The orbital layer of each rectus extraocular muscle (EOM) inserts on connective tissue, and the global layer inserts on the eyeball. The active-pulley hypothesis (APH) proposes that a condensation of this connective tissue constitutes a pulley serving as the functional origin of the rectus EOM, and that this pulley makes coordinated, gaze-related translations along the EOM axis to implement a linear ocular motor plant. This study was designed to measure gaze-related shifts in EOM pulley locations. Magnetic resonance imaging (MRI) was performed in eight normal volunteers in 2-mm thickness coronal planes perpendicular to the orbital axis for nine cardinal gaze directions. Intravenous gadodiamide contrast was administered to define EOM tendons anterior to the globe equator. Paths of EOMs, defined by their area centroids, were transformed into an oculocentric coordinate system. Sharp inflections in EOM paths in secondary and tertiary gaze positions defined pulley locations which were then correlated with gaze direction and compared with theoretical predictions. Rectus pulley positions were consistent with a central primary position. In tertiary gaze positions, each of the four rectus pulleys translated posteriorly with EOM contraction and anteriorly with EOM relaxation by a significant (P < 0.02) amount predicted by the APH, but more than 100 times greater than the translation predicted by a passive pulley model. The APH prediction of coordinated anteroposterior shifting of EOM pulleys with gaze is quantitatively supported by changes in EOM path inflections among tertiary-gaze positions. Human rectus pulleys move to shift the ocular rotational axis to attain commutative behavior of the ocular motor plant.