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The ultrastructure of the intestinal nerve of Remak in the domestic fowl

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Summary

An ultrastructural study was made of the neurons, satellite cells and vesiculated axons of the intestinal nerve of the domestic fowl. Broad membrane-to-membrane contacts between adjacent nerve cell bodies were sometimes observed. The cell bodies and processes were not always separated from the extracellular space by a capsule of satellite cells. Following fixation using potassium permanganate, catecholamine (CA)-containing neurons in the intestinal nerve, unlike those in the lumbar parasympathetic ganglia, did not possess any small granular vesicles (SGV). Following exposure to noradrenaline, SGV could be demonstrated in the cell bodies of the juxta-ileal ganglia but not the juxta-rectal ganglia of the intestinal nerve. Non-CA axons were examined in tissue from birds that had been pretreated with 6-hydroxydopamine. Approximately one half of the non-CA axons formed axo-somatic contacts. Most of the non-CA axons contained varying proportions of small clear vesicles, large clear vesicles and large granular vescles. Statistical analysis showed that the non-CA axons could not be subdivided according to their vesicle content. CA-axons contained many SGV and were found in close apposition to neuronal somata and processes, and in the neuropil.

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References

  • Ahmad A, Singh RCP, Garg BD (1978) Evidence of non-cholinergic excitatory nervous transmission in chick ileum. Life Sci 22:1049–1058

    Google Scholar 

  • Akester AR (1979) The autonomic nervous system. In: King AS, McLelland J (eds) Form and function in birds, Vol. 1. Academic Press, New York, pp 381–441

    Google Scholar 

  • Akester AR, Akester B (1975) Ultrastructural and experimental studies of Remak's autonomic nerve trunk in the fowl. J Anat 119:416–417

    Google Scholar 

  • Baluk P, Gabella G (1987) Fine structure of the autonomic ganglia of the mouse pulmonary vein. J Neurocytol 16:169–184

    Google Scholar 

  • Baluk P, Fujiwara T, Matsuda S (1985) The fine structure of the ganglia of the guinea-pig trachea. Cell Tissue Res 239:51–60

    Google Scholar 

  • Bartlet AL, Hassan T (1971) Contraction of chicken rectum to nerve stimulation after blockade of sympathetic and parasympathetic transmission. Q J Exp Physiol 56:178–183

    Google Scholar 

  • Bennett T, Malmfors T (1970) The adrenergic nervous system of the domestic fowl (Gallus domesticus L.). Z Zellforsch Mikrosk Anat 106:22–50

    Google Scholar 

  • Berger PJ, Gibbins IL, Hards DK, Crosby LJ (1982) The distribution and ultrastructure of sensory elements in the baroreceptor region of the truncus arteriosus of the lizard Trachydosaurus rugosus. Cell Tissue Res 226:389–406

    Google Scholar 

  • Bloom FE (1971) Fine structural changes in the rat brain after intracisternal injection of 6-hydroxydopamine. In: Malmfors T, Thoenen H (eds) 6-Hydroxydopamine and catecholamine neurons, North-Holland, Amsterdam, pp 135–150

    Google Scholar 

  • Burnstock G, Iwayama T (1971) Fine structural identification of autonomic nerves and their relation to smooth muscle. Prog Brain Res 34:389–404

    Google Scholar 

  • Campbell G, Haller CJ, Rogers DC (1978) Fine structural and cytochemical study of the innervation of smooth muscle in an amphibian (Bufo marinus) lung before and after denervation. Cell Tissue Res 194:419–432

    Google Scholar 

  • Cantino D (1968) Données preliminaires sur l'ultrastructure de nerf ganglionné de Remak. C R Ass Anat 63:640–644

    Google Scholar 

  • Cantino D, Mugnaini E (1974) Adrenergic innervation of the parasympathetic ciliary ganglion in the chick. Science 185:279–280

