Termination patterns of identified group II and III afferent fibres from deep tissues in the spinal cord of the cat

In chloralose-anaesthetized cats, the impulse activity of single afferent fibres supplying receptors in the deep tissues of the hindlimb (fasciae, muscles, ligaments, joint capsules) was recorded using micropipettes filled with a solution of horseradish peroxidase. Only myelinated fibres with conduction velocities up to 40 m/s (Group III and Group II units) were studied, i.e. fast conducting afferent fibres from muscle spindles and tendon organs were excluded. The fibres were functionally characterized with the use of mechanical stimuli such as local pressure and joint movements. The results show that a relationship exists between the functional properties of a given afferent unit and the location of its terminals in the spinal cord. Since the conduction velocity and hence the diameter of the fibres was similar in all the units studied, these factors appear not to be of importance for determining the pattern of spinal termination. Out of 84 units, 42 were classified as high-threshold mechanosensitive, 26 as low-threshold mechanosensitive, and 16 as secondary endings from muscle spindles. Following physiological identification the fibres were ionophoretically injected with horseradish peroxidase and their trajectory in the white and gray matter of the spinal cord visualized histologically with diaminobenzidine. High-threshold mechanosensitive units took a lateral course in the posterior funiculus and usually did not bifurcate. They exhibited two different patterns of spinal termination, one being characterized by terminal arborizations in both lamina I and deeper laminae (mostly IV/V), the other one by an exclusive projection to lamina I. Low-threshold mechanosensitive units often showed a bifurcation in the posterior funiculus and did not have a uniform termination pattern. The main areas of termination were lamina II and laminae IV-VI. The slowly conducting secondary endings from muscle spindles projected mainly to laminae VI and VII with additional collaterals entering the ventral horn. They thus had a termination pattern similar to that reported for fast conducting afferent fibres (above 50 m/s) from muscle spindle secondary endings. With the exception of one high-threshold mechanosensitive unit none of the stained fibres possessed terminal arborization and boutons in lamina III. It is concluded that different types of Group II and III primary afferent fibres from deep tissues exhibit different patterns of spinal termination.(ABSTRACT TRUNCATED AT 400 WORDS)     

Changes in PAD patterns of group I muscle afferents after a peripheral nerve crush

In the anesthetized cat we have analyzed the changes in primary afferent depolarization (PAD) evoked in single muscle spindle and tendon organ afferents at different times after their axons were crushed in the periphery and allowed to regenerate. Medial gastrocnemius (MG) afferents were depolarized by stimulation of group I fibers in the posterior biceps and semitendinosus nerve (PBSt), as soon as 2 weeks after crushing their axons in the periphery, in some cases before they could be activated by physiological stimulation of muscle receptors. Two to twelve weeks after crushing the MG nerve, stimulation of the PBSt produced PAD in all MG fibers reconnected with presumed muscle spindles and tendon organs. The mean amplitude of the PAD elicited in afferent fibers reconnected with muscle spindles was increased relative to values obtained from Ia fibers in intact (control) preparations, but remained essentially the same in fibers reconnected with tendon organs. Quite unexpectedly, we found that, between 2 and 12 weeks after crushing the MG nerve, stimulation of the bulbar reticular formation (RF) produced PAD in most afferent fibers reconnected with muscle spindle afferents. The mean amplitude of the PAD elicited in these fibers was significantly increased relative to the PAD elicited in muscle spindle afferents from intact preparations (from 0.08–0.4 to 0.47-0.34 mV). A substantial recovery was observed between 6 months and 2.5 years after the peripheral nerve injury. Stimulation of the sural (SU) nerve produced practically no PAD in muscle spindles from intact preparations, and this remained so in those afferents reconnected with muscle spindles impaled 2–12 weeks after the nerve crush. The mean amplitude of the PAD produced in afferent fibers reconnected with tendon organs by stimulation of the PBSt nerve and of the bulbar RF remained essentially the same as the PAD elicited in intact afferents. However, SU nerve stimulation produced a larger PAD in afferents reconnected with tendon organs 2–12 weeks after the nerve crush (mean PAD changed from 0.05-0.04 to 0.32-0.17 mV). The results obtained indicate that the PAD patterns of the afferent fibers reconnected with muscle spindle and tendon organ afferents are changed after crushing their axons in the periphery: stimulation of the bulbar RF appears to produce larger PAD in fibers reconnected with muscle spindles, and stimulation of cutaneous afferents produces larger PAD in fibers reconnected with tendon organs. It is suggested that these alterations in the patterns of PAD of muscle afferents result from central changes in the balance of excitatory and inhibitory influences acting on the segmental pathways mediating the PAD. Although the functional role of these changes has not been established, they may reflect compensatory changes aimed to adjust information arising from damaged afferents.     

