The eye muscles and their innervation inChaetodon trifasciatus (Pisces,Teleostei, Chaetodontidae)

Synopsis InChaetodon trifasciatus, the large eye has the form of a thick disk rather than that of a globe. A deep cutaneous groove surrounds the eyeball, probably allowing rapid eye movements. The form and innervation of the three pairs of extraocular muscles are described. Each muscle is made of two types of fascicles of fibres, thick and thin. There is neither an anterior nor posterior myodome. The skull attachment of the obliques and of the inferior rectus is made on the thin sagittal ethmoidal membranous septum while that of the other recti occurs on osseous pieces of the skull. The attachment on the eyeball is made on the cartilaginous sclera. The ratio of the lengths of the antagonist muscles, superior vs. inferior oblique, superior vs. inferior rectus and medial vs. lateral rectus, is about 1.43:1. The three oculomotor nerves (III: common oculomotor, IV: trochlear and VI: abducens) as well as the ciliary system are described. For the following reasons, an analogy between the lateral rectus ofChaetodon trifasciatus and the lateral rectus + retractor bulbi of other vertebrates is indicated: (1) the nucleus of nerve III (which innervates four muscles) has four sectors, while that of IV (which innervates only the superior oblique) is made of one sector; (2) nerve VI consists of two roots corresponding to two groups of nerve cells of its motor nucleus and (3) in other vertebrates, nerve VI innervates both the lateral rectus and the retractor bulbi.     

Distribution of motoneurones innervating extraocular muscles in the brain of the marmoset (Callithrix jacchus)

Extraocular muscle motoneurones were localised in the oculomotor nucleus (ON), trochlear nucleus (TN) and abducens nucleus (AN) in the marmoset brain using the horseradish peroxidase (HRP) retrograde labelling technique. HRP pellets injected into individual extraocular muscles revealed one or more groups of labelled neurones occupying discrete loci within these nuclei. Relatively little overlap of motoneurone pools was observed, except in the case of the inferior oblique and superior rectus muscles. Injections of HRP into the medial rectus muscle revealed three separate populations of labelled cells in the ipsilateral ON. Motoneurones innervating the inferior rectus muscle were mainly localised in the lateral somatic cell column of the ipsilateral ON. A second smaller grouping was observed in the medial longitudinal fasciculus. The inferior oblique muscle motoneurones were localised in the ipsilateral medial somatic cell column intermingled with motoneurones supplying the superior rectus muscle of the opposite eye. The superior oblique muscle motoneurones occupied the entire TN and the lateral rectus muscle motoneurones the AN. It was concluded that the organisation of nuclei and subnuclei responsible for controlling the extraocular muscles in the marmoset is broadly similar to that of other primates.     

Stromal cell‐derived factor‐1 and hepatocyte growth factor guide axon projections to the extraocular muscles

Vertebrate eye movements depend on the co‐ordinated function of six extraocular muscles that are innervated by the oculomotor, trochlear, and abducens nerves. Here, we show that the diffusible factors, stromal cell‐derived factor‐1 (SDF‐1) and hepatocyte growth factor (HGF), guide the development of these axon projections. SDF‐1 is expressed in the mesenchyme around the oculomotor nerve exit point, and oculomotor axons fail to exit the neuroepithelium in mice mutant for the SDF‐1 receptor CXCR4. Both SDF‐1 and HGF are expressed in or around the ventral and dorsal oblique muscles, which are distal targets for the oculomotor and trochlear nerves, respectively, as well as in the muscles which are later targets for oculomotor axon branches. We find that in vitro SDF‐1 and HGF promote the growth of oculomotor and trochlear axons, whereas SDF‐1 also chemoattracts oculomotor axons. Oculomotor neurons show increased branching in the presence of SDF‐1 and HGF singly or together. HGF promotes the growth of trochlear axons more than that of oculomotor axons. Taken together, these data point to a role for both SDF‐1 and HGF in extraocular nerve projections and indicate that SDF‐1 functions specifically in the development of the oculomotor nerve, including oculomotor axon branch formation to secondary muscle targets. HGF shows some specificity in preferentially enhancing development of the trochlear nerve. © 2010 Wiley Periodicals, Inc. Develop Neurobiol 70: 549–564, 2010     

Effect of oculomotor and trigeminal nerve section on the ultrastructure of different myoneural junctions in the rat extraocular muscles

Summary The intramuscular nerves and myoneural junctions in the rat rectus superior, medialis and inferior muscles from 10 hours to about 10 days after section of the trigeminal and oculomotor nerves were studied with the electron microscope. Two different kinds of myoneural junctions are to be observed; one type derives from myelinated nerves and is similar to the ordinary myoneural junctions (motor end plates) of other striated skeletal muscles, while the other type derives from unmyelinated nerves, is smaller in size and has many myoneural synapses distributed along a single extrafusal muscle fibre.Section of the trigeminal nerve caused no changes in the myoneural synapses. After section of the oculomotor nerve degenerative changes occur in both the myelinated and unmyelinated nerves and in both types of myoneural junctions. In the axon terminals of both the myelinated and unmyelinated nerves the earliest changes are to be observed 10 to 15 hours after section of the nerve. First, swelling of the axoplasm, fragmentation of microtubules and microfilaments and swelling of mitochondria takes place, somewhat later agglutination of the axonal vesicles and mitochondria. The axon terminals are separated from the postsynaptic muscle membrane by hypertrophied teloglial cells about 24 hours after section of the nerve. The debris of the axon terminals is usually digested by the teloglial cells within 42 to 48 hours in both types of myoneural junction.Changes in the postsynaptic membrane are observed in the myoneural junctions of the unmyelinated nerves as disappearance of the already earlier irregular infoldings, whereas no changes take place in the infoldings of the motor end plates. The postsynaptic sarcoplasm and its ribosomal content increase somewhat.The earliest changes occur along unmyelinated axons 10 to 15 hours and along myelinated axons 15 to 24 hours after nerve section. The unmyelinated axons are usually totally digested within 48 hours, whereas the myelinated axons took between 48 hours and 4 days to disappear. The degeneration, fragmentation and digestion of the myelin sheath begin between 24 and 42 hours and still continues 10 days after the operation.The results demonstrate that in the three muscles studied structures underlying the physiologically well known double innervation of the extraoccular muscles are all part of the oculomotor system.We are grateful to Professor Antti Telkkä, M. D. Head of the Electron Microscope Laboratory, University of Helsinki, for permission to use the facilities of the laboratory.     

The eye muscles and their innervation in the gobiid fishTridentiger trigonocephalus

The morphology and innervation of the six oculomotor muscles in the gobiid fishTridentiger trigonocephalus are described. Every rectus muscle is composed of two types of muscle fibres. Muscles attach onto the cartilaginous or fibrous sclerotica. Oblique muscles attach onto the ethmoidal plate; recti muscles attach onto the parasphenoid or a thick fibrous membrane. There is no myodome. The common oculomotor nerve is composed of four bundles, the trochlear and the externus of two. The two kinds of fibres of the lateral rectus and the two distinct bundles of the nerve VI suggest a possible homology between this muscle in fishes and the lateral rectus+retractor bulbi in mammals.     

Peripheral pathway of proprioceptive fibres from feline extra-ocular muscles. I. A histological study.

The findings of the previous study (1976) involving orbital operations in 12 cats have been confirmed in this study involving intracranial operations in 20 more cats. The perikarya of origin of afferent fibres from feline extra-ocular msucles have been clearly localised to the trigeminal mesencephalic nucleus. The functional subdivision in the nucleus that was noted earlier has been reaffirmed. Thus the caudal or pontine part was the location of cell bodies from the lateral rectus muscle, the intermediate part contained those from the superior oblique, while the other muscles were represented by cell bodies in the rostral part, there being some degree of overlap in the last two zones. In every instance the representation was shown to be bilateral and the total ratio of cellular representation was in the region of 4:1 (ipsilateral-contralateral). The peripheral pathway of the proprioceptive fibres has been shown to be exclusively along the oculomotor, trochlear and abducent nerves which are therefore sensorimotor.     

