A commentary on muscle unit properties in cat hindlimb muscles

A broad survey of muscle unit properties in 14 muscles of the cat hind limb is presented which emphasizes some general features of unit properties in mammalian muscles. A more detailed analysis of muscle unit properties in three muscles of the posterior compartment of the lower leg is then presented using Burke's tetrapartite (FF, FI or F (Int.), FR, and S) unit classification scheme. Our data on the properties of motor units in cat tibialis posterior (TP) have been compared to those generated by Burke and colleagues on units in flexor digitorum longus (FDL) and medial gastrocnemius (MG). In all three muscles, twitch contraction time was distinctly slower for type S units and specific tension outputs were substantially greater for type FF units than for type S units. The innervation ratios of type FR units were slightly lower than for type S units but the specific tension of the FR units was closer to FF units than to type S units. The FF units controlled 70–74% of the cumulative force output of each muscles, indicating a substantial capacity for powerful rapid contractions of all three of these muscles despite their differences in “size,” action, and force generation. Distinctive features of the three muscles included differences in the unit types' force producing capabilities and in the relative representation of “nonfatigable” type FR and S units in each muscle. In particular, TP is endowed with some unusually powerful type FF units and a high percentage (42%) of type S units. In contrast, FDL has units that develop relatively little force and an unusually high representation (56%) of type FR units. The possible relationships between these muscle features and their presumed role in posture and locomotion is discussed.     

Histochemical profiles of cat intrafusal muscle fibers and their motor innervation

Summary Muscle spindles were examined histochemically in serial transverse sections of cat tenuissimus muscles. The myofibrillar adenosine triphosphatase (ATPase) staining reaction was used to identify nuclear bag₁, bag₂ and nuclear chain intrafusal muscle fibers. Regional differences in ATPase staining occurred along the bag₁ and bag₂ fibers but not along the chain fibers. All intrafusal fiber types displayed regional variability in staining for nicotinamide adenine dinucleotide tetrazolium reductase (NADH-TR). Motor nerve terminals were demonstrated along the poles of bag₁, bag₂ and chain fibers by staining for cholinesterase (ChE). There was no consistent spatial correlation between the intensity of regional ATPase staining along the bag fibers and location, number or type of motor endings. However, most ChE deposits occurred in intrafusal fiber regions that displayed the greatest NADH-TR variability. Some fiber poles or whole intrafusal fibers were devoid of any ChE deposits but their ATPase and NADH-TR content was comparable to that of fibers bearing ChE deposits. The observations suggested that motor nerve fibers per se may not play a major role in determining the histoenzymatic content of intrafusal fibers.     

Histochemical profiles of cat intrafusal muscle fibers and their motor innervation

Muscle spindles were examined histochemically in serial transverse sections of cat tenuissimus muscles. The myofibrillar adenosine triphosphatase (ATPase) staining reaction was used to identify nuclear bag1, bag2 and nuclear chain intrafusal muscle fibers. Regional differences in ATPase staining occurred along the bag1 and bag2 fibers but not along the chain fibers. All intrafusal fiber types displayed regional variability in staining for nicotinamide adenine dinucleotide tetrazolium reductase (NADH-TR). Motor nerve terminals were demonstrated along the poles of bag1, bag2 and chain fibers by staining for cholinesterase (ChE). There was no consistent spatial correlation between the intensity of regional ATPase staining along the bag fibers and location, number or type of motor endings. However, most ChE deposits occurred in intrafusal fiber regions that displayed the greatest NADH-TR variability. Some fiber poles or whole intrafusal fibers were devoid of any ChE deposits but their ATPase and NADH-TR content was comparable to that of fibers bearing ChE deposits. The observations suggested that motor nerve fibers per se may not play a major role in determining the histoenzymatic content of intrafusal fibers.     

