Cell and Tissue Research

, Volume 326, Issue 2, pp 205–220 | Cite as

Structure of peripheral synapses: autonomic ganglia

  • Ian L. Gibbins
  • Judy L. Morris


Final motor neurons in sympathetic and parasympathetic ganglia receive synaptic inputs from preganglionic neurons. Quantitative ultrastructural analyses have shown that the spatial distribution of these synapses is mostly sparse and random. Typically, only about 1%–2% of the neuronal surface is covered with synapses, with the rest of the neuronal surface being closely enclosed by Schwann cell processes. The number of synaptic inputs is correlated with the dendritic complexity of the target neuron, and the total number of synaptic contacts is related to the surface area of the post-synaptic neuron. Overall, most neurons receive fewer than 150 synaptic contacts, with individual preganglionic inputs providing between 10 and 50 synaptic contacts. This variation is probably one determinant of synaptic strength in autonomic ganglia. Many neurons in prevertebral sympathetic ganglia receive additional convergent synaptic inputs from intestinofugal neurons located in the enteric plexuses. The neurons support these additional inputs via larger dendritic arborisations together with a higher overall synaptic density. There is considerable neurochemical heterogeneity in presynaptic boutons. Some synapses apparently lack most of the proteins normally required for fast transmitter release and probably do not take part in conventional ganglionic transmission. Furthermore, most preganglionic boutons in the ganglionic neuropil do not form direct synaptic contacts with any neurons. Nevertheless, these boutons may well contribute to slow transmission processes that need not require conventional synaptic structures.


Autonomic ganglion Synapse Ultrastructure Quantification Amphibians Mammals Birds 


  1. Anderson RL, Jobling P, Gibbins IL (2001) Development of electrophysiological and morphological diversity in autonomic neurons. J Neurophysiol 86:1237–1251PubMedGoogle Scholar
  2. Anderson RL, Jobling P, Matthew SE, Gibbins IL (2002) Development of convergent synaptic inputs to subpopulations of autonomic neurons. J Comp Neurol 447:218–233PubMedCrossRefGoogle Scholar
  3. Armour JA, Murphy DA, Yuan BX, MacDonald S, Hopkins DA (1997) Gross and microscopic anatomy of the human intrinsic cardiac nervous system. Anat Rec 247:289–298PubMedCrossRefGoogle Scholar
  4. Asmar R, Kummer W (1993) Ultrastructural connectivity of [leu]5-enkephalin-immunoreactive synapses in the guinea-pig stellate ganglion: involvement of spines and triads. Ann Anat 175:277–281PubMedGoogle Scholar
  5. Baluk P (1986) Scanning electron microscopic studies of bullfrog sympathetic neurons exposed by enzymatic removal of connective tissue elements and satellite cells. J Neurocytol 15:85–95PubMedCrossRefGoogle Scholar
  6. Baluk P, Gabella G (1987) Fine structure of the autonomic ganglia of the mouse pulmonary vein. J Neurocytol 16:169–184PubMedCrossRefGoogle Scholar
  7. Baluk P, Fujiwara T, Matsuda S (1985) The fine structure of the ganglia of the guinea-pig trachea. Cell Tissue Res 239:51–60PubMedCrossRefGoogle Scholar
  8. Beckers HJ, Klooster J, Vrensen GF, Lamers WP (1991) Ultrastructural identification of trigeminal nerve terminals in the pterygopalatine ganglion of rats: an anterograde tracing and immunohistochemical study. Brain Res 557:22–30PubMedCrossRefGoogle Scholar
