The differentiation of two types of intrafusal fibres in rabbit muscle spindles

1970 ◽  
Vol 317 (3) ◽  
pp. 187-197 ◽  
Author(s):  
N. Corvaja ◽  
O. Pompeiano
1973 ◽  
Vol 12 (1) ◽  
pp. 175-195
Author(s):  
ALICE MILBURN

The morphogenesis of muscle spindles in rat lower hind-limb muscles has been investigated using the electron microscope. The earliest detectable spindles are seen in the 19.5-day foetus and consist of a single myotube bearing simple nerve terminals of the large primary afferent axon from nearby unmyelinated intramuscular nerve trunks. The capsule forms by an extension of the perineural epithelium of the supplying nerve fasciculus, and is confined initially to the innervated zone. Myonuclei accumulate in this region, so that the first intrafusal muscle fibre to develop is a nuclear-bag fibre. Myoblasts, present within the capsule of the spindle throughout its development, fuse to form a smaller less-differentiated myotube by the 20-day foetal stage. This new myotube matures by close association with the initial fibre, and by birth (21-22 days gestation) has formed the smaller, intermediate bag fibre, that has been identified histochemically and ultrastructurally in the adult. The nuclear-chain fibres develop in the same way; myoblasts fuse to form satellite myotubes that mature in pseudopodial apposition to one of the other fibres within its basement membrane. This apposition consists of extensions of sarcoplasm from the developing myotube into the supporting fibre. By the 4-day postnatal stage the full adult complement of 4 intrafusal muscle fibres is present, although ultrastructural variations, seen in the adult, are not differentiated. The fusimotor innervation begins to arrive at birth, but is not mature until the 12th postnatal day, when the myofibrillar ultrastructural differentiation, including the loss of the M-line in the large-diameter bag fibre, is complete. The periaxial space appears at the same time. It is suggested that the sequential development of the intrafusal fibres is a reflexion of the decreasing morphogenetic effect of the afferent innervation, whereas the role of the fusimotor innervation is in ultrastructural, myofibrillar differentiation.


1960 ◽  
Vol 7 (4) ◽  
pp. 725-742 ◽  
Author(s):  
Neil C. R. Merrillees

Lumbrical muscles of young rats were fixed with OsO4 and embedded in methacrylate for electron microscopy. The spindle capsule was found to be continuous with and similar in structure to the sheath of Henle surrounding the nerves supplying the spindle. The capsule consists of several closely applied concentric cytoplasmic sheets. Each sheet is about 1,000 A thick and has no fenestrations. Many caveolae and vesicles in the cytoplasm suggest active transport through the sheets. The periaxial space fluid contains much solid material. It is suggested that the capsule and periaxial space regulate internal chemical environment. The interfibrillar structures are less evident in the polar regions of intrafusal fibres than in extrafusal fibres. Simple motor end-plates occur on the polar regions of intrafusal fibres. In the myotube region of the intrafusal fibre a peripheral zone of myofibrils surrounds a cytoplasmic core containing nuclei, mitochondria, Golgi bodies, reticulum, and a few lipid-like granules. Naked sensory endings lie on the myotube "in parallel" with the underlying myofilaments. Naked processes of the primary sensory ending deeply indent the muscle plasma membrane and the underlying wisps of myofilament in the nuclear bag region. The plasma membranes of sensory nerve ending and intrafusal muscle fibre are about 200 A apart.


1969 ◽  
Vol 17 (5) ◽  
pp. 348-349 ◽  
Author(s):  
ALFRED J. SPIRO ◽  
REBECCA L. BEILIN

Using the adenosine triphosphatase reaction two histochemically distinct types of intrafusal fibers were demonstrated in rabbit muscle spindles despite morphologic homogeneity of these fibers. This finding, reflecting metabolic differences between these fiber types, is offered as an explanation for the previously unexplained heterogeneity of their physiologic responses.


