Skip to main content
SpringerLink
Log in

Extraocular muscles light microscopy and ultrastructural features

  • Original Investigations
  • Published:
Acta Neuropathologica Aims and scope Submit manuscript

Summary

Thirty extraocular muscles (EOM) from 20 patients were evaluated by light microscopy (LM), electron microscopy (EM), and enzyme histochemistry (EZH). Twenty-one EOM were obtained from 13 patients with strabismus, 9 EOM from 4 patients undergoing eye surgery for other reasons and from 3 autopsy cases. One μm thick sections revealed marked variation in muscle fibre shape and size and in myofibrillar structure; also noted were small, hypertrophied, whorled, and ringbinden fibres. Dense and granular material in the central portion of some fibres and sarcomere disruption in 2–3 μm sections was observed. EZH revealed the absence of the classical mosaic pattern usually found in skeletal muscles. ATPase studies were inconsistent and did not correlate with the expected reciprocal activity of NAD-H diaphorase, particularly on the large fibres.

Ultrastructural features consisted of vacuoles within myofilament bundles, “smearing” of Z bands, and “nemaline rods”. Occasional myelin figures and lipid-like droplets were observed in subsarcolemmal spaces, associated with scattered clusters of glycogen granules. Abnormal mitochondria and subsarcolemmal inclusions of dense and granular material were conspicuous. “Leptomeric” profiles, “Zebra bodies”, or “striated bodies” were noted in 8 EOM's, and an Hirano body was found in 1. The intramuscular nerves contained structures resembling “Luse bodies” in 7 cases.

These observations suggest that EOM from individuals with and without strabismus possess unique structural characteristics suggestive of developmental and morphological disarrangement of contractile elements. Some of these changes might play a role in the pathogenesis of strabismus and in the development of clinical symptoms.

These features are significantly different from striated skeletal muscle. Therefore the criteria used in the pathological evaluation and diagnosis of skeletal muscle disorders cannot be unequivocally applied to EOM investigations. These data establish the necessity to determine histological norms, ultrastructural patterns, and develop new enzyme histochemistry criteria for the evaluation of EOM. Only then can an acceptable comparison of EOM and skeletal muscle be made.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Adachi, M., Torii, J., Vold, B. W., Briet, P., Wolintz, A., Schneck, L.: Electron microscopic and enzyme histochemical studies of cerebellum, ocular and skeletal muscles in chronic progressive ophthalmoplegia with cerebellar ataxia. Acta neuropath. (Berl.)23, 300–312 (1973)

    Google Scholar 

  2. Aichmair, H., Mayr, R.: Electron microscopic study of the mitochondria in extraocular muscles of squinting eyes. Albrecht v. Graefes Arch. klin. exp. Ophthal.186, 45–54 (1973)

    Google Scholar 

  3. Alberca, R., Coca, M. C., Gil Peralta, A., Gómez-Bosque, P., Navarro, A.: Miopatía ocular familiar. (Estudio Inmunoelectroforético y de Microscopía Electrónica). Rev. clín. esp.,123, 45–52 (1971)

    Google Scholar 

  4. Allen, R. D., David, G. B., Nomarski, G.: The Zeiss-Nomarski differential interference equipment for transmitted-light microscopy. Z. wiss. Mikr.69, 193–221 (1969)

    Google Scholar 

  5. Bach y Rita, P.: Personal communication (1975)

  6. Brandt, D. E., Lesson, C. R.: Structural differences of fast and slow fibers in human extraocular muscle. Amer. J. Ophthal.62, 478–487 (1966)

    Google Scholar 

  7. Caesar, R., Edwards, G. A., Ruska, H.: Electron microscopy of the impulse conducting system of the sheep heart. Z. Zellforsch.48, 698–719 (1958)

    Google Scholar 

  8. Casanova, P.: Techniques de coloration des tissus osmiés et inclu dans l'araldite ou l'epon. Ann. Anat. path.19, 2231–243 (1974)