The afferent innervation of two infrahyoid muscles of the cat

1. The afferent innervation of the straplike muscles of the infrahyoid region were investigated in two ways. The morphology of spindles and counts of tendon organs were investigated by the gold chloride technique in ten muscles. Spindle counts were made in forty pairs of thyrohyoid and infrahyoid muscles. De-efferenting of the nerves to these muscles was done in three cats and the calibre spectra of the afferent innervation investigated. These were compared with the total counts of fibres in intact nerves.2. In the thyrohyoid, spindles are frequently absent. No tendon organs were seen. In the large infrahyoid (combined sternohyoid and sternothyroid), spindle counts varied from 0 to 20 and the mean spindle count per gram of muscle was 3.5. A maximum of five tendon organs were seen in the muscle. Both spindle and tendon organ counts are low when compared with a limb muscle of similar weight and size.3. In the infrahyoid muscle complex spindles were about equal in number to simple spindles.4. Counts of spindles in the infrahyoid muscle in families of three or more siblings suggest that some families of kittens tend to have higher spindle counts than other families.5. The afferent innervation of the two muscles varied between 21 and 42% of the total fibre population and the fibre diameter spectrum is in keeping with the low counts of encapsulated endings.     

Muscle spindle discharge in response to contraction of single motor units

1. In human subjects, microelectrode recordings were made from 25 muscle spindle afferents and two tendon organ afferents coming from muscles innervated by the peroneal nerve. 2. Stimulation at low intensity through the recording microelectrode activated efferent axons innervating motor units in close proximity to the muscle spindle or tendon organ. There was a clear alteration in the discharge of 17 afferents (15 muscle spindle, 2 tendon organ) in response to twitch contractions that involved only one, two, or three motor units. With three other afferents there was a less overt but statistically significant alteration in discharge rate by the twitch contraction of a single motor unit. 3. The sensitivity of 21 receptors (20 spindles, 1 tendon organ) to twitch contractions of anatomically close motor units was contrasted with their sensitivity to twitches of more remote motor units in the muscle. In no instance was the sensitivity to the contraction of remote motor units greater than that to the contraction of local motor units stimulated through the microelectrode; with remote stimulation many units usually had to be activated before the resulting twitch contraction altered the discharge of an afferent. 4. It is concluded that muscle spindles as well as tendon organs can play a role in monitoring the activity of motor units anatomically close to the receptor.     

Effects of temperature on the discharges of muscle spindles and tendon organs

1. In anaesthetized cats the effects of temperature on the nervous outflow from skeletal muscle via thick myelinated afferent fibres were studied. Single unit recordings were made from afferents of muscle spindles and tendon organs during slow and fast temperature changes of the medial gastrocnemius muscle which was deefferented by ventral root section and prestretched to a tension of 100 p.
2. Group I afferent units from muscle spindles were activated by warming and depressed by cooling, the effect of warming being much more pronounced than that of cooling. Afferents from secondary spindle endings with a high background discharge behaved similar to Ia fibres, whereas those with a low initial discharge rate showed an activation by cooling and a depression (mostly to cessation of firing) by warming. The discharges of group I afferents from tendon organs varied; an activation by warming was the most frequently observed reaction.
3. Some of the afferents from muscle spindles and tendon organs showed signs of a dynamic sensitivity to thermal stimulation, but in general the dynamic component in the responses to temperature changes was only small.
4. The results suggest that the afferent outflow via thick myelinated fibres from a resting, moderately prestretched muscle strongly depends on temperature. At raised intramuscular temperatures (about 42°C) the nervous outflow is characterized by an increased activity in all of the I a and many of the I b afferents, while the majority of group II spindle afferents will be depressed. In contrast, in a cold muscle (about 29°C) the nervous outflow via afferents from primary spindle endings will be reduced, while the net activity from secondary spindle endings will be increased and no marked changes are expected to occur in the discharges of I b fibres.

