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 journalArticle

2 Citations (Scopus)

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 1 2018

Fingerprint

Oculomotor Muscles
Connective Tissue
Collagen
Muscles
Elastin
Laminin
Tissue Distribution
Fibronectins
Electron Scanning Microscopy
Basement Membrane
Immunohistochemistry
Rabbits

Keywords

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

PubMed: MeSH publication types

  • Journal Article
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

Cite this

Composition, architecture, and functional implications of the connective tissue network of the extraocular muscles. / McLoon, Linda K.; Vicente, André; Fitzpatrick, Krysta R.; Lindström, Mona; Pedrosa Domellöf, Fatima.

In: Investigative Ophthalmology and Visual Science, Vol. 59, No. 1, 01.01.2018, p. 322-329.

Research output: Contribution to journalArticle

McLoon, Linda K. ; Vicente, André ; Fitzpatrick, Krysta R. ; Lindström, Mona ; Pedrosa Domellöf, Fatima. / Composition, architecture, and functional implications of the connective tissue network of the extraocular muscles. In: Investigative Ophthalmology and Visual Science. 2018 ; Vol. 59, No. 1. pp. 322-329.
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AU - Vicente, André

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AB - 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.

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KW - Epimysium

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KW - Muscle force

KW - Perimysium

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