Extrafusal Muscle Research Articles

Microvasculature of Rabbit Muscle Spindles

The microvasculature of the muscle spindle and its relationship to the microcirculation of teniussimus extrafusal muscle is described. Muscle spindles lie in close proximity and parallel to the central artery, vein, and nerve. The arterioles to spindle capillaries are third to fourth order branches of the central artery, whereas most arterioles to extrafusal capillaries are sixth to eighth order. Two or three capillaries enter each spindle. At least one entry consistently was encountered in the equatorial area near the sensory endings. Branches of intrafusal capillaries run longitudinally, anastomose with each other, and cradle the sensory zone in a longitudinal capillary loop. Capillaries in muscle spindles are larger than those in extrafusal muscle. These characteristic features are presumed to enhance the capability of these capillaries to provide sufficient circulation to the spindle, particularly to the region of the sensory endings.

The regularity of muscle spindle discharge in man.

1. The variability of discharge of thirty-nine muscle spindle afferents from the pretibial muscles of normal human subjects was determined for spike train sequences recorded with the ankle joint fixed in 25 degrees plantar flexion, during further stretch and during graded voluntary contractions of the receptor-bearing muscle. 2. In non-contracting muscles with the ankle joint in 25 degrees plantar flexion, a sustained discharge was maintained by twenty-four of the thirty-nine endings. The mean discharge frequency for the active endings was 11.1 Hz (range 4.8--22.1 Hz), the mean coefficient of variation 0.073 (range 0.021--0.183). With further stretch, the discharge of endings maintaining frequencies below 10--12 Hz became more regular. For endings maintaining higher frequencies, changes in the coefficient of variation were small and occurred in either direction. All secondary endings maintained a highly regular discharge, but, at these frequencies, there was no statistically significant difference in the variability of primary and secondary endings. 3. It is considered that these findings are comparable to those of Matthews & Stein (1969) for de-efferented feline spindle endings, and support the view that there is no functionally effective background fusimotor drive to non-contracting muscles of normal human subjects. 4. A voluntary contraction sufficient to accelerate a spindle ending invariably decreased the regularity of its afferent discharge. During voluntary contractions, coefficients of variation up to 0.345 were recorded. However, coefficients as low as 0.1 were not uncommon, and thus the absence of fusimotor drive cannot necessarily be inferred from a regular afferent discharge pattern. 5. With contractions of different strength, the increase in the coefficient of variation did not parallel the increase in discharge frequency. It is concluded that not all fusimotor influences acting on a spindle ending are translated into variability, and that measurements of the variability of discharge do not accurately reflect the level of fusimotor drive. 6. The discharge frequency of some spindle endings decreased slightly in some contractions and this was accompanied by an increase in the variability of discharge. It is suggested that contracting extrafusal muscle fibres can modulate the discharge pattern of spindle endings and contribute to the variability of discharge during a voluntary contraction. 7. In contracting muscles the irregular fusimotor-driven spindle discharge contained a 'hidden' periodicity, but this was not as extensive as has been reported for the cat. No such periodicity could be demonstrated for spindle endings in non-contracting human muscles.

Histophysiological observations on fast skeleto-fusimotor axons

In three instances, repetitive stimulation of a single fast skeleto-fusimotor axon supplying cat tenuissimus muscle was observed to activate a secondary ending belonging to a precisely located spindle. Prolonged repetitive stimulation of these β-axons elicited glycogen depletion in the intrafusal muscle fibres of the located spindles and in extrafusal fibres. The intrafusal depletion affected the longest of the chain fibres in two instances, and the bag 1 and bag 2 fibres in the third instance. In one experiment, the discharge from the primary ending of the located spindle was also recorded. The fast β-axon (it supplied the longest chain fibre in the spindle) had a static action on the primary ending. The extrafusal muscle fibres of the 3 fast β-motor units belonged to the fast oxidative-glycolytic type.

Permeability of muscle spindle capillaries and capsule

The permeability of capillaries in rabbit muscle spindles, intramuscular nerves, and extrafusal muscle to intraaortically infused horseradish peroxidase (HRP) was studied. The permeability of the capsule cells of the muscle spindles was also examined. Immediately following the infusion of HRP, most extrafusal capillaries contained a dense accumulation of HRP reaction product, which began to escape into the surrounding extracellular space within 2-3 min. In contrast, the concentration of HRP in the intrafusal and endoneurial capillaries was much lower than that in extrafusal capillaries, and HRP was never found outside the former vessels. In addition, HRP never completely penetrated through the spindle capsule from the extracellular into the periaxial space, although it was regularly found between the outer two or three layers of capsule cells. The results indicate that the permeability characteristics of the muscle spindle capillaries and capsule to the tracer protein HRP are very similar to those of capillaries in peripheral nerve.