  9. Benfares J, Henry M, Cupo A, Jule Y (1995) An immunoelectron microscopic study of methionine-enkephalin structures in cat prevertebral ganglia. Neuropeptides 28:131–136PubMedCrossRefGoogle Scholar
  10. Boyd HD, McLachlan EM, Keast JR, Inokuchi H (1996) Three electrophysiological classes of guinea pig sympathetic postganglionic neurone have distinct morphologies. J Comp Neurol 369:372–387PubMedCrossRefGoogle Scholar
  11. Brookes SJH, Costa M (eds) (2002) Innervation of the gastrointestinal tract. Taylor & Francis, London New YorkGoogle Scholar
  12. Cajal SR y (1995) Histology of the nervous system of man and vertebrates (translated by N. Swanson, L. Swanson). Oxford University Press, New YorkGoogle Scholar
  13. Cantino D, Mugnaini E (1975) The structural basis for electrotonic coupling in the avian ciliary ganglion. A study with thin sectioning and freeze-fracturing. J Neurocytol 4:505–536PubMedCrossRefGoogle Scholar
  14. Coggan JS, Paysan J, Conroy WG, Berg DK (1997) Direct recording of nicotinic responses in presynaptic nerve terminals. J Neurosci 17:5798–5806PubMedGoogle Scholar
  15. Coggan JS, Bartol TM, Esquenazi E, Stiles JR, Lamont S, Martone ME, Berg DK, Ellisman MH, Sejnowski TJ (2005) Evidence for ectopic neurotransmission at a neuronal synapse. Science 309:446–451PubMedCrossRefGoogle Scholar
  16. Conroy WG, Liu ZP, Nai Q, Coggan JS, Berg DK (2003) Pdz-containing proteins provide a functional postsynaptic scaffold for nicotinic receptors in neurons. Neuron 38:759–771PubMedCrossRefGoogle Scholar
  17. Cornbrooks EB, Pouliot WA, Mawe GM (1992) Structure of neurons and ganglia of the guinea pig gallbladder: light and electron microscopic studies. J Comp Neurol 317:31–44PubMedCrossRefGoogle Scholar
  18. De Lorenzo AJ (1966) Electron microscopy: tight junctions in synapses of the chick ciliary ganglion. Science 152:76–78PubMedCrossRefGoogle Scholar
  19. De Stefano ME, Ciofi Luzzatto A, Mugnaini E (1993) Neuronal ultrastructure and somatostatin immunolocalization in the ciliary ganglion of chicken and quail. J Neurocytol 22:868–892PubMedCrossRefGoogle Scholar
  20. Dennis MJ, Sargent PB (1978) Multiple innervation of normal and re-innervated parasympathetic neurones in the frog cardiac ganglion. J Physiol (Lond) 281:63–75Google Scholar
  21. Dickinson-Nelson A, Reese TS (1983) Structural changes during transmitter release at synapses in the frog sympathetic ganglion. J Neurosci 3:42–52PubMedGoogle Scholar
  22. Edwards FR, Hirst GD, Klemm MF, Steele PA (1995) Different types of ganglion cell in the cardiac plexus of guinea-pigs. J Physiol (Lond) 486:453–471Google Scholar
  23. Ehinger B, Sundler F, Uddman R (1983) Functional morphology in two parasympathetic ganglia: the ciliary and pterygopalatine. In: Elfvin LG (ed) Autonomic ganglia. Wiley, Chichester New York, pp 97–123Google Scholar
  24. Elfvin LG (1976) The ultrastructure of neuronal contacts. Progr Neurobiol 8:45–79CrossRefGoogle Scholar
  25. Elfvin LG (1983) Autonomic ganglia. Wiley, Chichester New YorkGoogle Scholar
  26. Elfvin LG, Lindh B, Hökfelt T, Terenius L (1989) An ultrastructural study of dynorphin-immunoreactive nerve fibers and terminals in the celiac-superior mesenteric ganglion of the guinea pig. Brain Res 502:341–348PubMedCrossRefGoogle Scholar
  27. Elfvin LG, Lindh B, Hökfelt T (1993) The chemical neuroanatomy of sympathetic ganglia. Annu Rev Neurosci 16:471–507PubMedCrossRefGoogle Scholar
