Development of the trigeminal motor neurons in parrots: Implications for the role of nervous tissue in the evolution of jaw muscle morphology

Vertebrates have succeeded to inhabit almost every ecological niche due in large part to the anatomical diversification of their jaw complex. As a component of the feeding apparatus, jaw muscles carry a vital role for determining the mode of feeding. Early patterning of the jaw muscles has been attributed to cranial neural crest‐derived mesenchyme, however, much remains to be understood about the role of nonneural crest tissues in the evolution and diversification of jaw muscle morphology. In this study, we describe the development of trigeminal motor neurons in a parrot species with the uniquely shaped jaw muscles and compare its developmental pattern to that in the quail with the standard jaw muscles to uncover potential roles of nervous tissue in the evolution of vertebrate jaw muscles. In parrot embryogenesis, the motor axon bundles are detectable within the muscular tissue only after the basic shape of the muscular tissue has been established. This supports the view that nervous tissue does not primarily determine the spatial pattern of jaw muscles. In contrast, the trigeminal motor nucleus, which is composed of somata of neurons that innervate major jaw muscles, of parrot is more developed compared to quail, even in embryonic stage where no remarkable interspecific difference in both jaw muscle morphology and motor nerve branching pattern is recognized. Our data suggest that although nervous tissue may not have a large influence on initial patterning of jaw muscles, it may play an important role in subsequent growth and maintenance of muscular tissue and alterations in cranial nervous tissue development may underlie diversification of jaw muscle morphology. J. Morphol. 275:191–205, 2014. © 2013 Wiley Periodicals, Inc.     

Differential expression of caveolins and myosin heavy chains in response to forced exercise in rats

Exercise training can improve strength and lead to adaptations in the skeletal muscle and nervous systems. Skeletal muscles can develop into two types: fast and slow, depending on the expression pattern of myosin heavy chain (MHC) isoforms. Previous studies reported that exercise altered the distribution of muscle fiber types. It is not currently known what changes in the expression of caveolins and types of muscle fiber occur in response to the intensity of exercise. This study determined the changes in expression of caveolins and MHC type after forced exercise in muscular and non-muscular tissues in rats. A control (Con) group to which forced exercise was not applied and an exercise (Ex) group to which forced exercise was applied. Forced exercise, using a treadmill, was introduced at a speed of 25 m/min for 30 min, 3 times/day (07:00, 15:00, 23:00). Homogenized tissues were applied to extract of total RNA for further gene analysis. The expression of caveolin-3 and MHC2a in the gastrocnemius muscle of female rats significantly increased in the Ex group compared with the Con group (P<0.05). Furthermore, in the gastrocnemius muscle of male rats, the expression of MHC2x was significantly different between the two groups (P<0.05). There was an increased expression in caveolin-3 and a slightly decreased expression in TGFβ-1 in muscular tissues implicating caveolin-3 influences the expression of MHC isoforms and TGFβ-1 expression. Eventually, it implicates that caveolin-3 has positive regulatory function in muscle atrophy induced by neural dysfunction with spinal cord injury or stroke.     

Craniofacial growth in a whole rat head transplant: how does a non-functional head grow?

To evaluate factors intrinsic to the regulation of craniofacial bone growth, we have developed a new experimental model in which the whole head of an infant rat is transplanted to the body of an isohistogenic rat by means of microvascular anastomosis. In our model, the transplanted head has neither scars nor any moving soft tissue that could modify growth around facial bones. Using this model, we evaluated the growth pattern of the craniofacial complex by means of serial roentgenographic cephalometrics. Ten transplantations were performed using 10-day-old rats as donors and 8-week-old rats as recipients. Cephalograms were taken from the lateral direction at 10, 20, 30, and 40 days after transplantation. Several reference points were selected to analyze the growth pattern. In the present study, we conclude that the size and form of the bony complex are mainly determined genetically. There is craniofacial skeletal growth in the absence of muscle function and brain growth. Further, both the nasal cartilage and the sutures appear to be autonomous growth centers having intrinsic growth potential. Genetic or epigenetic information plays an important role at the skeletal level, but it also affects the muscles through the medium of the muscular tonus responsible for posture and other related phenomena.     

The structure of the nervous system of the pluteus larva of Strongylocentrotus purpuratus

Summary Tissues that have the ultrastructural characteristics of nervous tissues are associated with ciliary and muscular elements of the pluteus larva of Strongylocentrotus purpuratus. The nerve cells are found along the margins of the ciliary bands, which are composed predominantly of spindle-shaped ciliated cells. The nerve cells contribute axonal processes to a tract of axons, which runs at the base of the ciliary band throughout its length. Axonal tracts, in the esophagus, lie beneath the circumesophageal muscles. Branched microvilli, which have been interpreted as sensory receptors, are located on the oral side of the main ciliary band and connect with the nerve cells in the ciliary band. The nervous structures described here, and other tissues of the pluteus that have been previously described as nervous, are compared on the basis of their association with receptor and effector organs, and their ultrastructural characteristics.     

Myogenic defect in muscular dystrophy of the chicken.

Inherited muscular dystrophy of the chicken is thought to arise from abnormal development of trophic regulation of skeletal muscles by their innervating nerves. To determine whether expression of muscular dystrophy in the chicken is a property of the nerves or of the muscles, wing limb buds were transplanted between normal and dystrophic chick embryos at $\text{3}\text{1}\text{2}$ days of incubation (stage 19–20). Muscles of donor limbs innervated by nerves of the hosts were compared to contralateral unoperated host limb muscles in chicks from 6 to 25 weeks after hatching. Expression of normal or dystrophic phenotype was determined by examination of five different properties which are altered in dystrophic chick muscle: electromyographic evidence of myotonia; fiber diameter; acetylcholinesterase activity, localization, and isozymes; lactic dehydrogenase activity; and succinic dehydrogenase activity. Genetically normal muscle innervated by nerves of normal or dystrophic hosts was phenotypically normal while genetically dystrophic muscle innervated by normal nerves was phenotypically dystrophic. The results suggest that inherited muscular dystrophy of the chicken arises from a defect of muscle rather than from a lesion in the nerves themselves.     

MUSCULAR ACTIVITY AND BUBBLE FORMATION IN ANIMALS DECOMPRESSED TO SIMULATED ALTITUDES

1. Muscular activity during decompression causes bubble formation in the blood of intact bullfrogs. The amount of gas liberated depends on the degrees of muscular activity and supersaturation (as influenced by altitude). In decompressed dissected bullfrogs, bubbles appear in veins leading from active but not from inactive muscles. 2. Muscular activity during decompression similarly causes bubble formation in rats. Bubbles appear in veins coming from muscles, and often in the lymphatic system. Quiescent rats do not form bubbles. 3. Violent muscular activity before decompression favors bubble formation in bullfrogs during ensuing decompression, but it is less effective than exercise during decompression. The effect persists in large frogs for about an hour. 4. Pre-oxygenation for 2 to 4 hours before decompression reduces the incidence of bubble formation in decompressed bullfrogs. It thus has the same effect on bubble formation in bullfrogs as it does on the "bends" in man. The effect is presumably due to removal of nitrogen. 5. Possible mechanisms by which muscular activity causes bubble formation are discussed. The effects of mechanical agitation and of metabolic CO₂ are considered to be the dominant factors.     

Neuronal adaptation of corticospinal mechanisms of muscle contraction regulation in athletes

Physiological mechanisms of neuronal adaptation of the human corticospinal pathways in response to long-term intense motor activity have been studied insufficiently. In this work, we investigated adaptational changes in corticospinal mechanisms of muscular contraction control in athletes. We measured parameters of motor evoked potentials of lower limb skeletal muscles under voluntary static loads of various intensity and duration, using the transcranial magnetic stimulation method. Elite athletes, as compared to the reference group, in the course of increased intensity and duration of isometric muscular contractions demonstrated more expressed increase in the maximum amplitude of the motor evoked potentials of lower limb skeletal muscles, smaller decrease in the time of central motor conduction of nervous pulses and the peripheral period in electromyograms, and less expressed increase in the cortical and segmental silent periods. Mechanisms of adaptation of corticospinal regulation of human muscular contraction to specific conditions of extreme motor activities are discussed.     

Developmental origins of species-specific muscle pattern

Vertebrate jaw muscle anatomy is conspicuously diverse but developmental processes that generate such variation remain relatively obscure. To identify mechanisms that produce species-specific jaw muscle pattern we conducted transplant experiments using Japanese quail and White Pekin duck, which exhibit considerably different jaw morphologies in association with their particular modes of feeding. Previous work indicates that cranial muscle formation requires interactions with adjacent skeletal and muscular connective tissues, which arise from neural crest mesenchyme. We transplanted neural crest mesenchyme from quail to duck embryos, to test if quail donor-derived skeletal and muscular connective tissues could confer species-specific identity to duck host jaw muscles. Our results show that duck host jaw muscles acquire quail-like shape and attachment sites due to the presence of quail donor neural crest-derived skeletal and muscular connective tissues. Further, we find that these species-specific transformations are preceded by spatiotemporal changes in expression of genes within skeletal and muscular connective tissues including Sox9, Runx2, Scx, and Tcf4, but not by alterations to histogenic or molecular programs underlying muscle differentiation or specification. Thus, neural crest mesenchyme plays an essential role in generating species-specific jaw muscle pattern and in promoting structural and functional integration of the musculoskeletal system during evolution.     

Glycogen content and glucose-6-phosphatase activity in the tissues of the adult frog and tadpole

Studies have been made on the content of glycogen and the activity of glucose-6-phosphatase in tissues of adult frog Rana temporaria (liver, brain, pia mater, n. ischiadicus, fast and slow muscles) and tadpoles (liver, tail muscles). It was found that the enzymic activity is somewhat higher in the liver of tadpoles than that in the liver of adult frogs, being low in the tail muscles. Pia mater and n. ischiadicus exhibit higher activity of glucose-6-phosphatase as compared to the liver. In tadpoles, glycogen content of the liver increases from the 40th stage of metamorphosis and decreases in the tail muscles to the 42nd-50th stages. Glycogen content in tissues other than liver of adult frogs is higher than in similar tissues of mammals.     

A comparative study of the regeneration of the striated and smooth-muscle tissues of the esophagus]

By means of electron microscopy and observational histological techniques, using a similar experimental model, regeneration of the striated and smooth muscle tissues of the esophagus has been studied in rats. During early periods after lesion in both muscle tissues destructive-necrotic changes develop. Beginning from the 2nd-3d days regeneration processes are observed. The course and periodicity of the regenerative processes are specific for the types of the muscle tissues studied. Each of the muscle tissues of the esophagus has its own source of regeneration. For the smooth muscles those are myoblasts, that convert into smooth myocytes, for the striated ones--myosatellites, which after activation get out of the muscle fiber. During the restorative process of the muscular membrane no tissue interconnections are observed. This also proves certain specificity of the striated and smooth muscle tissues of the esophagus.     

Innervation and maturation of muscular tissue in testicular teratomas in strain 129/Sv-ter mice

In strain 129/Sv-ter mice, teratomas develop spontaneously during the 13th day of gestation. These testicular germ cell tumors exhibit characteristics of different germ layers closely resembling normal embryonic tissue. We investigated the interrelationship between nervous and muscular tissues (often found side by side) in teratomas of 4-week-old 129/Sv-ter mice. In well-differentiated mouse teratomas, histochemically and immunohistochemically distinct muscle fiber types could be distinguished, but not with all reactions. According to its aerobic oxidative capacity, teratoma muscle tissue was comparable with normal muscles. However, with respect to myosin-related properties, fiber type differentiation was incomplete. The muscle fibers - generally arranged in bundles - contained one centrally located endplate which was contacted mostly by a single nerve terminal. From this, proper endplate zones within the fiber bundles were formed. Occasionally "type grouping" was encountered, suggesting collateral axonal branching paralleled by synapse elimination. Together with the earlier in vivo observation of muscular contractions, we assume that teratoma muscle fibers are innervated by nerve cells (within the nervous tissue compartments) corresponding to spinal motoneurons. Thus, myogenesis, maturation and innervation of skeletal muscular tissue in mouse teratomas are largely comparable to normal development.     

Sympathetic neural influences on muscle blood flow in rats during submaximal exercise

These experiments were designed to estimate the involvement of the sympathetic innervation in regulation of hindlimb muscle blood flow distribution among and within muscles during submaximal locomotory exercise in rats. Blood flows to 32 hindlimb muscles and 13 other selected tissues were measured using the radiolabeled microsphere technique, before exercise and at 0.5, 2, 5, and 15 min of treadmill exercise at 15 m/min. The two groups of rats studied were 1) intact control, and 2) acutely sympathectomized (hindlimb sympathectomy accomplished by bilateral section of the lumbar sympathetic chain and its connections to the spinal cord at L2-L3). There were no differences in total hindlimb muscle blood flow among the two groups during preexercise or at 30 s or 2 min of exercise. However, flow was higher in eight individual muscles at 2 min of exercise in the sympathectomized rats. At 5 and 15 min of exercise there was higher total hindlimb muscle blood flow in the denervated group compared with control. These differences were also present in many individual muscles. Our results suggest that 1) sympathetic nerves do not exert a net influence on the initial elevations in muscle blood flow at the beginning of exercise, 2) sympathetic nerves are involved in regulating muscle blood flow during steady-state submaximal exercise in conscious rats, and 3) these changes are seen in muscles of all fiber types.     

Prey location,biomechanical constraints,and motor program choice during prey capture in the tomato frog, <Emphasis Type="Italic">Dyscophus guineti</Emphasis>

This study investigated how visual information about prey location and biomechanical constraints of the feeding apparatus influence the feeding behavior of the tomato frog, Dyscophus guineti. When feeding on prey at small azimuths (less than ± 40°), frogs aimed their heads toward the prey but did not aim their tongues relative to their heads. Frogs projected their tongues rapidly by transferring momentum from the lower jaw to the tongue. Storage and recovery of elastic energy by the mouth opening muscles amplified the velocities of mouth opening and tongue projection. This behavior can only occur when the lower jaw and tongue are aligned (i.e., within the range of motion of the neck). When feeding on prey at large azimuths (greater than ± 40°), frogs aimed both the head and tongue toward the prey and used a muscular hydrostatic mechanism to project the tongue. Hydrostatic elongation allows for frogs to capture prey at greater azimuthal locations. Because the tongue moves independently of the lower jaw, frogs can no longer take advantage of momentum transfer to amplify the speed of tongue projection. To feed on prey at different azimuthal locations, tomato frogs switch between alternative strategies to circumvent these biomechanical constraints.     

Coordination and Integration of Metabolism in Insect Flight*

Insect flight is the most energy-demanding activity of animals. It requires the coordination and cooperation of many tissues, with the nervous system and neurohormones controlling the performance and energy metabolism of muscles, and of the fat body, ensuring that the muscles and nerves are supplied with essential fuels throughout flight. Muscle metabolism can be based on several different fuels, the proportions of which vary according to the insect species and the stage in flight activity. Octopamine, which acts as neurotransmitter, neuromodulator or neurohormone in insects, has a central role in flight. It is present in brain, ventral ganglia and nerves, supplying peripheral tissues such as the flight muscles, and its concentration in hemolymph increases during flight. Octopamine has multiple effects during flight in coordinating and stimulating muscle contraction and also energy metabolism partly by activating phosphofructokinase via the glycolytic activator, fructose 2,6-bisphosphate. One important muscle fuel is trehalose, synthesized by the fat body from a variety of precursors, a process that is regulated by neuropeptide hormones. Other fuels for flight include proline, glycerol and ketone bodies. The roles of these and possible regulation in some insect species are discussed.     

Effect of innervation and hormones on enzyme activation and synthesis

Data from the literature and own ones indicate the key role of the nervous system in regulation of the activity and synthesis of the enzymes of energy metabolism in skeletal muscles. Hepatic cells are highly sensitive both to regulation of their metabolism by the vegetative, especially sympathetic nervous system, and hormonal regulation. The enzymic activity and metabolism in the kidneys are controlled mainly by hormones and are not subjected or poorly monitored by the nervous system. Hormonal regulation of the enzymic activity in the bone marrow is presumably rather poor, whereas the question of nervous regulation of its metabolism remains nuclear.     

The physiology and ontogeny of daily oral behaviors

In the masticatory system, activities of muscles are the main source of force. The daily activity of the jaw muscle is a measure of the total daily loading of the tissues involved. This article gives an overview on the recent assessments of the physiology and ontogeny of the daily use of the jaw muscles. Variations in the characteristics of daily activity could be linked to differences in the types of fibers composing the muscles as well as to the properties of the underlying bone, although these relationships are not absolute. Experimental decrease of the hardness of foods eaten by rats and rabbits showed a significant decrease in the number of daily bursts of feeding. These reductions in daily muscular activity were accompanied by higher mineralization of bone and by a transition toward "faster" fiber types in the muscles. It was revealed in rabbits that the characteristics of the daily activities of muscles (total duration of activity, number and lengths of bursts) were not altered during the transition from suckling to chewing and remained largely unaffected during further postnatal development. These results suggest that, despite large anatomical and functional changes, the average daily load on the jaw muscles by the masticatory system appears to be established before chewing develops and remains largely unchanged all the way through development. Whenever the daily muscular activity changes, this seems to have a significant effect on the properties of the tissues involved.     

