The transduction properties of intercostal muscle mechanoreceptors

Background  

Intercostal muscles are richly innervated by mechanoreceptors. In vivo studies of cat intercostal muscle have shown that there are 3 populations of intercostal muscle mechanoreceptors: primary muscle spindles (1°), secondary muscle spindles (2°) and Golgi tendon organs (GTO). The purpose of this study was to determine the mechanical transduction properties of intercostal muscle mechanoreceptors in response to controlled length and velocity displacements of the intercostal space. Mechanoreceptors, recorded from dorsal root fibers, were localized within an isolated intercostal muscle space (ICS). Changes in ICS displacement and the velocity of ICS displacement were independently controlled with an electromagnetic motor. ICS velocity (0.5 – 100 μm/msec to a displacement of 2,000 μm) and displacement (50–2,000 μm at a constant velocity of 10 μm/msec) parameters encompassed the full range of rib motion.     

Postinspiratory activity of the parasternal and external intercostal muscles in awake canines.

Previous studies have shown in awake dogs that activity in the crural diaphragm, but not in the costal diaphragm, usually persists after the end of inspiratory airflow. It has been suggested that this difference in postinspiratory activity results from greater muscle spindle content in the crural diaphragm. To evaluate the relationship between muscle spindles and postinspiratory activity, we have studied the pattern of activation of the parasternal and external intercostal muscles in the second to fourth interspaces in eight chronically implanted animals. Recordings were made on 2 or 3 successive days with the animals breathing quietly in the lateral decubitus position. The two muscles discharged in phase with inspiration, but parasternal intercostal activity usually terminated with the cessation of inspiratory flow, whereas external intercostal activity persisted for 24.7 +/- 12.3% of inspiratory time (P < 0.05). Forelimb elevation in six animals did not affect postinspiratory activity in the parasternal but prolonged postinspiratory activity in the external intercostal to 45.4 +/- 16.3% of inspiratory time (P < 0.05); in two animals, activity was still present at the onset of the next inspiratory burst. These observations support the concept that muscle spindles are an important determinant of postinspiratory activity. The absence of such activity in the parasternal intercostals and costal diaphragm also suggests that the mechanical impact of postinspiratory activity on the respiratory system is smaller than conventionally thought.     

One-bag-fiber muscle spindles in tenuissimus muscles of the cat

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.     

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.     

Autonomic innervation of receptors and muscle fibres in cat skeletal muscle

Cat hindlimb muscles, deprived of their somatic innervation, have been examined with fluorescence and electron microscopy and in teased, silver preparations; normal diaphragm muscles have been examined with electron microscopy only. An autonomic innervation was found to be supplied to both intra- and extrafusal muscle fibres. It is not present in all muscle spindles and is not supplied at all to tendon organs. Fluorescence microscopy revealed a noradrenergic innervation distributed to extrafusal muscle fibres and some spindles. On the basis of the vesicle content of varicosities the extrafusal innervation was identified as noradrenergic (32 axons traced), and the spindle innervation as involving noradrenergic, cholinergic and non-adrenergic axons (14 traced). Some of the noradrenergic axons that innervate spindles and extrafusal muscle fibres are branches of axons that also innervate blood vessels. We cannot say whether there are any noradrenergic axons that are exclusively distributed to intra- or extrafusal muscle fibres. The varicosities themselves may be in neuroeffective association with striated muscle fibres only, or with both striated fibres and the smooth muscle cells in the walls of blood vessels. The functional implications of this direct autonomic innervation of muscle spindles and skeletal muscle fibres are discussed and past work on the subject is evaluated.     