     

Organization of group I activated cells in the main and external cuneate nuclei of the cat: Identification of muscle receptors

Summary Extracellular recording was made from 77 primary afferent fibres, 106 cells in the external cuneate nucleus, and 60 cells in the main cuneate nucleus, all activated by slowly adapting muscle stretch receptors. The nature of the muscle receptors responsible for the activation was determined by various types of receptor stimulation.Primary group I afferents from muscle spindles and tendon organs in distal forelimb muscles showed complete overlap of conduction velocities and thresholds to electrical stimulation. Both types of group I afferents as well as group II muscle spindle afferents were shown to ascend through the dorsal funiculus to the level of the cuneate nuclei.Three groups of cells were identified in the external cuneate nucleus, activated by group I muscle spindle afferents, tendon organ afferents and group II muscle spindle afferents, respectively.Almost all group I activated cells in the main cuneate nucleus, including all 34 cells identified as cuneo-thalamic relay cells, received their afferent input from muscle spindle afferents. Three cells were activated by tendon organ afferents.     

A comparative analysis of the encapsulated end-organs of mammalian skeletal muscles and of their sensory nerve endings

The encapsulated sensory endings of mammalian skeletal muscles are all mechanoreceptors. At the most basic functional level they serve as length sensors (muscle spindle primary and secondary endings), tension sensors (tendon organs), and pressure or vibration sensors (lamellated corpuscles). At a higher functional level, the differing roles of individual muscles in, for example, postural adjustment and locomotion might be expected to be reflected in characteristic complements of the various end‐organs, their sensory endings and afferent nerve fibres. This has previously been demonstrated with regard to the number of muscle‐spindle capsules; however, information on the other types of end‐organ, as well as the complements of primary and secondary endings of the spindles themselves, is sporadic and inconclusive regarding their comparative provision in different muscles. Our general conclusion that muscle‐specific variability in the provision of encapsulated sensory endings does exist demonstrates the necessity for the acquisition of more data of this type if we are to understand the underlying adaptive relationships between motor control and the structure and function of skeletal muscle. The present quantitative and comparative analysis of encapsulated muscle afferents is based on teased, silver‐impregnated preparations. We begin with a statistical analysis of the number and distribution of muscle‐spindle afferents in hind‐limb muscles of the cat, particularly tenuissimus. We show that: (i) taking account of the necessity for at least one primary ending to be present, muscles differ significantly in the mean number of additional afferents per spindle capsule; (ii) the frequency of occurrence of spindles with different sensory complements is consistent with a stochastic, rather than deterministic, developmental process; and (iii) notwithstanding the previous finding, there is a differential distribution of spindles intramuscularly such that the more complex ones tend to be located closer to the main divisions of the nerve. Next, based on a sample of tendon organs from several hind‐foot muscles of the cat, we demonstrate the existence in at least a large proportion of tendon organs of a structural substrate to account for multiple spike‐initiation sites and pacemaker switching, namely the distribution of sensory terminals supplied by the different first‐order branches of the Ib afferent to separate, parallel, tendinous compartments of individual tendon organs. We then show that the numbers of spindles, tendon organs and paciniform corpuscles vary independently in a sample of (mainly) hind‐foot muscles of the cat. Grouping muscles by anatomical region in the cat indicated the existence of a gradual proximo‐distal decline in the overall average size of the afferent complement of muscle spindles from axial through hind limb to intrinsic foot muscles, but with considerable muscle‐specific variability. Finally, we present some comparative data on muscle‐spindle afferent complements of rat, rabbit and guinea pig, one particularly notable feature being the high incidence of multiple primary endings in the rat.     

Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study

Summary The activities of single proprioceptive fibres were recorded from the lateral peroneal nerve using transcutaneously implanted tungsten microelectrodes. Unitary discharges originating from muscle spindle primary and secondary endings and Golgi tendon organs were identified by means of various physiological tests. The sensitivity of proprioceptors to mechanical vibrations with a constant low amplitude (0.2–0.5 mm) applied at various frequencies to the tendon of the receptor-bearing muscle was studied. Muscle spindle primary endings (Ia fibres) were found to be the most sensitive to this mechanical stimulus. In some cases their discharge could be driven in a one-to-one manner up to 180 Hz. Most of them also fired harmonically with the vibration up to 80 Hz and then discharged in a subharmonic manner (1/2–1/3) with increasing vibration frequencies. Muscle spindle secondary endings (II fibres) and Golgi tendon organs (Ib fibres) were found to be either insensitive or only slightly sensitive to tendon vibration in relaxed muscles. The effects of tendon vibration on muscle spindle sensory endings response to muscle lengthening and shortening induced by imposed constant velocity or sinusoidal movements of the ankle joint were studied. Modulation of the proprioceptive discharge frequency coding the various joint movement parameters was either completely or partly masked by the receptor response to vibration, depending on the vibration frequency. Moreover, vibrations combined with sinusoidal joint movements elicited quantitatively erroneous proprioceptive messages concerning the movement parameters (amplitude, velocity). The sensitivity of the Golgi tendon organs to vibration increased greatly when the receptor-bearing muscle was tonically contracted. These data confirm that vibration is able to preferentially activate the Ia afferent channel, even when the vibration amplitude is low. They define the frequency sensitivity of the muscle spindle primary and secondary endings and the Golgi tendon organs. They also show that the physiological messages triggered by ongoing motor activities undergo a series of changes during the exposure of muscles to vibration.     

Segmental and supraspinal control of synaptic effectiveness of functionally identified muscle afferents in the cat

The present investigation documents the patterns of primary afferent depolarization (PAD) of single, functionally identified muscle afferents from the medial gastrocnemius nerve in the intact, anesthetized cat. Classification of the impaled muscle afferents as from muscle spindles or from tendon organs was made according to several criteria, which comprised measurement of conduction velocity and electrical threshold of the peripheral axons, and the maximal frequency followed by the afferent fibers during vibration, as well as the changes in discharge frequency during longitudinal stretch, the projection of the afferent fiber to the motor pool, and, in unparalyzed preparations, the changes in afferent activity during a muscle twitch. In confirmation of a previous study, we found that most muscle spindle afferents (46.1–66.6%, depending on the combination of criteria utilized for receptor classification) had a type A PAD pattern. That is, they were depolarized by stimulation of group I fibers of the posterior biceps and semitendinosus (PBSt) nerve, but not by stimulation of cutaneous nerves (sural and superficial peroneus) or the bulbar reticular formation (RF), which in many cases inhibited the PBSt-induced PAD. In addition, we found a significant fraction of muscle spindle primaries that were depolarized by stimulation of group I PBSt fibers and also by stimulation of the bulbar RF. Stimulation of cutaneous nerves produced PAD in 9.1–31.2% of these fibers (type B PAD pattern) and no PAD in 8.2–15.4% (type C PAD pattern). In contrast to muscle spindle afferents, only the 7.7–15.4% of fibers from tendon organs had a type A PAD pattern, 23–46.1% had a type B and 50–61.5% a type C PAD pattern. These observations suggest that the neuronal circuitry involved in the control of the synaptic effectiveness of muscle spindles and tendon organs is subjected to excitatory as well as to inhibitory influences from cutaneous and reticulospinal fibers. As shown in the accompanying paper, the balance between excitation and inhibition is not fixed, but can be changed by crushing the afferent axons in the peripheral nerve and allowing subsequent reconnection of these afferent fibers with muscle receptors.     