Changes in ATPase and SDH reactions of the rat extrafusal and intrafusal muscle fibres after preincubations at different pH

The dependence of adenosine-triphosphatase (ATPase) and succinic dehydrogenase (SDH) histochemical reactions on the pH of the preincubation medium was studied in serial cross sections of 1- to 6-month-old rat extensor digitorum longus (EDL) and soleus (SOL) muscles. The use of a wide spectrum of pH values confirmed the previous results showing that: (1) according to their ATPase and SDH reactions 3 types of extrafusal muscle fibres, i.e., fast-twitch glycolytic (FG), fast-twitch oxidative-glycolytic (FOG) and slow-twitch oxidative (SO) and 3 types of intrafusal muscle fibres, i.e. typical and intermediate nuclear bag fibres and nuclear chain fibres were observed; (2) only acid preincubation (pH 4.35) is necessary to demonstrate the reversal of the ATPase reaction; while (3) alkali preincubation (pH 10.4) does not provide any new important information as compared with ATPase without preincubation. Furthermore, it was shown that: (4) fast-twitch muscle fibres exhibited high ATPase activity on preincubations at pH 4.9 to 10.4, slow-twitch fibres had very high ATPase activity on preincubation at pH 4.3 and 4.5; (5) after preincubation at pH 4.5 two types of FOG fibres were observed, differing in their ATPase activity; (6) in both muscles there were fibres with intermediate ATPase activity both after acid and/or alkali preincubations; (7) the intrafusal muscle fibres exhibited some specific characteristics when compared with extrafusal fibres. In contrast to the ATPase reactions, SDH activity was decreased equally, in both extra- and intrafusal fibres, with increasing acidity and alkality of the preincubation medium.

The fine structure of denervated and reinnervated muscle spindles: Morphometric study of intrafusal muscle fibers

The fine structure of normal, denervated, and reinnervated muscle spindles in lower lumbrical muscles of rats was studied morphometrically at time intervals ranging from 3-14 months. In control spindles, the mean transverse area of mitochondria was estimated to be more than twice as large in nuclear chain than in typical nuclear bag fibers. Following denervation, there was a severe decrease of the mean number and transverse area of mitochondria, and a moderate, but statistically significant decrease of the mean transverse area of intrafusal muscle fibers (IMFs) despite an increase of the number of IMFs. At 12-14 months of reinnervation, changes of the transverse areas of IMFs were statistically insignificant, but the mean values for the mitochondria were incompletely restored. At 4 x 3 months, after fourfold repeated crush injuries to the nerve, most of the values estimated (transverse area of mitochondria; number, shape, and transverse area of IMFs and nuclei) tended to approach those in denervated rather than in reinnervated IMFs. The differences of the reactions of intra- and extrafusal muscle fibers following complete motor and sensory denervation appeared to be in accordance with their normal dimensional dissimilarities.

Small-signal analysis of response of mammalian muscle spindles with fusimotor stimulation and a comparison with large-signal responses.

1. Response dynamics of primary and secondary muscle spindle endings to small-amplitude sinusoidal stretches were found to be unaltered by tonic repetitive stimulation of fusistatic or fusidynamic fibers. 2. Overall sensitivity of these receptors is decreased by fusistatic stimulation and either unchanged, increased, or decreased by fusidynamic stimulation at rates of 75/s or greater. 3. In the case of primary endings, the results obtained with small-amplitude sinusoidal stretches are not compatible with the response of these receptors to large-amplitude ramp stretches. The difference is explained by dependence of receptor dynamics on stretch amplitude. Fusistatic stimulation tends to prevent those changes in dynamics, whereas fusidynamic stimulation tends to enhance them. 4. In the case of secondary endings, the results obtained with small- and large-amplitude stretches appear to be compatible with a linear model for this receptor (i.e., one with dynamics independent of input parameters). 5. By modulating the frequency of stimulation applied to fusimotor fibers and comparing the resulting afferent response to the receptor response to stretch dynamic characteristics of intrafusal muscle contraction can be deduced. The results suggest that the dynamics of fusiastatic and fusidynamic contraction are the same and, furthermore, that they are the same as those of extrafusal muscle. We note that the result is incompatible with measurements of the time course of twitch and tetanus development and suggest, therefore, that muscle dynamics are a function of contractile state.

