Skip to main content
SpringerLink
Log in

The Three Faces of Norepinephrine: Plasticity at the Perforant Path-Dentate Gyrus Synapse

  • Chapter
Synaptic Plasticity and Transsynaptic Signaling

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.

10. References

  • Andres ME, Bustos G, Gysling K (1993) Regulation of [3H]norepinephrine release by N-methyl-D-aspartate receptors in minislices from the dentate gyrus and the CA1-CA3 area of the rat hippocampus. Biochem Pharmacol 46: 1983–1987.

    Article  PubMed  CAS  Google Scholar 

  • Aston-Jones G, Bloom FE (1981) Nonrepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli. J Neurosci 1: 887–900.

    PubMed  CAS  Google Scholar 

  • Babstock DM, Harley CW (1992) Paragigantocellularis stimulation induces beta-adrenergic hippocampal potentiation. Brain Res Bull 28: 709–714.

    Article  PubMed  CAS  Google Scholar 

  • Babstock DM, Harley CW (1993) Lateral olfactory tract input to dentate gyrus is depressed by prior noradrenergic activation using nucleus paragigantocellularis stimulation. Brain Res 629: 149–154.

    Article  PubMed  CAS  Google Scholar 

  • Bergado JA, Almaguer W, Ravelo J, Rosillo JC, Frey JU (2001) Behavioral reinforcement of long-term potentiation is impaired in aged rats with cognitive deficiencies. Neuroscience 108: 1–5.

    Article  PubMed  CAS  Google Scholar 

  • Bliss TV, Gardner-Medwin AR (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. J Physiol 232: 357–374.

    PubMed  CAS  Google Scholar 

  • Bliss TV, Goddard GV, Riives M (1983) Reduction of long-term potentiation in the dentate gyrus of the rat following selective depletion of monoamines. J Physiol 334: 475–491.

    PubMed  CAS  Google Scholar 

  • Bliss TV, Lømo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232: 331–356.

    PubMed  CAS  Google Scholar 

  • Bouret S, Sara SJ (2004) Reward expectation, orientation of attention and locus coeruleus-medial frontal cortex interplay during learning. Eur J Neurosci 20: 791–802.

    Article  PubMed  Google Scholar 

  • Bramham CR, Bacher-Svendsen K, Sarvey JM (1997) LTP in the lateral perforant path is beta-adrenergic receptor-dependent. Neuroreport 8: 719–724.

    PubMed  CAS  Google Scholar 

  • Bronzino JD, Kehoe P, Hendriks R, Vita L, Golas B, Vivona C, Morgane PJ (1999) Hippocampal neurochemical and electrophysiological measures from freely moving rats. Exp Neurol 155: 150–155.

    Article  PubMed  CAS  Google Scholar 

  • Bronzino JD, Kehoe P, Mallinson K, Fortin DA (2001) Increased extracellular release of hippocampal NE is associated with tetanization of the medial perforant pathway in the freely moving adult male rat. Hippocampus 11: 423–429.

    Article  PubMed  CAS  Google Scholar 

  • Burgard EC, Cote TE, Sarvey JM (1993) Muscarinic depression of synaptic transmission and blockade of norepinephrine-induced long-lasting potentiation in the dentate gyrus. Neuroscience 54: 377–389.

    Article  PubMed  CAS  Google Scholar 

  • Burgard EC, Decker G, Sarvey JM (1989) NMDA receptor antagonists block norepinephrine-induced long-lasting potentiation and long-term potentiation in rat dentate gyrus. Brain Res 482: 351–355.

    Article  PubMed  CAS  Google Scholar 

  • Burgard EC, Sarvey JM (1990) Muscarinic receptor activation facilitates the induction of long-term potentiation (LTP) in the rat dentate gyrus. Neurosci Lett 116: 34–39.

    Article  PubMed  CAS  Google Scholar 

  • Burgard EC, Sarvey JM (1991) Long-lasting potentiation and epileptiform activity produced by GABAB receptor activation in the dentate gyrus of rat hippocampal slice. J Neurosci 11: 1198–1209.

    PubMed  CAS  Google Scholar 

  • Chen HX, Roper SN (2003) PKA and PKC enhance excitatory synaptic transmission in human dentate gyrus. J Neurophysiol 89: 2482–2488.

    Article  PubMed  CAS  Google Scholar 

  • Dahl D, Burgard EC, Sarvey JM (1990) NMDA receptor antagonists reduce medial, but not lateral, perforant path-evoked EPSPs in dentate gyrus of rat hippocampal slice. Exp Brain Res 83: 172–177.

