Extraocular Muscle Spindles Research Articles

Peripheral Muscle Targets and Central Projections of the Mesencephalic Trigeminal Nucleus in Macaque Monkeys

The mesencephalic trigeminal nucleus (MesV) contains the somata of primary afferent neurons that innervate muscle spindles in masticatory muscles and mechanoreceptors in the periodontal ligaments. There are conflicting reports about additional peripheral targets of MesV, such as the extraocular muscles, as well as about its central targets. In addition, only limited primate data are available. Consequently, we examined MesV projections in macaque monkeys. The retrograde tracer wheat germ agglutinin-conjugated horseradish peroxidase (WGA-HRP) was injected into masticatory or extraocular muscles to define the peripheral targets of the primate MesV. Numerous labeled neurons were found in ipsilateral MesV after masticatory muscle injections. The scattered distribution of labeled cells, and their presence among clusters of unlabeled cells, suggests the muscle representations overlap. Just a few MesV neurons were labeled after extraocular muscle injections. This correlates with the small number of muscle spindles present in macaque extraocular muscles, suggesting MesV cells supplying extraocular muscle spindles may contribute a minor component to oculomotor proprioception. To examine the central connections of MesV, biotinylated dextran amine (BDA) was injected into the spinal trigeminal nucleus (Vs). The presence of retrogradely labeled MesV cells indicated a projection to Vs from MesV. These injections also anterogradely labeled terminals that lay in close association with MesV cells, suggesting an ascending projection from Vs to MesV. Finally, a small number of MesV neurons were labeled after WGA-HRP injections into the upper cervical spinal cord. This pattern of central connections indicates MesV and Vs information is combined to guide mastication.

Histochemical and immunohistochemical study on muscle fibers in human extraocular muscle spindles

Human extraocular muscles are unique in several ways including their endowment with proprioceptive organs. Aim of this study was to establish a classification of intrafusal muscle fibers of human extraocular muscles based on their histochemical and immunohistochemical properties and to determine their relationship to extrafusal extraocular muscle fiber types in this respect. Using light microscopy, intrafusal muscle fibers were followed on consecutive cross-sections and classified according to the localization of their myonuclei and to their enzyme- and myosin-immunohistochemical characteristics. Sixteen muscle spindles in human extraocular muscles counted as ‘true’ spindles revealed 27% nuclear chain fibers [40.1 μm ± 10.4; perimeter ± SD] and 73% anomalous fibers [44.1 μm ± 12]. Seven ‘false’ muscle spindles showed only anomalous fibers [43.8 μm ± 11.1] and entirely lacked nuclear chain fibers. Six fiber types were distinguished according to their histochemical and myosin heavy chain immunohistochemical properties. Fiber type 1 [46.3 μm ± 13.3] was made up of fast-twitch myosin heavy chain isoform. Fiber type 2 [39.5 μm ± 10] additionally expressed a developmental myosin heavy chain isoform. Fiber type 3 [42.8 μm ± 10.4] consisted of pure slow-twitch positive muscle fibers. Slow-twitch MHC and fast-twitch myosin heavy chain isoform were found in fiber type 4 [43.3 μm ± 9]. Fiber types 5 and 6 showed different myosin heavy chain patterns than fiber types 1–4. The vast majority of nuclear chain fibers displayed fiber type 2 features, but 12% of nuclear chain fibers were found to be of fiber type 1. Among anomalous fibers in true spindles the frequency of fiber type 1 was much higher than in false spindles. On the other hand, fiber type 4 was found more often in false than in true spindles. With regard to their histochemical and immunohistochemical properties intrafusal muscle fibers in human extraocular muscles differ both from intrafusal muscle fibers in other skeletal muscles and from extrafusal muscle fibers in extraocular eye muscles. These conspicuous differences to skeletal muscle spindles relate to their morphology and myosin heavy chain characteristics. In particular, the occurrence of anomalous fibers might reflect dynamic neuronal processes and might be necessary for modulating and adapting processes in advancing age, as well as maintaining proprioceptive input during the whole life.