Origin and nature of correlations in the Ia feedback pathway of the muscle control system

Mammalian primary muscle spindle endings receive two inputs from fusimotor fibres and length changes of their extrafusal environment. Both inputs are also powerful noise sources disturbing the discharge patterns of the receptors. In this paper emphasis is laid on the extrafusal component. It is shown that extrafusal muscle activity can be viewed as a stochastic process which, acting as a common source, can correlate discharge patterns of adjacent muscle spindles. Some quantitative characteristics of these correlations and their relation to the underlying mechanical events are investigated in some detail in order to provide data for more theoretical considerations on their possible physiological importance.

Occurrence of an “Extrafusal Muscle Fiber” in the Spindle Capsule of Normal Adult Zebra-Finches: An Electron Microscopical Study

Occurrence of an “Extrafusal Muscle Fiber” in the Spindle Capsule of Normal Adult Zebra-Finches: An Electron Microscopical Study

Types of intra- and extrafusal muscle fibre innervated by dynamic skeleto-fusimotor axons in cat peroneus brevis and tenuissimus muscles, as determined by the glycogen-depletion method.

1. The types of intra- and extrafusal muscle fibre innervated by dynamic skeleto-fusimotor (beta) axons were determined by using a modification of the glycogen-depletion method of Edström & Kugelberg (1968) combined with histochemical tests for various enzyme reactions. A single beta axon was prepared in each of the experiments, which were carried out on six peroneus brevis and two tenuissimus muscles. 2. The intrafusal distribution of dynamic beta axons is almost exclusively restricted to bag1 fibres. The bags fibre was depleted in each of twenty-four beta-innervated spindle poles; the only fibres of a different type depleted intrafusally were a bag2 fibre in one pole and a long chain in another. 3. Depletion in the bag1 fibres was usually restricted to one zone in one pole, generally in a mid-polar location. 4. The extrafusal muscle fibres depleted by dynamic beta axons belong to the slow oxidative type as defined by Ariano, Armstrong & Edgerton (1973). The number of such fibres in each motor unit could not be accurately determined, but is almost certainly small. 5. The slow oxidative muscle fibres innervated by dynamic beta axons were not depleted over their entire length. Since there is no reason to assume that they are not twitch fibres, it would seem that the localized depletions result from the conditions required to obtain glycogen depletion, i.e. long periods of motor stimulation applied during the occlusion of the muscle's blood supply. Under similar experimental conditions depletion of glycogen was also restricted to portions of fibres in fast oxidative-glycolytic motor units, but extended over most of the length of the fibres in fast glycolytic units.

Muscular dysgenesis in the mouse (mdg/mdg). I. Ultrastructural study of skeletal and cardiac muscle.

Muscular dysgenesis (mdg/mdg), transmitted as an autosomal recessive trait in the mouse, is characterized by a total inability to contract any skeletal muscle. In addition, there is fixation of posture at multiple joints at the time of birth (arthrogryposis multiplex congenital). This muscular disorder has been studied by light, phase and electron microscopic techniques, combined with cytochemical methods. The homozygous mutant fetuses (mdg/mdg) and their littermates(+/?) were studied at time intervals of from 18 to 20 days of gestation. Four litters of non mdg mice (+/+) resulting from the matings of Harvard white mice also served as controls. Structural alterations were found both in cardiac ancd skeletal intrafusal and extrafusal muscle. These changes were characterized by a deviation in the course of muscle development. The most significant change was considered to be in the contractile substance, particularly in the Z band structure. Changes in the sarcotubular system and the retarded development of the motor end plate appeared to result from this primary abnormality in contractile substance. Contraction bodies were consistently located close to close to the motor end plate. The presence of contraction bodies, and the failure of muscle-tendon junctions to form seemed to be related to an alteration of the contractile filaments. Limited longitudinal growth of the muscle fibers and disorganization of myofibrils were attributed to the incomplete development of the Z band.

The influence of extrafusal muscle activity on discharge patterns of primary muscle spindle endings.

