Morphogenesis of the Extraocular Muscles During the Human Embryonic and Early Fetal Periods

Previous histological studies have shown that the extraocular muscles (EOMs) within the orbit are unique among skeletal muscles in both developmental origin and timing. However, three-dimensional (3D) morphological information and quantitative growth data remain limited. This study aimed to reconstruct 3D images of the EOMs during the human embryonic and early fetal periods (crown-rump length, 20-86 mm) using magnetic resonance imaging (MRI) data and quantify their growth. In specimens from the late embryonic period, all six EOMs controlling eye movement were recognizable on MRI and could be segmented for morphological analysis. The five EOMs originating from the common tendinous ring appeared to become closer as they widened during growth. Overall, the basic morphology of each EOM was broadly maintained from the late embryonic to early fetal period, with the most prominent change observed in the superior oblique muscle (SOM), whose bending angle at the trochlea changed from nearly rectangular at the end of the embryonic period to acute during the early fetal period. The lateral rectus muscle showed the largest volume and mean cross-sectional area among the EOMs in the early fetal period. Mean cross-sectional area increased at a similar rate among the four rectus muscles, but less in the inferior oblique muscle and much less in the SOM. Growth of each EOM strongly correlated with eyeball growth. These findings suggest that the four rectus muscles grow in a coordinated manner, whereas the oblique muscles follow distinct growth patterns during early orbital development.