Skip to main content

The History of the Neuronal Nicotinic Receptors

  • Chapter

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 144))

Abstract

Studies on neuronal nicotinic receptors really started with the experiments of LANGLEY and DICKENSON in 1889 on the cat superior cervical ganglion. In fact, they were not particularly interested in the action of nicotine as such, but were employing it as a tool to map out the distribution of the sympathetic fibres. For this, they used it as a blocking agent rather than as a stimulating agent. However, they did define its site of action quite precisely, as the following quotation from their paper shows:

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Armett CJ, Ritchie JM (1960) The action of acetylcholine on conduction in mammalian non-myelinated fibres and its prevention by an anticholinesterase. J Physiol 152:141–158

    CAS  PubMed  Google Scholar 

  • Armett CJ, Ritchie JM (1961) The action of acetylcholine and some related substances on conduction in mammalian non-myelinated nerve fibres. J Physiol 155:372–384

    CAS  PubMed  Google Scholar 

  • Ascher P, Large WA, Rang HP (1979) Studies on the mechanism of action of acetylcholine antagonists on rat parasympathetic ganglion cells. J Physiol 295:139–170

    CAS  PubMed  Google Scholar 

  • Berger F, Gage FH, Vijayaraghavan S (1998) Nicotinic receptor-induced apoptotic cell death of hippocampal progenitor cells. J Neurosci 18:6871–6881

    CAS  PubMed  Google Scholar 

  • Bertrand D, Galzi JL, Devillers-Thiery A, Bertrand S, Changeux JP (1993) Mutations at two distinct sites within the channel domain M2 alter calcium permeability of neuronal α7 nicotinic receptor. Proc Natl Acad Sci USA 90:6971–6975

    Article  CAS  PubMed  Google Scholar 

  • Blackman JG (1959) PhD Thesis, University of Otago

    Google Scholar 

  • Blackman JG (1970) Dependence on membrane potential of the blocking action of hexamethonium at a sympathetic ganglionic synapse. Proc Univ Otago Med Sch 48:4–5

    Google Scholar 

  • Bowman WC, Marshall IG, Gibb AJ, Harborne AJ (1988) Feedback control of transmitter release at the neuromuscular junction. Trends in Pharmacol Sci 9:16–20

    Article  CAS  Google Scholar 

  • Briggs CA (1995) Long-term potentiation of synaptic transmission in the sympathetic ganglion: multiple types and mechanisms. In: McLachlan EM (ed) Autonomic Ganglia. Harwood Academic, Luxembourg, pp 297–348

    Google Scholar 

  • Brown DA (1979) Neurotoxins and the ganglionic (C6) type of nicotinic receptor. In: Ceccarelli B, Clementi F (eds) Advances in Cytopharmacology, vol 3. Raven, New York, pp 225–230

    Google Scholar 

  • Brown DA, Adams PR, Higgins AJ, Marsh SJ (1979) Distribution of GABA-receptor and GABA-carriers in the mammalian nervous systems. J Physiol Paris 75:667–671

    CAS  PubMed  Google Scholar 

  • Brown DA, Docherty RJ, Halliwell JV (1983) Chemical transmission in the rat interpeduncular nucleus in vitro. J Physiol 341:655–670

    CAS  PubMed  Google Scholar 

  • Brown DA, Docherty RJ, Halliwell JV (1984) The action of cholinomimetic substances on impulse conduction in the habenulointerpeduncular pathway of the rat in vitro. J Physiol 353:101–109

    CAS  PubMed  Google Scholar 

  • Brown DA, Garthwaite J, Hayashi E, Yamada S (1976) Action of surugatoxin on the nicotinic receptors in the superior cervical ganglion of the rat. Br J Pharmacol 58:157–159

    Article  CAS  PubMed  Google Scholar 

  • Brown DA, Jones KB, Halliwell JV, Quilliam JP (1970) Evidence against a presynaptic action of acetylcholine during ganglionic transmission. Nature 226:958–959

    Article  CAS  PubMed  Google Scholar 

  • Cannon WB, Aub JC, Binger CAL (1912) A note on the effect of nicotin injection on adrenal secretion. J Pharmacol Exper Ther 3:379–388

    CAS  Google Scholar 

  • Clarke PBS (1987) Recent progress in identifying nicotinic cholinoceptors in mammalian brain. Trends in Pharmacol Sci 8:32–35

