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.     

Morphometric studies on tenuissimus muscle spindles in the cat

Muscle spindles were studied histochemically in serial transverse sections of 42 cat tenuissimus muscle specimens. Staining for myofibrillar adenosine triphosphatase was employed to identify nuclear bag 1, nuclear bag 2, and nuclear chain intrafusal muscle fibers. The nuclear chain fibers were further subdivided into three categories according to their polar length and the intensity of their staining for nicotinamide adenine dinucleotide tetrazolium reductase. A total of 430 spindle poles were surveyed. The mean spindle content of bag 1, bag 2, and chain fibers was established. The mean polar length of intrafusal fibers as well as that of the intracapsular and extracapsular spindle regions was determined. A cholinesterase (ChE) staining technique was used to demonstrate the termination sites of motor axons along intrafusal fibers. Two types of circumscribed ChE deposits. The "rim" and the "plate," occurred on the fibers. The nuclear chain fibers usually carried both the ChE rims and plates, while most nuclear fibers displayed only the plates. The ChE plates were assessed in term of their appearance, staining intensity, length, and location along the fibers. The mean number of ChE plates found along the fibers was established for each of the various intrafusal fiber types. These histochemical observations are discussed with regard to the current concepts of cat spindle morphology and motor innervation. The results suggest a degree of predictability in the spindle fiber content and in the distribution of motor nerve terminals along intrafusal muscle fibers, at least in the tenuissimus muscle.     

Observations on the primary sensory ending of tenuissimus muscle spindles in the cat

Summary The arrangement of preterminal and terminal axon branches in the primary sensory endings of cat tenuissimus muscle spindles was studied using whole-mount and serial-section techniques. Although in every case one firstorder preterminal branch was supplied exclusively to the bag₁ type of intrafusal muscle fibre, the preterminal branching patterns differed considerably in detail.Terminals varied widely in size and location. Their precise form varied according to their position on the intrafusal muscle fibres rather than their relationship to preterminal branches. Terminals derived from separate preterminal branches remained separate and did not fuse with themselves or each other. Individually bag₁ fibres had most terminals, chain fibres least. The surface of the muscle fibres were differentially indented by the terminals, least in bag₁ fibres and most in chain fibres.The results are discussed in relation to mechanosensory transduction and to the factors involved in determining the form of the primary ending.     

The organization of muscle spindles in the tenuissimus muscle of the cat during late development

Intrafusal muscle fibers in the tenuissimus muscle of the cat develop as two separate groups; one being a single nuclear bag fiber while the other comprises a second nuclear bag fiber along with all the nuclear chain fibers. The groupings are very distinctive in the late fetus (55 days gestation) and remain so until 18 days of age. In the adult, the grouping is less distinctive but can often be recognized and followed for considerable distances within the capsular region of the spindle. Each group develops under its own basement membrane and is separated from the other by fibrocytes. ATPase histochemistry indicates the isolated single nuclear bag fiber is slow twitch while the fibers of the other group, the second bag and all the nuclear chains, are fast twitch. The organization of intrafusal fibers in late development into two groups of different fiber types is discussed in relation to their selective innervation by γ fibers.     

Dynamic properties of cat tenuissimus muscle

Some of the factors which influence the development of tension in cat tenuissimus muscle were studied quantitatively. Under isometric conditions, it was shown that the dynamic properties of the relationship between the tension of the muscle and its electrical stimulation depend on the mean rate of stimulation. This non-linear effect cannot be explained on the basis of the dependence of muscle tension on instantaneous rate of stimulation since the tension due to a stimulus following closely a previous stimulus is augmented, but the time course of the twitch response is unaltered. The interaction between the tension due to active contraction and that due to the viscoelastic properties of the muscle was investigated by independently varying muscle length and the rate of stimulation. Within the limits of resolution of the data, it was concluded that these two components of tension are additive and that muscle stiffness is related to the instantaneous tension of the muscle.     

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.     

Spontaneous activity of passive muscle spindles of the cat triceps surae muscle

The hypothesis that one possible cause of the spontaneous discharge of muscle spindles in the totally relaxed and de-efferented triceps surae muscle, with its tendon divided, is the mechanical factor due to extrafusal-intrafusal interaction was tested in experiments on anesthetized cats. Responses of spontaneously active units were similar with respect to many indices to responses of silent receptors capable of generating a long discharge in response to an increase in static length of the muscle. Isotonic contraction of the relaxed muscle during direct or indirect stimulation was accompanied by a pause in spontaneous activity. The prolonged increase in discharge frequency sometimes arising as a result of pressure on the muscle in the region of the receptor also was abolished by weak isotonic contraction of the muscle. If a long posttetanic sensory discharge was induced in a spontaneously active receptor by intensive tetanization of the nerve to the muscle, and it was then abolished by short stretching of the muscle, the initial spontaneous discharge frequency was restored. The dynamic thresholds of spontaneously active receptors were lower than for silent receptors. In some spontaneously active receptors an initial slowing of the discharge was observed during linear or stepwise stretching of the muscle. It is suggested that the ability of sensory endings to generate a long spontaneous discharge is due to initial stretching of the spindle inside the relaxed muscle.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 10, No. 3, pp. 287–294, May–June, 1978.     

The occurrence of muscle spindles in extraocular muscles of various vertebrates

Extraocular muscles from representative species of vertebrate groups ranging from amphibians to the higher mammals were examined in serial histological sections for the presence of muscle spindles. These observations and data from the literature indicate that extraocular muscles of the pig, calf, sheep and other even-toed ungulates are richly supplied with well-defined spindles having a generous complement of intrafusal fibers distinguishable as nuclear bag and chain fibers. Spindles in human eye muscles are also numerous. In macaque and chimpanzee muscles a few poorly developed spindles were present in some, but not all, muscles. No encapsulated receptors were found in 20 other mammalian and submammalian species examined in this study. When present, spindles tended to be located in the zone of small muscle fibers found along the orbital surface of the muscle. Rectus and oblique muscles in all species had such a zone, so that its existence did not determine whether spindles would occur.     

Examination of chronically de-efferented cat muscle spindles for cholinesterase activity

Summary Cat tenuissmus muscles were deprived of motor nerve supply for three months by sectioning of the appropriate ventral spinal roots. Muscle spindles were located in the chronically de-efferented muscles and examined histochemically in serial transverse sections. Staining for nicotinamide adenine dinucleotide tetrazolium reductase showed that the spindle sensory innervation was preserved. The de-efferented intrafusal muscle fibers retained their differential staining with the reaction for myosin adenosine triphosphatase. However, all cholinesterase-active areas that are normally found along nuclear bag and nuclear chain intrafusal fibers demonstrated loss of the enzyme activity in the chronically de-efferented spindles. It is concluded that all histochemically demonstrable cholinesterase activity within the cat muscle spindle is dependent upon the continuous presence of motor innervation.     

Effects of stimulating the lumbar sympathetic trunk on cat hindlimb muscle spindles

1. The effect of stimulating the lumbar sympathetic trunk has been observed on cat lumbrical and tenuissimus muscle spindles. 2. Spindle afferent discharges were recorded either from single Ia fibers in teased dorsal root filaments or from a large number of spindles by integrating their discharges led from muscles nerves. 3. Blood flow in small arteries supplying the muscle was observed through a microscope during and after the stimulation of the sympathetic trunk. 4. In some spindles repetitive stimulation of the sympathetic trunk elicited, after a few seconds delay, a small increase in firing rate. This can be ascribed to a direct action of sympathetic axons on the spindles because it precedes by about 20-30 sec the reduction of blood flow observed in the muscle arteries. This effect is not accompanied by a change in dynamic sensitivity of the primary ending. 5. This early effect is followed, after 20-30 sec, by a later rise in firing frequency which still progresses after the end of stimulation and eventually terminates in an abrupt fall in firing often leading to interruption of the ending activity. Recovery takes places at a variable time after the blood flow has bee reestablished. These long lasting effects can be ascribed to reduction of blood flow in muscle spindles since they are always associated with changes in blood flow in muscle arteries and since they are mimicked by occlusion of the muscle circulation. 6. In some spindles, the amplitudes of frequencygrams elicited by stimulation of static gamma axons were slightly increased suggesting a weak facilitatory effect on the contraction of some intrafusal muscle fibers.     

Occurrence and distribution of muscle spindles in masticatory and suprahyoid muscles of the rat.

The occurrence and distribution of muscle spindles was studied in histochemically and conventionally stained serial cross sections of 6-week-old and adult rat masticatory and suprahyoid muscles. Spindles were present in moderate to large numbers in jaw closers, but they were absent in jaw openers and two of four muscles of an accessory suprahyoid group. In jaw closers, 67% or more of the total spindle population was concentrated relatively distant from the temporomandibular joint, in muscle portions which contained large numbers of extrafusal fibers reacting strongly for oxidative enzymes. Because of their location, spindles in these portions should be stretched more and, subsequently, should respond with a greater afferent discharge at any given muscle length than spindles situated nearer to the joint. Spindles in jaw closers, especially the medial pterygoid and deep masseter, often occurred in clusters and complex forms near the terminal branching of intramuscular nerve trunks. No such concentrations were seen in the two muscles of the accessory suprahyoid group that had spindles. The association in jaw closers of spindles with extrafusal fibers high in oxidative enzyme activity is consistent with the view that spindles are the sensory component of a reflex system that recruits these fibers for finely-graded contractions in response to small internal length-changes of the muscle (Botterman et al., '78); however, in jaw openers and two muscles of the accessory suprahyoid group, the absence of spindles, coupled with the presence of large populations of extrafusal fibers high in oxidative enzyme activity, is not easily reconciled with this concept.     

A new grouping of intrafusal muscle fibers based on developmental studies of muscle spindles in the cat.

The development of muscle spindles was studied using the tenuissimus muscle of the cat. Observations show that the intrafusal muscle fibers develop as two separate groups: one group represented by a single nuclear bag fiber while the second group comprises the second nuclear bag fiber in association with all the nuclear chain fibers. This grouping is most pronounced in the fetus and is clearly seen in neonatal kittens (i.e., up to 2 weeks of age). As the intrafusal fibers begin to separate from each other, the groupings become less noticeable, although this basic pattern is often retained in the adult. The pattern of intrafusal fiber grouping is most noticeable in the equatorial regions of the spindle and least noticeable in the polar regions. This is not the grouping of fibers which would have been expected from a consideration of existing reports on muscle spindles. The implications for spindle form and function are considered.