Inflection in Inactive Lateral Rectus Muscle: Evidence Suggesting Focal Mechanical Effects of Connective Tissues

The seminal x-ray tomographic observations of Simonsz1 and the magnetic resonance imaging (MRI) observations of Miller2 showed for the first time that extraocular muscles (EOMs) do not follow the shortest paths from their origins in the orbital apex to their insertions on the globe. It has subsequently emerged that connective tissue pulleys surround the rectus and inferior oblique EOMs at their points of perforation of posterior Tenon fascia.3,4 In secondary and tertiary gazes, at the locations of these pulley rings, the paths of the EOMs are inflected away from the shortest paths to their scleral insertions, which have been shifted by ocular rotation.5–8 Because the direction of force exerted on the globe is determined by EOM path direction at the point at which the EOM inserts on the globe, the inflections in the EOM path determine the directions of EOM force and produce a dependence of EOM pulling direction on instantaneous eye position.9–12 Because of systematic variation in EOM paths, pulling directions of rectus EOMs change with eye position so as to implement Listing’s law of ocular torsion,7 a robust kinematic feature of visually guided eye movements that has been shown not to be encoded in the neural commands to the EOMs normally regarded as having torsional actions.13 Conversely, pathologically abnormal paths14–17 or variations in EOM paths with gaze8 are associated with strabismus. It has been argued that specialized connective tissues, the pulleys, underlie the stability and gaze direction dependence of EOM paths because the sharp inflections in rectus and inferior oblique paths occur at the sites corresponding to the pulley rings. Rectus EOM pulleys, however, consist of more than focal pulley rings. The focal rings, consisting of dense,3,18,19 woven20 collagen reinforced by elastin3 and some adjacent smooth muscle,3,19,21 are embedded in an extensive sleeve with a much longer anteroposterior dimension along the EOM.4,18 The rings are roughly located at the anteroposterior midpoint of extensive tubular sleeves. The classical centrifugal bowing of rectus EOMs away from the orbital center, observed by Simonsz1 and Miller,2 does not correspond in location to the EOM path inflections due to the more anterior pulley rings.22 Given that centrifugal bowing of the rectus EOM path occurs farther posterior than the pulley rings, centrifugal bowing has a less significant potential effect on EOM pulling direction. In addition, given that this effect does not depend geometrically on eye rotational eye position, the kinematic consequences to EOM pulling direction are minimal. As a functional anatomic phenomenon, centrifugal rectus path bowing is nonetheless instructive. It has long been suggested that some inflection of EOM paths is caused by pressure on compartmentalized orbital fat.2,23,24 Quantitative histologic examination of the human orbit, however, does not suggest that the fat is compartmentalized into distinct “intraconal” and “extraconal” spaces that would seemingly be required to create the centrifugal gradient of fat pressure required to bow the rectus EOMs away from the orbital center.3 More recently, Schutte et al.24 have offered an alternative explanation for rectus EOM path behavior based on constraints caused by generally homogeneous and isotropic orbital fat, discounting the contribution of the pulleys or connective tissues entirely.24 Based on a finite element model of the mechanical properties that lumps together all the nonmuscular orbital tissues as intraconal fat or extraconal fat, Schutte et al.24 suggested that properties of the orbital fat may be responsible for the bowing and stability of rectus EOMs and that specialized connective tissue structures do not even stabilize EOM paths during gaze shifts. If, however, the orbit is effectively filled with only EOMs and “fat” not distinguished by focal mechanical properties, one would not anticipate the existence of abrupt direction changes in EOM paths not associated with substantial changes in EOM properties such as stiffness. It seems reasonable to assume that EOM cross-section would be an indicator of stiffness or resistance to deformation. Consequently, examination of path bowing could be informative about the uniformity of the mechanical properties of tissues surrounding an EOM and the relative mechanical contributions of surrounding orbital connective tissues to EOM paths. In theory, the location of centrifugal inflections in rectus EOM paths could be informative about the mechanical stiffness of the collagenous posterior pulley sleeve relative to EOM tension and the relative contribution of pressure from more distributed and homogeneous tissues such as loose orbital fat. In physiological situations, centrifugal EOM path bowing is a gradual and poorly localized phenomenon. The relative contributions of orbital fat and pulley tissues may be difficult to discriminate in the normal orbit in the absence of perturbations such as large ocular rotations. Different types of perturbation to normal anatomy are, therefore, instructive. The current report used MRI to characterize the more pronounced and localized centrifugal inflection of the paths of paralyzed, atrophic lateral rectus (LR) EOMs in humans with denervation myopathy and correlated path changes with the known anatomy of the pulley connective tissue system. A further control consisted of subjects with large-angle, nonparalytic esotropia in maximal adduction, which produces maximum physiological LR relaxation in the absence of denervation.