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Impulse rates and sensitivity to stretch of soleus muscle spindle afferent fibers during locomotion in premammillary cats.

Impulse from soleus muscle afferents were recorded in premammillary cats that were walking on a treadmill. In normal walking the effects of gamma-motoneurons on impulse rates of muscle spindle afferents are confounded by the effects of the large length changes that occur. To isolate the effects of gamma-motoneurons the leg was fixed in place for recording and denervated except for soleus muscle. Because gamma-motoneurons produce marked effects on the stretch sensitivity of muscle afferents, soleus muscle was oscillated about a present length so the stretch sensitivity of its afferents could be determined. The impulse rate of secondary muscle spindle afferents in soleus muscle was generally increased at all phases of the step cycle. The mean rate approximately doubled during walking (82 imp/s), compared with nonwalking (rest) periods (44 imp/s). The sensitivity to sinusoidal length changes was generally reduced throughout the step cycle (mean reduction = 33%). Primary muscle spindle afferents also showed an increased mean rate during walking (47 imp/s) compared with rest (24 imp/s). The impulse rate peaked after the muscle reached its maximum force and often showed a second peak before the maximum electromyogram (EMG) activity. The sensitivity to sinusoidal stretches varied cyclically during locomotion. During the extension phase it sometimes exceeded the resting value, but was greatly reduced during the flexion phase (mean reduction = 49% over whole cycle). Control experiments were carried out in which static and dynamic gamma-motoneurons were stimulated and activity from muscle spindle afferents was recorded in anesthetized cats. With the amplitude and frequency of stretch applied, stimulation of dynamic gamma-motoneurons usually increased and stimulation of static gamma-motoneurons usually decreased the sensitivity of primary muscle spindle afferents to sinusoidal stretch. The patterns observed in muscle spindle afferents suggest a strong, maintained activation of static gamma-motoneurons throughout the step cycle and a phasic activation of dynamic gamma-motoneurons, which is consistent with previous direct recordings from gamma-motoneurons. With this pattern of activating gamma-motoneurons, the secondary muscle spindle afferents will provide a good feedback signal of the large length changes that normally occur in the muscle during locomotion. The changes in sensitivity of primary muscle spindle afferents will complement central changes so the gain of the stretch reflex from extensors is high during extension (when required to help support the weight of the body) and low during flexion (when a high gain would be counterproductive).

Anesthesia, General↗

The early development of muscle spindle in human foetus.

The normal development of muscle spindles has been carefully described in a variety of species but only a few attempts were made to study the embryological development of the muscle spindle in humans. Most of the studies aimed to define the early development of muscle spindle in human foetuses, stated the begin of this process at the 11th week of intrauterine life, when the formation of a network of very fine nerve fibres with enlargements and ringle around developing muscle cells occur. In the present study we tried to document the probably earliest time of appearance of muscle spindles in the skeletal muscle of human foetuses. To this aim we examined fragments of deltoid and gastrocnemius muscles removed from human foetuses at the 9th and 10th week of gestation by using the light microscope technique. Data collected in muscle specimens at the 9th and 10th week of gestation showed the presence, at this time, of a structure with features clearly different from that of the adjacent muscular areas. This structure consists in a number of flat mesenchymal cells surrounding and forming several layers around a bundle of myoblasts smaller and lesser differentiated than the muscle cells located around and it is in close relationship with nervous fibres. These morphological findings might allow to identify the earliest stage of muscle spindle formation in human species.

Gestational Age↗

Impulse activity and receptor potential of primary and secondary endings of isolated mammalian muscle spindles.

