Abstract
This review focuses on the more recent findings of the structure of sympathetic postganglionic axons and the association of their varicose terminals with vascular smooth muscle. These studies have investigated the innervation of a wide range of vessels from different regions of the vasculature in the rat, guinea pig and rabbit and have predominantly used serial sections and computerised three-dimensional reconstructions of entire varicosities. They have shown, contrary to previous studies conducted in the 1960s and 1970s, that sympathetic axon varicosities commonly form structurally specialised neuromuscular junctions with vascular smooth muscle cells of most resistance arteries and some small veins. In addition, they have shown that most axon varicosities innervating small arterioles and small mesenteric veins form neuromuscular junctions, indicating that neurotransmitter is primarily released at such neuromuscular junctions. This review discusses the structure of sympathetic neuromuscular junctions, their development, structural diversity and distribution on vessels from different regions of the vasculature. These more recent structural findings and their possible significance for our understanding of mechanisms involved in neural transmission in blood vessels is discussed.
Similar content being viewed by others
References
Ackerman KD, Felten SY, Bellinger DL, Felten DL (1987) Noradrenergic sympathetic innervation of the spleen. III. Development of innervation in the rat spleen. J Neurosci Res 18:49–54
Ackerman KD, Felten SY, Dijkstra CD, Livnat S, Felten DL (1989) Parallel development of noradrenergic innervation and cellular compartmentation in the rat spleen. Exp Neurol 103:239–255
Albert V, Campbell GR (1990) Relationship between the sympathetic nervous system and vascular smooth muscle: a morphometric study of adult and juvenile spontaneously hypertensive rat/Wistar-Kyoto rat caudal artery. Heart Vessels 5:129–139
Anderson CR, McLachlan EM (1991) The time course of the development of the sympathetic innervation of the vasculature of the rat tail. J Auton Nerv Syst 35:117–132
Åstrand P, Stjärne L (1989) On the secretory activity of single varicosities in the sympathetic nerves innervating the rat tail artery. J Physiol (Lond) 409:207–220
Barajas L, Müller J (1973) The innervation of the juxtaglomerular apparatus and surrounding tubules: a quantitative analysis by serial section electron microscopy. J Ultrastruct Res 43:107–132
Bennett MK, Calakos N, Scheller RH (1992) Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257:255–259
Bennett MR (1972) Autonomic neuromuscular transmission. Cambridge University Press, Cambridge
Bevan JA (1977) Some functional consequences of variation in adrenergic synaptic cleft width and in nerve density and distribution. Fed Proc Fed Am Soc Exp Biol 36:2439–2443
Bevan JA, Bevan RD, Purdy RE, Robinson CP, Su C, Waterson JG (1972) Comparison of adrenergic mechanisms in an elastic and a muscular artery of the rabbit. Circ Res 30:541–548
Bevan JA, Bevan RD, Duckles SP (1980) Adrenergic regulation of vascular smooth muscle. In: Bohr DF, Somlyo AP, Sparks HV (eds) Handbook of physiology, cardiovascular system, vascular smooth muscle. Section 2. American Physiological Society, Baltimore, pp 515–566
Blakeley AGH, Brown DA, Cunnane TC, French AM, McGrath JC, Scott NC (1981) Effects of nifedipine on electrical and mechanical responses of rat and guinea-pig vas deferens. Nature 294:759–761
Boatman DL, Shaffer RA, Dixon RL, Brody MJ (1965) Function of vascular smooth muscle and its sympathetic innervation in the newborn dog. J Clin Invest 44:241–246
Bolton TB, Large WA (1986) Are junction potentials essential? Dual mechanism of smooth muscle cell activation by transmitter released from autonomic nerves. Q J Exp Physiol 71:1–28
Brock JA, Cunnane TC (1987) Relationship between the nerve action potential and transmitter release from sympathetic postganglionic nerve terminals. Nature 326:605–607
