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J M Walro

Publications and source records attributed to J M Walro.

49 records · Page 3Linked to original sources

Motor and sensory innervation of muscle spindles in the neonatal rat.

Neural and muscular elements of three muscle spindles from the soleus muscles of 4-day-old rats were reconstructed by electron microscopy of skip-serial transverse ultrathin sections. Each spindle contained four encapsulated intrafusal fibers, including a minimum of one bag1, one bag2 and one chain fiber. The fibers were innervated by unmyelinated motor and sensory axons. The primary and secondary afferents approached the spindles as single axons and terminated on the central region of the intrafusal fibers. Single profiles of terminal axons occupied the sites of sensory neuromuscular junctions, similar to adult sensory endings. No morphological features suggested retraction of afferents from 4-day postnatal spindles. Motor axons approached spindles tightly packed in bundles of 5-20 axons and terminated in the juxtaequatorial and polar regions of both bag and chain fibers. Multiple profiles of terminal axons were visible for each intrafusal motor ending. More motor axons innervated 4-day postnatal spindles and a greater number of axon terminals were visible in immature intrafusal motor endings than in adult spindles. The data suggest that postnatal maturation of motor innervation to intrafusal fibers involves the elimination of supernumerary motor nerve inputs. Synapse elimination in the development of the fusimotor system might represent a mechanism whereby individual gamma axons adjust the number of spindles they innervate.

Animals↗

The effect of neonatal deafferentation or defferentation on myosin heavy chain expression in intrafusal muscle fibers of the rat.

Muscle spindles were either deafferented or deefferented by selectively severing the sensory or motor nerve supply to neonatal soleus muscles of rats at a time when spindles are formed but when intrafusal muscle fibers are structurally and immunocytochemically immature. Experimental muscles were excised two months after nerve section. Control and experimental spindles were examined using monoclonal antibodies specific for myosin heavy chains of slow-tonic (ALD58) and fast-twitch (MF30) chicken muscles. Only intrafusal fibers bound these antibodies in intact soleus muscles. The deefferented spindles exhibited a pattern of ALD58 and MF30 binding similar to that of normal adult intrafusal fibers, whereas deafferented intrafusal fibers were unreactive with the two antibodies. Thus intact sensory innervation is essential for myosin heavy chain expression in intrafusal muscle fibers during postnatal development of rat spindles.

Afferent Pathways↗

Sharing of sensory terminals between the dynamic bag1 and static bag2 fibers in the rat muscle spindle.

The nuclear bag1 intrafusal fiber mediates the dynamic (velocity) sensitivity, whereas the nuclear bag2 and nuclear chain fibers mediate the static (length) sensitivity of muscle spindles to stretch. The pattern of branching of primary and secondary afferents, the distribution of their terminals to the 3 types of intrafusal fibers, and the incidence of sensory cross-terminals were determined by reconstruction of 4 spindles from serial 1-micron and ultrathin transverse sections of rat extensor digitorum longus muscles. A single primary afferent supplied each spindle, and secondary afferents innervated intrafusal fibers in 3 spindles. Only static intrafusal fibers shared cross-terminals of the secondary afferents. In contrast, the dynamic bag1 and static bag2 fibers of each spindle shared at least one terminal of the primary afferent. Cross-terminals shared by the dynamic bag1 and static bag2 fiber parallel the presence of fusimotor (gamma) axons which coinnervate these types of intrafusal fibers in muscle spindles of rats. Consequently, the greater degree of overlap of elements comprising the dynamic and static systems of spindles of the rat relative to that of the cat reduces the probability of generating a purely dynamic or purely static response to an applied stretch.

Animals↗

Heterogeneity of spindle units in the cat tenuissimus muscle.

Three tandem spindles and their nerve supplies, reconstructed by light microscopy of serial transverse sections of the cat tenuissimus muscle, were compared to single spindle units. Each tandem spindle consisted of one large unit containing a dynamic bag1, a static bag2, and several static chain fibers (b1b2c unit) linked by the bag2 fiber to a small unit containing only a bag2 and chain fibers (b2c unit). Most features of primary afferents, secondary afferents, and motor neurons were qualitatively and quantitatively similar in both single and tandem b1b2c units. However, b1b2c units of tandem spindles had a lower density of skeletofusimotor innervation than did single b1b2c spindles. The b2c spindle units differed greatly from single or tandem b1b2c units. The b2c spindle units had fewer intrafusal fibers and incoming axons than either the tandem or single b1b2c units. The motor innervation of b2c units was typified by nonselective gamma axons that coinnervated both bag2 and chain fibers, in contrast to the regular occurrence of both selective and nonselective motor axons in b1b2c spindle units. The afferent located at the equator of b2c units differed in size, branching pattern, and intrafusal distribution of its ending from both the primary and secondary sensory axons of b1b2c units and, therefore, might represent a third category of spindle afferent. Thus, cat tenuissimus muscles contain three types of spindle units that differ in the number and organization of muscular and neural elements. These differences in structure and neural organization among tenuissimus spindle units may be a source for generation of different sensory signals in response to common mechanical or fusimotor stimuli.