A comparative study of oculomotor,trochlear and abducens nerves in Arabian foals

We investigated the microscopic structure of transverse sections of the oculomotor, trochlear and abducens nerves of Arabian foals using stereological methods. Bilateral nerve pairs from 2-month-old female Arabian foals were analyzed. The tissues were embedded in plastic blocks, then 1 µm thick sections were cut and stained with osmium tetroxide and methylene blue-azure II. Stereology was performed using light microscopy. Morphometry showed that the right and left pairs of nerves were similar. The transverse sectional areas of the oculomotor, trochlear and abducens nerves were 1.93 ± 0.19 mm², 0.32 ± 0.06 mm² and 0.70 ± 0.08 mm², respectively. The oculomotor nerve exhibited a significantly greater number of myelinated axons (16755 ± 1279) and trochlear (2656 ± 494) and the abducens nerves (4468 ± 447). The ratio of the axon diameter to myelinated nerve fiber diameter was 0.58, 0.55 and 0.55 for the oculomotor, trochlear and abducens nerves, respectively. Of the three nerves studied, the abducens nerve exhibited the greatest nerve fiber area, myelin area, nerve and axon diameters, and myelin thickness. The ratio of small myelinated nerve fibers was greatest in the oculomotor nerve.     

Congenital fibrosis of the extraocular muscles type 2, an inherited exotropic strabismus fixus,maps to distal 11q13.

The extraocular fibrosis syndromes are congenital ocular-motility disorders that arise from dysfunction of the oculomotor, trochlear, and abducens nerves and/or the muscles that they innervate. Each is marked by a specific form of restrictive paralytic ophthalmoplegia with or without ptosis. Individuals with the classic form of congenital fibrosis of the extraocular muscles (CFEOM1) are born with bilateral ptosis and a restrictive infraductive external ophthalmoplegia. We previously demonstrated that CFEOM1 is caused by an autosomal dominant locus on chromosome 12 and results from a developmental absence of the superior division of the oculomotor nerve. We now have mapped a variant of CFEOM, exotropic strabismus fixus ("CFEOM2"). Affected individuals are born with bilateral ptosis and restrictive ophthalmoplegia with the globes "frozen" in extreme abduction. This autosomal recessive disorder is present in members of three consanguineous Saudi Arabian families. Genetic analysis of 70 individuals (20 affected individuals) reveals linkage to markers on chromosome 11q13, with a combined LOD score of 12.3 at the single nonrecombinant marker, D11S1314. The 2.5-cM CFEOM2 critical region is flanked by D11S4196/D11S4162 and D11S4184/1369. Two of the three families share a common disease-associated haplotype, suggesting a founder effect for CFEOM2. We hypothesize that CFEOM2 results from an analogous developmental defect to CFEOM1, one that affects both the superior and inferior divisions of the oculomotor nerve and their corresponding alpha motoneurons and extraocular muscles.     

Somatotopic localization of the eye muscle afferents in the semilunar ganglion.

In the medial dorsolateral portion of the semilunar ganglion of curarized and anaesthetized lambs a cellular pool has been identified which contains the perikarya of the first-order neurons of the eye muscle proprioception. Responses to moderate manual stretch of individual eye muscles were recorded by means of tungsten microelectrodes, from single units of the ganglion. They were of the type induced by muscle spindle excitation. Such responses showed a somatotopic localization. The superior rectus and the superior oblique muscles were represented in the most dorsal layers of the ganglion, while the inferior rectus and the inferior oblique muscles projected on the most ventral portion of the pool. The medial and the lateral recti were represented in the medial and lateral parts and occasionally wedged themselves between the cells innervating the superior and the inferior muscles. Thus a somatotopic arrangement of the eye muscle proprioception has been demonstrated for the first time in the semilunar ganglion.     

Position of the areae nervosae of the eye muscles innervated by the n. oculomotorius and their distances from the orbital border

The length of the oculomotory nerve in the midbrain, in the cisterns, and the orbit to the muscles Mm. rectus superior, rectur inferior, obliquus inferior, and rectus medialis are measured on 91 objects. Also the distances between the margins of the orbit and the most anterior nerve fibers to the muscles are estimated.     

Somatotopic organization of second order neurons of the eye muscle proprioception

Unit activity was recorded extracellularly from lamb's nucleus principalis and pars oralis of trigeminal nuclear complex following moderate manual stretching of individual extraocular muscles. The oral portion of the spinal trigeminal nucleus and the main sensory nucleus have been investigated by systematic exploration of the second-order neurons of the eye muscle proprioception. Such responses were somatotopically organized. In particular, each single extraocular muscle was represented along the main dorso-ventral axis in this manner: superior oblique and superior rectus in a dorsal layer; inferior rectus and inferior oblique in an intermediate layer, while the medial rectus and the lateral rectus were represented more ventrally. In a few experiments this representation was not observed, due to intermingling of the units. The topographic organization of eye muscle proprioception in the trigeminal nuclear complex described above closely corresponds to that reported by previous authors in the Gasser ganglion.     

Number and arrangement of extraocular muscles in primitive gnathostomes: evidence from extinct placoderm fishes

Exceptional braincase preservation in some Devonian placoderm fishes permits interpretation of muscles and cranial nerves controlling eye movement. Placoderms are the only jawed vertebrates with anterior/posterior obliques as in the jawless lamprey, but with the same function as the superior/inferior obliques of other gnathostomes. Evidence of up to seven extraocular muscles suggests that this may be the primitive number for jawed vertebrates. Two muscles innervated by cranial nerve 6 suggest homologies with lampreys and tetrapods. If the extra muscle acquired by gnathostomes was the internal rectus, Devonian fossils show that it had a similar insertion above and behind the eyestalk in both placoderms and basal osteichthyans.     

Innervation of the respiratory muscles of Gallus domesticus

A detailed gross anatomical study of the innervation of the respiratory muscles was made on twenty mature, male, Single Comb White Leghorn chickens. The aim was to demonstrate the general pattern and degree of terminal branching of the intercostal and lumbar nerves that innervate respiratory muscles. The point of entry for all nerves was on the medial face of the proximal third of the belly of the muscles, except for the transversus abdominis and costopulmonary muscles. The nerves were not always accompanied by blood vessels at the point of entry but both were invariably related at their terminal branches within the muscle belly and the tendon or aponeurosis. Within the muscle, primary, secondary, tertiary, and quarternary subdivisions of nerves coursed parallel to the muscle fibers, but some were tortuous. Plexus formation and/or segmental nerve anastomosis was most evident in strongly active expiratory and inspiratory muscles, i.e., all abdominal muscles and the m. costisternalis pars major. A craniocaudal gradient in the size and development of the contractile mass of the intercostal muscles was observed. The mm. intercostales interni increased in size in the caudal intercostal spaces, while the reverse was true for the mm. intercostales externi. Variable forms and sizes of lateroventral abdominal muscles were observed and the m. rectus abdominis was consistently present. The mm. intercostales interni and externi received branches from both the nn. intercostales interni and externi.     

Central connection of the optic, oculomotor, trochlear and abducens nerves in medaka, Oryzias latipes

Medaka (Oryzias latipes) is one of the few vertebrate experimental animals in which inbred lines have been established. It is also a species that has advanced in genetic studies in a manner comparable to zebrafish. This fish is therefore a good model for studying functional organization of the nervous system, but anatomical analysis of its nervous system has been limited to embryonic stages. In the present study, we investigated anatomy of cranial nerves in adult fish focusing on the visual function, using an inbred strain of medaka. Cranial nerves of medaka were labeled using biocytin, revealing a central distribution of retinofugal terminals, retinopetal neurons, and oculomotor, trochlear and abducens motor neurons. The optic nerve of the adult medaka was of a complete decussation type. Retinofugal terminals were located in 8 brain nuclei, the suprachiasmatic nucleus, nucleus pretectalis superficialis, nucleus dorsolateralis thalami, area pretectalis pars dorsalis (APd), area pretectalis pars ventralis (APv), nucleus of the posterior commissure (NPC), accessory optic nucleus, and the tectum opticum. Retinopetal neurons were identified in 6 brain nuclei, the ganglion of the terminal nerve, preoptic retinopetal nucleus, nucleus dorsolateralis thalami, APd, APv, and NPC. The oculomotor neurons were mostly labeled ipsilaterally and were located dorsomedially, abutting the fasciculus longitudinalis medialis in the mesencephalon. The trochlear nucleus was located contralaterally and dorsolaterally adjacent to the fasciculus longitudinalis medialis in the mesencephalon. The abducens nucleus was located ipsilaterally in a ventrolateral part of the rhombencephalic reticular formation. These results, generally similar to those in other teleosts, provide the basis for future behavioral and genetic studies in medaka.     

鱼类滑车神经的形态学研究

目的：应用生物胞素法观察罗非鱼滑车神经的形态分布。方法：本实验用罗非鱼,10只（性别不限）,体长12～16cm,动物浸入140mg／L三卡因间氨苯酸乙脂甲磺酸盐{tricainemethanesulfonate（MS222）}溶液中麻醉,在手术显微镜下暴露滑车神经,通过生物胞素（Biocytin）结晶追踪技术研究定位硬骨鱼类滑车神经的形态分布。结果：①被标记的神经纤维长而粗细不等,平行致密排列,从后外下向前内上方向行走,逐渐上行,于中脑水管正中背侧部,进行交叉到对侧,终于中脑水管腹侧部的滑车神经核细胞。②神经核细胞呈圆形和卵圆形,大小不一,亦可见神经元的突起,有的突起呈螺旋状连于胞体,有的呈线状连于胞体,形成神经终末及突触联系,并可见到多极神经元。结论：鱼类滑车神经纤维在中脑内的走行与人类基本一致,滑车神经核位于中脑水管腹侧部。     

Development of midbrain and anterior hindbrain ocular motoneurons in normal and Wnt-1 knockout mice

The effect of homozygotic Wnt-1^?/? mutations on the development of ocular motoneurons was examined with the lipophilic dye DiI and compared to control and phenotypic wild-type mouse embryos. A piece of DiI-soaked filter paper was inserted into the orbit, the midbrain, or rhombomere 5 of the hindbrain in six paraformaldehydefixed litters (10.5, 12.5, and 14.5 days postcoitum) containing Wnt-1, Wnt^+/?, and Wnt-1^+/+ individuals and three control litters. We labeled all ocular motoneurons retrogradely and all relevant nerves anterogradely in all control and phenotypic wild-type animals. In all phenotypically identified Wnt-1^?/? mutants we could always label the abducens nerve and motoneurons and the optic fibers to the thalamus, but we were unable to lable oculomotor or trochlear nerves or motoneurons. In addition to Wnt-1 knockout mutants, we also labeled mice from the WZT9B transgenic line carrying a lacZ reporter gene driven by the Wnt-1 gene enhancer. In these embryos we tested for co-localization of Wnt-1 expression in biotinylated dextran amine-labeled ocular motoneurons using a newly developed technique. In younger embryos we obtained evidence for co-localization of the β-galactosidase reaction product derived from lacZ gene activity in some retrogradely filled oculomotor motoneurons and adjacent to other oculomotor and the trochlear motoneurons. Acetylcholine esterase, a marker of early differentiating cholinergic neurons, showed a similar topology with respect to the lacZ reaction product. Thus, at least some future oculomotor motoneurons express Wnt-1, whereas others and the trochlear motoneurons caudal to the ventral midbrain expression of Wnt-1 may be exposed to the short range diffusion of the Wnt-1 gene product. Thus, the Wnt-1^?/? mutation precludes formation or survival of midbrain and anterior hindbrain neurons, including oculomotor and trochlear motoneurons. © 1995 John Wiley & Sons, Inc.     

Cranial endothermy and a putative brain heater in the most basal tuna species, Allothunnus fallai

Field studies on the slender tuna Allothunnus fallai revealed cranial temperatures that were 4·8 ± 0·4° C (mean ± s . d .) above the ambient sea surface temperature. Dissections aimed at documenting the cranial heat source revealed a fused extraocular muscle complex positioned beneath the brain of this basal tuna species. The muscle complex is structurally distinct from that documented for any other fish species. In A. fallai , all four extraocular rectus muscle pairs (superior, inferior, medial and lateral rectus) are incorporated into one distinct tissue complex which is positioned between the orbits and in direct contact with the braincase. A combination of morphological, physiological and biochemical techniques were used to characterize the modified muscle tissue, and high-resolution magnetic resonance imaging was used to illustrate its association with the brain and optic nerves. The modified eye muscles lack organized contractile proteins and are perfused by an extensive vascular counter-current system that originates from the internal carotid artery. Vessel diameters, artery–vein configuration, and anatomic position between the systemic circulation and the warm eye muscles all suggest that this system is a heat exchanger. Collectively, these findings suggest that A. fallai has evolved extraocular muscles that may function to warm the brain and eye region. This is the first record of a cranial modification comprised of all four rectus muscles and the only documented occurrence of this mechanism for cranial endothermy among the tunas.     

Morphometric comparison between human and rat abducens and oculomotor nerves

A morphologic and morphometric comparison between normal human and rat extraocular muscle nerves was performed using a computer-assisted method to obtain scatter diagrams of relative sheath thickness (g ratio = quotient axon diameter/fiber diameter). Human and rat extraocular muscle nerves (nervus abducens and ramus medialis n. oculomotorii) were excised immediately before the nerve branching at the entering point into the muscle. There was no difference in the absolute number of myelinated fibers between the oculomotor and abducens nerves in both species. The distribution of myelinated fibers was classified according to their g ratios into a two-stage density cluster analysis. Two main populations of nerve fibers for human oculomotor and rat oculomotor and abducens nerves and three main populations for human abducens nerve were differentiated morphometrically and mathematically, differing in their relative sheath thicknesses. There are distinct differences between scatter diagrams of human and rat extraocular muscle nerves, in correlation with the basically different oculomotor functions of these two species. The morphometric differences between human and rat extraocular muscle nerves suggest a difference in the myelination process and the presence of functionally different nerve fibers, strongly indicated by the populations and subpopulations of myelinating nerve fibers peculiar to extraocular muscle. The existence of more than two different types of myelinated fibers in the human nerves implies that the traditional classification based on fiber caliber must be reviewed and a comparison of different classes of nerve and muscle fibers should be performed.     

Trochlear-oculomotor nerve interactions in Xenopus laevis tadpoles: a temporal study.

When the trochlear nerve (NIV), which innervates the superior oblique muscle (SOM), is crushed or cut at stages 48-49 in Xenopus tadpoles, fibers from the oculomotor nerve (NIII) sprout and invade the SOM. The maximal percentage of specimens having at least one oculomotor nerve fiber on the SOM on a given day increased from 9.1% following a single crushing of NIV to 84.2% following three successive severings of NIV and the average number of silver-impregnated NIII fibers per specimen increased from 0.23 +/- 0.16 (mean +/- S.E.M.) in the single-crush experiment to 7.35 +/- 1.33 in the triple-cut experiment. This increase directly reflects the delay in the return of NIV. As NIV returns to the SOM, a portion of the inappropriate innervation is lost; while another portion appears to be stable and is in evidence 90 days after a single sectioning of NIV. The more rapidly NIV returns to the SOM, the more complete is the displacement of the NIII fibers. This suggests that the association between NIII and the SOM changes with time so that easy displacement of the inappropriate innervation is likely only when the reinnervation by the appropriate nerve fibers is rapid.