Morphometry, histochemistry, and innervation of cervical shoulder muscles in the cat

Morphometric and histochemical methods were used to estimate the force-developing capabilities and fiber-type contents of four muscle complexes (rhomboideus, levator scapulae, trapezius, and sternomastoideus) that link the shoulder girdle to the skull and cervical vertebrae. Each complex contained at least two member muscles that were distinctive architecturally and often had specialized innervation patterns. Trapezius and sternocleidomastoideus were innervated by both cranial nerve XI and cervical spinal nerves. Glycogen depletion of trapezius suggested that the nerves derived from cervical roots might be entirely sensory. Muscles within each complex varied in physiological cross-sectional area from less than 0.1 cm2 to greater than 1 cm2. They showed differences in fiber-type composition that suggested specialized roles for different behaviors. The morphometric features of the cervical shoulder muscles suggest that they have considerable potential to produce head movements and should be incorporated into feline head-movement models.     

Interfiber tension transmission in series-fibered muscles of the cat hindlimb

Several muscles of the cat hindlimb, including biceps femoris and tenuissimus, are composed of short, in-series muscle fibers with tapered intrafascicular terminations. Tension generation and transmission within such muscles requires that active fibers should be mechanically coupled in series via myomyous junctions, specialized connective tissue attachments, or the endomysium. This report establishes that the tapered fibers of the cat biceps femoris and tenuissimus muscles have insignificant numbers of either myomyous or specialized connective tissue junctions. Tension appears to be transmitted in a distributed manner across the plasmalemma of the tapered (and probably the non-tapered) portions of the fibers to the connective tissue of the endomysium, which is therefore an essential series elastic element in these muscles. Subplasmalemmal dense plaques were identified and may play a role in transmembrane force transmission. In addition to the endomysium, passive muscle fibers may also serve to transmit tension between active fibers, and therefore should also be considered to be series elastic elements.     

Seven skeletal muscles rich in slow muscle fibers may function to sustain neutral position in the rodent hindlimb

Skeletal muscles consist of slow-twitch and fast-twitch muscle fibers, which have distinct physiological and biochemical properties. The muscle fiber composition determines the contractile velocity and fatigability of a particular skeletal muscle. We analyzed the systemic distribution of slow muscle fibers in all rodent skeletal muscles by myosin ATPase staining and found that only seven hindlimb skeletal muscles were extremely rich in slow muscle fibers. These included the mouse piriformis (56.5%), gluteus minimus (35.7%), vastus intermedius (24.7%), quadratus femoris (69.9%), adductor brevis (44.3%), gracilis (24.6%), and soleus muscles (35.1%). In mice, the relative proportion of slow muscle fibers did not exceed 15% in skeletal muscles in other regions. The distribution of slow muscle fibers was well conserved in rats and rabbits. The soleus muscle is an important antigravity muscle in both rodents and humans; therefore, these skeletal muscles rich in slow muscle fibers might play an important role in sustaining neutral alignment of the lower extremity.     

Distribution of muscle fibers in skeletal muscles of the cheetah (Acinonyx jubatus)

We examine the muscle fiber population of skeletal muscles from whole body in the cheetah (Acinonyx jubatus). In the present experiments, we showed the characteristics of fiber composition in the cheetah by comparative studies among the cheetah, domestic cat, and the beagle dog. Fiber population was determined on muscle fibers stained with monoclonal antibody to each myosin heavy chain isoform. Histochemical analysis demonstrated that many muscles in the cheetah and domestic cat had a low percentage of Type I fibers and a high percentage of Type IIx fibers, while those in the beagle dog showed a high percentage of Type IIa. The hindlimb muscles in the cheetah had a higher percentage of Type II (Type IIa + IIx) fiber than the forelimb muscles. This fact suggests that the propulsive role of the hindlimb is greater than the forelimb in the cheetah. The longissimus in the cheetah had a high percentage of Type IIx fibers over a wide range from the thoracic to lumbar parts, while the population of muscle fibers in this muscle was different depending on the parts in the domestic cat and beagle dog. This indicates that the cheetah can produce a strong and quick extension of the spinal column and increase its stiffness during locomotion. Furthermore, we found the notable difference of muscle fiber type population between flexors and extensors of digits in the cheetah. The present experiments show the characteristics of muscle fibers in the cheetah, corresponded to its ability to perform high-speed running.     

