Skip to main content
SpringerLink
Log in

Presynaptic Inhibition of Glutamate Release by Neuropeptides: Use-Dependent Synaptic Modification

  • Chapter
  • First Online:
Inhibitory Regulation of Excitatory Neurotransmission

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 44))

Abstract

Neuropeptides are signaling molecules that interact with G-protein coupled receptors located both pre- and postsynaptically. Presynaptically, these receptors are localized in axons and terminals away from presynaptic specializations. Neuropeptides are stored in dense core vesicles that are distinct from the clear synaptic vesicles containing classic neurotransmitters such as glutamate and GABA. Because they require a stronger Ca2+ signal than synaptic vesicles, dense core vesicles do not release neuropeptides with single action potentials but rather require high-frequency trains. Thus, neuropeptides only modulate strongly stimulated synapses, providing negative or positive feedback. Many neuropeptides have been found to inhibit glutamate release from presynaptic terminals, and the major mechanism is likely direct interaction of βγ G-protein subunits with presynaptic proteins such as SNARE (soluble N-ethylmaleimide-sensitive factor attachment protein receptor). The use of mouse genetic models and specific receptor antagonists are beginning to unravel the function of inhibitory neuropeptides. The opioid receptors kappa and mu, which are activated by endogenous opioid peptides such as dynorphin, enkephalin, and possibly the endomorphins, are important in modulating pain transmission. Dynorphin, nociceptin/orphanin FQ, and somatostatin and its related peptide cortistatin appear to play a role in modulation of learning and memory. Neuropeptide Y has important functions in ingestive behavior and also in entraining circadian rhythms. The existence of neuropeptides greatly expands the computational ability of the brain by providing additional levels of modulation.

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 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover 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

  1. Aimone L, Gebhart G (1986) Stimulation-produced spinal inhibition from the midbrain in the rat is mediated by an excitatory amino acid neurotransmitter in the medial medulla. J Neurosci 6:1803–1813

    PubMed  CAS  Google Scholar 

  2. Anton B, Fein J, To T, Li X, Silberstein L, Evans CJ (1996) Immunohistochemical localization of ORL-1 in the central nervous system of the rat. J Comp Neurol 368:229–251

    PubMed  CAS  Google Scholar 

  3. Artalejo CR, Elhamdani A, Palfrey HC (1998) Secretion: dense-core vesicles can kiss-and-run too. Curr Biol 8:R62–65

    PubMed  CAS  Google Scholar 

  4. Bains JS, Ferguson AV (1999) Activation of N-methyl-d-aspartate receptors evokes calcium spikes in the dendrites of rat hypothalamic paraventricular nucleus neurons. Neuroscience 90:885–891

    PubMed  CAS  Google Scholar 

  5. Baratta MV, Lamp T, Tallent MK (2002) Somatostatin depresses long-term potentiation and Ca2+ signaling in mouse dentate gyrus. J Neurophys 88:3078–3086

    CAS  Google Scholar 

  6. Barral J, Mendoza E, Galarraga E, Bargas J (2003) The presynaptic modulation of corticostriatal afferents by mu opioids is mediated by K+ conductances. Eur J Pharmacol 462:91–98

    PubMed  CAS  Google Scholar 

  7. Bie B, Pan ZZ (2003) Presynaptic mechanism for anti-analgesic and anti-hyperalgesic actions of kappa opioid receptors. J Neurosci 23:7262–7268

    PubMed  CAS  Google Scholar 

  8. Blackmer T, Larsen EC, Takahashi M, Martin TF, Alford S, Hamm HE (2001) G-protein βγ subunit-mediated presynaptic inhibition: regulation of eocytotic fusion downstream of Ca2+ entry. Science 292:293–297

    PubMed  CAS  Google Scholar 

  9. Blackmer T, Larsen EC, Bartleson C, Kowalchyk JA, Yoon E-J, Preininger AM, Alford S, Hamm HE, Martin TFJ (2005) G-protein βγ directly regulates SNARE protein fusion machinery for secretory granule exocytosis. Nat Neurosci 8:421–425

    PubMed  CAS  Google Scholar 

  10. Boehm S, Betz H (1997) Somatostatin inhibits excitatory transmission at rat hippocampal synapses via presynaptic receptors. J Neurosci 17:4066–4075