  28. Forehand CJ (1985) Density of somatic innervation on mammalian autonomic ganglion cells is inversely related to dendritic complexity and preganglionic convergence. J Neurosci 5:3403–3408PubMedGoogle Scholar
  29. Forehand CJ (1987) Ultrastructural analysis of the distribution of synaptic boutons from labeled preganglionic axons on rabbit ciliary neurons. J Neurosci 7:3274–3281PubMedGoogle Scholar
  30. Forehand CJ, Konopka LM (1989) Frog sympathetic ganglion cells have local axon collaterals. J Comp Neurol 289:294–303PubMedCrossRefGoogle Scholar
  31. Furness JB (2003) Intestinofugal neurons and sympathetic reflexes that bypass the central nervous system. J Comp Neurol 455:281–284PubMedCrossRefGoogle Scholar
  32. Furness JB (2006a) The enteric nervous system. Blackwell, Massachusetts Oxford CarltonGoogle Scholar
  33. Furness JB (2006b) Novel gut afferents: intrinsic afferent neurons and intestinofugal neurons. Auton Neurosci 125:81–85PubMedCrossRefGoogle Scholar
  34. Furness JB, Morris JL, Gibbins IL, Costa M (1989) Chemical coding of neurons and plurichemical transmission. Annu Rev Pharmacol Toxicol 29:289–306PubMedCrossRefGoogle Scholar
  35. Gabella G (1976) Structure of the autonomic nervous system. Chapman & Hall, LondonGoogle Scholar
  36. Gabella G (1979) Innervation of the gastrointestinal tract. Int Rev Cytol 59:129–193PubMedCrossRefGoogle Scholar
  37. Gibbins IL (1991) Vasomotor, pilomotor and secretomotor neurons distinguished by size and neuropeptide content in superior cervical ganglia of mice. J Autonom Nerv Syst 34:171–183CrossRefGoogle Scholar
  38. Gibbins IL (1995) Chemical neuroanatomy of sympathetic ganglia. In: McLachlan EM (ed) Autonomic ganglia. Harwood, Luxembourg, pp 73–121Google Scholar
  39. Gibbins IL, Matthew SE (1996) Dendritic morphology of presumptive vasoconstrictor and pilomotor neurons and their relations with neuropeptide-containing preganglionic fibres in lumbar sympathetic ganglia of guinea-pigs. Neuroscience 70:999–1012PubMedCrossRefGoogle Scholar
  40. Gibbins IL, Rodgers HF, Matthew SE, Murphy SM (1998) Synaptic organisation of lumbar sympathetic ganglia of guinea pigs: serial section ultrastructural analysis of dye-filled sympathetic final motor neurons. J Comp Neurol 402:285–302PubMedCrossRefGoogle Scholar
  41. Gibbins IL, Teo EH, Jobling P, Morris JL (2003a) Synaptic density, convergence and dendritic complexity of prevertebral sympathetic neurons. J Comp Neurol 455:285–298PubMedCrossRefGoogle Scholar
  42. Gibbins IL, Jobling P, Teo EH, Matthew S, Morris JL (2003b) Heterogeneous expression of SNAP-25 and synaptic vesicle proteins by central and peripheral inputs to sympathetic neurons. J Comp Neurol 459:25–43PubMedCrossRefGoogle Scholar
  43. Grkovic I, Edwards SL, Murphy SM, Anderson CR (1999) Chemically distinct preganglionic inputs to iris-projecting postganglionic neurons in the rat: a light and electron microscopic study. J Comp Neurol 412:606–616PubMedCrossRefGoogle Scholar
  44. Hess A, Pilar G, Weakly JN (1969) Correlation between transmission and structure in avian ciliary ganglion synapses. J Physiol (Lond) 202:339–354Google Scholar
  45. Hume RI, Purves D (1983) Apportionment of the terminals from single preganglionic axons to target neurones in the rabbit ciliary ganglion. J Physiol (Lond) 338:259–275Google Scholar
  46. Jacob MH, Berg DK (1983) The ultrastructural localization of alpha-bungarotoxin binding sites in relation to synapses on chick ciliary ganglion neurons. J Neurosci 3:260–271PubMedGoogle Scholar
