Skip to main content
SpringerLink
Log in

An associativity requirement for locus coeruleus-induced long-term potentiation in the dentate gyrus of the urethane-anesthetized rat

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Norepinephrine has been hypothesized to provide a learning and memory signal. Norepinephrine long-term potentiation of perforant path input to the dentate gyrus of the hippocampus provides a model for norepinephrine initiated memory processes. However, in vitro, the pairing of perforant path stimulation and norepinephrine is not required for the occurrence of norepinephrine-dependent long-term potentiation. Since bath application of norepinephrine induces long-term changes in 2nd messenger signalling and differs in a number of ways from physiological norepinephrine release, the present study is an in vivo test of the associative requirement for the pairing of perforant path input with norepinephrine to induce long-term potentiation. Phasic activation of the locus coeruleus is provided by glutamate infusion into the locus coeruleus to initiate transient norepinephrine release in the hippocampus of urethane-anesthetized Sprague-Dawley rats. Perforant path stimulation (0.067 Hz) was given throughout the experiment in the paired condition. In the unpaired condition perforant path stimulation was interrupted 10 min prior to locus coeruleus activation and resumed 10 min after locus coeruleus activation. Locus coeruleus-induced long-term potentiation of both EPSP slope and population spike only occurred in the pairing condition. This result argues that, in vivo, temporal proximity of locus coeruleus-associated norepinephrine release and perforant path stimulation are required to induce long-term plasticity. The associativity requirement for locus coeruleus activation and perforant path stimulation in vivo is consistent with the hypothesis that norepinephrine can initiate circuit changes supporting learning and memory.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alger BE, Teyler TJ (1976) Long-term and short-term plasticity in the CA1, CA3, and dentate regions of the rat hippocampal slice. Brain Res 110:463–480

    Article  CAS  PubMed  Google Scholar 

  • Aston-Jones G, Shipley MT, Grzanna R (1995) The locus coeruleus, A5 and A7 noradrenergic cell groups. In: Paxinos G (ed) The rat nervous system. Academic Press, New York, pp 183–214

    Google Scholar 

  • Bliss TV, Lomo 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

    CAS  PubMed  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 USA 86:4776–4780

    Article  CAS  PubMed  Google Scholar 

  • Dahl D, Sarvey JM (1990) Beta-adrenergic agonist-induced long-lasting synaptic modifications in hippocampal dentate gyrus require activation of NMDA receptors, but not electrical activation of afferents. Brain Res 526:347–350

    Article  CAS  PubMed  Google Scholar 

  • Diamond DM, Campbell AM, Park CR, Halonen J, Zoladz PR (2007) The temporal dynamics model of emotional memory processing: a synthesis on the neurobiological basis of stress-induced amnesia, flashbulb and traumatic memories, and the Yerkes-Dodson law. Neural Plast 2007:60803

    Article  PubMed  Google Scholar 

  • Elmslie KS, Cohen DH (1990) Iontophoresis of norepinephrine onto neurons of the pigeon’s lateral geniculate nucleus: characterization of an inhibitory response. Brain Res 517:134–142

    Article  CAS  PubMed  Google Scholar 

  • Frey S, Bergado-Rosado J, Seidenbecher T, Pape HC, Frey JU (2001) Reinforcement of early long-term potentiation (early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: heterosynaptic induction mechanisms of late-LTP. J Neurosci 21:3697–3703

    CAS  PubMed  Google Scholar 

  • Gibbs CM, Cohen DH, Broyles JL (1986) Modification of the discharge of lateral geniculate neurons during visual learning. J Neurosci 6:627–636

    CAS  PubMed  Google Scholar 

  • Gilbert ME, Mack CM (1999) Field potential recordings in dentate gyrus of anesthetized rats: stability of baseline. Hippocampus 9:277–287

    Article  CAS  PubMed  Google Scholar 

  • Harley CW, Evans S (1988) Locus coeruleus-induced enhancement of the perforant path evoked potential: effects of intradentate beta blockers. In: Woody CD, Alkon DL, McGaugh JL (eds) Cellular mechanisms of conditioning and behavioral plasticity. Plenum, New York, pp 415–423

    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  CAS  PubMed  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Harris EW, Lasher SS, Steward O (1978) Habituation-like decrements in transmission along the normal and lesion-induced temporodentate pathways in the rat. Brain Res 151:623–631

    Article  CAS  PubMed  Google Scholar 

  • Harris EW, Lasher SS, Steward O (1979) Analysis of the habituation-like changes in transmission in the temporodentate pathway of the rat. Brain Res 162:21–32

    Article  CAS  PubMed  Google Scholar 

  • Kety SS (1970) The biogenic amines in the central nervous system: their possible roles in arousal, emotion and learning. In: Schmidt FO (ed). Rockefeller Press, New York, pp 324–335

  • 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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Moriceau S, Wilson DA, Levine S, Sullivan RM (2006) Dual circuitry for odor-shock conditioning during infancy: corticosterone switches between fear and attraction via amygdala. J Neurosci 26:6737–6748

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Palamarchouk VS, Zhang J, Zhou G, Swiergiel AH, Dunn AJ (2000) Hippocampal norepinephrine-like voltammetric responses following infusion of corticotropin-releasing factor into the locus coeruleus. Brain Res Bull 51:319–326

    Article  CAS  PubMed  Google Scholar 

  • Palamarchouk VS, Swiergiel AH, Dunn AJ (2002) Hippocampal noradrenergic responses to CRF injected into the locus coeruleus of unanesthetized rats. Brain Res 950:31–38

    Article  CAS  PubMed  Google Scholar 

  • Rick JT, Milgram NW (1999) Instability of dentate gyrus field potentials in awake and anesthetized rats. Hippocampus 9:333–339

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Stanton PK, Sarvey JM (1985a) 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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Stone EA, John SM (1990) In vivo measurement of extracellular cyclic AMP in the brain: use in studies of beta-adrenoceptor function in nonanesthetized rats. J Neurochem 55:1942–1949

    Article  CAS  PubMed  Google Scholar 

  • Stone EA, Zhang Y, Carr KD (1995) Massive activation of c-fos in forebrain after mechanical stimulation of the locus coeruleus. Brain Res Bull 36:77–80

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Walling SG, Nutt DJ, Lalies MD, Harley CW (2004) Orexin-A infusion in the locus ceruleus triggers norepinephrine (NE) release and NE-induced long-term potentiation in the dentate gyrus. J Neurosci 24:7421–7426

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors wish to acknowledge support from the Natural Sciences and Engineering Council of Canada whose support to CWH permitted these experiments to be carried out.

Author information

Authors and Affiliations

  1. Section Neurophysiology and Neuroinformatics, Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen Medical Center, Nijmegen, 6500 HB, Netherlands

    Andrew T. Reid

  2. Vogt Brain Research Institute, University Clinics Dusseldorf, Heinrich Heine University, Dusseldorf, 40225, Germany

    Andrew T. Reid

  3. Department of Psychology, Memorial University of Newfoundland, St. John’s, NL, A1B3X9, Canada

    Carolyn W. Harley

Authors
  1. Andrew T. Reid
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carolyn W. Harley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carolyn W. Harley.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reid, A.T., Harley, C.W. An associativity requirement for locus coeruleus-induced long-term potentiation in the dentate gyrus of the urethane-anesthetized rat. Exp Brain Res 200, 151–159 (2010). https://doi.org/10.1007/s00221-009-1955-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-009-1955-6

Keywords

Search

Navigation