Animals↗

Postnatal maturation of spindles in deafferented rat soleus muscles.

Whether the motor innervation can direct the morphological and histochemical differentiation of developing muscle spindles in the absence of sensory innervation was investigated by deafferentation of the soleus muscle in immature rats. Dorsal root ganglia containing the cell bodies of afferents from the soleus muscle were removed surgically at a stage of postnatal development when spindles already contain the full complement of intrafusal fibers innervated by both afferents and efferents, but when the fibers are histochemically and structurally immature. Experimental soleus muscles were excised one year after deafferentation and sectioned frozen at a thickness of 8 micron. Sections were stained for enzymes indicative of types of muscle fibers and sites of neuromuscular junctions, and were examined by light microscopy. Spindles of muscles that matured in the absence of sensory innervation were abnormal. They lacked the periaxial fluid space and contained fewer intrafusal fibers than did normal spindles. The morphological and histochemical profiles of the encapsulated fibers present in the deafferented spindles more closely resembled extrafusal rather than intrafusal muscle fibers. These observations suggest that deafferentation of the immature spindles induces disintegration of some intrafusal fibers and alters maturation of others. Moreover, motor axons terminated less frequently along muscle fibers in deafferented spindles than on intrafusal fibers of normal spindles. Thus, maintenance of a full complement of intrafusal fibers in the developing spindle, emergence of histochemical profiles typical of normal intrafusal fibers, and development of adult pattern of fusimotor innervation require intact sensory innervation.

Adenosine Triphosphatases↗

Factors that determine the form of neuromuscular junctions of intrafusal fibers in the cat.

The form of terminations of fusimotor (gamma) and skeletofusimotor (beta) axons on intrafusal fibers was analyzed in serial sections of 20 spindles of the cat tenuissimus muscle. Seven synaptic features were assessed either qualitatively or quantitatively from electron micrographs of transverse sections of 184 intrafusal and 30 extrafusal endings. Features were compared among endings that were terminations of gamma or beta axons on different types of intrafusal fiber at different distances from the spindle equator. These comparisons indicated that interactions of several factors, and not the motor axon alone, determine the form of motor endings. Intrafusal muscle fiber type is dominant to the motor axon in regulation of the number and depth of postsynaptic folds. Separation of the influence of the motor axon from the muscle fiber was less clear with respect to the size of ending. Complete expression of the muscle fiber-motor axon interaction reflected by the form of motor endings is dependent upon location of the ending relative to the sensory region. Both depth of the primary synaptic cleft and size of the soleplate of motor endings increased with increasing distance of the ending from the spindle equator. A system of classification of cat intrafusal motor endings that reflects the multiplicity of factors that determine the form of endings, and one that simplifies the current terminology, is proposed.

Animals↗

Rat muscle spindles deficient in elements of the static system.

Motor nerve supplies to 15 poles of rat lumbrical spindle were reconstructed from serial, 1-micron transverse sections of muscle embedded in resin. Neural and muscular elements associated with the modulation of static sensitivity of afferents were deficient in these spindles relative to cat tenuissimus and rat soleus spindles. Rat lumbrical spindles contained fewer static fusimotor axons, fewer static chain intrafusal fibers, fewer motor-innervated static bag2 and chain fibers and fewer secondary afferents. The sparsity of static elements in spindles of the rat lumbrical muscle may correlate with the distal location or with the delicate motor tasks performed by the muscle.

Animals↗

Motor innervation of intrafusal fibers in rat muscle spindles: incomplete separation of dynamic and static systems.

Distributions of 53 motor axons to different types of intrafusal fibers were reconstructed from serial 1-micron-thick transverse sections of 13 poles of spindles in the rat soleus muscle. The mean number of motor axons that innervated a spindle pole was 4.1. Approximately 60% of motor axons lost their myelination prior to or shortly after entry into the periaxial fluid space of spindles. Motor innervation to the juxtaequatorial portion of nuclear bag fibers (particularly the bag1) consisted of groups of short, synaptic contacts that were terminations of thin, unmyelinated axons. In contrast, motor endings on both the bag1 and bag2 fibers were platelike in the polar intracapsular region. Chain fibers had a single midpolar platelike ending. The ratio of motor axons that innervated the bag1 fiber exclusively to axons that innervated bag2 and/or chain fibers was 1:1. However, one-fourth of motor axons coinnervated the dynamic bag1 fiber in conjunction with static bag2 and/or chain fibers. Thus the complete separation of motor control of the dynamic bag1 and static bag2 intrafusal systems observed in cat tenuissimus spindles is neither representative of the pattern of motor innervation in all other species of mammals nor essential to normal spindle function.

