Summary
It has been suggested that age changes in the morphology of the neuromuscular junction (NMJ) may reflect altered physical activity levels rather than the unique effects of ageing. Additionally, previous studies have indicated that the structure of the NMJ may be modulated with exercise. To investigate these questions, quantitative morphometry was determined on soleus and extensor digitorum longus (EDL) nerve terminals stained with zinc iodide-osmium from C57BL/6NNia mice under control and endurance exercised conditions at 12, 18 and 24 months of age.
As previously observed, the area, perimeter, extent length and branch number of nerve terminals increased with age in both soleus and EDL. The changes were similar between the muscle types, although the changes were more pronounced in the phasic EDL. In 12-month-old animals, 2 months of endurance exercise resulted in significantly larger nerve terminals in both soleus and EDL, suggesting a functional adaptation. Exercised 18- and 24-month-old nerve terminals were smaller than corresponding controls, which indicated that exercise minimized or prevented further age-related nerve terminal elaboration. At all ages the exercised nerve terminals comprised a more homogeneous population than corresponding controls, which indicates that uniform physical activity can modulate NMJ morphometry. The magnitude of the changes suggests that subtle alterations in normal cage activity with advancing age do not have a significant effect on the morphology of nerve terminals. However, the morphology of the NMJ does change significantly in response to physical exercise training.
Similar content being viewed by others
References
Akert, K. &Sandri, C. (1968) An electron microscope study of zinc iodide/osmium impregnation of neurones.Brain Research 7, 286–95.
Andonian, M. H. (1986) Effects of age and exercise on the morphology of fast and slow twitch neuromuscular junctions. PhD Dissertation, University of Southern California.
Appell, H. J. (1984) Proliferation of motor end-plates induced by increased muscular activity.International Journal of Sports Medicine 5, 125–9.
Banker, B. Q., Kelly, S. S. &Robbins, N. (1983) Neuromuscular transmission and correlative morphology in young and old mice.Journal of Physiology 339, 355–77.
Barker, D. &Ip, M. C. (1966) Sprouting and degeneration of mammalian motor axons in normal and deafferented skeletal muscle.Proceedings of the Royal Society of London, Series B 163, 538–54.
Brown, M. C., Holland, R. L. &Hopkins, W. G. (1981) Motor nerve sprouting.Annual Review of Neuroscience 4, 17–42.
Cardasis, C. A. (1983) Ultrastructural evidence of continued reorganization at the ageing (11–26 months) rat soleus neuromuscular junction.Anatomical Record 207, 399–415.
Cardasis, C. A. &Padykula, H. A. (1981) Ultrastructural evidence indicating reorganization at the neuromuscular junction in the normal rat soleus muscle.Anatomical Record 200, 41–59.
Chappell, M. A. (1984) Maximum oxygen consumption during exercise and cold exposure in deer mice,peromyscus maniculatus.Respiratory Physiology 55, 366–77.
Colton, T. (1974)Statistics in Medicine. Boston: Little Brown and Company.
Crockett, J. L., Edgerton, V. R., Max, S. R. &Barnard, R. J. (1976) The neuromuscular junction in response to endurance training.Experimental Neurology 51, 207–15.
Dekosky, S. T., Scheff, S. W. &Cotman, C. W. (1984) Elevated corticosterone levels: A possible cause of reduced axon sprouting in aged animals.Neuroendocrinology 38, 33–8.
Dudley, G. A., Abraham, W. A. &Terjung, R. J. (1982) Influence of exercise intensity and duration on biochemical adaptations in skeletal muscle.Journal of Applied Physiology 53, 844–55.
Edwards, A. L. (1979)Multiple Regression and the Analysis of Variance and Covariance. San Francisco: W. H. Freeman and Co.
Elias, P. K., Elias, M. F. &Eleftheriou, B. E. (1975) Emotionality, exploratory behavior, and locomotion in ageing inbred strains of mice.Gerontology 21, 46–55.
Fahim, M., Economos, M., Mazella, G., Weese, D. &Andonian, M. H. (1986) Chronic corticosterone treatment alters the morphology of soleus and extensor digitorum longus neuromuscular junctions in the rat.Society for Neuroscience Abstracts 12, 116.