    Article  PubMed  CAS  Google Scholar 

  • Dahl D, Li J (1994a) Induction of long-lasting potentiation by sequenced applications of isoproterenol. Neuroreport 5: 657–660.

    PubMed  CAS  Google Scholar 

  • Dahl D, Li J (1994b) Interactive and discontinuous long-lasting potentiation in the dentate gyrus. Neuroreport 5: 1769–1772.

    Article  PubMed  CAS  Google Scholar 

  • Dahl D, Li J (1994c) Long-lasting potentiation and depression by novel isoproterenol and cholecystokinin 8-S interactions in the dentate gyrus. Exp Brain Res 100: 155–159.

    Article  PubMed  CAS  Google Scholar 

  • Dahl D, Sarvey JM (1989) Norepinephrine induces pathway-specific long-lasting potentiation and depression in the hippocampal dentate gyrus. Proc Natl Acad Sci U S A 86: 4776–4780.

    Article  PubMed  CAS  Google Scholar 

  • Dahl D, Winson J (1985) Action of norepinephrine in the dentate gyrus. I. Stimulation of locus coeruleus. Exp Brain Res 59: 491–496.

    Article  PubMed  CAS  Google Scholar 

  • Daoudal G, Debanne D (2003) Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn Mem 10: 456–465.

    Article  PubMed  Google Scholar 

  • Desai MA, Valli MJ, Monn JA, Schoepp DD (1995) 1-BCP, a memory-enhancing agent, selectively potentiates AMPA-induced [3H]norepinephrine release in rat hippocampal slices. Neuropharmacology 34: 141–147.

    Article  PubMed  CAS  Google Scholar 

  • Emptage NJ, Carew TJ (1993) Long-term synaptic facilitation in the absence of short-term facilitation in Aplysia neurons. Science 262: 253–256.

    PubMed  CAS  Google Scholar 

  • Ezrokhi VL, Zosimovskii VA, Korshunov VA, Markevich VA (1999) Restoration of decaying long-term potentiation in the hippocampal formation by stimulation of neuromodulatory nuclei in freely moving rats. Neuroscience 88: 741–753.

    Article  PubMed  CAS  Google Scholar 

  • Fink K, Gothert M, Molderings G, Schlicker E (1989) N-methyl-D-aspartate (NMDA) receptor-mediated stimulation of noradrenaline release, but not release of other neurotransmitters, in the rat brain cortex: receptor location, characterization and desensitization. Naunyn Schmiedebergs Arch Pharmacol 339: 514–521.

    Article  PubMed  CAS  Google Scholar 

  • Frick A, Magee J, Johnston D (2004) LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat Neurosci 7: 126–135.

    Article  PubMed  CAS  Google Scholar 

  • Frizzell LM, Harley CW (1994) The N-methyl-D-aspartate channel blocker ketamine does not attenuate, but enhances, locus coeruleus-induced potentiation in rat dentate gyrus. Brain Res 663: 173–178.

    Article  PubMed  CAS  Google Scholar 

  • Gray R, Johnston D (1987) Noradrenaline and beta-adrenoceptor agonists increase activity of voltage-dependent calcium channels in hippocampal neurons. Nature 327: 620–622.

    Article  PubMed  CAS  Google Scholar 

  • Haas HL, Rose GM (1987) Noradrenaline blocks potassium conductance in rat dentate granule cells in vitro. Neurosci Lett 78: 171–174.

    Article  PubMed  CAS  Google Scholar 

  • Harley C, Milway JS, Lacaille JC (1989) Locus coeruleus potentiation of dentate gyrus responses: evidence for two systems. Brain Res Bull 22: 643–650.

    Article  PubMed  CAS  Google Scholar 

  • Harley CW, Lalies MD, Nutt DJ (1996) Estimating the synaptic concentration of norepinephrine in dentate gyrus which produces beta-receptor mediated long-lasting potentiation in vivo using microdialysis and intracerebroventricular norepinephrine. Brain Res 710: 293–298.

    Article  PubMed  CAS  Google Scholar 

  • Harley CW, Milway JS (1986) Glutamate ejection in the locus coeruleus enhances the perforant path-evoked population spike in the dentate gyrus. Exp Brain Res 63: 143–150.

    Article  PubMed  CAS  Google Scholar 

  • Harley CW, Sara SJ (1992) Locus coeruleus bursts induced by glutamate trigger delayed perforant path spike amplitude potentiation in the dentate gyrus. Exp Brain Res 89: 581–587.

