The autonomic innervation of smooth muscle
Clawson, Jean Robertson
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A thesis reviewing the recent work concerning the autonomic innervation of smooth muscle cells has been prepared, and without the support of individual investigations by the author a few conclusions have been proposed. The nature of the gross anatomy of the autonomic nervous system is well-known, and is not discussed in the paper. The function of the autonomic system is "briefly described as the "maintenance of stability or homeostasis in the fluid matrix of the organism." (Cannon and Rosenblueth, 1937) There are found in the literature two theories which deal with the nature of smooth muscle cells. The work of McGill (1907, 1909) and Tiegs (1924) was presented as evidence for the action of neurofibrillae in contraction. Observations of McGill (1907, 1909), Evans (1926), Bozler (1938, 1939) and others indicated that the smooth musculature of the viscera, and particularly that of the uterus, is syncytial, and that conduction from muscle cell to muscle cell takes place directly through interprotoplasmic bridges. Fulton and Lutz (1942) have described a vascular smooth muscle syncytium, discontinuous at the junctions of the vessels, in the retrolingual membrane of the frog. On the other hand, the work of Tiegs (1924), Eccles and Magladery (1937b) and Cannon and Rosenblueth (1937) showed that in certain areas of the smooth musculature, particularly in the nictitating membrane, there is no evidence for the presence of a syncytium. In this case the transfer of impulses from cell to cell is probably humoral. It may be concluded that there are two types of smooth muscle, one syncytial and the other consisting of independent cells, and that these occur in characteristic regions of the body. The various mechanisms for the contraction of capillaries are also discussed in the literature. Clark and Clark (1925b, 1940), Florey and Carleton (1925), Michels (1935) and Zweifach (1934, 1937) have found no evidence for the dependence of the capillaries on the Rouget cells (pericytes, pericapillary cells) for contraction; on the other hand, Vimtrup (1922), Bensley and Vimtrup (1920), Jones (1935), and Fulton and Lutz (1940, 1941, 1942) presented experiments on living tissue and observations on fixed preparations as evidence for the contractility of certain pericapillary cells (the Rouget cells). Zweifach (1937) suggested a classification of the capillaries based on the structure of their walls. Thus he described arterio-venous bridges, which are muscular and actively contractile, and true capillaries, which are endothelial, and do not possess muscular perivascular elements. In connection with the distribution of smooth muscle cells in the body, the papers of Ingalls (1933), Macklin (1929) and Acheson (1938) were outlined. Ingalls described the embryology and the anatomy of the dilator and the sphincter muscles of the iris; Macklin classified the pulmonary musculature as bronchial and interstitial, and defined the limits of both; and Acheson stated that the musculature of the nictitating membrane does not extend to its outer limit but only to its origin. The differences in the physiology of smooth muscle from that of striated muscle were discussed briefly, and the work of Ferguson (1940) on the nerve-free smooth muscle of the chick amnion was presented here. There are three broad theories concerning the morphological relations between smooth muscle cell and nerve fiber, and the monograph by Boeke (1940) describes them briefly. The first theory states that the postganglionic fibers go directly and independently to innervate the effector cells. The second theory says that the interstitial cells of Cajal intervene between the postganglionic fiber and the effector; and the third theory describes a gradual transition from a neuro-fibrillar network into a terminal reticulum which is apparently present everywhere in the body. The work of many authors in relation to these theories was presented, and it would appear that the real nature of the autonomic innervation of smooth muscle may involve a combination of these three theories. Thus it appears that the postganglionic fibers are in contact with Cajal's interstitial cells, which are syncytial in nature, and that the fibers of these cells are in contact with, and may form, a delicate terminal reticulum of nerve fibers throughout the body. Regional descriptions of the innervation of the smooth muscle of the various systems of the body were given. In the vascular musculature, Larsell (1921, 1922), J. D. Boyd (1937, 1941) and others describe endings on the muscle cells of arteries and arterioles; Michels (1935, 1936) and Larsell and Dow (1933) were unable to find endings on either the endothelium or the pericytes of capillaries, though many have shown that these smaller vessels are accompanied by nerves. Boeke (1932) reported that in the vessels of the human eye the nerve fibers extended to the muscle cells and continued into an extremely delicate network within them. In the urogenital musculature, the work of Gruber (1938), Stewart (1937), Kleyntjens and Langworthy (1937), Langworthy and Murphy (1939), Davis (1933) and others was outlined. Ho nerve endings were found in the ureter or the uterus, but were demonstrated in the bladder and the fallopian tube. Nerve endings in the gut musculature were found by Carpenter (1918), Hill (1927), Irwin (1931) and Li (1940). The plexuses in the walls of the gastrointestinal tract were described by Langley (1921), Hill (1927), van Esveld (1923), Schabadasch (1930), Irwin (1931), McSwiney (1931) and Li (1940). These plexuses, while independent, are connected to the vagus and sympathetic fibers. The majority of these authors also indicate that the interstitial cells of Cajal are to be considered as the end-point of the enteric system. Plexuses around the sphincter and dilator muscles of the iris were described by Boeke (1933), Jones (1932) and S. L. Clark (1937), and endings on or in the cells of these muscles were also described. The work of Larsell (1921, 1922), Larsell and Mason (1921), Larsell and Dow (1933) and Macklin (1929) defined plexuses in the respiratory musculature; nerve terminations are also described. Cannon and Eosenblueth (1937), in dealing with the physiology of the autonomic neuro-effector system, describe the dual innervation of the smooth musculature from neurons of both the sympathetic and parasympathetic systems, and repeat the well-known fact that this innervation is antagonistic. The theories of chemical mediation are discussed; these lead to the belief that autonomic impulses are transmitted from neuron to neuron and from neuron to plain muscle fiber by the intervention of either acetylcholine or an adrenalinlike substance, sympathin. Also, there are apparently two sympathins, an inhibitory one and an excitatory one. The significance of the relative stability of sympathin and the rapid destruction of acetylcholine in the function of the sympathetic and the parasympathetic systems is discussed. Also mentioned is the theory of electrical transmission of impulses; this postulates that the electrical changes produced during conduction in the nerve serve in the transmission of the impulse across the synapse. It is probable that both mechanisms are involved, and that when the electrical impulse fails to reach adjacent nerve or muscle cells the chemical mediator may intervene to complete the transmission. The steps in the transmission of impulses from neuron to muscle fiber are outlined briefly, and the action of various drugs in blocking this transmission is described. The experiments on denervation are also discussed; these indicate that the severing of the nerve supply to the effector increases its response to mechanical stimulation and may decrease its response to electrical and chemical stimulation. In criticizing the discrepancies in the results on the morphology of autonomic innervation of smooth muscles, the variation, in staining techniques, together with the results obtained with silver and with methylene blue techniques, is discussed. It is concluded that the work on this problem is by no means finished, and that consistent results can be produced moat reliably with similar methods.
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