    Article  CAS  Google Scholar 

  • Clarke PBS, Hommer DW, Pert A, Skirboll LR (1987) Innervation of substantia nigra neurons by cholinergic afferents from the pedunculopontine nucleus in rats: neuroanatomical and electrophysiological evidence. Neuroscience 23:1011–1020

    Article  CAS  PubMed  Google Scholar 

  • Coggan JS, Paysan J, Conroy WG, Berg D (1997) Direct recording of nicotinic responses in presynaptic nerve terminals. J Neurosci 17:5798–5806

    CAS  PubMed  Google Scholar 

  • Couturier S, Bertrand D, Matter J-M, Hernandez M-C, Bertrand S, Millar N, Valera S, Barkas T, Ballivet M (1990) A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-Btx. Neuron 5:847–856

    Article  CAS  PubMed  Google Scholar 

  • Covernton PJO, Kojima H, Sivilotti L, Gibb AJ, Colquhoun D (1994) Comparison of neuronal nicotinic receptors in rat sympathetic neurones with subunit pairs expressed in Xenopus oocytes. J Physiol 481:27–34

    CAS  PubMed  Google Scholar 

  • Craig CR, Curtis DR, Lodge D (1977) Dual effects of hemicholinium-3 at central synapses. J Physiol 264:367–377

    CAS  PubMed  Google Scholar 

  • Dale HH, Laidlaw PP (1912) The significance of the supra-renal capsules in the action of certain alkaloids. J Physiol 45:1–26

    CAS  PubMed  Google Scholar 

  • Duggan AW, Hall JG, Headley PM, Hendry A, Minchin MCW (1976a) Absence of binding of α-bungarotoxin and cobra neurotoxin to central acetylcholine receptors—an autoradiographic study. Neurosci Lett 3:123–127

    Article  CAS  PubMed  Google Scholar 

  • Duggan AW, Hall JG, Lee CY (1976b) Alpha-bungarotoxin cobra neurotoxin and excitation of Renshaw cells by acetylcholine. Brain Res 107:166–170

    Article  CAS  PubMed  Google Scholar 

  • Eccles JC, Eccles RM, Fatt P (1956) Pharmacological investigations on a central synapse operated by acetylcholine. J Physiol 131:154–169

    CAS  PubMed  Google Scholar 

  • Eccles JC, Fatt P, Koketsu K (1954) Cholinergic and inhibitory synapses in a pathway from motor axon colaterals to motoneurones. J Physiol 126:524–562

    CAS  PubMed  Google Scholar 

  • Fumagalli L, De Renzis G, Miani N (1976) Acetylcholine receptors: number and distribution in intact and deafferented superior cervical ganglion of the rat. J Neurochem 27:47–52

    Article  CAS  PubMed  Google Scholar 

  • Futami T, Takakusaki K, Kitai ST (1995) Glutamatergic and cholinergic inputs from the pedunculo-pontine tegmental nucleus to dopamine neurons in the substantia nigra pars compacta. Neurosci Res 21:331–342

    Article  CAS  PubMed  Google Scholar 

  • Goodman AG, Gilman LS (1980) The pharmacological basis of therapeutics, 6th edn. Macmillan, New York, p 217

    Google Scholar 

  • Gray R, Rajan AS, Radcliffe KA, Yakehoiro M, Dani JA (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383:713–716

    Article  CAS  PubMed  Google Scholar 

  • Greene LA (1976) Binding of alpha-bungarotoxin to chick sympathetic ganglia: properties of the receptor and its rate of appearance during development. Brain Res 111:135–145

    Article  CAS  PubMed  Google Scholar 

  • Ginsborg BL, Guererro S (1964) On the action of depolarizing drugs on sympathetic ganglion cells of the frog. J Physiol 172:189–206

    CAS  PubMed  Google Scholar 

  • Gurney AM, Rang HP (1984) The channel-blocking action of methonium compounds on rat submandibular ganglion cells. Br J Pharmacol 82:623–642

    Article  CAS  PubMed  Google Scholar 

  • Hayashi E, Yamada S (1975) Pharmacological studies on surugatoxin the toxin principle from Japanese ivory mollusc. Br J Pharmacol 53:207–215

    Article  CAS  PubMed  Google Scholar 

  • Hefft S, Hulo S, Bertrand D, Muller D (1999) Synaptic transmission at nicotinic acetyl-choline receptors in rat hippocampal organotypic cultures and slices. J Physol 515:769–776