Brock JA, Cunnane TC (1990) Transmitter release from sympathetic nerve terminals on an impulse-by-impulse basis and presynaptic receptors. Ann N Y Acad Sci 604:176–187
Brock JA, Cunnane TC (1992) Electrophysiology of neuroeffector transmission in smooth muscle. In: Burnstock G, Hoyle CHV (eds) Autonomic neuroeffector mechanisms. Harwood Academic, Chur, Switzerland, pp 121–213
Bunge RP, Bunge MB, Eldridge CF (1986) Linkage between axonal ensheathment and basal lamina production by Schwann cells. Annu Rev Neurosci 9:305–328
Burnstock G (1972) Purinergic nerves. Pharmacol Rev 24:509–581
Burnstock G (1986) Autonomic neuromuscular junctions: current developments and future directions. J Anat 146:1–30
Burnstock G, Costa M (1975) Adrenergic neurons, their organization, function and development in the peripheral nervous system. Chapman and Hall, London
Caesar R, Edwards GA, Ruska H (1957) Architecture and nerve supply of mammalian smooth muscle tissue. J Biophys Biochem Cytol 3:867–891
Cassell JF, McLachlan EM, Sittiracha T (1988) The effect of temperature on neuromuscular transmission in the main caudal artery of the rat. J Physiol (Lond) 397:31–49
Cech S, Dolezel S (1967) Monoaminergic innervation of the pulmonary vessels in various laboratory animals (rat, rabbit, cat). Experientia 23:114–115
Champlain J de, Malmfors T, Olson L, Sachs C (1970) Ontogenesis of peripheral adrenergic neurons in the rat: pre- and postnatal observations. Acta Physiol Scand 80:276–288
Cheung DW (1985) An electrophysiological study of α-adrenoceptor mediated excitation-contraction coupling in the smooth muscle cells of the rat saphenous vein. Br J Pharmacol 84:265–271
Choate JK, Klemm M, Hirst GDS (1993) Sympathetic and parasympathetic neuromuscular junctions in the guinea pig sinoatrial node. J Auton Nerv Syst 44:1–16
Coimbra A, Ribeiro-Silva A, Osswald W (1974) Fine structural and autoradiographical study of the adrenergic innervation of the dog lateral saphenous vein. Blood Vessels 11:128–144
Cowen T (1984a) Image analysis of FITC-immunofluorescence histochemistry in perivascular substance P-positive nerves. Histochemistry 81:609–610
Cowen T (1984b) An ultrastructural comparison of neuromuscular relationships in blood vessels with functional and “non-functional” neuromuscular transmission. J Neurocytol 13:369–392
Cowen T, Burnstock G (1980) Quantitative analysis of the density and pattern of adrenergic innervation of blood vessels. A new method. Histochemistry 66:19–34
Dahlström A, Häggendahl J (1966) Some quantitative studies on the noradrenaline content in the cell bodies and terminals of a sympathetic adrenergic neuron system. Acta Physiol Scand 67:271–277
De Deyn PP, Pickut BA, Verzwijvelen A, D'Hooge R (1989) Subcellular distribution and axonal transport of noradrenaline, dopamine-β-hydroxylase and neuropeptide Y in dog splenic nerve. Neurochem Int 19:39–47
Desmond NL, Levy WB (1988) Synaptic interface surface area increases with long-term potentiation in the hippocampal dentate gyrus. Brain Res 453:308–314
Devine CE, Simpson FO (1967) The fine structure of vascular sympathetic neuromuscular contacts in the rat. Am J Anat 121:153–174
Devine CE, Simpson FO, Bertaud WS (1971) Freeze-etch studies on the innervation of mesenteric arteries and vas deferens. J Cell Sci 9:411–425
Dun WR, Daly CJ, McGrath JC, Wilson VG (1991) The effect of nifedipine on α2-adrenoceptor-mediated contractions in several blood vessels from the rabbit. Br J Pharmacol 103:1493–1499
Evans RJ, Surprenant A (1992) Vasoconstriction of guinea-pig submucosal arterioles following sympathetic nerve stimulation is mediated by the release of ATP. Br J Pharmacol 106:242–249
Falck B, Hillarp N-Å, Thieme G, Torp A (1962) Fluorescence of catechol amines and related compounds condensed with formaldehyde. J Histochem Cytochem 10:348–354
Fillenz M (1970) Innervation of pulmonary and bronchial blood vessels of the dog. J Anat 106:449–461
Fillenz M (1971) Fine structure of noradrenaline storage vesicles in nerve terminals of the rat vas deferens. Phil Trans R Soc Ser B 261:319–323