    PubMed  CAS  Google Scholar 

  11. Buckmaster PS, Otero-Corchon V, Rubinstein M, Low MJ (2002) Heightened seizure severity in somatostatin knockout mice. Epilepsy Res 48:43–56

    PubMed  CAS  Google Scholar 

  12. Chen X, Pittman QJ (1999) Vasopressin and amastatin induce V(1)-receptor-mediated suppression of excitatory transmission in the rat parabrachial nucleus. J Neurophys 82:1689–1696

    CAS  Google Scholar 

  13. Chronwall BM, DiMaggio DA, Massari VJ, Pickel VM, Ruggiero DA, O'Donohue TL (1985) The anatomy of neuropeptide-Y-containing neurons in rat brain. Neuroscience 15:1159–1181

    PubMed  CAS  Google Scholar 

  14. Colmers WF, Lukowiak K, 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 

  15. Commons KG (2003) Translocation of presynaptic delta opioid receptors in the ventrolateral periaqueductal gray after swim stress. J Comp Neurol 464:197–207

    PubMed  Google Scholar 

  16. Dournaud P, Jazat-Poindessous F, Slama A, Lamour Y, Epelbaum J (1996a) Correlations between water maze performance and cortical somatostatin mRNA and high-affinity binding sites during ageing in rats. Eur J Neurosci 8:476–485

    PubMed  CAS  Google Scholar 

  17. Dournaud P, Gu YZ, Schonbrunn A, Mazella J, Tannenbaum GS, Beaudet A (1996b) Localization of the somatostatin receptor SST2A in rat brain using a specific anti-peptide antibody. J Neurosci 16:4468–4478

    PubMed  CAS  Google Scholar 

  18. Drake CT, Chang PC, Harris JA, Milner TA (2002) Neurons with mu opioid receptors interact indirectly with enkephalin-containing neurons in the rat dentate gyrus. Exp Neurol 176:254–261

    PubMed  CAS  Google Scholar 

  19. Drake CT, Patterson TA, Simmons ML, Chavkin C, Milner TA (1996) Kappa opioid receptor-like immunoreactivity in guinea pig brain: ultrastructural localization in presynaptic terminals in hippocampal formation. J Comp Neurol 370:377–395

    PubMed  CAS  Google Scholar 

  20. Drake CT, Terman GW, Simmons ML, Milner TA, Kunkel DD, Schwartzkroin PA, Chavkin C (1994) Dynorphin opioids present in dentate granule cells may function as retrograde inhibitory neurotransmitters. J Neurosci 14:3736–3750

    PubMed  CAS  Google Scholar 

  21. Dutar P, Vaillend C, Viollet C, Billard JM, Potier B, Carlo AS, Ungerer A, Epelbaum J (2002) Spatial learning and synaptic hippocampal plasticity in type 2 somatostatin receptor knock-out mice. Neuroscience 112:455–466

    PubMed  CAS  Google Scholar 

  22. Emmerson PJ, Miller RJ (1999) Pre- and postsynaptic actions of opioid and orphan opioid agonists in the rat arcuate nucleus and ventromedial hypothalamus in vitro. J Physiol 517:431–445

    PubMed  CAS  Google Scholar 

  23. Frey U, Morris RGM (1997) Synaptic tagging and long-term potentiation. Nature 385:533–536

    PubMed  CAS  Google Scholar 

  24. Fu L-Y, Acuna-Goycolea C, van den Pol AN (2004) Neuropeptide Y inhibits hypocretin/orexin neurons by multiple presynaptic and postsynaptic mechanisms: tonic depression of the hypothalamic arousal system. J Neurosci 24:8741–8751

    PubMed  CAS  Google Scholar 

  25. Gao X-B, van den Pol AN (2001) Melanin concentrating hormone depresses synaptic activity of glutamate and GABA neurons from rat lateral hypothalamus. J Physiol 533:237–252

    PubMed  CAS  Google Scholar 

  26. Garzon M, Pickel VM (2001) Plasmalemmal mu opioid receptor distribution mainly in nondopaminergic neurons in the rat ventral tegmental area. Synapse 41:311–328

    PubMed  CAS  Google Scholar 

  27. Gerachshenko T, Blackmer T, Yoon E-J, Bartleson C, Hamm HE, Alford S (2005) Gβγ acts at the C-terminus of SNAP-25 to mediate presynaptic inhibition. Nat Neurosci 8:597–605