Oro-facial muscles: internal structure,function and ageing

Structure and function are reviewed in the masticatory muscles and in the muscles of the lower face and tongue. The enormous strength of jaw closure is in large part due to the pinnated arrangement of the muscle fibres in the masseter. This muscle, like other masticatory muscles, is unusual in that the cell bodies of the muscle spindle afferents lie in the brain stem rather than in an external ganglion; spindles are absent in the lower facial muscles. Although few data are available, the numbers of motor units in the masticatory muscles, and probably in the lower facial muscles also, appear to he much greater than in limb muscles. The motor units in the facial and tongue muscles are largely composed of histochemical type II (‘fast-twitch’) fibres, but in the masticatory muscles there are substantial numbers of fibres intermediate between type I (‘slow twitch’) and type II, and fibre type grouping is present. In comparison with limb muscles, there is little information on ageing changes in oro-facial muscles. The masticatory muscles do, however, show some atrophy and loss of X-ray density, while motor unit twitches are prolonged. Strength is reduced in the tongue and masticatory muscles. It is known that limb muscle properties are largely governed by their innervation, both through the pattern and amount of impulse activity, and the delivery of trophic messengers; the situation for oro-facial muscles is unclear. The structural and functional differences between the two types of muscle indicate the need for conducting ageing studies on the oro-facial muscles, rather than relying on extrapolations from limb muscles.     

Role of nerve and muscle factors in the development of rat muscle spindles

The soleus muscles of fetal rats were examined by electron microscopy to determine whether the early differentiation of muscle spindles is dependent upon sensory innervation, motor innervation, or both. Simple unencapsulated afferent-muscle contacts were observed on the primary myotubes at 17 and 18 days of gestation. Spindles, encapsulations of muscle fibers innervated by afferents, could be recognized early on day 18 of gestation. The full complement of spindles in the soleus muscle was present at day 19, in the region of the neuromuscular hilum. More afferents innervated spindles at days 18 and 19 of gestation than at subsequent developmental stages, or in adult rats; hence, competition for available myotubes may exist among afferents early in development. Some of the myotubes that gave rise to the first intrafusal (bag2) fiber had been innervated by skeletomotor (alpha) axons prior to their incorporation into spindles. However, encapsulated intrafusal fibers received no motor innervation until fusimotor (gamma) axons innervated spindles 3 days after the arrival of afferents and formation of spindles, at day 20. The second (bag1) intrafusal fiber was already formed when gamma axons arrived. Thus, the assembly of bag1 and bag2 intrafusal fibers occurs in the presence of sensory but not gamma motor innervation. However, transient innervation of future bag2 fibers by alpha axons suggests that both sensory and alpha motor neurons may influence the initial stages of bag2 fiber assembly. The confinement of nascent spindles to a localized region of the developing muscle and the limited number of spindles in developing muscles in spite of an abundance of afferents raise the possibility that afferents interact with a special population of undifferentiated myotubes to form intrafusal fibers.     

Formation of muscle spindles in regenerated avian muscle grafts

Summary Pigeon muscles lacking muscle spindles were grafted into sites which normally have a muscle containing spindles. The reciprocal transplantations were also made. After two to eight months, the graft of the donor muscle without spindles had regenerated into a muscle containing muscle spindles. The reciprocal grafts, muscles containing spindles transplanted to a site lacking spindle innervation, had neither muscle spindles nor remnants of the spindles. These experiments demonstrate that 1) the innervation is required for formation of the spindle; 2) the original spindles do not survive transplantation; and 3) parts of the original spindle are not required for spindle regeneration.This work was supported in part by NSF grants PCM 77-15960 and PCM 79-16540     

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.     