    Article  PubMed  CAS  Google Scholar 

  • Jester JM, Campbell LW, Sejnowski TJ (1995) Associative EPSP—spike potentiation induced by pairing orthodromic and antidromic stimulation in rat hippocampal slices. J Physiol 484 (Pt 3): 689–705.

    PubMed  CAS  Google Scholar 

  • Kitchigina V., Vankov A., Harley C., Sara S.J. (1997) Novelty-elicited, noradrenaline-dependent enhancement of excitability in the dentate gyrus. Eur. J. Neurosci. 9: 41–47.

    Article  PubMed  CAS  Google Scholar 

  • Klukowski G, Harley CW (1994) Locus coeruleus activation induces perforant path-evoked population spike potentiation in the dentate gyrus of awake rat. Exp Brain Res 102: 165–170.

    Article  PubMed  CAS  Google Scholar 

  • Kohara K, Ogura A, Akagawa K, Yamaguchi K (2001) Increase in number of functional release sites by cyclic AMP-dependent protein kinase in cultured neurons isolated from hippocampal dentate gyrus. Neurosci Res 41: 79–88.

    Article  PubMed  CAS  Google Scholar 

  • Lacaille JC, Harley CW (1985) The action of norepinephrine in the dentate gyrus: beta-mediated facilitation of evoked potentials in vitro. Brain Res 358: 210–220.

    Article  PubMed  CAS  Google Scholar 

  • Loy R, Koziell DA, Lindsey JD, Moore RY (1980) Noradrenergic innervation of the adult rat hippocampal formation. J Comp Neurol 189: 699–710.

    Article  PubMed  CAS  Google Scholar 

  • Lynch MA, Bliss TV (1986) Noradrenaline modulates the release of [14C]glutamate from dentate but not from CA1/CA3 slices of rat hippocampus. Neuropharmacology 25: 493–498.

    Article  PubMed  CAS  Google Scholar 

  • Mauclshagen J, Sherff CM, Carew TJ (1998) Differential induction of long-term synaptic facilitation by spaced and massed applications of serotonin at sensory neuron synapses of Aplysia californica. Learn Mem 5: 246–256.

    Google Scholar 

  • Mermelstein PG, Deisseroth K, Dasgupta N, Isaksen AL, Tsien RW (2001) Calmodulin priming: nuclear translocation of a calmodulin complex and the memory of prior neuronal activity. Proc Natl Acad Sci U S A 98: 15342–15347.

    Article  PubMed  CAS  Google Scholar 

  • Munro CA, Walling SG, Evans JH, Harley CW (2001) Beta-adrenergic blockade in the dentate gyrus in vivo prevents high frequency-induced long-term potentiation of EPSP slope, but not long-term potentiation of population spike amplitude. Hippocampus 11: 322–328.

    Article  PubMed  CAS  Google Scholar 

  • Neuman RS, Harley CW (1983) Long-lasting potentiation of the dentate gyrus population spike by norepinephrine. Brain Res 273: 162–165.

    Article  PubMed  CAS  Google Scholar 

  • Nguyen PV, Kandel ER (1996) A macromolecular synthesis-dependent late phase of long-term potentiation requiring cAMP in the medial perforant pathway of rat hippocampal slices. J Neurosci 16: 3189–3198.

    PubMed  CAS  Google Scholar 

  • Parfitt KD, Doze VA, Madison DV, Browning MD (1992) Isoproterenol increases the phosphorylation of the synapsins and increases synaptic transmission in dentate gyrus, but not in area CA1, of the hippocampus. Hippocampus 2: 59–64.

    Article  PubMed  CAS  Google Scholar 

  • Parfitt KD, Hoffer BJ, Browning MD (1991) Norepinephrine and isoproterenol increase the phosphorylation of synapsin I and synapsin II in dentate slices of young but not aged Fisher 344 rats. Proc Natl Acad Sci U S A 88: 2361–2365.

    Article  PubMed  CAS  Google Scholar 

  • Pelletier MR, Kirkby RD, Jones SJ, Corcoran ME (1994) Pathway specificity of noradrenergic plasticity in the dentate gyrus. Hippocampus 4: 181–188.

    Article  PubMed  CAS  Google Scholar 

  • Pittaluga A, Raiteri M (1992) N-methyl-D-aspartic acid (NMDA) and non-NMDA receptors regulating hippocampal norepinephrine release. III. Changes in the NMDA receptor complex induced by their functional cooperation. J Pharmacol Exp Ther 263: 327–333.