1. The structure and innervation of muscle spindles from normal, de-afferented and de-efferented muscles of the cat hind limb were studied. The spindles were either completely isolated by microdissection, or were serially sectioned transversely. 2. All spindles contain two distinct types of intrafusal muscle fibre, ‘nuclear bag fibres’ and ‘nuclear chain fibres’, which differ in structure and innervation. 3. Nuclear bag muscle fibres, usually two per spindle, are less than half the diameter of extrafusal fibres, and each contains numerous large nuclei packed together in the equatorial region of the spindle. Nuclear bag fibres practically never branch. The fibres contain numerous myofibrils uniformly distributed in cross-sections, and relatively little sarcoplasm; they atrophy very slowly after the ventral spinal roots are cut. Several small motor nerve fibres (y, fibres) enter each spindle and terminate in a number of discrete motor end-plates on the nuclear bag muscle fibres. These y x end-plates lie in a group at each spindle pole and long lengths of nuclear bag fibre are free of motor innervation. 4. Nuclear chain muscle fibres, usually four per spindle, are about half the length and diameter of nuclear bag fibres in spindles in the leg muscles. The nuclear chain fibres in spindles from the small muscles of the foot may, however, equal the nuclear bag fibres in length, and in diameter beyond the ends of the lymph space. Each nuclear chain fibre contains a single row of central nuclei in the equatorial region; the fibres occasionally branch, but often none of them do so. They contain fewer myofibrils per unit area, irregular in size and distribution, and relatively more sarcoplasm, than nuclear bag fibres. Nuclear chain fibres atrophy nearly as rapidly as extrafusal fibres after the ventral roots are cut. A number of very fine motor nerve fibres fibres) enter each spindle and terminate in a network of fine axons and small nerve endings (the network’) situated on the nuclear chain muscle fibres in most regions other than the nuclear region. 5. All spindles receive both y 1 xand y 2 innervation, fibres forming slightly more than half of the total number of motor fibres which varies from seven in simple spindles in phasic muscles to twenty-five in the most complex spindles in tonic muscles. Both y 1 and y 2 fibres remain intact after dorsal root transection and degenerate following ventral root transection. The histological evidence supports the view that the yj and y2 nerve fibres at the spindles are derived from two types of stem fibre, neither of which belongs to the a group. 6. Each spindle has one primary sensory nerve ending, supplied by one group 1 a afferent nerve fibre, and from zero to five secondary sensory nerve endings, each supplied by one group II afferent nerve fibre. The primary sensory terminations lie on both nuclear bag and nuclear chain muscle fibres. The secondary sensory terminations lie predominantly on the nuclear chain muscle fibres. In spindles with several secondary sensory endings, their terminations may lie on the same region of nuclear chain fibres as motor endings of the y 2 network. 7. In general, spindles in tonic muscles have more secondary sensory endings and motor nerve fibres and endings than those in other muscles. Nuclear chain intrafusal fibres are probably functionally ‘slower’ than nuclear bag intrafusal fibres, while both types are ‘slower’ than extrafusal fibres. Both nuclear chain fibres and nuclear bag fibres, however, probably show a gradation in activity related to the nature of the muscle in which they lie. The reader is advised to study figure 33 and its legend first, at the same time studying the plate figures to which reference is made in figure 33 b , then to read the portions of the Results in italics consecutively followed by the Discussion, finally studying the detailed Results. Further details of many of the illustrations and tables are available for reference in the Archives of the Royal Society.


