Skip to main content
Log in

Ballooning of myelin sheaths in normally aged macaques

  • Published:
Journal of Neurocytology

Abstract

In aged animal brains, a variety of holes are formed in the neuropil. One type of hole, here designated as the myelin balloon, is an abnormality of the myelin sheath and is found in a number of diverse sites in the brain. Profiles of myelin balloons display rather smoothly rounded peripheral contours and typically range up to 10 μm in diameter, although exceptionally large examples may be twice this size. The balloons are bounded by lamellae of myelin, and to accommodate the contents of the balloon, the myelin sheath becomes split at the intraperiod line. Since the intraperiod line is formed by the apposition of the outer faces of the myelin-forming plasma membrane, the contents of the myelin balloons are, in effect, in continuity with the extracellular space, and it is suggested that the contents of the balloons are fluid, with the fluid exerting an outward pressure on the walls of the balloons to produce their spherical shapes. Myelin balloons are not only produced during aging but also occur in a number of genetic strains of mice and in a number of human disease states. They thus represent a non-specific, though distinctive and common, alteration of the myelin sheath and are a reflection of the fact that under a variety of conditions, including normal aging, oligodendrocytes are unable to maintain the integrity of their sheaths.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anderson, T.J., Schneider, A., Barrie, J.A., Klugmann, M., McCulloch, M.C., Kirkham, D., Kyriades, E., Nave, K.A. & Griffiths, I.R. (1998) Late-onset neurodegeneration in mice with increased dosage of the proteolipid protein gene. Journal of Comparative Neurology 394, 506–19.

    Article  CAS  Google Scholar 

  • Blakemore, W.F. (1978) Observations on remyelination in the rabbit spinal cord following demyelination induced by lysolecithin. Neuropathology and Applied Neurobiology 4, 47–59.

    Article  CAS  Google Scholar 

  • Coetzee, T., Fujita, N., Dupree, J., Shi, R., Blight, A., Susuki, K. & Popko, B. (1996) Myelination in the absence of galactocerebroside and sulfatide: normal structure with abnormal function and regional instability. Cell 86, 209–219.

    Article  CAS  Google Scholar 

  • Coetzee, T., Susuki, K. & Popko, B. (1998) New perspectives on the function of myelin galactolipids. Trends in Neuroscience 21, 126–30.

    Article  CAS  Google Scholar 

  • Czibulka, A. & Schwartz, I. R. (1993) Glial or neuronal origin of microcysts in the gerbil PVCN? Hearing Research 67, 1–12.

    Article  CAS  Google Scholar 

  • Duncan, I. D., Hammang, J. P. & Trapp, B. D. (1987) Abnormal compact myelin in the myelin-deficient rat. Absence of proteolipid protein correlates with a defect in the intraperiod line. Proceedings of the National Academy of Science USA 84, 6287–91.

    Article  CAS  Google Scholar 

  • Faddis, B. T. & McGinn, M. D. (1997) Spongiform degeneration of the gerbil cochlear nucleus: an ultrastructural and immunohistochemical evaluation. Journal of Neurocytology 26, 625–35.

    Article  CAS  Google Scholar 

  • Feldman, M. L. (1994) Neuropil ″holes″ in auditory and non-auditory structures of aged macaques and aged rats. Association for Research in Otolaryngology 17, 27.

    Google Scholar 

  • Feldman, M. L. & Vaughan, D. W. (1979) Changes in the auditory pathway with age. In: Special Senses in Aging (edited by Han, S.S. & Coons, D.H.), pp. 143–62. Ann Arbor: University of Michigan Press.

    Google Scholar 

  • Felts, P.A., Baker, T.A. & Smith, K.J. (1997) Conduction in segmentally demyelinated mammalian central axons. Journal of Neuroscience 17, 7267–77.

    Article  CAS  Google Scholar 

  • Gutierrez, R., Boison, D., Heinemann, U. & Stoffel, W. (1995) Decompaction of CNS myelin leads to a reduction of the conduction velocity of action potentials in optic nerve. Neuroscience Letters 195, 93–6.

    Article  CAS  Google Scholar 

  • Hildebrand, C. (1982) Electron-microscopic identification of Gomori-positive rings in normal spinal cord white matter. Acta Neuropathologica (Berlin) 56, 29–34.

    Article  CAS  Google Scholar 

  • Hirano, A. (1969) The fine structure of the brain in edema. In: The Structure and Function of Nervous Tissue, vol.II (edited by Bourne, G.H.), pp. 69–135. New York: Academic Press.

    Google Scholar 

  • Hirano, A. (1981) A Guide to Neuropathology. New York: Igaku-Shoin.

    Google Scholar 

  • Hoeffding, V. & Feldman, M.L. (1988) Changes with agein the morphology of the cochlear nerve in rats: light microscopy. Journal of Comparative Neurology 276, 537–46.

    Article  CAS  Google Scholar 

  • KAE S , T. (1907)Die grosshirnrinde des Menschen in ihren Mas-sen und in ihrem Fasergehalt. Jena: Gustav Fischer.