  47. Jänig W (1995) Ganglionic transmission in vivo. In: McLachlan EM (ed) Autonomic ganglia. Harwood, Luxembourg, pp 349–395Google Scholar
  48. Järvi R (1989) Localization of bombesin-, neuropeptide Y-, enkephalin- and tyrosine hydroxylase-like immunoreactivities in rat coeliac-superior mesenteric ganglion. Histochemistry 92:231–236PubMedCrossRefGoogle Scholar
  49. Jobling P, Gibbins IL (1999) Electrophysiological and morphological diversity of mouse sympathetic neurons. J Neurophysiol 82:2747–2764PubMedGoogle Scholar
  50. Jobling P, Messenger JM, Gibbins IL (2001) Differential expression of functionally identified and immunohistochemically identified NK1 receptors on sympathetic neurons. J Neurophysiol 85:1888–1898PubMedGoogle Scholar
  51. Jobling P, Gibbins IL, Morris JL (2003) Functional organization of vasodilator neurons in pelvic ganglia of female guinea-pigs: comparison with uterine motor neurons. J Comp Neurol 459:223–241PubMedCrossRefGoogle Scholar
  52. Jobling P, Gibbins IL, Lewis RJ, Morris JL (2004) Differential expression of calcium channels in sympathetic and parasympathetic preganglionic inputs to neurons in paracervical ganglia of guinea-pigs. Neuroscience 127:455–466PubMedCrossRefGoogle Scholar
  53. Karila P, Horn JP (2000) Secondary nicotinic synapses on sympathetic B neurons and their putative role in ganglionic amplification of activity. J Neurosci 20:908–918PubMedGoogle Scholar
  54. Kawai Y (1996) Ultrastructure of neuronal circuitry in sympathetic ganglia. Microsc Res Tech 35:146–156PubMedCrossRefGoogle Scholar
  55. Kawai Y, Senba E (1995) Correlation between dendrodendritic synapses of adrenergic type and synaptically evoked hyperpolarization in the sympathetic ganglion of adult rats. Neuroscience 68:925–935PubMedCrossRefGoogle Scholar
  56. Kawai Y, Senba E (1997) Noradrenaline-mediated lateral inhibition in the sympathetic ganglion. Neurosci Lett 238:87–89PubMedCrossRefGoogle Scholar
  57. Kawai Y, Tamai Y, Senba E (1993) Principal neurons as local circuit neurons in the rat superior cervical ganglion: the synaptology of the neuronal processes revealed by intracellular injection of biocytin. J Comp Neurol 328:562–574PubMedCrossRefGoogle Scholar
  58. Kondo H, Yui R (1981) An electron microscopic study on substance P-like immunoreactive nerve fibers in the celiac ganglion of guinea pigs. Brain Res 222:134–137PubMedCrossRefGoogle Scholar
  59. Kondo H, Yui R (1982) An electron microscopic study on enkephalin-like immunoreactive nerve fibers in the celiac ganglion of guinea pigs. Brain Res 252:142–145PubMedCrossRefGoogle Scholar
  60. Kreulen D, Peters (1986) Non-cholinergic transmission in a sympathetic ganglion of the guinea-pig elicited by colon distension. J Physiol (Lond) 374:315–334Google Scholar
  61. Kummer W (1992) Ultrastructure of calcitonin gene-related peptide-immunoreactive nerve fibres in guinea-pig peribronchial ganglia. Regul Pept 37:135–142PubMedCrossRefGoogle Scholar
  62. Lascar G, Eugene D, Taxi J (1996) Synaptic organization of amphibian sympathetic ganglia. Microsc Res Tech 35:157–178PubMedCrossRefGoogle Scholar
  63. Li ZS, Furness JB (2000) Inputs from intrinsic primary afferent neurons to nitric oxide synthase-immunoreactive neurons in the myenteric plexus of guinea pig ileum. Cell Tissue Res 299:1–8PubMedCrossRefGoogle Scholar
