Abstract
The fine structure of taenia coli was studied by electron microscopy in guinea-pigs from birth to old age (over 2 years old). Smooth muscle cells are ∼1,000 μm3 in volume at birth, 2,200 μm3 in young adults and 4,500 μm3 in old age. Muscle growth and muscle cell enlargement continue throughout life, an increase in muscle volume of about 240 times. Differentiated muscle cells divide during development and in adults. Because mitoses are found in any part of the muscle, the tissue grows from within, rather than by addition at the ends or borders. There is progressive increase in nucleus volume, and decrease in surface-to-volume ratio and in nucleus-cell volume ratio in muscle cells. At all ages the taenia consists of a uniform population of muscle cells (apart from dividing cells); there are no undifferentiated cells, no precursor cells or myoblasts, and no degenerating cells. Interstitial cells and fibroblasts are observed at all ages with only small variations in relative number. The amount of intramuscular collagen increases in old age. There is roughly one capillary for every 170 muscle cell profiles at birth, and one for every 200 in adults and in old age. The innervation is dense and reaches all parts of the muscle. In adults there are ∼1,300 axons per 10,000 μm2 of sectional area, or between 8,000 and 38,000 axons in a full cross section of taenia; this amounts to ∼2% of the muscle volume. An answer to the question of why there are so many nerves in the taenia was not found. Expanded axon profiles are part of typical varicose fibres. Varicosities are packed with small clear vesicles and lie at the surface of nerve bundles. Absence of strong, constant patterns indicating specialized contacts of the nerve terminals is a feature of these nerves at all ages. Some varicosities are closest to interstitial cells; more commonly they are close to muscle cells at sites that strongly suggest a neuro-muscular junction. The additional possibility that some varicosities are part of afferent fibres is discussed. The innervation is well developed at birth and the highest density of innervation is found around day 4 when 4% of the taenia consists of nervous tissue. The innervation of immature taenia is characterized by close juxtaposition of axons and muscle cells. Axon profiles packed with vesicles, varicosities and presumptive neuro-muscular junctions are present at birth. The extent of Schwann cells in intramuscular nerves is markedly less than in adults, and virtually all the axons have maximal membrane-to-membrane contact with other axons. In taenia of aged guinea-pigs, the density of innervation is reduced. There is no actual loss of nerve tissue; the total amount of nerve tissue is greater than in young adults, and the apparent reduction reflects a more intense growth of muscle cells. The Schwann cell component becomes more conspicuous than in young adults and there is a greater number of axons fully wrapped by a Schwann cell. Presumptive neuro-muscular junctions are common and probably commoner than in young adults. Growth of muscle cells, changes in their cytological features and in the stroma occur throughout life, including old age. Nerves too continue to grow and undergo structural changes in pattern of distribution, relation with Schwann cells and effector cells.
Similar content being viewed by others
References
Anderson, R. G. (1998) The caveolae membrane system. Annual Reviews of Biochemistry 67, 199–225.
Bailey, P., Holowacz, T. & Lassar, A. B. (2001) The origin of skeletal muscle stem cells in the embryo and the adult. Current Opinion in Cell Biology 13, 679–689.
Bennett, T. & Cobb, J. L. S. (1969) Studies of the avian gizzard: The development of the gizzard and its innervation. Zeitschrift f ¨ur Zellforschung und mikroskopische Anatomie 98, 599–621.
Berkovitz, B. K. V. & Robinson, S. (1991) Ultrastructural quantification of collagen fibrils in chordae tendineae of the sheep and rabbit. Journal of Anatomy 178, 127–132.
Birk, D. E. & Zycband, E. (1994) Assembly of the tendon extracellular matrix during development. Journal of Anatomy 184, 457–463.
BÜlbring, E. (1954) Membrane potentials of smooth muscle fibres of the taenia coli of the guinea-pig. Journal of Physiology 125, 302–315.
BÜlbring, E. & Tomita, T. (1967) Property of the inhibitory potential of smooth muscle as observed in the response to field stimulation of the guinea-pig taenia coli. Journal of Physiology 189, 299–315.
Burnstock, G. (1981) Development of smooth muscle and its innervation. In Smooth Muscle: An Assessment of Current Knowledge (edited by BÜlbring, E., Brading, A. F., Jones, A. W. & Tomita, T.) pp. 431–457. London: Arnold.
Campbell, G. R., Chamley, J. H. & Burnstock, G. (1974) Development of smooth muscle cells in tissue culture. Journal of Anatomy 117, 295–312.
Chang, I.-Y., Glasgow, N. J., Takayama, I., Horigichi, K., Sanders, K. M. & Ward, S. M. (2001) Loss of interstitial cells of Cajal and development of electrical dysfunction in murine bowel obstruction. Journal of Physiology 536, 555–568.
Daniel, E. E. & Posey-Daniel, V. (1984) Neuromuscular structures in opossum esophagus, role of interstitial cells of Cajal. American Journal of Physiology 246, G305–G315.
Faussone-Pellegrini, M.-S. & Thuneberg, L. (1999) Guide to the identification of interstitial cells of Cajal. Microscopy Research and Techniques 47, 248–266.
Gabella, G. (1981) On the musculature of the gastrointestinal tract of the guinea-pig. Anatomy & Embryology 163, 135–156.
Gabella, G. (1989a) Development of smooth muscle: Ultrastructural study of the chick embryo gizzard. Anatomy & Embryology 180, 213–226.
Gabella, G. (1989b) Structure of the intestinal musculature. In Handbook of Physiology. Sec. 6: The Gastrointestinal System. Motility and Circulation, Vol. I. (edited by Wood, L. D.) pp. 103–139. Bethesda, Maryland: American Physiological Society.