Fried G, Lundberg JM, Theodorsson-Norheim E (1985) Subcellular storage and axonal transport of neuropeptide Y (NPY) in relation to catecholamines in the cat. Acta Physiol Scand 125:145–154
Furness JB (1973) Arrangement of blood vessels and their relation with adrenergic nerves in the rat mesentery. J Anat 115:347–364
Furness JB, Costa M (1975) 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
Furness JB, Costa M (1987) The Enteric nervous system. Churchill Livingstone, Edinburgh
Gabella G (1974) The sphincter pupillae of the guinea-pig: structure of muscle cells, intercellular relations and density of innervation. Proc R. Soc Lond B 186:369–386
Gabella G (1976) The structure of smooth muscles of the eye and intestine. Raven Press, New York
Gabella G (1992) Fine structure of post-ganglionic nerve fibres and autonomic neuroeffector junctions. In: Burnstock G, Hoyle CHV (eds) Autonomic neuroeffector mechanisms. Harwood Academic, Chur, Switzerland, pp 1–31
Gabella G (1995) The structural relations between nerve fibres and muscle cells in urinary bladder of the rat. J Neurocytol 24:159–187
Gallen DD, Cowen T, Griffith SG, Haven AJ, Burnstock G (1982) Functional and non-functional nerve-smooth muscle transmission in the renal arteries of the newborn and adult rabbit and guniea-pig. Blood Vessels 19:237–246
Geffen LB, Livett BG (1971) Synaptic vesicles in sympathetic neurons. Physiol Rev 51:98–157
Geffen LB, Ostberg A (1969) Distribution of granular vesicles in normal and constricted sympathetic neurones. J Physiol (Lond) 204:583–592
Gordon-Weeks PR (1988) The ultrastructure of noradrenergic and cholinergic neurons in the autonomic nervous system. In: Björklund A, Hökfelt T, Owman C (eds) Handbook of chemical neuroanatomy, vol 6. The peripheral nervous system. Elsevier, Amsterdam, pp 117–142
Gordon-Weeks PR, Hobbs MJ (1979) A non-adrenergic nerve ending containing small granular vesicles in the guniea-pig gut. Neurosci Lett 12:81–86
Gordon-Weeks PR, Burgoyne RD, Gray EG (1982) Presynaptic microtubules: organisation and assembly/disassembly. Neuroscience 7:739–749
Gorgas K (1978) Structure and innervation of the juxtaglomerular apparatus of the rat. Adv Anat Embryol Cell Biol 54:5–84
Gosling JA, Dixon JS (1969) The fine structure of the vasa recta and associated nerves in the rabbit kidney. Anat Rec 165:503–514
Govyrin VA (1976) Spatial neuromuscular relations in rabbit ear arteries. In: Bülbring E, Shuba MF (eds) Physiology of smooth muscle. Raven Press, New York, pp 279–285
Greengard P, Valtorta F, Czernik AJ, Benfenati F (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259:780–785
Griffith SG, Crowe R, Lincoln J, Haven AJ, Burnstock G (1982) Regional differences in the density of perivascular nerves and varicosities, noradrenaline content and responses to nerve stimulation in the rabbit ear artery. Blood Vessels 19:41–52
Häggendal J, Malmfors T (1969) The effect of nerve stimulation on adrenergic nerves after reserpine pretreatment. Acta Physiol Scand 75:33–38
Herrera AA, Grinnell AD, Wolowske B (1985) Ultrastructural correlates of naturally occurring differences in transmitter release efficacy in frog motor nerve terminals. J Neurocytol 14:193–202
Hill CE, Ngu MC (1987) Development of the extrinsic sympathetic innervation to the enteric neurones of the rat small intestine. J Auton Nerv Syst 19:85–93
Hill CE, Hirst GDS, Helden DF van (1983) Development of sympathetic innervation to proximal and distal arteries of the rat mesentery. J Physiol (Lond) 338:129–147
Hill CE, Hirst GDS, Silverberg GD, Helden DF van (1986) Sympathetic innervation and excitability of arterioles originating from the rat middle cerebral artery. J Physiol (Lond) 371:305–316
Hill CE, Klemm M, Edwards FR, Hirst GDS (1993) Sympathetic transmission to the dilator muscle of the rat iris. J Auton Nerv Syst 45:107–123
Hillarp N-Å (1959) The construction and functional organization of the autonomic innervation apparatus. Acta Physiol Scand [Suppl] 46:1–38
Hirst GDS (1977) Neuromuscular transmission in arterioles of guinea-pig submucosa. J Physiol (Lond) 273:263–275
Hirst GDS, Edwards FR (1989) Sympathetic neuroeffector transmission in arteries and arterioles. Physiol Rev 69:546–604
Hirst GDS, Neild TO (1980) Some properties of spontaneous excitatory junction potentials recorded from arterioles of guineapigs. J Physiol (Lond) 303:43–60
Hirst GDS, Gleria S de, Helden DF van (1985) Neuromuscular transmission in arterioles. Experientia 41:874–879
Hökfelt T (1973) On the origin of adrenergic vesicles: evidence for local formation in nerve endings after reserpine treatment. Experientia 29:580–582
Hökfelt T, Jonasson G (1968) Studies on the reaction and binding of monamines after fixation and processing for electron microscopy with potassium permanganate. Histochimie 16:45–67
Holman ME, Kasby CB, Suthers MB, Wilson JAF (1968) Some properties of the smooth muscle of rabbit portal vein. J Physiol (Lond) 196:111–132
Illes P, Ramme D, Starke K (1986) Presynaptic opioid δ-receptors in the rabbit mesenteric artery. J Physiol (Lond) 379:217–228
Iversen LL, Glowinsky J, Axelrod J (1965) The uptake and storage of 3H-norepinephrine in the reserpine-treated rat heart. J Pharmacol Exp Ther 150:173–183
Karashima T, Kuriyama H (1981) Electrical properties of smooth muscle cell membrane and neuromuscular transmission in the guinea pig basilar artery. Brit J Pharmacol 74:495–504
Keatinge WR (1966) Electrical and mechanical responses of arteries to stimulation of sympathetic nerves. J Physiol (Lond) 185:710–715
Klein RL, Lagercrantz H (1981) Noradrenergic vesicles: composition and function. In: Stjärne L, Hedqvist P, Lagercrantz H, Wennmalm A (eds) Chemical neurotransmission — 75 years. Academic Press, London, pp 69–83
Klemm MF, Hirst GDS, Campbell G (1992) Structure of autonomic neuromuscular junctions in the sinus venosus of the toad. J Auton Nerv Syst 39:139–150
Klemm MF, Helden DF van, Luff SE (1993) Ultrastructural analysis of sympathetic neuromuscular junctions on mesenteric veins of the guinea pig. J Comp Neurol 334:159–167
Kügelgen IV, Starke K (1985) Noradrenaline and adenosine triphosphate as co-transmitters of neurogenic vasoconstriction in rabbit mesenteric artery. J Physiol (Lond) 367:435–455
Kuriyama H, Suzuki H (1981) Adrenergic transmission in the guinea pig mesenteric artery and their cholinergic modulations. J Physiol (Lond) 317:383–396
Lasek RJ, Katz MJ (1987) Mechanisms at the axon tip regulate metabolic processes critical to axonal elongation. Prog Brain Res 71:49–60
Lavidis NA, Bennett MR (1992) Probabilistic secretion of quanta from visualized sympathetic nerve varicosities in mouse vas deferens. J Physiol (Lond) 454:9–26
Lee RMKW (1985) Vascular changes at the prehypertensive phase in the mesenteric arteries from spontaneously hypertensive rats. Blood Vessels 22:105–126
Lee TJ-F (1981) Nerve-muscle relationship in cerebral artery. Blood Vessels 18:218
Lever JD, Ahmed M, Irvine G (1965) Neuromuscular and intercellular relationships in the coronary arterioles. A morphological and quantitative study by light and electron microscopy. J Anat 99:829–840
Luff SE (1994) Early postnatal development of the innervation of rat mesenteric arteries. J Hypertens 12:337
Luff SE, McLachlan EM (1988) The form of sympathetic postganglionic axons at clustered neuromuscular junctions near branch points of arterioles in the submucosa of the guniea pig ileum. J Neurocytol 17:451–463
Luff SE, McLachlan EM (1989) Frequency of neuromuscular junctions on arteries of different dimensions in the rabbit, guinea pig and rat. Blood Vessels 26:95–106
Luff SE, McLachlan EM, Hirst GDS (1987) An ultrastructural analysis of the sympathetic neuromuscular junctions on arterioles of the submucosa of the guinea pig ileum. J Comp Neurol 257:578–594
Luff SE, Hengstberger SG, McLachlan EM, Anderson WP (1991) Two types of sympathetic axon innervating the juxtaglomerular arterioles of the rabbit and rat kidney differ structurally from those supplying other arteries. J Neurocytol 20:781–795
Luff SE, Hengstberger SG, McLachlan EM, Anderson WP (1992) Distribution of sympathetic neuroeffector junctions in the juxtaglomerular region of the rabbit kidney. J Auton Nerv Syst 40:239–254
Luff SE, Young SB, McLachlan EM (1995) The proportions and structure of contacting and non-contacting varicosities in the perivascular plexus of the rat tail artery. J Comp Neurol 361:699–709
Lundberg J, Ljung B, Stage D, Dahlström A (1976) Postnatal ontogenic development of the adrenergic innervation pattern in the rat portal vein. Cell Tissue Res 172:15–27
Malmfors T, Sachs C (1965) Direct demonstration of the systems of terminals belonging to an individual adrenergic neuron and their distribution in rat iris. Acta Physiol Scand 64:377–382
Matsuyama T, Shiosaka S, Wanaka A, Yoneda S, Kimura K, Hayakawa T, Emson PC, Tohyama M (1985) Fine structure of peptidergic and catecholaminergic nerve fibers in the anterior cerebral artery and their interrelationship: an immunoelectron microscopic study. J Comp Neurol 235:268–276
McGrath JC, Brown CM, Wilson VG (1989) Alpha-adrenoceptors: a critical review. Med Res Rev 9:407–533
McMahan UJ, Kuffler SW (1971) Visual identification of synaptic boutons on living gangion cells and of varicosities in postganglionic axons in the heart of the frog. Proc R Soc Lond [Biol] 177:485–508
Merrillees NCR (1968) The nervous environment of individual smooth muscle cells of the guinea pig vas deferens. J Cell Biol 37:794–817
Minneman KP (1988) α1-adrenoceptors, inositol phosphates, and sources of cell Ca2+. Pharmacol Rev 40:87–119
Morhri K, Ohgushi N, Ikeda M, Yamamoto K, Tsunekawa T (1969) Histochemical demonstration of adrenergic fibres in smooth muscle layer of media of arteries supplying abdominal organs. Arch Jpn Chir 38:236–248
Morris JL, Gibbins IL (1992) Co-transmission and neuromodulation. In: Burnstock G, Hoyle CHV (eds) Autonomic neuroeffector mechanisms. Harwood Academic, Chur, Switzerland, pp 33–119
Navone F, Jahn R, Di Gioia G, Stukenbrok H, Greengard P, De Camilli P (1986) Protein p38: an integral membrane protein specific for small vesicles of neurons and neuroendocrine cells. J Cell Biol 103:2511–2527
Olson L, Malmfors T (1970) Growth characteristics of adrenergic nerves in the adult rat. Acta Physiol Scand Suppl 348:1–147
Owman C (1988) Autonomic innervation of the cardiovascular system. In: Björklund A, Hökfelt T, Owman C (eds) Handbook of chemical neuroanatomy. The peripheral nervous system. Elsevier, Amsterdem, pp 327–389
Pergram BL, Bevan RD, Bevan JA (1976) Facial vein of the rabbit: neurogenic vasodilation mediated by β-adrenergic receptors. Circ Res 39:854–860
Pierce JP, Lewin GR (1994) An ultrastructural size principle. Neuroscience 58:441–446
Pierce JP, Mendell LM (1993) Quantitative ultrastructure of Ia boutons in the ventral horn: scaling and positional relationships. J Neurosci 13:4748–4763
Potter LT (1967) Role of intraneuronal vesicles in the synthesis, storage and release of noradrenaline. Circ Res Suppl 21:13–24
Propst JW, Ko C (1987) Correlations between active zone ultrastructure and synaptic function studied with freeze-fracture of physiologically identified neuromuscular junctions. J Neurosci 7:3654–3664
Purves D, Lichtman JW (1985) Geometrical differences among homologous neurons in mammals. Science 228:298–302
Purves D, Snider WD, Voyvodic JT (1988) Trophic regulation of nerve cell morphology and innervation in the autonomic nervous system. Nature 336:123–128
Richardson KC (1962) The fine structure of autonomic nerve endings in smooth muscle of the rat vas deferens. J Anat 96:427–442
Rowan RA, Bevan JA (1983) Distribution of adrenergic synaptic cleft width in vascular and nonvascular smooth muscle. In: Bevan JA, Fujiwara M, Maxwell RA, Mohri K, Shibata S, Toda N (eds) Vascular neuroeffector mechanisms: 4th international symposium. Raven Press, New York, pp 75–83
Rowan RA, Bevan JA (1987) Quantitative ultrastructural measurement of innervation density, neurotransmitter vesicles and neuromuscular cleft width in the rabbit central ear artery and its main side branch. Blood Vessels 24:181–191
Rowan RA, Bevan RD, Bevan JA (1981) Ultrastructural features of the innervation and smooth muscle of the rabbit facial vein, and their relationship to function. Circ Res 49:1140–1151
Sittiracha T, McLachlan EM, Bell C (1987) The innervation of the caudal artery of the rat. Neuroscience 21:647–659
Smith AD, Winkler H (1972) Fundamental mechanisms of the release of catecholamines. In: Blaschko H and Muscholl E (eds) Handbook of experimental pharmacology. Springer, Berlin Heidelberg New York, pp 538–617
Smith AD, De Potter WP, Moerman EJ, De Schaepdryver AF (1970) Release of dopamine β-hydroylase and chromogranin A upon stimulation of the splenic nerve. Tissue Cell 2:547–568
Sneddon P, Burnstock G (1984) ATP as a co-transmitter in rat tail artery. Eur J Pharmacol 106:149–152
Stage D, Ljung B (1978) Neuroeffector maturity of portal veins from newborn rat, rabbits, cats and guinea-pigs. Acta Physiol Scand 102:218–223
Stjärne L, Åstrand P (1984) Discrete events measure single quanta of adenosine 5′-triphosphate secreted from sympathetic nerves of guinea-pig and mouse vas deferens. Neuroscience 13:21–28
Surprenant A (1980) A comparative study of neuromuscular transmission in several mammalian muscular arteries. Pflügers Arch 386:85–91
Surprenant A, Neild TO, Holman ME (1987) Membrane properties of the rabbit basilar arteries and their responses to transmural stimulation. Pflügers Arch 410:92–101
Suzuki H (1981) Effects of endogenous and exogenous noradrenaline on the smooth muscle of guinea-pig mesenteric vein. J Physiol (Lond) 321:495–512
Taxi J (1961) On the innervation of the smooth muscle fibres of the mouse intestine. C R Acad Sci III 252:331–333
Taxi PJ (1965) Contribution a l'étude des connexions des neurones moteurs du système nerveux autonomc. Ann Sci Nat Zool Biol Anim 7:413–674
Thaemert JC (1963) The ultrastructure and disposition of vesiculated nerve processes in smooth muscle. J Cell Biol 16:361–377
Thaemert JC (1966) Ultrastructural interralationships of nerve processes and smooth muscle cells in three dimensions. J Cell Biol 28:37–49
Todd ME (1980) Development of adrenergic innervation in rat peripheral vessels: a fluorescence microscopic study. J Anat 131:121–133
Todd ME (1986) Trophic interactions between rat nerves and blood vessels in denervated arteries and in anterior eye chamber transplants. Circ Res 58:641–652
Todd ME, Tokito MK (1981) An ultrastructural investigation of developing vasomotor innervation in rat peripheral vessels. Am J Anat 160:195–212
Tomlinson DR (1975) Two populations of granular vesicles in constricted post-ganglionic sympathetic nerves. J Physiol (Lond) 245:727–735
Torre JC de la (1980) An improved approach to histofluorescence using the SPG method for tissue monoamines. J Neurosci Methods 3:1–5
Tranzer JP (1972) A new amine storing compartment in adrenergic axons. Nature 237:57–58
Tranzer JP, Richards JG (1976) Ultrastructural cytochemistry of biogenic amines in nervous tissue: methodologic improvements. J Histochem Cytochem 24:1178–1193
Tranzer JP, Thoenen H, Snipes RL, Richards JG (1969) Recent developments on the ultrastructural aspect of adrenergic nerve endings in various experimental conditions. Prog Brain Res 31:33–46
Tsunekawa K, Morhri K, Ikeda M, Ohgushi N, Fujiwara M (1967) Histochemical demonstration of adrenergic fibres in the smooth muscle layer of media of dorsal pedal artery in dog. Experientia 23:842–843
Uvnäs B, Åborg CH (1980) Possible role of nerve impulse induced sodium influx in a proposed multivesicular fractional release of adrenaline and noradrenaline from the chromaffin granule. Acta Physiol Scand 109:363–368
Van Helden DF (1988) Electrophysiology of neuromuscular transmission in guinea-pig mesenteric veins. J Physiol (Lond) 401:469–488
Verity MA, Bevan JA (1968) Fine structural study of the terminal effector plexus, neuromuscular and intermuscular relationships in the pulmonary artery. J Anat 103:49–63
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Luff, S.E. Ultrastructure of sympathetic axons and their structural relationship with vascular smooth muscle. Anat Embryol 193, 515–531 (1996). https://doi.org/10.1007/BF00187924
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00187924