Histological study of motor innervation to long nuclear chain intrafusal fibers in the muscle spindle of the cat

Several muscle spindles of the cat tenuissimus muscle were cut in serial, 1-micron thick transverse sections and stained with toluidine blue in search for long nuclear chain intrafusal muscle fibers. Five complete poles of the long chain fibers were located. Each fiber pole displayed one plate-type motor ending situated in the extracapsular fiber region. The endings were supplied by myelinated motor axons that originated from intramuscular nerve fascicles containing motor axons to extrafusal muscle fibers. One of the endings was innervated by a collateral from a motor axon that supplied an extrafusal end-plate. Ultrastructurally, the long chain endings resembled extrafusal end-plates. They were more complex, in terms of prominence of sole-plate and degree of post-junctional folding, than any other intrafusal ending present in the spindles. The motor endings of the long chain fibers were assumed to be the terminals of static (fast) skeletofusimotor axons, which preferentially innervate the longest nuclear chain fibers of cat muscle spindles.     

Autonomic innervation of receptors and muscle fibres in cat skeletal muscle

Cat hindlimb muscles, deprived of their somatic innervation, have been examined with fluorescence and electron microscopy and in teased, silver preparations; normal diaphragm muscles have been examined with electron microscopy only. An autonomic innervation was found to be supplied to both intra- and extrafusal muscle fibres. It is not present in all muscle spindles and is not supplied at all to tendon organs. Fluorescence microscopy revealed a noradrenergic innervation distributed to extrafusal muscle fibres and some spindles. On the basis of the vesicle content of varicosities the extrafusal innervation was identified as noradrenergic (32 axons traced), and the spindle innervation as involving noradrenergic, cholinergic and non-adrenergic axons (14 traced). Some of the noradrenergic axons that innervate spindles and extrafusal muscle fibres are branches of axons that also innervate blood vessels. We cannot say whether there are any noradrenergic axons that are exclusively distributed to intra- or extrafusal muscle fibres. The varicosities themselves may be in neuroeffective association with striated muscle fibres only, or with both striated fibres and the smooth muscle cells in the walls of blood vessels. The functional implications of this direct autonomic innervation of muscle spindles and skeletal muscle fibres are discussed and past work on the subject is evaluated.     

Growth of crustacean muscles and muscle fibers

Summary The superficial flexor (SF) muscle of the crayfish (Procambarus clarkii) abdomen increases in volume in direct proportion to increases in total body weight during ontogeny. This increase in SF muscle mass occurs solely (Figs. 1, 2) by an increase in the width and length of SF muscle fibers (i.e., the number of SF muscle fibers remains constant). Unlike vertebrate muscle fibers, these crustacean muscle fibers increase in length by increases in sarcomere length (Fig. 3). This increase in sarcomere length during ontogeny must occur via a continuous lengthening of actin and myosin filaments since the relative lengths of the A and I bands remain essentially unchanged as these fibers lengthen. Similar results are reported for the opener muscle of the cheliped (Figs. 5–7).We suggest that fiber number is specified for many crayfish muscle masses since for a given species of crayfish, certain muscle masses contain a set number of fibers within rather narrow limits, and the number of fibers is often significantly different in homologous muscle masses of the same species or in the same muscle mass of different species. Finally, it would seem that similar processes are operating both during embryonic growth and during regeneration in crayfish and in some other crustaceans, since fiber number is not significantly different in opener muscles from normal and regenerated limbs in crayfish and in the crabGecarcinus lateralis.We would like to thank Mr. Martis Ballinger and Mr. Mark R. Meyer for their aid and histology and photography, Mr. Michael Bouton for his assistance in several of the experiments, and Drs. Alan Templeton and Laurence Fox for their help in the statistical analysis of the data. This research was supported by NSF grant No. GB-30199 and NIH grant No. NS-08609.     

Comparative histology, histochemistry and innervation of the striated muscle fibers of the peroneus longus muscle

The morphology of the peroneus longus muscle was compared in three Galliformes and five Passeriformes in relation to partial behavioral characteristics. In the quail two fibre types are found, while the muscle of the other species is composed of three fibre types. The frequencies of these fibres are different, especially between Galliformes and Passeriformes. The peroneus longus muscle in the quail is innervated only from the phasic system. The other species show phasic and tonic innervation. There is a correlation between the muscle fibre calibre and the extent of the synaptic gutter.     