    PubMed  CAS  Google Scholar 

  • Pittaluga A, Thellung S, Maura G, Raiteri M (1994) Characterization of two central AMPA-preferring receptors having distinct location, function and pharmacology. Naunyn Schmiedebergs Arch Pharmacol 349: 555–558.

    Article  PubMed  CAS  Google Scholar 

  • Richter-Levin G, Segal M, Sara S (1991) An alpha 2 antagonist, idazoxan, enhances EPSP-spike coupling in the rat dentate gyrus. Brain Res 540: 291–294.

    Article  PubMed  CAS  Google Scholar 

  • Robinson GB, Racine RJ (1985) Long-term potentiation in the dentate gyrus: effects of noradrenaline depletion in the awake rat. Brain Res 325: 71–78.

    Article  PubMed  CAS  Google Scholar 

  • Sara SJ, Bergis O (1991) Enhancement of excitability and inhibitory processes in hippocampal dentate gyrus by noradrenaline: a pharmacological study in awake, freely moving rats. Neurosci Lett 126: 1–5.

    Article  PubMed  CAS  Google Scholar 

  • Sara SJ, Segal M (1991) Plasticity of sensory responses of locus coeruleus neurons in the behaving rat: implications for cognition. Prog Brain Res 88: 571–585.

    PubMed  CAS  Google Scholar 

  • Sara SJ, Vankov A, Herve A (1994) Locus coeruleus-evoked responses in behaving rats: a clue to the role of noradrenaline in memory. Brain Res Bull 35: 457–465.

    Article  PubMed  CAS  Google Scholar 

  • Sarvey JM, Burgard EC, Decker G (1989) Long-term potentiation: studies in the hippocampal slice. J Neurosci Methods 28: 109–124.

    Article  PubMed  CAS  Google Scholar 

  • Schrader LA, Anderson AE, Varga AW, Levy M, Sweatt JD (2002) The other half of Hebb: K+ channels and the regulation of neuronal excitability in the hippocampus. Mol Neurobiol 25: 51–66.

    Article  PubMed  CAS  Google Scholar 

  • Segal M, Greenberger V, Hofstein R (1981) Cyclic AMP-generating systems in rat hippocampal slices. Brain Res 213: 351–364.

    Article  PubMed  CAS  Google Scholar 

  • Segal M, Markram H, Richter-Levin G (1991) Actions of norepinephrine in the rat hippocampus. Prog Brain Res 88: 323–330.

    Article  PubMed  CAS  Google Scholar 

  • Seidenbecher T, Reymann KG, Balschun D (1997) A post-tetanic time window for the reinforcement of long-term potentiation by appetitive and aversive stimuli. Proc Natl Acad Sci U S A 94: 1494–1499.

    Article  PubMed  CAS  Google Scholar 

  • Staff NP, Spruston N (2003) Intracellular correlate of EPSP-spike potentiation in CA1 pyramidal neurons is controlled by GABAergic modulation. Hippocampus 13: 801–805.

    Article  PubMed  CAS  Google Scholar 

  • Stanton PK, Heinemann U (1986) Norepinephrine enhances stimulus-evoked calcium and potassium concentration changes in dentate granule cell layer. Neurosci Lett 67: 233–238.

    Article  PubMed  CAS  Google Scholar 

  • Stanton PK, Sarvey JM (1985a) Blockade of norepinephrine-induced long-lasting potentiation in the hippocampal dentate gyrus by an inhibitor of protein synthesis. Brain Res 361: 276–283.

    Article  PubMed  CAS  Google Scholar 

  • Stanton PK, Sarvey JM (1985b) Depletion of norepinephrine, but not serotonin, reduces long-term potentiation in the dentate gyrus of rat hippocampal slices. J. Neurosci. 5: 2169–2176.

    PubMed  CAS  Google Scholar 

  • Stanton PK, Sarvey JM (1985c) The effect of high-frequency electrical stimulation and norepinephrine on cyclic AMP levels in normal versus norepinephrine-depleted rat hippocampal slices. Brain Res 358: 343–348.

    Article  PubMed  CAS  Google Scholar 

  • Stanton PK, Sarvey JM (1987) Norepinephrine regulates long-term potentiation of both the population spike and dendritic EPSP in hippocampal dentate gyrus. Brain Res Bull 18: 115–119.

