Composition, Architecture, and Functional Implications of the Connective Tissue Network of the Extraocular Muscles

Abstract

PurposeWe examined the pattern and extent of connective tissue distribution in the extraocular muscles (EOMs) and determined the ability of the interconnected connective tissues to disseminate force laterally.MethodsHuman EOMs were examined for collagens I, III, IV, and VI; fibronectin; laminin; and elastin using immunohistochemistry. Connective tissue distribution was examined with scanning electron microscopy. Rabbit EOMs were examined for levels of force transmission longitudinally and transversely using in vitro force assessment.ResultsCollagens I, III, and VI localized to the endomysium, perimysium, and epimysium. Collagen IV, fibronectin, and laminin localized to the basal lamina surrounding all myofibers. All collagens localized similarly in the orbital and global layers throughout the muscle length. Elastin had the most irregular pattern and ran longitudinally and circumferentially throughout the length of all EOMs. Scanning electron microscopy showed these elements to be extensively interconnected, from endomysium through the perimysium to the epimysium surrounding the whole muscle. In vitro physiology demonstrated force generation in the lateral dimension, presumably through myofascial transmission, which was always proportional to the force generated in the longitudinally oriented muscles.ConclusionsA striking connective tissue matrix interconnects all the myofibers and extends, via perimysial connections, to the epimysium. These interconnections are significant and allow measurable force transmission laterally as well as longitudinally, suggesting that they may contribute to the nonlinear force summation seen in motor unit recording studies. This provides strong evidence that separate compartmental movements are unlikely as no region is independent of the rest of the muscle.

Changing muscle function with sustained glial derived neurotrophic factor treatment of rabbit extraocular muscle

“…It is possible that increased myofiber remodeling may result in increased numbers of short myofibers. This would be predicted to result in greater lateral dissipation of muscle force, which is already significant in EOM [ 47 – 49 ]. It is interesting to note that experimental recession surgery in adult rabbits resulted in a significant increase in myonuclear addition as visualized by bromodeoxyuridine labeling [ 50 ].…”

Instead of pulley bands, does retrobulbar fat keep the eye muscle bellies in place and thereby act like a pulley?

“…However, McLoon et al found significant interconnectedness of the connective-tissue elements with all the muscle fibers along the whole length of the muscle, including direct connection into the epimysium, strongly suggesting that individual isolated movements of compartments within the EOM are unlikely. 27 Fat with enveloping connective-tissue sheets keeps the muscle belly in place…”

EOM Pulleys and Sequelae: A Critical Review

“…The extraordinary fiber independence reported by Shin et al could be due to epimysium having been stripped off, damaging the connective tissue matrix that normally couples fibers, 36 and to the experimental procedure itself, in which connective tissues joining adjacent fibers were subjected to shear forces far exceeding those they normally sustain. A related study of tendon fiber independence 37 drew a similar, independent critique, complaining that muscle samples had been denuded of ''key surrounding structures'' and subjected to supraphysiologic forces, also citing surgical Z-tenotomy data inconsistent with fiber independence.…”

“…38 If EOMs were composed of parallel independent fibers their total force would be the sum of forces of the individual fibers, which several lines of evidence show is not the case. 33,[39][40][41] McLoon et al 36 showed that epimysium, perimysium, and endomysium of human EOMs form a dense and continuous collagen matrix, with no separations between any muscle regions, limiting relative fiber movements of any kind. Alan B. Scott (personal communication, 2018) sought to selectively ablate OL to weaken primary position forces without impairing eccentric gaze or saccades, but could find no natural laminar cleavage in the horizontal recti of cats, rabbits, or monkeys, even with sharp dissection and laser ablation.…”