    Google Scholar 

  • Cantino D, Barasa A, Guglielmone R (1982) Catecholamine-containing neurons in Remak's ganglion: a developmental and tissue culture study. J Neurocytol 11:763–778

    Google Scholar 

  • Cheah TB, Geffen B, Jarrott B, Ostberg A (1971) Action of 6-hydroxydopamine on lamb sympathetic ganglia, vas deferens and adrenal medulla: a combined histochemical, ultrastructural and biochemical comparison with the effects of reserpine. Br J Pharmacol 42:543–557

    Google Scholar 

  • Chiba T (1972) Fine structure of the baroreceptor nerve terminals in the carotid sinus of the dog. J Electron Microse (Tokyo) 21:139–148

    Google Scholar 

  • Chiba T, Yamauchi A (1970) On the fine structure of the nerve terminals in the human myocardium. Z Zellforsch Mikrosk Anat 108:324–338

    Google Scholar 

  • Cobb JLS, Bennett T (1971) An electron microscopic examination of the short term effects of 6-hydroxydopamine on the peripheral adrenergic nervous system. In: Malmfors T, Thoenen H (eds) 6-Hydroxydopamine and catecholamine neurons, North-Holland, Amsterdam, pp 33–46

    Google Scholar 

  • Costa M (1966) Contribution a l'étude de l'innervation adrénergique du canal alimentaire; le nerf ganglionné de Remak. C R Assoc Anat 51:249–252

    Google Scholar 

  • Costa M (1970) La chaine ganglionné de Remak chez le poulet: les neurones adrénergiques. CR Assoc Anat 55:720–724

    Google Scholar 

  • De Lemos C, Pick J (1966) The fine structure of thoracic sympathetic neurons in the adult rat. Z Zellforsch Mikrosk Anat 71:189–206

    Google Scholar 

  • Dixon JS (1966) The fine structure of parasympathetic nerve cells in the otic ganglia of the rabbit. Anat Rec 156:239–252

    Google Scholar 

  • Dixon JS, Gosling JA (1976) Extravesicular noradrenaline in developing peripheral adrenergic nerves. Experentia 32:1052–1053

    Google Scholar 

  • Dixon JS, Fozard JR, Gosling JA, Muscholl E, Ritzel H (1978) Atrial sympathetic nerves after perfusion of the rabbit heart with low sodium solutions containing potassium chloride or urea — a biochemical, histochemical and fine structural study. Neuroscience 3:1157–1167

    Google Scholar 

  • Ehinger B (1967) Adrenergic nerves in the avian eye and ciliary ganglion. Z Zellforsch Mikrosk Anat 82:577–588

    Google Scholar 

  • Elfvin L-G (1963) The ultrastructure of the superior cervical sympathetic ganglion of the cat. I. The structure of the ganglion cell processes as studied by serial sections. J Ultrastruct Res 8:403–440

    Google Scholar 

  • Epstein ML, Dahl JL (1982) Development of enkephalin in the rectum and the ganglion of Remak of the chick. Peptides 3:77–82

    Google Scholar 

  • Fischer JE, Snyder S (1965) Disposition of norepinephrine-H3 in sympathetic ganglia. J Pharmacol Exp Ther 150:190–195

    Google Scholar 

  • Gabella G (1972) Fine structure of the myenteric plexus of the guinea-pig ileum. J Anat 111:69–97

    Google Scholar 

  • Gabella G (1976) Structure of the autonomic nervous system. Chapman and Hall, London

    Google Scholar 

  • Geffen LB, Livett BG (1971) Synaptic vesicles in sympathetic neurons. Physiol Rev 51:98–157

    Google Scholar 

  • Gilpin CJ, Dixon JS, Gilpin SA, Gosling JA (1983) The fine structure of autonomic neurons in the wall of the human urinary bladder. J Anat 137:705–713

    Google Scholar 

  • Grillo MA (1966) Electron microscopy of sympathetic tissues. Pharmacol Rev 18:387–399