  64. Lindh B, Hökfelt T, Elfvin LG (1988) Distribution and origin of peptide-containing nerve fibers in the celiac superior mesenteric ganglion of the guinea-pig. Neuroscience 26:1037–1071PubMedCrossRefGoogle Scholar
  65. 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 10:331–352PubMedCrossRefGoogle Scholar
  66. Llewellyn-Smith IJ, Furness JB, Costa M (1989) Ultrastructural analysis of substance P-immunoreactive nerve fibers in myenteric ganglia of guinea pig small intestine. J Neurosci 9:167–174PubMedGoogle Scholar
  67. Lysakowski A, Figueras H, Price SD, Peng YY (1999) Dense-cored vesicles, smooth endoplasmic reticulum, and mitochondria are closely associated with non-specialized parts of plasma membrane of nerve terminals: implications for exocytosis and calcium buffering by intraterminal organelles. J Comp Neurol 403:378–390PubMedCrossRefGoogle Scholar
  68. Marshall LM (1981) Synaptic localization of alpha-bungarotoxin binding which blocks nicotinic transmission at frog sympathetic neurons. Proc Natl Acad Sci USA 78:1948–1952PubMedCrossRefGoogle Scholar
  69. Martin AR, Pilar G (1964) An analysis of electrical coupling at synapses in the avian ciliary ganglion. J Physiol (Lond) 171:454–475Google Scholar
  70. Masuko S, Chiba T (1988) Projection pathways, co-existence of peptides and synaptic organization of nerve fibers in the inferior mesenteric ganglion of the guinea-pig. Cell Tissue Res 253:507–516PubMedCrossRefGoogle Scholar
  71. Matthews MR (1983) The ultrastructure of junctions in sympathetic ganglia of mammals. In: Elvin LG (ed) Autonomic ganglia. Wiley, Chichester New York, pp 27–66Google Scholar
  72. Matthews MR, Cuello AC (1984) The origin and possible significance of substance P immunoreactive networks in prevertebral ganglia and related structures in the guinea-pig. Philos Trans Roy Soc Lond Biol 306:247–276CrossRefGoogle Scholar
  73. Mawe GM (1995) Prevertebral, pancreatic and gallbladder ganglia: non-enteric ganglia that are involved in gastrointestinal function. In: McLachlan EM (ed) Autonomic ganglia. Harwood, Luxembourg, pp 397–444Google Scholar
  74. May PJ, Warren S (1993) Ultrastructure of the macaque ciliary ganglion. J Neurocytol 22:1073–1095PubMedCrossRefGoogle Scholar
  75. McLachlan EM (1995) Autonomic ganglia. Harwood, LuxembourgGoogle Scholar
  76. McLachlan EM, Meckler R (1989) Characteristics of synaptic input to three classes of sympathetic neurone in the coeliac ganglion of the guinea-pig. J Physiol (Lond) 415:109–129Google Scholar
  77. McMahan UJ, Purves D (1976) Visual identification of two kinds of nerve cells and their synaptic contacts in a living autonomic ganglion of the mudpuppy (Necturus maculosus). J Physiol (Lond) 254:405–425Google Scholar
  78. Messenger JP, Anderson RL, Gibbins IL (1999) Neurokinin-1 receptor localization in guinea-pig autonomic ganglia. J Comp Neurol 412:693–704PubMedCrossRefGoogle Scholar
  79. Miller SM, Szurszewski JH (1997) Colonic mechanosensory afferent input to neurons in the mouse superior mesenteric ganglion. Am J Physiol Gastro Liver Physiol 35:G357–G366Google Scholar
  80. Morris JL, Gibbins IL (1992) Co-transmission and neuromodulation. In: Burnstock G, Hoyle C (eds) The autonomic nervous system, vol 1. Autonomic neuroeffector mechanisms. Harwood, Chur, Switzerland, pp 33–119Google Scholar
  81. Morris JL, König P, Shimizu T, Jobling P, Gibbins IL (2005) Most peptide-containing sensory neurons lack proteins for exocytotic release and vesicular transport of glutamate. J Comp Neurol 483:1–16PubMedCrossRefGoogle Scholar