Fahim, M. A., Holley, J. A. &Robbins, N. (1983) Scanning and light microscopic study of age changes at a neuromuscular junction in the mouse.Journal of Neurocytology 12, 13–25.
Fahim, M. A., &Holley, J. A. Robbins, N. (1984) opographic comparison of neuromuscular junctions in mouse slow and fast twitch muscles.Neuroscience 13, 227–35.
Fahim, M. A. &Robbins, N. (1982) Ultrastructural studies of young and old mouse neuromuscular junctions.Journal of Neurocytology 11, 641–56.
Fahim, M. A. &Robbins, N. (1986) Remodeling of the neuromuscular junction after subtotal disuse.Brain Research 383, 353–6.
Fischbach, G. D. &Robbins, N. (1969) Changes in contractile properties of disused soleus muscles.Journal of Physiology 201, 305–20.
Fitts, R. H. (1981) Ageing and skeletal muscle. InExercise and Ageing: The Scientific Basis (edited bySmith, E. L. &Servass, R. C.). Hillside, NJ: Enslow.
Frolkis, V., Martynenko, O. &Zamostyan, V. (1976) Aging of the neuromuscular apparatus.Gerontology 22, 353–66.
Gertler, R. A. &Robbins, N. (1978) Differences in neuromuscular transmission in red and white muscles.Brain Research 142, 160–4.
Girgis, F. &Finch, C. E. (1974) Enlarged seminal vesicles of senescent mice.Journal of Gerontology 29, 134–8.
Goldberg, A. L. &Goodman, H. M. (1969) Relationship between cortisone and muscle work in determining muscle size.Journal of Physiology (London) 200, 667–75.
Gollnick, P. D. &King, D. W. (1969) Effects of exercise and training on mitochondria of rat skeletal muscle.American Journal of Physiology 216, 1502–9.
Goodrick, C. (1980) Effects of long term voluntary wheel exercise on male and female wistar rats.Gerontology 26, 22–33.
Gutmann, E. &Hanzlikova, V. (1976) Fast and slow motor units in ageing.Gerontology 22, 280–300.
Gutmann, E., Hanzlikova, V. &Vyskocil, F. (1971) Age changes in cross striated muscle of the rat.Journal of Physiology 216, 331–43.
Hennig, R. &Lomo, T. (1985) Firing patterns of motor units in normal rats.Nature 314, 164–6.
Jakubczak, L. F. (1970) Age differences in the effects of water deprivation on activity, water loss and survival of rats.Life Sciences 9, 771–80.
Jans, H., Salzmann, R. &Wernig, A. (1986) Sprouting and nerve retraction in frog neuromuscular junctions during ontogenesis and environmental changes.Neuroscience 18, 773–81.
Kelly, S. S. &Robbins, N. (1983) Progression of age changes in synaptic transmission at mouse neuromuscular junctions.Journal of Physiology 343, 375–83.
Knochel, J. P., Carter, N. &Colton, J. R. (1977) Muscle hyperpolarization and potassium tolerance induced by exercise training.Clinical Research 22, 455.
Mondon, C. E., Dolkas, C. B., Sims, C. &Reaven, G. M. (1985) Spontaneous running activity in male rats: effects of age.Journal of Applied Physiology 58, 1553–7.
Moss, R. F., Raven, P. B., Knochel, J. P., Peckham, J. R. &Blanchley, J. D. (1983) The effect of training on resting membrane potentials. In: Knuttgen, H. G., Vogel, J., Poortmans, J. (eds)Biochemistry of Exercise (edited byKnuttgen, H. G., Vogel, J. &Poortmans, J.). Illinois: Human Kinetics.
Navarrete, R. &Vrbova, G. (1980) Electromyographic activity of rat slow and fast muscle during post-natal development.Journal of Physiology 305, 33–4P.
Pare, W. P. (1965) The effect of chronic environmental stress on premature ageing in the rat.Journal of Gerontology 20, 78–84.
Pestronk, A., Drachman, D. B. &Griffin, J. W. (1980) Effects of ageing on nerve sprouting and regeneration.Experimental Neurology 70, 65–82.