    Google Scholar 

  • Hamori J, Lang E, Simon L (1968) Experimental degeneration of the preganglionic fibres in the superior cervical ganglion of the cat. Z Zellforsch Mikrosk Anat 90:37–52

    Google Scholar 

  • Hervonen A, Kanerva L, Hervonen H (1977) Ultrastructure of human fetal sympathetic ganglia after permanganate fixation — absence of granular vesicles. Neurosci Lett 5:303–308

    Google Scholar 

  • Hodgkiss JP (1984) A study of excitatory efferent fibres in the intestinal nerve of the fowl (Gallus domesticus). Comp Biochem Physiol 79A:93–97

    Google Scholar 

  • Hökfelt T (1969) Distribution of noradrenaline storing particles in peripheral adrenergic neurons as revealed by electron microscopy. Acta Physiol Scand 76:427–440

    Google Scholar 

  • Hoyes AD, Barber P (1980) Innervation of the trachealis muscle in the guinea-pig: a quantitative ultrastructural study. J Anat 130:789–800

    Google Scholar 

  • Hruschak KA, Friedrich VL, Giacobini E (1982) Synaptogenesis in chick paravertebral sympathetic ganglia: a morphometric analysis. Dev Brain Res 4:229–240

    Google Scholar 

  • Hung KS, Hertweck MS, Hardy JD, Loosli CG (1973) Electron microscopic observations of nerve endings in the alveolar walls of mouse lungs. Am Rev Respir Dis 108:328–333

    Google Scholar 

  • Ishizuka N, Komori S, Ohashi H (1982) Evidence for adrenergic modulation of ganglionic transmission in the ganglia of nerve Remak of the chicken. J Auton Nerv Sys 6:185–198

    Google Scholar 

  • Kanazawa T, Ohashi H, Takewaki T (1980) Evidence that cell bodies of non-cholinergic, excitatory neurones which supply the smooth muscle of the chicken rectum are located in the ganglia of Remak's nerve. Br J Pharmacol 71:519–524

    Google Scholar 

  • Kanerva L, Teräväinen H (1972) Electron microscopy of the paracervical (Frankenhäuser) ganglion of the adult rat. Z Zellforsch Mikrosk Anat 129:161–177

    Google Scholar 

  • Komori S, Ohashi H (1984) Presynaptic, muscarinic inhibition of non-adrenergic, non-cholinergic neuromuscular transmission in the chicken rectum. Br J Pharmacol 82:73–84

    Google Scholar 

  • Komori S, Ohashi H (1987) Nerve pathways involved in adrenergic regulation of electrical and mechanical activities in the chicken rectum. Br J Pharmacol 90:121–130

    Google Scholar 

  • Llewellyn-Smith IJ, Wilson AJ, Furness JB, Costa M, Rush RA (1981) Ultrastructural identification of noradrenergic axons and their distribution within the enteric plexuses of the guinea-pig small intestine. J Neurocytol 10:331–352

    Google Scholar 

  • Marcel PM, Tusscher T, Klooster J, Vrensen GFJM (1989) Satellite cells as blood-ganglion cell barrier in autonomic ganglia. Brain Res 490:95–102

    Google Scholar 

  • Masuko S, Chiba T (1988) Projection pathways, co-existence of peptides and synaptic organization of nerve fibres in the inferior mesenteric ganglion of the guinea pig. Cell Tissue Res 253:507–516

    Google Scholar 

  • Masurvosky EB, Benitez HH, Kim SU, Murray MR (1970) Origin, development, and nature of intranuclear rodlets and associated bodies in chicken sympathetic neurons. J Cell Biol 44:172–191

    Google Scholar 

  • Matthews MR (1983) The ultrastructure of junctions of sympathetic ganglia of mammals. In: Elfvin L-G (ed) Autonomic ganglia, Wiley, New York, pp 27–66

    Google Scholar 

  • Newgreen DF, Allan IJ, Young HM, Southwell BR (1981) Accumulation of exogenous catecholamines in the neural tube and non-neural tissue of the early fowl embryo. Correlation with morphogenetic movements. Wilhelm Roux's Arch Dev Biol 190:320–330

