Development and ageing of intestinal musculature and nerves: the guinea-pig taenia coli

J Neurocytol. 2001 Sep-Oct;30(9-10):733-66. doi: 10.1023/a:1019660519961.

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 approximately 1,000 microm(3) in volume at birth, 2,200 microm(3) in young adults and 4,500 microm(3) 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 approximately 1,300 axons per 10,000 microm(2) of sectional area, or between 8,000 and 38,000 axons in a full cross section of taenia; this amounts to approximately 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.

MeSH terms

  • Actin Cytoskeleton / physiology
  • Actin Cytoskeleton / ultrastructure
  • Aging / physiology*
  • Animals
  • Animals, Newborn
  • Capillaries / physiology
  • Capillaries / ultrastructure
  • Cell Differentiation / physiology*
  • Cell Membrane / physiology
  • Cell Membrane / ultrastructure
  • Cell Size / physiology
  • Colon / growth & development*
  • Colon / innervation
  • Colon / ultrastructure
  • Cytoskeleton / physiology
  • Cytoskeleton / ultrastructure
  • Female
  • Fibroblasts / physiology
  • Fibroblasts / ultrastructure
  • Guinea Pigs
  • Male
  • Microscopy, Electron
  • Mitosis / physiology
  • Muscle, Smooth / growth & development*
  • Muscle, Smooth / innervation
  • Muscle, Smooth / ultrastructure
  • Myenteric Plexus / growth & development*
  • Myenteric Plexus / ultrastructure
  • Neuromuscular Junction / growth & development*
  • Neuromuscular Junction / physiology
  • Neuromuscular Junction / ultrastructure
  • Presynaptic Terminals / physiology
  • Presynaptic Terminals / ultrastructure*
  • Schwann Cells / physiology
  • Schwann Cells / ultrastructure
  • Stromal Cells / physiology
  • Stromal Cells / ultrastructure