    Google Scholar 

  9. Corvaja, N., Marinozzi, V., Pompeiano, O.: Muscle spindles in the lumbrical muscles of the adult cat: Electron microscopic observations and functional considerations. Arch. ital. Biol.107, 365–543 (1969)

    Google Scholar 

  10. Culebras, A., Merk, F. B.: Cytoplasmic inclusion bodies in superior rectus muscle of the eye. Neurology (Minneap.)25, 422–429 (1975)

    Google Scholar 

  11. Dahl, D. S., Klutzow, F. W.: Congenital rod disease. Further evidence of innervational abnormalities as the basis for the clinicopathologic features. J. neurol. Sci.23, 371–385 (1974)

    Google Scholar 

  12. Davidowitz, J., Philips, G. H., Pachter, B. R., Breinin, G. M.: Particle-free and glycogen bearing double membrane arrays in extraocular muscle of rabbit. Amer. J. Path.78, 191–196 (1975)

    Google Scholar 

  13. Drachman, D. A.: Ophthalmoplegia plus. The neurodegenerative disorders associated with progressive external ophthalmoplegia. Arch. Neurol. (Chic.)18, 654–674 (1968)

    Google Scholar 

  14. Drachman, D. A., Wetzel, N., Wasserman, M., Naito, H.: Experimental denervation of ocular muscles. A critique on the concept of “Ocular Myopathy”. Arch. Neurol. (Chic.)21, 170–183 (1969)

    Google Scholar 

  15. Engel, W. K.: Fiber-type nomenclature of human skeletal muscle for histochemical purposes. Neurology (Minneap.)24, 344–348 (1974)

    Google Scholar 

  16. Engel, W. K., Cunningham, G. C.: Rapid examination of muscle tissue. An improved trichrome method for fresh-frozen biopsy sections. Neurology (Minneap.)13, 919–929 (1963)

    Google Scholar 

  17. Fisher, E. R., Vuzevski, V. D.: Cytogenesis of Schwannoma (Neurilemoma), Neurofibroma, Dermatofibroma and Dermatofibrosarcoma as revealed by electron microscopy. Amer. J. clin. Path.49, 141–154 (1968)

    Google Scholar 

  18. Gruner, J. E.: La structure fine du fuseau neuromusculaire humain. Rev. neurol.104, 490–507 (1961)

    Google Scholar 

  19. Hirano, A.: Pathology of amyotrophic lateral sclerosis. In: Slow latent and temperate virus infections: NINDB monograph No. 2 pp. 23–37 (eds. D. C. Gajdusek and C. L. Gibbs). Bethesda National Institutes of Health (1965)

  20. Johnson, E. A., Sommer, J. R.: A strand of cardiac muscle. Its ultrastructure and the electrophysiological implications of its geometry. J. Cell Biol.33, 103–129 (1967)

    Google Scholar 

  21. Karlsson, U., Andersson-Cedergren, E.: Small leptomeric organelles in intrafusal muscle fibers of the frog as revealed by electron microscopy. J. Ultrastruct. Res.23, 417–426 (1968)

    Google Scholar 

  22. Katz, B.: The terminations of the afferent nerve fiber in the muscle spindle of the frog. Phil. Trans. B243, 221 (1961)

    Google Scholar 

  23. Koerner, F., Schlote, W.: Chronic progressive external ophthalmoplegia. Association with retinal pigmentary changes and evidence in favor of ocular myopathy. Arch. Ophthal.88, 155–166 (1972)

    Google Scholar 

  24. Kroll, A. J., Kuwabara, T.: The fine structure of dysthyroid ocular myopathy. Proceeding 20th Int. Congress Ophthal. Munich Int. Congress Series 146, pp. 1137–1144, (ed. E. Weigelin) Amsterdam: Excerpta Medica 1966

    Google Scholar 

  25. Lake, B. D., Wilson, J.: Zebra body myopathy: Clinical, histochemical and ultrastructural studies. J. neurol. Sci.24, 437–446 (1975)