  82. Motosugi H, Chiba T, Konno A, Kaneko T (1992) Distribution of neuropeptides in rat pterygopalatine ganglion: light and electron microscopic immunohistochemical studies. Arch Histol Cytol 55:513–524PubMedCrossRefGoogle Scholar
  83. Murata Y, Chiba T, Kumamoto E, Kuba K (1989) Synaptic structure and axon collaterals of type B neurons in bullfrog sympathetic ganglia: intracellular horseradish peroxidase (HRP)-labeling study. Neurosci Res 7:33–42PubMedCrossRefGoogle Scholar
  84. Murphy SM, Matthew SE, Rodgers HF, Lituri DT, Gibbins IL (1998) Synaptic organisation of neuropeptide-containing preganglionic boutons in lumbar sympathetic ganglia of guinea pigs. J Comp Neurol 398:551–567PubMedCrossRefGoogle Scholar
  85. Myers AC (2000) Anatomical characteristics of tonic and phasic postganglionic neurons in guinea pig bronchial parasympathetic ganglia. J Comp Neurol 419:439–450PubMedCrossRefGoogle Scholar
  86. Myers A, Undem B, Kummer W (1996) Anatomical and electrophysiological comparison of the sensory innervation of bronchial and tracheal parasympathetic ganglion neurons. J Auton Nerv Syst 61:162–168PubMedCrossRefGoogle Scholar
  87. Ng YK, Wong WC, Ling EA (1992) The intraglandular submandibular ganglion of postnatal and adult rats. I. A light and electron microscope study. J Anat 180:305–314PubMedGoogle Scholar
  88. Nguyen D, Sargent PB (2002) Synaptic vesicle recycling at two classes of release sites in giant nerve terminals of the embryonic chicken ciliary ganglion. J Comp Neurol 448:128–137PubMedCrossRefGoogle Scholar
  89. Paysan J, Conroy WG, Coggan JS, Berg DK (2000) The neurofilament infrastructure of a developing presynaptic calyx. J Comp Neurol 425:284–294PubMedCrossRefGoogle Scholar
  90. Pick (1970) The autonomic nervous system; morphological, comparative, clinical and surgical aspects. Lippincott, PhiladelphiaGoogle Scholar
  91. Pomeroy SL, Purves D (1988) Neuron/glia relationships observed over intervals of several months in living mice. J Cell Biol 107:1167–1175PubMedCrossRefGoogle Scholar
  92. Pompolo S, Furness JB (1993) Origins of synaptic inputs to calretinin immunoreactive neurons in the guinea-pig small intestine. J Neurocytol 22:531–546PubMedCrossRefGoogle Scholar
  93. Pompolo S, Furness JB (1998) Quantitative analysis of inputs to somatostatin-immunoreactive descending interneurons in the myenteric plexus of the guinea-pig small intestine. Cell Tissue Res 294:219–226PubMedCrossRefGoogle Scholar
  94. Portbury AL, Pompolo S, Furness JB, Stebbing MJ, Kunze WA, Bornstein JC, Hughes S (1995) Cholinergic, somatostatin-immunoreactive interneurons in the guinea pig intestine: morphology, ultrastructure, connections and projections. J Anat 187:303–321PubMedGoogle Scholar
  95. Purves D (1988) Body and brain: a trophic theory of neural connections. Harvard University Press, Cambridge, Mass.Google Scholar
  96. Quinson N, Robbins HL, Clark MJ, Furness JB (2001) Locations and innervation of cell bodies of sympathetic neurons projecting to the gastrointestinal tract in the rat. Arch Histol Cytol 64:281–294PubMedCrossRefGoogle Scholar
  97. Robertson GN, Jackson PC (1996) Axosomatic synapses of the rat ciliary ganglion. Synapse 22:269–280PubMedCrossRefGoogle Scholar
  98. Sargent PB (1983) The number of synaptic boutons terminating on Xenopus cardiac ganglion cells is directly correlated with cell size. J Physiol (Lond) 343:85–104Google Scholar
