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Biomechanics of Compartmentalized Mechanical Properties of Extraocular Muscle and Tendon

Abstract

A controversial issue in the eye movement field involves the compartmentalization of extraocular muscle (EOM). Conventionally, it has been believed that each individual EOM is innervated uniformly by its motor nerve, and behaves uniformly. However, recent studies have revealed that motor nerves innervating horizontal rectus EOMs are bifurcated into two divisions that control, respectively, the superior and inferior zones of muscle fibers. This finding has motivated the proposition that each of the two compartments of these EOMs might be controlled independently, so that each EOM could behave as it were two parallel but independent actuators. The compartmental independence postulate requires a mechanically low degree of transverse force coupling among parallel EOM and extraocular tendon (EOT) fibers. This project aimed to employ biomechanical characterization to EOM and EOT to test the plausibility of this hypothesis.

The first study described the biomechanical characterization of EOT, in both at the level of individual fibers and whole tendon. Nano indentation of EOT fiber bundles analyzed within the Hertzian framework effectively characterized the transverse Young's modulus for bovine EOT fiber bundles using atomic force microscopy (AFM). A precise estimate of the Poisson ratio (PR) of bovine EOTs was calculated using optical coherence tomography (OCT) during tensile loading.

The second study investigated mechanical potential for independent compartmental behavior in EOM and EOT. Extensive experimental study was performed to examine the passive mechanical interaction between sets compartments using a custom fabricated dual channel micro-tensile load cell. Independent active contractile behavior of EOM compartments was also examined using calcium-induced EOM contraction. Both passive loading and active contraction findings indicate that EOM and tendon have a high degree of biomechanical independence, sufficient to support the proposed functional diversity of actions in distinct neuromuscular compartments of the horizontal rectus EOMs.

Finally, biomechanical effects of Z-tenotomy and Z-myotomy, surgical techniques employing transverse incisions for EOT or EOM weakening to correct strabismus (misalignment of the eyes), were characterized using tensile loading. Both Z-tenotomy and Z-myotomy demonstrated minimal shear force coupling, which confirms and extends the findings of independent compartmental behavior in second study, and explains the surgical effects of the procedure. Additional viscoelastic characterization was performed using EOM specimens.

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