Fusimotor innervation in the cat

The motor innervation of cat spindles was examined in hindlimb muscles using a variety of techniques employed in light and electron microscopy. Observations were made on teased, silver preparations of 267 spindles sampled from the peroneal, flexor hallucis longus, and soleus muscles, hereafter referred to as the PER/FHL/SOL series. The γ innervation. Trail endings are almost invariably present, and innervate both bag and chain muscle fibres. Trail fibres accounted for 64.6 to 74.8% of the total fusimotor supply to samples of spindle poles in the PER/FHL/SOL series, the mean number of fibres per pole varying from 2.7 to 5.0 in the different muscles, and the mean number of ramifications (areas of synaptic contact) per fibre being 3.7. By contrast, the p?innervation of a spindle pole generally consists of a single fibre supplying only one plate. In the above samples p(2) fibres accounted for 4.1 to 28.0% of the total fusimotor supply, and the mean number of fibres per pole varied from 0.3 to 1.2 in the different muscles. Ninety per cent of p(2) plates innervate bag fibres. The α innervation. The structure of p?plates as seen in both light and electron microscopy compares very closely with that of extrafusal plates. After nerve section p?plates degenerate at the same time as extrafusal plates, being the first of the three types of fusimotor ending to disappear. The frequency of the p?innervation is similar to that of the p?innervation. In the same samples of PER/FHL/SOL spindle poles as above p? fibres accounted for 6.0 to 28.8% of the total fusimotor supply, the mean number of fibres per pole varying from 0.25 to 2.1 in the different muscles. The majority of p? fibres enter a pole to terminate in one plate only. Seventy-five per cent of the plates innervate bag fibres. The three types of fusimotor ending are thus not selectively distributed to the two types of intrafusal muscle fibre. All three types of fusimotor fibre may branch within the spindle so as to innervate both bag and chain fibres. Bag fibres receive both types of plate ending as well as trail endings. Most chain fibres receive trail endings only; the rest receive either a p?or a p?plate innervation in addition, 25% of the p?and 10% of the p?innervation being distributed to chain fibres. The significance of this nonselective innervation is interpreted as indicating that the type of contraction elicited by stimulating a fusimotor fibre depends upon the type of ending initiating it rather than upon the type of muscle fibre executing it. Reasons are given for concluding that the dynamic response is controlled via the p?and p?plates, and that the static response is controlled by the trail endings. The participation of the α fibres in mammalian fusimotor innervation, previously regarded as a vestigial feature, proved to be widespread in the muscles studied and more prevalent in fast muscles (FHL, peroneus digiti quinti) than slow (soleus). A low frequency of p?innervation is offset by a high frequency of p?(as in peroneus longus), and vice versa (as in FHL). It is unlikely that collaterals from slow α fibres innervating type B muscle fibres are wholly responsible for the high frequency of the p?innervation in FHL, and it is suggested that collaterals may also be derived from fast α fibres innervating type C muscle fibres. The possibility of there being some motor fibres of α conduction velocity and with an exclusively fusimotor distribution is also taken into account.     

The pregenital abdominal musculature in phasmids and its implications for the basal phylogeny of Phasmatodea (Insecta: Polyneoptera)

Recently several conflicting hypotheses concerning the basal phylogenetic relationships within the Phasmatodea (stick and leaf insects) have emerged. In previous studies, musculature of the abdomen proved to be quite informative for identifying basal taxa among Phasmatodea and led to conclusions regarding the basal splitting events within the group. However, this character complex was not studied thoroughly for a representative number of species, and usually muscle innervation was omitted. In the present study the musculature and nerve topography of mid-abdominal segments in both sexes of seven phasmid species are described and compared in detail for the first time including all putative basal taxa, e.g. members of Timema, Agathemera, Phylliinae, Aschiphasmatinae and Heteropteryginae. The ground pattern of the muscle and nerve arrangement of mid-abdominal segments, i.e. of those not modified due to association with the thorax or genitalia, is reconstructed. In Timema, the inner ventral longitudinal muscles are present, whereas they are lost in all remaining Phasmatodea (Euphasmatodea). The ventral longitudinal muscles in the abdomen of Agathemera, which span the whole length of each segment, do not represent the plesiomorphic condition as previously assumed, but might be a result of secondary elongation of the external ventral longitudinal muscles. Sexual dimorphism, common within the Phasmatodea, also applies to the muscle arrangement in the abdomen of some species. Only in the females of Haaniella dehaanii (Heteropteryginae) and Phyllium celebicum (Phylliinae) the ventral external longitudinal muscles are elongated and span the length of the whole segment, possibly as a result of convergent evolution.     

Muscle spindle formation and differentiation in regenerating rat muscle grafts

Muscle spindle development and function are dependent upon sensory innervation. During muscle regeneration, both neural and muscular components of spindles degenerate and it is not known whether reinnervation of a regenerating muscle results in reestablishment of proper neuromuscular relationships within spindles or whether sensory neurons may exert an influence upon differentiation of these spindles. Muscle spindle regeneration was studied in bupivacaine-treated grafts of rat extensor digitorum longus (EDL) muscles. Three types of EDL graft were performed in order to manipulate the extent to which regenerating spindles might be reinnervated: (1) grafts reinnervated following severance of their nerve supply (standard grafts); (2) grafts in which intact nerve sheaths appear to facilitate reinnervation (nerveintact grafts); and (3) grafts in which reinnervation was prevented (nonreinnervated grafts). Complete degeneration of muscle fibers occurred in all grafts prior to regeneration. Initial formation of spindles in regenerating EDL grafts is independent of innervation; intrafusal muscle fibers degenerate and regenerate within spindle capsules that remain intact and viable. The extent of spindle differentiation was evaluated in each type of graft using criteria that included nucleation and ATPase activity, both of which have been shown to be regulated by sensory innervation, as well as the number of muscle fibers/spindle and morphology of spindle capsules.While most spindles contained normal numbers of muscle fibers, most of these fibers were morphologically and histochemically abnormal. Alterations of ATPase activity occurred in all spindles, but were least severe in nerve-intact grafts. While fully differentiated nuclear bag and chain fibers were not observed in regenerated spindles, large, vesicular nuclei, similar to those of normal intrafusal fibers, were present in a small number of spindles in nerve-intact grafts. Sensory nerve terminations were observed only in those spindles that also contained the distinctive nuclei. This study suggests that a specific neurotrophic influence is necessary for regeneration of normal intrafusal muscle fibers and that this influence corresponds to the properly timed sensory neuron-muscle interaction which directs muscle spindle embryogenesis. However, the infrequent occurrence of characteristics unique to intrafusal muscle fibers indicates that reinnervation of regenerating muscle grafts by sensory neurons is inadequate and/or faulty.     

The effect of neonatal deafferentation or defferentation on myosin heavy chain expression in intrafusal muscle fibers of the rat

Muscle spindles were either deafferented or deefferented by selectively severing the sensory or motor nerve supply to neonatal soleus muscles of rats at a time when spindles are formed but when intrafusal muscle fibers are structurally and immunocytochemically immature. Experimental muscles were excised two months after nerve section. Control and experimental spindles were examined using monoclonal antibodies specific for myosin heavy chains of slow-tonic (ALD58) and fast-twitch (MF30) chicken muscles. Only intrafusal fibers bound these antibodies in intact soleus muscles. The deefferented spindles exhibited a pattern of ALD58 and MF30 binding similar to that of normal adult intrafusal fibers, whereas deafferented intrafusal fibers were unreactive with the two antibodies. Thus intact sensory innervation is essential for myosin heavy chain expression in intrafusal muscle fibers during postnatal development of rat spindles.     

Distribution of sensory receptors in the flexor carpi radialis muscle of the cat

The structures and distribution of encapsulated muscle receptors were examined in serial transverse sections of flexor carpi radialis in the adult cat. Four types of receptors (muscle spindles, Golgi tendon organs, paciniform, and Pacinian corpuscles) were identified. Their structures resembled those encountered in other limb muscles. Pacinian corpuscles were rare and occurred only in the external fascial coat of the muscle near its origin. The other three receptor types were distributed in an uneven but consistent pattern throughout the muscle. As noted previously (Gonyea and Ericson, '77), spindles were largely confined to a deep muscle region comprising less than 20% of the muscle volume, located directly between the long tendon of origin and the tendon of insertion. This region contains the largest proportion of type SO muscle fibers (Gonyea and Ericson, '77). Tendon organs and paciniform corpuscles were concentrated along the tendons that lined the spindle-rich muscle region. This region appeared to be composed of extrafusal fibers that were shorter and of more oblique pinnation than those in other regions. The localization of muscle receptors to the "oxidative" core of the muscle in its direct line of pull may have functional implications for afferent input to the spinal cord which are discussed. In addition, the possibility is raised that there are more paciniform corpuscles in flexor carpi radialis (and possibly other muscles) than previously thought.     