  99. Sargent PB, Pang DZ (1989) Acetylcholine receptor-like molecules are found in both synaptic and extrasynaptic clusters on the surface of neurons in the frog cardiac ganglion. J Neurosci 9:1062–1072PubMedGoogle Scholar
  100. Sargent PB, Garrett EN (1995) The characterization of alpha-bungarotoxin receptors on the surface of parasympathetic neurons in the frog heart. Brain Res 680:99–107PubMedCrossRefGoogle Scholar
  101. Shoop RD, Martone ME, Yamada N, Ellisman MH, Berg DK (1999) Neuronal acetylcholine receptors with alpha7 subunits are concentrated on somatic spines for synaptic signaling in embryonic chick ciliary ganglia. J Neurosci 19:692–704PubMedGoogle Scholar
  102. Shoop RD, Esquenazi E, Yamada N, Ellisman MH, Berg DK (2002) Ultrastructure of a somatic spine mat for nicotinic signaling in neurons. J Neurosci 22:748–756PubMedGoogle Scholar
  103. Smith PA (1994) Amphibian sympathetic ganglia: an owner’s and operator’s manual. Prog Neurobiol 43:439–510PubMedCrossRefGoogle Scholar
  104. Taxi JP (1976) Morphology of the autonomic nervous system. In: Llinas R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg New York, pp 93–150Google Scholar
  105. Watanabe H (1983) The organization and fine structure of autonomic ganglia of amphibia. In: Elfvin LG (ed) Autonomic ganglia. Wiley, Chichester New York, pp 183–201Google Scholar
  106. Watanabe H, Burnstock G (1976) Junctional subsurface organs in frog sympathetic ganglion cells. J Neurocytol 5:125–136PubMedCrossRefGoogle Scholar
  107. Weitsen HA, Weight FF (1977) Synaptic innervation of sympathetic ganglion cells in the bullfrog. Brain Res 128:197–211PubMedCrossRefGoogle Scholar
  108. Wilson AJ, Furness JB, Costa M (1981a) The fine structure of the submucous plexus of the guinea-pig ileum. I. The ganglia, neurons, Schwann cells and neuropil. J Neurocytol 10:759–784PubMedCrossRefGoogle Scholar
  109. Wilson AJ, Furness JB, Costa M (1981b) The fine structure of the submucous plexus of the guinea-pig ileum. II. Description and analysis of vesiculated nerve profiles. J Neurocytol 10:785–804PubMedCrossRefGoogle Scholar
  110. Wilson Horch HL, Sargent PB (1996) Synaptic and extrasynaptic distribution of two distinct populations of nicotinic acetylcholine receptor clusters in the frog cardiac ganglion. J Neurocytol 25:67–77PubMedCrossRefGoogle Scholar
  111. Yamakado M, Yohro T (1977) Population and structure of nerve cells in mouse submandibular ganglion. Anat Embryol 150:301–312PubMedCrossRefGoogle Scholar
  112. Yokota R, Burnstock G (1983) Synaptic organisation of the pelvic ganglion in the guinea-pig. Cell Tissue Res 232:379–397PubMedCrossRefGoogle Scholar
  113. Young HM, Furness JB (1995) Ultrastructural examination of the targets of serotonin-immunoreactive descending interneurons in the guinea pig small intestine. J Comp Neurol 356:101–114PubMedCrossRefGoogle Scholar
  114. Zaidi ZF, Matthews MR (1997) Exocytotic release from neuronal cell bodies, dendrites and nerve terminals in sympathetic ganglia of the rat, and its differential regulation. Neuroscience 80:861–891PubMedCrossRefGoogle Scholar
  115. Zhao FY, Saito K, Yoshioka K, Guo JZ, Murakoshi T, Konishi K, Otsuka M (1996) Tachykininergic synaptic transmission in the coeliac ganglion of the guinea-pig. Br J Pharmacol 118:2059–2066PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of Anatomy & Histology, and Centre for NeuroscienceFlinders UniversityAdelaideAustralia

Personalised recommendations