Proprioception and Palisade Endings in Extraocular Eye Muscles

Palisade endings occur only in extraocular muscles, and their function is unknown. They form a cuff of nerve terminals around the tips of muscle fibers. We describe here the advantages of using antibodies to a synaptosomal-associated protein (SNAP-25) to study properties of palisade endings in man, monkey, and rat. The stain can be combined readily with other immunofluorescence procedures, and results suggest that the synapses of palisade endings do not bind alpha-bungarotoxin (i.e., are not motor), nor do they contain substance P. These double-labeling data support the hypothesis that palisade endings are non-nociceptive sensory receptors, and could serve a proprioceptive function. With SNAP-25 immunolabeling, palisade endings were identified in the rat for the first time. Thus, palisade endings appear to be present in all vertebrate extraocular muscles studied to date. Their apparent universality, which contrasts with the more variable manifestation of extraocular muscle spindles and Golgi tendon organs, would be expected if proprioceptive feedback is necessary to the function of the ocular motor system, and if palisade endings are the critical proprioceptive structure.

Morphological variability and specializations in bovine extraocular muscle spindles

Bovine extraocular muscles were examined to determine whether the structure of their muscle spindles was notably different from those commonly encountered in mammalian limb muscles. Extraocular muscle spindles on the whole were shorter, and intrafusal fiber counts/spindle were more variable than in somatic muscles. No pronounced nuclear bags were seen in intrafusal fibers. Based on cross-sectional areas, intrafusal fibers in extraocular muscles could be loosely categorized as small or large types. Small fibers expressed more neonatal/fast myosin heavy chain and less embryonic myosin heavy chain than large fibers. When incubated for myosin ATPase, about 70% of the large fibers and 15% of the small fibers in spindles presented profiles that were characteristic of type I extrafusal fibers, and not of nuclear bag or nuclear chain fibers. The ratio of number of small intrafusal fibers to number of large intrafusal fibers in extraocular spindles was on average greater than the ratio of nuclear chain fibers to nuclear bag fibers that is typical for limb spindles of rodents and cats. Structural modifications at muscle spindle sensory regions, extrafusal-like fibers and intrafusal-like fibers with few equatorial nuclei and many myofibrils, may produce distinct afferent signals that are appropriate for sensorimotor integration in the specialized extraocular muscles.

Propriozeption aus äußeren Augenmuskeln des Menschen: Zur Morphologie ihrer Muskelspindeln

Increasing importance is attributed to the proprioceptive innervation of extraocular muscles for the development of binocular vision. In the literature, data on proprioceptors in human extraocular muscles are rare and inconsistent. Therefore a detailed morphological analysis of spindles in human extraocular muscles appeared indicated. Complete serial sections of all extraocular muscles of 3 human individuals, 67, 72, and 83 years of age, were alternately impregnated with silver, stained following Mowry and immunohistochemically stained for S100 or PGP 9.5. Distal parts of extraocular muscles from multiorgan donors, 2, 17, and 34 years of age, were prepared for electron microscopy. Spindles contained 1 to 18 intrafusal muscle fibers, 55% of which were nuclear chain fibers, 2% nuclear bag fibers, and 43% fibers exhibiting the same morphological features as extrafusal fibers. The latter had been previously described as "anomalous fibers" (Ruskell). This intrafusal type exclusively occurs in human extraocular muscle spindles. Ultrastructural analysis revealed morphologically normal sensory terminals on all 3 types of intrafusal fibers. Findings in a two-year-old individual were similar to those in aged individuals. Spindles in human extraocular muscles are specifically structured. Their special morphological features are also present during the development of binocular vision. Spindles are supposed to play a role in the (fine) control of eye movements.