One-bag-fiber muscle spindles in tenuissimus muscles of the cat

Summary Over 150 complete and 139 incomplete single muscle spindles were examined in serial transverse sections of cat tenuissimus muscles in search for spindles lacking one of the two types of nuclear bag intrafusal fiber. Several histochemical reactions were used to type the intrafusal muscle fibers and assess the spindle motor and sensory innervation. One complete spindle lacked a bag₁ fiber, and another spindle lacked a bag₂ fiber. Several incomplete spindles also lacked bag₁ fibers. In addition, ten double tandem spindles contained one capsular unit each that lacked the bag₁ fiber, and one triple tandem spindle had two such capsules. All one-bag-fiber spindles had primary sensory innervation, but none had secondary sensory innervation. Their motor innervation was similar to that of the usual two-bag-fiber spindles in the number and disposition of intrafusal motor endings. It is unclear whether the one-bag fiber spindles, either single or tandem-linked, are products of an aberrant spindle development or represent a true anatomical and functional subcategory of the cat muscle spindle.     

Multiple-bag-fiber muscle spindles in tenuissimus muscles of the cat

Over 300 complete and incomplete cat muscle spindles were examined in serial transverse sections of tenuissimus muscles in search of spindles with more than two nuclear bag intrafusal muscle fibers. Several histochemical and histological stains were used to identify the intrafusal fibers and assess their motor and sensory innervation. About 13% of the spindles contained either three or four bag fibers rather than the usual two. Every multiple-bag-fiber spindle possessed at least one nuclear bag1 and one nuclear bag2 fiber. The supernumerary bag fibers were either another bag1 and/or bag2 fiber, or a mixed bag fiber. The extra bag fibers had the usual morphologic and histochemical properties of cat nuclear bag fibers. All multiple-bag spindles received primary sensory innervation, and most had secondary sensory endings in addition. Their motor pattern was similar in the number, appearance and disposition of intrafusal motor endings to that of the usual two-bag-fiber spindles. Bag fibers of the same kind shared motor nerve supply in three multiple-bag spindles in which tracings of individual motor axons were obtained histologically. It is unclear whether any functional advantage is conveyed to a muscle spindle by its having more than one bag1 and one bag2 fiber.     

One-bag-fiber muscle spindles in tenuissimus muscles of the cat

Over 150 complete and 139 incomplete single muscle spindles were examined in serial transverse sections of cat tenuissimus muscles in search for spindles lacking one of the two types of nuclear bag intrafusal fiber. Several histochemical reactions were used to type the intrafusal muscle fibers and assess the spindle motor and sensory innervation. One complete spindle lacked a bag1 fiber, and another spindle lacked a bag2 fiber. Several incomplete spindles also lacked bag1 fibers. In addition, ten double tandem spindles contained one capsular unit each that lacked the bag1 fiber, and one triple tandem spindle had two such capsules. All one-bag-fiber spindles had primary sensory innervation, but none had secondary sensory innervation. Their motor innervation was similar to that of the usual two-bag-fiber spindles in the number and disposition of intrafusal motor endings. It is unclear whether the one-bag fiber spindles, either single or tandem-linked, are products of an aberrant spindle development or represent a true anatomical and functional subcategory of the cat muscle spindle.     

Histochemistry, immunocytochemistry, and biometry of muscle fibers and their innervation of the peroneus longus muscle]

The morphology of the peroneus longus muscle of the Chinese quail was studied in relation to partial behavorial characteristics. On the basis of the actomyosin ATPase reaction after alkaline and acid preincubation, three fiber types are revealed. The indirect immunofluorescence, using specific antibodies against 'slow' myosin from the human vastus lateralis muscle, provokes a strong reaction on the small fiber type. The characteristics of the innervation revealed by the cholinesterase activity, concentrated in the synaptic gutters and the direct study of the nerve fibres, show focal, mono-axonal 'en plaques' endings, typical of the phasic motor system.