    Article  CAS  Google Scholar 

  • Koelle GB (1961) A proposed dual neurohumoral role of acetylcholine: its functions at the pre-and postsynaptic sites. Nature 190:208–211

    Article  CAS  PubMed  Google Scholar 

  • Kuryatov A, Gerzanich V, Nelson M, Olale F, Lindstrom J (1997) Mutation causing autosomal dominant nocturnal frontal lobe epilepsy alters Ca2+ permeability conductance and gating of human α4β2 nicotinic acetylcholine receptors. J Neurosci 17:9035–9047

    CAS  PubMed  Google Scholar 

  • Langley JN (1909) On the contraction of muscle chiefly in relation to the presence of “receptive” substances. Part IV The effect of curari and of some other substances on the nicotine response of the sartorius and gastrocnemius muscles of the frog. J Physiol 39:235–239

    CAS  PubMed  Google Scholar 

  • Langley JN, Dickenson WL (1889) On the local paralysis of peripheral ganglia and on the connexion of different classes of nerve fibres within them. Proc Roy Soc (Lond) 46:423–431

    Article  Google Scholar 

  • Liang SD, Vizi ES (1997) Positive feedback modulation of acetylcholine release from isolated rat superior vertical ganglion. J Pharmacol Exp Ther 280:650–655

    CAS  PubMed  Google Scholar 

  • Loring RH, Zigmond RE (1988) Characterization of neuronal nicotinic receptors by snake venom neurotoxins. Trends in Neurosci 11:73–78

    Article  CAS  Google Scholar 

  • Luetje CW, Patrick J (1991) Both α-and β-subunits contribute to the agonist sensitivity of neuronal nicotinic acetylcholine receptors. J Neurosci 11:837–845

    CAS  PubMed  Google Scholar 

  • Marsh SJ, Trouslard J, Leaney JA, Brown DA (1995) Synergistic regulation of a neuronal chloride current by intracellular calcium and muscarinic receptor activation: a role for protein kinase C. Neuron 15:729–737

    Article  CAS  PubMed  Google Scholar 

  • McGehee DS, Heath MJS, Gelber S, Devay P, Role LW (1995) Nicotine enhancement of excitatory synaptic transmission in CNS by presynaptic receptors. Science 269:1692–1696

    Article  CAS  PubMed  Google Scholar 

  • McGehee DS, Role LW (1995) Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Ann Rev Physiol 57:521–546

    Article  CAS  Google Scholar 

  • McGehee DS, Role LW (1996) Presynaptic ionotropic receptors. Curr Op Neurobiol 6:342–349

    Article  CAS  PubMed  Google Scholar 

  • Messing RO, Stevens AM, Kitasu E, Sneade AN (1989) Nicotinic and muscarinic agonists stimulate rapid protein kinase C translocation in PC12 cells. J Neurosci 9:507–512

    CAS  PubMed  Google Scholar 

  • Mulle C, Vidal C, Benoit P, Changeux J-P (1991) Existence of different subtypes of nicotinic acetylcholine receptors in the rat habenulo-interpeduncular system. J Neurosci 11:2588–2597

    CAS  PubMed  Google Scholar 

  • Paton WDM, Zaimis EJ (1949) Pharmacological actions of polymethylene bistrimethy-lammonium salts. Br J Pharmacol 4:381–400

    CAS  Google Scholar 

  • Picciotto MR, Zoli M, Rimondini R, Lena C, Marubio LM, Pich EM, Fuxe K, Changeux JP (1998) Acetylcholine receptors containing the β2 subunit are involved in the reinforcing properties of nicotine. Nature 391:173–177

    Article  CAS  PubMed  Google Scholar 

  • Ravdin PM, Berg DW (1979) Inhibition of neuronal acetylcholine sensitivity by α-toxins from Bungarus multicinctus venom. Proc Natl Acad Sci USA 76:2072–2076

    Article  CAS  PubMed  Google Scholar 

  • Riker WF, Standaert FG (1966) The action of facilitatory drugs and acetylcholine on neuromuscular transmission. Ann N Y Acad Sci 135:163–176

    Article  PubMed  Google Scholar 

  • Roerig B, Nelson A, Katz LC (1997) Fast synaptic signaling by nicotinic acetylcholine and serotonin 5-HT3 receptors in developing visual cortex. J Neurosci 17: 8353–8362