An immunohistochemical approach to the intrafusal fibers of extraocular muscle spindles in sheep, cow, and pig

Intrafusal muscle fibers of the extraocular muscles (EOMs) of the sheep, cow, and pig were studied histochemically and immunohistochemically. In sheep and cow spindles, three intrafusal fiber types, namely the bag1, bag2, and chain fibers, were identified by a combination of standard histochemical methods and immunohistochemical staining with antibodies selective for slow-tonic (antitonic ALD) and slow twitch (anti-I BA-D5) myosin. The bag1 and bag2 fibers appeared immunologically different on the basis of their differential reactivity with the two antisera. Anti-tonic ALD preferentially stained the bag1 fibers, whereas anti-I BA-D5 labeled the bag2 fibers. Chain fibers did not react with either antisera. In the pig EOM spindles, in general, one bag and some chain intrafusal fibers were identified. The bag fiber was labeled by anti-tonic ALD, but it did not react with the anti-I BA-D5. These findings point to the existence in pig EOM spindles of only one bag fiber antigenically similar to the bag1 fiber of the other species examined.

The responses of muscle spindles in sheep extraocular muscles.

1. Responses from de-efferented muscle spindles in sheep extraocular muscles have been recorded in the Gasserian ganglion using glass microelectrodes. 2. The afferent fibre conduction velocities ranged from 32 to 106 m/sec and most were intermediate. The distribution was unimodal. 3. The afferent responses to ramp stretches and longitudinal vibration of the muscle could not be divided into two groups, but both the dynamic indices and vibration sensitivities of the afferents increased with their conduction velocities. 4. Injection of suxamethonium did not help to classify afferents with intermediate conduction velocity. 5. It is concluded that the afferents from sheep extraocular muscle spindles form a single population whose properties are correlated with their nerve fibre diameters.

Blink reflex in man in response to stretching of extraocular muscles?

An unilateral oculo-palpebral reflex evoked by weakly tapping the eyeball is described. It has a latency of 8–9 msec and a well-synchronized aspect. It is often followed by a silent period lasting 20–80 msec and is accompanied by a reciprocal inhibitory pause in the homolateral frontal muscle. It is unaffected by local anesthesia of the homolateral supra and infraorbital nerves, but is abolished by a homolateral retrogasserian neurotomy. Our results suggest that this short-latency blink reflex is produced by the stretching of extraocular muscles. It seems, therefore, likely that it originates in extraocular muscle spindles whose primary afferents are known to run with the ophthalmic branch of the trigeminal nerve. This reflex response can be facilitated by voluntary activation of the opposite orbicularis oculi muscle and in spastic hemiplegic patients it is potentiated on the affected side. Stronger tapping of the eyeball evokes a bilateral blink reflex with characteristics of a nociceptive reflex. It is suggested that this reflex originates in pain receptors located in extraocular muscles.

Extraocular muscle proprioception and the descending trigeminal nucleus

Scope of the present investigation was to look for the termination within the brain stem of the central process of the perikarya contained in the semilunar ganglion which provide the extraocular muscle spindles. Unitary responses to stretching single eye muscles were recorded by means of tungsten microelectrodes from the pars oralis of the ipsilateral descending trigeminal tract and nucleus in the lamb. The responses were characterized by a sudden increase in discharge rate of the units followed by a modest adaptation; the firing ceased as soon as the stretch was released. Single-pulse electrical stimulation of the cellular pool of the medial dorsolateral part of the semilunar ganglion which innervate the eye muscle proprioceptors elicited evoked potentials in the same ipsilateral pontine sites responsive to stretching the extraocular muscles. The latency of such evoked potentials was very short: 0.42–0.95 msec. We conclude that the afferent impulses from the eye muscles project to the descending trigeminal nucleus. Thus the central process of the semilunar ganglion cells concerned with the eye muscle proprioception enters the brain stem through the trigeminal sensory root, runs along the ipsilateral descending trigeminal tract, and terminates within the homonymous nucleus.