Synaptic activation of mGluR1 generates persistent depression of a fast after-depolarizing potential in CA3 pyramidal neurons

European Journal of Neuroscience

Volumn 33, Issue 5, 2011, Pages 879-889

  Brown, Jon T ^a   Booth, Clair A ^a   Randall, Andrew D ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Burst; Excitability; Glutamate receptor; Hippocampus; Plasticity

Indexed keywords

ADENOSINE DIPHOSPHATE; CALCIUM ION; METABOTROPIC RECEPTOR 1;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; HIPPOCAMPAL CA3 REGION; MALE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL STIMULATION; NEUROMODULATION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; RECEPTOR BLOCKING; SYNAPSE;

ACTION POTENTIALS; ANIMALS; BENZOATES; EXCITATORY AMINO ACID ANTAGONISTS; GLYCINE; HIPPOCAMPUS; MALE; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPSES;

EID: 79952441783     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07565.x     Document Type: Article

References (39)

1. Bean, B.P. (2007) The action potential in mammalian central neurons. Nat. Rev., 8, 451-465.
2. Bianchi, R., Chuang, S.C., Zhao, W., Young, S.R. & Wong, R.K. (2009) Cellular plasticity for group I mGluR-mediated epileptogenesis. J. Neurosci., 29, 3497-3507.
3. Brager, D.H. & Johnston, D. (2007) Plasticity of intrinsic excitability during long-term depression is mediated through mGluR-dependent changes in I(h) in hippocampal CA1 pyramidal neurons. J. Neurosci., 27, 13926-13937.
4. Brown, J.T. & Randall, A.D. (2009) Activity-dependent depression of the spike after-depolarization generates long-lasting intrinsic plasticity in hippocampal CA3 pyramidal neurons. J. Physiol., 587, 1265-1281.
5. Campanac, E. & Debanne, D. (2007) Plasticity of neuronal excitability: Hebbian rules beyond the synapse. Arch. Ital. Biol., 145, 277-287.
6. Carlier, E., Sourdet, V., Boudkkazi, S., Deglise, P., Ankri, N., Fronzaroli-Molinieres, L. & Debanne, D. (2006) Metabotropic glutamate receptor subtype 1 regulates sodium currents in rat neocortical pyramidal neurons. J. Physiol., 577, 141-154.
7. Chuang, S.C., Zhao, W., Young, S.R., Conquet, F., Bianchi, R. & Wong, R.K. (2002) Activation of group I mGluRs elicits different responses in murine CA1 and CA3 pyramidal cells. J. Physiol., 541, 113-121.
8. Clement, J.P., Randall, A.D. & Brown, J.T. (2009) mGluR1 activity generates persistent, NMDA receptor-dependent, depression of hippocampal pyramidal cell excitability. Eur. J. Neurosci., 29, 2347-2362.
9. Daoudal, G. & Debanne, D. (2003) Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn. Mem., 10, 456-465.
10. Davies, C.H., Clarke, V.R., Jane, D.E. & Collingridge, G.L. (1995) Pharmacology of postsynaptic metabotropic glutamate receptors in rat hippocampal CA1 pyramidal neurones. Br. J. Pharmacol., 116, 1859-1869.
11. Derjean, D., Bertrand, S., Le Masson, G., Landry, M., Morisset, V. & Nagy, F. (2003) Dynamic balance of metabotropic inputs causes dorsal horn neurons to switch functional states. Nat. Neurosci., 6, 274-281.
12. Dutar, P. & Nicoll, R.A. (1988) Classification of muscarinic responses in hippocampus in terms of receptor subtypes and second-messenger systems: electrophysiological studies in vitro. J. Neurosci., 8, 4214-4224.
13. Fan, Y., Fricker, D., Brager, D.H., Chen, X., Lu, H.C., Chitwood, R.A. & Johnston, D. (2005) Activity-dependent decrease of excitability in rat hippocampal neurons through increases in I(h). Nat. Neurosci., 8, 1542-1551.
14. Fitzjohn, S.M., Palmer, M.J., May, J.E., Neeson, A., Morris, S.A. & Collingridge, G.L. (2001) A characterisation of long-term depression induced by metabotropic glutamate receptor activation in the rat hippocampus in vitro. J. Physiol., 537, 421-430.
15. Higgs, M.H. & Spain, W.J. (2009) Conditional bursting enhances resonant firing in neocortical layer 2-3 pyramidal neurons. J. Neurosci., 29, 1285-1299.
16. Ireland, D.R., Guevremont, D., Williams, J.M. & Abraham, W.C. (2004) Metabotropic glutamate receptor-mediated depression of the slow afterhyperpolarization is gated by tyrosine phosphatases in hippocampal CA1 pyramidal neurons. J. Neurophysiol., 92, 2811-2819.
17. Kaczorowski, C.C., Disterhoft, J. & Spruston, N. (2007) Stability and plasticity of intrinsic membrane properties in hippocampal CA1 pyramidal neurons: effects of internal anions. J. Physiol., 578, 799-818.