Purves, D. &Lichtman, J. (1985)Principles of Neural Development. Sunderland: Sinauer.
Reznick, A. Z., Gershon, D. &Steinhagen-Thiessen, E. (1982) The effect of exercise on enzyme activities in cardiac muscles of mice of various ages.Biochemical Medicine 28, 347–52.
Robbins, N. &Fahim, M. A. (1985) Progression of age changes in mature mouse motor nerve terminals and its relation to locomotor activity.Journal of Neurocytology 14, 1019–36.
Robbins, N. &Fischbach, G. D. (1971) Effect of chronic disuse of rad soleus neuromuscular junctions on presynaptic function.Journal of Neurophysiology 34, 570–8.
Rosenheimer, J. (1985) Effects of chronic stress and exercise on age-related changes in end-plate architecture.Journal of Neurophysiology 53, 1582–9.
Rosenheimer, J. L. &Smith, D. O. (1985) Differential changes in the end-plate architecture of functionally diverse muscles during ageing.Journal of Neurophysiology 53, 1567–81.
Salminen, A., Kainulainen, H., &Vihko, V. (1982) Lysosomal changes related to ageing and physical exercise in mouse cardiac and skeletal muscles.Experientia. 38, 781–2.
Samorajski, T., Delaney, C. &Durham, L. (1985) Effects of exercise on longevity, body weight, locomotor performance, and passive-avoidance memory of C57BL/6J mice.Neurobiology of Aging 6, 17–24.
Schlesselman, J. (1982)Case-control Studies. New York: Oxford University Press.
Silberman, M., Finkelbrand, S., Weiss, A., Gershon, D. &Reznick, A. (1983) Morphometric analysis of ageing skeletal muscle following endurance training.Muscle and Nerve 6, 136–43.
Smith, D. O. &Rosenheimer, J. L. (1982) Decreased sprouting and degeneration of nerve terminals of active muscles in aged rats.Journal of Neurophysiology 48, 101–9.
Sokal, R. R. &Rohlf, F. J. (1969)Biometry. San Francisco: W. H. Freeman and Co.
Sprott, R. I. &Eleftheriou, B. E. (1974) Open-field behavior in ageing inbred mice.Gerontology 20, 155–62.
Stebbins, C., Schultz, E., Smith, R. &Smith, E. (1985) Effects of chronic exercise during ageing on muscle and endplate morphology in rats.Journal of Applied Physiology 58, 45–51.
Steinhagen-Thiessen, E., Reznick, A. &Hilz, H. (1980) Negative adaptation to physical training in senile mice.Mechanisms of Ageing and Development 12, 231–6.
Steinhagen-Thiessen, E., Reznick, A. &Hilz, H. (1981) Positive and negative adaptation of muscle enzymes in ageing mice subjected to physical exercise.Mechanisms of Ageing and Development 16, 363–9.
Taylor, C. M., Schmidt-Nielsen, K. &Raab, J. (1970) Scaling of energetic cost of running to body size in mammals.Journal of Physiology 219, 1104–7.
Tuffery, R. A. (1971) Growth and degeneration of motor end-plates in normal cat hind limb muscles.Journal of Anatomy 110, 221–47.
Wernig, A., Carmody, J. J., Anzil, A. P., Hansert, E., Marciniak, M. &Zucker, H. (1984) Persistence of nerve sprouting with features of synapse remodelling in soleus muscles of adult mice.Neuroscience 11, 241–53.
Wernig, A. &Herrera, A. A. (1986) Sprouting and remodelling at the nerve-muscle junction.Progress in Neurobiology 27, 251–91.
Wernig, A., Pécot-Dechavassine, M. &Stöver, H. (1980) Sprouting and regression of the nerve at the frog neuromuscular junction in normal conditions and after prolonged paralysis with curare.Journal of Neurocytology 9, 277–303.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Andonian, M.H., Fahim, M.A. Effects of endurance exercise on the morphology of mouse neuromuscular junctions during ageing. J Neurocytol 16, 589–599 (1987). https://doi.org/10.1007/BF01637652
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01637652