July 2005
Volume 46, Issue 7
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Anatomy and Pathology/Oncology  |   July 2005
The Anatomy of the Muscle Insertion (Scleromuscular Junction) of the Lateral and Medial Rectus Muscle in Humans
Author Affiliations
  • Gregor P. Jaggi
    From the Department of Ophthalmology, and the
  • Hubert R. Laeng
    Institute of Pathology, Kantonsspital, Aarau, Switzerland; the
  • Markus Müntener
    Department of Anatomy, University of Zürich, Zürich, Switzerland; the
    Department of Chemistry and Applied Biosciences, Swiss Federal Institute of Technology (ETH), Zürich, Switzerland; and the
  • Hanspeter E. Killer
    From the Department of Ophthalmology, and the
    Department of Ophthalmology, University of Basel, Basel, Switzerland.
Investigative Ophthalmology & Visual Science July 2005, Vol.46, 2258-2263. doi:10.1167/iovs.04-1164
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      Gregor P. Jaggi, Hubert R. Laeng, Markus Müntener, Hanspeter E. Killer; The Anatomy of the Muscle Insertion (Scleromuscular Junction) of the Lateral and Medial Rectus Muscle in Humans. Invest. Ophthalmol. Vis. Sci. 2005;46(7):2258-2263. doi: 10.1167/iovs.04-1164.

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      © ARVO (1962-2015); The Authors (2016-present)

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Abstract

purpose. To analyze the histologic features of the insertion of the medial and the lateral rectus muscles in humans.

methods. Postmortem study performed on 49 extraocular muscles from 21 subjects without known ocular disease. All muscles were obtained no longer than 8 hours after death, after consent for autopsy. Thirty-seven lateral recti muscles and 12 medial recti muscles were studied with light microscopy (hematoxylin-eosin and Goldner stains) as well as with enzyme histochemistry and immunohistochemistry, with monoclonal-human tenascin C antibody.

results. Light microscopic studies of muscle insertions of the lateral and the medial rectus muscle demonstrated muscle tissue connecting directly to the sclera without a tendon. These findings were confirmed immunohistochemically with tenascin C-antibody staining.

conclusions. Based on the results of this postmortem study in humans the term “muscle tendon” should be used with caution for the insertional area (scleromuscular junction) of the lateral and medial extraocular muscles. Light microscopy, histochemistry, and immunohistochemistry demonstrate that the tissue at the scleromuscular junction contains striated muscle with minimal connective (tendinous) tissue connecting to the sclera. To the best of the authors’ knowledge, this is the first study in which enzyme histochemistry and immunohistochemistry have been used to investigate the anatomy of the insertional area (muscle-tendon-sclera junction) of the extraocular muscles in humans.

Knowledge of the anatomic characteristics of the extraocular muscles and their insertional area is of vital interest for understanding the physiology of eye movements. 1 2 3 4 Most studies of the tendons of the extraocular muscles and the scleromuscular junction were performed macroscopically. Quantitative data concerning the length of the muscles and the tendons were obtained with calipers and were highly variable in the literature. 5 6 7 8 9 10 11 12 13  
Material and Methods
Forty-nine extraocular muscles (37 lateral rectus muscles and 12 medial rectus muscles) from 21 subjects (13 females and 8 males) without known ocular disease were obtained no later than 8 hours after death, after consent for autopsy according to the tenets of the Declaration of Helsinki. All muscles were dissected through transconjunctival access and removed with a small piece of adhering sclera. The specimens were embedded in optimal cutting temperature (OCT) compound (Tissue Tek; Miles, Elkhart, IN) and frozen in melting isopentane (−160°C) within 2 hours after excision. Some muscles were fixed in formaldehyde (4%) and embedded in paraffin (56–58°C, paraffin embedding system TBS88, Tissuewax; Medite Medizintechnik, Burgdorf, Germany). 
Serial sections (8 μm) of the frozen muscles were cut at −20°C (Cryocut Jung CM 3000; Leica, Glattbrugg, Switzerland). The specimens embedded in paraffin were cut longitudinally (5 μm) with a rotation microtome (Microm HM 325; Carl Zeiss Meditec, Jena, Germany). 
Some sections of each specimen were stained with hematoxylin-eosin (HE). For simultaneous demonstration of muscle fiber types and motor endplates, 20-μm-thick sections were processed according the method of Ashmore et al. 14 For demonstration of the position of the endplates alone, acetylcholinesterase was shown in sections (14 μm), according to the method of Karnovsky and Roots. 15  
One lateral rectus muscle was completely sectioned longitudinally and all sections processed to demonstrate the distribution of motor endplates along the entire length of the muscle. For the demonstration of motor end plates together with the terminal axons, sections (40 μm) were processed according to the methods of Karnovsky and Roots 15 and Pestronk and Drachman. 16 Serial consecutive sections (14 μm) were stained for myofibrillar adenosine triphosphatase (mATPase), cytochrome c oxidase and α-glycerophosphate-dehydrogenase. 17 18 19 20 21  
The extracellular glycoprotein tenascin C (monoclonal anti-human-tenascin C antibodies (Clon: B28-13; donated by Ruth Chiquet-Ehrismann, Miescher Institut Basel, Switzerland) was detected in longitudinal cryosections (8 μm) immunohistochemically, as described by Chiquet and Fambrough. 22  
Tenascin C, an extracellular glycoprotein, is present in the tendons of skeletal muscle but absent in scleral tissue. In addition, tenascin C is found in the connective tissue of the walls of blood vessels and of peripheral nerves. 22 23 24 25 26 27 28 In control experiments, biopsy specimens of human multifidus muscles were processed in the same way. 
The sections were evaluated with a light microscope (Axioscop; Carl Zeiss Meditec) and photographed with the microscopic system (Progress 3012 mF; Jenoptik Laseroptik Systeme, Jena, Germany) and further processed on computer (Photoshop 7.0; Adobe Systems Inc., Mountain View, CA). 
Results
All muscle insertions (scleromuscular junctions) of the medial and lateral rectus muscle were investigated, and in all muscles a global and an orbital portion was identified. (Fig. 1) . The two portions were separated by connective tissue that displayed multiple medium-sized blood vessels. The same type of arterioles was regularly demonstrated at the scleromuscular junction. 
In all muscles, short tendinous fibers were found between the muscle fibers and the sclera. For semiquantitative measurement of the length of these tendons, longitudinal sections (HE, anti-tenascin-C) were used. The length of the tendon was determined from the distance between the sclera and the first appearance of muscle tissue. The maximum length of tendon (HE staining) measured 3 mm in a lateral rectus muscle (Fig. 2) . In the specimens stained with anti-tenascin, neither medial nor lateral rectus muscles demonstrated a tendon length of more than 1 mm. In 75% of the specimens, muscle tissue was demonstrated connecting to the sclera (Fig. 3) . Direct contact between muscle and sclera was also demonstrated with hematoxylin-eosin stain. The global portion of the muscle inserted into the sclera more remotely in relation to the limbus (Fig. 4)
In all specimens examined, immunohistochemical staining demonstrated small amounts of tendon embedded in muscle tissue, but not necessarily connecting to the sclera. In most of the immunohistochemical specimens, striation of the muscle tissue remained intact. In all sections examined, tenascin-containing connective tissue was demonstrated. There was a slight increase in the amount of tenascin-stained tendon tissue found immediately adjacent to the sclera. These tendon fibers run parallel to the direction of the muscle fibers (Fig. 5) . The multifidus muscle that was used as a control for the stain showed a strong reaction to the antibody (Fig. 6)
The specimens stained for motor endplates 14 15 and terminal axons 15 16 were evaluated on a qualitative basis. Motor endplates and terminal axons were also found in the immediate vicinity of the sclera. 
Discussion
This histologic investigation (light microscopy, immunohistochemistry, and enzymohistochemistry) of the insertion of the lateral and medial extraocular muscles in humans demonstrated large amounts of muscle tissue that contained only minimal islands of tendon and connected directly with the sclera. A distinct tendon was not demonstrated. These findings contrast with former studies 6 7 11 29 that reported a proper muscle tendon connecting the muscle to the sclera. However, in only one of these former studies were histologic methods used for tissue identification. Histologic evidence of the presence of a tendon was only presented in one study of the superior oblique muscle. 30 Whether the term “tendon” is appropriate for extraocular muscles has been questioned by Apt, 7 who at the same time has raised doubt about the accuracy of the measurements of the length of the tendons reported in previous articles. He has suggested that the term “aponeurosis” would be more appropriate than the term tendon. Most of the literature dealing with eye movements has not fully explained eye muscle functions based on current anatomic knowledge. 29 31 32 33 The recent discovery of the pulley system has delivered powerful functional and anatomic insight into the way eye movements take place. 31 32 34 35 36 37  
With classic histologic staining such as hematoxylin-eosin or Goldner, tendon and sclera cannot be distinguished. Therefore, splitting off of scleral fibers due to inadvertent dissection could be misinterpreted to represent tendon (Fig. 2) . We used anti-tenascin C antibodies as a reliable tissue marker for distinguishing among muscle, tendon, and sclera. Tenascin C has been demonstrated in the limbus region of the eye, conjunctiva, Descemet’s membrane, and the tunica interna of blood vessels. The high specificity of tenascin C for collagen-containing tendon tissue is reflected by the lack of reaction to the connective tissue in the endomysium and the positive reaction to the connective tissue in the walls of blood vessels and in the perineurium. 22 23 24 25 26 27 28 The reaction of these tissues was used as a positive control. 
In contrast to other publications examining the “tendons” of extraocular muscles, we were unable to demonstrate the presence of a true tendon connecting muscle directly with the sclera in neither the medial nor the lateral rectus muscles. In the region of the muscle insertion (scleromuscular junction), we found muscle tissue containing only small islands of tendon tissue in the vicinity of the sclera. Such a situation was proposed by De Gottrau and Gajisin, 8 albeit without proper histologic or immunohistochemical evidence. The absence of Golgi-spindle organs in the distal portion of the extraocular muscles, as described by Blumer et al., 38 Bruenech and Ruskell, 39 and Richmond et al., 40 correlates with our findings of the paucity of tendon tissue in that region. The presence of motor endplates is further evidence for muscle tissue in the scleromuscular junction. 
Electromyographic (EMG) recordings demonstrating EMG potentials (Killer HE, personal experience) in the vicinity of the insertion of the lateral rectus and medial rectus muscle supplies clinical evidence for the presence of muscle endplates near the insertion of the muscle into the sclera. Innervated myotendinous cylinders (IMCs) were found abundantly in the proximal segments (insertional zone) of extraocular muscles. 2 10 As functional structures, IMCs are highly important for the proprioceptive innervation of human extraocular muscles. 41 Ophthalmologists performing eye muscle surgery should be aware that when they perform muscle resection they reduce the number of IMCs as well as the number of sarcomeres and motor endplates. In comparison with recession for surgical correction of strabismus, marginal myotomy was found to be more proprioceptively “deafferenting” than recession, probably due to a greater disruption of palisade endings. 42 Our findings showing that the medial and lateral recti insert without a tendon directly into the sclera indicate that resection of muscle tissue containing proprioceptive elements may also be more “deafferenting” than recession. Eye muscles are neded to perform extremely rapid (saccades) and highly coordinated movements (versions). To perform these movements, it is desirable that the generator of force (muscle) and the object being rotated (eyeball) be in direct contact. The interposition of a tendon between muscle and eyeball would probably impair the efficiency of ocular muscle function. 
 