  • Kemper, T. L. (1994) Neuroanatomical and neuropathological changes during aging and dementia. In: Clinical Neurology of Aging (edited by Albert, M.L. & Knoefel, J.E.), pp. 3–67. NewYork: Oxford University Press.

    Google Scholar 

  • Kondo, A., Sendoh, S., Miyata, K. & Takamatsu, J. (1995) Spongy degeneration in the zitter rat: ultrastructural and immunohistochemical studies. Journal of Neurocytology 24, 533–44.

    Article  CAS  Google Scholar 

  • Lintl, P. & Braak, H. (1983) Loss of intracortical myelinated fibers: a distinctive age-related alteration in the human striate area. Acta Neuropathologica 61, 178–82.

    Article  CAS  Google Scholar 

  • Ludwin, S.K. Pathology of the myelin sheath. In: Axon: Structure, Function and Pathophysiology (edited by Waxman, S. G., Kocsis, J.D., & Stys, P.K.), pp. 412– 37. New York: Oxford University Press.

  • Malamud, N. & Hirano, A. (1973) Atlas of Neuropathology. Berkerley: University of California Press.

    Google Scholar 

  • McGinn, M. D. & Faddis, B. T. (1987) Auditory experience affects degeneration of the ventral cochlear nucleus in Mongolian gerbils. Hearing Research 31, 235–44.

    Article  CAS  Google Scholar 

  • McGinn, M.D. & Faddis, B.T. (1997) Kangaroo rats exhibit spongiform degeneration of the central auditory system similar to that found in gerbils. Hearing Research 104, 90–100.

    Article  CAS  Google Scholar 

  • Miller, A. K. H., Alston, R. L. & Corsellis, J. A. N. (1980) Variations with age in the volumes of grey and white matter in the cerebral hemisphere of man: measurements with an image analyser. Neuropathology and Applied Neurobiology 6, 119–32.

    Article  CAS  Google Scholar 

  • Monuki, E. S. & Lemke, G. (1995) Molecular biology of myelination. In: The Axon: Structure, Function and Pathophysiology (edited by Waxman, S.G., Kocsis, J.D. & Stys, P.K.), pp. 144–163. New York: Oxford University Press.

    Chapter  Google Scholar 

  • Ostapoff, E.-M. & Morest, D.K. (1989) A degenerative disorder of the central auditory system of the gerbil. Hearing Research 37, 141–62.

    Article  CAS  Google Scholar 

  • Peters, A. (1960) The formation and structure of myellin sheaths in the central nervous system. Journal of Biophysical and Biochemical Cytology 8, 431–46.

    Article  CAS  Google Scholar 

  • Peters, A. (1991) Aging in monkey cerebral cortex. In: Normal and Altered States of Function (edited by Peters, A. & Jones, E.G.), pp. 485–510. Cerebral Cortex, vol. 9. New York: Plenum Press.

    Chapter  Google Scholar 

  • Peters, A. (1996) Age-related changes in oligodendrocytes in monkey cerebral cortex. Journal of Comparative Neurology 371, 153–63.

    Article  CAS  Google Scholar 

  • Peters, A., Leahu, D., Moss, M. B. & MCNally, K. J. (1994) The effects of aging on area 46 of the frontal cortex of the rhesus monkey. Cerebral Cortex 6, 621–35.

    Article  Google Scholar 

  • Peters, A., Palay, S. L. & Webster, DeF. H. (1991) The Fine Structure of the Nervous System. New York & Oxford: Oxford University Press.

    Google Scholar 

  • Raine, C. (1984) The neuropathology of myelin diseases. In: Myelin (edited by Morrell, P.), pp. 259–310. New York: Plenum Press.

    Chapter  Google Scholar 

  • Tamura, E. & Parry, G. J. (1994) Severe radicular pathology in rats with longstanding diabetes. Journal of Neurological Science 127, 29–35.

    Article  CAS  Google Scholar 

  • Tigges, J., Gordon, T. P., MCClure, H. M., Hall, E. C. & Peters, A. (1988) Survival rate and life span of rhesus monkeys at the Yerkes Regional Primate Research Center. American Journal of Primatology 15, 263–73.

    Article  Google Scholar 

  • Waxman, S. G. (1977) Conduction in myelinated, unmyelnated, and demyelinated fibers. Archives of Neurology 34, 585–589.

    Article  CAS  Google Scholar 

  • Yagi, H., Irino, M., Matsushita, T., Katoh, S., Umezawa, M., Tsuboyama, T., Hosokawa, M., Akiguchi, I., Tokunaga, R. & Takeda, T. (1989) Spontaneous spongy degeneration of the brain stem in SAM-P/8 mice, a newly developed memory deficient strain. Journal of Neuropathology and Experimental Neurology 48, 577–90.

    Article  CAS  Google Scholar 

  • Zhou, R., Abbas, P.J. & Assouline, J.G. (1995) Electrically evoked auditory brainstem response in peripherally myelin-deficient mice. Hearing Research 88, 98–106.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Feldman, M.L., Peters, A. Ballooning of myelin sheaths in normally aged macaques. J Neurocytol 27, 605–614 (1998). https://doi.org/10.1023/A:1006926428699

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006926428699

Keywords

Navigation