    PubMed  CAS  Google Scholar 

  28. Ghijsen WE, Leenders AG (2005) Differential signaling in presynaptic neurotransmitter release. Cell Mol Life Sci 62:937–954

    PubMed  CAS  Google Scholar 

  29. Glass MJ, Chan J, Pickel VM (2002) Ultrastructural localization of neuropeptide Y Y1 receptors in the rat medial nucleus tractus solitarius: relationships with neuropeptide Y or catecholamine neurons. J Neurosci Res 67:753–765

    PubMed  CAS  Google Scholar 

  30. Grilli M, Raiteri L, Pittaluga A (2004) Somatostatin inhibits glutamate release from mouse cerebrocortical nerve endings through presynaptic SST2 receptors linked to the adenylyl cyclase–protein kinase A pathway. Neuropharmacology 46:388–396

    PubMed  CAS  Google Scholar 

  31. Guo H, Castro PA, Palmiter RD, Baraban SC (2002) Y5 receptors mediate neuropeptide Y actions at excitatory synapses in area CA3 of the mouse hippocampus. J Neurophys 87:558–566

    CAS  Google Scholar 

  32. Haj-Dahmane S, Shen RY (2005) The wake-promoting peptide orexin-B inhibits glutamatergic transmission to dorsal raphe nucleus serotonin neurons through retrograde endocannabinoid signaling. J Neurosci 25:896–905

    PubMed  CAS  Google Scholar 

  33. Hall AC, Earle-Cruikshanks G, Harrington ME (1999) Role of membrane conductances and protein synthesis in subjective day phase advances of the hamster circadian clock by neuropeptide Y. Eur J Neurosci 11:3424–3432

    PubMed  CAS  Google Scholar 

  34. Harvey J, Lacey MG (1997) A postsynaptic interaction between dopamine D1 and NMDA receptors promotes presynaptic inhibition in the rat nucleus accumbens via adenosine release. J Neurosci 17:5271–5280

    PubMed  CAS  Google Scholar 

  35. Higgins GA, Kew JN, Richards JG, Takeshima H, Jenck F, Adam G, Wichmann J, Kemp JA, Grottick AJ (2002) A combined pharmacological and genetic approach to investigate the role of orphanin FQ in learning and memory. Eur J Neurosci 15:911–922

    PubMed  CAS  Google Scholar 

  36. Hirasawa M, Kombian SB, Pittman QJ (2001) Oxytocin retrogradely inhibits evoked, but not miniature, EPSCs in the rat supraoptic nucleus: role of N- and P/Q-type calcium channels. J Physiol 532:595–607

    PubMed  CAS  Google Scholar 

  37. Hirasawa M, Schwab Y, Natah S, Hillard CJ, Mackie K, Sharkey KA, Pittman QJ (2004) Dendritically released transmitters cooperate via autocrine and retrograde actions to inhibit afferent excitation in rat brain. J Physiol 559:611–624

    PubMed  CAS  Google Scholar 

  38. Honda E, Ono K, Inenaga K (2004) DAMGO suppresses both excitatory and inhibitory synaptic transmission in supraoptic neurones of mouse hypothalamic slice preparations. J Neuroendocrinol 16:198–207

    PubMed  CAS  Google Scholar 

  39. Jamot L, Matthes HW, Simonin F, Kieffer BL, Roder JC (2003) Differential involvement of the mu and kappa opioid receptors in spatial learning. Genes Brain Behav 2:80–92

    PubMed  CAS  Google Scholar 

  40. Kagimoto S, Yamada Y, Kubota A, Someya Y, Ihara Y, Yasuda K, Kozasa T, Imura H, Seino S, Seino Y (1994) Human somatostatin receptor, SST2, is coupled to adenylyl cyclase in the presence of Gia1 protein. Biochem Biophys Res Commun 202:1188–1195

    PubMed  CAS  Google Scholar 

  41. Kalivas PW, Miller JS (1984) Substance P modulation of dopamine in the nucleus accumbens. Neurosci Lett 48:55–59

    Article  PubMed  CAS  Google Scholar 

  42. Kinney GA, Emmerson PJ, Miller RJ (1998) Galanin receptor-mediated inhibition of glutamate release in the arcuate nucleus of the hypothalamus. J Neurosci 18:3489–3500