Response characteristics of muscle afferents in the domestic duck

1. Response patterns of 116 muscle stretch receptor units isolated from the sciatic nerve of the duck have been studied, and the units classified as muscle spindles and tendon organs.2. Units classified as spindles had low threshold tensions for maintained discharge. From conduction-velocity measurements, the calculated fibrediameter spectrum appears to be unimodal, ranging from 5 to 11-12 mum.3. Spindle units showed essentially ;in parallel' behaviour, though increase in initial tension often led to the appearance of ;in series' responses. Although apparent ;alpha-excitation' during maximal tetanic contractions was a common occurrence, no direct evidence of alpha-innervation of spindles was obtained.4. Evidence has been obtained for motor innervation of spindles by fibres distinct from those constituting the alpha supply to extrafusal muscle fibres. Afferent response attributable to this fusimotor innervation is influenced by initial tension and stimulus-frequency. Electrical thresholds for fusimotor responses ranged from 1.1 to 4.03 times alpha maximum.5. Tendon organ units consistently showed ;in series' response patterns during muscle contractions. They were not influenced by stimulation of the high-threshold efferent nerve supply to the muscles.6. Threshold tensions required for maintained discharge in tendon organ units from m. gastrocnemius pars lateralis were characteristically high; however, many units from m. flexor perforans et perforatus d. 3 had unexpectedly low mechanical thresholds. The calculated fibre-diameter spectrum for tendon organ units is unimodal, ranging from 4-7 to 10-11 mum. As in mammals, they contribute to the coarse-fibre component in the muscle nerve and include the fastest fibres present.     

Physiological properties of muscle spindles in dorsal neck muscles of the cat.

1. Single-fiber recording was used to examine the properties of 107 spindle endings in cat biventer cervicis (BC) and complexus (CM) muscles. Responses of receptors were examined following muscle contraction and ramp and hold stretch. Twenty-two endings in splenius (SP) were also examined, but their responses could not be quantitated because the anatomy of SP prevented the application of appropriate stretches. 2. Conduction velocitites of spindle afferents ranged from 13 to 90 m/s. Endings with primary response patterns usually had faster conduction velocities than secondary endings, but there was overlap in the conduction velocity ranges of the two subgroups. 3. Most neck spindle afferents could be classified as either primary or secondary by a constellation of physiological criteria including dynamic response pattern, dynamic index, and variability of resting discharge frequency. However, 22 of 107 endings from BC and CM had responses with characteristics intermediate between primary and secondary responses. The possible sources of these characteristics are discussed. 4. Despite the similarity in properties between spindles of different neck muscles, the length sensitivities of CM spindles were high compared to those of BC spindles. CM spindles showed length-related modulation of firing frequency over a more restricted range of initial muscle lengths than did BC spindles. 5. Eight Golgi tendon organs (GTO) were identified by their characteristics responses. Conduction velocities obtained for five GTO afferent nerves ranged from 50 to 67 m/s. Recordings were also made from receptros in deep muscles surrounding the vertebrae. These receptors had properties characteristic of muscle spindles.     

Innervation of muscle receptors in the cross-reinnervated soleus muscle of the cat

It has recently been reported (Gregory et al., J. Physiol., 331:367-383, 1982) that cutting a muscle nerve and letting it grow back into the muscle or cross-uniting the muscle with a foreign nerve results in major disruption of the normal response patterns of muscle spindles and tendon organs. Here we report observations on the structure of muscle receptors in cross-reinnervated and self-reinnervated soleus muscles in an attempt to detect abnormalities that might account for their disturbed function. Eight soleus muscles were reinnervated with the extensor digitorum longus nerve for periods up to 449 days and two were self-reinnervated. Following the physiological investigation, the muscle was fixed and stained according to the method of Barker and Ip (J. Physiol., 69:73P-74P, 1963). Spindles and tendon organs were teased from the muscle and photographed. In one cross-reinnervated muscle an attempt was made to isolate all receptors. About two-thirds of the normal number of spindles and tendon organs were found. Three categories of receptor were identified: normal, abnormal, and those having no visible nerve endings. There appeared to be little difference in degree of abnormality of receptors in self- and cross-reinnervated muscles. Of the 180 spindles, 3% were normal, 43% had no visible endings, and 54% had abnormal endings. Of 80 tendon organs, 38% were normally innervated, 33% were without visible innervation, and 29% had abnormal endings. We conclude that following long-term cross-reinnervation and self-reinnervation of soleus there is extensive disruption of the normal innervation pattern of both spindles and tendon organs which could account for their functional abnormalities.     