18. Kandel, E.R. & Spencer, W.A. (1961) Electrophysiology of hippocampal neurons II. After-potentials and repetitive firing. J. Neurophysiol., 24, 243-259.
19. Madison, D.V. & Nicoll, R.A. (1982) Noradrenaline blocks accommodation of pyramidal cell discharge in the hippocampus. Nature, 299, 636-638.
20. Melyan, Z., Wheal, H.V. & Lancaster, B. (2002) Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron, 34, 107-114.
21. Metz, A.E., Jarsky, T., Martina, M. & Spruston, N. (2005) R-type calcium channels contribute to afterdepolarization and bursting in hippocampal CA1 pyramidal neurons. J. Neurosci., 25, 5763-5773.
22. Moore, S.J., Cooper, D.C. & Spruston, N. (2009) Plasticity of burst firing induced by synergistic activation of metabotropic glutamate and acetylcholine receptors. Neuron, 61, 287-300.
23. Moult, P.R., Schnabel, R., Kilpatrick, I.C., Bashir, Z.I. & Collingridge, G.L. (2002) Tyrosine dephosphorylation underlies DHPG-induced LTD. Neuropharmacology, 43, 175-180.
24. Moult, P.R., Correa, S.A., Collingridge, G.L., Fitzjohn, S.M. & Bashir, Z.I. (2008) Co-activation of p38 mitogen-activated protein kinase and protein tyrosine phosphatase underlies metabotropic glutamate receptor-dependent long-term depression. J. Physiol., 586, 2499-2510.
25. Muller, W. & Misgeld, U. (1986) Slow cholinergic excitation of guinea pig hippocampal neurons is mediated by two muscarinic receptor subtypes. Neurosci. Lett., 67, 107-112.
26. Palmer, M.J., Irving, A.J., Seabrook, G.R., Jane, D.E. & Collingridge, G.L. (1997) The group I mGlu receptor agonist DHPG induces a novel form of LTD in the CA1 region of the hippocampus. Neuropharmacology, 36, 1517-1532.
27. Piccinin, S., Thuault, S.J., Doherty, A.J., Brown, J.T., Randall, A.D., Davies, C.H., Bortolotto, Z.A. & Collingridge, G.L. (2008) The induction of long-term plasticity of non-synaptic, synchronized activity by the activation of group I mGluRs. Neuropharmacology, 55, 459-463.
28. Schorge, S. & Walker, M.C. (2009) A self-activating intrinsic brake on bursting in CA3 neurons. J. Physiol., 587, 1143-1144.
29. Shigemoto, R., Kinoshita, A., Wada, E., Nomura, S., Ohishi, H., Takada, M., Flor, P.J., Neki, A., Abe, T., Nakanishi, S. & Mizuno, N. (1997) Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J. Neurosci., 17, 7503-7522.
30. Snyder, E.M., Philpot, B.D., Huber, K.M., Dong, X., Fallon, J.R. & Bear, M.F. (2001) Internalization of ionotropic glutamate receptors in response to mGluR activation. Nat. Neurosci., 4, 1079-1085.
31. Sourdet, V., Russier, M., Daoudal, G., Ankri, N. & Debanne, D. (2003) Long-term enhancement of neuronal excitability and temporal fidelity mediated by metabotropic glutamate receptor subtype 5. J. Neurosci., 23, 10238-10248.
32. Spruston, N. & McBain, C.J. (2007) Structural and functional properties of hippocampal neurons. In Andersen, P., Morris, R., Amaral, D., Bliss, T.V. & O'Keefe, J. (Eds), The Hippocampus Book. Oxford University Press, New York, NY, pp. 133-201.
33. Wittner, L., Henze, D.A., Zaborszky, L. & Buzsaki, G. (2007) Three-dimensional reconstruction of the axon arbor of a CA3 pyramidal cell recorded and filled in vivo. Brain Struct. Funct., 212, 75-83.
34. Wong, R.K. & Prince, D.A. (1978) Participation of calcium spikes during intrinsic burst firing in hippocampal neurons. Brain Res., 159, 385-390.
35. Young, S.R., Chuang, S.C. & Wong, R.K. (2004) Modulation of afterpotentials and firing pattern in guinea pig CA3 neurones by group I metabotropic glutamate receptors. J. Physiol., 554, 371-385.
36. Young, S.R., Bianchi, R. & Wong, R.K. (2008) Signaling mechanisms underlying group I mGluR-induced persistent AHP suppression in CA3 hippocampal neurons. J. Neurophysiol., 99, 1105-1118.
37. Yue, C. & Yaari, Y. (2004) KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons. J. Neurosci., 24, 4614-4624.
38. Yue, C., Remy, S., Su, H., Beck, H. & Yaari, Y. (2005) Proximal persistent Na+ channels drive spike afterdepolarizations and associated bursting in adult CA1 pyramidal cells. J. Neurosci., 25, 9704-9720.
39. Zhang, W. & Linden, D.J. (2003) The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat. Rev., 4, 885-900.