    PubMed  CAS  Google Scholar 

  43. Kombian SB, Ananthalakshmi KVV, Parvathy SS, Matowe WC (2003) Substance P depresses excitatory synaptic transmission in the nucleus accumbens through dopaminergic and purinergic mechanisms. J Neurophys 89:728–737

    CAS  Google Scholar 

  44. Kombian SB, Ananthalakshmi KVV, Parvathy SS, Matowe WC (2004) Cholecystokinin activates CCKB receptors to excite cells and depress EPSCs in the rat rostral nucleus accumbens in vitro. J Physiol 555:71–84

    PubMed  CAS  Google Scholar 

  45. Kosaka T, Wu J-Y, Benoit R (1988) GABAergic neurons containing somatostatin-like immunoreactivity in the rat hippocampus and dentate gyrus. Exp Brain Res 71:388–398

    PubMed  CAS  Google Scholar 

  46. Lamirault L, Guillou JL, Micheau J, Jaffard R (2001) Intrahippocampal injections of somatostatin dissociate acquisition from the flexible use of place responses. Eur J Neurosci 14:567–570

    PubMed  CAS  Google Scholar 

  47. Law SF, Zaina S, Sweet R, Yasuda K, Bell GI, Stadel J, Reisine T (1994) Gi alpha 1 selectively couples somatostatin receptor subtype 3 to adenylyl cyclase: identification of the functional domains of this alpha subunit necessary for mediating the inhibition by somatostatin of cAMP formation. Mol Pharmacol 45:587–590

    PubMed  CAS  Google Scholar 

  48. Ludwig M (1998) Dendritic release of vasopressin and oxytocin. J Neuroendocrinol 10:881–895

    PubMed  CAS  Google Scholar 

  49. Ludwig M, Sabatier N, Bull PM, Landgraf R, Dayanithi G, Leng G (2002) Intracellular calcium stores regulate activity-dependent neuropeptide release from dendrites. Nature 418:85–89

    PubMed  CAS  Google Scholar 

  50. Madamba SG, Schweitzer P, Siggins GR (1999) Nociceptin augments K+ currents in hippocampal CA1 neurons by both ORL-1 and opiate receptor mechanisms. J Neurophys 82:1776–1785

    CAS  Google Scholar 

  51. Manabe T, Noda Y, Mamiya T, Katagiri H, Houtani T, Nishi M, Noda T, Takahashi T, Sugimoto T, Nabeshima T, Takeshima H (1998) Facilitation of long-term potentiation and memory in mice lacking nociceptin receptors. Nature 394:577–581

    PubMed  CAS  Google Scholar 

  52. Martin TF (2003) Tuning exocytosis for speed: fast and slow modes. Biochim Biophys Acta 1641:157–165

    PubMed  CAS  Google Scholar 

  53. Matsuoka N, Maeda N, Yamaguchi I, Satoh M (1994) Possible involvement of brain somatostatin in the memory formation of rats and the cognitive enhancing action of FR121196 in passive avoidance task. Brain Res 642:11–19

    PubMed  CAS  Google Scholar 

  54. McQuiston AR, Colmers WF (1996) Neuropeptide Y2 receptors inhibit the frequency of spontaneous but not miniature EPSCs in CA3 pyramidal cells of rat hippocampus. J Neurophys 76:3159–3168

    CAS  Google Scholar 

  55. Medanic M, Gillette MU (1993) Suprachiasmatic circadian pacemaker of rat shows two windows of sensitivity to neuropeptide Y in vitro. Brain Res 620:281–286

    PubMed  CAS  Google Scholar 

  56. Meis S, Pape HC (2001) Control of glutamate and GABA release by nociceptin/orphanin FQ in the rat lateral amygdala. J Physiol 532:701–712

    PubMed  CAS  Google Scholar 

  57. Meis S, Munsch T, Pape H-C (2002) Antioscillatory effects of nociceptin/orphanin FQ in synaptic networks of the rat thalamus. J Neurosci 22:718–727

    PubMed  CAS  Google Scholar 

  58. Merighi A (2002) Costorage and coexistence of neuropeptides in the mammalian CNS. Prog Neurobiol 66:161–190

    PubMed  CAS  Google Scholar 

  59. Meunier JC, Mollereau C, Toll L, Suaudeau C, Moisand C, Alvinerie P, Butour JL, Guillemot JC, Ferrara P, Monsarrat B, Marzagull H, Vassart G, Parmentier M, Costentin J (1995) Isolation and structure of the endogenous agonist of opioid receptor-like ORL1 receptor. Nature 377:532–535

    PubMed  CAS  Google Scholar 

  60. Mollereau C, Parmentier M, Mailleux P, Butour JL, Moisand C, Chalon P, Caput D, Vassart G, Meunier JC (1994) ORL1, a novel member of the opioid receptor family. Cloning, functional expression and localization. FEBS Lett 341:33–38

    PubMed  CAS  Google Scholar 

  61. Moore SD, Madamba SG, Joels M, Siggins GR (1988) Somatostatin augments the M-current in hippocampal neurons. Science 239:278–280

    PubMed  CAS  Google Scholar 

  62. Morrison JH, Benoit R, Maigistretti P, Ling N, Bloom FE (1982) Immunohistochemical distribution of pro-somatostatin-related peptides in hippocampus. Neurosci Lett 34:137–142

    PubMed  CAS  Google Scholar 

  63. Murthy KS, Coy DH, Makhlouf GM (1996) Somatostatin receptor-mediated signaling in smooth muscle. Activation of phospholipase C-β3 by Gβγ and inhibition of adenylyl cyclase by Gαi1 and Gαo. J Biol Chem 271:23458–23463

    PubMed  CAS  Google Scholar 

  64. Nakazawa K, Quirk MC, Chitwood RA, Watanabe M, Yeckel MF, Sun LD, Kato A, Carr CA, Johnston D, Wilson MA, Tonegawa S (2002) Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297:211–218

    PubMed  CAS  Google Scholar 

  65. Neal CR Jr, Mansour A, Reinscheid R, Nothacker HP, Civelli O, Watson SJ Jr (1999a) Localization of orphanin FQ (nociceptin) peptide and messenger RNA in the central nervous system of the rat. J Comp Neurol 406:503–547

    PubMed  CAS  Google Scholar 

  66. Neal CR Jr, Mansour A, Reinscheid R, Nothacker HP, Civelli O, Akil H, Watson SJ Jr (1999b) Opioid receptor-like (ORL1) receptor distribution in the rat central nervous system: comparison of ORL1 receptor mRNA expression with 125I-[(14)Tyr]-orphanin FQ binding. J Comp Neurol 412:563–605

    PubMed  CAS  Google Scholar 

  67. Pickel VM, Beck-Sickinger AG, Chan J, Weiland HA (1998) Y1 receptors in the nucleus accumbens: ultrastructural localization and association with neuropeptide Y. J Neurosci Res 52:54–68

    PubMed  CAS  Google Scholar 

  68. Pittman QJ, Kombian SB, Mouginot D, Chen X, van Eerdenberg FJ (1998) Electrophysiological studies of neurohypophysial neurons and peptides. Prog Brain Res 119:311–320

    Article  PubMed  CAS  Google Scholar 

  69. Qian J, Colmers WF, Saggau P (1997) Inhibition of synaptic transmission by neuropeptide Y in rat hippocampal area CA1: modulation of presynaptic Ca2+ entry. J Neurosci 17:8169–8177

    PubMed  CAS  Google Scholar 

  70. Qiu C, Suzuki C, Zeyda T, Hochgeschwender U, de Lecea L, Tallent MK (2005) Increased seizure severity and reduced somatostatin effects in hippocampus of somatostatin receptor subtype 4 (SST4) knockout mice. Program no. 607.11, 2005 Abstract viewer/itinerary planner. Society for Neuroscience, Washington DC. Available online at http://sfn.scholarone.com/itin2005/ , last visted: 7 May 2007

  71. Rawls SM, McGinty JF, Terrian DM (1999) Presynaptic kappa opioid and muscarinic receptors inhibit the calcium-dependent component of evoked glutamate release from striatal synaptosomes. J Neurochem 73:1058–1065

    PubMed  CAS  Google Scholar 

  72. Reinscheid RK, Nothacker HP, Bourson A, Ardati A, Henningsen RA, Bunzow JR, Grandy DK, Langen H, Monsma FJ Jr, Civelli O (1995) Orphanin FQ: a neuropeptide that activates an opioid-like G protein coupled receptor. Science 270:792–794

    PubMed  CAS  Google Scholar 

  73. Robishaw JD, Berlot CH (2004) Translating G protein subunit diversity into functional specificity. Curr Opin Cell Biol 16:206–209

    PubMed  CAS  Google Scholar 

  74. Saleh TM, Kombian SB, Zidichouski JA, Pittman QJ (1996) Peptidergic modulation of synaptic transmission in the parabrachial nucleus in vitro: importance of degradative enzymes in regulating synaptic efficacy. J Neurosci 16:6046–6055

    PubMed  CAS  Google Scholar 

  75. Saleh TM, Kombian SB, Zidichouski JA, Pittman QJ (1997) Cholecystokinin and neurotensin inversely modulate excitatory synaptic transmission in the parabrachial nucleus in vitro. Neuroscience 77:23–35

    PubMed  CAS  Google Scholar 

  76. Sanchez-Alavez M, Gomez-Chavarin M, Navarro L, Jimenez-Anguiano A, Murillo-Rodriguez E, Prado-Alcala RA, Drucker-Colin R, Prospero-Garcia O (2000) Cortistatin modulates memory processes in rats. Brain Res 858:78–83

    PubMed  CAS  Google Scholar 

  77. Sandin J, Georgieva J, Schott PA, Ogren SO, Terenius L (1997) Nociceptin/orphanin FQ microinjected into hippocampus impairs spatial learning in rats. Eur J Neurosci 9:194–197

    PubMed  CAS  Google Scholar 

  78. Schulz S, Handel M, Schreff M, Schmidt H, Hollt V (2000) Localization of five somatostatin receptors in the rat central nervous system using subtype-specific antibodies. J Physiol Paris 94:259–264

    PubMed  CAS  Google Scholar 

  79. Schweitzer P, Madamba SG, Siggins GR (1998) Somatostatin increases a voltage-insensitive K+ conductance in rat CA1 hippocampal neurons. J Neurophys 79:1230–1238

    CAS  Google Scholar 

  80. Sekizawa S-I, Joad JP, Bonham AC (2003) Substance P presynaptically depresses the transmission of sensory input to bronchopulmonary neurons in the guinea pig nucleus tractus solitarii. J Physiol 552:547–559

    PubMed  CAS  Google Scholar 

  81. Shaham Y, Kelsey JE, Stewart J (1995) Temporal factors in the effect of restraint stress on morphine-induced behavioral sensitization in the rat. Psychopharmacology (Berl) 117:102–109

    CAS  Google Scholar 

  82. Shen K-Z, Johnson SW (2002) Presynaptic modulation of synaptic transmission by opioid receptor in rat subthalamic nucleus in vitro. J Physiol 541:219–230

    PubMed  CAS  Google Scholar 

  83. Shibuya I, Noguchi J, Tanaka K, Harayama N, Inoue U, Kabashima N, Ueta Y, Hattori Y, Yamashita H (1998) PACAP increases the cytosolic Ca2+ concentration and stimulates somatodendritic vasopressin release in rat supraoptic neurons. J Neuroendocrinol 10:31–42

    PubMed  CAS  Google Scholar 

  84. Shuster SJ, Riedl M, Li X, Vulchanova L, Elde R (1999) Stimulus-dependent translocation of kappa opioid receptors to the plasma membrane. J Neurosci 19:2658–2664

    PubMed  CAS  Google Scholar 

  85. Shuster SJ, Riedl M, Li X, Vulchanova L, Elde R (2000) The kappa opioid receptor and dynorphin co-localize in vasopressin magnocellular neurosecretory neurons in guinea-pig hypothalamus. Neuroscience 96:373–383

    PubMed  CAS  Google Scholar 

  86. Simmons ML, Chavkin C (1996) kappa opioid receptor activation of a dendrotoxin-sensitive potassium channel mediates presynaptic inhibition of mossy fiber neurotransmitter release. Mol Pharmacol 50:80–85

    PubMed  CAS  Google Scholar 

  87. Simmons ML, Terman GW, Drake CT, Chavkin C (1994) Inhibition of glutamate release by presynaptic kappa 1-opioid receptors in the guinea pig dentate gyrus. J Neurophys 72:1697–1705

    CAS  Google Scholar 

  88. Simmons ML, Terman GW, Gibbs SM, Chavkin C (1995) L-type calcium channels mediate dynorphin neuropeptide release from dendrites but not axons of hippocampal granule cells. Neuron 14:1265–1272

    PubMed  CAS  Google Scholar 

  89. Straiker AJ, Borden CR, Sullivan JM (2002) G-protein alpha subunit isoforms couple differentially to receptors that mediate presynaptic inhibition at rat hippocampal synapses. J Neurosci 22:2460–2468

