Skip to main content
SpringerLink
Log in

A Family Of Neurotransmitter Receptors Couple to a Potassium Conductance

  • Conference paper
Modulation of Synaptic Transmission and Plasticity in Nervous Systems

Part of the book series: NATO ASI Series ((ASIH,volume 19))

Abstract

It has been well known for several years that an important inhibitory mechanism in mammalian nervous tissue is an increase in the conductance of the membrane to chloride ions (Coombs et al. 1955). The two major substances involved in this mechanism are GABA and glycine and it is now known that their action is exerted through membrane receptors which incorporate the chloride ion channel (Grenningloh et al. 1987; Schofield et al. 1987). The role of potassium conductance increase in neuronal inhibition has been less clearly demonstrated except for some notable work in the invertebrate nervous system (Kehoe, 1972) and, particularly, in the mechanism of vagal inhibition of the heart (Trautwein & Dudel, 1958). Whereas the effects of agents that increase chloride conductance may be either excitatory or inhibitory, depending on the absolute magnitude of the chloride equilibrium potential, an increase in the cell conductance to potassium ions is universally inhibitory if it is sufficiently strong. This chapter describes some examples of synaptic inhibition mediated by potassium conductance increase in mammalian neurones, and points out that this mechanism of neuronal inhibition seems likely to be common to the action of agonists at an increasing number of neurotransmitter receptors.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
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

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Adrian RH (1964) The rubidium and potassium permeability of frog muscle membrane. J Physiol Lond 175:134–159.

    PubMed  CAS  Google Scholar 

  • Aghajanian GK, Lakoski JM (1984) Hyperpolarization of serotonergic neurons by serotonin and LSD; studies in brain slices showing increased K conductance. Brain Res 305:181–190.

    Article  PubMed  CAS  Google Scholar 

  • Aghajanian GK, Wang YY (1986) Pertussis toxin blocks the outward currents evoked by opiate and a2 agonists in locus coeruleus neurons. Brain Res 371:390–394.

    Article  PubMed  CAS  Google Scholar 

  • Andrade R, Malenka RC, Nicoll, RA (1986) A G-protein couples serotonin and GABA b receptors to the same channels in hippocampus. Science 234:1261–1265.

    Article  PubMed  CAS  Google Scholar 

  • Breitwieser GE, Szabo G (1985) Uncoupling of cardiac muscarinic and adrenergic receptors from ion channels by a guanine nucleotide analogue. Nature 317:538–540.

    Article  PubMed  CAS  Google Scholar 

  • Codina J, Yatani A, Grenet D, Brown AM, Birnbaumer L (1987) The a subunit of the GTP binding protein Gk opens atrial potassium channels. Science 236:442–445.

    Article  PubMed  CAS  Google Scholar 

  • Colino A, Halliwell JV (1987) Differential modulation of three separate K-conductances in hippocampal CAl neurons by serotonin. Nature 328:73–77.

    Article  PubMed  CAS  Google Scholar 

  • Coombs JS, Eccles JC, Fatt P (1955);The inhibitory suppression of reflex discharges from motoneurones. J Physiol Lond 130:396–413.

    PubMed  CAS  Google Scholar 

  • Del Castillo J, Katz B (1955) Production of membrane potential changes in the frog’s heart by inhibitory nerve impulses. Nature 175:1035.

    Article  Google Scholar 

  • Dodd J, Horn JP (1983) Muscarinic synaptic inhibition of sympathetic C neurones in the bullfrog. J Physiol Lond 334:271–291.

    PubMed  CAS  Google Scholar 

  • Egan TM, Henderson G, North RA, Williams JT (1983) Noradrenaline mediated synaptic inhibition in locus coeruleus neurones. J Physiol Lond 345:477–488.

    PubMed  CAS  Google Scholar 

  • Egan TM, North RA (1986) Acetylcholine hyperpolarizes central neurones by acting on a muscarinic receptor subtype. Nature 319:405–407.

    Article  PubMed  CAS  Google Scholar 

  • Grenningloh G, Rienitz A, Schmitt B, Methfessel C, Zenson M, Beyreuther K, Gundelfinger ED, Betz H (1987) The strychnine-binding subunit of the glycine receptor shows homology with nicotinic acetylcholine receptors. Nature 328:215–220.

    Article  PubMed  CAS  Google Scholar 

  • Hagiwara S, Takahashi K (1974) The anomalous rectification and cation selectivity of the membrane of a starfish egg cell. J Membr Biol 18:61–80.

    Article  PubMed  CAS  Google Scholar 

  • Hartzell HC, Kuffler SW, Stickgold R, Yoshikami D (1977) Synaptic excitation and inhibition resulting from direct action of acetylcholine on two types of chemoreceptors on individual amphibian parasympathetic neurones. J Physiol Lond 271:817–846.

    PubMed  CAS  Google Scholar 

  • Hill-Smith I, Purves RD (1978) Synaptic delay in the heart: an ionophoretic study. J Physiol Lond 279:31–54.

    PubMed  CAS  Google Scholar 

  • Hirst GDS, McKirdy HC (1975) Synaptic potentials recorded from some neurones of the submucous plexus of the guinea-pig small intestine. J Physiol Lond 249:369–385.

    PubMed  CAS  Google Scholar 

  • Innis RB, Aghajanian GK (1987) Pertussis toxin blocks autoreceptor- mediated inhibition of dopaminergic neurons in rat substantia nigra. Brain Research 411:139–143.

    Article  PubMed  CAS  Google Scholar 

  • Inoue M, Nakajima S, Nakajima Y (1987) Pertussis toxin abolishes somatostatin-induced enhancement of inward rectification in brain neurones. J Physiol Lond (in press).

    Google Scholar 

  • Israel JM, Jaquet P, Vincent JD (1985) The electrical properties of isolated human prolactin-secreting adenoma cells and their modification by dopamine. Endocrinology 117:1448–1455.

    Article  PubMed  CAS  Google Scholar 

  • Katz, B (1949) Les constantes electrique de la membrane du muscle. Arch Sci Physiol 2:285–299.

    Google Scholar 

  • Kehoe J (1972) Ionic mechanisms of a two component cholinergic inhibition in Aplysia neurones. J Physiol Lond 225:85–114.

    PubMed  CAS  Google Scholar 

  • Kurachi Y, Nakajima T, Sugimot T (1986) On the mechanism of activation of muscarinic K+ channels by adenosine in isolated atrial cells: involvement of GTP—binding proteins. Pflugers Archives 407:264–274.

    Article  CAS  Google Scholar 

  • Lacey MG, Mercuri N, North RA Dopamine acts on D2 receptors to increase potassium conductance in neurones of the rat substantia nigra zona compacta. J Physiol Lond (in press)

    Google Scholar 

  • MacVicar BA, Pittman QJ (1986) Novel synaptic responses mediated by dopamine and 7-aminobutyric acid in neuroendocrine cells of the intermediate pituitary. Neurosci Lett 64:35–40.

    Article  PubMed  CAS  Google Scholar 

  • McCormick DA, Prince DA (1986) Acetylcholine induces burst firing in thalamic reticular neurones by activating a potassium conductance. Nature 319:402–405.

    Article  PubMed  CAS  Google Scholar 

  • Mihara S, Nishi S, North RA, Surprenant A (1987) A nonadrenergic, noncholinergic slow inhibitory postsynaptic potential in neurones of the guinea-pig submucous plexus. J Physiol Lond 390:335–355.

    PubMed  CAS  Google Scholar 

  • Mihara S, North RA, Surprenant A (1987) Somatostatin increases an inwardly rectifying potassium conductance in guinea-pig submucous plexus neurons. J Physiol Lond 390:357–365.

    PubMed  CAS  Google Scholar 

  • Morita K, North RA (1981) Clonidine activates potassium conductance in myenteric neurones. Br J Pharmac 74:419–428.

    CAS  Google Scholar 

  • Morita K, North RA (1982) Opiate activation of potassium conductance: inhibition by calcium ions. Brain Res 242:145–150.

    Article  PubMed  CAS  Google Scholar 

  • Newberry NR, Nicoll RA (1983) A bicuculline-resistant inhibitory postsynaptic potential in rat hippocampal pyramidal cells in vitro. J Physiol Lond 348:239–254.

    Google Scholar 

  • North RA, Surprenant A (1985) Inhibitory synaptic potentials resulting from α2-adrenoceptor activation in guinea-pig submucous plexus neurones. J Physiol Lond 358:17–32.

    PubMed  CAS  Google Scholar 

  • North RA, Williams JT, Surprenant A, Christie MJ (1987)µ and δ 6 receptors belong to a family of receptors that are coupled to potassium channels. Proc Natl Acad Sci USA 84:5487–5491.

    Google Scholar 

  • North RA, Williams JT (1985) On the potassium conductance increased by opioids in rat locus coeruleus neurones. J Physiol Lond 364:265–280.

    PubMed  CAS  Google Scholar 

  • North RA, Yoshimura M (1984) The actions of noradrenaline on neurones of the rat substantia gelatinosa in vitro. J Physiol Lond 349:43–55.

    PubMed  CAS  Google Scholar 

  • Peralta EG, Winslow JW, Peterson GL, Smith DH, Ashkenazi A, Ramachandran J, Schimerlik MI, Capon DJ (1987) Primary structure and biochemical properties of an M2 muscarinic receptor. Science 236:600–605.

    Article  PubMed  CAS  Google Scholar 

  • Pfaffinger PJ, Martin JM, Hunter DD, Nathanson NM, Hille B (1985) GTP-binding proteins couple cardiac muscarinic receptors to a K channel. Nature 317:536–538.

    Article  PubMed  CAS  Google Scholar 

  • Sakmann B, Noma A, Trautwein W (1984) Acetylcholine activation of single muscarinic K+ channels in isolated pacemaker cells of mammalian heart. Nature 303:250–253.

    Article  Google Scholar 

  • Sasaki K, Sato M (1987) A single GTP-binding protein regulates K+-channels coupled with dopamine, histamine and acetylcholine receptors. Nature 325:259–262.

    Article  PubMed  CAS  Google Scholar 

  • Schofield PR, Darlison MG Fujita N, Burt DR, et al (1987) Sequence and functional expression of GABA a receptor shows a ligand-gated receptor super-family. Nature 328:221–227.

    Article  PubMed  CAS  Google Scholar 

  • Soejima M, Noma A (1984) Mode of regulation of the ACh-sensitive K channel by the muscarinic receptor in rabbit atrial cells. Pflugers Archives 400:424–431.

    Article  CAS  Google Scholar 

  • Sprouse JS, Aghajanian GK (1987) Electrophysiological responses of serotoninergic dorsal raphe neurons to 5-HT1A and 5-HT1B agonists. Synapse 1:3–9.

    Article  PubMed  CAS  Google Scholar 

  • Trautwein W, Dudel J (1958) Zum Mechanismus der Membranwirkung des Acetylcholin an der Herzmuskelfaser. Pflugers Arch ges Physiol 266:324–334.

    Article  CAS  Google Scholar 

  • Trussell LO, Jackson MB (1985) Adenosine-activated potassium conductance in cultured striatal neurons. Proc Natl Acad Sci USA 82:4857–4861.

    Article  PubMed  CAS  Google Scholar 

  • Werz MA, Macdonald RL (1983) Opioid peptides with differential affinity for mu and delta receptors decrease sensory neuron calcium-dependent action potentials. J Pharmac exp Ther 227:394–402.

    CAS  Google Scholar 

  • Williams JT, Henderson G, North RA (1985) Characterization of the α2adrenoceptors which increase potassium conductance in rat locus coeruleus neurones. Neuroscience 14:95–102.

    Article  PubMed  CAS  Google Scholar 

  • Worley PF, Baraban JM, McCarren M, Snyder SH, Alger BE (1987) Cholinergic phosphatidylinositol modulation of inhibitory, G protein-linked, neurotransmitter actions: electrophysiological studies in rat hippocampus. Proc Natl Acad Sci USA 84:3467–3471.

    Article  PubMed  CAS  Google Scholar 

  • Yamashita N, Shibuya N, Ogata E (1986) Hyperpolarization of the membrane potential caused by somatostatin in dissociated human pituitary adenoma cells that secrete growth hormone. Proc Natl Acad Sci USA 83:6198–6202.

    Article  PubMed  CAS  Google Scholar 

  • Yatani A, Codina J, Brown AM, Birnbaumer L (1987a) Direct activation of mammalian atrial muscarinic potassium channels by GTP regulatory protein GK. Science 235:207–211.

    Article  PubMed  CAS  Google Scholar 

  • Yatani A, Codina J, Sekura RD, Birnbaumer L, Brown AM (1987b) Reconstitution of somatostatin and muscarinic receptor mediated stimulation of K channels by isolated GK protein in clonal rat anterior pituitary cell membranes. Molec Endocrin (in press).

    Google Scholar 

  • Yoshimura M, Hisgashi H (1985) 5-Hydroxytryptamine mediates inhibitory postsynaptic potentials in rat dorsal raphe neurons. Neurosci Lett 53:69–74.

    Google Scholar 

  • Yoshimura M, North RA (1983) Substantia gelatinosa neurones in vitro hyperpolarized by enkephalin. Nature 305:529–530.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Vollum Institute, Oregon Health Sciences University, 3181 SW Sam Jackson Park Road, 97201, Portland, Oregon, USA

    R. Alan North

Authors
  1. R. Alan North
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Institut für Pharmakologie, Universität Freiburg, Hermann-Herder-Str. 5, 7800, Freiburg i. Br., Germany

    Georg Hertting

  2. Institut Für Biologie III, Universität Freiburg, Schänzlestr. 1, 7800, Freiburg i. Br., Germany

    Hanns-Christof Spatz

Rights and permissions

Reprints and permissions

Copyright information

© 1988 Springer-Verlag Berlin Heidelberg

About this paper

Cite this paper

North, R.A. (1988). A Family Of Neurotransmitter Receptors Couple to a Potassium Conductance. In: Hertting, G., Spatz, HC. (eds) Modulation of Synaptic Transmission and Plasticity in Nervous Systems. NATO ASI Series, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-73160-0_15

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-73160-0_15

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-73162-4

  • Online ISBN: 978-3-642-73160-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation