted by multiple axon terminals. At 18 days in ovo, the majority of the neuromuscular junctions in the pectoralis continued to be multiterminal, whereas all but one of the terminals had been withdrawn from each endplate in the PLD. This single terminal had a unique form that distinguished it from the embryonic pectoralis and also from the two adult muscles. By 7 days after hatching, the neuromuscular junctions of both muscles had single terminals. They were different from the embryonic terminals, though not necessarily equivalent to adult terminals. The results show that multiple terminals persist at 18 days in ovo in the muscle that continues to express an embryonic myosin, but they have been withdrawn from the muscle that has lost this myosin. It is concluded, from combined data on the two muscles, that maturation of the neuromuscular junction during embryonic and late posthatch development is correlated with transitions in the myosin pattern and in contractile properties.     

Visualization and Quantification of Digitally Dissected Muscle Fascicles in the Masticatory Muscles of Callithrix jacchus Using Nondestructive DiceCT

The organization and length of a muscle's fascicles imparts its contractile properties. Longer fascicles permit increased muscle excursion, whereas changes in fascicle orientation relate to the overall vector of contractile force. Collecting data on fascicle architecture has traditionally involved destructive and irreversible gross dissection. In recent years, however, new imaging modalities have permitted muscles and their fascicles to be visualized nondestructively. Here, we present data from a primate (Callithrix jacchus), in which, for the first time, individual muscle fascicles are digitally “dissected” (segmented and reconstructed) using nondestructive, high-resolution diffusible iodine-based contrast-enhanced computed tomography (DiceCT) techniques. We also present quantitative data on the length and orientation of these fascicles within 10 muscle divisions of the jaw adductor and abductor musculature (superficial, deep, and zygomatic portions of temporalis and masseter; medial and lateral pterygoid; anterior and posterior digastric) and compare these digitally measured lengths to fascicular lengths measured using traditional gross and chemical dissection. Digitally derived fascicle lengths correspond well to their dissection-derived counterparts. Moreover, our analyses of changes in fascicle orientation across the adductor complex enable us to visualize previously uncharacterized levels of detail and highlight significant variation between adjacent muscle layers within muscle groups (e.g., between superficial, deep, and zygomatic portions of masseter and temporalis). We conclude that this technique offers great potential to future research, particularly for questions centered around the visualization and quantification of obscured and often-overlooked muscles such as the pterygoid and digastric muscles, and for deriving more accurate models of the masticatory system as a whole. Anat Rec, 302:1891–1900, 2019. © 2019 American Association for Anatomy     

Internal structure of cat extraocular muscle.

Teasing preparations of cat extraocular muscles (EOM) were used to study the arrangement of muscle fibers and the distribution of the different cholinesterase-positive sites, i.e. (1) large motor endplates, (2) small motor endings of the 'en grappe' type, (3) myotendinous junctions and (4) myomyous junctions. The distribution of these cholinesterase-positive structures gives clear evidence of a complex muscle architecture of cat EOM. In the global layer of cat EOM, only multiply innervated muscle fibers run the whole length of the muscle. The focally innervated muscle fibers are generally shorter; they are usually arranged in series of two to three fibers being interconnected by myomyous junctions. Moreover, muscle fiber splitting is frequently present resulting in a netlike arrangement of muscle fibers. Most of the myomyous junctions occur between focally innervated muscle fibers, but also end-to-side connections of focally to multiply innervated muscle fibers are observed; multiply innervated muscle fi0ers have not been found connected to each other. In this layer, large motor endplates are distributed in several bands between origin and insertion. In the orbital layer all muscle fibers run from tendon to tendon, focally as well as multiply innervated ones. Here, large motor endplates are confined to a band in the middle of the muscle, and myomyous junctions are generally absent. Some functional implications of this complex architecture of cat EOM are discussed.     

Rapid neuromuscular remodeling following limb immobilization

The effect of immobilization on endplate morphology of the rat soleus muscles was studied qualitatively and quantitatively. The endplate was visualized by light microscopic zinc iodide osmium (ZIO) staining and by electron microscopy. The soleus muscle was immobilized by pinning of ankle and knee joints at right angles for 5 days. Immobilized muscles were then compared to the contralateral side and to normal litter mates. After 5 days of partial disuse, muscle fibers atrophied and nerve terminal area increased in ZIO-determined measurements. Neuromuscular junctions (NMJs) of disuse muscle fibers visualized by electron microscopy exhibited greater amounts of degeneration than either contralateral or control NMJs. Degeneration consisted of nerve terminal disruption, exposed junctional folds, and postsynaptic areas which contained little or no postjunctional folds. Regeneration also occurred in the same NMJs, consisting of small terminals associated with large expansion of junctional folds, several small terminals occurring within the same primary synaptic cleft, and several axons wrapped by the same Schwann cell. These observations demonstrate, for the first time, that partial disuse for only 5 days produces muscle atrophy as well as denervation-like changes at the NMJ, which leads to terminal sprouting within the endplate area and remodeling.     

Nerve terminal distribution in the human tongue intrinsic muscles: An immunohistochemical study using midterm fetuses

Intrinsic tongue muscles, especially the transverse and vertical (T&V) muscles, regulate the shape of the tongue. However, little information is available on the nerve distribution pattern in human T&V muscles. Using S100 protein immunohistochemistry for paraffin-embedded histology, we investigated semiserial sagittal or frontal sections of eight human fetal tongues (180-240 mm crown-rump length: CRL). The height of the T&V muscle bundle showed a threefold difference between specimens with a small and a large CRL. Thus, the T&V muscles were still growing at the stages examined. In the intrinsic longitudinal muscles and all extrinsic tongue muscles, we observed the typical motor endplate band. In lower-magnification views, the T&V muscles also appeared to carry the band in the lateral part of the tongue, where the genioglossus muscle fibers did not cross these muscles. However, in higher magnification views, the nerve terminal distribution in the T&V muscles showed a unique rule: the nerve terminal for the transverse muscle bundle was located distantly from that of the adjacent vertical muscle bundle. This pattern seemed to be established during the stages examined. To provide such "distantly separated nerve terminals," thin nerve twigs took a highly curved course oblique to the T&V muscle bundles. We hypothesize that the unique nerve course and terminal distribution in the T&V muscles are a result of sorting to provide a good functional match between the nerve fiber and the muscle bundle. After sorting, the T&V muscle cells may initiate proliferation to increase the muscle bundle.     

Increased and decreased activity elicits specific morphological adaptations of the neuromuscular junction

The objective of this investigation was to compare the effects of decreased vs. increased activity on the neuromuscular system. Twenty-four young adult (7 weeks old) Sprague-Dawley rats were randomly assigned to three treatment groups (N=8/group). Increased activity was achieved by treadmill running for up to 1 h/day. Decreased activity was induced by muscle unloading via the hindlimb suspension model. Control animals engaged in normal weight bearing and ambulatory activity. At the end of the 10 week intervention period, animals were killed and soleus muscles were removed, quickly frozen, and examined using cytofluorescent (neuromuscular junctions) and histochemical (myofibers) procedures. Pre-synaptic morphology was quantified by measuring nerve terminal branching, and post-synaptic assessment was conducted by staining acetylcholine receptors at the endplate. Myofiber profiles of solei were compiled by determining fiber size (cross-sectional area) and fiber type composition. Results show that exercise training significantly (P相似文献   

The Arrangement of Fascicles in Whole Muscle

The architecture of the muscle fascicles, here meaning their lengths and their arrangement relative to one another, has important implications for the force a muscle can produce. Therefore, quantifying this architectural arrangement and understanding the implications of the architecture are important for understanding muscle function in vivo. There were two purposes of this study: (1) to assess, via blunt dissection, the number and the length of all the fascicles comprising the First Dorsal Interosseous (FDI) muscle and (2) to visually identify, via magnetic resonance imaging (MRI), the arrangement of the fascicles comprising the FDI. Simple blunt dissection of all the fascicles comprising four FDI muscles and their subsequent measurement demonstrated that the fascicles comprising the whole muscle were not as long as the muscle belly from which they were extracted. Muscle fascicles are surrounded by connective tissue hence the paths of the fascicles in two whole FDI muscles were identified via MRI by tracking the connective tissue surrounding the fascicles. The fascicles had a spiral pattern along the length of each muscle, within both muscles many of the fascicles were arranged in series with other fascicles. These architectural features of the fascicles of the FDI have important implications for the force–length and force–velocity properties of the whole muscle. Anat Rec, 2012. © 2012 Wiley Periodicals, Inc.     

Topographical relationships of intramuscular nerves and vessels of the motor endplates in the thigh and gluteal regions of human fetuses: an immunohistochemical study

Purpose

The aim of this study was to describe topography of vessels and nerves in striated muscles to understand individual muscle function.

Materials and methods

Immunohistochemistry for nerve and artery was used to examine the thigh and gluteal muscles of six human midterm fetuses.

Results

The supplying nerves often accompanied arteries along epimysium bundling muscle fibers as well as in the covering fascia surrounding the entire muscle mass. However, courses of nerve twigs were usually independent of those of vessels in muscle bundles. Notably, irrespective of whether or not the vascular bundle accompanied the nerves at the muscle surface or hilus, most of the motor endplate bands did not accompany the vessels.

Conclusion

Since the motor endplates were low vascularised, a chemical induction of vessels for nerve terminal development (or the reversed induction) seemed unlikely in striated muscles. In contrast to proprioceptive neuromuscular facilitation, manual stimulation of the endplate bands may stimulate muscle activity without sympathetic reflexes through vessel-accompanying nerves.

     

The localization of axon branchings in two muscle nerves of the rat

Summary The distribution of fiber branching in the proximal intramuscular motor nerves of the gracilis and gastrocnemius muscles of the rat was studied in whole-mount preparations of teased nerves. Branchings of nerve fibers were clustered at fascicular divisions. Such concurrence of fascicular and fiber branchings determines the dispersion of the single muscle fibers belonging to a motor unit. The distribution of fiber branching reveals the wiring pattern of muscle fibers. These patterns differed for the gracilis and gastrocnemtus muscles in correspondence with their functional organization.This study was supported by grant Fr 609/1 from the Deutsche Forschungsgemeinschaft     

Marked non-uniformity of fiber-type composition in the primate suboccipital muscle obliquus capitis inferior

 Obliquus capitis inferior (OCI) is a monoarticular suboccipital muscle linking the transverse process of the atlas (C1) to the spinous process of the axis (C2). Histochemical analysis of fiber-type composition showed that the muscle has a marked gradient of fiber-type distribution in which type I fibers comprise 95–100% of fibers in the deepest region but less than 10% of fibers in the superficial layer. Step-like changes in fiber-type proportions occurred between groups of fascicles. In most instances the boundaries between these fascicles did not exhibit different perimysial features from those fascicles with similar fiber-type proportions. OCI contained large numbers of muscle spindles, which were concentrated in deep regions rich in type I fibers. The degree of nonuniformity in fiber-type distribution seen in OCI is unusually large when compared with patterns described in other primate muscles, and has implications for the way that the muscle is studied anatomically and physiologically. Received: 11 August 1998 / Accepted: 23 September 1998