The responses of secondary endings of cat soleus muscle spindles to succinyl choline

This report describes the effects of succinylcholine (SCh) on the secondary endings of cat soleus muscle spindles and attempts to explain them in terms of the action of the drug on intrafusal fibres. All but 2 of 41 secondary endings studied in detail showed a significant response to a single intravenous injection of 200 g kg^-1 SCh. This consisted of a rise in the resting rate or development of a resting discharge if the spindle had previously been silent and an increase in the response to stretch. The increases in the responses to stretch were weaker than those observed for primary endings of spindles, but were much larger than those of tendon organs, which showed very little effect with this concentration of drug. The response to SCh showed two features consistent with its action being mediated via an intrafusal muscle fibre contraction rather than a direct depolarising action on the afferent nerve ending. In the presence of SCh, secondary endings were able to maintain a discharge during muscle shortening at rates, on average, more than 5 times greater than under control conditions. Secondly, the increase in spindle discharge produced by SCh showed a length dependence similar to that for fusimotor stimulation. Further support for the action of SCh being principally via an intrafusal fibre contraction was provided by the observation that its effects were abolished by the neuromuscular blocker gallamine triethiodide. The time course of recovery of SCh responses, following their blockade by gallamine, was much slower than recovery of extrafusal tension and closely paralleled that for the recovery of fusimotor responses. In three separate experiments on the medial gastrocnemius muscle the possibility that SCh may exert an excitatory action on spindle sensory endings through the liberation of potassium ions from the muscle was tested by tetanic stimulation of the muscle. This had no detectable excitatory effect. Several observations were made on the effect of SCh on responses of cutaneous receptors. SCh did not change levels of spontaneous activity or responses to mechanical stimulation of either slowly or rapidly adapting mechanoreceptors. It was argued for both tendon organs and cutaneous receptors that if SCh had a direct action on the nerve ending at the concentrations used here, some responses of these receptors to the drug might have been expected. All of the above supports the view that secondary endings of spindles are able to respond to SCh by the development of an intrafusal fibre contracture. The question of the intrafusal fibre types involved is discussed.     

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.     

Topography of muscle spindles and Golgi tendon organs in shoulder muscles of "Monodelphis domestica".

The topography of muscle spindles and Golgi tendon organs in the rotator cuff and surrounding shoulder muscles of a small laboratory marsupial (monodelphis domestica) were studied using light microscopy of serial sections. The shoulder joint of monodelphis has a large degree of freedom of movement allowing this animal to use the upper extremities for a wide range of activities like climbing and manipulating food. Thus, similar to the situation in man the shoulder joint is mainly secured by muscles. Silver stained serial paraffin sections were examined under the light microscope and the distribution of muscle spindles and Golgi tendon organs was reconstructed using three-dimensional image processing. In the two animals examined 113 and 131 muscle spindles respectively were found within the 4 rotator cuff muscles. In addition, 76 and 40 Golgi tendon organs respectively were seen at the musculo-tendinous junctions of these muscles preferentially close to the insertion at the humerus head. Also the surrounding shoulder muscles contain both muscle spindles and Golgi tendon organs in large numbers, but the ratio of Golgi tendon organs per muscle spindle appears to be lower. Number and localization of muscle spindles and Golgi tendon organs suggest, that these receptors are important for both reflex control of shoulder muscle tone as well as monitoring of static position and movement in the shoulder joint.     

Joint receptors modulate short and long latency muscle responses in the awake cat

