Abstract
Binocular vision requires intricate control of eye movement to align overlapping visual fields for fusion in the visual cortex, and each eye is controlled by 6 extraocular muscles (EOMs). Disorders of EOMs are an important cause of symptomatic vision loss. Importantly, EOMs represent specialized skeletal muscles with distinct gene expression profile and susceptibility to neuromuscular disorders. We aim to investigate and describe the anatomy of adult zebrafish extraocular muscles (EOMs) to enable comparison with human EOM anatomy and facilitate the use of zebrafish as a model for EOM research. Using differential interference contrast (DIC), epifluorescence microscopy, and precise sectioning techniques, we evaluate the anatomy of zebrafish EOM origin, muscle course, and insertion on the eye. Immunofluorescence is used to identify components of tendons, basement membrane and neuromuscular junctions (NMJs), and to analyze myofiber characteristics. We find that adult zebrafish EOM insertions on the globe parallel the organization of human EOMs, including the close proximity of specific EOM insertions to one another. However, analysis of EOM origins reveals important differences between human and zebrafish, such as the common rostral origin of both oblique muscles and the caudal origin of the lateral rectus muscles. Thrombospondin 4 marks the EOM tendons in regions that are highly innervated, and laminin marks the basement membrane, enabling evaluation of myofiber size and distribution. The NMJs appear to include both en plaque and en grappe synapses, while NMJ density is much higher in EOMs than in somatic muscles. In conclusion, zebrafish and human EOM anatomy are generally homologous, supporting the use of zebrafish for studying EOM biology. However, anatomic differences exist, revealing divergent evolutionary pressures.
Highlights
Zebrafish and humans both utilize six highly specialized extraocular muscles (EOMs) per eye to control the precise pursuit and saccade movements required to track moving items and maintain stable images on the retina for high acuity vision
The dorsal side of the adult zebrafish eye revealed a significant overlap of the superior rectus (SR) and superior oblique (SO; Figure 2C) at their common insertion site near the SC junction
A similar overlap of the inferior oblique (IO) and inferior rectus (IR) muscles appeared to take place on the ventral side of the globe (Figure 2D), but these muscles were not as visualized in vivo because it required rotating the eye to the point of stretching the muscles
Summary
Zebrafish and humans both utilize six highly specialized extraocular muscles (EOMs) per eye to control the precise pursuit and saccade movements required to track moving items and maintain stable images on the retina for high acuity vision. The sixth muscle, inferior oblique (IO), has a separate origin point on the orbital side of the bony maxilla at the anterior inferomedial strut. Each of these muscles has a distinct insertion site on the globe (Figure 1) and generates a unique primary rotation of the eye when acting alone. Coordinated contraction of the proper EOMs at the proper time allows humans to achieve binocular vision. This mode of vision provides stereoptic cues for depth perception and object size determination, but limits the range of the cumulative visual field
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