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A n understanding of extraocular muscle function requires not only the anatomic study of static, fixed specimens, but also the detailed evaluation of dynamic muscle contractile properties and paths at different gaze positions-innervation levels (see refs. 1 and 2). John D. Porter*^ Vadims Poukens,%$ Using contemporary, high-resolution imaging ivchRobert S. Baker,,f and Joseph L. Demer§ niques, individual muscles are observed to swinsj in Purpose. Fibroelastic pulleys function like the trochlea toward the optic nerve with contraction and outv ard with relaxation.3 The normal occurrence of muscle to fix the position and pulling direction of the recti excursions in the radial direction as they shorten or extraocular muscles within the orbit. This study characterized the fine structure of the human medial rectus lengthen most likely is not relevant, and therefore is muscle pulley. not accounted for, in the neural programming of eye Methods. Human medial rectus muscle pulley tissue was movements. In contrast to the relative mobility in the radial direction, recti muscle paths are nearly immobidissected at autopsy, immersed in aldehydefixativesolulized over the full range of gaze, with minimal sidetion, and processed for and examined with light and slip along the surface of the globe in a direction orelectron microscopy. 34 Results. Pulley structures were located within posterior thogonal to muscle pulling directions. The muscle path stabilization was predicted by biomechanical Tenon's fascia, closely surrounding the medial rectus modeling56 and was confirmed using computerized muscle. Pulleys were comprised of a dense collagen matomography in humans,7 conventional x-ray imaging trix with alternating bands of collagen fibers precisely in alert monkeys,4 and magnetic resonance imaging arranged at right angles to one another. This threein humans.3'8 dimensional organization most likely confers high ten- Structure-Function Correlations in the Human Medial Rectus Extraocular Muscle Pulleys sile strength to the pulley. Elastin fibrils were interspersed in the collagen matrix. Fibroblasts and mast cells were scattered throughout the relatively acellular and avascular collagen latticework. Connective tissue and smooth muscle bundles suspended the pulley from the periorbita. Smooth muscle was distributed in small, discrete bundles attached deeply into the dense pulley tissue. The orbit contains an organized system of connective tissues.9"11 Anatomic studies of human orbits have shown that the stabilization of rectus muscle paths is mediated by identifiable connective tissue pulleys that are elastically suspended from the orbital walls.12 Fibroelastic pulleys, consisting of connective tissue sheaths in posterior Tenon's fascia, surround the recti Conclusions. Fine structural observations confirm the ex- extraocular muscles and function like the trochlea. The pulleys thus serve as mechanical origins that fix istence and substantial structure of a pulley system in the position and pulling direction of the muscles association with the medial rectus extraocular muscle. within the orbit.12 Extraocular muscle pulleys have a The presence of pulleys must be considered in models of the oculomotor plant. The cytoarchitecture and significant effect on orbital mechanics. The existence placement of pulleys suggest that they are internally of muscle pulleys also has an effect on strabismus surrigid structures and are consistent with the idea that gery outcomes.8 The current study used fine structural they determine functional origins for the extraocular analysis of human extraocular muscle pulleys to exmuscles. However, the nature of the connective tissue— tend understanding of the role of the peripheral ocusmooth muscle struts suspending the pulley system to lomotor plant in eye movement control. the orbit supports the notion that the pulley position, and thus the vector force of the eye muscles, may be adjustable. Invest Ophthalmol Vis Sci. 1996; 37:468472. From the Departments of * Anatomy and Neurobiology and f Ophthalmology, University of Kentucky Medical Center; and from the Departments of%Palhology and Laboratory Medicine, §Ophthalmology and Neurology, and the $Jules Stein Eye Institute, University of California, Los Angeles. Presented in part at the annual meeting of the Association for Research in Vision and Ophthalmology, Fort lMuderdale, Florida, May 1995. Supported by National Eye Institute grants EY09834 (pP) and EY08313 (JLD) and by Research to Prevent Blindness. JDP is the recipient of a Research to Prevent Blindness ljew R. Wasserman Merit Aiuard. Submitted for publication September 14, 1995; revised November 8, 1995; accepted November 9, 1995. Proprietary interest category: N. Reprint requests: John D. Porter, Department of Anatomy and Neurobiology, University of Kentucky Medical Center, 800 Rose Street, Ijixington, KY 405360084. METHODS. All human studies adhered to the tenets of the Declaration of Helsinki and were approved by institutional review boards, and informed, written consent was obtained. In this study, medial rectus muscle pulleytissuewas dissected from exenterated fresh adult orbits at autopsy with authorization by next of kin. Pulleys are associated with all four recti muscles.12 The most highly developed pulley in humans, that associated with the medial rectus, was selected for analysis. Pulleys were divided to enhance fixative penetration and were immersed in 4% glutaraldehyde fixative solution in 0.1 M phosphate buffer for 48 hours and then processed by routine methods for light and electron microscopy, as described in de- 468 Investigative Ophthalmology & Visual Science, February 1996, Vol. 37, No. 2 Copyright © Association for Research in Vision and Ophthalmology Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933192/ on 04/29/2017 Report :\ FIGURE i. light (A,B) and ^ electron (C,D) photomicro- J," graphs of the dense connective tissue of the orbital side of a human medial rectus muscle pulley. Note muscle fibers of the adjacent medial rectus (arrow) and the dense collagen matrix of the pulley proper with embedded elastin filaments (AJB). The general organization of the pulley tissue proper is a dense, relatively acellular collagen matrix. Alternating bands of collagen fibers were arranged precisely at right angles to one another (C), likely conferring high tensile strength to the pulley (x-s indicates cross-sectioned collagen; I-s indicates longitudinally oriented collagen). Elastin fibrils (e) were interspersed in the collagen matrix and were most densely distributed in regions adjacent to the medial rectus. Fibroblasts (f in C) and mast cells (m in D) also were scattered at intervals throughout the dense pulley matrix. Scale bars = 50 pirn (A), 25 /xm (B), 5//m ( C ) , 2 ^ m (D). tail previously.13 Briefly, tissues were postfixed in 1% osmium tetroxide, stained en bloc with 0.05% uranyl acetate, dehydrated in a graded series of methanols followed by propylene oxide, embedded in epoxy resin, and sectioned for light and electron microscopy. Semithin (1 /im) sections were stained with toluidine blue and examined with bright-field microscopy; ultrathin (90 nm) sections were stained with uranyl acetate and lead citrate and examined using a Hitachi (Mountain View, CA) HM-7000 electron microscope. Pulley smooth muscle cytoarchitecture and organization were compared with those of specimens of Miiller's muscle that were surgically excised in cases of congenital ptosis and were processed similarly. RESULTS. Rectus muscle pulley sleeves are continuous with the tough peripheral portion of posterior Tenon's fascia and become incomplete slings both anteriorly and posteriorly. Sleeves are stabilized by the fibromuscular septae extending from the pulleys proper to the orbital walls and to adjacent pulleys by way of posterior Tenon's fascia. Details of the general pulley architecture have been published elsewhere.'2 In this study, analyses were directed to the fine structure of the dense, orbital portions of the medial rectus pulley sleeve and the "struts" that anchor the pulley to the periorbita and orbital walls. The core structure of the pulley was a densely packed collagen matrix (Figs. 1A, IB). Elastin fibrils were interspersed in the collagen matrix and were most densely distributed on the orbital side of the pulley, immediately adjacent to the extraocular muscle. There did not appear to be any substantive, specialized covering of either the internal surface of the pulley or the external surface of the muscle tendon as it passed through the pulley. It has been suggested that entire recti tendons slide smoothly within the pulley sleeves by the telescoping of loose connective Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933192/ on 04/29/2017 470 Investigative Ophthalmology & Visual Science, February 1996, Vol. 37, No. 2 FIGURE 2. light (A) and electron (B,C) photomicrographs of the discrete smooth muscle bundles that extend radially from and are involved in suspension of the medial rectus pulley. Smooth muscle cells were distributed into bundles (s), usually 30 to 150 /tm in diameter, which were tightly encased in collagen and attached into die dense pulley tissue. Muscle cells (n denotes representative nuclei) were segregated into small, discrete bundles. Fine structural features of individual smooth muscle cells in pulleys (C) were identical witfi diose in other muscles, with few, scattered mitochondria (m), caveolae (open arrows), and dense bodies-attachment plaques {arrowheads). Note that collagen (c) surrounds individual smooth muscle cells with no direct cell-cell contact Scale bars = 50 /j,m <A), 5/xm (B), 0.5 Mm (C). tissue that surrounds the tendon.12 Current observations are not inconsistent with this hypothesis. At the ultrastructural level, pulleys consisted of alternating lamellae of collagen fibers precisely arranged at right angles to one another (Fig. 1C), likely conferring high tensile strength. Fibroblasts and mast cells were interspersed throughout the collagen latticework (Figs. 1C, ID). The dense pulley tissues had a low vascular content. Connective tissue and smooth muscle bundles provided a suspension system for the pulleys, extending radially away from the globe to anchor the pulley directly to the periorbita (Fig. 2). Smooth muscle was distributed in discrete bundles, usually 30 to 150 fj,m in cross-sectional diameter, that were tightly encased in collagen and were attached into the dense portion of the pulley tissue. This arrangement contrasted with the thin, wide sheet of smooth muscle fibers, encased in a loose connective tissue matrix, that characterized Muller's muscle (Fig. 3). In both Muller's muscle and the pulley struts, individual smooth muscle cells were separated by wide extracellular spaces occupied by collagen, and neither muscle exhibited gap junction contacts between adjacent cells (Fig. 2C). The cytoarchitectural features of individual smooth muscle cells (i.e., contractile filaments, caveolae, dense bodies) in the pulley struts were identical to those in other muscles, including Muller's muscle. Although the fixation of human pulley tissues was moderately good, the necessary reliance on autopsy material for these studies precluded identification of smooth muscle-associated autonomic nerve terminals14'15 at the electron microscopic level. DISCUSSION. Extraocular muscle pulleys, although compliant, stabilize the position of individual recti muscles within the orbit The existence of the pulleys requires alteration of long-held concepts of orbital dynamics and must be considered in modeling of the oculomotor plant. Radial movement of the recti Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933192/ on 04/29/2017 Report FIGURE 3. Electron photomicrograph of Miiller's muscle. As is the smooth muscle of the recti muscle pulleys, the smooth muscle cells of Miiller's muscle are isolated from one another (n denotes representative nuclei). However, the discrete bundles of smooth muscle associated with the pulleys contrast with the smooth muscle sheet seen in Miiller's muscle. This organizational difference may facilitate more efficient neural activation of the smooth muscle associated with the pulleys. Associated collagen is less dense than in pulleys. Scale bar = 5 fj,m. muscles, toward and away from the optic nerve, is allowed by the arrangement of orbital connective tissues. By contrast, the side-slip of recti muscle bellies across the globe is markedly restricted.3 Current data support the notions that mechanically substantial pulleys exist in Tenon's capsule and that these are capable of directing muscle paths during gaze changes. Not unlike the trochlea that anchors the superior oblique, the cytoarchitecture of medial rectus pulleys suggests that the fibroelastic muscle sheaths are highly stiff structures. Their relatively acellular nature and the presence of dense collagen arrays oriented at right angles to one another confer substantial three-dimensional strength to the pulley, precisely at the site of attachment of its suspension system. Ultrastructural data suggest that the pulleys are sufficiently stiff to stabilize the rectus muscles during large changes in gaze, as was independently demonstrated with magnetic resonance imaging.3 i2 The contrast between the anchoring system of the recti muscle pulleys and the trochlea suggests a difference in the two strategies of establishing functional muscle origins. Rigid anchoring of the trochlea supports the view that it mediates a fixed, passive change in superior oblique line of force. By contrast, the nature of the connective tissue—smooth muscle struts suspending the pulley system to the orbit supports the hypothesis that the pulley position, and thus the vector force of the eye muscles, may be adjustable by either passive stiffness or active (e.g., smooth muscle innervation, hormonal) mechanisms. Although orbital smooth muscle is not uncommon in mammals, it is unlikely that the pulley support structure is vestigial. Phylogenetic studies (Demer JL, unpublished, 1995) suggest that the pulleys are of particular importance in humans. Moreover, an intricate innervation pattern, including rich sympathetic, parasympathetic, and nitroxidergic innervation1415 to pulley smooth muscle, further supports the hypothesis of a refined role in eye alignment, movement, or both. Innervation of smooth muscle in the pulley struts, albeit slower than skeletal muscle activation mechanisms, may alter the functional muscle origin in accordance with gaze changes.1415 Despite substantial temporal differences in excitation-contraction coupling for skeletal versus smooth muscle, coordinated function of Muller's muscle and the levator palpebrae superioris does occur in the control of vertical eyelid position. Applying a similar skeletal-smooth muscle interactive scheme to the recti muscle pulleys, the smooth muscle in the pulley struts might serve to alter dynamically pulley position during gaze changes. Either innervation or an intrinsic contractile response to stretch could provide temporally appropriate changes in pulley position. Alternatively, slow, attention-related changes in smooth muscle force in the pulley struts might serve simply to maximize extraocular muscle force generation in the alert state. Finally, the presence of pulleys, in association with the rectus extraocular muscles, may have implications for the computations required of brainstem circuitry in the neural control of eye movements. Although some high level oculomotor centers clearly operate in a spatial coordinate scheme,16 the motor command is decomposed into signals appropriate for activating individual muscles that must relate to retinocentric coordinates. Taken together, the properties of the recti extraocular muscle pulleys and the role they play in stabilization of muscle paths must be understood to resolve contemporary questions regarding the axes of ocular rotation during reflexive eye movements.17"19 Key Words extraocular muscle, oculomotor, orbital mechanics, strabismus, Tenon's capsule Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933192/ on 04/29/2017 472 Investigative Ophthalmology & Visual Science, February 1996, Vol. 37, No. 2 Acknowledgments The authors thank Mary Gail Engle and Olga Itkis for technical assistance. They also thank Dr. Paul May for helpful discussions concerning the interpretation of pulley function. References 1. Porter JD, Baker RS, Ragusa RJ, Brueckner JK. Extraocular muscles: Basic and clinical aspects of structure and function. Surv Ophthalmol. 1995;39:451-484. 2. Miller JM, DemerJL. Biomechanical analysis of strabismus. Binoc Vis. 1992;7:233-248. 3. Miller JM. Functional anatomy of normal human rectus muscles. Vision Res. 1989; 29:223-240. 4. Miller JM, Robins D. Extraocular muscle sideslip and orbital geometry in monkeys. Vision Res. 1987; 27:381392. 5. Miller JM, Robinson DA. A model of the mechanics of binocular alignment. Comput Biomed Res. 1984; 17:436-470. 6. Robinson DA. A quantitative analysis of extraocular muscle cooperation and squint. Invest Ophthalmol. 1975; 14:801-825. 7. Simonsz HJ, Harting F, de Waal BJ, Verbeeten WJM. Sideways displacement and curved path of recti eye muscles. Arch Ophthalmol. 1985; 103:124-128. 8. Miller JM, DemerJL, Rosenbaum AL. Effect of transposition surgery on rectus muscle paths by magnetic resonance imaging. Ophthalmology. 1993; 100:475-487. 9. Koomneef L. New insights in the human orbital connective tissue. Arch Ophthalmol. 1977;95:1269-1273. 10. Koomneef L. Details of the orbital connective tissue system in the adult. Ada MorpholNeerl Scand. 1977; 15:1-34. 11. Koomneef L. The architecture of the musculo-fi brous apparatus in the human orbit. Acta Morphol Neerl Scand. 1977; 15:35-64. 12. DemerJL, Miller JM, Poukens V, Vinters HV, Glasgow BJ. Evidence for fibromuscular pulleys of the recti extraocular muscles. Invest Ophthalmol Vis Sci. 1995; 36:1125-1136. 13. Porter JD, Burns LA, May PJ. Morphological substrate for eyelid movements: Innervation and structure of primate levator palpebrae superioris and orbicularis oculi muscles. / Comp Neurol. 1989; 287:64-81. 14. DemerJL, Poukens V, Micevych P. Innervation of the smooth muscle of the extraocular recti pulleys in humans and monkeys. Soc Neurosci Abstr. 1995; 21:1919. 15. DemerJL, Poukens V, Micevych P. Nitroxidergic and catecholaminergic innervation of the smooth muscle of the medial rectus pulley in humans. ARVO Abstracts. Invest Ophthalmol Vis Sci. 1995;36:S959. 16. Mays LE, Sparks DA. Saccades are spatially, not retinocentrically, coded. Science. 1980;208:1163-1165. 17. Haustein W. Considerations on Listing's law and the primary position by means of a matrix description of eye position control. Biol Cybernet. 1989; 60:411-420. 18. Crawford JD, Vilis T. Axes of eye rotation and Listing's law during rotations of the head. J Neurophysiol. 1991;65:407-423. 19. Misslisch H, Tweed D, Fetter M, Sievering D, Koenig E. Rotational kinematics of the human vestibuloocular reflex: III: Listing's law. / Neurophysiol. 1994; 72:24902502. Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933192/ on 04/29/2017