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Inhibition of associative long-term depression by activation of β-adrenergic receptors in rat hippocampal CA1 synapses

  • Published:
Journal of Biomedical Science

Abstract

The aim of this study was to investigate the role of β-adrenergic receptors in modulating associative long-term depression (LTD) at CA1 synapses in rat hippocampal slices. Standard extracellular electrophysiological techniques were employed to record field excitatory post-synaptic potential (fEPSP) activity and to induce associative LTD. Two independent Schaffer collateral pathways were elicited in hippocampal CA1 areas. In one (weak) pathway, the stimulating intensity was adjusted to elicit small fEPSP activity (20–30% of the maximum response). In contrast, 80–90% of the maximum response was evoked in the other (strong) pathway. Associative LTD of weak pathway could be induced by paired stimulation of weak and the strong pathways, repeated 100 times at 0.167 Hz. The associative LTD of weak pathway was NMDA receptor- and phophatase 2B dependent, because bath application of 50 µM D, L-AP5 or 10 µM cypermethrin blocked its induction. Bath application of 1 µM isoproterenol inhibited associative LTD, and this effect was blocked by timolol, suggesting the involvement of β-adrenergic receptors. The inhibitory effect of β-adrenergic receptors on LTD induction was blocked in slices pretreated with inhibitors of protein kinase A and mitogen-activated protein kinase, suggesting that these signal cascades are downstream effectors following activation of β-adrenergic receptors. Nevertheless, bath application of timolol or cypermethrin alone did not have significant effect on associative LTD induction, suggesting neither endogenous function of β-adrenergic receptor nor endogenous PKA activity does have a role in associative LTD induction.

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References

  1. Bliss T.V.P., Collingridge G.L. Synaptic model of memory: long term potantiation in the hippocampus. Nature 361:31–39, 1993

    Article  PubMed  CAS  Google Scholar 

  2. Malenka R.C., Nicoll R.A. Long term potentiation: a decade of progress? Science 285:1870–1875, 1999

    Article  PubMed  CAS  Google Scholar 

  3. Barrionuevo G., Schottler F., Lynch G. The effects of repetitive low frequency stimulation on control and “potentate” synaptic responses in the hippocampus. Life Sci. 27(24):2385–2391, 1980

    Article  PubMed  CAS  Google Scholar 

  4. Kemp N., Bashir Z.I. Long-term depression: a cascade of induction and expression mechanisms. Prog. Neurobiol. 65(4):339–365, 2001

    Article  PubMed  CAS  Google Scholar 

  5. Mulkey R.M., Malenka R.C. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9(5):967–975, 1992

    Article  PubMed  CAS  Google Scholar 

  6. Dudek S.M., Bear M.F. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J. Neurosci. 13(7):2910–2918, 1993

    PubMed  CAS  Google Scholar 

  7. D’Alcantara P., Schiffmann S.N., Swillens S. Bidirectional synaptic plasticity as a consequence of interdependent Ca2+-controlled phosphorylation and dephosphorylation pathways. Eur. J. Neurosci. 17(12):2521–2528, 2003

    Article  PubMed  Google Scholar 

  8. Bi G.-Q., Poo M.-M. Synaptic modification in cultured hippocampal neuron: dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18:10464–10472, 1998

    PubMed  CAS  Google Scholar 

  9. Feldman D.E. Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27:45–56, 2000

    Article  PubMed  CAS  Google Scholar 

  10. Bi G.-Q. Spatiotemporal specificity of synaptic plasticity: cellular rules and mechanisms. Biol. Cybern. 87(5–6):319–332, 2002

    Article  PubMed  Google Scholar 

  11. Tzounopoulos T., Rubio M.E., Keen J.E., Trussell L.O. Coactivation of pre- and postsynaptic signaling mechanisms determines cell-specific spike-timing-dependent plasticity. Neuron 54:291–301, 2007

    Article  PubMed  CAS  Google Scholar 

  12. Froemke R.C., Dan Y. Spike-timing-dependent synaptic modification induced by natural spike trains. Nature 416:433–438, 2002

    Article  PubMed  CAS  Google Scholar 

  13. Lin Y.-W., Min M.-Y., Chiu T.-H., Yang H.-W. Enhancement of associative long-term potentiation by activation of β-adrenergic receptors at CA1 synapses in rat hippocampal slices. J. Neurosci. 23:4173–4181, 2003

    PubMed  CAS  Google Scholar 

  14. Lin Y.-W., Yang H.-W., Wang H.-J., Gong C.-L., Chiu T.-H., Min M.-Y. Spike-timing-dependent plasticity at resting and conditioned lateral perforant path synapses on granule cells in the dentate gyrus: different roles of N-methyl-d-aspartate and group I metabotropic glutamate receptors. Eur. J. Neurosci. 23:2362–2374, 2006

