Composition, architecture, and functional implications of the connective tissue network of the extraocular muscles

Linda K. McLoon, André Vicente, Krysta R. Fitzpatrick, Mona Lindström, Fatima Pedrosa Domellöf

Research output: Contribution to journalArticlepeer-review

7 Scopus citations

Abstract

PURPOSE. We 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. METHODS. Human 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. RESULTS. Collagens 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. CONCLUSIONS. A 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.

Original languageEnglish (US)
Pages (from-to)322-329
Number of pages8
JournalInvestigative Ophthalmology and Visual Science
Volume59
Issue number1
DOIs
StatePublished - Jan 2018

Bibliographical note

Funding Information:
The authors thank the Cheng Choo Nikki Lee for technical assistance and the facilities of the Umeå Core Facility Electron Microscopy (UCEM) at the Chemical Biological Centre (KBC), Umeå University. Supported by grants from the Swedish Research Council (2015- 02438; Stockholm, Sweden), County Council of Västerbotten (Umeå, Sweden), Ögonfonden (Umeå, Sweden), Kronprinsessan Margaretas Arbetsnämnd för Synskadade (Valdemarsvik, Sweden), and The Medical Faculty, Umeå University (Umeå, Sweden); National Eye Institute Grant RO1 EY15313 (LKM), National Institute of Health grant P30 EY11375, the Minnesota Lions Foundation, and an unrestricted grant to the Department of Ophthalmology from Research to Prevent Blindness, Inc.

Funding Information:
Supported by grants from the Swedish Research Council (2015-02438; Stockholm, Sweden), County Council of Västerbotten (Umeå, Sweden), Ögonfonden (Umeå, Sweden), Kronprinsessan Margaretas Arbetsnämnd för Synskadade (Valdemarsvik, Sweden), and The Medical Faculty, Umeå University (Umeå, Sweden); National Eye Institute Grant RO1 EY15313 (LKM), NIH grant P30 EY11375, the Minnesota Lions Foundation, and an unrestricted grant to the Department of Ophthalmology from Research to Prevent Blindness, Inc.

Publisher Copyright:
© 2018 The Authors.

Copyright:
Copyright 2018 Elsevier B.V., All rights reserved.

Keywords

  • Collagen
  • Connective tissue
  • Epimysium
  • Extraocular muscles
  • Muscle force
  • Perimysium
  • Scanning electron microscopy

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