Skip to main content
SpringerLink
Log in
Book cover

Presynaptic Receptors in the Mammalian Brain pp 87–103Cite as

Presynaptic Inhibition Mediated by Neuropeptide Y in the Mammalian CNS: Possible Physiological Implications

  • Chapter

  • 35 Accesses

Abstract

Although numerous transmitters are released by central neurons to mediate conventional synaptic transmission, it has become evident recently that there are other substances that can alter conventional synaptic transmission on a prolonged time scale relative to conventional transmitters. These substances, broadly classified as neuromodulators, can include most conventional transmitters, peptides, and other substances released by neurons, which act through pre- or postsynaptic receptors to change the level of transmitter release, change the properties of postsynaptic ion channels, alter the response of the postsynaptic cell to the actions of conventional transmitters, or alter other aspects of the biochemical machinery of the nerve cell or presynaptic terminal. In most cases, neuromodulators activate G protein-coupled receptors, which can activate (or inhibit) all known second messenger cascades, as well as ion channels and other cell surface effectors. While the interpretation of conventional fast chemical neurotransmission has been relatively straightforward, understanding the purpose of modulatory transmitters within a particular physiological system has not always been intuitive. This chapter addresses the presynaptic actions of one modulatory substance, neuropeptide Y (NPY), and advances hypotheses regarding the action of NPY in two central systems: the hippocampus and the serotonergic dorsal raphe nucleus of the brain stem.

This is a preview of subscription content, 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   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

  • Aicher SA, Springston M, Berger SB, Reis DJ, Wahlestedt C (1991): Receptor-selective analogues demonstrate NPY/PYY receptor heterogeneity in rat brain. Neurosci Lett 130:32–36

    Article  PubMed  CAS  Google Scholar 

  • Aitken A, Tork I (1988): Early development of serotonin-containing neurons and pathways as seen in wholemount preparations of fetal rat brains. J Comp Neurol 274:32–47

    Article  PubMed  CAS  Google Scholar 

  • Andén NE, Dahlstrom A, Fuxe K, Larsson K, Olson L, Ungerstedt U (1966): Ascending monoamine neurons to the telencephalon and diencephalon. Acta Physiol Scand 67:313–326

    Article  Google Scholar 

  • Azmitia EC, Segal M (1978): An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol 179:641–668

    Article  PubMed  CAS  Google Scholar 

  • Balasubramaniam A, Sheriff S (1990): Neuropeptide Y(18–36) is a competitive antagonist of neuropeptide Y in rat cardiac ventricular membranes. J Biol Chem 265:14724–14727

    PubMed  CAS  Google Scholar 

  • Baraban JM, Aghajanian, GK (1980): Suppression of firing activity of 5-HT neurons in the dorsal raphe by alpha-adrenoceptor antagonists. Neuropharmacology 19:355–363

    Article  PubMed  CAS  Google Scholar 

  • Bartfai T, Iverfeldt K, Fisone G, Serfözö P (1988): Regulation of the release of coexisting neurotransmitters. Annu Rev Pharmacol Toxicol 28:285–310

    Article  PubMed  CAS  Google Scholar 

  • Bicknell RJ, Flint APF, Leng G, Sheldrick EL (1982): Phasic pattern of electrical stimulation enhances oxytocin secretion from the isolated neurohypophysis. Neurosci Lett 30:47–50

    Article  CAS  Google Scholar 

  • Bleakman DB, Colmers WF, Fournier A, Miller RJ (1991): Neuropeptide Y inhibits Ca+ + influx into cultured dorsal root ganglion neurones at the rat via a Y2 receptors. Br J Pharmacol 103:1781–1789

    PubMed  CAS  Google Scholar 

  • Bleakman D, Harrison NL, Colmers WF, Miller RJ (1992): Investigations into neuropeptide Y-mediated presynaptic inhibition in cultured hippocampal neurones of the rat. Br J Pharmacol 107:334–340

    PubMed  CAS  Google Scholar 

  • Bobker DH, Williams JT (1990): Serotonin-mediated inhibitory postsynaptic potentials in guinea pig prepositus hypoglossi and feedback inhibition by serotonin. J Physiol 422:447–462

    PubMed  CAS  Google Scholar 

  • Bourque CW, Renaud LP (1990): Electrophysiology of mammalian magnocellular vasopressin and oxytocin neurosecretory neurons. Front Neuroendocrinol 11:183–212

    Google Scholar 

  • Colmers WF (1989): Neuropeptide Y inhibits only selected excitatory synapses in the rat hippocampal slice. Can J Physiol Pharmacol 67:Avii

    Google Scholar 

  • Colmers WF (1990): Modulation of synaptic transmission in hippocampus by NPY: presynaptic actions. Ann NY Acad Sci 611:206–218

    Article  PubMed  CAS  Google Scholar 

  • Colmers WF, Lukowiak KD, Pittman QJ (1985): Neuropeptide Y reduces orthodromically-evoked population spike in rat hippocampal CA1 by a possibly presynaptic mechanism. Brain Res 346:404–408

    Article  PubMed  CAS  Google Scholar 

  • Colmers WF, Lukowiak KD, Pittman QJ (1987): Presynaptic action of neuropeptide Y in CA1 of rat hippocampal slice. J Physiol 383:285–299

    PubMed  CAS  Google Scholar 

  • Colmers WF, Lukowiak KD, Pittman QJ (1988): Neuropeptide Y action in the rat hippocampal slice: site and mechanism of presynaptic inhibition. J Neurosci 8:3827–3837

    PubMed  CAS  Google Scholar 

  • Colmers WF, Klapstein GJ, Fournier A, St-Pierre S, Treherne KA (1991): Presynaptic inhibition by Neuropeptide Y in rat hippocampal slice in vitro is mediated by a Y2 receptor. Br J Pharmacol 120:41–44

    Google Scholar 

  • Colmers WF, Wahlestedt C, eds. (1993): The Biology of Neuropeptide Y and related peptides. Totowa, NJ: Humana Press

    Google Scholar 

  • Davies CH, Davies SN, Collingridge GL (1990): Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus. J Physiol 424:513–531

    PubMed  CAS  Google Scholar 

  • de Quidt ME, Emson PC (1986): Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system—II. Immunohistochemical analysis. Neuroscience 18:545–618

    Article  PubMed  Google Scholar 

  • Edwards FA, Konnerth A, Sakmann B (1990): Quantal analysis of inhibitory synaptic transmission in the dentate gyrus of rat hippocampal slices: a patch-clamp study. J Physiol 430:213–249

    PubMed  CAS  Google Scholar 

  • Ewald DA, Matthies HJG, Perney TM, Walker MW, Miller RJ (1988): The effect of down regulation of protein kinase C on the inhibitory modulation of dorsal root ganglion neuron Ca2+ currents by Neuropeptide Y. J Neurosci 8:2447–2451

    PubMed  CAS  Google Scholar 

  • Ewald DA, Pang I-H, Sternweis PC, Miller RJ (1989): Differential G-protein mediated coupling of neurotransmitter receptors to Ca2+ channels in rat dorsal root ganglion neurons in vitro. Neuron 2:1185–1193

    Article  PubMed  CAS  Google Scholar 

  • Fuhlendorff J, Johansen NL, Melberg SG, Thogersen H, Schwartz TW (1990): The antiparallel pancreatic polypeptide fold in the binding of Neuropeptide Y to Y1 and Y2 receptors. J Biol Chem 265:11706–11712

    PubMed  CAS  Google Scholar 

  • Fuxe K, Jonsson G (1974): Further mapping of central 5-hydroxytryptamine neurons: studies with the neurotoxic dihydroxytryptamine. In: Serotonin: New Vistas, Histochemistry and Pharmacology, Costa E, Gessa GL, Sandler M, eds.

    Google Scholar 

  • Fuxe K, Jonsson G (1974): Further mapping of central 5-hydroxytryptamine neurons: studies with the neurotoxic dihydroxytryptamine. Adv Biochem Psychopharmacol 10:1–12

    PubMed  CAS  Google Scholar 

  • Haas HL, Hermann A, Greene RW, Chan-Palay V (1987): Action and location of neuropeptide tysosine (Y) on hippocampus neurons of the rat in slice preparations. J Comp Neurol 257:208–215

    Article  PubMed  CAS  Google Scholar 

  • Hendry SHC (1993): Organization of Neuropeptide Y neurons in the mammalian central nervous system. In: The Biology of Neuropeptide Y and related peptides, Colmers WF, Wahlestedt C, eds. Totowa, NJ: Humana Press

    Google Scholar 

  • Illes P, Regenold JT (1990): Interaction between neuropeptide Y and noradrenaline on central catecholamine neurons. Nature 344:62–63

    Article  PubMed  CAS  Google Scholar 

  • Johnston D, Brown TH (1984): Biophysics and microphysiology of synaptic transmission in hippocampus. In: Brain Slices, Dingledine R, ed. New York: Plenum

    Google Scholar 

  • Kalen P, Karlson M, Wiklund L (1985): Possible excitatory amino acid afferents to nucleus raphe dorsalis of the rat investigated with retrograde wheat germ agglutinin and D-[3H]-aspartate tracing. Brain Res 360:285–297

    Article  PubMed  CAS  Google Scholar 

  • Kalen P, Pritzel M, Nieoullon A, Wiklund L (1986): Further evidence for excitatory amino acid transmission in the lateral habernular projection to the rostral raphe nuclei: lesion-induced decrease of high affinity glutamate uptake. Neurosci Lett 68:35–40

    Article  PubMed  CAS  Google Scholar 

  • Klapstein GJ, Colmers WF (1992): 4-Aminopyridine and low Ca2+ differentiate presynaptic inhibition mediated by neuropeptide Y, baclofen and 2-chloroadenosine in rat hippocampal CA1 in vitro. Br J Pharmacol 105:470–474

    Google Scholar 

  • Klapstein GJ, Colmers WF (1991): NPY inhibits feedforward IPSP’s in hippocampus by reducing excitatory input to interneurons. Soc Neurosci Abstr 17:975

    Google Scholar 

  • Klapstein GJ and Colmers WF (1993): On the sites of presynaptic inhibition by neuropeptide Y in rat hippocampus in vitro. Hippocampus 3:103–112

    Article  PubMed  CAS  Google Scholar 

  • Köhler C, Eriksson L, Davies S, Chan-Palay V (1986): Neuropeptide Y innervation of the hippocampal region in the rat and monkey brain. J Comp Neurol 244:384–400

    Article  PubMed  Google Scholar 

  • Köhler C, Schultzberg M, Radesäter AM (1987): Distribution of neuropeptide Y receptors in the rat hippocampal region. Neurosci Lett 75:141–146

    Article  PubMed  Google Scholar 

  • Kombian SB, Colmers WF (1992): Neuropeptide Y selectively inhibits slow synaptic potentials in rat dorsal raphe nucleus in vitro by a presynaptic action. J Neurosci 12:1086–1093

    PubMed  CAS  Google Scholar 

  • Lacaille JC, Kunkel DD, Schwartzkroin PA (1989): Electrophysiological and morphological characterization of hippocampal interneurons. In: The Hippocampus: New Vistas, Chan-Palay V, Köhler C, eds. New York: Alan R. Liss

    Google Scholar 

  • Lopez-Ibor JJ (1988): The involvement of serotonin in psychiatric disorders and behavior. Br J Psychiatr 153(Suppl 3):26–39

    Google Scholar 

  • Madison DV, Nicoli RA (1982): Noradrenaline blocks accommodation of pyramidal cell discharge in hippocampus. Nature 299:636–638

    Article  PubMed  CAS  Google Scholar 

  • Manabe T, Renner P, Nicoli RA (1992): Postsynaptic contribution to long-term potentiation revealed by the analysis of miniature synaptic currents. Nature 355:50–55

    Article  PubMed  CAS  Google Scholar 

  • Martel J-C, Fournier A, St. Pierre S, Quirion R (1990): Quantitative autoradiographic distribution of [125I] Bolton-Hunter neuropeptide Y receptor binding sites in rat brain. Comparison with [125I]-peptide YY receptor sites. Neuroscience 36:255–283

    Article  PubMed  CAS  Google Scholar 

  • Martel J-C, St-Pierre S, Quirion R (1986): Neuropeptide Y receptors in rat brain: autoradiographic localization. Peptides 7:55–60

    Article  PubMed  CAS  Google Scholar 

  • McBain CJ, Dingledine R (1990): Patch clamp recording of spontaneous synaptic currents from CA3 pyramidal neurons in rat hippocampal slices. Soc Neurosci Abstr 16:60

    Google Scholar 

  • McCarren M, Alger BE (1985): Use-dependent depressions of IPSP’s in rat hippocampal pyramidal cells in vitro. J Neurophysiol 53:557–571

    PubMed  CAS  Google Scholar 

  • McLean LR, Buck SH, Krstenansky JL (1990): Examination of the role of the amphipathic α-helix in the interaction of neuropeptide Y and active cyclic analogues with cell membrane receptors and dimyristoylphosphatidylcholine. Biochemistry 29:2016–2022

    Article  PubMed  CAS  Google Scholar 

  • McQuiston AR, Colmers WF (1991): Neuropeptide Y (NPY) does not alter postsynaptic NMDA currents in pyramidal neurons of area CA3 of the rat hippocampal slice. Soc Neurosci Abstr 17:975

    Google Scholar 

  • McQuiston AR, Colmers WF (1992): Neuropeptide Y does not alter NMDA conductances in rat pyramidal neurons in he in vitro hippocampal slice preparation. Neurosci Lett 138:261–264

    Article  PubMed  CAS  Google Scholar 

  • Milner TA, Veznedaroglu E (1992): Ultrastructural localization of neuropeptide Y-like immunoreactivity in the rat hippocampal formation. Hippocampus 2:107–126

    Article  PubMed  CAS  Google Scholar 

  • Mulligan KA, Tork I (1987): Serotonergic axons form basketlike terminals in cerebral cortex. Neurosci Lett 81:7–12

    Article  PubMed  CAS  Google Scholar 

  • Mulligan KA, Tork I (1988): Serotonergic innervation of the cat cerebral cortex. J Comp Neurol 270:86–110

    Article  PubMed  CAS  Google Scholar 

  • O’Donoghue TL, Chronwall BM, Pruss RM, Mezey E, Kiss JZ, Eiden LE, Massari VJ, Tessei RE, Pickel VM, DiMaggio DA, Hotchkiss AJ, Crowley WR, Zukowska-Grojec Z (1985): Neuropeptide Y and peptide YY neuronal and endocrine systems. Peptides 6:755–768

    Article  Google Scholar 

  • Pan ZZ, Colmers WF, Williams JT (1989): 5-HT mediated synaptic potentials in the dorsal raphe nucleus: interactions with excitatory amino acid and GABA neurotransmission. J Neurophysiol 62:481–486

    Google Scholar 

  • Pan ZZ, Williams JT (1989a): Differential actions of cocaine and amphetamine on dorsal raphe neurons in vitro. J Pharmacol Exp Ther 251:56–62

    PubMed  CAS  Google Scholar 

  • Pan ZZ, Williams JT (1989b): GABA- and glutamate-mediated synaptic potentials in rat dorsal raphe nucleus in vitro. J Neurophysiol 61:719–726

    PubMed  CAS  Google Scholar 

  • Paxinos G, Watson C (1986): The Rat Brain in Stereotaxic Coordinates. New York: Academic Press

    Google Scholar 

  • Schofield GG, Ikeda SR (1988): Neuropeptide Y blocks a calcium current in C cells of bullfrog sympathetic ganglia. Eur J Pharmacol 151:131–134