Gabella, G. (1990) Hypertrophy of visceral smooth muscle. Anatomy & Embryology 182, 409–424.
Gabella, G. (1991) Ultrastructure of tracheal muscle in developing, adult and ageing guinea-pigs. Anatomy & Embryology 183, 71–79.
Gabella, G. (1992) Intestinal smooth muscle development. In Advances in the Innervation of the Gastrointestinal Tract (edited by Holle, G. E.) pp. 35–47. Elsevier: Amsterdam.
Gabella, G. (1995) The structural relations between nerve fibres and muscle cells in the urinary bladder of the rat. Journal of Neurocytology 24, 159–187.
Gabella, G. (1999) Structure of the intramural nerves in the rat bladder. Journal of Neurocytology 28, 615–637.
Huizinga, J. D. (1999) Gastrointestinal peristalsis: Joint action of enteric nerves, smooth muscle, and interstitial cells of Cajal. Microscopy Research and Technique 47, 239–247.
la Mantia, J. & Shafiq, S. A. (1982) Developmental changes in the plasma membrane of gizzard smooth muscle of the chicken. A freeze-fracture study. Journal of Anatomy 134, 243–253.
Lecoin, L., Gabella, G. & le Douarin, N. (1996) Origin of the c-kit-positive interstitial cells in the avian bowel. Development 122, 725–733.
Liddell, R. A., Syms, M. & McHugh, K. M. (1993) Heterogeneous isoactin gene expression in the adult 766 rat gastrointestinal tract. Gastroenterology 105, 347–356.
McGeachie, J. K. (1975) Smooth muscle regeneration. A review and experimental study. Monographs of Developmental Biology 9, 1–190.
McHugh, K. M. (1995) Molecular analysis of smooth muscle development in the mouse. Developmental Dynamics 204, 278–290.
McHugh, K. M., Crawford, K. & Lessard, J. L. (1991) A comprehensive analysis of the developmental and tissue-specific expression of the isoactin multigene family in the rat. Developmental Biology 148, 442–458.
Nehls, V. & Drenkhahn, D. (1993) The versatility of microvascular pericytes: From mesenchyme to smooth muscle? Histochemistry 99, 1–12.
Olivetti, G., Anversa, P., Melissari, M. & Loud, A. V. (1980) Morphometric study of early postnatal development of the thoracic aorta in the rat. Circulation Research 47, 417–424.
Parry, D. A., Barnes, G. R. G. & Craig, A. S. (1978a) A comparison of the size distribution of collagen fibrils in connective tissues as a function of age and a possible relation between fibril size distribution and mechanical properties. Proceedings of the Royal Society of London B 203, 305–321.
Parry, D. A., Craig, A. S. & Barnes, G. R. G. (1978b) Tendon and ligament from the horse: An ultrastructural study of collagen fibrils and elastic fibres as a function of age. Proceedings of the Royal Society of London B 203, 293–303.
Patteson, K. J. C., Firth, E. C., Goodship, A. E. & Parry, D. A. (1997) Age-related differences in collagen crimp patterns in the superficial digital flexor tendon core region of untrained horses. Australian Veterinary Journal 75, 39–44.
Roman, C., Gonella, J., Niel, J. P., Condamin, M. & Miolan, J. P. (1975) Effects de la stimulation vagale et de l'adrenaline sur la musculeuse lisse du bas oesophage du chat. Colloques INSERM 50, 415–422.
Sander, K. M. (1996) A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterology 111, 492–515.
Scott, J. E. (1995) Extracellular matrix, supramolecular organization and shape. Journal of Anatomy 187, 259–1269.
Serot, J.-M., Foliguet, B., BÉnÉ. M. C. & Faure, G. C. (2001) Choroid plexus and ageing in rats: A morphometric and ultrastructural study. European Journal of Neuroscience 14, 794–798.
Shin, J.-S. & Abraham, S. N. (2001) Caveolae. Not just craters in the cellular landscape. Science 293, 1447–1448.
Torihashi, S., Horisawa, M. U. & Watanabe, Y. (1999) c-Kit immunoreactive interstitial cells in the human gastrointestinal tract. Journal of the Autonomic Nervous System 75, 38–50.
Thuneberg, L. (1982) Interstitial cells of Cajal: Intestinal pacemaker cells? Advances in Anatomy, Embryology and Cell Biology 71, 1–130.
Trelstad, R. L. & Hayashi, K. (1979) Tendon collagen fibrillogenesis: Intracellular subassemblies and cell surface changes associated with fibril growth. Developmental Biology 71, 228–242.
Ward, S. M. & Sanders, K. M. (2001) Interstitial cells of Cajal: Primary target of enteric motor innervation. Anatomical Record 262, 125–135.
Ward, S. M. & Torihashi, S. (1995) Morphological changes during ontogeny of the canine proximal colon. Cell Tissue Research 282, 93–108.
Xi, Y. P., Nette, E. G., King, D. W. & Rosen, M. (1982) Age-related changes in normal human basement membrane. Mechanisms of Ageing and Development 19, 315–324.
Yamauchi, A. & Burnstock, G. (1969) Post-natal development of smooth muscle cells in the mouse vas deferens. Journal of Anatomy 104, 1–15.
Rights and permissions
About this article
Cite this article
Gabella, G. Development and ageing of intestinal musculature and nerves: the guinea-pig taenia coli. J Neurocytol 30, 733–766 (2001). https://doi.org/10.1023/A:1019660519961
Issue Date:
DOI: https://doi.org/10.1023/A:1019660519961