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The Journal of Neuroscience, January 28, 2009, 29(4):939-950; doi:10.1523/JNEUROSCI.3251-08.2009

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Cellular/Molecular
Role of Ionotropic Glutamate Receptors in Long-Term Potentiation in Rat Hippocampal CA1 Oriens-Lacunosum Moleculare Interneurons

Iris Oren,1 Wiebke Nissen,2 Dimitri M. Kullmann,1 Peter Somogyi,3 and Karri P. Lamsa2

1Institute of Neurology, University College London, London WC1N 3BG, United Kingdom, 2Department of Pharmacology, Oxford University, Oxford OX1 3QT, United Kingdom, and 3Medical Research Council Anatomical Neuropharmacology Unit, Oxford University, Oxford OX1 3HT, United Kingdom

Correspondence should be addressed to Karri P. Lamsa, Department of Pharmacology, Oxford University, Mansfield Road, Oxford OX1 3QT, UK. Email: karri.lamsa{at}pharm.ox.ac.uk

Some interneurons of the hippocampus exhibit NMDA receptor-independent long-term potentiation (LTP) that is induced by presynaptic glutamate release when the postsynaptic membrane potential is hyperpolarized. This "anti-Hebbian" form of LTP is prevented by postsynaptic depolarization or by blocking AMPA and kainate receptors. Although both AMPA and kainate receptors are expressed in hippocampal interneurons, their relative roles in anti-Hebbian LTP are not known. Because interneuron diversity potentially conceals simple rules underlying different forms of plasticity, we focus on glutamatergic synapses onto a subset of interneurons with dendrites in stratum oriens and a main ascending axon that projects to stratum lacunosum moleculare, the oriens-lacunosum moleculare (O-LM) cells. We show that anti-Hebbian LTP in O-LM interneurons has consistent induction and expression properties, and is prevented by selective inhibition of AMPA receptors. The majority of the ionotropic glutamatergic synaptic current in these cells is mediated by inwardly rectifying Ca2+-permeable AMPA receptors. Although GluR5-containing kainate receptors contribute to synaptic currents at high stimulus frequency, they are not required for LTP induction. Glutamatergic synapses on O-LM cells thus behave in a homogeneous manner and exhibit LTP dependent on Ca2+-permeable AMPA receptors.

Key words: inhibition; GABAergic; kainate; network; plasticity; interneuron

Received July 10, 2008; revised Nov. 19, 2008; accepted Nov. 26, 2008.

Correspondence should be addressed to Karri P. Lamsa, Department of Pharmacology, Oxford University, Mansfield Road, Oxford OX1 3QT, UK. Email: karri.lamsa{at}pharm.ox.ac.uk






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