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

Summary Distributions of motor axons to different types of intrafusal fiber were reconstructed from serial 1-m 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.     

Histological study of an unusual cat muscle spindle deficient in motor innervation

Summary An unusual muscle spindle innervated by only one somatic motor axon and one primary sensory axon was encountered in a cat tenuissimus muscle cut in serial transverse sections and examined by light and electron microscopes. The motor axon branched to supply the distal poles of the nuclear bag₂ and nuclear chain intrafusal muscle fibers through motor terminals of several types. The proximal poles of the bag₂ and chain fibers and both poles of the nuclear bag₁ fiber were devoid of motor endings. In spite of the limited motor nerve supply the bag₁, bag₂ and chain fibers exhibited the usual morphologic characteristics in terms of the appearance of the equatorial region, relative fiber lengths and diameters, and the number of associated elastic fibers. It appears that motor axons may play only a limited role, if any, in the differentiation and maintenance of the three types of intrafusal muscle fiber in the cat.     

Morphology and morphometry of motor endings in primate intrafusal fibers

Summary The pre- and postsynaptic structure of 243 axon terminals of bag 1, bag 2, and chain fibers were studied in cynomolgus monkey skeletal muscle spindles. The motor endings of the biceps and gastrocnemius spindles (long limb muscle) were compared to the motor endings of lumbricals and opponens pollicis (intrinsic hand muscle) spindles. In both muscle groups the only significant difference observed in the presynaptic features was in the presynaptic membrane length. The postsynaptic features of bag 1, bag 2 and chain endings were similar in the long limb muscle spindles. In the intrinsic hand muscle, however, the bag 1 and chain endings showed complex postsynaptic structure which resembled the extra fusal endings while the postsynaptic structure of bag 2 endings was much simpler. From these studies we conclude that the postsynaptic structure of various intrafusal fiber types is dissimilar in different muscles.     

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-μm-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.     

An ultrastructure investigation of intrafusal muscle fibers in myotonic dystrophy

Summary Ultrastructure features of muscle spindles from two patients with myotonic dystrophy are described. Intrafusal muscle fibers exhibit extensive splitting with nuclear bag fibers affected more so than nuclear chain fibers. No sensory endings are present on nuclear chain fibers nor on one nuclear bag fiber throughout the equatorial and myotube regions. Small motor end plates are evident on various segments of split intrafusal fibers in the polar region and some of these extend into the myotube region. Satellite cells are numerous on both nuclear bag and nuclear chain fibers. These frequently occupy the cleft space between segments of split intrafusal fibers. The myotonic dystrophy muscle spindle ultrastructure features seem to closely resemble the appearance of developing mammalian muscle spindles as illustrated with opossum fetal tissue.Supported in part by federal grants 5TO1 AMO5401-12 and 5RO1 HDO2788-06     

Structure, distribution and innervation of muscle spindles in avian fast and slow skeletal muscle

Muscle spindles in 2 synergistic avian skeletal muscles, the anterior (ALD) and posterior (PLD) latissimus dorsi, were studied by light and electron microscopy to determine whether morphological or quantitative differences existed between these sensory receptors. Differences were found in the density, distribution and location of muscle spindles in the 2 muscles. They also differed with respect to the morphology of their capsules and intracapsular components. The slow ALD possessed muscle spindles which were evenly distributed throughout the muscle, whereas in the fast PLD they were mainly concentrated around the single nerve entry point into the muscle. The muscle spindle index (number of spindles per gram wet muscle weight) in the ALD was more than double that of its fast-twitch PLD counterpart (130.5±2.0 vs 55.4±2.0 respectively, n=6). The number of intrafusal fibres per spindle ranged from 1 to 8 in the ALD and 2 to 9 in the PLD, and their diameters varied from 5.0 to 16.0 μm and 4.5 to 18.5 μm, respectively. Large diameter intrafusal fibres were more frequently encountered in spindles of the PLD. Unique to the ALD was the presence of monofibre muscle spindles (12.7% of total spindles observed in ALD) which contained a solitary intrafusal fibre. In muscle spindles of both the ALD and PLD, sensory nerve endings terminated in a spiral fashion on the intrafusal fibres in their equatorial regions. Motor innervation was restricted to either juxtaequatorial or polar regions of the intrafusal fibres. Outer capsule components were extensive in polar and juxtaequatorial regions of ALD spindles, whereas inner capsule cells of PLD spindles were more numerous in juxtaequatorial and equatorial regions. Overall, muscle spindles of the PLD exhibited greater complexity with respect to the number of intrafusal fibres per spindle, range of intrafusal fibre diameters and development of their inner capsules. It is postulated that the differences in muscle spindle density and structure observed in this study reflect the function of the muscles in which they reside.     

Sympathetic innervation of human muscle spindles

The aim of the present study was to investigate the presence of sympathetic innervation in human muscle spindles, using antibodies against neuropeptide Y (NPY), NPY receptors and tyrosine hydroxylase (TH). A total of 232 muscle spindles were immunohistochemically examined. NPY and NPY receptors were found on the intrafusal fibers, on the blood vessels supplying muscle spindles and on free nerve endings in the periaxial space. TH‐immunoreactivity was present mainly in the spindle nerve and vessel. This is, to our knowledge, the first morphological study concerning the sympathetic innervation of the human muscle spindles. The results provide anatomical evidence for direct sympathetic innervation of the intrafusal fibers and show that sympathetic innervation is not restricted to the blood vessels supplying spindles. Knowledge about direct sympathetic innervation of the muscle spindle might expand our understanding of motor and proprioceptive dysfunction under stress conditions, for example, chronic muscle pain syndromes.     

Distribution of skeletofusimotor axons in lumbrical muscles of the monkey

Summary The nerve supply to 25 poles of muscle spindles in the monkey was reconstructed by light microscopy of serial 1-m thick transverse sections of lumbrical muscles. Twenty of 60 motor axons that supplied the spindle poles were identified as skeletofusimotor (). Twenty-eight percent of the spindle poles were innervated by axons, in addition to axons. Every -innervated spindle pole transected an endplate zone of extrafusal muscle. Most axons coinnervated extrafusal fibers rich in mitochondria and the nuclear bag₁ or nuclear chain intrafusal fibers. All but two axons innervated one type of intrafusal fiber only. The intramuscular organization of motor system in lumbrical muscles of the monkey was similar to that of the cat tenuissimus muscle. The function of -innervated spindles may be preferentially to monitor mechanical disturbances arising from the activity of extrafusal muscle units with which they share motor innervation.     

First dorsal interosseous muscle of the foot and its innervation

During dissection of the foot region, it is frequently found that some nerve branches run close to the tibial surface of the second metatarsal bone. To investigate the nerve branches, detailed dissection of the first dorsal interosseous muscle was performed in 10 Japanese adult feet with special reference to its innervation. In all specimens the muscle was clearly separated into lateral and medial parts. The branches ran between these parts and innervated the parts. The small dorsal region of the medial part of the muscle was also innervated by a branch of the deep peroneal nerve. Based on its innervation, the muscle appears to be composed of two elements from the flexores breves profundi and an element from the dorsal primordium. A possible schematic model of the origins of this muscle is proposed. Clin. Anat. 12:12–15, 1999. © 1999 Wiley‐Liss, Inc.     

The innervation of the muscle spindle: a personal history

I present a brief review of current understanding of the innervation of the mammalian muscle spindle, from a personal historical perspective. The review begins with comparative studies on the numbers of spindle afferents and considers how their relative abundance may best be assessed. This is followed by an examination of the distribution and some functional properties of the motor innervation. The primary ending is the subject of the final section, in particular, I look at what can be learned from serial sectioning and volumetric reconstruction, and present new results on a model and simulations concerning sensory terminal deformation during stretch.     

Sympathetically-induced development of tension in jaw muscles: the possible contraction of intrafusal muscle fibres

In rabbits, cats and rats anaesthetized, curarized, with the skull fixed in a stereotaxic apparatus, the peripheral stump of the cervical sympathetic nerve (c.s.n.) was electrically stimulated at frequencies within the physiological range and the isometric tension was recorded at the lower jaw. In a group of experiments the afferent discharges from the jaw elevator muscle spindles was also recorded, in the mesencephalic nucleus of the fifth cranial nerve.Unilateral stimulation of the c.s.n. induced in jaw elevator muscles of rabbits an increase of tension of 5.5±0.5 g (latency: 0.5–2 s, time constant: 2.5–5 s) maintained with little or no decrement until the end of stimulation. This response proved not to be secondary to vasomotor changes since: i) approximately half of it was mediated by the fastest conducting component of the c.s.n. fibres, ii) it was not mimicked by a sudden reduction of blood supply to the muscles, iii) it was unaffected by 10 min bilateral occlusion of both the external and the internal carotid arteries. During c.s.n. stimulation the afferent discharge from spindles belonging to jaw elevator muscles exhibited an increase of firing (often preceded by a transient decrease) lasting throughout the stimulation. Also, the position sensitivity of all the spindle afferents tested was modified by the sympathetic stimulation.The results presented are interpreted to suggest that the sympathetic system may induce an intrafusal muscle fibre contraction in jaw elevator muscles. The possible functional implications are also discussed.This investigation was supported by CNR (Progetto Finalizzato: Medicina Preventiva e Riabilitativa — Sottoprogetto: Controllo del Dolore)     

Intracellular potentials from intrafusal muscle fibers evoked by stimulation of static and dynamic fusimotor axons in the cat

1. Membrane potential changes of single intrafusal muscle fibres were intracellularly recorded in spindles of cat's tenuissimus muscle on stimulating single static or dynamic fusimotor axons.

2. One third of responses elicited on stimulating static fusimotor axons were action potentials while the remainder were junction potentials. Repetitive stimulation of static axons eliciting junction potentials produced summation, facilitation and in some instances the appearance of propagated potentials.

3. All the responses evoked on stimulating dynamic fusimotor axons were junction potentials which summated but never produced propagated potentials during repetitive stimulation.

4. Most of the impalements leading to junction potentials were located in the transition zone between intra- and extra-capsular regions of spindle poles.