    PubMed  CAS  Google Scholar 

  90. Sun QQ, Huguenard JR, Prince DA (2002) Somatostatin inhibits thalamic network oscillations in vitro: actions on the GABAergic neurons of the reticular nucleus. J Neurosci 22:5374–5386

    PubMed  CAS  Google Scholar 

  91. Sutton LC, Lea SE, Will MJ, Schwartz BA, Hartley CE, Poole JC, Watkins LR, Maier SF (1997) Inescapable shock-induced potentiation of morphine analgesia. Behav Neurosci 111:1105–1113

    PubMed  CAS  Google Scholar 

  92. Svingos AL, Moriwaki A, Wang JB, Uhl GR, Pickel VM (1996) Ultrastructural immunocytochemical localization of mu opioid receptors in rat nucleus accumbens: extrasynaptic plasmalemmal distribution and association with Leu5-enkephalin. J Neurosci 16:4162–4173

    PubMed  CAS  Google Scholar 

  93. Svingos AL, Moriwaki A, Wang JB, Uhl GR, Pickel VM (1997) μ-Opioid receptors are localized to extrasynaptic plasma membranes of GABAergic neurons and their targets in the rat nucleus accumbens. J Neurosci 17:2585–2594

    PubMed  CAS  Google Scholar 

  94. Tallent M, Reisine T (1992) Giα1 selectively couples somatostatin receptors to adenyly cyclase in pituitary-derived AtT-20 cells. Mol Pharm 41:452–455

    CAS  Google Scholar 

  95. Tallent MK, Siggins GR (1997) Somatostatin depresses excitatory but not inhibitory neurotransmission in rat CA1 hippocampus. J Neurophys 78:3008–3018

    CAS  Google Scholar 

  96. Tallent MK, Siggins GR (1999) Somatostatin acts in CA1 and CA3 to reduce hippocampal epileptiform activity. J Neurophys 81:1626–1635

    CAS  Google Scholar 

  97. Tallent MK, Madamba SG, Siggins GR (1997) Somatostatin depresses excitatory neurotransmission in CA1 hippocampal neurons by a SST2-receptor-linked N-ethylmaleimide-sensitive G protein. Soc Neurosci Abstr 23:121

    Google Scholar 

  98. Tallent MK, Madamba SG, Siggins GR (2001) Nociceptin reduces epileptiform events in CA3 hippocampus via presynaptic and postsynaptic mechanisms. J Neurosci 21:6940–6948

    PubMed  CAS  Google Scholar 

  99. Tallent MK, Patterson C, Hon B, Qiu C, Zeyda T, Hochgeschwender U, de Lecea L (2005a) Somatostatin receptor subtype 3 is critical for hippocampal-dependent memory: studies in SST3 receptor knockout mice. Program no. 607.10, 2005 Abstract viewer/itinerary planner. Society for Neuroscience, Washington DC. Available online at http://sfn.scholarone.com/itin2005/ , last visted: 7 May 2007

  100. Tallent MK, Fabre V, Qiu C, Calbet M, Lamp T, Baratta MV, Suzuki C, Levy CL, Siggins GR, Henriksen SJ, Criado JR, Roberts A, de Lecea L (2005b) Cortistatin overexpression in transgenic mice produces deficits in synaptic plasticity and learning. Mol Cell Neurosci 30:465–475

    PubMed  CAS  Google Scholar 

  101. Terman GW, Wagner JJ, Chavkin C (1994) Kappa opioids inhibit induction of long-term potentiation in the dentate gyrus of the guinea pig hippocampus. J Neurosci 14:4740–4747

    PubMed  CAS  Google Scholar 

  102. van Bockstaele EJ, Commons K, Pickel VM (1997) Delta-opioid receptor is present in presynaptic axon terminals in the rat nucleus locus coeruleus: relationships with methionine5-enkephalin. J Comp Neurol 388:575–586

    PubMed  Google Scholar 

  103. van den Pol AN, Obrietan K, Chen G, Belousov AB (1996) Neuropeptide Y-mediated long-term depression of excitatory activity in suprachiasmatic nucleus neurons. J Neurosci 16:5883–5895