    Article  PubMed  CAS  Google Scholar 

  • Silinsky EM (1985): The biophysical pharmacology of calcium-dependent acetylcholine secretion. Pharmacol Rev 37:81–132

    PubMed  CAS  Google Scholar 

  • Sloviter RS, Nilaver G (1987): Immunocytochemical localization of GABA-, cholecysto-kinin-, vasoactive intestinal polypeptide-, and somatostatin-like immunoreactivity in the area dentata and hippocampus of the rat. J Comp Neurol 256:42–60

    Article  PubMed  CAS  Google Scholar 

  • Sloviter RS (1987): Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235:73–76

    Article  PubMed  CAS  Google Scholar 

  • Sloviter RS (1989): L Chemically-define hippocampal interneurons and their possible relationship to seizure mechanisms. In: The Hippocampus: New Vistas, Chan-Palay V, Köhler C, eds. New York: Alan R. Liss

    Google Scholar 

  • Staley KJ, Mody I, (1991): Integrity of perforant path fibers and the frequency of action potential independent excitatory and inhibitory events in dentate gyrus granule cells. Synapse 9:219–224

    Article  PubMed  CAS  Google Scholar 

  • Stretton D, Miura M, Belvisi MG, Barnes PJ (1992): Calcium-activated potassium channels mediate prejunctional inhibition of peripheral sensory nerves. Proc Nat Acad Sci USA 89:1325–1329

    Article  PubMed  CAS  Google Scholar 

  • Wahlestedt C, Grundemar L, Håkanson R, Heilig M, Shen GH, Zukowska-Grojec Z, Reis DJ (1990): Neuropeptide Y receptor subtypes, Y1 and Y2. Ann NY Acad Sci 611:7–26

    Article  PubMed  CAS  Google Scholar 

  • Wahlestedt C, Yanaihara N, Hâkanson R (1986): Evidence for different pre and postjunctional receptors for neuropeptide Y and related peptides. Reg Pept 13:307–318

    Article  CAS  Google Scholar 

  • Widerlöv E, Heilig M, Ekman R, Wahlestedt C (1989): Neuropeptide Y—possible involvement in depression and anxiety. In: Nobel Conference on NPY, Mutt V, Fuxe K, Hökfelt T, eds. New York: Raven Press

    Google Scholar 

  • Zidichouski JA, Chen H, Smith PA (1990): Neuropeptide Y activates inwardly-rectifying K+-channels in C-cells of amphibian sympathetic ganglia. Neurosci Lett 117:123–128

    Article  PubMed  CAS  Google Scholar 

Download references

Authors
  1. William F. Colmers
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Rory McQuiston
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Samuel B. Kombian
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gloria J. Klapstein
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. V.A. Medical Center, 80220, Denver, CO, USA

    Thomas V. Dunwiddie

  2. Department of Pharmacology C-236, University of Colorado Health Sciences Center, 80220, Denver, CO, USA

    Thomas V. Dunwiddie

  3. Department of Molecular Physiology and Biophysics, Vanderbilt University School of Medicine, 37232, Nashville, TN, USA

    David M. Lovinger

Rights and permissions

Reprints and permissions

Copyright information

© 1993 Birkhäuser Boston

About this chapter

Cite this chapter

Colmers, W.F., McQuiston, A.R., Kombian, S.B., Klapstein, G.J. (1993). Presynaptic Inhibition Mediated by Neuropeptide Y in the Mammalian CNS: Possible Physiological Implications. In: Dunwiddie, T.V., Lovinger, D.M. (eds) Presynaptic Receptors in the Mammalian Brain. Birkhäuser Boston. https://doi.org/10.1007/978-1-4684-6825-0_6

Download citation

  • DOI: https://doi.org/10.1007/978-1-4684-6825-0_6

  • Publisher Name: Birkhäuser Boston

  • Print ISBN: 978-1-4684-6827-4

  • Online ISBN: 978-1-4684-6825-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation