Quantitative analysis of the structure of the human extraocular muscle pulley system

Abstract

Purpose: Extraocular muscle (EOM) paths are constrained by connective tissue pulleys serving as functional origins. The quantitative structural features of pulleys and their intercouplings and orbital suspensions remain undetermined. This study was designed to quantify the composition of EOM pulleys and suspensory tissues.

Methods: Five human orbits, ages 33 weeks gestation to 93 years, were imaged intact by magnetic resonance (MRI), serially sectioned at 10 micro m thickness, and stained for collagen, elastin, and smooth muscle (SM). With MRI used as a reference, digital images of sections were geometrically corrected for shrinkage and processing deformations, and normalized to standard normal adult globe diameter. EOM pulleys, interconnections, suspensory tissues, and entheses were quantitatively analyzed for collagen, elastin, and SM thickness and density.

Results: Rectus and inferior oblique pulleys had uniform structural features in all specimens, comprising a dense EOM encirclement by collagen 1 to 2 mm thick. Elastin distribution varied, but was greatest in the orbital suspension of the medial rectus pulley and in a band from it to the inferior rectus pulley. This region corresponded to maximum SM density. Structural features of pulleys, intercouplings, and entheses were similar among specimens. The major mechanical couplings to the osseous orbit were near the medial and lateral rectus pulleys.

Conclusions: Quantitative analysis of structure and composition of EOM pulleys and their suspensions is consistent with in vivo MRI observations showing discrete inflections in EOM paths that shift predictably with gaze. Focal SM distributions in the suspensions suggest distinct roles in stiffening as well as shifting rectus pulleys.