    PubMed  Google Scholar 

  104. Van Uden E, Veinbergs I, Mallory M, Orlando R, Masliah E (1999) A novel role for receptor-associated protein in somatostatin modulation: implications for Alzheimer's disease. Neuroscience 88:687–700

    PubMed  Google Scholar 

  105. Vaughan CW, Christie MJ (1997) Presynaptic inhibitory action of opioids on synaptic transmission in the rat periaqueductal grey in vitro. J Physiol 498:463–472

    PubMed  CAS  Google Scholar 

  106. Vaughan CW, Ingram SL, Christie MJ (1997a) Actions of the ORL1 receptor ligand nociceptin on membrane properties of rat periaqueductal gray neurons in vitro. J Neurosci 17:996–1003

    PubMed  CAS  Google Scholar 

  107. Vaughan CW, Ingram SL, Connor MA, Christie MJ (1997b) How opioids inhibit GABA-mediated neurotransmission. Nature 390:611–614

    PubMed  CAS  Google Scholar 

  108. Videau C, Hochgeschwender U, Kreienkamp HJ, Brennan MB, Viollet C, Richter D, Epelbaum J (2003) Characterisation of [125I]-Tyr0DTrp8-somatostatin binding in SST1- to SST4- and SRIF-gene-invalidated mouse brain. Naunyn Schmiedebergs Arch Pharmacol 367:562–571

    PubMed  CAS  Google Scholar 

  109. Wagner JJ, Caudle RM, Chavkin C (1992) Kappa-opioids decrease excitatory transmission in the dentate gyrus of the guinea pig hippocampus. J Neurosci 12:132–141

    PubMed  CAS  Google Scholar 

  110. Wagner JJ, Terman GW, Chavkin C (1993) Endogenous dynorphins inhibit excitatory neurotransmission and block LTP induction in the hippocampus. Nature 363:451–454

    PubMed  CAS  Google Scholar 

  111. Wang H, Moriwaki A, Wang JB, Uhl GR, Pickel VM (1996) Ultrastructural immunocytochemical localization of mu opioid receptors and Leu5-enkephalin in the patch compartment of the rat caudate-putamen nucleus. J Comp Neurol 375:659–674

    PubMed  CAS  Google Scholar 

  112. Weisskopf MG, Zalutsky RA, Nicoll RA (1993) The opioid peptide dynorphin mediates heterosynaptic depression of hippocampal mossy fibre synapses and modulates long-term potentiation. Nature 362:423–427

    PubMed  CAS  Google Scholar 

  113. Williams SH, Johnston D (1996) Actions of endogenous opioids on NMDA receptor-independent long-term potentiation in area CA3 of the hippocampus. J Neurosci 16:3652–3660

    PubMed  CAS  Google Scholar 

  114. Wotjak CT, Ganster J, Kohl G, Holsboer F, Landgraf R, Engelmann M (1998) Dissociated central and peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: new insights into the secretory capacities of peptidergic neurons. Neuroscience 85:1209–1222

    PubMed  CAS  Google Scholar 

  115. Yu TP, Xie CW (1998) Orphanin FQ/nociceptin inhibits synaptic transmission and long-term potentiation in rat dentate gyrus through postsynaptic mechanisms. J Neurophys 80:1277–1284

    CAS  Google Scholar 

  116. Yu TP, Fein J, Phan T, Evans CJ, Xie CW (1997) Orphanin FQ inhibits synaptic transmission and long-term potentiation in rat hippocampus. Hippocampus 7:88–94

    PubMed  CAS  Google Scholar 

  117. Zhu W, Pan ZZ (2005) mu-opioid-mediated inhibition of glutamate synaptic transmission in rat central amygdala neurons. Neuroscience 133:97–103

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pharmacology and Physiology, 245 N. 15th Street, PA 19102, Philadelphia, USA

    Melanie K. Tallent

Authors
  1. Melanie K. Tallent
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Melanie K. Tallent .

Editor information

Mark G. Darlison

Rights and permissions

Reprints and permissions

Copyright information

© 2007 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Tallent, M.K. (2007). Presynaptic Inhibition of Glutamate Release by Neuropeptides: Use-Dependent Synaptic Modification. In: Darlison, M.G. (eds) Inhibitory Regulation of Excitatory Neurotransmission. Results and Problems in Cell Differentiation, vol 44. Springer, Berlin, Heidelberg. https://doi.org/10.1007/400_2007_037

Download citation

Publish with us

Policies and ethics

Search

Navigation