The influence of extrafusal muscle activity in anaemically decerebrate cats upon discharge patterns of primary spindle endings was ascertained by simultaneously recording spike trains from several Ia afferents and muscle tension fluctuations of the triceps-surae muscle. 1. Tension fluctuations were averaged with respect to spikes from primary endings yielding tension "trajectories" of specific shape for each spindle and probably reflecting frequently recurring mechanical events in the spindles' surroundings. 2. Spindles situated in close vicinity and influenced by similar mechanical events as evidenced by similar average tension trajectories are correlated in their discharge patterns to a degree depending on the strength of their mechanical coupling. 3. The modulation of spindle discharge frequency in response to average tension changes at the muscle tendon is very different in amplitude for different spindles; this response may show a high sensitivity. It is usually phase advanced by 90-180 degrees with respect to the "internal length" changes; between spindles ther may be phase differences of up to 180 degrees. 4. It is concluded that primary endings react very sensitively to local extrafusal events. The CNS receives much more accurate information about these events in the correlation of several Ia afferents than in the discharge of a single fibre.

Sensory terminals on extrafusal muscle fibres in myotendinous regions of developing rat muscles.

Axon terminals were observed to form neuromuscular contacts with extrafusal muscle fibres in myotendinous regions of developing rat muscles up to 5 days after birth. These neuromuscular contacts are found in fascicles of muscle fibres connected with differentiating Golgi tendon organs. Axon terminals establishing these contacts are obviously sensory, since they do not degenerate after de-efferentation performed in neonatal rats. The terminals contain mainly clear and dense core vesicles and form neuromuscular connections resembling developing motor endplates, with a cleft about 60 nm wide and basal lamina interposed between the axolemma and the sarcolemma. Each terminal, however, also forms a close contact in a restricted region where the basal lamina is missing; there the cleft is reduced to 20 nm and the axolemmal and sarcolemmal membranes are linked by desmosome-like attachment plaques. After the fifth postnatal day, axon terminals become detached from muscle fibres and are only found among collagen bundles of the tendon organ. The functional significance of these temporary neuromuscular contacts is not clear.

Analysis of the dynamic responses of deefferented primary muscle spindle endings to ramp stretch.

A detailed analysis of the complex dynamic response of 8 deefferented primary muscle spindle endings to ramp stretches of the extensor digitorum longus muscle (EDL) was made in anaesthetized cats. The analysis was based on Lennerstand's linear muscle spindle model, in which the dynamic peak, i.e. the peak frequency at the end of the dynamic phase of a ramp stretch, is assumed to consist of three components: a position response, a slow velocity response, and a quick velocity response. The components of the dynamic peaks analysed were fairly well correlated with the static behaviour of the primary muscle spindle endings, the latter, in turn, being regarded as an indicator of the spindles' location in the non-homogeneous extrafusal muscle. The results thus provide a satisfactory explanation of the high correlations between the static and gross dynamic behaviour of deefferented primary muscle spindle endings of the EDL previously reported from our laboratory.

The Skeleto-fusimotor Innervation of Cat Muscle Spindle

Publisher Summary In this chapter, physiological and histological observations are reviewed, which shows that a significant proportion of spindles are innervated by collaterals from motor axons that supply extrafusal muscle fibres, that is, by skeleto-fusimotor or β axons. The following points are considered—rate of degeneration of p 1 plates after section of the muscle nerve, experimental demonstration of β axons in large hind limb muscles, proportion of spindles supplied by dynamic β axons in the peroneus brevis muscle, and histophysiological determination of the types of muscle fibres innervated by β-axons using the glycogen depletion technique.

Proportion of muscles spindles supplied by skeletofusimotor axons (beta-axons) in peroneus brevis muscle of the cat.

Of 32 cat peroneus brevis spindles, 23 (72%) were found to be supplied by a least 1 skeletofusimotor or beta-axon. A motor axon was identified as skeletofusimotor when repetitive stimulation of it elicited both the contraction of extrafusal muscle fibers and as acceleration of the discharge of primary ending, which persisted after selective block of the neuromuscular junctions of extrafusal muscle fibers. The block was obtained by stimulating single axons at 400-500/s for a few seconds. Of 135 axons supplying extrafusal muscle fibers, 24 (18%) were shown to be beta-axons; 22 beta-axons had conduction velocities ranging from 45 to 75 m/s. All but three beta-axons increased the dynamic sensitivity of primary endings. Beta-innervated spindles may also be supplied by dynamic gamma-axons.