    Article  PubMed  Google Scholar 

  15. Debanne D., Gahwiler B.H., Thomson S.M. Asynchronous pre- and postsynaptic activity induces associative long-term depression in area CA1 of the rat hippocampus in vitro. Proc. Natl. Acad. Sci. USA 91:1148–1152, 1994

    Article  PubMed  CAS  Google Scholar 

  16. Markram H., Lubke J., Frotscher M., Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213–215, 1997

    Article  PubMed  CAS  Google Scholar 

  17. Debanne D., Gahwiler B.H., Thomson S.M. Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J. Physiol. (Lond) 507:237–247, 1998

    Article  CAS  Google Scholar 

  18. Jacob B., Brasier D.J., Erchova I., Feldman D., Shulz D.E. Spike timing-dependent synaptic depression in the in vivo barrel cortex of the rat. J. Neurosci. 27(6):1271–1284, 2007

    Article  PubMed  CAS  Google Scholar 

  19. Lante F., Cavalier M., Cohen-Solal C., Guiramand J., Vignes M. Developmental switch from LTD to LTP in low frequency-induced plasticity. Hippocampus 16(11):981–989, 2006

    Article  PubMed  CAS  Google Scholar 

  20. Kirkwood A., Silva A., Bear M.F. Age-dependent decrease of synaptic plasticity in the neocortex of alphaCaMKII mutant mice. Proc. Natl. Acad. Sci. USA 94(7):3380–3383, 1997

    Article  PubMed  CAS  Google Scholar 

  21. Oliet S.H., Malenka R.C., Nicoll R.A. Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron 18:969–982, 1997

    Article  PubMed  CAS  Google Scholar 

  22. Nicoll R.A., Oliet S.H., Malenka R.C. NMDA receptor-dependent and metabotropic glutamate receptor-dependent forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neurobiol. Learn. Mem. 70:62–72, 1998

    Article  PubMed  CAS  Google Scholar 

  23. Zho W.-M., You J.-L., Huang C.-C., Hsu K.-S. The group I metabotropic glutamate receptor agonist (S)-3, 5-dihydroxyphenylglycine induces a novel form of depotentiation in the CA1 region of the hippocampus. J. Neurosci. 22:8838–8849, 2002

    PubMed  CAS  Google Scholar 

  24. Mulkey R.M., Herron C.E., Malenka R.C. An essential role for protein phosphatases in hippocampal long term depression. Science 261:1051–1055, 1993

    Article  PubMed  CAS  Google Scholar 

  25. Mulkey R.M., Endo S., Shenolikar S., Malenka R.C. Involvement of a calcineurin/inhibitor I phosphatase cascade in hippocampal long-term depression. Nature 36: 486–488, 1994

    Article  Google Scholar 

  26. Katsuki H., Izumi Y., Zorumski C.F. Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region. J. Neurosphysiol. 77:3013–3020, 1997

    CAS  Google Scholar 

  27. Yang H.-W., Lin Y.-W., Yen C.-D., Min M.-Y. Change in bidirectional plasticity at CA1 synapses in hippocampal slices taken from 6-hydroxydopamine treated rats: the role of endogenous norepinephrine. Eur. J. Neurosci. 16:1117–1128, 2002

    Article  PubMed  Google Scholar 

  28. Aston-Jones G., Shipley M.T., Grzanna P. The locus coeruleus and A7 noradrenergic cell groups. In Paxions G. (Ed) The rat Nervous System. Academic Press, San Diego 183–213, 1993

    Google Scholar 

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Authors and Affiliations

  1. Institute of Biomedical Science, Academia Sinica, Taipei, 115, Taiwan

    Yi-Wen Lin

  2. Department of Life Sciences, Chung Shan Medical University, Taichung, 402, Taiwan

    Hsiu-Wen Yang

  3. Department of Life Science, National Taiwan University, Taipei, 106, Taiwan

    Ming-Yuan Min

  4. Department of Physiology, National Yang Ming University, Taipei, 102, Taiwan

    Tsai-Hsien Chiu

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  1. Yi-Wen Lin
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  2. Hsiu-Wen Yang
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Correspondence to Yi-Wen Lin.

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Lin, YW., Yang, HW., Min, MY. et al. Inhibition of associative long-term depression by activation of β-adrenergic receptors in rat hippocampal CA1 synapses. J Biomed Sci 15, 123–131 (2008). https://doi.org/10.1007/s11373-007-9205-z

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  • DOI: https://doi.org/10.1007/s11373-007-9205-z

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