Underdeveloped extraocular muscles in the naked mole rat (Heterocephalus glaber)

Abstract

The extraocular muscles (EOM) are the final effector arm of the ocular motor system. These small muscles have a unique embryological origin and phenotype. Their diversity is highlighted by their resistance to some neuromuscular disorders (muscular dystrophy, ALS) and increased susceptibility to others (myasthenia gravis and mitochondrial myophathies). The naked mole rat (NMR) is a subterranean rodent with a reduced visual system; it is an ideal model to examine the potential codependence of full EOM and visual system phenotype development and evolution. Our goal was to compare the structural features of NMR EOMs to those of a similar sized rodent with a fully developed visual system. Whole orbits and EOMs were dissected from perfusion-fixed adult NMR and C57BL mice and examined by light and electron microscopy. NMR orbital anatomy showed smaller EOMs in roughly the same distribution around the eye as in mouse and surrounded by a very small Harderian gland. The NMR EOMs did not appear to have the two-layer fiber distribution (orbital and global) seen in mouse EOMs; fibers were also significantly smaller (118 vs. 551 sq um in mouse EOMs). Myofibrillar density was less in NMR EOMs, and triad and other membranous structures were rudimentary. Finally, mitochondrial volume density was significantly less in NMR EOMs than in mouse EOM (4.5% vs. 21.2% respectively). These results demonstrate that NMR EOMs are smaller and less well organized than those in a rodent with a fully developed visual system. It is likely that at least some aspects of EOM organization depend on visual experience.