    Article  PubMed  CAS  Google Scholar 

  • Straubc T, Frcy JU (2003) Involvement of beta-adrencrgic receptors in protein synthesis-dependent late long-term potentiation (LTP) in the dentate gyrus of freely moving rats: the critical role of the LTP induction strength. Neuroscience 119: 473–479.

    Article  CAS  Google Scholar 

  • Straube T, Korz V, Balschun D, Frey JU (2003) Requirement of beta-adrenergic receptor activation and protein synthesis for LTP-reinforcement by novelty in rat dentate gyrus. J Physiol 552: 953–960.

    Article  PubMed  CAS  Google Scholar 

  • Swanson-Park JL, Coussens CM, Mason-Parker SE, Raymond CR, Hargreaves EL, Dragunow M, Cohen AS, Abraham WC (1999) A double dissociation within the hippocampus of dopamine D1/D5 receptor and beta-adrenergic receptor contributions to the persistence of long-term potentiation. Neuroscience 92: 485–497.

    Article  PubMed  CAS  Google Scholar 

  • Vankov A, Herve-Minvielle A, Sara SJ (1995) Response to novelty and its rapid habituation in locus coeruleus neurons of the freely exploring rat. Eur J Neurosci 7: 1180–1187.

    Article  PubMed  CAS  Google Scholar 

  • Walling SG, Harley CW (2004) Locus ceruleus activation initiates delayed synaptic potentiation of perforant path input to the dentate gyrus in awake rats: a novel beta-adrenergic-and protein synthesis-dependent mammalian plasticity mechanism. J Neurosci 24: 598–604.

    Article  PubMed  CAS  Google Scholar 

  • Walling, S. G., Nutt, D. J., Lalies, M. D., and Harley, C. W. Orexin-A infusion in the locus coeruleus triggers norepinephrine (NE) release and NE-induced long-term potentiation in the dentate gyrus. J. Neurosci. 24: in press.

    Google Scholar 

  • Washburn M, Moises HC (1989) Electrophysiological correlates of presynaptic alpha 2-receptor-mediated inhibition of norepinephrine release at locus coeruleus synapses in dentate gyrus. J Neurosci 9: 2131–2140.

    PubMed  CAS  Google Scholar 

  • Wigstrom H, Gustafsson B (1983a) Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition. Nature 301: 603–604.

    Article  PubMed  CAS  Google Scholar 

  • Wigstrom H, Gustafsson B (1983b) Large long-lasting potentiation in the dentate gyrus in vitro during blockade of inhibition. Brain Res 275: 153–158.

    Article  PubMed  CAS  Google Scholar 

  • Winson J, Dahl D (1985) Action of norepinephrine in the dentate gyrus. II. Iontophoretic studies. Exp Brain Res 59: 497–506.

    Article  PubMed  CAS  Google Scholar 

  • Xie CW, Lewis DV (1997) Involvement of cAMP-dependent protein kinase in mu-opioid modulation of NMDA-mediated synaptic currents. J Neurophysiol 78: 759–766.

    PubMed  CAS  Google Scholar 

  • Zhang W, Linden DJ (2003) The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci 4: 885–900.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Memorial University, St. John’s, Newfoundland, A1B 3X9

    Carolyn W. Harley

  2. Mount Allison University, Sackville, New Brunswick, EIG 1H7

    Susan G. Walling

  3. University of California, Los Angeles, Los Angeles, California, 90095

    Robert A. M. Brown

Authors
  1. Carolyn W. Harley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susan G. Walling
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert A. M. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Neurology, New York Medical College, Valhalla, NY, 10595, USA

    Patrick K. Stanton

  2. Department of Physiology, University of Bergen, Bergen, 5009, Norway

    Clive Bramham

  3. CNRRR Department, Helen Hayes Hospital, West Haverstraw, NY, 10993, USA

    Helen E. Scharfman

Rights and permissions

Reprints and permissions

Copyright information

© 2005 Springer Science+Business Media, Inc.

About this chapter

Cite this chapter

Harley, C.W., Walling, S.G., Brown, R.A.M. (2005). The Three Faces of Norepinephrine: Plasticity at the Perforant Path-Dentate Gyrus Synapse. In: Stanton, P.K., Bramham, C., Scharfman, H.E. (eds) Synaptic Plasticity and Transsynaptic Signaling. Springer, Boston, MA. https://doi.org/10.1007/0-387-25443-9_1

Download citation

Publish with us

Policies and ethics

Search

Navigation