Animals↗

Quantification and origin of spindles in orthotopic and heterotopic grafts of avian muscles.

Regeneration of muscle spindles was quantified in a series of orthotopically and heterotopically autografted muscles of pigeons. Significantly fewer spindles relative to numbers of extrafusal fibers were present in grafts than in normal muscles. These results are in marked contrast to observations of free-grafted muscles of rats. A majority of grafts of the metapatagialis, a muscle devoid of spindles, into the site of the anterior latissimus dorsi contained spindles. A few spindles were present in grafts of the extensor digitorum communis, which normally contains many spindles, into the site formerly occupied by the metapatagialis whereas muscle spindles were absent in orthotopic grafts of the metapatagialis muscle. These observations suggest that the spindle-like structures observed in the extensor digitorum communis muscles, which regenerated in the sites of the metapatagialis, were derived from spindles of the donor muscle. Thus muscle spindles in transplanted avian muscle can form by two distinct developmental processes.

Animals↗

Nonselective motor innervation of intrafusal fibers in muscle spindles of the rat.

Distributions of motor axons to different types of intrafusal fiber were reconstructed from serial 1-micron thick transverse sections of six poles of muscle spindle in the rat soleus. Motor axons innervated (dynamic) bag1 fibers, or (static) bag2 fibers in conjunction with chain fibers. However, approximately forty percent of axons that supplied the spindles synapsed on both bag1 and bag2 or bag1 and chain fibers. The significance of this co-innervation of dynamic and static intrafusal fibers is discussed relative to the general organization and function of mammalian spindles.

Animals↗

Ischemic degeneration of the avian muscle spindle.

The neurovascular supply to the pigeon's extensor digitorum communis muscle was disrupted. The muscle spindles were studied by light and electron microscopy to determine whether their degeneration was compatible with regeneration by activation of satellite cells within an intact spindle capsule. The denervation and ischemia induced intrafusal muscle fiber necrosis and degeneration of the sarcolemma and basal lamina. The muscle fibers in the equatorial region were often absent and their sites were indicated by collagenous caps which usually covered the sensory nerve terminal regions. These collagenous caps enclosed amorphous material derived from the intrafusal fibers and degenerating mitochondria from the sensory terminals. In this equatorial region, the basal lamina was present only under the collagenous cap and was disrupted elsewere . The cells of the muscle spindle capsule were more sparse or absent, but the collagen content had increased. The sheath lacked continuity, containing numerous gaps. These observations indicate that the basal lamina does not remain intact, and regeneration may not occur by activation of satellite cells within the former basal lamina, as reported for regenerating rat muscle spindles. This suggests that the mechanisms of regeneration of muscle spindles in rat and pigeon muscle may not be similar.

Animals↗

Patterns of avian muscle fiber type regeneration. Evidence for a myotrophic influence.

Serratus superficialis metapatagialis (SSM) and posterior biventer cervicis (BVC) muscles were free-grafted into the site of the slow tonic anterior latissimus dorsi (ALD) of adult pigeons. Grafts were prepared for histochemical examination at 1, 3, 7, 12 and 15 days; at monthly intervals from 1 to 4 months; and at various intervals up until 23 months after surgery. Few original muscle fibers survived the trauma of grafting and contributed to the regenerated muscle. The arrangement of fast and slow fibers and the percentage of slow fibers were recorded for each graft at least one month of age. Young grafts of the SSM (one to four months of age) regenerated a segregated pattern of fast and slow fibers that resembled control SSM muscles, whereas early grafts of the BVC regenerated a mosaic arrangement characteristic of normal BVC muscles. The percentages of slow fibers in both SSM and BVC grafts up to 4 months after surgery did not significantly differ from control muscles. Both SSM and BVC grafts older than 4 months of age had a significantly higher percentage of slow fibers than control muscles. These data indicate that the donor muscle influences the pattern of fiber types that is originally manifested and this pattern is maintained relatively intact for 4 months. Eventually the nerve at the host site modifies this pattern, and the fibers of the graft assume the histochemical characteristics of the muscle removed from the host site. In addition, the time required for histochemical stabilization of muscle fibers of avian heterotopic autografts is longer than that for whole muscle grafts in rats or avian minced muscle preparations, and is comparable to tenotomized avian muscle.

Animals↗

Absence of changes in fiber type with aging in avian muscles.

The anterior latissimus dorsi of the pigeon, a slow tonic muscle, and biventer cervicis, a mixed muscle, of two age groups (1-2 years old versus 6-8 years old) were compared with respected to percentages of fiber types and activities of adenosine triphosphatase (ATPase) and succinic dehydrogenase (SDH), as estimated histochemically, to determine whether these became altered with old age. These parameters did not change between the young and old birds for either type of muscle.

Adenosine Triphosphatases↗