Evidence for Active Control of Rectus Extraocular Muscle Pulleys

PURPOSE. Connective tissue structures constrain paths of the rectus extraocular muscles (EOMs), acting as pulleys and serving as functional EOM origins. This study was conducted to investigate the relationship of orbital and global EOM layers to pulleys and kinematic implications of this anatomy. METHODS. High-resolution magnetic resonance imaging (MRI) was used to define the anterior paths of rectus EOMs, as influenced by gaze direction in living subjects. Pulley tissues were examined at cadaveric dissections and surgical exposures. Human and monkey orbits were step and serially sectioned for histologic staining to distinguish EOM fiber layers in relationship to pulleys. RESULTS. MRI consistently demonstrated gaze-related shifts in the anteroposterior locations of human EOM path inflections, as well as shifts in components of the pulleys themselves. Histologic studies of human and monkey orbits confirmed gross examinations and surgical exposures to indicate that the orbital layer of each rectus EOM inserts on its corresponding pulley, rather than on the globe. Only the global layer of the EOM inserts on the sclera. This dual insertion was visualized in vivo by MRI in human horizontal rectus EOMs. CONCLUSIONS. The authors propose the active-pulley hypothesis: By dual insertions the global layer of each rectus EOM rotates the globe while the orbital layer inserts on its pulley to position it linearly and thus influence the EOM's rotational axis. Pulley locations may also be altered in convergence. This overall arrangement is parsimoniously suited to account for numerous aspects of ocular dynamics and kinematics, including Listing's law. (Invest Ophthalmol Vis Sci. 2000;41: 1280 -1290 I nitial attempts to mathematically model binocular alignment showed the importance to extraocular muscle (EOM) action of EOM paths and the pivotal mechanical role of orbital connective tissues. The need for EOM path data motivated early radiographic studies in monkeys 1 and humans, 2 suggesting that paths of rectus EOMs are stabilized relative to the orbit. A decade ago, Miller 3 used relatively low-resolution MRI with three-dimensional (3-D) reconstruction to demonstrate stability of rectus EOM belly paths throughout the oculomotor range

Evidence for Active Control of Rectus Extraocular Muscle Pulleys

PURPOSE. Connective tissue structures constrain paths of the rectus extraocular muscles (EOMs), acting as pulleys and serving as functional EOM origins. This study was conducted to investigate the relationship of orbital and global EOM layers to pulleys and kinematic implications of this anatomy. METHODS. High-resolution magnetic resonance imaging (MRI) was used to define the anterior paths of rectus EOMs, as influenced by gaze direction in living subjects. Pulley tissues were examined at cadaveric dissections and surgical exposures. Human and monkey orbits were step and serially sectioned for histologic staining to distinguish EOM fiber layers in relationship to pulleys. RESULTS. MRI consistently demonstrated gaze-related shifts in the anteroposterior locations of human EOM path inflections, as well as shifts in components of the pulleys themselves. Histologic studies of human and monkey orbits confirmed gross examinations and surgical exposures to indicate that the orbital layer of each rectus EOM inserts on its corresponding pulley, rather than on the globe. Only the global layer of the EOM inserts on the sclera. This dual insertion was visualized in vivo by MRI in human horizontal rectus EOMs. CONCLUSIONS. The authors propose the active-pulley hypothesis: By dual insertions the global layer of each rectus EOM rotates the globe while the orbital layer inserts on its pulley to position it linearly and thus influence the EOM's rotational axis. Pulley locations may also be altered in convergence. This overall arrangement is parsimoniously suited to account for numerous aspects of ocular dynamics and kinematics, including Listing's law. (Invest Ophthalmol Vis Sci. 2000;41: 1280 -1290 I nitial attempts to mathematically model binocular alignment showed the importance to extraocular muscle (EOM) action of EOM paths and the pivotal mechanical role of orbital connective tissues. The need for EOM path data motivated early radiographic studies in monkeys 1 and humans, 2 suggesting that paths of rectus EOMs are stabilized relative to the orbit. A decade ago, Miller 3 used relatively low-resolution MRI with three-dimensional (3-D) reconstruction to demonstrate stability of rectus EOM belly paths throughout the oculomotor range

Compartmental Innervation of the Superior Oblique Muscle in Mammals

PURPOSE: Intramuscular innervation of mammalian horizontal rectus extraocular muscles (EOMs) is compartmental. We sought evidence of similar compartmental innervation of the superior oblique (SO) muscle. METHODS: Three fresh bovine orbits and one human orbit were dissected to trace continuity of SO muscle and tendon fibers to the scleral insertions. Whole orbits were also obtained from four humans (two adults, a 17-month-old child, and a 33-week stillborn fetus), two rhesus monkeys, one rabbit, and one cow. Orbits were formalin fixed, embedded whole in paraffin, serially sectioned in the coronal plane at 10-μm thickness, and stained with Masson trichrome. Extraocular muscle fibers and branches of the trochlear nerve (CN4) were traced in serial sections and reconstructed in three dimensions. RESULTS: In the human, the lateral SO belly is in continuity with tendon fibers inserting more posteriorly on the sclera for infraducting mechanical advantage, while the medial belly is continuous with anteriorly inserting fibers having mechanical advantage for incycloduction. Fibers in the monkey superior SO insert more posteriorly on the sclera to favor infraduction, while the inferior portion inserts more anteriorly to favor incycloduction. In all species, CN4 bifurcates prior to penetrating the SO belly. Each branch innervates a nonoverlapping compartment of EOM fibers, consisting of medial and lateral compartments in humans and monkeys, and superior and inferior compartments in cows and rabbits. CONCLUSIONS: The SO muscle of humans and other mammals is compartmentally innervated in a manner that could permit separate CN4 branches to selectively influence vertical versus torsional action

Effects of Intracranial Trochlear Neurectomy on the Structure of the Primate Superior Oblique Muscle

The diagnosis of superior oblique palsy is commonly invoked to explain acquired diplopia, but the clinical features of this form of cyclovertical strabismus are inconsistent and poorly understood. The primate model of acquired superior oblique palsy reported in this article provides surprising anatomic insights into the selective response of extraocular muscle layers to denervation and sheds light on some mysterious aspects of human superior oblique palsy

Compartmentalized Innervation of Primate Lateral Rectus Muscle

Innervation to monkey and human lateral rectus muscles is segregated into well-defined superior and inferior zones, so that the lateral rectus may function as two parallel muscles under separate control. Differential activation of the two lateral rectus zones could impart previously unrecognized torsional and vertical actions to this nominally “horizontal” rectus muscle, potentially resolving an important paradox in ocular kinematics

Intramuscular Innervation of Primate Extraocular Muscles: Unique Compartmentalization in Horizontal Recti

Segregation of intramuscular motor nerves indicates distinct superior and inferior zones within the horizontal but not vertical rectus extraocular muscles in humans and monkeys, supporting a potential functional role for differential innervation that might mediate oculorotary actions

Characterization of Ocular Tissues Using Microindentation and Hertzian Viscoelastic Models

Microindentation permits biomechanical characterization of small specimens of ocular tissues and demonstrates that although properties of periocular fatty tissues vary markedly by location, comparable bovine and human tissues behave similarly