    Google Scholar 

  • Pick J (1970) The autonomic nervous system. Lippincott, Philadelphia Toronto

    Google Scholar 

  • Quilliam JD, Tamarind JP (1972) Electron microscopy of degenerative changes in decentralized rat superior cervical ganglia. Micron 3:454–472

    Google Scholar 

  • Richardson KC (1960) Studies on the structure of autonomic nerves in the small intestine, correlating the silver-impregnated image in light microscopy with the permanganate-fixed ultrastructure in electron microscopy. J Anat 94:457–472

    Google Scholar 

  • Richardson KC (1966) Electron microscope identification of autonomic nerve endings. Nature 210:756

    Google Scholar 

  • Szentágothai J (1964) The structure of the autonomic interneuronal synapse. Acta Neuroveg 26:338–359

    Google Scholar 

  • Takahashi K, Hama K (1965) Some observations on the fine structure of nerve cell bodies and their satellite cells in the ciliary ganglion of the chick. Z Zellforsch Mikrosk Anat 67:835–843

    Google Scholar 

  • Taxi J, Derer M, Domich A (1983) Morphology and histophysiology of SIF cells in the autonomic ganglia. In: Elfvin L-G (ed) Autonomic ganglia, Wiley, New York, pp 67–95

    Google Scholar 

  • Till R, Banks P (1976) Pharmacological and ultrastructural studies on the electron dense cores of the vesicles that accumulate in noradrenergic axons constricted ‘in vitro’. Neuroscience 1:49–55

    Google Scholar 

  • Tomlinson DR (1975) Two populations of granular vesicles in constricted post-ganglionic sympathetic nerves. J Physiol (Lond) 245:727–735

    Google Scholar 

  • Unsicker K (1973) Fine structure and innervation of the avian adrenal gland. 1. Fine structure of adrenal chromaffin cells and ganglion cells. Z Zellforsch Mikrosk Anat 145:389–416

    Google Scholar 

  • Van Orden LS, Bensch KG, Giarman NJ (1967) Histochemical and functional relationships of catecholamines in adrenergic nerve endings. II. Extravesicular norepinephrine. J Pharmacol Exp Ther 155:428–439

    Google Scholar 

  • Van Orden LS, Schaefer J-M, Burke JP, Lodoen FV (1970) Differentiation of norepinephrine storage compartments in peripheral adrenergic nerves. J Pharmacol Exp Ther 174:357–368

    Google Scholar 

  • Watanabe T (1971) Adrenergic nerve elements in the hypogastric ganglion of the guinea pig. Am J Anat 130:305–330

    Google Scholar 

  • Wilson AJ, Furness JB, Costa M (1981) The fine structure of the submucous plexus of the guinea-pig ileum. II. Description and analysis of vesiculated nerve profiles. J Neurocytol 10:785–804

    Google Scholar 

  • Yamakoda M, Yohru T (1977) Population and structure of nerve cells in mouse submandibular ganglion. Anat Embryol 150:301–312

    Google Scholar 

  • Yokota R, Burnstock G (1983) Synaptic organisation of the pelvic ganglion in the guinea pig. Cell Tissue Res 232:379–397

    Google Scholar 

  • Yokota R, Yamauchi A (1974) Ultrastructure of the mouse superior cervical ganglion, with particular reference to the pre- and post-ganglionic elements covering the soma of its principal neurons. Am J Anat 140:281–297

    Google Scholar 

  • Yoshida M (1968) Vergleichende elektronenmikroskopische Untersuchungen an sympathischen und parasympathischen Ganglien des Goldhamsters. Z Zellforsch Mikrosk Anat 88:138–144

    Google Scholar 

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Young, H.M. The ultrastructure of the intestinal nerve of Remak in the domestic fowl. Cell Tissue Res 260, 601–616 (1990). https://doi.org/10.1007/BF00297241

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