Coccygeus and levator ani muscles in the rabbit: morphology and proprioceptive innervation

The Authors have studied the morphological features and the proprioceptive nervous component in the coccygeus and levator ani muscles of the rabbit, using Ruffini's and Barker-Ip's impregnations. The coccygeus muscle originates from ischiatic spine and inserts on the last three sacral vertebrae and on the first four or five caudal vertebrae. The levator ani muscle originates from the ischiatic spine and the coccygeus muscle aponeurosis and inserts directly on the caudal vertebrae 3-5 or 4-6. The proprioceptive innervation in both muscles is constituted by muscle spindles and Golgi tendon organs with a typical structure. Muscle spindles are more numerous than Golgi tendon organs and the spindle density is higher in the levator ani muscle.     

Neural organization of spindles in three hindlimb muscles of the rat.

The neuroanatomical organization of the dynamic (bag1) and static (bag2 and chain) intrafusal systems was compared by light and electron microscopy of serial sections among 71 poles of muscle spindle in soleus (SOL), extensor digitorum longus (EDL), and lumbrical (LUM) muscles in the rat. Eighty-four percent of 195 fusimotor (gamma) axons to the spindles innervated either the dynamic bag1 fiber or the static bag2 and/or chain fibers. Sixteen percent of the gamma axons coinnervated the dynamic and static intrafusal fibers. Some of these nonselective axons were branches of effernts that also gave rise to axons selective to either the dynamic or static types of intrafusal fibers in one or more spindles. Thus activation of individual stem gamma efferents might not have a purely dynamic or purely static effect on the integrated afferent outflow from spindles of a hindlimb muscles in the rat. In addition, primary afferents in all muscles had terminations that cross-innervated the dynamic bag1 and static bag1 and/or chain intrafusal fibers in individual spindles, an arrangement that may enhance the mixed dynamic/static behavior of afferents when different intrafusal fibers are activated concurrent. Spindles of the slow SOL and fast EDL muscles had similar features, whereas differences were observed in the organization of the proximal (SOL and EDL) and distal (LUM) muscles. Spindles in LUM muscles had fewer static intrafusal fibers, a higher ratio of dynamic to static gamma axons, and a higher incidence of skeletofusimotor (beta) innervation to intrafusal fibers than spindles in the SOL or EDL muscles. Thus, the relative contribution of dynamic and static systems to muscle afferent outflow may differ among spindles located in different segments of the rat hindlimb. However, the dynamic and static intrafusal systems of spindle were less sharply demarcated in each of the three hindlimb rat muscles than in the cat tenuissimus muscle.     

The effect of neonatal deafferentation or deefferentation on myosin heavy chain expression in intrafusal muscle fibers of the rat

Summary Muscle spindles were either deafferented or deefferented by selectively severing the sensory or motor nerve supply to neonatal soleus muscles of rats at a time when spindles are formed but when intrafusal muscle fibers are structurally and immunocytochemically immature. Experimental muscles wereexcised two months after nerve section. Control and experimental spindles were examined using monoclonal antibodies specific for myosin heavy chains of slow-tonic (ALD58) and fast-twitch (MF30) chicken muscles. Only intrafusal fibers bound these antibodies in intact soleus muscles. The deefferented spindles exhibited a pattern of ALD58 and MF30 binding similar to that of normal adult intrafusal fibers, whereas deafferented intrafusal fibers were unreactive with the two antibodies. Thus intact sensory innervation is essential for myosin heavy chain expression in intrafusal muscle fibers during postnatal development of rat spindles.     

Structure of the neuromuscular spindles in the tongue of human fetuses

The dynamics in development of some components--of the neuromuscular spindles in the human fetus and newborn tongues have been studied by means of certain general and neurohistological methods with elements of morphometry. During the whole prenatal period of the human life, there is a certain synchronism in the development of the lingual proper muscles and the neuro-muscular spindles. Certain integration in the development of the neuro-muscular spindles is observed in 4-6-month-old fetuses; in 8-9-month-old fetuses and in newborns it is substituted for heterochronicity. By the time of birth, the muscle spindle contractile elements are supplied with a more differentiated efferent innervation. The latter actively effects the morphological state of the intrafusal muscle fibers and forms a base for functional activity of the tongue.