The pathology of the muscle spindle in myasthenia gravis

Abnormalities in the morphology and motor innervation of the muscle spindles are described in 4 autopsied cases of myasthenia gravis. There were changes consistent with motor denervation in 5 of 118 spindles examined in sectioned material. In 65 teased, silver-impregnated spindles there was proliferation of the fusimotor innervation due to axonal sprouting occurring in the endings themselves. Motor end-plates on the intrafusal muscle fibres showed “dystrophic” changes similar to those previously described in extrafusal muscle in this disease. The sensory innervation was normal. The possible significance of these findings is discussed.

Skeleto-fusimotor axons in the hind-limb muscles of the cat.

1. Motor axons supplying various hind-limb muscles of the cat (flexor hallucis lingus, peroneus brevis, peroneus digiti quinti, tibialis anterior, soleus and tenuissimus) were identified as skeleto-fusimotor or beta axons because their repetitive stimulation elicited both the contraction of extrafusal muscle fibres and an increase in the rate of discharge of spindle primary endings which perisited after selective blockade of extrafusal neuromuscular junctions. 2. The conduction velocity of these axons ranged from 39 to 92 m/sec. 3. Of seventy-six beta axons, seventy-two had a dynamic action on the sensitivity to velocity of stretching of primary endings, four had a static action. 4. The dynamic action of six beta axons was observed only after the contraction of extrafusal muscle fibres was selectively suppressed. 5. Tendon organs can be activated by beta motor units.

Discharge of spindle afferents from jaw-closing muscles during chewing in alert monkeys.

The discharge of muscle spindle afferents from monkey spindle afferents from monkey jaw-closing muscles was studied during mastication of natural foods by extracellular recording from the fibers or cell bodies of the tract and mesencephalic nucleus of the fifth nerve. In all, 39 muscle afferents were studied. The spindle associated with 18 of the afferents was positively identified by the afferent's response to gentle, localized palpation of either the temporalis or masseter muscle. Discharge patterns were observed during mastication, and in the majority of cases the qualitative passive response characteristics of the spindle afferent were determined. During steady chewing spindle afferent discharge typically paused briefly during the initial rapid upward part of the chewing cycle. Firing generally began as the jaw slowed its upward movement, and firing rates during the slow grinding portion of the upward movement were within the range of 50-80 spikes/s. All spindles exhibited a brisk discharge during the opening movement, typically within the range of 100-150 spikes/s. One-third of the spindle afferents exhibited a brief, high-frequency burst of firing at the very beginning of the opening movement, presumably as a result of stretch applied to a spindle just previously subjects to fusimotor excitation. Although the results of the study make it clear that spindles in jaw-closing muscles are coactived along with the extrafusal muscle fibers, the fusimotor bias does not seem capable of sustaining discharge in the face of rapid shortening of the muscle. Furthermore, the fact that discharge rate during opening, when the jaw-closing motoneurons are quiescent, is much higher than at any part of the closing cycle, when the motoneurons are active, suggests that the muscle spindles cannot provide the primary excitatory drive to the motoneurons.

THE FINE STRUCTURE OF THE SPINDLE ABNORMALITY IN MYOTONIC DYSTROPHY

The fine structure of the intrafusal muscle fibres, and of their innervation, has been studied in three muscle spindles found in muscle biopsies from two patients with myotonic dystrophy. The poles of the intrafusal muscle fibres were longitudinally fragmented. The fragments were arranged in up to twenty clusters, each bounded by a single layer of basement membrane. Degenerative and regenerative changes were observed in the fibre fragments. The most abnormal fragments were situated at the periphery of the clusters and there was some evidence that these degenerate fragments were extruded from the clusters, into the periaxial space. Many fibre fragments were anucleate. Only six motor endplates were found, despite a search of the spindle poles by serial section. All were simplified in form. The fine structure of the primary and secondary sensory innervation was normal, and the equatorial regions of the intrafusal fibres were not fragmented. It is suggested that these observations are consistent with the hypothesis that the characteristic spindle abnormality in myotonic dystrophy is due to fragmentation of the poles of the intrafusal muscle fibres, due to mechanical stresses imposed on abnormal muscle fibres by myotonia or myotonic after‐discharges, and that this, as a continuing process, leads to denervation of the individual fragments, and to the observed degenerative changes, at a time when the extrafusal muscle fibres may appear relatively mildly affected.