Development ◽  
1984 ◽  
Vol 82 (1) ◽  
pp. 177-216
Author(s):  
Alice Milburn

The structure of developing spindles has been examined in cat peroneal muscles by light and electron microscopy, beginning at the 34- to 38-day foetal stage. By this stage α motoneurons have formed end-plates on primary myotubes. Secondary extrafusal myotubes then develop beneath the basal lamina of primary myotubes, and are innervated by motor axons early in their assembly. First-series secondary myotubes separate from primary myotubes prior to the development of subsequent series. The assembly of extrafusal fibres is completed by birth. Intrafusal fibres assemble in a similar manner. At the 34- to 38-day foetal stage developing spindles consist of a single primary myotube containing a small accumulation of myonuclei beneath the terminals of the la afferent axon. Simple motor nerve terminals also innervate this myotube, which will ultimately become the bag2 fibre of the mature spindle. Secondary intrafusal myotubes then assemble beneath the basal lamina of the primary bag2 myotube, in the order presumptive bag1, long-chain, intermediate-chain and typical-chain fibres. Their assembly begins at the equator, beneath the sensory terminals, and spreads to the poles. The bag1 and long-chain myotubes separate from the bag2 in the spindle pole prior to the development of the other chain fibres. The assembly of intrafusal fibres is completed by birth. The Periaxial space begins to develop in the first postnatal week. The development of tandem spindles containing b2C units is described. The role of sensory and motor innervation in the assembly and differentiation of mammalian intrafusal fibres is discussed.


Development ◽  
1986 ◽  
Vol 92 (1) ◽  
pp. 223-254
Author(s):  
F. H. Diwan ◽  
Alice Milburn

Soleus muscle of adult rat is revascularized 5–8 days after sectioning the supplying blood vessels. The temporary ischaemia thus produced results in the rapid concomitant degeneration of extra- and intrafusal muscle fibres along with their nerve terminals and supplying axons. The basal lamina of all muscle fibres usually remains intact throughout the degenerative phase. Necrotic sarcoplasm is removed by phagocytic cells. Satellite cells survive the temporary ischaemia and give rise to presumptive myoblasts which fill the basal-lamina tubes. These myoblasts fuse to form myotubes which, by the 14th day after devascularization, are maturing into muscle fibres in the absence of any innervation. Within the spindle, nuclear-bag fibres degenerate more rapidly than nuclear-chain fibres. Regeneration proceeds more rapidly within the basal-lamina tubes of the original bag fibres than within those of the chain fibres. Reinnervation of regenerating extra- and intrafusal fibres begins 21 days after devascularization and is completed some 7 days later, during which time further equatorial differentiation of some reinnervated intrafusal fibres may occur. Regenerated spindles vary considerably with respect to their innervation and equatorial nucleation. Most contain short, thin, additional muscle fibres as well as those that have regenerated within the basal-lamina tubes of the original fibres.


1982 ◽  
Vol 74 (3) ◽  
pp. 355-366 ◽  
Author(s):  
G. te Kronnie ◽  
Y. Donselaar ◽  
T. Soukup ◽  
J. Zelená

The occurrence of collateral and ultraterminal sprouting by skeletomotor and fusimotor axons is described in teased, silver preparations of normal and de-afferentated hindlimb skeletal muscles. In twelve cat and ten rabbit muscle spindles the proportions of plate-ending fusimotor axons showing sprouting were 30.4 and 34.0 % , respectively. If small end-plates, previously described in the literature as ‘accessory endings’, are regarded as young plates newly formed by collateral sprouts, the degree of sprouting in the two spindle samples is increased to 33.9 and 38.3 % , respectively. Sprouting by skeletomotor axons was observed in a variety of cat, rabbit, and rat muscles taken from normal muscles. In a sample of 567 terminal branches examined in muscles from the three animals, 8.1% bore sprouts, or 19.4% if the collaterals forming accessory endings are included as sprouts. Some evidence of retrograde degeneration among the terminal branches of skeletomotor axons innervating normal muscle is described. It is suggested that sprouting effects the replacement of old end-plates which degenerate after a limited life-span; and that it is a general property of the vertebrate motoneuron for its peripheral terminals to undergo cyclic renewal in this way. The greater degree of sprouting shown by fusimotor plate-ending axons as compared with skeletomotor ones is attributed to the fact that the innervation supplied to spindles by such axons is both multiple and polyneuronal. In conclusion, some of the implications of the replacement hypothesis, e.g. with regard to neuromuscular pathology, are discussed.


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