Figure 1.
 
Horizontal section through human globe. (∗) Insertion of medial rectus displaying global portion (GP) and orbital portion (OP). H E stain. MR, medial rectus muscle; LR, lateral rectus muscle.
Figure 1.
 
Horizontal section through human globe. (∗) Insertion of medial rectus displaying global portion (GP) and orbital portion (OP). H E stain. MR, medial rectus muscle; LR, lateral rectus muscle.
Figure 2.
 
Scleromuscular junction of lateral rectus muscle displaying a maximum of 3 mm of tendon. Some of the material appearing as tendon (arrow) may be due to inadvertent dissection of sclera during preparation of the specimen. Multiple blood vessels (arrowhead). H E stain.
Figure 2.
 
Scleromuscular junction of lateral rectus muscle displaying a maximum of 3 mm of tendon. Some of the material appearing as tendon (arrow) may be due to inadvertent dissection of sclera during preparation of the specimen. Multiple blood vessels (arrowhead). H E stain.
Figure 3.
 
Scleromuscular junction (dotted line). Blood vessels in the muscle (M) show staining of the connective tissue in their walls with anti-tenascin C. Inset: tendon tissue surrounded by striated muscle. ( Image not available ) Musculotendinous junction. Only the connective tissue of the tendon was stained; the sclera remained unstained. Anti-tenascin C stain.
Figure 3.
 
Scleromuscular junction (dotted line). Blood vessels in the muscle (M) show staining of the connective tissue in their walls with anti-tenascin C. Inset: tendon tissue surrounded by striated muscle. ( Image not available ) Musculotendinous junction. Only the connective tissue of the tendon was stained; the sclera remained unstained. Anti-tenascin C stain.
Figure 4.
 
(A) Medial rectus muscle inserting into the sclera (Goldner staining). Note two-finger–type insertion (i.e., the global portion insertion is more remote from the limbus than the orbital portion). OP, orbital portion; GP global portion. (B) Higher magnification of the medial rectus insertion showing multiple layers of muscle connecting directly to the sclera (S).
Figure 4.
 
(A) Medial rectus muscle inserting into the sclera (Goldner staining). Note two-finger–type insertion (i.e., the global portion insertion is more remote from the limbus than the orbital portion). OP, orbital portion; GP global portion. (B) Higher magnification of the medial rectus insertion showing multiple layers of muscle connecting directly to the sclera (S).
Figure 5.
 
Detail from lateral rectus muscle displaying striated muscle fibers (MF) and antitenascin-C–stained tendon tissue running parallel to muscle fibers. Note the intact striation of the muscle tissue. Tenascin-C free endomysium (arrow).
Figure 5.
 
Detail from lateral rectus muscle displaying striated muscle fibers (MF) and antitenascin-C–stained tendon tissue running parallel to muscle fibers. Note the intact striation of the muscle tissue. Tenascin-C free endomysium (arrow).
Figure 6.
 
Human multifidus muscle demonstrating a global, strong anti-tenascin-C reaction.
Figure 6.
 
Human multifidus muscle demonstrating a global, strong anti-tenascin-C reaction.
The authors thank Michael C. Brodsky, MD (Arkansas Children’s Hospital, Little Rock, AR), and Jody Stähelin, MD (Department of Pediatrics, Kantonsspital, Aarau, Switzerland), for helpful comments on the manuscript. 
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Figure 1.
 
Horizontal section through human globe. (∗) Insertion of medial rectus displaying global portion (GP) and orbital portion (OP). H E stain. MR, medial rectus muscle; LR, lateral rectus muscle.
Figure 1.
 
Horizontal section through human globe. (∗) Insertion of medial rectus displaying global portion (GP) and orbital portion (OP). H E stain. MR, medial rectus muscle; LR, lateral rectus muscle.
Figure 2.
 
Scleromuscular junction of lateral rectus muscle displaying a maximum of 3 mm of tendon. Some of the material appearing as tendon (arrow) may be due to inadvertent dissection of sclera during preparation of the specimen. Multiple blood vessels (arrowhead). H E stain.
Figure 2.
 
Scleromuscular junction of lateral rectus muscle displaying a maximum of 3 mm of tendon. Some of the material appearing as tendon (arrow) may be due to inadvertent dissection of sclera during preparation of the specimen. Multiple blood vessels (arrowhead). H E stain.
Figure 3.
 
Scleromuscular junction (dotted line). Blood vessels in the muscle (M) show staining of the connective tissue in their walls with anti-tenascin C. Inset: tendon tissue surrounded by striated muscle. ( Image not available ) Musculotendinous junction. Only the connective tissue of the tendon was stained; the sclera remained unstained. Anti-tenascin C stain.
Figure 3.
 
Scleromuscular junction (dotted line). Blood vessels in the muscle (M) show staining of the connective tissue in their walls with anti-tenascin C. Inset: tendon tissue surrounded by striated muscle. ( Image not available ) Musculotendinous junction. Only the connective tissue of the tendon was stained; the sclera remained unstained. Anti-tenascin C stain.
Figure 4.
 
(A) Medial rectus muscle inserting into the sclera (Goldner staining). Note two-finger–type insertion (i.e., the global portion insertion is more remote from the limbus than the orbital portion). OP, orbital portion; GP global portion. (B) Higher magnification of the medial rectus insertion showing multiple layers of muscle connecting directly to the sclera (S).
Figure 4.
 
(A) Medial rectus muscle inserting into the sclera (Goldner staining). Note two-finger–type insertion (i.e., the global portion insertion is more remote from the limbus than the orbital portion). OP, orbital portion; GP global portion. (B) Higher magnification of the medial rectus insertion showing multiple layers of muscle connecting directly to the sclera (S).
Figure 5.
 
Detail from lateral rectus muscle displaying striated muscle fibers (MF) and antitenascin-C–stained tendon tissue running parallel to muscle fibers. Note the intact striation of the muscle tissue. Tenascin-C free endomysium (arrow).
Figure 5.
 
Detail from lateral rectus muscle displaying striated muscle fibers (MF) and antitenascin-C–stained tendon tissue running parallel to muscle fibers. Note the intact striation of the muscle tissue. Tenascin-C free endomysium (arrow).
Figure 6.
 
Human multifidus muscle demonstrating a global, strong anti-tenascin-C reaction.
Figure 6.
 
Human multifidus muscle demonstrating a global, strong anti-tenascin-C reaction.
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