Summary Nerve cuff electrodes were chronically implanted around multiple peripheral nerves in adult cats, including the medial and posterior articular nerves (MAN and PAN) to the knee while EMG electrodes were implanted into seven hindlimb muscles. Randomized load perturbations producing mid-range knee flexions at varying angular velocities were subsequently applied to awake cats. Recordings were initially obtained with knee joint innervation intact and then after local anaesthetic or saline control solution was injected into the knee. Averaged neurogram and EMG responses to the imposed movements were utilized to assess the contribution of joint mechanoreceptor activity to the evoked muscle responses. Additionally, spike-triggered averaging techniques and peri-stimulus time histograms of single joint afferent units isolated from the articular nerve cuffs were utilized to characterize unitary joint receptor responses. The averaged whole nerve response to knee joint perturbations on each of the cuffed articular nerves revealed phasic increases in activity relative to constant background levels. The earliest phasic responses on the articular nerves were initiated at latencies that were too short to be voluntary, occurring in the short latency (reflex) period. Detectable joint receptors were not recruited until after the earliest excitatory responses of agonist/antagonist muscle pairs acting across the knee had occurred, presumably resulting in mechanical loading of the knee joint capsule and subsequent activation of articular mechanoreceptors. Introduction of local anaesthetic into the knee was accompanied by marked diminution in joint afferent activity. Perturbation-evoked muscle responses were characterized by increased activity above background levels in all seven muscles studied, including antagonist muscle pairs. Local anaesthetic-mediated loss of knee joint mechanoreceptor input altered the latency, amplitude and duration of EMG responses in each muscle. The effect of joint anaesthesia in the short latency period was a generalized decrease in all muscle responses relative to normal and saline controls. The loss of afferent input after joint anaesthesia was also associated with altered muscle responses during the long latency period, when both reflex and voluntary mechanisms could potentially contribute to the generation of EMG activity. Interestingly, long latency activity after joint anaesthesia was characterized by unbalancing in the EMG responses of some antagonist muscle pairs. This alteration of normal antagonist pair co-contraction patterns served to increase the magnitude of the imposed perturbations, rather than to bring the movements under control. Analysis of single joint afferents isolated from whole joint nerve recordings demonstrated that some joint afferent units were tonically active at quiescent, mid-range knee positions. Additionally, isolated afferents demonstrated different time courses of response to imposed perturbations. Some afferents responded with decreased or absent firing activity (TONIC units) while other joint afferents responded with phasic bursts of activity which were greatly increased above their relatively low levels of tonic, background activity (TONIC-PHASIC units). In addition to TONIC and TONIC-PHASIC units, other joint afferents were identified which were only active after imposition of passive knee movements (PHASIC units). In conclusion, data obtained from whole joint nerve recordings as well as data from isolated, single joint afferents demonstrate that joint receptors can modulate short and long latency muscle responses to passively-imposed knee movements in the awake cat.Supported by Medical Research Council of Canada (MRC) grant MT5218. KWM is an MRC fellow     

A comparison of the spindles in two different muscles of the frog

1. The responses of spindles in the iliofibularis muscle of frogs to stretch during either small motor nerve fibre stimulation or the application of suxamethonium were compared.2. All spindles which were excited by small motor nerve fibre stimulation were also excited by suxamethonium, and their responses to these two methods of excitation were very similar. The drug dose was usually 5-10 mug/ml. but smaller and larger doses were effective. Large doses (> 100 mug/ml.) could sometimes lead to a reversible partial block of the spindle response to stretch.3. Suxamethonium also caused a prolonged contraction in extrafusal slow muscle fibres. This contraction was not responsible for the effect on the spindle, because the time course of its action on the muscle tension and on the spindle afferent was different.4. It was concluded that suxamethonium stimulated prolonged contraction in the small intrafusal muscle fibres, which are known to be innervated by the small motor nerve fibres.5. Only about half of the spindles in the iliofibularis muscle were excited by suxamethonium.6. In the sartorius muscle which has no slow extrafusal muscle fibres, no spindles were found to be excited by suxamethonium in the way characteristic of that due to small intrafusal muscle fibre contraction.7. It is concluded that, in frog muscles which have no slow extrafusal fibres, the muscle spindles do not have small intrafusal muscle fibres of the kind found in the iliofibularis muscle.     

The responses of frog muscle spindles and fast and slow muscle fibres to a variety of mechanical inputs

1. The tension in the iliofibularis muscle of frogs was recorded while the muscle was stretched or released. At the same time recordings were made from single spindle afferents in dorsal root filaments. Either large or small motor nerve fibres were stimulated in split ventral root filaments.2. While small motor nerve fibres were stimulated the discharge from muscle spindle afferents was greatly increased by stretching, and greatly reduced by shortening the muscle. This sensitivity to movement was shown even if the movements were small, so that a stretch of 0.2% of the muscle length was sufficient to cause a pronounced increase in the afferent discharge.3. In contrast, during stimulation of the large motor nerve fibres the spindle was much less sensitive to movements with the result that even stretches or releases of the muscle by 1 mm did not cause very large changes in the discharge frequency.4. The tension in slow extrafusal muscle fibres in many ways mirrored the spindle discharge during the stimulation of small motor nerve fibres, for the tension was greatly increased by stretching, even through small distances, and greatly reduced by releasing the muscle. The tension in fast extrafusal muscle fibres was much less changed by such movements, and thus was rather like the spindle discharge during stimulation of large motor nerve fibres.5. As the extrafusal muscle fibres do not directly pull on and excite the spindle afferents, the simplest explanation for the similarities between the muscle tension and the spindle discharge is that the mechanical properties of the intrafusal muscle fibres innervated by the large motor nerve fibres are like those of fast extrafusal muscle fibres, and that the mechanical properties of the small intrafusal fibres are similar to those of slow extrafusal muscle fibres.6. It is shown that the cross-bridge sliding filament mechanism of muscle contraction provides a ready explanation for the differences found between fast and slow muscles, and it is concluded that a most important functional difference between the two sorts of intrafusal muscle fibres is the speed of their contractions, for it is this which determines their contrasting actions on the spindle.7. It was also found that low rates (< 4/sec) of small motor nerve fibre stimulation were often very effective in exciting the spindles. These rates produced rather little extrafusal tension.     