THE RELATION OF EXERCISE TO BUBBLE FORMATION IN ANIMALS DECOMPRESSED TO SEA LEVEL FROM HIGH BAROMETRIC PRESSURES

1. Bullfrogs (Rana catesbiana) and rats have been subjected to high barometric pressures and studied for bubble formation on subsequent decompression to sea level. Pressures varying from 3 to 60 pounds per square inch, in excess of atmospheric pressure, were used. 2. Muscular activity after decompression is necessary for bubble formation in bullfrogs after pressure treatment throughout the above range. Anesthetized frogs remained bubble-free following decompression. Rats compressed at 15 to 45 pounds per square inch likewise did not contain bubbles unless exercised on return to sea level. 3. Bubbles form without voluntary muscular activity in anesthetized rats previously subjected to pressure of 60 pounds per square inch. Small movements involved in breathing and other vital activities are believed sufficient to initiate bubbles in the presence of very high supersaturations of N₂. 4. Bubbles appear (with exercise) in rats previously compressed at 15 pounds per square inch, and in bullfrogs subjected to pressure at levels as low as 3 pounds per square inch above atmospheric pressure. The percentage drop in pressure necessary for bubble formation is less in compressed animals than in those decompressed from sea level to simulated altitudes. 5. The action of exercise on bubble formation in compressed frogs and rats is attributed to mechanical factors associated with muscular activity, combined with the high supersaturation of N₂. CO₂ probably is not greatly involved, since its concentration does not reach supersatuation, as it does at high altitude. 6. Anoxia following decompression from high barometric pressures has no observable facilitating effect on bubble formation.     

Current knowledge of dystrophin and dystrophin-associated proteins in the retina

Dramatical development of molecular genetics has been disclosing the molecular mechanism of Duchenne muscular dystrophy (DMD) and Becker muscular dystrophy (BMD). DMD gene product, dystrophin, is a submembranous cytoskeletal protein and many dystrophin-associated proteins (DAPs) have been identified, such as utrophin, dystroglycans, sarcoglycans, syntrophins and dystrobrevins. Dystrophin and DAPs are very important proteins not only for skeletal, cardiac, or smooth muscles but also for peripheral and central nervous systems including the retina. The retina has been extensively examined to demonstrate that dystrophin and beta-dystroglycan localize at the photoreceptor terminal, and their deficiency produces the abnormal neurotransmission between photoreceptor cells and ON-bipolar cells. Dystrophin has seven isoforms in variable tissues, and the retina contains full-length dystrophin (Dp427), Dp260, and Dp71. Recent studies have demonstrated that Dp71 localizes in the inner limiting membrane (INL) and around the blood vessel, and Dp260 is expressed in the outer plexiform layer (OPL). beta-dystroglycan is also expressed in the same regions as well as dystrophin, but it remains unclear whether other DAPs are expressed in the retina or not. It is generally assumed that dystrophin functions to stabilize muscle fibers with DAPs by linking the sarcolemma to the basement membrane, but its function in the retina is totally unknown so far.     

Partial laminin alpha2 chain restoration in alpha2 chain-deficient dy/dy mouse by primary muscle cell culture transplantation

Laminin-2 is a component of skeletal and cardiac basal lamina expressed in normal mouse and human. Laminin alpha2 chain (LAMA2), however, is absent from muscles of some congenital muscular dystrophy patients and the dystrophia muscularis (dy/dy) mouse model. LAMA2 restoration was investigated following cell transplantation in vivo in dy/dy mouse. Allogeneic primary muscle cell cultures expressing the beta- galactosidase transgene under control of a muscular promoter, or histocompatible primary muscle cell cultures, were transplanted into dy/dy mouse muscles. FK506 immunosuppression was used in noncompatible models. All transplanted animals expressed LAMA2 in these immunologically-controlled models, and the degrees of LAMA2 restoration were shown to depend on the age of the animal at transplantation, on muscle pretreatment, and on duration time after transplantation in some cases. LAMA2 did not always colocalize with new or hybrid muscle fibers formed by the fusion of donor myoblasts. LAMA2 deposition around muscle fibers was often segmental and seemed to radiate from the center to the periphery of the injection site. Allogeneic conditionally immortalized pure myogenic cells expressing the beta-galactosidase transgene were characterized in vitro and in vivo. When injected into FK506- immunosuppressed dy/dy mice, these cells formed new or hybrid muscle fibers but essentially did not express LAMA2 in vivo. These data show that partial LAMA2 restoration is achieved in LAMA2-deficient dy/dy mouse by primary muscle cell culture transplantation. However, not all myoblasts, or myoblasts alone, or the muscle fibers they form are capable of LAMA2 secretion and deposition in vivo.