    CAS  PubMed  Google Scholar 

  • Rogers M, Colquhoun LM, Parick JW, Dani JA (1997) Calcium flux through predominantly independent purinergic ATP and nicotinic acetylcholine receptors. J Neurophysiol 77:1407–1417

    CAS  PubMed  Google Scholar 

  • Rogers M, Dani JA (1995) Comparison of quantitative calcium flux through NMDA ATP and ACh receptor channels. Biophys J 68:501–506

    Article  CAS  PubMed  Google Scholar 

  • Role LW, Berg DK (1996) Nicotinic receptors in the development and modulation of CNS synapses. Neuron 16:1077–1085

    Article  CAS  PubMed  Google Scholar 

  • Sastry BR, Zialkowske SE, Hansen LM, Kavanagh JP, Evoy EM (1979) Acetylcholine release in interpeduncular nucleus following stimulation of habenula. Brain Res 164:334–337

    Article  CAS  PubMed  Google Scholar 

  • Schoepfer R, Conroy WG, Whiting P, Gore M, Lindtsrom J (1990) Brain α-bungarotoxin binding protein cDNAs and Mabs reveal subtypes of this branch of the ligand-gated ion channel gene family. Neuron 5:35–48

    Article  CAS  PubMed  Google Scholar 

  • Seguela P, Wadiche J, Dineley-Miller K, Dabi JA, Patrick JW (1993) Molecular cloning functional properties and distribution of rat barin α7: a nicotinic cation channel highly permeable to calcium. J Neurophysiol 13:596–604

    CAS  Google Scholar 

  • Sivilotti L, Colquhoun D (1995) Acetylcholine receptors: too many channels too few functions. Science 269:1681–1682

    Article  CAS  PubMed  Google Scholar 

  • Sivilotti LG, McNeil DK, Lewis TM, Nassar MA, Schoepfer R, Colquhoun D (1997) Recombinant nicotinic receptors expressed in Xenopus oocytes do not resemble native rat sympathetic ganglion receptors in single-channel behaviour. J Physiol 500:123–138

    CAS  PubMed  Google Scholar 

  • Steinlein OK, Mulley JC, Propping P, Wallace RH, Phillips HA, Sutherland GR, Scheffer IE, Berkovic SF (1995) A missense mutation in the neuronal acetylcholine receptor αA subunit is associated with autosomal dominant nocturnal frontal lobe epilepsy. Nature Genetics 11:201–203

    Article  CAS  PubMed  Google Scholar 

  • Thomas RC, Wilson VJ (1965) Precise localization of Renshaw cells with a new marking technique. Nature 206:211–213

    Article  CAS  PubMed  Google Scholar 

  • Tokimasa T, North RA (1984) Calcium entry through nicotinic receptor channels can activate potassium conductance in bullfrog sympathetic neurons. Brain Res 295:364–367

    Article  CAS  PubMed  Google Scholar 

  • Trouslard J, Marsh SJ, Brown DA (1993) Calcium entry through nicotinic and calcium channels in cultured rat superior cervical ganglion (SCG) neurones. J Physiol 468:53–72

    CAS  PubMed  Google Scholar 

  • Vernallis AB, Conroy WG, Berg DK (1995) Neurons assemble acetylcholine receptors with as many as three kinds of subunits while maintaining subunit segregation among receptor subtypes. Neuron 10:451–563

    Article  Google Scholar 

  • Wonnacott S (1997) Presynaptic nicotinic ACh receptors. Trends in Neurosci 20:92–98

    Article  CAS  Google Scholar 

  • Zhang M, Wang YT, Vyas DM, Neumann RS, Bieger D (1993) Nicotinic cholinocep-tor-mediated excitatory postsynaptic potentials in rat nucleus ambiguous. Exp Brain Res 96:83–88

    CAS  PubMed  Google Scholar 

  • Zhang ZW, Coggan JS, Berg DK (1996) Synaptic currents generated by neuronal acetylcholine receptors sensitive to α-bungarotoxin. Neuron 17:1231–1240

    Article  CAS  PubMed  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Brown, D.A. (2000). The History of the Neuronal Nicotinic Receptors. In: Clementi, F., Fornasari, D., Gotti, C. (eds) Neuronal Nicotinic Receptors. Handbook of Experimental Pharmacology, vol 144. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-57079-7_1

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-57079-7_1

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-63027-9

  • Online ISBN: 978-3-642-57079-7

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics