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On the intrinsic innervation of normal rat liver

Histochemical and scanning electron microscopical studies

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Summary

With the Bodian method stained fibers were observed in the lobules of the rat liver and with the modified Karnovsky and Roots thiocholine method cholinesterase (presumably acetylcholinesterase (AChE))-positive nerve fibers were found in a pattern similar to that of the Bodian-stained fibers. The AChE positive nerve fibers form a network in the liver lobules in close relation to hepatocytes and sinusoids. Fluorescent varicose nerve fibers demonstrated by the glyoxylic acid and Falck-Hillarp fluorescence methods were found only in the interlobular spaces associated with vessels. As no overlapping of distribution patterns of AChE-positive nerve fibers and fluorescent nerve fibers occurs, the AChE activity of the nerves of the liver lobules probably reflects the associated presence of acetylcholine in the nerve fibers. In consequence we suggest that nerves of the liver lobules belong to the autonomic parasympathetic nervous system.

SEM of liver tissue revealed light cords apparently situated in smooth surfaced channels between adjacent hepatocytes and in the space of Disse, where fibers also cross sinusoids. We tentatively suggest that the cords of the SEM represent the AChE-positive nerve fibers of our LM observations'.

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References

  • Anufriev, B.T., Eletskii, Yu.K., Smitten, N.A.: Histochemical investigation of the adrenergic innervation of the liver. Bull. exp. Biol. Med. 75, 584–586 (1973)

    Google Scholar 

  • Barajas, L., Silverman, A.J., Muller, J.: Ultrastructural localization of acetylcholinesterase in the renal nerves. J. Ultrastruct. Res. 49, 297–311 (1974)

    Google Scholar 

  • Black, I.B., Axelrod, J.: Inhibition of tyrosine transaminase activity by norepinephrine. J. biol. Chem. 244, 6124–6129 (1969)

    Google Scholar 

  • Black, I.B., Reis, D.J.: Cholinergic regulation of hepatic tyrosine transaminase activity. J. Physiol. (Lond.) 213, 421–433 (1971)

    Google Scholar 

  • Boyde, A., James, D.W., Tresman, R.L., Willis, R.A.: Outgrowth from chicken embryo spinal cord in vitro, studied with the scanning electron microscope. Z. Zellforsch. 90, 1–18 (1968)

    Google Scholar 

  • Civen, M., Ulrich, R., Trimmer, B.M., Brown, C.B.: Circadian rhythms of liver enzymes and their relationship to enzyme induction. Science (N.Y.) 157, 1563–1564 (1967)

    Google Scholar 

  • El-Badawi, A., Schenk, E.A.: Histochemical methods for separate, consecutive and simultaneous demonstration of acetylcholinesterase and norepinephrine in cryostat sections. J. Histochem. Cytochem. 18, 580–588 (1967)

    Google Scholar 

  • Elias, H., Petty, D.: Terminal distribution of the hepatic artery. Anat. Rec. 116, 9–17 (1953)

    Google Scholar 

  • Falck, B., Owman, Ch.: A detailed methodological description of the fluorescence method for cellular demonstration of biogenic monoamines. Acta Univ. Lund. Sect. II, No. 7, 1–23 (1965)

    Google Scholar 

  • Forssmann, W.G., Ito, S.: Innervation of hepatocytes in the tree shrew. Proc. 10th Int. Cong. Anat. Tokyo, 430 (1975)

  • Furness, J.B., Costa, M.: The use of glyoxylic acid for the fluorescence histochemical demonstration of peripheral stores of noradrenaline and 5-hydroxytryptamine in whole mounts. Histochemistry 41, 335–352 (1975)

    Google Scholar 

  • Gruber, H., Zenker, W., Hohberg, E.: Untersuchungen über die Spezifität der Cholinesterasen im peripheren Nervensystem der Ratte. Histochemie 27, 78–86 (1971)

    Google Scholar 

  • Holbrook, gnM.L.: The termination of the nerves in the liver. Proc. Amer. Soc. Microsc., 95–100 (1882)

  • Jacobowitz, D., Koelle, G.B.: Histochemical correlations of acetylcholinesterase and catecholamines in postganglionic autonomic nerves of the cat, rabbit and guinea pig. J. Pharmacol. exp. Ther. 148, 225–237 (1965)

    Google Scholar 

  • Karnovsky, M.J.: The localization of cholinesterase activity in rat cardiac muscle by electron microscopy. J. Cell Biol. 23, 217–232 (1964)

    Google Scholar 

  • Karnovsky, M.J., Roots, L.: A “direct-coloring” thiocholine method for cholinesterases. J. Histochem. Cytochem. 12, 219–221 (1964)

    Google Scholar 

  • Karupu, V.J.: Some data on the peripheral nervous system of the liver in animals and man. Arkh. Anat. Gistol. Embriol. 41, 83–90 (1961)

    Google Scholar 

  • Korolkow, P.: Ueber die Nervenendigungen in der Leber. Anat. Anz. 8, 751–753 (1893)

    Google Scholar 

  • Luna, L.C. (Ed.): Manual of histologic staining methods of the Armed Forces Institute of Pathology. III ed. New York: McGraw-Hill Book Company 1968

    Google Scholar 

  • Macallum, A.B.: The termination of nerves in the liver. Quart. J. micr. Sci. 27, 439–460 (1887)

    Google Scholar 

  • Mikhail, Y., Saleh, A.L.: Intrinsic nerve fibers in the liver parenchyma. Anat. Rec. 141, 317–323 (1961)

    Google Scholar 

  • Nesterowsky, M.: Ueber die Nerven der Leber. Virchows Arch. path. Anat. 63, 412–421 (1875)

    Google Scholar 

  • Papka, R.E.: Localization of acetylcholinesterase in granule-containing cells of glomus-like bodies in preand postnatal rabbits by electron microscopy. Cell Tiss. Res. 162, 185–194 (1975)

    Google Scholar 

  • Pflüger, E.: Ueber die Abhängigkeit der Leber von dem Nervensystem. Pflügers Arch. ges. Physiol. 2, 459–491 (1869)

    Google Scholar 

  • Riegele, L.: Über das feinere Verhalten der Nerven in der Leber von Mensch und Säugetier. Z. mikr. anat. Forsch. 14, 73–98 (1928)

    Google Scholar 

  • Russu, I.G., Vaida, Al., Dumitrascu, D., Lucaciu, O.: Beiträge zur Innervation der Leber. Acta anat. (Basel) 44, 70–79 (1961)

    Google Scholar 

  • Sætersdal, T.S., Myklebust, R.: Identification of nerve fibres in the scanning electron microscope. J. Microsc. 103, 63–69 (1975)

    Google Scholar 

  • Satler, J.J., Predan, S., Brzin, M.: The activity and cytochemical localization of acetylcholinesterase and butyrylcholinesterase in the rat liver. Histochemistry 39, 65–70 (1974)

    Google Scholar 

  • Shambaugh, G.E. III., Warner, D.A., Beisel, W.P.: Hormonal factors altering rhythmicity of tyrosinealfaketoglutarate transaminase in rat liver. Endocrinology 81, 811–818 (1967)

    Google Scholar 

  • Shimazu, T.: The effect of electric stimulation of hypothalamus on rabbit liver tryptophan pyrrolase. Biochim. biophys. Acta (Amst.) 65, 373–375 (1962)

    Google Scholar 

  • Shimazu, T.: Regulation of glycogen metabolism in liver by the autonomous nervous system. V. Activation of glycogen synthetase by vagal stimulation. Biochim. biophys. Acta (Amst.) 252, 28–38 (1971)

    Google Scholar 

  • Shimazu, T., Fujimoto, T.: Regulation of glycogen metabolism in liver by the autonomic nervous system. IV. Neural control of glycogen biosynthesis. Biochim. biophys. Acta (Amst.) 252, 18–27 (1971)

    Google Scholar 

  • Spencer, P.S., Lieberman, A.R.: Scanning electron microscopy of isolated peripheral nerve fibers. Z. Zellforsch. 119, 534–551 (1971)

    Google Scholar 

  • Sutherland, S.D.: An evaluation of cholinesterase techniques in the study of the intrinsic innervation of the liver. J. Anat. (Lond.) 98, 321–326 (1964)

    Google Scholar 

  • Te Lin Tsai: A histological study of sensory nerves in the liver. Acta neuroveg. (Wien) 17, 354–385 (1958)

    Google Scholar 

  • Ungváry, Gy., Donáth, T.: On the monoaminergic innervation of the liver. Acta anat. (Basel) 72, 446–459 (1969)

    Google Scholar 

  • Waris, T., Partanen, S.: Demonstration of catecholamines in peripheral adrenergic nerves in stretch preparations with fluorescence induced by aqueous solution of glyoxylic acid. Histochemistry 41, 369–372 (1975)

    Google Scholar 

  • Wurtman, R.J., Axelrod, J.: Daily rhythmic changes in tyrosine transaminase activity in rat liver. Proc. nat. Acad. Sci. (Wash.) 57, 1594–1598 (1967)

    Google Scholar 

  • Yamada, E.: Some observations on the nerve terminal on the liver parenchymal cell of the mouse as revealed by electron microscopy. Okajimas Folia anat. jap. 40, 663–677 (1965)

    Google Scholar 

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The skilled assistance of Dr. Esther Hage, Department of Pathology, Odense Sygehus, Denmark, in the Falck-Hillarp fluorescence work is gratefully acknowledged

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Skaaring, P., Bierring, F. On the intrinsic innervation of normal rat liver. Cell Tissue Res. 171, 141–155 (1976). https://doi.org/10.1007/BF00219403

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