Specific metabolic properties of rat oculorotatory extraocular muscles can be linked to their low force requirements.

Purpose: To gain insight into the metabolic pathways of oculorotatory extraocular muscle (EOM) fiber types at the cellular level to explain their high fatigue resistance, rapid contraction, and low force output.

Methods: In consecutive sections of adult rat EOMs, the cross-sectional area (CSA) was calculated, and the activities of succinate-dehydrogenase (SDH) and alpha-glycerophosphate dehydrogenase (GPDH) were measured by quantitative histochemistry of different fiber types classified by the myofibrillar adenosine triphosphatase (mATPase) staining pattern.

Results: In the orbital regions, type 1 (fast) fibers were present, showing small CSA, medium SDH, and low GPDH activity. The type 2 (slow) fibers exhibited extremely small CSA and low SDH and GPDH activity. In the global region, fast types 3 to 5 fibers were found, forming a continuum with an inverse correlation between CSA and enzyme activity. SDH and GPDH activity showed an unusual positive relationship in contrast to the skeletal muscle fiber types. The type 6 fibers were slow forming a close and clearly separated group with medium CSA and extremely low SDH and low GPDH activity.

Conclusions: Muscle fibers in adult rat EOMs show unique metabolic properties not seen in other skeletal muscles, covering their extraordinary functional demands. It can be speculated that the EOMs embedded within the orbit material do not need to perform with high force, and therefore they could develop extensive systems that ensure both fatigue resistance (many mitochondria) and fast contraction with high mATPase activity (a well-developed sarcotubular system).