Double insertions of extraocular rectus muscles in humans and the pulley theory

Abstract

Recent studies have promoted the concept that rectus muscles pass through connective tissue pulleys located near the equator of the eye and act, in effect, as the muscle origins. Orbital muscle fibres (facing bone) terminate in pulleys, permitting adjustment of their position independent of the global fibres responsible for rotating the eye.The structure of pulleys (or muscle sleeves) and the passage taken by their muscle fibre insertions are unclear, and a detailed description is presented here together with a review of the active pulley hypothesis. Segments including the full width of single muscles were removed from the full orbital contents of dissection room cadavers and fresh perfusion-fixed rhesus and cynomolgus monkeys and prepared for light microscopy. Thin longitudinal sections were cut as facets from resin-embedded tissue blocks and montages assembled. Interrupted serial sections of selected regions of both species and ultrathin sections of monkey material were prepared for light and electron microscopy, respectively. Slender tendons leave the orbital surface of rectus muscles at intervals, aggregating and entering sleeves in humans and monkey; less frequently, tendons pass from the global surface to sleeves or insert directly in the posterior fascia bulbi. The orbital sides of sleeve rings are continuous with the fascial canopy of the globe and are 5 -6 times as thick as the global sides; sleeve structure differs in the four recti. Medial rectus sleeves are the thickest, and contain smooth muscle, whereas little or none is present in the other rectus sleeves. Superior rectus sleeves are variable in structure and relatively insubstantial. A narrow interval separates muscles from the surrounding connective tissue equatorially in some preparations, consistent with a capacity to slide, but the tissues are contiguous in others, especially in monkey material. The structural organization of sleeves and their tendons, together with other presented factors, is inconsistent with a facility for the separate adjustment of sleeve position.The results favour the theory that sleeve tendons have just one role, to counter the viscoelastic resistance of global fascia -ocular and sleeve muscle fibres acting in unison. Whether the fragile sleeve structure can meet the physical demands of pulleys is questionable; but otherwise the veracity of the pulley hypothesis cannot be assessed from the structural relations of muscles and fascia bulbi reported.

Three-Dimensional Kinematics at the Level of the Oculomotor Plant

“…Finally, some studies have claimed that the pulleys only serve passive orbital properties (Dimitrova et al, 2003) and that the orbital muscle fibers do not appear to terminate in the pulleys themselves (McClung et al, 2006), such that the pulleys are dragged along because of their physical attachment [rather than being actively and independently controlled (Miller, 1989)]. Still, other studies strongly dispute this latter claim, showing that orbital layers terminate in the pulleys of man and monkey (Ruskell et al, 2005). Thus, despite extensive evidence for differences in the activity-dependent properties of orbital and global layers, more studies are required to understand their neurophysiological and dynamic functional properties.…”

“…In addition to the numerous aforementioned anatomical and imaging studies showing pulleymediated position dependencies, support for this hypothesis has come from several studies that have found this type of muscle segregation in monkey, man, and other mammalian species (Khanna and Porter, 2001;Oh et al, 2001;Demer, 2004;Ruskell et al, 2005). In addition, differences in the types of muscle fibers projecting to either layer have also been noted (Collins, 1975;Spencer and Porter, 1981;Porter et al, 1995).…”

Mechanics of the Orbita

“…Each rectus orbital layer (OL) contains 40-60% of all the EOM's fibers. The OL terminates well posterior to the sclera, and at least some of its fibers insert on connective tissue pulleys [6,7]. The OL is located on the orbital surface of rectus EOMs, sometimes C shaped, and constitutes the concentric peripheral layer of the oblique EOMs.…”

How does the structure of extraocular muscles and their nerves affect their function?

“…46 These layers insert onto the globe and into fibromuscular structures, respectively, and hence subserve different functions in oculomotor control. 4,5 Although the facility for separate adjustments of these layers were argued to be limited in a previous histological study, 5 the global layer seems to provide the force for ocular rotation, while the orbital layer influences the muscle's direction of pull, as suggested in the pulley hypothesis. 47 This view has been elaborated in more recent studies, where it is promoted that the superior and inferior compartments of horizontal rectus muscles also can be controlled differently.…”

“…2 This has created controversy about the role of proprioception and has challenged the notion that it participates in the development of binocular vision, ocular alignment, and adaptive processes. 3 Furthermore, recent observations suggest that EOMs are compartmentalised, not only into global and orbital layers, 4,5 but also into superior and inferior compartments of horizontal rectus muscles. [6][7][8][9] This implies a broader division of labour between muscle segments than previously assumed, which in turn should require a highly structured and specific neural feedback.…”