    Google Scholar 

  26. Luse, S. A.: Electron microscopic studies of brain tumors. Neurology (Minneap.)10, 881–905 (1960)

    Google Scholar 

  27. Mair, W. G. P., Tomé, F. M. S.: Atlas of the ultrastructure of diseased human muscle. Edinburgh: Churchill-Livingstone 1972

    Google Scholar 

  28. McLeod, J. G., Baker, W. DeC., Shorey, C. D., Kerr, C. B.: Mitochondrial myopathy with multisystem abnormalities and normal ocular movements. J. neurol. Sci.24, 39–52 (1975)

    Google Scholar 

  29. Miller, J. E.: Recent histologic and electron microscopic findings in extraocular muscle. Trans. Amer. Acad. Ophthal. Otolaryng.75, 1175–1185 (1971)

    Google Scholar 

  30. Minoda, K.: Histochemical and electron microscopic studies of extraocular muscles: IV. Fine structure of neuropathic extraocular muscles. Acta Soc. Ophthal. Jap.75, 1184–1195 (1971)

    Google Scholar 

  31. Morgan-Hughes, J. A., Mair, W. G. P.: Atypical muscle mitochondria in oculoskeletal myopathy. Brain96, 215–224 (1973)

    Google Scholar 

  32. Mori, M.: Striated annular-fibers in ocular muscle. Arch. Histologicum Jap.5, 485–488 (1953)

    Google Scholar 

  33. Mukuno, K.: The fine structures of the human extraocular muscles. (1). A “Laminated Structure” in the muscle fibers. J. Electron Micr.15, 4, 227–236 (1966)

    Google Scholar 

  34. Mukuno, K.: Electron microscopic studies on the human extraocular muscles under pathologic conditions. Part 1. Rod formation in normal and diseased muscles (Polymyositis and Ocular Myasthenia), Jap. J. Ophthal.13, 35–51 (1969)

    Google Scholar 

  35. Mukuno, K.: Fine structures of the human extraocular muscles with special reference to ring band, rod-like structures, and satellite cells. Advance Neurol. Invest.14, 508–514 (1970)

    Google Scholar 

  36. Mukuno, K.: Chronic progressive ophthalmoplegia (CPEO) clinical features and histopathology of the extraocular muscles. Neurosurgery2, 529–535 (1974)

    Google Scholar 

  37. Novikoff, A. B., Shin, W. Y., Drucker, J.: Mitochondrial localization of oxidative enzymes: Staining results with two tetrazolium salts. J. biophys. biochem. Cytol.9, 47–61 (1961)

    Google Scholar 

  38. Padykula, H. A., Herman, E.: Specificity of the histochemical method for adenosine triphosphatase. J. Histochem. Cytochem.3, 170–195 (1955)

    Google Scholar 

  39. Pachter, B. R., Davidowitz, J., Breinin, G. M.: A light and electron microscopic study in serial reactions of dystrophic extraocular muscles. Invest. Ophthal.2, 917–923 (1974)

    Google Scholar 

  40. Peachy, L. D., Takeichi, M., Nag, A. C.: Muscle fiber types and innervation in adult cat extraocular muscles. In: Exploratory concepts in muscular dystrophy. II. Proceeding of an International Conference, Carefree, Arizona, October 15–19, 1973, pp. 246–257 (ed. A. T. Milhorat). Amsterdam: Excerpta Medica 1974

    Google Scholar 

  41. Ogata, J., Budzilovich, G. N., Cravioto, H.: A study of rodlike structures (Hirano bodies) in 240 normal and pathological brains. Acta neuropath. (Berl.)21, 61–67 (1972)

    Google Scholar 

  42. Ovalle, W. K.: Fine structure of rat intrafusal muscle fibers. The equatorial region. J. Cell Biol.52, 382–396 (1972)

    Google Scholar 

  43. Radnót, M., Follman, P.: Ultrastructural changes in senile atrophy of the orbicularis oculi muscle. Amer. J. Ophthal.78, 689–699 (1974)

    Google Scholar 

  44. Raimondi, A. J., Mullan, S., Evans, J. P.: Human brain tumors. An electronmicroscopic study. J. Neurosurg.19, 731–753 (1962)

    Google Scholar 

  45. Rebeiz, J. J., Caulfield, J. B., Adams, R. D.: Oculopharyngeal dystrophy. A presenescent myopathy: A clinico-pathologic study. Int. Congress of Neurogenetics. Progress in Neuroophthalmology (ed. J. R. Brunette) Vol. 2, pp. 12–31 (1967)

    Google Scholar 

  46. Rumpelt, H. J., Schmalbruch, H.: Zur Morphologie der Bauelemente von Muskelspindeln bei Mensch und Ratte. Z. Zellforsch.102, 601–630 (1969)

    Google Scholar 

  47. Ruska, H., Edwards, G. A.: A new cytoplasmic pattern in striated muscle fibers and its possible relation to growth (1957)

  48. Sakimoto, T.: Electron microscopic studies on human ocular muscles. (1). Filamentous and membranous structures in the extraocular muscle fibers. Acta Soc. Ophthal. Jap.72, 175–189 (1968)

    Google Scholar 

  49. Sakimoto, T.: Fine structure of extraocular muscle with myasthenia gravis. Jap. J. Ophthal.14, 60–72 (1970)

    Google Scholar 

  50. Sakimoto, T.: Descending ocular myopathy, electron microscopic studies on human ocular muscles, III. Fine structural findings in extraocular muscles with descending ocular myopathy. Acta Soc. Ophthal. Jap.75, 748–764 (1971)

    Google Scholar 

  51. Schneck, L., Adachi, M., Briet, P., Wolintz, A., Volk, B. W.: Ophthalmoplegia plus with morphological and chemical studies of cerebellar and muscle tissue. J. neurol. Sci.19, 37–44 (1973)

    Google Scholar 

  52. Shy, G. M., Engel, W. K., Somers, J. E., Wanko, T.: Nemaline myopathy. A new congenital myopathy. Brain86, 793–810 (1963)

    Google Scholar 

  53. Sulaiman, W. R., Doyle, D., Johnson, R. H., Jennett, S.: Myopathy with mitochondrial inclusion bodies: Histological and metabolic studies. J. Neurol. Neurosurg. Psychiat.37, 1236–1246 (1974)

    Google Scholar 

  54. Sun, C. N., White, H. J.: An electron-microscopic study of a schwannoma with special reference to banded structures and peculiar membranous multiple-chambered spheroids. J. Path.114, 13–16 (1974)

    Google Scholar 

  55. Thomas, C., Spielmann, A.: Revue du strabisme. Arch. Ophtal. (Paris)34, 513–528 (1974)

    Google Scholar 

  56. Toga, M., Bérard-Badier, M., Gambarelli, D., Pinsard, N., Hassoun, J.: Un cas de dystrophie neuroaxonale infantile ou maladie de Seitelberger, III. Étude ultrastructurale du muscle strié. Acta neuropath. (Berl.)18, 327–341 (1971)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pathology, (Division of Neuropathology) Medical College of Virginia, Virginia Commonwealth University, Health Sciences Division, Box 17, Richmond, Virginia, 23298, USA

    A. Julio Martinez, Sam Hay & Keith W. McNeer

  2. DDepartment of Ophthalmology, Medical College of Virginia, Virginia Commonwealth University, Health Sciences Division, 23298, Richmond, Virginia, USA

    A. Julio Martinez, Sam Hay & Keith W. McNeer

Authors
  1. A. Julio Martinez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sam Hay
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Keith W. McNeer
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martinez, A.J., Hay, S. & McNeer, K.W. Extraocular muscles light microscopy and ultrastructural features. Acta Neuropathol 34, 237–253 (1976). https://doi.org/10.1007/BF00688678

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00688678

Key words

Search

Navigation