A functional analysis of the components of the mesencephalic nucleus of the fifth nerve in the cat

1. The mesencephalic nucleus of the trigeminal nerve has been studied using extracellular micro-electrode recording and the constituent cell types identified.2. Two types of unit were found, namely, muscle spindle first order afferents of ipsilateral jaw-closing muscles and mechanoreceptor afferents of ipsilateral maxillary and mandibular teeth.3. No evidence was found for representation of extra-ocular muscle stretch receptors, of temporo-mandibular joint receptors or of tendon organs of jaw muscles.4. Spindle units of each of the jaw-closing muscles were recorded in all parts of the nucleus and there was no evidence of their segregation according to muscle of origin.5. Attempts to classify spindle units by their dynamic response to ramp stretches, their following of high frequency vibration and their interspike interval variability at constant length gave no indication of two populations when fusimotor activity was suppressed.6. Following the injection of suxamethonium, however, units fell into two groups according to their dynamic index. Their behaviour resembled that described for primary and secondary spindle afferents. In data pooled from all of the jaw-closing muscles there were approximately equal numbers of units in each group.     

PAD patterns of physiologically identified afferent fibres from the medial gastrocnemius muscle

Summary Intracellular recordings were made in the barbiturate-anesthetized cat from single afferent fibres left in continuity with the medial gastrocnemius muscle to document the transmembrane potential changes produced in functionally identified fibres by stimulation of sensory nerves and of the contralateral red nucleus (RN). Fifty five fibres from muscle spindles had conduction velocities above 70 m/s and were considered as from group Ia. Stimulation of group I afferent fibres of the posterior biceps and semitendinosus nerve (PBSt) produced primary afferent depolarization (PAD) in 30 (54%) Ia fibres. Stimulation of the sural (SU) nerve produced no transmembrane potential changes in 39 (71%) group Ia fibres and dorsal root reflex-like activity (DRRs) in 16 (29%) fibres. In 17 out of 28 group Ia fibres (60.7%) SU conditioning inhibited the PAD generated by stimulation of the PBSt nerve. Facilitation of the PBSt-induced PAD by SU conditioning was not seen. Repetitive stimulation of the RN had mixed effects: it produced PAD in 1 out of 8 fibres and inhibited the PAD induced by PBSt stimulation in 2 other fibres. Nine fibres connected to muscle spindles had conduction velocities below 70 m/s and were considered to be group II afferents. No PAD was produced in these fibres by SU stimulation but DRRs were generated in 5 of them. In 23 out of 31 fibres identified as from tendon organs group I PBSt volleys produced PAD. However, stimulation of the SU nerve produced PAD only in 3 out of 34 fibres, no transmembrane potential changes in 30 fibres and DRRs in 1 fibre. The effects of SU conditioning on the PAD produced by PBSt stimulation were tested in 19 Ib fibres and were inhibitory in 12 of them. In 9 of these fibres SU alone produced no transmembrane potential changes. Repetitive stimulation of the RN produced PAD in 3 out of 9 Ib fibres. SU conditioning inhibited the RN-induced PAD. The present findings support the existence of an alternative inhibitory pathway from cutaneous to Ib fibres, in addition to the well known excitatory pathway producing PAD. Possible functional implications of inhibitory actions of cutaneous fibres with the pathways mediating the PAD of group Ia and Ib fibres are discussed.