1. An isolated muscle spindle preparation from a tail muscle of cat is described. The afferent response to a ramp-and-hold stretch was recorded in individual axons from identified primary and secondary endings. 2. Primary endings exhibit a prominent dynamic response, including an initial burst. They also show a well-maintained static discharge. Secondary endings also show a well-sustained static discharge but generally have a much lower dynamic sensitivity. The response of primary and secondary endings of the isolated spindle are similar to the typical responses seen in vivo in groups Ia or group II afferent fibres respectively. 3. Following impulse blockade by tetrodotoxin, the receptor potential was recorded from primary and from secondary endings in response to ramp-and-hold stretch. 4. During the dynamic phase the receptor potential of primary endings consists of a depolarization which has two components. (a) An initial component occurs early during ramp stretch, depends in rate of rise and amplitude on velocity of stretch and is reduced on repetitive stretch; it appears to be responsible for the initial burst. (b) A late dynamic component, which follows, is also dependent on stretch velocity and produces the late dynamic discharge. At the end of ramp stretch the receptor potential falls, and may undershoot, the static level. There is a subsequent adaptive fall during hold stretch, then a maintained static level of receptor potential. On release from stretch the membrane is hyperpolarized. 5. Secondary endings usually show a smaller dynamic response, lacking the initial component seen in primary endings. They also generally lack an undershoot following the ramp and have less of a post-release hyperpolarization. 6. Static levels of receptor potential in both primary and secondary endings are related to amplitude of stretch. 7. The receptor potentials of primary and secondary endings account for the major features of the impulse responses of these endings to ramp-and-hold stretch. In primary endings the dynamic frequencies may also depend upon a sensitivity of the impulse initiating site to rate of change of receptor current.

Animals↗

Identification of muscle spindles by direct and indirect electrical stimulation of intrafusal muscle fibers.

In two series of acute experiments on 25 anesthetized cats methods of rapid identification of muscle spindles based on electrical stimulation either of fusimotor nerve fibers or directly of the intrafusal muscle fibers were tested. The methods used are more reliable tests for the identification of muscle spindles than the generally accepted method of investigating the velocity of conduction of excitation along a single afferent fiber, for receptors both of the joints and of the deep tissues may also be innervated by fibers of the same diameter.

Animals↗

The number and distribution of muscle spindles and tendon organs in the peroneal muscles of the cat.

An analysis has been made of the numbers and distributions of muscle spindles and tendon organs in the three peroneal muscles of the lower hindlimb of the adult cat. Both peronei brevis and tertius were richly supplied with spindle capsules and tendon organs in comparison with peroneus longus and other muscles of the cat's lower hindlimb. A large number of the capsules in each muscle was involved in tandem linkages, some of these capsules comprising only a bag and some chain fibres. Such capsules were especially prevalent in peroneus tertius. The numbers of extrafusal muscle fibres inserting into each tendon organ indicated that the activity of each motor unit should be monitored by at least one tendon organ. The distributions of the receptors are discussed in relation to the proportion and density of oxidative muscle fibres.

Animals↗

Abnormal sensory and motor reinnervation of rat muscle spindles following nerve transection and suture.

Muscle spindles from the lower lumbrical muscles of rats were studied by transmission and scanning electron microscopy following reinnervation (i) after a single sciatic nerve crush lesion and (ii) after transection and immediate epineurial suture of the sciatic nerve. In all muscle spindles, regenerated sensory or motor nerve endings were encountered 3 months after making the lesions although in the nerve-transection group, regenerated nerve endings were seen less frequently before 6 months of recovery. Abnormalities in reinnervated spindles following neurotomy comprised: (1) multiplicity of axonal sprouts (hyperinnervation), sometimes irregularly related to, although never in direct contact with, regenerated sensory nerve endings; (2) altered contact relationships between sensory nerve endings and intrafusal muscle fibers; (3) abnormal structure of nerve endings; and (4) irregular association of Schwann cell processes to regenerated sensory nerve endings. These findings indicate that reinnervation of muscle spindles following transection and suture of a peripheral nerve, i.e., after complete interruption of its continuity, in fact, occurs although the fine structural abnormalities observed are supposed to interfere with adequate functional restoration.

Animals↗

[Changes in the sensitivity of the muscle spindles of fast and slow-contracting muscle fibers following chronic deafferentation].

The activity of muscle spindles was investigated in fast (m. EDL) and slow (m. sol) muscles of the cat 2-5 weeks after chronic deefferentation. The spontaneous activity of spindles in both muscles remains unchanged. The background activity and activity in dynamic and static phases of stretching both in primary and in secondary endings was much in chronic denervated muscle than in control. This increase in spindle activity was more pronounced in the slow muscle.

Muscle Contraction↗

Stimulation of chemosensitive afferents from multifidus muscle does not sensitize multifidus muscle spindles to vertebral loads in the lumbar spine of the cat.

STUDY DESIGN: Electrophysiologic recordings from muscle spindle afferents innervating the lumbar multifidus muscle of the cat while loading the L6 vertebra at its spinous process and while exposing the segmentally adjacent lumbar multifidus muscles to algesic and inflammatory mediators. OBJECTIVES: The purpose of this study was to investigate a possible mechanism underlying muscle spasm and pain in the lumbar spine. The hypothesis was tested that stimulation of chemosensitive afferents with receptive endings in the paraspinal muscle increases the discharge of paraspinal muscle spindle afferents during loading of a lumbar vertebra. The presence of such a phenomenon would provide a mechanism by which pain or inflammation could alter segmental lumbar biomechanics and contribute to lumbar spine dysfunction. SUMMARY OF BACKGROUND DATA: Muscle pain, tenderness, and altered muscle tone are often associated with musculoskeletal disorders. The literature suggests that stimulation of Group III and IV muscle afferents sensitive to algesic or inflammatory metabolites increases the stretch sensitivity of muscle spindles via a reflex pathway involving gamma-motoneurons. The reflex increase in muscle spindle activity, in turn, reflexly increases the excitability of alpha-motoneurons leading to enhanced muscle tone and the further accumulation of muscle metabolites and subsequent pain. Studies in the cervical spine support this hypothesis. It has not been investigated in the lumbar spine. METHODS: Single unit activity from muscle spindles in the L6 multifidus muscle were recorded from the cut peripheral end of the L6 dorsal root in alpha-chloralose-anesthetized cats and in decerebrate unanesthetized cats. The L6 vertebra was loaded at its spinous process using a force-feedback motor. Ramp and hold loads were delivered at 25%, 50%, 75%, and 100% body weight. Chemosensitive afferents in the L5 and L7 multifidus muscle were stimulated by bathing (subfascial injection) or infiltrating (intramuscular injection) the L5 and L7 multifidus muscles with bradykinin or capsaicin. RESULTS: Loading the L6 vertebra stimulated muscle spindles in the L6 multifidus muscle. Neither the saline volume control nor bradykinin nor capsaicin injected subfascially or intramuscularly affected the response of L6 multifidus muscle spindles to ramp and hold vertebral loads in the alpha-chloralose-anesthetized cat. In addition, neither saline nor bradykinin nor capsaicin injected intramuscularly affected the activity of L6 multifidus muscle spindles to ramp and hold vertebral loads in the unanesthetized decerebrate cat. CONCLUSIONS: These results indicate that stimulation of small diameter muscle afferents in a deep muscle of the lumbar spine does not sensitize muscle spindles to vertebral loads. These data do not support the hypothesis that fusimotor reflexes evoked by chemosensitive muscle afferents contribute to muscle spasm or to changes in muscle tone in the lumbar spine. In addition, the present results do not provide evidence for the pain-spasm-pain cycle in the lumbar spine.

Action Potentials↗

The initial burst of impulses in responses of toad muscle spindles during stretch.

The responses of muscle spindles in the iliofibularis muscle of the cane toad Bufo marinus were examined during constant velocity stretch of the passive muscle. Spindles were found to show an 'initial burst' of high frequency impulses at the onset of stretch. Associated with the initial burst was a steep passive tension rise in the whole muscle, the short-range elastic component (Hill, 1968), called here the passive stiffness. The size of the initial burst was found to depend on muscle length in a similar way as whole-muscle tetanic tension. Repetitive stretch was found to reduce both the initial burst and passive stiffness. The time taken for both to return to their control values was 3 and 10 s respectively. If immediately following repetitive stretch the muscle, and hence the spindle, was held stretched for 3 s, the initial burst in response to a subsequent stretch from a shorter length remained reduced in size for 300 s. The depression could be reversed by a brief period of fusimotor stimulation. Hypertonic Ringer solutions were found to increase the initial burst and passive stiffness, while both were reduced in hypotonic solutions. Low concentrations of caffeine (1.5 mM) produced a similar decrease in both the initial burst and the passive stiffness. Calcium-free Ringer solution left the stiffness unchanged, and increased the whole dynamic response of the spindle. Metabolic exhaustion and poisoning of the muscle caused the initial burst to increase while decreasing the active tension. It is concluded that the initial burst is an intrafusal manifestation of the passive short-range stiffness of extrafusal muscle which is thought to be due to the formation of stable cross-bridges between the actin and myosin filaments of myofibrils.

Action Potentials↗

[Role of muscle spindle afferents in the control of jaw-closing muscle activity].

In order to understand how muscle spindle afferents contribute to the control of jaw-closing muscle activity, the following two experiments were performed in the urethane anesthetized rabbits; 1) EMG activities of the masseter muscle during chewing a test strip were compared before and after the trigeminal mesencephalic tract (Mes V) lesion. The Mes V, where the ganglion cells of jaw-closing muscle spindle afferents are located, was lesioned by thermal cauterization. Since the cells lying around the Mes V may also be damaged, it is possible that the effects of lesioning may partly be ascribed to the destruction of these cells. In order to circumvent this problem, kainic acid was injected into the Mes V one week before the lesioning. 2) Unit discharges were recorded from the Mes V during passive jaw-opening and during chewing a test strip. The response of these units to suxamethonium (SCh) administration was also examined. The results were as follows; 1) In the animals with the Mes V lesion, the facilitatory response of the masseter muscle during chewing the test strip was significantly reduced on the side ipsilateral to the Mes V lesion, while the contralateral masseteric activities were not affected. 2) The Mes V units were classified as the primary and secondary spindle afferents depending on the responses to SCh administration. During chewing, the Mes V units showed discharges locked to a certain phase of a single masticatory cycle. They were classified into 4 types, depending on the time relation between unit discharges and the jaw movement; 1) those fired predominantly on the jaw-opening phase, 2) those fired on the jaw-closing phase, 3) those excited at the beginning of both-jaw opening and power phases and 4) those fired within the period of the masseteric burst. The firing frequency of the third type units increased during the jaw-closing muscle burst induced by application of the test strip between the opposing molars. They were sensitive to SCh administration and supposed to be the primary spindle afferents. It is concluded that the muscle spindles of jaw-closing muscles (presumably primary endings) contribute to the enhancement of jaw-closing muscle activities during chewing.

Animals↗

Histological and histochemical comparisons of muscle spindles in three hind limb muscles of the guinea pig.

Guinea pig soleus, medial gastrocnemius and vastus lateralis muscles were compared for spindle density and distribution, number of intrafusal fibers per spindle and histochemical appearance of the axial bundle. A total of 326 spindles was used in the comparisons. Spindle density was over four times greater in the soleus than in either the medial gastrocnemius or vastus lateralis. In the soleus the spindles were distributed at random, but in the other two muscles no spindles were found in those fascicles in which fast-twitch glycolytic extrafusal fibers predominated. The average number of intrafusal fibers per spindle varied by less than 5% between the three kinds of muscles. About 80% of all spindles located had four intrafusal fibers, two of the nuclear bag type and two of the nuclear chain type. The histochemical appearance of the axial bundle was the same in each kind of muscle. Based on intensities of the myofibrillar adenosine triphosphatase reaction product at polar regions nuclear bag fibers were separable into two histochemical groups; nuclear chain fibers were of only one histochemical type.

Adenosine Triphosphatases↗

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.

Animals↗

[Identification of muscle spindles by direct and indirect electric stimulation of intrafusal muscle fibers].

In two series of experiments on 25 anesthetized deefferented cats methods of quick identification of muscle spindles were used. The first method was based on the postcontractory sensory discharge in a muscle spindle after brief strong electrical stimulation of the muscle nerve. In another approach the concentric electrodes inserted into the muscle were used. If the intrafusal muscle fibers were selectively contracted by direct electrical stimulation the sensory discharge appeared without any increase in the total muscle tension. It seems that these methods enable to identify the unit under study more precisely in comparison with conduction velocity measurements, as the group I and II afferents are sometimes present in muscle nerve from joint and deep tissues.

Animals↗

Trigeminal mesencephalic neurons innervating functionally identified muscle spindles and involved in the monosynaptic stretch reflex of the lateral pterygoid muscle of the guinea pig.

Location of the neurons in the trigeminal mesencephalic nucleus innervating stretch receptors of the lateral pterygoid muscle and the mode of their synaptic connection on the lateral pterygoid motoneurons of the guinea pig were studied physiologically as well as morphologically, in comparison with the trigeminal mesencephalic neurons innervating muscle spindles in the superficial masseter muscle, with the following results: stimulation of the caudal half of the trigeminal mesencephalic nucleus evoked monosynaptic excitatory postsynaptic potentials in the ipsilateral lateral pterygoid motoneurons. Stimulation of the lateral pterygoid nerve directly evoked spike potentials in the neurons located in the caudal half of the ipsilateral trigeminal mesencephalic nucleus, which responded with increased firing to stretch, and with silent period to twitch, of the ipsilateral lateral pterygoid muscle. Averaging of intracellular potentials of the lateral pterygoid motoneurons with extracellular spike potentials of these trigeminal mesencephalic neurons revealed excitatory postsynaptic potentials after a monosynaptic latency, but no inhibitory postsynaptic potentials. Injection of horseradish peroxidase into the lateral pterygoid muscle labeled 15-20 cells in the caudal half of the ipsilateral trigeminal mesencephalic nucleus, while 174-228 cells retrogradely labeled by horseradish peroxidase were found throughout the whole rostrocaudal extent of the ipsilateral trigeminal mesencephalic nucleus following injection of horseradish peroxidase into the masseter muscle. It was concluded that neurons in the caudal half of the trigeminal mesencephalic nucleus send their peripheral processes to stretch receptors, presumably muscle spindles, in the ipsilateral lateral pterygoid muscle and that their central processes have excitatory synapses on ipsilateral lateral pterygoid motoneurons, thus comprising the afferent limb of a monosynaptic stretch reflex arc of the lateral pterygoid muscle of the guinea pig.

Animals↗

Histological study of motor innervation to long nuclear chain intrafusal fibers in the muscle spindle of the cat.

Several muscle spindles of the cat tenuissimus muscle were cut in serial, 1-micron thick transverse sections and stained with toluidine blue in search for long nuclear chain intrafusal muscle fibers. Five complete poles of the long chain fibers were located. Each fiber pole displayed one plate-type motor ending situated in the extracapsular fiber region. The endings were supplied by myelinated motor axons that originated from intramuscular nerve fascicles containing motor axons to extrafusal muscle fibers. One of the endings was innervated by a collateral from a motor axon that supplied an extrafusal end-plate. Ultrastructurally, the long chain endings resembled extrafusal end-plates. They were more complex, in terms of prominence of sole-plate and degree of post-junctional folding, than any other intrafusal ending present in the spindles. The motor endings of the long chain fibers were assumed to be the terminals of static (fast) skeletofusimotor axons, which preferentially innervate the longest nuclear chain fibers of cat muscle spindles.

Animals↗

Neurotrophin-3 and trkC in muscle are non-essential for the development of mouse muscle spindles.

Neurotrophin-3 (NT3) or TrkC null mutant mice were examined for the presence of muscle spindles. Muscles of mastication, but not limbs, contained spindles in newborn and adolescent mutants. The intramuscular distribution and morphological properties of spindles in mutant masticatory muscles were indistinguishable from those of wild-type spindles. Intrafusal fibers of NT3- or trkC-deficient spindles-expressed the slow-tonic isoform of myosin heavy chains, characteristic of wild-type spindles. Sensory nerve endings were observed in spindles of mutants by electron microscopy. Thus, NT3 or trkC, which is expressed in wild-type spindles, may serve functions other than those related to spindle assembly. Presumably, proprioceptive neurons innervating jaw muscles are dependent on factors other than NT3 for survival and maintenance.

Animals↗

The affinity of concanavalin A and wheat germ agglutinin for components of the muscle spindle.

Sections through the soleus muscle of the rat were incubated with concanavalin A (Con A) or wheat germ agglutinin (WGA) conjugated to fluorescein isothiocyanate. Binding of these lectins to structures which comprise the muscle spindle was studied by fluorescence microscopy. The distribution of the lectins was heaviest in the outer capsule of the spindle and at the surface of intrafusal muscle fibres. The periaxial space in the equatorial region of spindles was unlabelled except in the immediate vicinity of the axial bundle. Binding by Con A was more extensive than by WGA, suggesting that more glucopyranoside units are accessible within the muscle spindle than are those of N-acetylglucosamine.

Animals↗