5. The relation between extracellular and intracellular potentials elicited by stimulation of a fusimotor axon (static or dynamic) makes it possible to assign a physiological nature to the junction potentials recorded intracellularly and to exclude effects attributable to injury.

6. A coupling between junction potential and local contraction is indirectly inferred from the frequencygrams which have been previously obtained during single shock stimulation of dynamic fusimotor axons.

     

Multifocal innervation and muscle length

Summary The dependence of the inner organisation and innervation of a skeletal muscle on its size was studied at the level of single muscle fiber architecture and motor endplate topography in muscles of different size, all of them lacking a tendinous scaffolding. The muscles evaluated in this study were: Mm. sternomastoideus, gracilis and latissimus dorsi of the rat and the M. sternocephalicus of the horse. In these muscles a subdivision into two or more innervation-compartments becomes obvious in fascicles reaching a certain length. This provides the possibility of an almost synchronous activation of the entire muscle by its nerve. At the level of single muscle fiber elements, large numbers of myo-myonal junctions were discernible in many sites. However, unequivocal multiple innervation was found, with several endplates per single muscle fiber, without the interposition of any junctional structure.Myo-myonal junctions, combined with a characteristic branching pattern of many muscle fibers, and scattered innervation sites, obviously play an important role in the architecture of fan-like muscles lacking a tendinous scaffolding.     

Correlated histological and physiological observations on a case of common sensory output and motor input of the bag1 fibre and a chain fibre in a cat tenuissimus spindle

In muscle spindles of the cat, independent control of dynamic and static components of the response of the primary sensory ending to stretch is provided by separate motor inputs to the various kinds of intrafusal muscle fibre: dynamic axons (γ or β) to the bag₁ fibres and static axons to the bag₂ (typically γ only) and chain (γ or β) fibres. Nonlinear summation of separately evoked effects during combined stimulation of dynamic and static motor axons appears to be due to mutual resetting by antidromic invasion of separate encoding sites, leading to partial occlusion of the momentarily lesser response by the greater. The encoding sites are thought to be located within the primary ending's preterminal branches which from first-order level are normally segregated to the bag₁ fibre and to the bag₂ and chain fibres. Here we describe the analysis of a special case that arose in a histophysiological study which had shown that the degree of occlusion was related to the minimum number of nodes between the putative encoding sites. Three-dimensional reconstruction of the primary ending revealed that the terminals of one chain fibre were derived entirely from the first-order branch that supplied the bag₁ fibre, including one terminal that was shared directly with the bag₁ (sensory cross-terminal). The other first-order branch supplied the bag₂ and remaining chain fibres as normal. The degree of occlusion seen during simultaneous stimulation of a dynamic β axon and a static γ axon indicated that the encoding sites were separated by both first-order branches. Schematic reconstruction of the motor innervation revealed that the static γ axon was most unlikely to have supplied the chain fibre which shared sensory terminals with the bag₁, but that these fibres also shared a motor input with histological characteristics of β type. Ramp-frequency stimulation of the dynamic β axon at constant length evoked a driving effect which persisted after fatiguing the extrafusal component and was therefore explicable on the basis of the observed pattern of motor innervation, though the identity of the axon could not be conclusively proved. Individually, instances of shared sensory terminals and motor input of bag₁ and chain fibres are rare in the cat; their combination in a single spindle with correlated physiology is described here for the first time. The observation is considered in relation to the importance of dynamic and static segregation in motor control, since it may imply that there is a lower limit to the degree of segregation that the developmental programme can provide.     

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.     

Characterstics of motor innervation of muscle spindles in the monkey

The motor nerve supplies of four whole muscle spindles and 16 half spindles (equator and one pole) from lumbrical muscles of the monkey were reconstructed by light microscopy of serial, 1-μm-thick transverse sections. The 24 poles of spindle were innervated by 37 fusimotor (γ) axons and 18 skeletofusimotor (β) axons. Sixty-seven percent of spindle poles received γ axons only, 25% were supplied by both γ and β axons or β axons only, and 8% were not innervated by motor axons. All β axons except one and 35% of the γ axons innervated one type of intrafusal fiber only. The other 65% of γ axons coinnervated two or three different types of intrafusal fiber. Gamma axons innervated the (dynamic) bag₁ intrafusal fiber together with the (static) bag₂ and/or chain fibers in 65% of the poles of spindle in which the bag₁ fiber received motor supply. The bag₂ fiber shared γ-innervation with either the bag₁ or chain fibers in nearly every spindle pole. The chain fibers were usually coinnervated with the bag₂ fiber by γ axons. Compared to spindles in the cat tenuissimus muscle, the monkey spindle received fewer γ axons and had a higher incidence of shared γ-innervation between the dynamic and static intrafusal fibers. Unlike cat tenuissimus spindles, the monkey spindles lacked γ axons selective to the bag₂ fiber. However, the β motor system within the monkey lumbrical muscle was organized in a manner similar to the cat tenuissimus muscle. The significance of these observations is discussed relative to the general motor organization and function of spindles in different muscles and species of mammals.